Research ArticlePhlebotomines (Diptera Psychodidae) in a HydroelectricSystem Affected Area from Northern Amazonian BrazilFurther Insights into the Effects of Environmental Changeson Vector Ecology

Nercy Virginia Rabelo Furtado1 Allan Kardec Ribeiro Galardo1 Clicia Denis Galardo1

Viviane Caetano Firmino2 and Thiago Vasconcelos dos Santos3

1Laboratorio de Entomologia Medica Instituto de Pesquisas Cientıficas e Tecnologicas do Estado do Amapa Macapa AP Brazil2Universidade Federal do Amapa Campus Binacional Oiapoque AP Brazil3Instituto Evandro Chagas Secretaria de Vigilancia em Saude Ministerio da Saude Ananindeua PA Brazil

Correspondence should be addressed toThiago Vasconcelos dos Santos thiagovasconcelosiecpagovbr

Received 3 August 2016 Revised 6 October 2016 Accepted 12 October 2016

Academic Editor Aditya Prasad Dash

Copyright copy 2016 Nercy Virginia Rabelo Furtado et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

During 2012ndash2015 an entomological survey was conducted as part of a phlebotomine (Diptera Psychodidae) monitoring programin an area influenced by the Santo Antonio do Jari hydroelectric system (Amapa State Brazil) The purpose was to study aspects ofAmazonGuiananAmerican cutaneous leishmaniasis (ACL) vectors subjected to stresses by anthropogenic environmental changesFor sampling CDC light traps were positioned 05 1 and 20m above ground at five capture locations along the Jari River BasinFluctuations in phlebotomine numbers were analyzed to determine any correlation with rainfall dam waterlogging andor ACLcases fromMay 2012 toMarch 2015 We captured 2800 individuals and among 45 species identified Bichromomyia flaviscutellataNyssomyia umbratilis and Psychodopygus squamiventris sl were determined to be the main putative vectors based on currentknowledge of the AmazonGuianan ACL scenario Rainfall but not complete flooding was relatively correlated with phlebotominefluctuation mainly observed for Ps squamiventris sl as were ACL cases with Ny umbratilis Behavioral changes were observed inthe unexpected high frequency of Bi flaviscutellata among CDC captures and the noncanopy dominance ofNy umbratilis possiblyattributable to environmental stress in the sampled ecotopes Continuous entomological surveillance is necessary to monitor theoutcomes of these findings

1 Introduction

Insects of Phlebotominae (Diptera Psychodidae) species areof great medical interest because of their implications inthe transmission of some vector-borne diseases in partic-ular leishmaniasis [1ndash3] American cutaneous leishmaniasis(ACL) is known to be endemic in Amazonian Brazil and isregarded as a serious risk to public health The high biodi-versity of the region induces a complex mosaic of ecologicalinteractions among reservoirs vectors and parasites andconsequently awide spectrumofACL clinicalmanifestationsincluding disfiguring and potentially life-threatening cases

[4] Moreover this diversity of transmission cycles becomeseven more complex to understand in the context of theinfluence of anthropic effects on natural ecological systemsThe consequences of anthropogenic environmental stress onthe expansion of the geographical distribution of ACL aretherefore difficult to predict with any certainty [5]

Over the past 30 years one of the main causes of humaninfluence on the environment in the Brazilian Amazon Basinis its exploitation for generating energy from hydropowerNegative effects of some of the resultant environmentalchanges have been observed an example is the disturbancecaused by the proliferation ofMansonia (Diptera Culicidae)

Hindawi Publishing CorporationJournal of Tropical MedicineVolume 2016 Article ID 9819723 12 pageshttpdxdoiorg10115520169819723

2 Journal of Tropical Medicine

in the dammed lake associatedwith theTucuruı hydroelectricsystem [6] Vector monitoring programs which are essentialto being granted a license to operate are included in environ-mental and public health planning in order to predict andminimize the effects of vector-borne diseases in hydroelectricsystems [7] This monitoring includes spatialtemporal stud-ies of phlebotomines and their potential implications for thetransmission dynamics of leishmaniasis agents [8]

The geographically closely related Brazilian states of Para(PA) and Amapa (AP) share a border through the JariRiver and cover a region historically associated with theexploitation and processing of cellulose Early informationabout leishmaniasis in the region first emerged in the 1970ndash1980s In this period studies conducted in ldquoMonte Douradordquo(Almeirim PA) provided substantial knowledge about ACLecoepidemiology with particular reference to the ldquopian-boisrdquo a form of cutaneous leishmaniasis caused by Leishma-nia (Viannia) guyanensis (formerly referred to as Leishmaniabraziliensis guyanensis) and its respective identity-obscuredvector Nyssomyia umbratilis [9ndash16]

Since those original studies were undertaken the regionalso now hosts the Santo Antonio do Jari hydroelectricsystem The present study therefore aimed to characterizephlebotomine fauna in the area in order to assess thepotential impact of the Santo Antonio do Jari hydroelectricsystem and in particular the spatiotemporal implications ofenvironmental changes on the ecology of ACL vectors in thatregion

2 Materials and Methods

21 Study Area The Santo Antonio do Jari hydroelectricsystem (0∘39101584002410158401015840S 52∘30101584056910158401015840W) is situated between themunicipalities of Almeirim (PA) and Laranjal do Jari (AP) aregion within the Guianan Ecoregion Complex The hydro-electric system comprises 3734 MW of installed potency anda reservoir area of 317 km2 Its construction began in 2011and the system was totally operative from 2014

The Amazon Region has a ldquohot-humidrdquo equatorial cli-mate however only minor differences are observed in thedistinct ecoregions In this study four Guianan EcoregionComplex seasons were characterized as follows a short rainy(wet) season from mid-November (ldquonovembre humiderdquo) tolate January a short dry season between early February andmid-March a long rainy season from late March to late Julyand a long dry season from late July to mid-November [17]

22 Sampled Locations Five locations each with the follow-ing characteristics were sampled up- and downstream of thecaisson (Figure 1)

The eastern bank of the Jari River (AP) covered by alluvialdense forest

(I) Porto Sabao (S 00∘37101584002210158401015840 W 052∘30101584042110158401015840) a for-ested area with only a few dwelling A small harboroperates from the opposite side of the river

(II) Iratapuru Village (S 00∘33101584050910158401015840 W 052∘34101584048510158401015840) acluster of dwellings forming a community of approx-imately 200 inhabitants which primarily acts as anextractive reserve

(III) SantoAntonioVillage (S 00∘38101584057410158401015840W052∘30101584027910158401015840)which is the only site downstreamof the caisson com-prising 27 agriculturist families inhabiting riverinewooden buildingsThe western bank of the Jari River (PA) covered bysubmontane (lowland) dense forest

(IV) Traıra (S 00∘37101584050710158401015840W052∘31101584048810158401015840) a locationwithno dwellings on the Traıra river

(V) the power Plant (S 00∘39101584007710158401015840 W 052∘31101584006410158401015840) themost affected area close to the construction site andwith very little vegetation

23 Sampling Phlebotomine captures were undertaken dur-ing 2012 to 2015 in fourteen quadrimonthly field expedi-tions which aimed to sample periods in the short dry(FebruaryMarch) rainy to dry (JuneJuly) and dry to rainy(OctoberNovember) AmazonGuianan seasons Eight expe-ditions were undertaken before and six after dammed lakelevels were replenished (in May 2014) In each of the abovedescribed five areas a randomly selected horizontal transectwas established in the direction of the primarily forested areacomprising a phlebotomine monitoring station (MS) sitedapproximately 200m distance from the forest edge wherehuman settlementswere present EachMS incorporated threeCDC miniature light traps (Sudia and Chamberlain model)installed between 1800 and 0600 for two consecutive nightsEach was placed according to the following different verticalstrata 05m from ground level 1m from ground level andat 20m in the tree canopy they were placed 10m apartfrom each other Trees used for canopy placement of CDCtraps were selected based on a minimum height of 20mregardless of speciesThe ground level surface was composedof humid decomposed organic material originating fromthe trees Phlebotomines were triaged in a stereomicroscopecleaned with neutral detergent [1 (Extran)] washed withNaCl 09 and then stored in 70 ethanol In the laboratoryspecimens were processed according to the methodologyof Ryan [18] mounted in Berlese fluid (GBI LaboratoriesManchester England) and identified according toGalati [19]

24 Data Analysis Sampling effort was calculated basedon number of expeditions versus the number of installedCDC traps versus hours of exposition Phlebotomine fre-quency was analyzed for correlation with climatic data(monthly average rainfall temperature and air relativehumidity) sourced from the Jari Meteorological Station (ldquoJariEnergiardquo database) and with epidemiology (ACL monthlyprevalence) obtained after interrogating the database of theldquoCoordenacao de Vigilancia em Sauderdquo (Coordination ofSurveillance in Health) of the ldquoSecretaria de Estado da Saudedo Amapa-SESArdquo (Amapa State Health Secretary) Data weretested by a single linear regression with Pearsonrsquos coefficient(r) using BioEstat 50 where the r-value represents a strongcorrelation if above 07 a moderate correlation if between03 and 07 a weak correlation if between 01 and 03and an insignificant correlation if below 01 The index ofspecies abundance (ISA) and the standard index of speciesabundance (SISA) were calculated using Microsoft Excel for

Journal of Tropical Medicine 3

Atlantic Ocean

Brazil

PacificOcean

Atlantic Ocean

Amapaacute State(Brazil)

French Guiana

Paraacute State(Brazil)

IratapuruVillage

Traiacutera River

Power Plant

PortoSabatildeo

Santo AntocircnioVillage

Jari River

Almeirim(Paraacute State)

Laranjal do Jari(Amapaacute State)

2000 km 200 km

2 km

N N

N

Figure 1 Study area Maps showing the five surveyed locations for phlebotomine captures (2012ndash2015) in Santo Antonio do Jari hydroelectricsystem impacted area between the states of Para and Amapa BrazilM locations

the five ecotopes surveyed as described by Roberts and Hsi[20] Species diversity (Shannonrsquos diversity index H1015840) andthe coefficient of variation (S1015840) between monthly records(climatic and epidemiological) were calculated using Pastsoftware [21] All comparisons were performed using a t-testto determine significance level (119901 value le 005)

3 Results

A total of 2800 individuals were captured (1894 femalesand 906 males) belonging to 45 species in approximately

2520 h of sampling effort Females of Trichophoromyia(exceptionally Th ubiquitalis) and Pressatia (not identifiableat species level) and some unidentified Evandromyia Nys-somyia and Psychodopygus species were allocated at genericlevel (Table 1)

