Tardigrade distribution in a medium-sized city of central Argentina

Marıa Cristina Moly de Peluffo*, Julio Ricardo Peluffo, Alejandra Mariana Rocha& Irene Luisa DomaFacultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa, Uruguay 151, 6300,Santa Rosa, La Pampa, Argentina(*Author for correspondence: Tel.: +54-2954-43-6787; Fax: +54-2954-43-2535; E-mail: molpel@cpenet.com.ar)

Key words: urban environment, tardigrades, Argentina, bioindicators

Abstract

The distribution and abundance of tardigrades in the city of General Pico (Argentina) are analyzed fromsamples collected during autumn and spring 2001. Sample sites included paved urban locations withdifferent traffic intensities, non-paved periurban places, and places with peculiar conditions such as the cityindustrial area and the bus station. Trees of the same species were selected in each area and from each ofthem nine subsamples of lichens and/or moss, 11 mm in diameter, were taken with steel corers. Thediversity, density and relative abundance of tardigrades was recorded and analyzed. Sampling sites wereordinated and classified with PCA and clustering. The number total of species collected in the research was5. The maximum number of species per site and per tree was 4. The species recorded were: Echiniscusrufoviridis, Milnesium cf. tardigradum, Ramazzottius oberhaeuseri, Macrobiotus areolatus and an unde-scribed species of the genus Macrobiotus. The average density was approximately 10 specimens per cm2 andthe maximum values reach over 50 specimens per cm2. R. oberhaeuseri and M. cf. tardigradum were themost frequent species. R. oberhaeuseri dominates in periurban areas with high suspension dust and veryexposed to the sun. M. cf. tardigradum dominates on paved streets with intense vehicle traffic. Resultssupported the hypothesis of the relationship between air quality and tardigrade diversity.

Introduction

As occurs with other organisms, tardigrades havebeen more thoroughly studied in the wild than inurbanized environments. There are few observa-tions on city-dwelling tardigrades (Kinchin, 1994)and these are restricted to the northern hemi-sphere. Examples are the papers by Semeria (1981,1982) for France, Meininger et al. (1985) for USA,Utsugi (1986) for Japan and Steiner (1994a, b, c)for Switzerland.

Knowledge on animals living in the urban areamay allow, among other things, to establish thetolerance of the different species to the peculiarconditions of these environments (Semeria, 1981).Meininger et al. (1985) found that DiphasconscoticumMurray dominated in dry areas with poor

air quality while other species such as Milnesiumtardigradum Doyere thrived under opposite con-ditions. Their results also suggest a positive rela-tionship between the species richness of urbantardigrades and the environment humidity and airquality. Steiner (1994b, c) observed that the moss-dwelling fauna of Zurich was sensitive to pollutionand qualitatively stable over several years. It canbe concluded that this fauna may be a convenientbiological system for measuring levels of air pol-lution. Steiner also stated that because of the closesimilarity between the moss-dwelling and edaphicfaunas, the former can be a sensitive enough toolfor measuring the ecological consequences ofpollution on the soil biota.

The poor quality of the urban environment is amajor concern in Latin America and the Carib-

Hydrobiologia (2006) 558:141–150 � Springer 2006J.R. Garey, D.R. Nelson & P.B. Nichols (eds), The Biology of TardigradesDOI 10.1007/s10750-005-1413-9

bean. While much attention has been devoted toair pollution in large cities, much less is knownabout the large number of small and medium sizedcities in which about 47% of the urban populationof the region lives (de Vries, 2001). Thus theimportance of studying possible bioindicators ofair quality such as tardigrades that inhabit thissize-class of cities.

Systematic studies on urban tardigrades areonly beginning in the Neotropical region. Duringthe past few years studies in this direction havebeen undertaken in the province of La Pampa(Argentina) (Peluffo et al., 2000, 2002; Rochaet al., 2002). In this contribution we analyze thedistribution and abundance of epiphytic tardi-grades found in the city of General Pico, in sam-ples collected in autumn and spring 2001.