New AP records includedTh castanheirai Th eurypygaEvandromyia begonae Ev bacula Pressatia equatorialis andPsathyromyia punctigeniculata

The five most frequent species captured were Sciopemyiasordellii (119899 = 316 SISA = 087) Ps davisi (119899 = 314 SISA =074) Bichromomyia flaviscutellata (119899 = 265 SISA= 095) Ev

4 Journal of Tropical MedicineTa

ble1Ph

ebotom

inespeciescompo

sitionofSantoAnton

iodo

Jarihydroelectric

syste

mim

pacted

area

(AmapaS

tateA

mazon

ianBrazil)

ontheb

asisoffivesurveyedlocatio

ns(2012ndash2015)

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

1Sciopemyiasordellii

149

6613

1015

442

16mdash

136

087

2nd

316

1129

2Psycho

dopygu

sdavisi

4637

9556

1510

3817

mdashmdash

64

074

3rd

314

1121

mdashTrich

ophoromyiaspp

177

mdash34

mdash40

mdash17

mdashmdash

mdashmdash

mdashmdash

268

957

3Bichromom

yiafla

viscutellata

7632

2414

2211

5231

12

2095

1st

265

946

4Evandrom

yiainfra

spinosa

4410

2518

32

3018

mdashmdash

9206

6th

150

536

5Ny

ssom

yiaum

bratilis

2612

3130

196

139

mdashmdash

86

063

5th

146

521

6Trich

ophoromyiacasta

nheir

aimdash

104

mdash6

mdash14

mdash11

mdashmdash

112

051

9th

135

482

mdashPressatia

spp

43mdash

1mdash

9mdash

78mdash

mdashmdash

mdashmdash

mdash131

468

mdashEvandrom

yiaspp

5210

4mdash

3911

12mdash

mdashmdash

mdashmdash

mdash128

457

7Viannamyiafurcata

444

115

111

305

mdashmdash

104

055

7th

111

396

8Psycho

dopygu

ssqu

amiventrissensulato

3614

155

10mdash

9mdash

mdashmdash

11052

8th

89318

9Trich

opygom

yiatrichopyga

1116

98

9mdash

2112

mdashmdash

7207

4th

86307

10Tricho

phorom

yiaub

iquitalis

216

58

148

139

2mdash

114

05

10th

86307

11Evandrom

yiasaulensis

409

5mdash

44

121

mdashmdash

128

043

11th

75268

12Psycho

dopygu

shirs

utus

hirsutus

13mdash

204

144

mdashmdash

mdashmdash

136

04

12th

5519

613

Trich

ophoromyiabrachypyga

mdash36

mdash12

mdash2

mdash2

mdashmdash

152

032

14th

5218

614

Pressatia

choti

mdash17

mdash3

mdash5

mdash25

mdashmdash

142

037

13th

5017

915

Nyssom

yiaan

duzei

65

2410

mdashmdash

mdashmdash

mdashmdash

17023

16th

4516

116

Lutzom

yiagomezi

2711

mdashmdash

mdashmdash

mdashmdash

mdashmdash

194

012

22th

3813

6mdash

Nysso

myiaspp

mdashmdash

mdash1

1mdash

1125

mdashmdash

mdashmdash

mdash38

136

17Ny

ssom

yiaan

tunesi

mdash2

9mdash

52

mdashmdash

1mdash

142

037

13th

19068

18Sciopemyiaflu

viatilis

21

3mdash

91

mdashmdash

mdashmdash

18019

18th

16057

19Micropygom

yiarorotaensis

4mdash

mdashmdash

8mdash

21

mdashmdash

178

02

17th

15054

20Psycho

dopygu

sparaensis

mdashmdash

mdashmdash

63

51

mdashmdash

176

02

17th

15054

21Psychodopygusclaustre

i7

1mdash

mdashmdash

mdash2

mdash3

1154

031

15th

14050

mdashPsychodopygusspp

4

mdash2

mdash6

mdash2

mdashmdash

mdashmdash

mdashmdash

14050

22Trich

ophoromyiaeurypyga

mdash8

mdashmdash

mdash3

mdash1

mdashmdash

182

018

19th

12043

23Psathyromyiaaragaoi

mdashmdash

52

mdashmdash

4mdash

mdashmdash

188

015

20th

11039

24Evandrom

yiabrachyphalla

43

21

1mdash

mdashmdash

mdashmdash

19014

21th

11039

25Psychodopyguscarreraicarrerai

11

mdash7

mdashmdash

mdashmdash

mdashmdash

202

008

26th

9032

26Evandrom

yiabegona

e2

2mdash

mdash4

mdashmdash

mdashmdash

mdash196

011

23th

8029

27Ny

ssom

yiawh

itman

imdash

mdashmdash

mdashmdash

mdash8

mdashmdash

mdash20

009

25th

8029

28Psathyromyiascaffi

32

mdashmdash

2mdash

mdashmdash

mdashmdash

198

01

24th

7025

29Pressatia

trispinosa

mdashmdash

mdash7

mdashmdash

mdashmdash

mdashmdash

204

007

27th

7025

30Micropygom

yiatrinidadensis

7mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

7025

31Viannamyiatuberculata

6mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

21004

30th

6021

32Pintom

yiadamascenoi

mdashmdash

mdashmdash

mdashmdash

5mdash

mdashmdash

20009

25th

5018

33Evandrom

yiaevandroi

mdashmdash

mdashmdash

41

mdashmdash

mdashmdash

204

007

27th

5018

34Psathyromyialutziana

5mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

212

003

31th

5018

35Brum

ptom

iatra

vasso

simdash

mdashmdash

mdashmdash

mdash3

1mdash

mdash196

011

23th

4014

36Evandrom

yiabacula

mdashmdash

mdashmdash

1mdash

3mdash

mdashmdash

202

008

26th

4014

37Evandrom

yiamonstruosa

mdashmdash

4mdash

mdashmdash

mdashmdash

mdashmdash

206

006

28th

4014

Journal of Tropical Medicine 5

Table1Con

tinued

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

38Psychodopygusa

mazonensis

mdashmdash

mdashmdash

22

mdashmdash

mdashmdash

21004

30th

4014

39Psychodopyguscorossoniensis

mdashmdash

mdashmdash

mdash2

mdashmdash

mdashmdash

206

006

28th

2007

40Pressatia

equatoria

lismdash

2mdash

mdashmdash

mdashmdash

mdashmdash

mdash21

004

30th

2007

41Psathyromyiainflata

mdashmdash

mdashmdash

mdashmdash

2mdash

mdashmdash

21004

30th

2007

42Micropygom

yiamicropyga

mdashmdash

mdashmdash

mdashmdash

11

mdashmdash

214

002

32th

2007

43Psychodopygusgenicu

latus

mdashmdash

mdash2

mdashmdash

mdashmdash

mdashmdash

218

033th

2007

44Lu

tzom

yiacarvalhoi

mdashmdash

1mdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

1004

45Psathyromyiapunctigenicu

lata

mdashmdash

mdashmdash

1mdash

mdashmdash

mdashmdash

216

001

32th

1004

Total

856

411

342

209

274

96415

186

74

2800

1000

1267

551

370

601

11Ea

chlocatio

ncomprise

dam

onito

ringstation(M

S)sampled

with

051and20

mCD

Ctrapsprovidingapproxim

ately

504h

MS

Cfem

aleDm

aleISAind

exof

speciesa

bund

anceSISAstand

ardindexof

speciesa

bund

ance

ldquothe

bold

italic

fontrdquoP

rovenandor

putativ

eACL

vectorsintheA

mazon

Region

based

inYo

ungandDun

can[1]Ra

ngelandLainson[4]Re

ady[2]andLainsonandShaw

[16]

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Research and TreatmentAIDS

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

2 Journal of Tropical Medicine

in the dammed lake associatedwith theTucuruı hydroelectricsystem [6] Vector monitoring programs which are essentialto being granted a license to operate are included in environ-mental and public health planning in order to predict andminimize the effects of vector-borne diseases in hydroelectricsystems [7] This monitoring includes spatialtemporal stud-ies of phlebotomines and their potential implications for thetransmission dynamics of leishmaniasis agents [8]

The geographically closely related Brazilian states of Para(PA) and Amapa (AP) share a border through the JariRiver and cover a region historically associated with theexploitation and processing of cellulose Early informationabout leishmaniasis in the region first emerged in the 1970ndash1980s In this period studies conducted in ldquoMonte Douradordquo(Almeirim PA) provided substantial knowledge about ACLecoepidemiology with particular reference to the ldquopian-boisrdquo a form of cutaneous leishmaniasis caused by Leishma-nia (Viannia) guyanensis (formerly referred to as Leishmaniabraziliensis guyanensis) and its respective identity-obscuredvector Nyssomyia umbratilis [9ndash16]

Since those original studies were undertaken the regionalso now hosts the Santo Antonio do Jari hydroelectricsystem The present study therefore aimed to characterizephlebotomine fauna in the area in order to assess thepotential impact of the Santo Antonio do Jari hydroelectricsystem and in particular the spatiotemporal implications ofenvironmental changes on the ecology of ACL vectors in thatregion

2 Materials and Methods

21 Study Area The Santo Antonio do Jari hydroelectricsystem (0∘39101584002410158401015840S 52∘30101584056910158401015840W) is situated between themunicipalities of Almeirim (PA) and Laranjal do Jari (AP) aregion within the Guianan Ecoregion Complex The hydro-electric system comprises 3734 MW of installed potency anda reservoir area of 317 km2 Its construction began in 2011and the system was totally operative from 2014

The Amazon Region has a ldquohot-humidrdquo equatorial cli-mate however only minor differences are observed in thedistinct ecoregions In this study four Guianan EcoregionComplex seasons were characterized as follows a short rainy(wet) season from mid-November (ldquonovembre humiderdquo) tolate January a short dry season between early February andmid-March a long rainy season from late March to late Julyand a long dry season from late July to mid-November [17]

22 Sampled Locations Five locations each with the follow-ing characteristics were sampled up- and downstream of thecaisson (Figure 1)

The eastern bank of the Jari River (AP) covered by alluvialdense forest

(I) Porto Sabao (S 00∘37101584002210158401015840 W 052∘30101584042110158401015840) a for-ested area with only a few dwelling A small harboroperates from the opposite side of the river

(II) Iratapuru Village (S 00∘33101584050910158401015840 W 052∘34101584048510158401015840) acluster of dwellings forming a community of approx-imately 200 inhabitants which primarily acts as anextractive reserve

(III) SantoAntonioVillage (S 00∘38101584057410158401015840W052∘30101584027910158401015840)which is the only site downstreamof the caisson com-prising 27 agriculturist families inhabiting riverinewooden buildingsThe western bank of the Jari River (PA) covered bysubmontane (lowland) dense forest

(IV) Traıra (S 00∘37101584050710158401015840W052∘31101584048810158401015840) a locationwithno dwellings on the Traıra river

(V) the power Plant (S 00∘39101584007710158401015840 W 052∘31101584006410158401015840) themost affected area close to the construction site andwith very little vegetation

23 Sampling Phlebotomine captures were undertaken dur-ing 2012 to 2015 in fourteen quadrimonthly field expedi-tions which aimed to sample periods in the short dry(FebruaryMarch) rainy to dry (JuneJuly) and dry to rainy(OctoberNovember) AmazonGuianan seasons Eight expe-ditions were undertaken before and six after dammed lakelevels were replenished (in May 2014) In each of the abovedescribed five areas a randomly selected horizontal transectwas established in the direction of the primarily forested areacomprising a phlebotomine monitoring station (MS) sitedapproximately 200m distance from the forest edge wherehuman settlementswere present EachMS incorporated threeCDC miniature light traps (Sudia and Chamberlain model)installed between 1800 and 0600 for two consecutive nightsEach was placed according to the following different verticalstrata 05m from ground level 1m from ground level andat 20m in the tree canopy they were placed 10m apartfrom each other Trees used for canopy placement of CDCtraps were selected based on a minimum height of 20mregardless of speciesThe ground level surface was composedof humid decomposed organic material originating fromthe trees Phlebotomines were triaged in a stereomicroscopecleaned with neutral detergent [1 (Extran)] washed withNaCl 09 and then stored in 70 ethanol In the laboratoryspecimens were processed according to the methodologyof Ryan [18] mounted in Berlese fluid (GBI LaboratoriesManchester England) and identified according toGalati [19]

24 Data Analysis Sampling effort was calculated basedon number of expeditions versus the number of installedCDC traps versus hours of exposition Phlebotomine fre-quency was analyzed for correlation with climatic data(monthly average rainfall temperature and air relativehumidity) sourced from the Jari Meteorological Station (ldquoJariEnergiardquo database) and with epidemiology (ACL monthlyprevalence) obtained after interrogating the database of theldquoCoordenacao de Vigilancia em Sauderdquo (Coordination ofSurveillance in Health) of the ldquoSecretaria de Estado da Saudedo Amapa-SESArdquo (Amapa State Health Secretary) Data weretested by a single linear regression with Pearsonrsquos coefficient(r) using BioEstat 50 where the r-value represents a strongcorrelation if above 07 a moderate correlation if between03 and 07 a weak correlation if between 01 and 03and an insignificant correlation if below 01 The index ofspecies abundance (ISA) and the standard index of speciesabundance (SISA) were calculated using Microsoft Excel for

Journal of Tropical Medicine 3

Atlantic Ocean

Brazil

PacificOcean

Atlantic Ocean

Amapaacute State(Brazil)

French Guiana

Paraacute State(Brazil)

IratapuruVillage

Traiacutera River

Power Plant

PortoSabatildeo

Santo AntocircnioVillage

Jari River

Almeirim(Paraacute State)

Laranjal do Jari(Amapaacute State)

2000 km 200 km

2 km

N N

N

Figure 1 Study area Maps showing the five surveyed locations for phlebotomine captures (2012ndash2015) in Santo Antonio do Jari hydroelectricsystem impacted area between the states of Para and Amapa BrazilM locations

the five ecotopes surveyed as described by Roberts and Hsi[20] Species diversity (Shannonrsquos diversity index H1015840) andthe coefficient of variation (S1015840) between monthly records(climatic and epidemiological) were calculated using Pastsoftware [21] All comparisons were performed using a t-testto determine significance level (119901 value le 005)

3 Results

A total of 2800 individuals were captured (1894 femalesand 906 males) belonging to 45 species in approximately

2520 h of sampling effort Females of Trichophoromyia(exceptionally Th ubiquitalis) and Pressatia (not identifiableat species level) and some unidentified Evandromyia Nys-somyia and Psychodopygus species were allocated at genericlevel (Table 1)

New AP records includedTh castanheirai Th eurypygaEvandromyia begonae Ev bacula Pressatia equatorialis andPsathyromyia punctigeniculata

The five most frequent species captured were Sciopemyiasordellii (119899 = 316 SISA = 087) Ps davisi (119899 = 314 SISA =074) Bichromomyia flaviscutellata (119899 = 265 SISA= 095) Ev

4 Journal of Tropical MedicineTa

ble1Ph

ebotom

inespeciescompo

sitionofSantoAnton

iodo

Jarihydroelectric

syste

mim

pacted

area

(AmapaS

tateA

mazon

ianBrazil)

ontheb

asisoffivesurveyedlocatio

ns(2012ndash2015)

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

1Sciopemyiasordellii

149

6613

1015

442

16mdash

136

087

2nd

316

1129

2Psycho

dopygu

sdavisi

4637

9556

1510

3817

mdashmdash

64

074

3rd

314

1121

mdashTrich

ophoromyiaspp

177

mdash34

mdash40

mdash17

mdashmdash

mdashmdash

mdashmdash

268

957

3Bichromom

yiafla

viscutellata

7632

2414

2211

5231

12

2095

1st

265

946

4Evandrom

yiainfra

spinosa

4410

2518

32

3018

mdashmdash

9206

6th

150

536

5Ny

ssom

yiaum

bratilis

2612

3130

196

139

mdashmdash

86

063

5th

146

521

6Trich

ophoromyiacasta

nheir

aimdash

104

mdash6

mdash14

mdash11

mdashmdash

112

051

9th

135

482

mdashPressatia

spp

43mdash

1mdash

9mdash

78mdash

mdashmdash

mdashmdash

mdash131

468

mdashEvandrom

yiaspp

5210

4mdash

3911

12mdash

mdashmdash

mdashmdash

mdash128

457

7Viannamyiafurcata

444

115

111

305

mdashmdash

104

055

7th

111

396

8Psycho

dopygu

ssqu

amiventrissensulato

3614

155

10mdash

9mdash

mdashmdash

11052

8th

89318

9Trich

opygom

yiatrichopyga

1116

98

9mdash

2112

mdashmdash

7207

4th

86307

10Tricho

phorom

yiaub

iquitalis

216

58

148

139

2mdash

114

05

10th

86307

11Evandrom

yiasaulensis

409

5mdash

44

121

mdashmdash

128

043

11th

75268

12Psycho

dopygu

shirs

utus

hirsutus

13mdash

204

144

mdashmdash

mdashmdash

136

04

12th

5519

613

Trich

ophoromyiabrachypyga

mdash36

mdash12

mdash2

mdash2

mdashmdash

152

032

14th

5218

614

Pressatia

choti

mdash17

mdash3

mdash5

mdash25

mdashmdash

142

037

13th

5017

915

Nyssom

yiaan

duzei

65

2410

mdashmdash

mdashmdash

mdashmdash

17023

16th

4516

116

Lutzom

yiagomezi

2711

mdashmdash

mdashmdash

mdashmdash

mdashmdash

194

012

22th

3813

6mdash

Nysso

myiaspp

mdashmdash

mdash1

1mdash

1125

mdashmdash

mdashmdash

mdash38

136

17Ny

ssom

yiaan

tunesi

mdash2

9mdash

52

mdashmdash

1mdash

142

037

13th

19068

18Sciopemyiaflu

viatilis

21

3mdash

91

mdashmdash

mdashmdash

18019

18th

16057

19Micropygom

yiarorotaensis

4mdash

mdashmdash

8mdash

21

mdashmdash

178

02

17th

15054

20Psycho

dopygu

sparaensis

mdashmdash

mdashmdash

63

51

mdashmdash

176

02

17th

15054

21Psychodopygusclaustre

i7

1mdash

mdashmdash

mdash2

mdash3

1154

031

15th

14050

mdashPsychodopygusspp

4

mdash2

mdash6

mdash2

mdashmdash

mdashmdash

mdashmdash

14050

22Trich

ophoromyiaeurypyga

mdash8

mdashmdash

mdash3

mdash1

mdashmdash

182

018

19th

12043

23Psathyromyiaaragaoi

mdashmdash

52

mdashmdash

4mdash

mdashmdash

188

015

20th

11039

24Evandrom

yiabrachyphalla

43

21

1mdash

mdashmdash

mdashmdash

19014

21th

11039

25Psychodopyguscarreraicarrerai

11

mdash7

mdashmdash

mdashmdash

mdashmdash

202

008

26th

9032

26Evandrom

yiabegona

e2

2mdash

mdash4

mdashmdash

mdashmdash

mdash196

011

23th

8029

27Ny

ssom

yiawh

itman

imdash

mdashmdash

mdashmdash

mdash8

mdashmdash

mdash20

009

25th

8029

28Psathyromyiascaffi

32

mdashmdash

2mdash

mdashmdash

mdashmdash

198

01

24th

7025

29Pressatia

trispinosa

mdashmdash

mdash7

mdashmdash

mdashmdash

mdashmdash

204

007

27th

7025

30Micropygom

yiatrinidadensis

7mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

7025

31Viannamyiatuberculata

6mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

21004

30th

6021

32Pintom

yiadamascenoi

mdashmdash

mdashmdash

mdashmdash

5mdash

mdashmdash

20009

25th

5018

33Evandrom

yiaevandroi

mdashmdash

mdashmdash

41

mdashmdash

mdashmdash

204

007

27th

5018

34Psathyromyialutziana

5mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

212

003

31th

5018

35Brum

ptom

iatra

vasso

simdash

mdashmdash

mdashmdash

mdash3

1mdash

mdash196

011

23th

4014

36Evandrom

yiabacula

mdashmdash

mdashmdash

1mdash

3mdash

mdashmdash

202

008

26th

4014

37Evandrom

yiamonstruosa

mdashmdash

4mdash

mdashmdash

mdashmdash

mdashmdash

206

006

28th

4014

Journal of Tropical Medicine 5

Table1Con

tinued

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

38Psychodopygusa

mazonensis

mdashmdash

mdashmdash

22

mdashmdash

mdashmdash

21004

30th

4014

39Psychodopyguscorossoniensis

mdashmdash

mdashmdash

mdash2

mdashmdash

mdashmdash

206

006

28th

2007

40Pressatia

equatoria

lismdash

2mdash

mdashmdash

mdashmdash

mdashmdash

mdash21

004

30th

2007

41Psathyromyiainflata

mdashmdash

mdashmdash

mdashmdash

2mdash

mdashmdash

21004

30th

2007

42Micropygom

yiamicropyga

mdashmdash

mdashmdash

mdashmdash

11

mdashmdash

214

002

32th

2007

43Psychodopygusgenicu

latus

mdashmdash

mdash2

mdashmdash

mdashmdash

mdashmdash

218

033th

2007

44Lu

tzom

yiacarvalhoi

mdashmdash

1mdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

1004

45Psathyromyiapunctigenicu

lata

mdashmdash

mdashmdash

1mdash

mdashmdash

mdashmdash

216

001

32th

1004

Total

856

411

342

209

274

96415

186

74

2800

1000

1267

551

370

601

11Ea

chlocatio

ncomprise

dam

onito

ringstation(M

S)sampled

with

051and20

mCD

Ctrapsprovidingapproxim

ately

504h

MS

Cfem

aleDm

aleISAind

exof

speciesa

bund

anceSISAstand

ardindexof

speciesa

bund

ance

ldquothe

bold

italic

fontrdquoP

rovenandor

putativ

eACL

vectorsintheA

mazon

Region

based

inYo

ungandDun

can[1]Ra

ngelandLainson[4]Re

ady[2]andLainsonandShaw

[16]