Study area

General Pico (35� 40¢ S; 63� 44¢ W) is located inthe northeastern part of the province of La Pampa(Fig. 1), at 143 m above sea level. It lies in thesemi-arid region and in the bioclimatic classifica-tion of Argentina (IRAM 11.603, 1996), it classesas Zone IIIa – which is defined as warm temperate.Average summer temperatures are in the 20–26 �Cand the maximum average reach over 30 �C.Winter temperatures show averages that rangebetween 8 and 12 �C and minimums below 0 �C.Daily thermal variation is over 14 �C. Annualaverage relative humidity is 71%. Annual rainfallaverage of the decade is approximately 800 mm.The stable population of the city is about 52,000inhabitants. General Pico is a regional commercial

Figure 1. Map of South America, Argentina and La Pampa indicating the location of General Pico.

142

and administrative center. It has an industrialsector with over 20 facilities covering a total areaof 108 hectares. Its characteristics render it anintermediate or medium-sized city. According toLlop Torne & Bellet Sanfeliu (1999), these aredefined by the size of their population – between20,000 and 2,000,000 – and the role they play inthe territory immediately surrounding them and ofwhich they act as reference center.

Public forestation includes mainly specimens ofRobinia pseudoacacia, several species of Fraxinusand to a lesser extent Melia azedarach.

Materials and methods

Fourteen sampling sites were selected. Eight sam-pling sites separate from each other by about1000 m were selected along orthogonal imaginarylines running in NE–SW and NW–SE directions.These included paved urban sites with differenttraffic intensities, non-paved periurban sites withabundant dust in suspension. Six additional siteswith peculiar conditions such as the city industrialarea and the interurban bus station were also in-cluded (Table 1). No atmospheric pollutantrecords were available, as the necessary measuringinstruments were lacking. Therefore the sites weredescribed by means of observable charactersrelated to air quality. Two trees of the same species

and similar size were selected in each site and fromeach of them nine subsamples of lichens and/ormoss were taken with cylindrical steel corers, 11 mmin diameter (cores of ca. 1 cm2). Samples consistedmainly in lichens, except in site F, where moss waspredominant. Sample and subsample sizes werechosen following Morgan (1977) and Steiner(1994a). The sampling height on trees was stan-dardized at mean breast height (1.5 m). On side-walk trees, samples were taken on the trunk surfacefacing the street.

The samples, collected on May 23 and Novem-ber 22 of 2001 were stored in paper bags at roomtemperature. For study they were hydrated inplastic sieves placed in Petri dishes covered withwater. Examination of the material began 24 hlater using a stereoscopic microscope. Tardigrades,molts and eggs were separated with micropipette.Asphyxiation of active individuals was provokedby placing the tardigrades in a heater at about60 �C, or else they were killed using hot water. Hotwater was added to the material in the mesh after48 h, which was shaken to loosen any remainingtardigrades and eggs. They were fixed in 10%neutralized formaline. Part of the material wasprepared for microscopic study, mounting themwith Faure’s medium. Identification of tardigradesand their eggs was done using a KIOWA Medilux12 binocular microscope.

Table 1. Characteristics of study sites

Sites Pavement Traffic Sun exposure Special features

A Yes Medium–high Medium Street trees

B Yes Medium–high High Street trees

C Yes Medium–high High Street trees, bus station

D Yes Medium–high Medium Street trees

E Yes Medium–high Medium Street trees

F Yes Low Low Street trees

G No Low Low Street trees, periurban zone

H No – Medium Periurban zone

I No Low High Street trees, periurban zone

J Yes – Medium Town square

K Yes – Medium Town square

L No – Low Park, town hospital

M No – Low Park, industrial area

N Yes Low Medium Street trees, near battery factory

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The tardigrade species and individual numberswas recorded and the relative abundance calculated.

In order to analyze tardigrade diversity, speciesrichness (S), Shannon–Wiener’s (H’) and Simp-son’s (1/D) diversity indices (Magurran, 1989)were calculated for each site and each season. Thetest of Hutcheson (Moreno, 2001) was used tocompare the Shannon–Wiener index between sitesand between seasons. The differences in the den-sities of tardigrades between autumn and springwere analyzed by the Mann–Whitney test. Pearsoncorrelations were calculated to analyze the rela-tionship between tardigrade density and diversity(Sokal & Rohlf, 1979). The similarity of tardigradecommunities between fall and spring were com-pared using the Morisita–Horn index (Magurran,1989; Moreno, 2001). The variation in speciescomposition among sites was summarized throughprincipal components analysis (PCA) of the cor-relation matrix derived from species abundancedata using BioDiversity Pro software (Oban,Scotland). Classification of sites was performed onthe basis of specimen number of each species usingthe complete linkage method (Cluster and EisenTreeview, Stanford).