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

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Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Journal of Tropical Medicine 3

Atlantic Ocean

Brazil

PacificOcean

Atlantic Ocean

Amapaacute State(Brazil)

French Guiana

Paraacute State(Brazil)

IratapuruVillage

Traiacutera River

Power Plant

PortoSabatildeo

Santo AntocircnioVillage

Jari River

Almeirim(Paraacute State)

Laranjal do Jari(Amapaacute State)

2000 km 200 km

2 km

N N

N

Figure 1 Study area Maps showing the five surveyed locations for phlebotomine captures (2012ndash2015) in Santo Antonio do Jari hydroelectricsystem impacted area between the states of Para and Amapa BrazilM locations

the five ecotopes surveyed as described by Roberts and Hsi[20] Species diversity (Shannonrsquos diversity index H1015840) andthe coefficient of variation (S1015840) between monthly records(climatic and epidemiological) were calculated using Pastsoftware [21] All comparisons were performed using a t-testto determine significance level (119901 value le 005)

3 Results

A total of 2800 individuals were captured (1894 femalesand 906 males) belonging to 45 species in approximately

2520 h of sampling effort Females of Trichophoromyia(exceptionally Th ubiquitalis) and Pressatia (not identifiableat species level) and some unidentified Evandromyia Nys-somyia and Psychodopygus species were allocated at genericlevel (Table 1)

New AP records includedTh castanheirai Th eurypygaEvandromyia begonae Ev bacula Pressatia equatorialis andPsathyromyia punctigeniculata

The five most frequent species captured were Sciopemyiasordellii (119899 = 316 SISA = 087) Ps davisi (119899 = 314 SISA =074) Bichromomyia flaviscutellata (119899 = 265 SISA= 095) Ev

4 Journal of Tropical MedicineTa

ble1Ph

ebotom

inespeciescompo

sitionofSantoAnton

iodo

Jarihydroelectric

syste

mim

pacted

area

(AmapaS

tateA

mazon

ianBrazil)

ontheb

asisoffivesurveyedlocatio

ns(2012ndash2015)

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

1Sciopemyiasordellii

149

6613

1015

442

16mdash

136

087

2nd

316

1129

2Psycho

dopygu

sdavisi

4637

9556

1510

3817

mdashmdash

64

074

3rd

314

1121

mdashTrich

ophoromyiaspp

177

mdash34

mdash40

mdash17

mdashmdash

mdashmdash

mdashmdash

268

957

3Bichromom

yiafla

viscutellata

7632

2414

2211

5231

12

2095

1st

265

946

4Evandrom

yiainfra

spinosa

4410

2518

32

3018

mdashmdash

9206

6th

150

536

5Ny

ssom

yiaum

bratilis

2612

3130

196

139

mdashmdash

86

063

5th

146

521

6Trich

ophoromyiacasta

nheir

aimdash

104

mdash6

mdash14

mdash11

mdashmdash

112

051

9th

135

482

mdashPressatia

spp

43mdash

1mdash

9mdash

78mdash

mdashmdash

mdashmdash

mdash131

468

mdashEvandrom

yiaspp

5210

4mdash

3911

12mdash

mdashmdash

mdashmdash

mdash128

457

7Viannamyiafurcata

444

115

111

305

mdashmdash

104

055

7th

111

396

8Psycho

dopygu

ssqu

amiventrissensulato

3614

155

10mdash

9mdash

mdashmdash

11052

8th

89318

9Trich

opygom

yiatrichopyga

1116

98

9mdash

2112

mdashmdash

7207

4th

86307

10Tricho

phorom

yiaub

iquitalis

216

58

148

139

2mdash

114

05

10th

86307

11Evandrom

yiasaulensis

409

5mdash

44

121

mdashmdash

128

043

11th

75268

12Psycho

dopygu

shirs

utus

hirsutus

13mdash

204

144

mdashmdash

mdashmdash

136

04

12th

5519

613

Trich

ophoromyiabrachypyga

mdash36

mdash12

mdash2

mdash2

mdashmdash

152

032

14th

5218

614

Pressatia

choti

mdash17

mdash3

mdash5

mdash25

mdashmdash

142

037

13th

5017

915

Nyssom

yiaan

duzei

65

2410

mdashmdash

mdashmdash

mdashmdash

17023

16th

4516

116

Lutzom

yiagomezi

2711

mdashmdash

mdashmdash

mdashmdash

mdashmdash

194

012

22th

3813

6mdash

Nysso

myiaspp

mdashmdash

mdash1

1mdash

1125

mdashmdash

mdashmdash

mdash38

136

17Ny

ssom

yiaan

tunesi

mdash2

9mdash

52

mdashmdash

1mdash

142

037

13th

19068

18Sciopemyiaflu

viatilis

21

3mdash

91

mdashmdash

mdashmdash

18019

18th

16057

19Micropygom

yiarorotaensis

4mdash

mdashmdash

8mdash

21

mdashmdash

178

02

17th

15054

20Psycho

dopygu

sparaensis

mdashmdash

mdashmdash

63

51

mdashmdash

176

02

17th

15054

21Psychodopygusclaustre

i7

1mdash

mdashmdash

mdash2

mdash3

1154

031

15th

14050

mdashPsychodopygusspp

4

mdash2

mdash6

mdash2

mdashmdash

mdashmdash

mdashmdash

14050

22Trich

ophoromyiaeurypyga

mdash8

mdashmdash

mdash3

mdash1

mdashmdash

182

018

19th

12043

23Psathyromyiaaragaoi

mdashmdash

52

mdashmdash

4mdash

mdashmdash

188

015

20th

11039

24Evandrom

yiabrachyphalla

43

21

1mdash

mdashmdash

mdashmdash

19014

21th

11039

25Psychodopyguscarreraicarrerai

11

mdash7

mdashmdash

mdashmdash

mdashmdash

202

008

26th

9032

26Evandrom

yiabegona

e2

2mdash

mdash4

mdashmdash

mdashmdash

mdash196

011

23th

8029

27Ny

ssom

yiawh

itman

imdash

mdashmdash

mdashmdash

mdash8

mdashmdash

mdash20

009

25th

8029

28Psathyromyiascaffi

32

mdashmdash

2mdash

mdashmdash

mdashmdash

198

01

24th

7025

29Pressatia

trispinosa

mdashmdash

mdash7

mdashmdash

mdashmdash

mdashmdash

204

007

27th

7025

30Micropygom

yiatrinidadensis

7mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

7025

31Viannamyiatuberculata

6mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

21004

30th

6021

32Pintom

yiadamascenoi

mdashmdash

mdashmdash

mdashmdash

5mdash

mdashmdash

20009

25th

5018

33Evandrom

yiaevandroi

mdashmdash

mdashmdash

41

mdashmdash

mdashmdash

204

007

27th

5018

34Psathyromyialutziana

5mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

212

003

31th

5018

35Brum

ptom

iatra

vasso

simdash

mdashmdash

mdashmdash

mdash3

1mdash

mdash196

011

23th

4014

36Evandrom

yiabacula

mdashmdash

mdashmdash

1mdash

3mdash

mdashmdash

202

008

26th

4014

37Evandrom

yiamonstruosa

mdashmdash

4mdash

mdashmdash

mdashmdash

mdashmdash

206

006

28th

4014

Journal of Tropical Medicine 5

Table1Con

tinued

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

38Psychodopygusa

mazonensis

mdashmdash

mdashmdash

22

mdashmdash

mdashmdash

21004

30th

4014

39Psychodopyguscorossoniensis

mdashmdash

mdashmdash

mdash2

mdashmdash

mdashmdash

206

006

28th

2007

40Pressatia

equatoria

lismdash

2mdash

mdashmdash

mdashmdash

mdashmdash

mdash21

004

30th

2007

41Psathyromyiainflata

mdashmdash

mdashmdash

mdashmdash

2mdash

mdashmdash

21004

30th

2007

42Micropygom

yiamicropyga

mdashmdash

mdashmdash

mdashmdash

11

mdashmdash

214

002

32th

2007

43Psychodopygusgenicu

latus

mdashmdash

mdash2

mdashmdash

mdashmdash

mdashmdash

218

033th

2007

44Lu

tzom

yiacarvalhoi

mdashmdash

1mdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

1004

45Psathyromyiapunctigenicu

lata

mdashmdash

mdashmdash

1mdash

mdashmdash

mdashmdash

216

001

32th

1004

Total

856

411

342

209

274

96415

186

74

2800

1000

1267

551

370

601

11Ea

chlocatio

ncomprise

dam

onito

ringstation(M

S)sampled

with

051and20

mCD

Ctrapsprovidingapproxim

ately

504h

MS

Cfem

aleDm

aleISAind

exof

speciesa

bund

anceSISAstand

ardindexof

speciesa

bund

ance

ldquothe

bold

italic

fontrdquoP

rovenandor

putativ

eACL

vectorsintheA

mazon

Region

based

inYo

ungandDun

can[1]Ra

ngelandLainson[4]Re

ady[2]andLainsonandShaw

[16]

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

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Disease Markers

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OncologyJournal of

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Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Computational and Mathematical Methods in Medicine

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Research and TreatmentAIDS

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

4 Journal of Tropical MedicineTa

ble1Ph

ebotom

inespeciescompo

sitionofSantoAnton

iodo

Jarihydroelectric

syste

mim

pacted

area

(AmapaS

tateA

mazon

ianBrazil)

ontheb

asisoffivesurveyedlocatio

ns(2012ndash2015)

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

1Sciopemyiasordellii

149

6613

1015

442

16mdash

136

087

2nd

316

1129

2Psycho

dopygu

sdavisi

4637

9556

1510

3817

mdashmdash

64

074

3rd

314

1121

mdashTrich

ophoromyiaspp

177

mdash34

mdash40

mdash17

mdashmdash

mdashmdash

mdashmdash

268

957

3Bichromom

yiafla

viscutellata

7632

2414

2211

5231

12

2095

1st

265

946

4Evandrom

yiainfra

spinosa

4410

2518

32

3018

mdashmdash

9206

6th

150

536

5Ny

ssom

yiaum

bratilis

2612

3130

196

139

mdashmdash

86

063

5th

146

521

6Trich

ophoromyiacasta

nheir

aimdash

104

mdash6

mdash14

mdash11

mdashmdash

112

051

9th

135

482

mdashPressatia

spp

43mdash

1mdash

9mdash

78mdash

mdashmdash

mdashmdash

mdash131

468

mdashEvandrom

yiaspp

5210

4mdash

3911

12mdash

mdashmdash

mdashmdash

mdash128

457

7Viannamyiafurcata

444

115

111

305

mdashmdash

104

055

7th

111

396

8Psycho

dopygu

ssqu

amiventrissensulato

3614

155

10mdash

9mdash

mdashmdash

11052

8th

89318

9Trich

opygom

yiatrichopyga

1116

98

9mdash

2112

mdashmdash

7207

4th

86307

10Tricho

phorom

yiaub

iquitalis

216

58

148

139

2mdash

114

05

10th

86307

11Evandrom

yiasaulensis

409

5mdash

44

121

mdashmdash

128

043

11th

75268

12Psycho

dopygu

shirs

utus

hirsutus

13mdash

204

144

mdashmdash

mdashmdash

136

04

12th

5519

613

Trich

ophoromyiabrachypyga

mdash36

mdash12

mdash2

mdash2

mdashmdash

152

032

14th

5218

614

Pressatia

choti

mdash17

mdash3

mdash5

mdash25

mdashmdash

142

037

13th

5017

915

Nyssom

yiaan

duzei

65

2410

mdashmdash

mdashmdash

mdashmdash

17023

16th

4516

116

Lutzom

yiagomezi

2711

mdashmdash

mdashmdash

mdashmdash

mdashmdash

194

012

22th

3813

6mdash

Nysso

myiaspp

mdashmdash

mdash1

1mdash

1125

mdashmdash

mdashmdash

mdash38

136

17Ny

ssom

yiaan

tunesi

mdash2

9mdash

52

mdashmdash

1mdash

142

037

13th

19068

18Sciopemyiaflu

viatilis

21

3mdash

91

mdashmdash

mdashmdash

18019

18th

16057

19Micropygom

yiarorotaensis

4mdash

mdashmdash

8mdash

21

mdashmdash

178

02

17th

15054

20Psycho

dopygu

sparaensis

mdashmdash

mdashmdash

63

51

mdashmdash

176

02

17th

15054

21Psychodopygusclaustre

i7

1mdash

mdashmdash

mdash2

mdash3

1154

031

15th

14050

mdashPsychodopygusspp

4

mdash2

mdash6

mdash2

mdashmdash

mdashmdash

mdashmdash

14050

22Trich

ophoromyiaeurypyga

mdash8

mdashmdash

mdash3

mdash1

mdashmdash

182

018

19th

12043

23Psathyromyiaaragaoi

mdashmdash

52

mdashmdash

4mdash

mdashmdash

188

015

20th

11039

24Evandrom

yiabrachyphalla

43

21

1mdash

mdashmdash

mdashmdash

19014

21th

11039

25Psychodopyguscarreraicarrerai

11

mdash7

mdashmdash

mdashmdash

mdashmdash

202

008

26th

9032

26Evandrom

yiabegona

e2

2mdash

mdash4

mdashmdash

mdashmdash

mdash196

011

23th

8029

27Ny

ssom

yiawh

itman

imdash

mdashmdash

mdashmdash

mdash8

mdashmdash

mdash20

009

25th

8029

28Psathyromyiascaffi

32

mdashmdash

2mdash

mdashmdash

mdashmdash

198

01

24th

7025

29Pressatia

trispinosa

mdashmdash

mdash7

mdashmdash

mdashmdash

mdashmdash

204

007

27th

7025

30Micropygom

yiatrinidadensis

7mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

7025

31Viannamyiatuberculata

6mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

21004

30th

6021

32Pintom

yiadamascenoi

mdashmdash

mdashmdash

mdashmdash

5mdash

mdashmdash

20009

25th

5018

33Evandrom

yiaevandroi

mdashmdash

mdashmdash

41

mdashmdash

mdashmdash

204

007

27th

5018

34Psathyromyialutziana

5mdash

mdashmdash

mdashmdash

mdashmdash

mdashmdash

212

003

31th

5018

35Brum

ptom

iatra

vasso

simdash

mdashmdash

mdashmdash

mdash3

1mdash

mdash196

011

23th

4014

36Evandrom

yiabacula

mdashmdash

mdashmdash

1mdash

3mdash

mdashmdash

202

008

26th

4014

37Evandrom

yiamonstruosa

mdashmdash

4mdash

mdashmdash

mdashmdash

mdashmdash

206

006

28th

4014

Journal of Tropical Medicine 5

Table1Con

tinued

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

38Psychodopygusa

mazonensis

mdashmdash

mdashmdash

22

mdashmdash

mdashmdash

21004

30th

4014

39Psychodopyguscorossoniensis

mdashmdash

mdashmdash

mdash2

mdashmdash

mdashmdash

206

006

28th

2007

40Pressatia

equatoria

lismdash

2mdash

mdashmdash

mdashmdash

mdashmdash

mdash21

004

30th

2007

41Psathyromyiainflata

mdashmdash

mdashmdash

mdashmdash

2mdash

mdashmdash

21004

30th

2007

42Micropygom

yiamicropyga

mdashmdash

mdashmdash

mdashmdash

11

mdashmdash

214

002

32th

2007

43Psychodopygusgenicu

latus

mdashmdash

mdash2

mdashmdash

mdashmdash

mdashmdash

218

033th

2007

44Lu

tzom

yiacarvalhoi

mdashmdash

1mdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

1004

45Psathyromyiapunctigenicu

lata

mdashmdash

mdashmdash

1mdash

mdashmdash

mdashmdash

216

001

32th

1004

Total

856

411

342

209

274

96415

186

74

2800

1000

1267

551

370

601

11Ea

chlocatio

ncomprise

dam

onito

ringstation(M

S)sampled

with

051and20

mCD

Ctrapsprovidingapproxim

ately

504h

MS

Cfem

aleDm

aleISAind

exof

speciesa

bund

anceSISAstand

ardindexof

speciesa

bund

ance

ldquothe

bold

italic

fontrdquoP

rovenandor

putativ

eACL

vectorsintheA

mazon

Region

based

inYo

ungandDun

can[1]Ra

ngelandLainson[4]Re

ady[2]andLainsonandShaw

[16]

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

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Research and TreatmentAIDS

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Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Journal of Tropical Medicine 5

Table1Con

tinued

Species

PortoSabao

Traıra

River

Iratapuru

Santo

Power

Plant

ISA

SISA

Rank

Total

Village

Anton

ioVillage

CD

CD

CD

CD

CD

38Psychodopygusa

mazonensis

mdashmdash

mdashmdash

22

mdashmdash

mdashmdash

21004

30th

4014

39Psychodopyguscorossoniensis

mdashmdash

mdashmdash

mdash2

mdashmdash

mdashmdash

206

006

28th

2007

40Pressatia

equatoria

lismdash

2mdash

mdashmdash

mdashmdash

mdashmdash

mdash21

004

30th

2007

41Psathyromyiainflata

mdashmdash

mdashmdash

mdashmdash

2mdash

mdashmdash

21004

30th

2007

42Micropygom

yiamicropyga

mdashmdash

mdashmdash

mdashmdash

11

mdashmdash

214

002

32th

2007

43Psychodopygusgenicu

latus

mdashmdash

mdash2

mdashmdash

mdashmdash

mdashmdash

218

033th

2007

44Lu

tzom

yiacarvalhoi

mdashmdash

1mdash

mdashmdash

mdashmdash

mdashmdash

208

005

29th

1004

45Psathyromyiapunctigenicu

lata

mdashmdash

mdashmdash

1mdash

mdashmdash

mdashmdash

216

001

32th

1004

Total

856

411

342

209

274

96415

186

74

2800

1000

1267

551

370

601

11Ea

chlocatio

ncomprise

dam

onito

ringstation(M

S)sampled

with

051and20

mCD

Ctrapsprovidingapproxim

ately

504h

MS

Cfem

aleDm

aleISAind

exof

speciesa

bund

anceSISAstand

ardindexof

speciesa

bund

ance

ldquothe

bold

italic

fontrdquoP

rovenandor

putativ

eACL

vectorsintheA

mazon

Region

based

inYo

ungandDun

can[1]Ra

ngelandLainson[4]Re

ady[2]andLainsonandShaw

[16]

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

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Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

6 Journal of Tropical Medicine

Table 2 Vertical stratification of Phebotomine species composition of Santo Antonio do Jari hydroelectric system impacted area (AmapaState Amazonian Brazil) on the basis of five surveyed locations (2012ndash2015)

Species 05m ground 1m ground 20m canopy TotalC D C D C D

1 Sciopemyia sordellii 117 71 91 23 11 3 3162 Psychodopygus davisi 48 27 44 39 102 54 314mdash Trichophoromyia spp 117 mdash 127 mdash 24 mdash 2683 Bichromomyia flaviscutellata 85 45 79 41 11 4 2654 Evandromyia infraspinosa 38 18 48 27 16 3 1505 Nyssomyia umbratilis 35 23 26 13 28 21 1466 Trichophoromyia castanheirai mdash 50 mdash 59 mdash 26 135mdash Pressatia spp 66 mdash 39 mdash 26 mdash 131mdash Evandromyia spp 55 12 41 9 11 mdash 1287 Vianamyia furcata 42 8 46 6 8 1 1118 Psychodopygus squamiventris sl 27 11 20 1 23 7 899 Trichopygomyia trichopyga 18 20 10 5 22 11 8610 Trichophoromyia ubiquitalis 28 15 16 13 9 5 86mdash Other species (11ndash45) 137 112 129 69 71 57 575