Results

Species recorded

Tardigrades were found in 98.2% of the 56samples totalizing 4836 specimens. They wererepresented by the following taxa:

Class Heterotardigrada Marcus, 1927Order Echiniscoidea Marcus, 1927Family Echiniscidae Thulin, 1928Genus Echiniscus Schultze, 1840

1. Echiniscus rufoviridis du Bois-Raymond Marcus,1944

Present in 9.25% of samples. It was neverfound alone and it was never the dominant species.It appeared in very low numbers in sites G, L andM (only one specimen in G and L).

Class Eutardigrada Marcus, 1927Order Parachela Schuster, Nelson,Grigarick & Christenberry, 1980

Family Macrobiotidae Thulin, 1928Genus Macrobiotus Schultze, 1834

2. Macrobiotus areolatus Murray, 1907Present in 18.5% of samples. It appeared in

sites F, G and L. It was dominant in F during falland spring. At site G it was dominant in spring.

3. Macrobiotus sp. (A non-described species)Present in 7.40% of samples. It appeared in

moderate numbers and only in site K, where it wasthe dominant species.

Family Hypsibiidae Pilato, 1969Genus Ramazzottius Binda & Pilato, 1987

4. Ramazzottius oberhaeuseri (Doyere, 1840)Present in 74.07% of samples. In 3.7% of them

it was the only species and in 24.07% of them, thedominant species. Found in all sites. Dominant insites H, I, J, and M. Co-dominant with M. cf.tardigradum in site L.

Order Apochela Schuster, Nelson,Grigarick & Christenberry, 1980

Family Milnesiidae Ramazzotti, 1962Genus Milnesium Doyere, 1840

5. Milnesium cf. tardigradum Doyere, 1840Present in 88.88% of samples, it was the only

tardigrade in 14.8% and the dominant one in 26%of samples. Found in all sites. Dominant in sites A,B, C, D, and E during spring and fall and in site Gduring fall. Co-dominant with R. oberhaeuseri insite L.

Diversity and density

The total number of species collected in the studyarea in both fall and spring samplings was 5. Themaximum number of species per site and per treewas 4 (Table 2). Highest values of species richnessof tardigrades were measured in sites with nopavement and low sun exposure (G and L). Heavytraffic paved sites rendered only two species: R.oberhaeuseri and M. cf. tardigradum (A, B, C, Dand E). The same occurred in non-paved sites withmedium to high sun exposure (H and I).

The Shannon–Wiener and Simpson diversityindices (Table 2) showed the lowest value at site Efor both fall and spring. The indices showed thehighest value at the site M in fall and at the site Lin spring. T-test values obtained with theHutcheson’s method (Tables 3 and 4) forShannon–Wiener index indicates that significant

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differences between the study sites exist in manycases. Particularly the diversity of the site E inautumn was significantly different from those fromall other sites. On the other hand, the diversity ofsite J, both in fall as in spring, was significantlydifferent only with respect to other four sites. T-values were not significantly different when com-paring the diversity of each site in autumn andspring, except for sites H and E (Table 5).

Tardigrade density expressed in specimensper cm2 varied according to tree, site and season.Maximum values of density were in fall on a tree insite F (55.06 specimens per cm2; dominant specieswas M. areolatus with 44.50 specimens per cm2)and in spring on a tree of site I (49.92 specimens percm2; dominant species was R. oberhaeuseri with45.00 specimens per cm2). Minimum density valueswere recorded in site N, placed nearby a batteryfactory and exposed to lead emanations. No tar-digrades were found there during fall and in spring

only one specimen ofM. cf. tardigradum was foundin one tree and one specimen of R. oberhaeuseri onanother one. Mean tardigrade density for all siteswas about 10 specimens per cm2 (9.81 in fall and10.35 in spring). The differences in the densities oftardigrades between autumn and spring were notstatistically significant (Mann–Whitney U-test,p=0.887).

The relation between tardigrade density anddiversity was analyzed (Figs. 2 and 3). As reportedin Table 6 (Pearson correlation), the consideredvariables were not significantly correlated in fall.The results for spring showed a negative and sig-nificant correlation between density and diversityindices.

Relative abundance

At almost all sites, the presence and relative abun-dance of tardigrade species was relatively constant

Table 2. Tardigrades diversity: richness (S), Shannon–Wiener index (H’) and Simpson index (1/D) for each sampling sites in fall and

spring

Sites A B C D E F G H I J K L M

Fall

S 2 2 2 2 2 3 4 2 2 2 3 4 3

H’ 0.190 0.241 0.181 0.135 0.014 0.205 0.263 0.226 0.116 0.136 0.344 0.424 0.443

1/D 1.367 1.588 1.344 1.204 1.010 1.373 1.447 1.513 1.162 1.211 1.848 2.441 2.666

Spring

S 2 2 2 2 2 2 4 2 2 2 3 3 3

H’ 0.172 0.175 0.214 0.111 0.088 0.174 0.337 0.122 0.117 0.118 0.423 0.457 0.406

1/D 1.305 1.315 1.458 1.152 1.109 1.312 1.822 1.175 1.163 1.166 2.410 2.765 2.296

Table 3. Results of Hutcheson t-tests for Shannon–Wiener index between sampling sites in fall

Site A B C D E F G H I J K L

B )1.55 0

C )1.21 )0.34 0

D 1.49 2.96** 2.01* 0

E 4.77** 6.14** 3.68** 3.16** 0

F 0.44 2.29* 1.48 )1.41 )5.65** 0

G )1.75 )0.77 )0.29 )2.63* )4.50** )2.09* 0

H )0.63 1.21 0.97 )2.39* )6.48** )1.50 1.51 0

I 2.56* 4.11** 2.52* 0.90 )2.61* 2.89** 3.22** 3.93** 0

J )0.36 0.57 0.70 )1.23 )3.02** )0.61 1.05 )0.06 )1.75 0

K )3.24** )2.24* )1.38 )4.11** )6.01** )3.68** )1.16 )3.08** )4.76** )2.20* 0

L )5.81** )4.09** )2.04* )7.19** )10.57** )7.44** )1.85 )6.16** )8.75** )3.12** )0.39 0

M )6.48** )4.77** )2.47* )7.83** )11.16** )8.17** )2.33* )6.91** )9.41** )3.58** )0.88 )0.75

* p<0.05; ** p<0.01.

145

during the period considered. The greatest differ-ences were recorded at sites N and G. Themagnitude of the variation in site N can beexplained by the very low number of specimenspresent (none in autumn and two in spring). At siteG, M. cf. tardigradum is dominant in autumn andM. areolatus in spring.

Four of the species found in General Pico dom-inate in at least one of the samples (Table 7). The

dominant species in most of these samples was M.cf. tardigradum, followed by R. oberhaeuseri. Thesetwo species coexist at all sites and at many of themtheir cumulative relative abundance approaches100% (Fig. 4). The sites where both are the onlyspecies present are distributed in two groups, onedominated by R. oberhaeuseri and the other one byM. cf. tardigradum. In these groups, relative abun-dance of the dominant species is never below 75%.

Table 4. Results of Hutcheson t-tests for Shannon–Wiener index between sampling sites in spring

Site A B C D E F G H I J K L

B )0.22 0

C )1.92* )1.76 0

D 2.04* 2.17* 3.08** 0

E 1.73 1.86 2.92** 0.02 0

F 0.57 0.79 2.31* )1.92 )1.50 0

G )3.47** )3.22** )0.74 )5.05** )4.62** )4.16** 0

H 2.22* 2.34* 3.15** )0.02 )0.03 2.22* 5.25** 0

I 2.61* 2.70** 3.33** 0.35 0.25 2.80** 5.53** 0.44 0

J )0.13 0.03 1.50 )1.38 )1.29 )0.46 2.54* )1.41 )1.61 0

K )4.97** )4.75** )2.35* )6.23** )5.89** )5.53** )1.92 )6.38** )6.59** )4.01** 0

L )6.41** )6.05** )2.61* )8.27** )7.48** )7.47** )2.21* )8.66** )9.02** )4.65** 0.11 0

M )5.31** )4.96** )1.70 )7.26** )6.48** )6.38** )1.11 )7.65** )8.04** )3.72** 1.10 1.23

* p<0.05; ** p<0.01.