Total 813 412 716 305 362 192 2800Total (C + D) 1225 1021 554 mdash

Each stratum was sampled with approximately 840 h of CDC trapC female D male

infraspinosa (119899 = 150 SISA = 06) and Ny umbratilis (119899 =146 SISA = 063) Less frequently captured but nonethelessepidemiologically relevant species included Ps squamiventrissl (119899 = 89 SISA = 052) Th ubiquitalis (119899 = 86 SISA=05)Ps hirsutus hirsutus (119899 = 55 SISA = 04)Ny anduzei (119899 = 45SISA = 023) Lutzomyia gomezi (119899 = 38 SISA = 012) Nyantunesi (119899 = 19 SISA = 037) Ps paraensis (119899 = 15 SISA =02) and Ny whitmani (119899 = 8 SISA = 009)

Sampling effort for each area comprised approximately504 h of CDC trapping (14 expeditions 3 CDC traps and12-hour CDC exposition) Porto Sabao was the site of themost captured specimens (1267) followed by Santo AntonioVillage (601) The highest diversity was observed in capturesfrom Iratapuru Village (1198671015840 = 3027) All 1198671015840 value com-parisons between the different environments were significant(119901 le 005) except when comparing Traıra River and thePower Plant (119901 le 0099) (Figure 2)

Regarding vertical distribution sampling of the samecaptures described above accounted for approximately 840 hof CDC trapping by stratum (14 expeditions 5 ecotopes and12-hour CDC exposition) CDC traps placed 05m aboveground level accounted for a greater number of individuals(1225) than those placed 1m above ground level (1021) and20m above ground level in the canopy (554) (Table 2) WhilePs davisi was most likely to be found at canopy level (75individuals at 05m 83 at 1m and 156 at 20m) and Biflaviscutellata closer to ground level (130 at 05m 120 at 1mand 15 at 20m) there was little difference in numbers of Nyumbratilis individuals captured at the different levels of strata(58 at 05m 39 at 1m and 49 at 20m)

The monthly average rainfall was the only climatic datawith a representative coefficient of variance (1198781015840 = 7081)whentested against ACL occurrence and phlebotomine frequency

005

115

225

335

PortoSabatildeo

TraiacuteraRiver

IratapuruVillage

Santo AntocircnioVillage

PowerPlant

p = 0009p = 0099

p = 0007

p = 0012p = 0001

p = 0031

p = 0001p = 0004

p = 0001p = 00012855

26543027

2819

1468

Figure 2 Comparison of Shannon diversity indexes for CDC-captured phlebotomines from the five surveyed locations in SantoAntonio do Jari hydroelectric system impacted area between thestates of Para and Amapa Brazil (2012ndash2015)

(1198781015840 = 6595) in contrast to temperature (1198781015840 = 596)and relative air humidity (1198781015840 = 956) The available dataenabled correlations to be determined between the periodsof May 2012 to April 2015 a period within which nine of thefourteen capture efforts were undertaken Rainfall presenteda moderate correlation with overall phlebotomine frequency(119903 = 065 119901 = 000001) as also individually compared withPs squamiventris sl (119903 = 065 119901 = 000001) and a similarlymoderate but lower correlation with Bi flaviscutellata (119903 =048 119901 = 00021) and Ny umbratilis (119903 = 048 119901 = 0002)

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Journal of Tropical Medicine 7

A decrease in the overall phlebotomine population wasobserved after March until November 2014 coinciding withthe transition between the rainy and dry periods and withflooding (Figure 3)

The number of ACL cases presented a moderate cor-relation with overall phlebotomine frequency (119903 = 044119901 = 00063) and also with Ps squamiventris (119903 = 032119901 = 00003) and an insignificant negative correlation with Biflaviscutellata (119903 = minus002 119901 = 00001) A similarly moderatebut higher correlation was however found withNy umbratilis(119903 = 048 119901 = 0002) (Figure 4)

4 Discussion

It is important to consider current investigations of phle-botomine fauna in the Jari River Basin in the context ofthe historical findings from the 1970s and 1980s Theseearlier studies represent comprehensive research conductedin Monte Dourado (northern PA) a region close to thearea investigated in the present study and on which thepresent epidemiological background to ACL transmissionin the associated region is based In brief the previousresearch includes a description of Ny umbratilis (formerlyldquoobscuredrdquo as Ny anduzei) [13] and its incrimination as themain vector of L (V) guyanensis [9ndash11] confirmed by strongecological associations [15] Just as important a parasitemore recently described as L (V) naiffi was isolated fromthe armadilloDasypus novemcinctus for which transmissionwas locally driven and attributed to Ps squamiventris sl andother Psychodopygus species [22] this comprised a primarilyenzootic ACL occasionally infecting humans [23] Finallythe isolation of L (L) amazonensis from rodents in an areaaffected by occurrence of the main vector Bi flaviscutellata[11] comprised the third known Jari ACL transmission cycleThese facts described above suggest that Ny umbratilis Pssquamiventris sl and Bi flaviscutellata are implicated in thetransmission scenario of the area covered by the present studyand thus merit particular attention

The present study incorporated a representative compo-sition of the known AP fauna Considering the substantialsampling effort (2520 h) the determined diversity showedagreement with the findings of other inventories from theBrazilian Amazon basin [1 24] Moreover all new records forAP have already been recorded for PA [25]

Apart from Ny umbratilis Ps squamiventris sl and Biflaviscutellata other species captured were noted as beingepidemiologically relevant to ACL in the Brazilian AmazonRegion Ps paraensis Ps davisi and Ps hirsutus hirsutuswhich are putative vectors of L (V) naiffi [26 27] Thubiquitalis a proven vector of L (V) lainsoni [28] Nyanduzei a secondary vector of L (V) guyanensis [4] Nywhitmani and Lu gomezi proven and putative vectors of L(V) shawi respectively [4 26] and lastly Ny antunesi asuspected vector of L (V) lindenbergi [4]

Among the above species Ps davisi is notable as thethird highest ranking according to SISA (074) and as havingthe highest presence in all vertical strata in particular atthe canopy level This species is generally anthropophilic iswidely distributed in the Amazon Basin [1 24] and is related

to Leishmania (Viannia) infections in the States of Rondonia(RO) [29] and PA [27 30] Interestingly this species remainsfrequent in recently surveyed areas affected by hydroelectricschemes in RO [8] and PA (TVS unpublished) Theseobservations add weight to the need for further investigationinto the putative epidemiological role of Ps davisi in Jari

The species most frequently captured Sc sordellii wouldappear not to be of epidemiological concern Firstly theapparent abundance of a given phlebotomine species is notsufficient of itself to incriminate it as a vector [31] particularlywhen it does not demonstrate high levels of anthropophilicbehavior Secondly flagellate infections isolated from thisspecies (formerly referred to as Lutzomyia nordestina) arehistorically recognized as distinct from Leishmania [22] orremain undetermined [32] and are more likely to be othertrypanosomatids [22] Furthermore despite recent reports ofmolecular Leishmania ascribed to this fly [33 34] currentlypolymerase chain reaction-based techniques do not allowldquotrue infectionrdquo to be distinguished from a ldquosimple and occa-sionally ingestedrdquo DNA fragment [3] Thus there remainsinsufficient evidence for a potential vector role of S sordelliiin Leishmania transmission

High frequencies of light-trapped Bi flaviscutellata havebeen documented [8 35] despite rodent-baited trappingbeing better recognized as amethod for attracting the speciesAdditionally the first SISA Rank (095) was indicative ofthis high presence in all five surveyed ecotopes this hasbeen observed in the Belem metropolitan area (PA) whereBi flaviscutellata was the only omnipresent species in sevenurban and ecologically isolated forest fragments surveyed[36] Furthermore this species has been reported as beingable to adapt to plantations of introduced tree species and inother nonclimax forests in Jari [14] suggesting it is capableof responding positively to environmental change such asthe vegetal suppression and flooding caused by hydroelectricoperations Nonetheless ecological niche model projectionspredict no change in spatial distribution for Bi flaviscutellatain the Jari area which is an environment that remains suitablefor the species [37]

In an area in Regina French Guiana ecologically dis-turbed due to agricultural practices flagellates infecting a Biflaviscutellata specimen have been determined to be L (V)guyanensis [38] in similar circumstances to the observed lowpresence of Ny umbratilis Although this possibly changingpattern in ACL transmission should be interpreted withcaution it raises an intriguing possibility about the permis-siveness of Bi flaviscutellata to L (V) guyanensis in theAmazonGuianan ACL scenario

In the present study a higher number of Bi flaviscutellataindividuals was captured compared to Ny umbratilis (265versus 146 resp) A lack of available evidence for naturalinfection in this unnatural vectorparasite system howeverprecludes speculation about the possible involvement of Biflaviscutellata even in the context of occasional transmissionof parasites distinct from L (L) amazonensis Neverthelessthe current high occurrence of Bi flaviscutellata in theAmazonGuianan ACL scenario may be of future concernunnatural parasitevectorreservoir systems when closelyrelated in an ecological context can on a century-level scale

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

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Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

8 Journal of Tropical Medicine

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

0100200300400500600

050

100150200250300350400

2012 2013 2014 2015

Wat

erflo

odin

g

Ps s

quya

miv

entri

s sl

Bi fl

avisc

utell

ata

Ny u

mbr

atili

s

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

050

100150200250300350400

050

100150200250300350400

050

100150200250300350400

010203040506070

10000 20000 30000 40000000Rainfall (mm)

01020304050607080

10000 20000 30000 40000000Rainfall (mm)

Rainfall (mm)Overall

Rainfall (mm)

Rainfall (mm)

Rainfall (mm)

0100200300400500600

Ove

rall

10000 20000 30000 40000000Rainfall (mm)

05

10152025303540

10000 20000 30000 40000000Rainfall (mm)

r = 065 p = 000001

r = 048 p = 00021

r = 049 p = 00021

r = 065 p = 000001

Figure 3 Correlation between rainfall and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Journal of Tropical Medicine 9