Table 5. Results of Hutcheson t-tests between Shannon–Wiener index values from fall and spring for each of the sampling sites

A B C D E F G H I J K L M

0.44 1.63 )0.31 0.94 )2.02* 0.97 )0.81 4.51** 0.44 0.41 )1.34 )1.52 0.50

* p<0.05; ** p<0.01.

Figure 2. Variation of the tardigrade density and diversity between sites in fall.

146

The Morisita–Horn index (Cmh) showed veryhigh similarity in tardigrade composition betweenthe two sampling periods. It varied between 0.953and 1.000 for all sites, except for G (Cmh=0.485).

Ordination and classification of study sites

The first two components in the PCA performed(Fig. 5), accounted for only 51.87% of thevariability. M. cf. tardigradum obtained the high-est loading value in the first component whereas R.oberhaeuseri obtained it in PC2. From Fig. 5 it can

be seen that all paved and with medium–hightraffic sites are located on the right hand of PC1.

The results of complete linkage clustering basedon composition of the tardigrade fauna (Fig. 6)allowed identification of five groups: 1) dominatedby M. areolatus – a low traffic paved area; 2)characterized by the dominance of R. oberhaeuseriand occurring in the central zone of the townsquare and in periurban sites with high suspensiondust and medium to high sun exposure; 3) in whichM. cf. tardigradum and R. oberhaeuseri are equallywell represented and accompanied by other species

Figure 3. Variation of the tardigrade density and diversity between sites in spring.

Table 6. Pearson correlation between tardigrades density (d)

and species richness (S), Shannon–Wiener index (H’) and

Simpson index (1/D)

d/S d/H’ d/1/D

r p r p r p

Fall )0.1438 0.6393 )0.3008 0.3179 0.2823 0.3501

Spring )0.5058 0.0778 )0.6072 0.0278 )0.5835 0.0363

Table 7. Dominant species in at least one of the 49 samples

with n‡10 specimens, ranked according to mean relative

abundance in the assemblages dominated by these species

Mean relative

abundance

Standard

deviation

No. of

cases

M. areolatus 87.64 8.95 5

R. oberhaeuseri 84.16 15.21 17

M. cf. tardigradum 80.33 19.62 25

Macrobiotus sp. 64.06 19.89 2

Figure 4. Milnesium cf. tardigradum and Ramazzottius ober-

haeuseri: Relative abundance of both species at 12 sampling

sites in the study period. Letters refer to the sites described in

Table 1.

147

– it includes sites relatively well protected from thesun and wind; 4) dominated byM. cf. tardigradum,occurring in medium–high traffic urban areas; and5) dominated by Macrobiotus sp. and occupying aflower bed surrounding the town square.

Discussion

The total number of species (5) recorded inGeneral Pico, as well as the species richness at eachsite (4), agree with those recorded for Santa Rosa(La Pampa, Argentina). They also agree with thosestated by Semeria (1981) who found five urbanspecies with a maximum of four species per site inNice (France). Meininger et al. (1985) – who alsofound five species in urban samples fromCincinnati (Ohio, USA) – recorded no more thanthree together at any given urban site. The speciesrichness variation in the different kinds of sitesconfirms observations by other authors (Meiningeret al. 1985 and Steiner 1994b) as to the inverserelationship between air quality and species rich-ness of tardigrades. Indeed, the lowest values forthe calculated diversity indices were obtained froma site with medium–high traffic (site E).

Available information on the species of tardi-grades found in the sampled urban sites is sum-marized in Table 8. According to this information,there are four species that show the highest toler-ance to environmental conditions in differentcities, i.e., Macrobiotus hufelandi in Nice; Macro-biotus persimilis in Zurich, Diphascon scoticum inCincinnati and M. cf. tardigradum in Santa Rosaand in General Pico. However, it should be poin-ted out that the references to M. hufelandi inMeininger et al. (1985) and Semeria (1981) maynot represent specimens of M. hufelandi sensustricto as both papers were published before the

Figure 5. PCA ordination of 12 sites based on abundance data of tardigrade species. Letters refer to the sites described in Table 1.