2012 2013 2014 2015

Wat

erflo

odin

g

0100200300400500600

010203040506070

Bi flaviscutellata

01020304050607080

Ny umbratilis

0510152025303540

Ps squamiventris sl

Bi fl

avisc

utell

ata

05

1015202530

05

1015202530

05

1015202530

05

1015202530

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

May Ju

lSe

pN

ov Jan

Mar

0100200300400500600

Ove

rall

10 20 300ACL cases

010203040506070

10 20 300ACL cases

01020304050607080

Ny u

mbr

atili

s

10 20 300ACL cases

ACL casesOverall

ACL cases

ACL cases

ACL cases

05

10152025303540

Ps s

quam

iven

tris s

l

10 20 300ACL cases

r = 044 p = 00063

r = minus002 p = 00001

r = 048 p = 0002

r = 032 p = 00003

Figure 4 Correlation between ACL cases and phlebotomine putative vector species captured in Santo Antonio do Jari hydroelectric systemimpacted area between the states of Para and Amapa Brazil (2012ndash2015)

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

10 Journal of Tropical Medicine

undergo stress adaptation (evolutionary fitness) and formnew ecological systems driven by coevolution [39]

There is no doubt that Ny umbratilis is the main vectorof ACL in the Jari River Basin [15] Surprisingly the well-documented tree-dwelling behavior of this species [15 40]was not observed in CDC canopy captures in the presentstudy very little difference was found between the number ofindividuals captured in the three sampled strata (58 at 05m39 at 1m and 49 at 20m) Although Ny umbratilis is knownto climb into the canopy at night to feed on edentates (mainlysloths) [12 41] it is possible that an alternative terrestrialsource of blood such as rodents may be attracting femalestoward ground level Sloths are very slow moving and aretherefore commonly rescued for relocation during environ-mentalmonitoring operations their resulting rarenessmeansNy umbratilis has had to find other food sources Converselyblood meal analysis conducted during studies in a forestfragment of the Western Amazon has shown rodent bloodto be the predominant feeding source for Ny umbratilis [42]Wild and synanthropic rodents have been shown to surviveenvironmental disturbance in Jari and to proliferate in areasof introduced tree species [14] this indicated a plausiblereason not only for the putative adaptation of Ny umbratilisbut also for the increasing population levels of the rodentblood-feeder Bi flaviscutellata as already discussed

Given the clear importance of Psychodopygus of theChagasi series (formerly referred to as the Squamiventrisseries) in the context of ACL transmission [22] taxonomicstudies on identifying the cryptic females have been under-taken previously [43] and more recently with interestingresults (Rodrigo E Godoy unpublished) These techniqueshowever could not be employed in the field at the time Earlyconsideration of the assumed geographic distribution of thecomplex Ps squamiventris sl [1 44] shows that individualsfrom AP are likely to be predominantly Ps s maripaensisDetermining males of the species present could clarify thesetaxonomic uncertainties in the area covered by the presentstudy however doubts about identification of some malespecimens meant they were grouped as Ps squamiventris sl

Ryan et al [22] did not find Ps squamiventris sl to benaturally infected in the Jari area but proposed a link to L(V) naiffi along the same northern bank of the AmazonRiver through studies in Cachoeira Porteira (PA) Fouqueet al [38] came to the same conclusions in French GuianaInterestingly this fly species complex was found alongside L(V) braziliensis DNA in Suriname [45] an area where theknown Amazonian vectors of this parasite Ps complexus andPs wellcomei are unlikely to occur As previously discussedin the context of Bi flaviscutellata the changing transmissionpatterns of unnatural vectorparasite systems must be care-fully interpreted and only after strong ecological associationshave been determined Thus the putative vector importanceof Ps squamiventris sl in Jari can only be assumed in respectof L (V) naiffi

The five surveyed areas presented in general differentdiversity indexes showing variations in the phlebotominecomposition along the affected area This finding can beattributed not only to the distance between capture sitesbut also to forest composition fragmentation geographic

barriers and migration of mammal fauna between sites thislatter can occur naturally or be induced by rescue opera-tions involved in hydroelectric planning whereby animalsare moved to suitable ldquodry landrdquo environments safe frompotential flooding

A decrease in the phlebotomine population in 2014 inthe period after filling the reservoir could not be attributedexclusively either to flooding or to the transition from therainy to the dry season Both eventualities although oppositein effect are likely to lead to unsuitable conditions forphlebotomine reproduction However they did coincide inMay 2014 when rainfall decreased and the lake was formed

Conversely rainfall was a valid determinant of overallphlebotomine fluctuation Ps squamiventris sl was the mainputative vector directly correlated with this Other variablessuch as forest composition and altitudinal variation areknown to influence seasonal dynamics of species from thecomplex Ps squamiventris sl For example the dry periodfrom October to November in Serra dos Carajas (southernPA) can be unsuitable for Ps wellcomei which is adapted tohigh altitudes in contrast to Ps complexus which flourishesin lowland areas during the same months [46]

An insignificant negative to a moderate positive correla-tion was observed between cases of ACL and phlebotominefluctuations In the case of Ny umbratilis however theapparently higher correlation when compared with otherspecies is in agreement with its known vector importance inAmazonGuianan ACL A strong spatiotemporal associationbetween a given vector and ACL cases is considered essentialto maintenance of the Leishmania life cycle [2 14]

In summary the present study filled a temporal gapon phlebotomine data relating to the Jari area It providesa meaningful update on species composition and furtherinsights into seasonal dynamics of species under pressurescaused by environmental change The presence of ACLvectors in particular Ny umbratilis Bi flaviscutellata andPs squamiventris sl is noteworthy due to their directassociation with AmazonGuianan-ACL transmission ForNy umbratilis the lower frequency associatedwith the unpre-dicted lack of tree-dwelling behavior may be attributableto a reduction in numbers of canopy-dwelling mammalsdue to the environmental disturbance and relocation effortsthis could consequently have led to seeking for alternativeterrestrial blood sources at ground level The possible asso-ciation of Ps davisi with Leishmania transmission cycles inother Amazon ecoregions draws attention to its high rankposition in Jari Rainfall can be partly associated with localseasonal fluctuations in fly numbers mainly with respect toPs squamiventris sl Cases of ACL were also more highlycorrelated with Ny umbratilis dynamics Further attentionwas also given to results for Bi flaviscutellata which hasbeen apparently tolerant of anthropic activity continuedphlebotominemonitoring is proposed in order to evaluate theimplication for social welfare and health in the future

Competing Interests

The authors declare that they have no competing interests

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Journal of Tropical Medicine 11

Acknowledgments

Theauthorswish to thank the ldquoInstituto de Pesquisas Cientıfi-cas e Tecnologicas do Estado do Amapa IEPArdquo entomologyteam for the technical assistance given to the field work inparticular to Aderbal Amanajas Santana Rosalvo Dias deCastro Noel Fernandes Santos Neto Osita Cleyriane Lobatodo Nascimento Jose Luiz dos Santos Chaves and Joao doSocorro Gomes Campos Logistical facilities were financiallysupported by the ldquoJari Energiardquo

References

[1] D G Young and M A Duncan ldquoGuide to the identificationand geographic distribution of Lutzomyia sand flies in Mexicothe West Indies Central and South America (Diptera Psycho-didae)rdquo inMemoirs of the American Entomological Institute pp1ndash881 Associated Publishers American Entomological InstituteGainesville Fla USA 1994

[2] P D Ready ldquoBiology of phlebotomine sand flies as vectors ofdisease agentsrdquo Annual Review of Entomology vol 58 pp 227ndash250 2013

[3] R P Brazil A A Fuzzari and J D Andrade Filho ldquoSandfly vectors of Leishmania in the Americasmdasha mini reviewrdquoEntomology Ornithology amp Herpetology vol 4 no 2 Article ID1000144 2015

[4] E F Rangel and R Lainson ldquoProven and putative vectorsof American cutaneous leishmaniasis in Brazil aspects oftheir biology and vectorial competencerdquoMemorias do InstitutoOswaldo Cruz vol 104 no 7 pp 937ndash954 2009

[5] E F Rangel S M Costa and B M Carvalho ldquoEnvironmentalchanges and the geographic spreading of American cutaneousleishmaniasis in Brazilrdquo in Leishmaniasis-Trends in Epidemiol-ogy D Claborn Ed Diagnosis and Treatment InTech RijekaCroatia 2014

[6] W P Taddei ldquoO genero Mansonia (Diptera Culicidae) e aproliferacao de mosquitos na usina hidreletrica de Tucuruırdquo inEnergia na Amazonia S B Magalhaes R C Brito and E RCastro Eds vol 1 pp 311ndash318 MPEGFPAUNAMAZ BelemBrazil 1996 (Portuguese)

[7] A I A Oliveira Observacoes Sobre a Resolucao CONAMA no23797 que Dispoe Sobre o Licenciamento Ambiental MimeoConselho Empresarial Brasileiro Para o Desenvolvimento Sus-tentavel Rio de Janeiro Brazil 1997 (Portuguese)

[8] A K R Galardo C D Galardo G A Silveira et al ldquoPhle-botominae sand flies (Diptera Psychodidae) potential vectorsof American cutaneous leishmaniasis agents in the area asso-ciated with the Santo Antonio hydroelectric system in WesternAmazonian Brazilrdquo Revista da Sociedade Brasileira deMedicinaTropical vol 48 no 3 pp 265ndash271 2015

[9] R Lainson R DWard and J J Shaw ldquoCutaneous leishmaniasisin North Brazil Lutzomyia anduzei as a major vectorrdquo Transac-tions of the Royal Society of Tropical Medicine and Hygiene vol70 no 2 pp 171ndash172 1976

[10] R Lainson J J Shaw R D Ward P D Ready and R DNaiff ldquoLeishmaniasis in Brazil XIII Isolation of Leishmaniafrom armadillos (Dasypus novemcinctus) and observations onthe epidemiology of cutaneous leishmaniasis in north ParaStaterdquo Transactions of the Royal Society of Tropical Medicine andHygiene vol 73 no 2 pp 239ndash242 1979

[11] R Lainson J J Shaw P D Ready M A Miles and M PovoaldquoLeishmaniasis in Brazil XVI Isolation and identification of

Leishmania species from sandflies wild mammals and manin north Para State with particular reference to L braziliensisguyanensis causative agent of ldquopian-boisrdquordquo Transactions of theRoyal Society of Tropical Medicine and Hygiene vol 75 no 4pp 530ndash536 1981