Figure 6. Dendrogram representing inter-site relationships

based on abundance data of tardigrade species. Cluster-groups

are marked with a code and explained in the text. Letters refer

to the sites described in Table 1.

148

revisions of the M. hufelandi group (Biserov, 1990fide Kinchin, 1994; Bertolani & Rebecchi, 1993).

In the areas of heaviest traffic in Santa Rosa,M.cf. tardigradum was the only species present (Pel-uffo et al., 2000). In General Pico, although it isclearly dominant, it is always accompanied by R.oberhaeuseri. In the non-paved periurban sites thatare more exposed to the sun and with abundantsuspended dust in the air, the relative abundance ofspecies is inverted and R. oberhaeuseri is the dom-inant species. This agrees with the known higherresistance to drought of R. oberhaeuseri (Jonssonet al., 2001). E. rufoviridis is an uncommon species,in General Pico and in other cities in Argentina(Peluffo et al., 2002). The same thing occurs withMacrobiotus sp., and these two species can beplaced in the low tolerance group of Semeria(1982). M. areolatus is a medium tolerance species,considering its frequency in General Pico.

The results of PCA agree considerably withthose of clustering. In both cases there are sitesthat always appear grouped: L and M, sites rela-tively well protected from the sun and wind; H andI, non-paved periurban sites; A, B, D and E, pavedsites with medium–high traffic. In addition, site F,

paved with low traffic appear isolated in bothanalysis.

Although there are a few records of excep-tionally high densities in the literature – of over200 specimens per cm2 (e.g. Morgan, 1977) – Ra-mazzotti & Maucci (1983) considered that a mossnormally can be called rich if it hosts 10–20 indi-viduals per cm2. Lichens are normally less popu-lated and rarely reach 10 individuals per cm2. Innorthern regions very high exceptional values of10–30 specimens per cm2 have been recorded(Ramazzotti & Maucci, 1983). Therefore, densityin General Pico can be considered very high. Theaverage values for fall and spring are around 10specimens per cm2 and the maximum values reachover 50 specimens per cm2.

Autumn and spring samples are constant inspecies richness and tardigrade diversity through-out nearly all sites in General Pico. There were nosignificant differences in the scores of the tests usedto compare the tardigrade density and communitystructure between fall and spring. This agrees withSteiner (1994c) who stated that tardigradecommunities are stable through time. They alsolend support to the sampling methods used.

Table 8. Tardigrade species found in urban areas of the neotropical and holarctic cities

Nearctic Cincinnati,

USA Meininger

et al. 1985

Palearctic Niza,

France

Semeria 1981

Palearctic Zurich,

Switzerland

Steiner 1994b

Neotropical Sta.Rosa,

Argentina

Peluffo et al. 2000

Neotropical

G. Pico, Argentina

this work

Echiniscus rufoviridis + +Echiniscus testudo + +Macrobiotus areolatus + +Macrobiotus hibiscus +Macrobiotus hufelandi + +

2

+Macrobiotus persimilis +

2

Macrobiotus richtersi +Macrobiotus sp. + +Minibiotus intermedius +Hypsibius convergens +Isohypsibius prosostomus +Ramazzottius oberhaeuseri + + + +Itaquascon bartosi +Diphascon scoticum + 2

Milnesium tardigradum + +Milnesium cf. tardigradum +

2

+

2

+=present.

+ 2

=highest tolerance.

149

On the other hand, results confirm therelationship between vehicle traffic intensity andtardigrade diversity. At the same time, they sug-gest the existence of other important environ-mental factors influencing this diversity, thesignificance and interactions of which will besubject of further research.

Acknowledgements

The authors wish to thank M. Claps (UNLP,Argentina), G. Rossi (CEPAVE, Argentina) andE. Quiran (UNLPam, Argentina) for their biblio-graphic help. They also thank M. Griffin (UNL-Pam, Argentina) for his suggestions and help withthe English version of the paper and two anony-mous reviewers for their comments and sugges-tions. This research was partially supported byUniversidad Nacional de La Pampa, (Argentina).

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