[12] R Lainson J J Shaw and M Povoa ldquoThe importance of eden-tates (sloths and anteaters) as primary reservoirs of Leishmaniabraziliensis guyanensis causative agent of lsquopian boisrsquo in northBrazilrdquo Transactions of the Royal Society of Tropical Medicineand Hygiene vol 75 no 4 pp 611ndash612 1981

[13] R DWard and H Fraiha ldquoLutzomyia umbratilis a new speciesof sand fly from Brazil (Diptera Psychodidae)rdquo Journal ofMedical Entomology vol 14 no 3 pp 313ndash317 1977

[14] P D Ready R Lainson and J J Shaw ldquoLeishmaniasis in BrazilXX Prevalence of lsquoenzootic rodent leishmaniasisrsquo (Leishmaniamexicana amazonensis) and apparent absence of lsquopian boisrsquo(Le braziliensis guyanensis) in plantations of introduced treespecies and in other non-climax forests in eastern AmazoniardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 77 no 6 pp 775ndash785 1983

[15] P D Ready R Lainson J J Shaw and R DWard ldquoThe ecologyof Lutzomyia umbratilisWard amp Fraiha (Diptera Psychodidae)the major vector to man of Leishmania braziliensis guyanensisin north-eastern Amazonian Brazilrdquo Bulletin of EntomologicalResearch vol 76 no 1 pp 21ndash40 1986

[16] R Lainson and J J Shaw ldquoLeishmania (Viannia) naiffi spn a parasite of the armadillo Dasypus novemcinctus (L)in Amazonian Brazilrdquo Annales de Parasitologie Humaine etComparee vol 64 no 1 pp 3ndash9 1989

[17] A Roger M Nacher M Hanf et al ldquoClimate and leishmaniasisin French guianardquo The American Journal of Tropical Medicineand Hygiene vol 89 no 3 pp 564ndash569 2013

[18] L Ryan ldquoFlebotomos do estado do Para Brasil (Diptera Psy-chodidae)rdquo Thecnical Document 1 Instituto Evandro ChagasBelem Brazil 1986 (Portuguese)

[19] E A B Galati ldquoMorfologia e Taxonomia Morfologia termi-nologia de adultos e identificacao dos taxons da Americardquoin Flebotomıneos do Brasil E F Rangel and R LainsonEds pp 53ndash75 Editora Fiocruz Rio de Janeiro Brazil 2003(Portuguese)

[20] D R Roberts and B P Hsi ldquoAn index of species abundance foruse with mosquito surveillance datardquo Environmental Entomol-ogy vol 8 no 6 pp 1007ndash1013 1979

[21] Oslash Hammer D A T Harper and P D Ryan ldquoPast paleontolog-ical statistics software package for education and data analysisrdquoPalaeontologia Electronica vol 4 no 1 pp 1ndash9 2001

[22] L Ryan R Lainson J J Shaw R R Braga and E A IshikawaldquoLeishmaniasis in Brazil XXV Sandfly vectors of Leishmania inPara State Brazilrdquo Medical and Veterinary Entomology vol 1no 4 pp 383ndash395 1987

[23] R Lainson J J Shaw F T Silveira R R Braga and E AIshikawa ldquoCutaneous leishmaniasis of man due to Leishmania(Viannia) naiffirdquo Annales de Parasitologie Humaine et Compa-ree vol 65 no 5-6 pp 282ndash284 1990

[24] E G C Bermudez Lutzomyia Sand Flies in the BrazilianAmazon Basin (Diptera Psychodidae) INPA Manaus Brazil2009

[25] G M Aguiar and W M Medeiros ldquoDistribuicao regionale habitats das especies de flebotomıneos do Brasilrdquo in Fle-botomıneos do Brasil E F Rangel and R Lainson Eds pp 207ndash256 Fiocruz Rio de Janeiro Brazil 2003 (Portuguese)

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

12 Journal of Tropical Medicine

[26] J R Arias M A Miles R D Naiff et al ldquoFlagellate infectionsof Brazilian sand flies (Diptera Psychodidae) isolation invitro and biochemical identification of Endotrypanum andLeishmaniardquo The American Journal of Tropical Medicine andHygiene vol 34 no 6 pp 1098ndash1108 1985

[27] A A Souza T V Santos Y L Jennings et al ldquoNaturalLeishmania(Viannia) spp infections in phlebotomine sand flies(Diptera Psychodidae) from the Brazilian Amazon regionreveal new putative transmission cycles of American cutaneousleishmaniasisrdquo Parasite vol 23 article 22 2016

[28] F T Silveira A A Souza R Lainson J J Shaw R R Bragaand E A Ishikawa ldquoCutaneous leishmaniasis in the AmazonRegion natural infection of the sand fly Lutzomyia ubiquitalis(Psychodidae Phlebotominae) by Leishmania (Viannia) lain-soni in Para state BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 86 no 1 pp 127ndash130 1991

[29] LH S Gil S A Basano A A Souza et al ldquoRecent observationson the sand fly (Diptera Psychodidae) fauna of the state ofRondonia Western Amazonia Brazil the importance of Psych-dopygus davisi as a vector of zoonotic cutaneous leishmaniasisrdquoMemorias do Instituto Oswaldo Cruz vol 98 no 6 pp 751ndash7552003

[30] A A A Souza F T Silveira R Lainson et al ldquoThe Phlebotom-inae fauna of Serra dos Carajas Para Brazil and its possibleimplication in the transmission of American tegumentaryleishmaniasisrdquo Revista Pan-Amazonica de Saude vol 1 no 1pp 45ndash51 2010

[31] R Killick-Kendrick ldquoPhlebotomine vectors of the leishmani-ases a reviewrdquoMedical and Veterinary Entomology vol 4 no 1pp 1ndash24 1990

[32] M E C Dorval G Cristaldo H C da Rocha et al ldquoPhle-botomine fauna (Diptera Psychodidae) of an American cuta-neous leishmaniasis endemic area in the state of Mato Grossodo Sul Brazilrdquo Memorias do Instituto Oswaldo Cruz vol 104no 5 pp 695ndash702 2009

[33] V C F V Guimaraes P L Costa F J da Silva et al ldquoMoleculardetection of Leishmania in phlebotomine sand flies in a cuta-neous and visceral leishmaniasis endemic area in northeasternBrazilrdquo Revista do Instituto de Medicina Tropical de Sao Paulovol 56 no 4 pp 357ndash360 2014

[34] R S Lana E M Michalsky C L Fortes-Dias et al ldquoPhle-botomine sand fly fauna and Leishmania infection in thevicinity of the Serra do Cipo National Park a natural Brazilianheritage siterdquo BioMed Research International vol 2015 ArticleID 385493 9 pages 2015

[35] V R Alves R A de Freitas F L Santos A F J de OliveiraT V Barrett and P H F Shimabukuro ldquoSand flies (DipteraPsychodidae Phlebotominae) from central amazonia and fournew records for the Amazonas State Brazilrdquo Revista Brasileirade Entomologia vol 56 no 2 pp 220ndash227 2012

[36] J V S Ferreira T V Santos E M Santos and I S GorayebldquoPhlebotomine sand flies (Diptera Psychodidae) in forestfragments of Belem metropolitan area Para State Brazil withconsiderations on vectors of American cutaneous leishmaniasisagentsrdquo Revista Pan-Amazonica de Saude vol 5 no 2 pp 29ndash35 2014

[37] B M Carvalho E F Rangel P D Ready and M M ValeldquoEcological niche modelling predicts southward expansion ofLutzomyia (Nyssomyia) flaviscutellata (Diptera PsychodidaePhlebotominae) vector of Leishmania (Leishmania) amazonen-sis in South America under climate changerdquo PLoS ONE vol 10no 11 Article ID e0143282 2015

[38] F Fouque P Gaborit J Issaly et al ldquoPhlebotomine sand flies(Diptera Psychodidae) associatedwith changing patterns in thetransmission of the human cutaneous leishmaniasis in FrenchGuianardquoMemorias do Instituto Oswaldo Cruz vol 102 no 1 pp35ndash40 2007

[39] R Killick-Kendrick ldquoSome epidemiological consequences ofthe evolutionary fit between Leishmaniae and their phle-botomine vectorsrdquo Bulletin de la Societe de Pathologie Exotiqueet de ses Filiales vol 78 no 5 pp 747ndash755 1985

[40] F X Pajot F Le Pont BGentile andR Besnard ldquoEpidemiologyof leishmaniasis in French Guianardquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 76 no 1 pp 112ndash113 1982

[41] H A Christensen J R Arias A M De Vasquez and R ADe Freitas ldquoHosts of sandfly vectors of Leishmania braziliensisguyanensis in the central Amazon of Brazilrdquo The AmericanJournal of Tropical Medicine and Hygiene vol 31 no 2 pp 239ndash242 1982

[42] L C R Nery E S Lorosa andAM R Franco ldquoFeeding prefer-ence of the sand flies Lutzomyia umbratilis and L spathotrichia(Diptera Psychodidae Phlebotominae) in an urban forest patchin the City ofManaus Amazonas BrazilrdquoMemorias do InstitutoOswaldo Cruz vol 99 no 6 pp 571ndash574 2004

[43] PD Ready R Lainson J J Shaw andAA Souza ldquoDNAprobesfor distinguishing Psychodopygus wellcomei from Psychodopy-gus complexus (Diptera Psychodidae)rdquo Memorias do InstitutoOswaldo Cruz vol 86 no 1 pp 41ndash49 1991

[44] P D Ready H Fraiha R P Lane J R Arias and F X PajotldquoOn distinguishing the female of Psychodopygus wellcomei avector of mucocutaneous leishmaniasis from other squamiven-tris series females I Characterization of Ps squamiventrissquamiventris and Ps s maripaensis stat nov (Diptera Psycho-didae)rdquo Annals of Tropical Medicine and Parasitology vol 76no 2 pp 201ndash214 1982

[45] A D Kent T V dos Santos A Gangadin A Samjhawan DR A Mans and H D F H Schallig ldquoStudies on the sandfly fauna (Diptera Psychodidae) in high-transmission areas ofcutaneous leishmaniasis in the Republic of Surinamerdquo Parasitesand Vectors vol 6 no 1 article 318 2013

[46] P D Ready R Lainson and J J Shaw ldquoHabitat and seasonalityof Psychodopygus wellcomei help incriminate it as a vector ofLeishmania braziliensis in Amazonia and Northeast BrazilrdquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 78 no 4 pp 543ndash544 1984

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom