the potential utility of rodents and other small mammals...

The potential utility of rodents and other small mammalsas indicators of ecosystem lsquointegrityrsquo of South African grasslands

Nico Avenant

National Museum and Centre for Environmental Management University of the Free StatePO Box 266 Bloemfontein 9301 South AfricaEmail navenantnasmuscoza

AbstractContext The expansive grassland biome is one of the most extensively transformed in South Africa yet no strategy for

monitoring its integrity is in place A grassland health program incorporating different ecosystem levels was recentlyinitiated The suitability of three taxonomic groups as indicators has been tested so far vegetation (by calculating anecological index value El) insects (using the South African grassland scoring system SAGraSS) and small mammals (thisstudy) All of these methods aim to be rapid and easy to perform Whereas SAGraSS still needs further refinement severalfactors already indicate the importance of including small mammal community parameters in integrity assessments

Aims This contribution reports onmore than 12 years of results from various studies on small mammals in the Free StateGrasslands with the aim of exploring the utility of small mammal survey for assessment of ecosystem integrity

Methods The hypothesis was based on the outcomes of several short-term studies conducted in the grassland biomeCombining all previous results this paper re-evaluates the parameters of trap success species richness diversity evennessand individual species as bio-indicators

Key results By combining data from many sites and years the effect of seasonal and inter-annual variations in habitatand population parameters was diminished and a more general picture of small mammal community structure revealedNew insightswere gleaned into the status of several indicator species By providing a summary of smallmammal communityparameter scores and indices the study establishes a benchmark for future small mammal assessments and monitoringTo be effective small mammal surveys in the grassland biome of southern Africa should be carried out in autumn and earlywinter

Conclusions This study suggests that small mammal species richness and diversity decline with habitat degradationthat the generalist rodent Mastomys coucha dominates community numbers at low ecological integrity that thenumber of specialist species increases towards ecological climax and that specific species act as indicators during thesuccessional process

Implications This study should benefit the monitoring conservation and management of grassland ecosystems makeenvironmental impact assessments more effective and identify new topics for ecological research

Additional keywords community structure diversity ecological integrity species richness

Received 6 December 2010 accepted 1 September 2011 published online 30 November 2011

Introduction

Although plants have traditionally been used as indicators ofecosystem integrity (for example soil cover ecological valuepioneer to climax species ratio ndash see Vorster 1982) many othergroups of organisms hold potential as indicators of ecosystemfunction and integrity such as soil microbes (Mikola andSetaumllauml 1998) aquatic macro-invertebrates (Chutter 1988)spiders (Bultman et al 1982 New 1999) insects (Majer 1983Pearson and Cassola 1992 Beccaloni and Gaston 1995McGeoch 1998 Petit and Usher 1998 Rodriacuteguez et al 1998Jones and Eggleton 2000 Orgeas and Andersen 2001 McGeochet al 2002 Rainio and Niemelauml 2003 Baker 2006) fish (Karret al 1986 Kleynhans 1999 Avenant 2010) birds (Joubert and

Ryan1999Rich2002) reptiles (Letnic et al2004) andmammals(Fox 1982 1990 Joubert and Ryan 1999 Letnic et al 2004)In southern Africa the most popular bio-indicators are aquaticmacro-invertebrates (applying the South African scoringsystem SASS Chutter 1988) fish (determining a fishassemblage integrity index Kleynhans 1999) and vegetation(calculating an ecological index value El Vorster 1982 VanRooyen 2002)

The grassland biome is one of the most extensivelytransformed ecosystems in South Africa and it is undercontinuous threat from various sources including afforestationcultivation overgrazing and urban expansion (Low andRebelo 1996 DEAT 2005) Although environmental impact

CSIRO PUBLISHING

Wildlife Research 2011 38 626ndash639httpdxdoiorg101071WR10223

Journal compilation CSIRO 2011 wwwpublishcsiroaujournalswr

assessments typically sample several different groups oforganisms the development of an effective integratedmonitoring strategy for South African grassland ecosystems islong overdue A key step is the determination of informativeeasily assessed indicator groups Based on the success of theSASS and the River Health Program inmonitoring the ecologicalintegrity of South African rivers a grassland health programbased on insect assemblages was suggested (Seaman and Louw1999) However the proposed Southern African grasslandscoring system (SAGraSS) has proven time consuming anddifficult to implement and further refinement and testing ofthe system is essential (Kaiser et al 2009) In South Africathese environmental indicators lsquoform the basis of the state of theenvironment reportingrsquo (DEAT 2006) However when reportedon consistently over time they might also hold potential forassessing the effectiveness of management actions aimed atspecific environmental pressures

Small mammal communities have been investigated as bio-indicators in many different environmental contexts (Fox andFox 1984 Kirkland 1990 Carey and Wilson 2001 Ecke et al2002 Pearce and Venier 2005 Hoffmann and Zeller 2005Klinger 2006 Avenant and Cavallini 2007 Glennon andPorter 2007) This group offers multiple advantages as bio-indicators they typically are adapted for survival in relativelysmall areas most species reproduce rapidly and thus show goodresponse to successional changes in vegetation and theygenerally can be sampled using relatively quick easy andinexpensive methods (Ferreira and Avenant 2003 Avenantet al 2008) Compared with plants and invertebrates they arealso fairly easy to identify and for many there is a body ofnatural history information regarding their biology

In southern Africa variation in small mammal communitystructure is thought to reflect parameters such as habitat structureand complexity rainfall and primary productivity predationdisturbance history of the vegetation including firingtrampling and grazing patch size and the distance betweensimilar habitats and the presence of exotics (Avenant 2000a2000b) The impact of these factors on individual small mammalspecies can be expected to vary according to their physiologicalnutritional social and anti-predator requirements (see Birneyet al 1976) while the outcomes at a community level shouldreflect both the complex interplay of factors and the influence ofinter-specific competition Despite the inevitable complexity areasonable expectation is that prolonged or intense ecologicaldisturbancewill lead to a loss of ecosystem lsquointegrityrsquo associatedeither with invasion by exotic organisms with changes in soilfertility or structure or with loss of ecosystem function (egthrough removal of large mammals or predators) and that thiswill be reflected in a decline in small mammal species richness(Avenant 2000b 2005) A theoretical basis for this prediction isfound in Tilmanrsquos hump-shaped curve model (Tilman 1982Fig 1) which predicts an increase in the number of specieswith advancing successional stage after disturbance up to thepoint of ecological climax followed by a secondary decline inpost-climax contexts (also see Rosenzweig 1995) Tilmanrsquosmodel is supported by numerous empirical studies that havedemonstrated correlations between species diversity anddisturbance (eg Wootton 1998 Hastwell and Huston 2001)and between species diversity and declines in ecosystem

function resilience and resistance (Grime 1998 Cardinaleet al 2000 Chapin et al 2000 Johnson 2000 Loreau 2000McCann 2000 Petchey 2000 Fonseca and Ganade 2001)Although successional stage and lsquointegrityrsquo are not equivalentecological concepts (indeed natural disturbance regimes areundoubtedly essential in maintaining ecological integrity) inthe present context the level of historical and contemporarydisturbance is such as to expect that Tilmanrsquos model forsuccession can be applied to stages in ecosystem degradation(ie loss of integrity) and recovery (see also Avenant 2005)Application of the model to small mammal communities issupported by studies of rodents in Chinese grasslands (Wanget al 1999) and by several studies conducted on rodents in SouthAfrica (eg Rowe-Rowe and Lowry 1982 Rowe-Rowe 1995Ferreira and VanAarde 2000) and elsewhere (eg Abramsky andRosenzweig 1984 Abramsky 1988 Rosenzweig 1995)

In this paper I explore the utility of small mammals asindicators of habitat lsquointegrityrsquo in the grassland biome of theFree State of South Africa with a broader view to enhancing therole of this group of organisms in environmental assessment andmanagement Thedataset is a compilation of results obtainedoverthe past ~15 years (eg Avenant 1998 2002 2003b 2004 Nelet al 1996) and derives from many different short-term studiesand environmental assessments carried out for a variety ofreasons and with somewhat contrasting methodologies Whilea longer-term multi-organism project in one locality is inprogress this study uses all of the previously generated datafrom the Free State grassland biome to explore general aspects ofsmall mammal community structure and to provide a benchmarkagainst which future small mammal assessments and monitoringcan be measured

Materials and methodsStudy area

Table 1 and Fig 2 summarise the trapping history and effort atsix study areas ndash QwaQwa National Park (QQNP) WillemPretorius Nature Reserve (WPNR) Korannaberg Conservancy

SuccessionEcological integrity

Num

ber

of s

peci

es

Fig 1 Hypothesis for using small mammals as indicators of habitatintegrity in the South African grasslands tested in the current study

Rodents as indicators of ecosystem integrity Wildlife Research 627

(KC) Sandveld Nature Reserve (SNR) Caledon Nature Reserve(CNR) Tussen-die-Riviere Nature Reserve (TdR) ndash where themost detailed small mammal trapping has been done during thepast ~15 years in the Free State central South Africa All of thesesites fall within southern Africarsquos grassland biome and all are insome form of conservation area where no unnatural changeshave occurred within 1 km of transects just before or duringthe respective study periods Comparisons are made with otherlocalities surveyed by the author (eg the grasslands in Lesothoand Swaziland or in the Nama-Karoo in the drier western Free

State) The whole Free State area is characterised by cold drywinters and hot summers All areas receive summer rainfall butthe mean annual amount varies between ~500mm in the westand ~800mm in the east The average mean temperature variesfrom ~7C in July to ~22C in January with a mean minimumtemperature of ~5C in July and a mean maximum of 35C inJanuary The area rises gradually from west to east with atopographic low of ~1250m above sea level (asl) in the west(eg TdR and SNR) and peaks at ~2380m asl in the east(QQNP)

Table 1 The overall trap success species richness diversity and evenness of small mammals (rodents and shrews) on transectsduring previous standard surveys in the Free State province 1996ndash2003TN transect number EI ecological index value ndash cannot be calculated

Locality trap effort and year TN (EI) Trap Species Diversity Evennessof sampling success richness Shannon Simpson (1D) (Evar)

QwaQwa National Park28290S 28410E400 trap-nights per transect1994ndash95

1A

2A

3A

4A

5A

6A

7A

8A

9A

10A

11A

12A

13A

14A

15A

16A

17A

306186120094534040226134080160054134026040080320374

43215233412212263

09370892034900001141063710280639124200000693050000000637045117920956

22572257128510002793300329591608500010000000166700103003140000003003

045807510475ndash

03550924077706450884ndash

10000715ndash

0924063410000851

Willem Pretorius Nature Reserve28180S 27100E2400 trap-nights per transect1995ndash97

18B

19B

20B

21B

22B

23B

24B

25B

294169067058098160243436

22322323

01180692097002710655103904240734

12762049269511821942282513532020

05060998075603660950063605920236

Korannaberg Conservancy28550S 27150E1600 trap-nights per transect1996ndash97

26C

27C

28C

29C

30C

411189072124381

75552

18371325130412510292

61733021349731851188

08650747053904520394

Sandveld Nature Reserve27410S 25430E1600 trap-nights per transect1999ndash2000

31C

32C

33C

34C

35C

36C

151110071408

541134

125811910000000009081119

300331851000100022423115

059107680513060306940709

Caledon Nature Reserve29490S 26540E1600 trap-nights per transect2001ndash02

37C (430)38C (548)39C (629)40C (878)

075019188294

2236

0562063707301235

1692300317612924

0813092405310403

Tussen-die-Riviere NR30300S 26150E3200 trap-nights per transect2002ndash03

41C (240)42C (424)43C (491)44C (593)

1219096911562219

4346

1293079109801385

3717208321323333

0684050106110464

AOne-off sampling B10-weekly sampling Cseasonal sampling

628 Wildlife Research N Avenant

Data collection

Sampling regime varied between sites (see Table 1) Some weresampled once some every 10 weeks and some in the middle orsecond half of each of four successive seasons In the earlierstudies (at QQNP WPNR KC and SNR) a range of habitats wassampled on a variety of soil types with the aim of correlatingsmall mammal community structure with habitat features(Avenant 1997 2000a 2003a Avenant and Watson 2002) Inboth CNR (transects 37ndash40) and TdR (transects 42ndash44) similargrassland habitats were sampled at different successionalstages with the aim of correlating small mammal communitycharacteristics with a habitat EI value based on vegetation

At all localities except TdR 100 snap traps were spaced 5mapart on a single trap-line in an effort to detect all species presentin a specific habitat Transects were preferred to grids as theycover a larger area per number of traps used (Pearson andRuggiero 2003) Removal trapping with snap traps was usedon account of its greater effectiveness compared with live traps(N Avenant data not shown) and as part of an active strategy ofbuilding regional collections for taxonomic studies Traplineswere moved at least 200m every season and in such a way thatthey were never closer than 100m to the previous line in thesame habitat Traps were set for ~92 h (4 consecutive days andnights) and checked and rebaited with a mixture of peanutbutter rolled oats sunflower oil and marmite at sunrise andjust before sunset

At TdR 200 traps per transect were set for 10 consecutivedays with the aim of assessing variation in trap success speciesrichness diversity and evenness over a period longer than 4 daysFor this analysis I use only the results obtained during the first4 trap-nights at TdR thereby ensuring comparability with theother localities (but see lsquoDiscussionrsquo)

All specimens collected were deposited in the mammalcollection of the National Museum Bloemfontein

Three measures of abundance and community structure werecalculated trap success species richness anddiversity (calculatedusing the ShannonndashWeiner and Simpsonrsquos information indicesMagurran 2004) The term lsquotrap-nightrsquo was used to describe onetrap that was set for a 24-h period (following Rowe-Rowe andMeester 1982) and trap success (or percentage success) isthe number of small mammals captured per 100 trap-nightsNormality of data was checked with the ShapirondashWilkrsquos Wtest For non-normally distributed data standard nonparametrictests were used Statistical analyses were done with Statisticafor Windows (Statsoft Inc Tulsa OK) and the 95 level(Plt 005) was regarded as statistically significant for all tests

Results

Trap success and seasonal contrasts

Trap success differed substantially between transects in theFree State grasslands (Table 1) Trap success calculated acrossall 44 transects and all sampling periods was 168 122 with arange for individual transect values of 019ndash534 Howeverthese pooled values do not reflect the true variability in trapsuccess which for specific transects and trapping periods rangedbetween 0 and 105 (Table 2) For individual localities meantrap success on all transects ranged between 0125 and 525 atTdR (transect mean over four seasons = 139 140) between0 and 105 at CNR (mean = 144 288) and between 039and 548 at KC (mean = 235 161) At QQNP and SNRmean trap success on all transects was 086 070 and22 25 respectively

Significant contrasts in trap success were found betweenseasons for transects at WPNR and SNR (Table 2) At KCCNR and TdR there were clear seasonal differences on sometransects but no overall significant contrasts when all transectswere pooled Trap success also varied from year to year eg atWPNR trap success in autumn 1996 (the scores included in thisstudy) was significantly lower than in autumn 1997 (Avenant2000a) Differences in trap success between transects weregenerally more marked in autumn when trap success is highest(Fig 3) trap success was more often consistently low in springand summer At individual localities trap success was lowesteither during spring (WPNR) summer (SNR and KC) or springand summer (TdR and CNR)

Distribution and habitat associations of species

A total of 16 species was recorded across all transects (Table 3)Mastomys coucha and Rhabdomys pumilio were captured on themajority of transects while Micaelamys namaquensis Taterabrantsi T leucogaster and Mus minutoides were encounteredregularly at regional subsets of transects Six species wererecorded on fewer than five transects and three of these wererecorded on single transects only

Mastomys coucha has been termed a generalist andopportunist and occurs in virtually all habitats across the FreeState (Avenant 1996 Avenant et al 2008) Rhabdomys pumiliois the only diurnal rodent present in almost all habitats in theregion and it occurs in almost all habitats (Skinner andChimimba 2005) Tatera brantsi and T leucogaster wereconsistently present on transects where the substrate was sandwhile Micaelamys namaquensis was found only on rock

Fig 2 Localities where small mammal communities were sampled in theFree State province 1994ndash2003 ~ QwaQwa National Park amp WillemPretorius Nature Reserve + Korannaberg Conservancy SandveldNature Reserve Tussen-die-Riviere Nature Reserve amp CaledonNature Reserve


Table 2 The seasonal trap success species richness diversity and evenness of small mammals (rodents and shrews) on transectsduring previous standard surveys in the Free State province 1996ndash2003

WPNR Willem Pretorius Nature Reserve KC Korannaberg Conservancy SNR Sandveld Nature Reserve CNR Caledon Nature ReserveTdR Tussen-die-Riviere Nature Reserve TN transect number ndash cannot be calculated

Locality TN Season Trap Species Diversity Evennesssuccess richness Shannon Simpson (1D) (Evar)

WPNR 18 SpringSummerAutumnWinter

0270027024002130

1122

0000000003500380

1000100012851333

ndash

ndash

04750517


0000027018700000

0120

0000000006000000

0000100019080000

ndash

ndash

0868ndash


0000080010700000

0220

0000064005600000

0000300320000000

ndash

09240813ndash


0000000013300000

0020

0000000005000000

0000000016670000

ndash

ndash

0715ndash


0270000002700270

1011

0000000000000000

1000000010001000

1000ndash

10001000


0000000018700530

0022

0000000006800690

0000000023310000

ndash

ndash

09871000


0000000017800800

0022

0000000005000640

0000000016673003

ndash

ndash

07150924


0000053021300000

0110

0000000000000000

0000100010000000

ndash

10000850ndash

KC 26 SpringSummerAutumnWinter

4960365031304700

6557

1430143314741754

3891478554956369

0587071907840772


2220157032600520

4352

1232082411850562

3676212826112000

0681060205690813


0390052010400910

2333

0637104009740956

3003598831153003

0924093207820803


1830065010401430

3342

0980105513210474

2674500055871486

0866093209010672


3260261054803910

2212

0440019900000451

1230111110001403

0617027500000440

SNR 31 SpringSummerAutumnWinter

1750050020001750

3232

0796000010400683

2101100034972331

0773096209080987

(continued next page)


substrates When present the Tatera and Micaelamys speciesare usually caught on the first trap-night

Crocidura cyanea Dendromus melanotis Elephantulusmyurus Graphiurus murinus Malacothrix typica Saccostomus

campestris Mus minutoides Mystromys albicaudatusMyosorex varius and Otomys irroratus were all found in lownumbers and in specific habitats consistent with accounts ofSkinner and Chimimba (2005)

Table 2 (continued )



1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890

CNR 37 SpringSummerAutumnWinter

0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962

TdR 41 SpringSummerAutumnWinter

1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678


Although Otomys irroratus can be abundant in densevegetation close to relatively permanent water bodies such asstreams rivers and wetlands this species is not easily trappedunless the traps are set in its runway (N Avenant pers obs) It istherefore unlikely to be detected by a transect trapping approachAnother species that does not readily enter traps is the shrewSuncus infinitesimus This species can be dug from disusedtermitaria but it seldom enters traps even if they are placedimmediately alongside the entrance This species was notcaught in traps at any of the localities reported here

Dendromus melanotis was only caught on the least disturbedgrassland transects (at KC CNR and TdR)

Species richness

Species richness at individual transects varied between 1 and 7(Table 1) with a pooled mean across all transects and seasonsof 311 154 Significant contrasts were detected betweentransects (KruskalndashWallis H26108 = 69694 P lt 00001 Fig 4)Seasonal contrasts in species richness were significant at WP(H334 = 17705 P lt 0001) and SNR (H334 = 12158 Plt 001)but not at TdR CNR and KC Highest species richness at eachlocality was generally observed during autumn (Table 2 Fig 4)and a similar pattern is observed when the number of species foreach trap session was expressed as a percentage of the totalnumber of species trapped at the specific habitat (Figs 5 6) At allfive localities where seasonal trapping was carried out all thespecies were detected between the autumn and winter trapsessions

For all data pooled a significant correlation was foundbetween species richness and trap success (Spearmanr = 0693 Plt 005) as well as between the percentage of totalspecies richness and trap success (r= 0687 P lt 005) Whendata were pooled by season these correlations were significantfor spring summer and winter trapping When data were pooledby locality significant correlation between species richnessand trap success was found at WP SNR and CNR but not atKC or TdR The same analyses performed with percentage of

total species richness gave significant correlations at WP KCand CNR but not at SNR or TdR A significant correlationbetween species richness and trap success was reportedpreviously for Soetdoring Nature Reserve (Kuyler 2000) andMaguga (Avenant and Kuyler 2002)

Diversity and evenness

Shannon and Simpson diversity values vary considerablyamong the transects and between the seasonal samples(Tables 1 2 Figs 7 8) Scores for the two indices are stronglycorrelated when data are pooled across all transects (r= 0878n = 108 P lt 005) (Fig 8) Although the mean diversity scores ofboth indices were markedly higher in autumn significantseasonal contrasts were found only for the Shannon index(H3110 = 8102 P lt 005)

Evenness values on the different transects ranged from~0000to 1000 when seasonal values were pooled (Table 1) When allthe sites were pooled differences were evident between seasons(Table 2) with evenness scores significantly lower in autumnthan in summer (Fig 9) This is in stark contrast with what hasbeen found atWPNRWhen all datawere pooled Evar values arenegatively correlated with species richness (r = ndash053 P lt 005)and with both the Shannon and Simpson indices (r= ndash0418 andndash0382 respectively Plt 005) However when broken downinto seasons Evar correlated only with the density indices duringthe seasons when highest trap success and species richness werefound (winter and autumn)

Correlation with ecological integrity

Associated EI values are available for transects at CNR and TdR(Table 1) In both localities the transects appeared to cover arange of successional stages ndash EI increased from transect number(TN) 37 to TN40 at CNR (Avenant et al 2008) and fromTN42 toTN44 at TdR (Avenant and Cavallini 2007) At both localitiesthe number of species increased along with the EI value At CNRonly one species (Tatera leucogaster) occurred at all four plotsplots with the lowest EI values (TN37 and TN38) also housedone other speciesMastomys coucha TN39 with an intermediateEI value hosted both the species present at TN37 and TN38plus Rhabdomys pumilio TN40 with the highest EI valueshared two species (R pumilio and T leucogaster) with TN39but also housedOtomys irroratusMyosorex variusDendromusmelanotis and Mus minutoides A conspicuous absence fromthis plot wasM coucha (Table 2 Avenant et al 2008) A similarsuccession and increase in number of species with EI wasfound in the three similar plots at TdR (Avenant and Cavallini2007 Table 2) At both localities (CNR and TdR) Shannondiversity index increased with the EI value (KruskalndashWallisP lt 005) Although comparable trends were observed for theSimpsonrsquos diversity at both TdR and CNR the differencesbetween sites were not significant and no correlations with EIwere found

Small mammal densities also increased with EI at CNR andat TdR (TN41 an outgroup ndash see Avenant and Cavallini 2007) Itis also notable that the generalist species M coucha contributedmost to small mammal numbers at the plots with the lowest EIvalues and at CNR they were absent from the plot with thehighest EI value On the other hand the specialist species

30

25

20

15

10

05

Season

Trap

succ

ess pKruskal-Wallis H3 108 = 1740958 p lt 0001

Fig 3 Mean (95 CI) trap success on 27 transects in Free Stategrasslands Letters in superscript refer to homologous groupings derivedfrom multiple comparisons of mean ranks for all groups


D melanotis andMminutoideswere only found at the plots withthe highest EI values Comparable observations for these specieshave been made on the basis of several relatively long-termsouthern African studies (Rowe-Rowe and Lowry 1982

Rowe-Rowe 1995 Ferreira and Van Aarde 1999 2000) andfrom short-term studies in the Free State (Avenant 1996 19972000a 2000b 2002 2004 Avenant and Kuyler 2002 Avenantand Watson 2002)

Table 3 Percentage contribution of small mammal (rodent shrew and elephant shrew) species on snap trap transects in the Free State grasslandbiome 1994ndash2003

TN transect number ndash not trapped on transect

TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus

1 824 59 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash 59 59 ndash

2 643 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash 214 143 ndash

3 ndash ndash ndash 889 ndash ndash ndash ndash ndash ndash ndash ndash ndash 111 ndash ndash

4 ndash ndash 1000 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

5 400 450 ndash 100 ndash ndash ndash ndash ndash ndash ndash ndash ndash 25 25 ndash

6 667 ndash 333 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

7 353 176 471 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

8 ndash ndash 800 100 ndash ndash ndash ndash ndash 100 ndash ndash ndash ndash ndash ndash

9 500 167 167 167 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

10 1000 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash


12 800 200 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

13 ndash ndash ndash 1000 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

14 ndash 333 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash 667 ndash ndash

15 ndash ndash 833 ndash ndash ndash ndash ndash ndash 167 ndash ndash ndash ndash ndash ndash

16 167 167 167 ndash ndash ndash ndash ndash ndash 167 ndash ndash ndash 167 167 ndash

17 ndash ndash 286 ndash ndash ndash ndash ndash ndash 571 ndash ndash ndash ndash 143 ndash



20 ndash 333 133 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash 53321 ndash 923 77 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash




25 570 419 ndash ndash ndash 11 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

26 254 222 175 ndash ndash 95 ndash ndash ndash ndash ndash ndash ndash 95 79 7927 534 103 ndash ndash ndash 121 ndash ndash 155 ndash ndash ndash ndash 86 ndash ndash

28 182 ndash 273 ndash ndash 45 ndash ndash ndash 45 ndash ndash ndash ndash ndash 45529 53 132 395 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash 26 39530 915 85 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

31 125 542 ndash ndash 83 208 42 ndash ndash ndash ndash ndash ndash ndash ndash ndash

32 111 500 ndash ndash 278 111 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

33 ndash ndash ndash ndash 1000 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash


35 182 636 ndash ndash 182 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash

36 385 462 ndash ndash ndash 77 ndash ndash ndash ndash 77 ndash ndash ndash ndash ndash

37 ndash 250 ndash ndash 750 ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash ndash



40 447 ndash ndash ndash 43 20 85 ndash 20 ndash ndash ndash ndash 383 ndash ndash

41 258 387 ndash ndash ndash ndash ndash ndash ndash ndash ndash 97 258 ndash ndash ndash

42 615 ndash ndash ndash ndash 38 ndash 346 ndash ndash ndash ndash ndash ndash ndash ndash

43 667 167 ndash ndash ndash 67 ndash 100 ndash ndash ndash ndash ndash ndash ndash ndash

44 469 250 ndash ndash 141 16 ndash 78 47 ndash ndash ndash ndash ndash ndash ndash


Discussion

Sampling issues

The overall low trap success in the grassland biome of the FreeState represents a challenge for the use of small mammals forassessment of ecosystem integrity as does the relatively smallnumber of species that are captured with any regularityNevertheless a strong case can be made for following aconsistent sampling protocol for assessment of small mammalcommunity structure both in terms of the timing of surveys trapspacing and the duration of trapping periods

For small mammal surveys in the Free State grasslandssampling during the period autumn to early winter is clearlymost productive High trap success during these periods isprobably due to the fact that small mammal densities are attheir highest at the end of the breeding season which in thegrassland biome is in late autumn (National Museum recordsN Avenant pers obs) Also at this time food resources aredeclining while energy needs are increasing due to the drop intemperature The cold dry winters result in a sudden massivedrop in small mammal numbers annually observed from early tomid-winter (Bronner et al 1988 N Avenant pers obs) Thecombination of high population density and declining foodresources may encourage even trap-shy individuals andspecies to visit traps Conversely the low trap success inspring and summer may be attributed to the fact thatpopulation numbers are still low during these seasons whilefood is becoming relatively abundant reflecting the onset of plantgrowth in early spring

At the TdR locality where trapping occurred over an extendedperiod the highest species richness was reached between threeand four trap-nights with immigration starting to have asignificant effect on the diversity and evenness scores fromthe sixth day (Avenant and Cavallini 2007) A comparableresult has been obtained from several other studies (Avenant2000a 2000b Avenant et al 2008 unpublished results) andthe 3ndash4 night sampling period appears to be a useful robuststandard Likewise the 5m trap spacing on transects was shown

by Ferreira and Avenant (2003) to be optimal for determiningspecies richness diversity and similarity estimates

Individual species as indicator species

The multimammate mouse Mastomys coucha has exceptionallyhigh reproductive output and is commonly thought to be a goodindicator of disturbance In the Free State their numbersconsistently dominate small mammal communities inanthropogenically disturbed areas or in areas where primaryproductivity (inter alia food availability) increases shortly afternatural disturbances such as fire or periods of drought (Avenantet al 2008) This is consistent with studies on the specieselsewhere in South Africa and more widely in Africa Forexample Meester et al (1979) Mendelsohn (1982) Bronneret al (1988) Linn (1991)Rowe-Rowe (1995)Leirs et al (1996)Monadjem (1997) Ferreira and Van Aarde (2000) and Caro(2001) have all reported Mastomys spp to be the first smallmammal to colonise and flourish after disturbances such asdrought fire overgrazing and cultivation Recent work by theauthor (N Avenant and E Schulze unpubl data) even suggeststhat this species does not vacate an area during or immediatelyafter fire the survivors merely stay on and outbreed anycompetition Furthermore while M coucha becomes lessabundant with advancing successional stage (Avenant andCavallini 2007 Avenant et al 2008) the species never totallydisappears from the area Although this species was absent fromthe sites with the highest EI values at Soetdoring Nature Reserve(Kuyler 2000) De Brug Army Training Camp (Kaiser 2005) andCNR their presence at other sites with high EI values (eg TdRN Avenant unpubl data) and in post-climax habitats elsewhere(N Avenant pers obs) makes one believe that this species nevertotally disappears from an area

Dendromus melanotis was only caught on the least disturbedgrassland transects (at KC CNR and TdR) Comparableobservations for this specialist species have been made inother southern African habitats (eg Rowe-Rowe 1995Ferreira and Van Aarde 1997 Avenant and Kuyler 2002unpubl data from the Glen area and numerous environmentalimpact assessments in theFreeState andLesotho) It is consideredto be a valuable indicator of late successional stage vegetation

The occurrence of some species seems to be linked moreclosely with substrate than successional stage For example thegerbil species Tatera brantsi and T leucogaster were caught onall transects with sandy substrates at the CNR locality regardlessof the EI value Micaelamys namaquensis is similarly linkedspecifically with rocky substrates while Crocidura cyaneaDendromus melanotis Elephantulus myurus Graphiurusmurinus Malacothrix typica Saccostomus campestris Musminutoides Mystromys albicaudatus Myosorex varius andOtomys irroratus were all found only in fairly specifichabitats as described by Skinner and Chimimba (2005)

Mystromys albicaudatus has been recorded during fourFree State studies all of them in areas with very to fairly lowEI values (Kuyler 2000 Kaiser 2005 Avenant and Cavallini2007 N Avenant unpubl data) In one study (N Avenant andE Schulze unpubl data)M albicaudatus appeared to enter thegrassland habitat approximately six months after fire and thendisappear from the habitat as succession progressed This pattern

6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s

Fig 4 Mean sd of small mammal species richness observed at 27habitats in the Free State grasslands 1995ndash2003 For transect numbers seeTable 1


was also observed by Kuyler (2000) and Kaiser (2005) whorecordedMalbicaudatus in siteswith fairly lowEIvalues but notat the lowest or at high values

The indicator status of Mus minutoides andMyosorex variusin Free State grasslands remains uncertain Both species weregenerally recorded at sites with highest species richness EIvalues andor diversity indices (Tables 1 2) However therewere exceptions that belie any simple interpretation (eg forM varius at TN3 and TN14 for M minutoides at TN25 andTN42) Elsewhere in South Africa these species have beenrecorded as inhabitants of later successional stages (eg Rowe-Rowe (1995) ndash montane grasslands Ferreira and Van Aarde(1997) ndash rehabilitated coastal dunes) However M minutoideshas also been recorded as dominating the small mammal fauna

immediately after burning in the KwaZulu-Natal Midlandgrasslands (J Watson pers comm 2009) and Kern (1981)reported increased densities of this species in burnt areas inbushveld in the Kruger National Park


In the two localities where both sets of measures are available(CNR and TdR) small mammal species richness and diversity isclearly correlated with EI values This finding is consistent withAvenantrsquos (2005) application of the Tilman successional modelof species diversity to the related context of ecosystem integrityin the grassland biome Small mammal densities also increasedwith EI at CNR but not at TdR A significant finding is that theecological generalist Mastomys coucha was numerically mostdominant on transects with the lowest EI values and at CNR theywere absent from the transect with the highest EI value On theother hand the specialist species Dendromus melanotis and

4

3

2

1

0

Spring Summer Autumn

Season

Spe

cies

ric

hnes

s

Winter

Fig 5 Mean (95CI) seasonal small mammal species richness observedat five localities in the Free State grasslands 1995ndash2003 Tussen-die-Riviere Nature Reserve amp Caledon Nature Reservecurren Sandveld NatureReserve ~ Korannaberg Conservancy amp Willem Pretorius NatureReserve

80

70

60

50

40

30

Spring Summer AutumnSeason

o

f tot

al s

peci

es r

ichn

ess

Winter

Kruskal-Wallis H3 110 = 19012 p lt 00005

Fig 6 Mean (95CI) seasonal contribution towards total small mammalspecies richness observed on specific transects in the Free State grasslandsNumber of transects = 27 Letters in superscript refer to homologousgroupings derived from multiple comparisons of mean ranks for all groups

18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty

Transect number36 38 40 42 44

06

Fig 7 Mean sd and 95 CI of small mammal Shannon diversity in 27habitats in the Free State grasslands 1995ndash2003 For transect numberssee Table 1

25

20

15

10

05

00Spring Summer Autumn

Div

ersi

ty

SeasonWinter

Shannon Hprime H3 110 = 8102 p lt 005

Simpson (1D) H3 110 = 7454 p gt 005

Fig 8 Mean (95 CI) small mammal diversity on 27 transects in theFree State grasslands


Mus minutoides were only found at the plots with the highest EIvalues Comparable observations for these species have beenmade in several other relatively long-term southern Africanstudies (Rowe-Rowe and Lowry 1982 Rowe-Rowe 1995Ferreira and Van Aarde 1999 2000) and in the Free State inshort-term studies (Avenant 1996 1997 2000a 2000b 20022004 Avenant and Kuyler 2002 Avenant and Watson 2002)

While EI values are not available for QQNP and WPNRother observations at these localities support the notion thattransects were placed in disturbed vegetation (Avenant 1997Avenant 2000a J du Preez pers comm 1999) Both localitieshad small mammal communities with relatively lower thananticipated species richness (based on other regional records)low diversities (per trap season and site) and a relatively highcontribution by Mastomys coucha (in QQNP especially in aspecific area where anthropogenic disturbance is highest)

At the KC locality the four transects within the conservancyshowed high species richness and diversity the presence ofspecialists and a relatively low contribution of M couchaThese are interpreted here as indicators of a healthy andrelatively stable ecosystem In contrast the fifth transect(TN30) placed on the border of the conservancy in whatappeared to be a lsquoclimaxrsquo habitat housed very few speciesshowed low diversity with no specialists and the nocturnalsmall mammal component was completely dominated byMastomys coucha The high trap success (of M coucha andR pumilio) in this seemingly resource rich habitat confirmedour suspicion that lsquointegrityrsquo should not be strictly equatedwith food availability and that integrity should best be testedatmore than one ecosystem level This notionwas later supportedat the De Brug Army Training Base where SAGraSScorrelated with EI but where all small mammal variablessuggested ecosystem disturbance (Kaiser 2005) At KC thisgreater degree of disturbance was not necessarily due totrampling and grazing of domestic animals (TN27 was alsofrequently grazed by these animals) but probably due todifferences in the small- to medium-sized predator componentTransect number 30 is the only transect more accessible to people

and dogs the latter having been observed at some of the workersrsquohouses The absence of natural predators (Norrdahl andKorpimaumlki 1995 Cole and Wilson 1996) and the presence ofdogs (Lynch 1994 Nel et al 1996 Avenant 1997) have beenmentioned as factors that may decrease mammal diversity andtherefore indirectly lead to an overall decrease in biodiversity(Tilman et al1996 Griffiths 1999 Avenant 2000a)

At Maguga (Avenant and Kuyler 2002) further supportcame from a contrast between the two most disturbed sites(a cultivated area and a thicket under exotic Lantana sp) andthe two least disturbed sites (thicket and open woodland) In thetwomost disturbed habitats the lowest number of small mammalspecies was found (15 10 n= 4) Shannon diversity waslowest (0188 0375) and a multimammate Mastomys spdominated (6765 4718) In the two least disturbedhabitats species richness was highest (50 08 n= 4)Shannon diversity was highest (1438 0239) and themultimammate mouse contributed only 1395 752 to thetotal catch

This study has not produced any evidence relevant toassessing the reality of the post-climax component of theTilman model in regard to grassland rodents We anticipatethat species richness and diversity will decrease in the post-climax phase probably to fluctuate around a fairly low speciesrichness and diversity score (N Avenant and E Schulzeunpubl data) Rhabdomys pumilio and Mastomys coucha areboth candidates for decline in post-climax vegetation but ourlimited data from WPNR and Erfenisdam Nature Reserve (J duPreez pers comm 1999 E Schulze pers comm 2005)suggest that these species do not disappear altogether frompost-climax plots

Conclusions

The results of this study suggest that small mammals can beused in the assessment of ecosystem integrity in the grasslandbiome of southern Africa albeit under specific conditions andas a fairly coarse measure

One major conclusion is that in the Free State grasslandssmall mammal assessments should be done during autumn andearly winter Outside this time small mammal abundancesare either too low for practical assessment or specific speciesbecome difficult to trap on account of abundant alternative foodresources

Following this study more emphasis can be placed on theabundances of Mastomys coucha and Dendromus melanotis asgood indicators of disturbance history and integrity due to theirassociation with relatively more and less disturbed habitatsrespectively Mystromys albicaudatus is another potential goodindicator though less is known of its ecological role duringmid-successional stages High densities of Rhabdomyspumilio the only diurnal rodent in most of these habitats arenot necessarily an indication of ecosystem integrity but possiblyof primary productivity Species such as Tatera spp and Musminutoides do not behave consistently in relation to otherindicators of ecosystem integrity and should for now not beused as indicator species Elephantulus myurus Micaelamysnamaquensis Graphiurus murinus Saccostomus campestrisMalacothrix typica and Otomys irroratus should be regarded

095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001

Fig 9 Mean (95 CI) small mammal evenness on 27 transects in theFree State grasslands Letters in superscript refer to homologous groupingsderived from multiple comparisons of mean ranks for all groups


as habitat-specific species as insufficient data are available toafford them any other status Presence of insectivores in an area isthought to be an excellent indication of ecosystem integrity(Pocock and Jennings 2008) but in the present study theywere recorded infrequently and would need to be assessed bysome other means to become useful indicators of environmentalcondition in Free State habitats

Species richness and calculated diversity indices for smallmammals are probably good indicators of environmentalintegrity In this study these two variables correlatedpositively with each other However too much emphasisshould not be placed on diversity index values especiallywhere trap success is low Rather the combination of speciesrichness diversity relative contribution of Mastomys couchapresence or absence of specialist species and the presence orabsence of Mystromys albicaudatus should all be taken intoaccount The trapability of various species needs to betaken into account as chance captures of elusive species suchas Suncus varilla and Otomys irroratus can have a pronouncedimpact on the community variables investigated here

AcknowledgementsWe thank the Department of Economic Development Tourism andEnvironmental Affairs Free State Province (DETEA) and the Council andDirectors of the National Museum Bloemfontein for permission to carry outthis work Gratitude is also expressed towards the wardens and staff ofthe nature reserves in which the fieldwork was done The contributions ofJ Eksteen PWilliamsonWKaiser J du Plessis I Sekhuni and J Senoge inthe field are acknowledged as are the valuable contributions of all previousco-authors The comments of two reviewers have improved the manuscriptand are highly appreciated The protocols for the various sub-projects were allapprovedbyboth theNationalMuseumand theDEDTEAscientific divisionsThe followingpermitswere provided in recognition that the protocols adheredto theNationalMuseumcodeof practiseHKP5B01289002HKP105243001 HKP5B00837001 HKP105243003 and HKP5B00837002 Alarge part of this work would not have been possible without the financialsupport of the National Research Foundation of South Africa

References

Abramsky Z (1988) The role of habitat and productivity in structuringdesert rodent communities Oikos 52 107ndash114 doi1023073565989

Abramsky Z and Rosenzweig M L (1984) Tilmanrsquos predictedproductivity-diversity relationships shown by desert rodent Nature309 150ndash151 doi101038309150a0

Avenant M F (2010) Challenges in using fish communities for assessingthe ecological integrity of non-perennial riversWater SA 36 397ndash405

AvenantN L (1996) Identification and distribution of twoMastomys spp inLesotho and part of South AfricaNavorsinge van die NasionaleMuseumBloemfontein 12 49ndash58

Avenant N L (1997) Mammals recorded in the QwaQwa National Park(1994ndash1995) Koedoe 40 31ndash40

Avenant N L (1998) Mammals EIA Maguga Dam Swaziland (AfridevConsultants Darling South Africa)

Avenant N L (2000a) Small mammal community characteristics asindicators of ecological disturbance in the Willem Pretorius NatureReserve Free State South Africa South African Journal of WildlifeResearch 30 26ndash33

Avenant N L (2000b) Terrestrial small-mammal diversity in KorannabergConservancy Free State South Africa Navorsinge van die NasionaleMuseum Bloemfontein 16 69ndash82

Avenant N L (2002) Mammals In lsquoBiological Resource Monitoringrsquopp 81ndash91 (Ed C Mokuku) (NULS-Consuls Maseru Lesotho)

Avenant N L (2003a) The use of small-mammal communitycharacteristics as an indicator of ecological disturbance in theKorannaberg Conservancy In lsquoRats Mice and People Rodent Biologyand Managementrsquo (Eds G R Singleton L A Hinds C J Krebs andDM Spratt) pp 95ndash98 (AustralianCentre for InternationalAgriculturalResearch Canberra)

Avenant N L (2003b) Mammals In lsquoFaunal Rescue Program Mohalersquo(Ed T Moeti) pp 65ndash73 (National University of Lesotho RomaLesotho)

Avenant N L (2004) Mammal Report Submitted to UNDP Lesotho aspart of the lsquoConserving Mountain Biodiversity in Southern Lesothorsquoprogram

Avenant N L (2005) Barn owl pellets a useful tool for monitoring smallmammal communities Belgian Journal of Zoology 135 39ndash43

Avenant N L and Cavallini P (2007) Correlating rodent communitystructure with ecological integrity Tussen-die-Riviere Nature ReserveFree State Province South Africa Integrative Zoology 2 212ndash219doi101111j1749-4877200700064x

Avenant N L and Kuyler P (2002) Small mammal diversity in theMaguga area Swaziland South African Journal of Wildlife Research32 101ndash108

Avenant N L andWatson J P (2002) Mammals recorded in the SandveldNature Reserve Free State province South Africa Navorsinge van dieNasionale Museum Bloemfontein 18 1ndash12

Avenant N L Watson J P and Schulze E (2008) Correlating smallmammal community characteristics and ecosystem integrity in theCaledon Nature Reserve South Africa Mammalia 72 186ndash191doi101515MAMM2008023

Baker S C (2006)A comparison of litter beetle assemblages (Coleoptera) inmature and recently clearfelled Eucalyptus obliqua forest AustralianJournal of Ecology 45 130ndash136

Beccaloni G W and Gaston K J (1995) Predicting species richness ofneotropical forest butterflies ndash Ithomiinae (Lepidoptera Nymphalidae) asindicators Biological Conservation 71 77ndash86 doi1010160006-3207(94)00023-J

Birney E C GrantWC andBaird DD (1976) Importance of vegetativecover to cycles of Microtus populations Ecology 57 1043ndash1051doi1023071941069

Bronner G Rautenbach I L and Meester J (1988) Environmentalinfluence on reproduction in the Natal multimammate mouseMastomys natalensis (A Smith 1834) South African Journal ofWildlife Research 18 142ndash148

Bultman T Uetz GW andBrady A R (1982) A comparison of cursorialspider communities along a successional gradient The Journal ofArachnology 10 23ndash33

Cardinale B J Nelson K and Palmer M A (2000) Linking speciesdiversity to the functioning of ecosystems on the importance ofenvironmental context Oikos 91 175ndash183 doi101034j1600-07062000910117x

CareyAB andWilson SM (2001) Induced spatial heterogeneity in forestcanopies responses of small mammals The Journal of WildlifeManagement 65 1014ndash1027 doi1023073803050

Caro TM (2001) Species richness and abundance of small mammals insideand outside an African national park Biological Conservation 98251ndash257 doi101016S0006-3207(00)00105-1

Chapin F S Zavaleta E S Eviner V T Naylor R L Vitousek P MReynolds H L Hooper D U Lavorel S Sala O E Hobbie S EMackMC andDiaz S (2000)Consequencesof changingbiodiversityNature 405 234ndash242 doi10103835012241

Chutter F M (1988) Research on the rapid biological assessment of waterquality impacts in streams and rivers Report No 422198 (WaterResearch Commission Pretoria South Africa)


Cole F R and Wilson D E (1996) Mammalian diversity and naturalhistory In lsquoMeasuring and Monitoring Biological Diversity StandardMethods for Mammalsrsquo (Eds D E Wilson F R Cole J D NicholsR Rudran and M S Foster) pp 9ndash40 (Smithsonian InstitutionWashington DC)

DEAT(2005)SouthAfricarsquosNationalBiodiversityStrategyandActionPlan(Department of Environmental Affairs and Tourism Pretoria SouthAfrica)

DEAT (2006) South African Environment Outlook A Report on the State ofthe Environment (Department of Environmental Affairs and TourismPretoria South Africa)

Ecke F Loumlfgren O and Soumlrlin D (2002) Population dynamics of smallmammals in relation to forest age and structural habitat factors in northernSweden Journal of Applied Ecology 39 781ndash792 doi101046j1365-2664200200759x

Ferreira S M and Avenant N L (2003) Influences of trap-spacing ondescriptors of hypothetical small mammal communities in Free Stategrasslands Navorsinge van die Nasionale Museum Bloemfontein 1921ndash30

Ferreira S M and Van Aarde R J (1997) The chronosequence ofrehabilitating stands of coastal dune forest do small mammals confirmit South African Journal of Science 93 211ndash214

Ferreira S M and Van Aarde R J (1999) Habitat associations andcompetition in MastomysndashSaccostomysndashAethomys assemblages oncoastal dune forests African Journal of Ecology 37 121ndash136doi101046j1365-2028199900156x

Ferreira S M and Van Aarde R J (2000) Maintaining diversity throughintermediate disturbances evidence from rodents colonizingrehabilitating coastal dunes African Journal of Ecology 38 286ndash294doi101046j1365-2028200000254x

Fonseca C R and Ganade G (2001) Species functional redundancyrandom extinctions and the stability of ecosystems Journal of Ecology89 118ndash125 doi101046j1365-2745200100528x

Fox B J (1982) Fire andmammalian secondary succession in an Australiancoastal heath Ecology 63 1332ndash1341 doi1023071938861

Fox B J (1990) Changes in the structure of mammal communities oversuccessional time scales Oikos 59 321ndash329 doi1023073545142

FoxB J andFoxMD (1984)Smallmammal recolonizationof open forestfollowing sand mining Australian Journal of Ecology 9 241ndash252doi101111j1442-99931984tb01361x

GlennonM J and PorterW F (2007) Impacts of land-usemanagement onsmall mammals in the Adirondack Park New York NortheasternNaturalist 14 323ndash342 doi1016561092-6194(2007)14[323IOLMOS]20CO2

Griffiths D (1999) On investigating local-regional species richnessrelationships Journal of Animal Ecology 68 1051ndash1055 doi101046j1365-2656199900348x

Grime J P (1998) Benefits of plant diversity to ecosystems immediatefilter and founder effects Journal of Ecology 86 902ndash910 doi101046j1365-2745199800306x

Hastwell G T and Huston M A (2001) On disturbance and diversity areply to Mackey and Currie Oikos 92 367ndash371 doi101034j1600-07062001920220x

Hoffmann A and Zeller U (2005) Influence of variations in land useintensity on species diversity and abundance of small mammals in theNama Karoo Namibia Belgian Journal of Zoology 135 91ndash96

Johnson K H (2000) Trophic-dynamic considerations in relatingspecies diversity to ecosystem resilience Biological Reviews of theCambridge Philosophical Society 75 347ndash376 doi101017S0006323100005508

Jones D T and Eggleton P (2000) Sampling termite assemblagesin tropical forests testing a rapid biodiversity assessment protocolJournal of Applied Ecology 37 191ndash203 doi101046j1365-2664200000464x

Joubert D F and Ryan P G (1999) Differences in mammal and birdassemblages between commercial and communal rangelands in theSucculent Karoo South Africa Journal of Arid Environments 43287ndash299 doi101006jare19990553

Kaiser W (2005) The characteristics of insect and small mammalcommunities as a reflection of the ecological value of grasslandsMasters Thesis University of the Free State Bloemfontein South Africa

Kaiser W Avenant N L and Haddad C R (2009) Assessing theecological integrity of a grassland ecosystem refining the SAGraSSmethod African Journal of Ecology 47 308ndash317 doi101111j1365-2028200800962x

Karr J R Fausch K D Angermeier P L Yant P R and SchlosserI J (1986) Assessing biological integrity in running waters a methodand its rationale Illinois Natural History Survey Special Publication 5

Kern N G (1981) The influence of fire on populations of small mammals ofthe Kruger National Park Koedoe 24 125ndash157

KirklandGL Jr (1990) Patterns of initial smallmammal community changeafter clearcutting of temperate North American forests Oikos 59313ndash320 doi1023073545141

Kleynhans C J (1999) The development of a fish index to assess thebiological integrity of South African Rivers Water SA 25 265ndash278

Klinger R (2006) The interaction of disturbances and small mammalcommunity dynamics in a lowland forest in Belize Journal of AnimalEcology 75 1227ndash1238 doi101111j1365-2656200601158x

Kuyler P (2000) Veld condition assessment and small mammal communitystructure in the management of Soetdoring Nature Reserve Free StateSouth AfricaMasters Thesis University of the Free State BloemfonteinSouth Africa

Leirs H Verhagen R Verheyen W Mwanjabe P and Mbise T (1996)Forecasting rodent outbreaks in Africa an ecological basis forMastomyscontrol in Tanzania Journal of Applied Ecology 33 937ndash943doi1023072404675

Letnic M Dickman C R Tischler M K Tamayo B and Beh C L(2004) The responses of small mammals and lizards to post-firesuccession and rainfall in arid Australia Journal of Arid Environments59 85ndash114 doi101016jjaridenv200401014

Linn I J (1991) Influence of 6-methoxybenzoxazolinone and greenvegetation on reproduction of the multimammate rat Mastomyscoucha South African Journal of Wildlife Research 21 33ndash37

Loreau M (2000) Biodiversity and ecosystem functioning recenttheoretical advances Oikos 91 3ndash17 doi101034j1600-07062000910101x

Low A B and Rebelo A G (1996) lsquoVegetation of South Africa Lesothoand Swazilandrsquo (Department of Environmental Affairs and TourismPretoria South Africa)

LynchCD (1994)Themammals ofLesothoNavorsinge vandieNasionaleMuseum Bloemfontein 10 177ndash241

Magurran A E (2004) lsquoMeasuring Biological Diversityrsquo (BlackwellOxford)

Majer J D (1983) Ants bio-indicators of minesite rehabilitation land-useand land conservation Environmental Management 7 375ndash383doi101007BF01866920

McCann K S (2000) The diversity-stability debate Nature 405 228ndash233doi10103835012234

McGeoch M A Van Rensburg B J and Botes A (2002) Theverification and application of bioindicators a case study of dungbeetles in a savanna ecosystem Journal of Applied Ecology 39661ndash672 doi101046j1365-2664200200743x

McGeoch M A (1998) The selection testing and application of terrestrialinsects as bioindicators Biological Reviews of the CambridgePhilosophical Society 73 181ndash201 doi101017S000632319700515X

Meester JA J LloydCNV andRowe-RoweDT (1979)Anote on theecological role of Praomys natalensis South African Journal of Science75 183ndash184


Mendelsohn J M (1982) Notes on small mammals on the Springbok FlatsTransvaal South African Journal of Zoology 17 197ndash201

Mikola J and Setaumllauml H (1998) Relating species diversity to ecosystemfunctioning mechanistic backgrounds and experimental approach witha decomposer food web Oikos 83 180ndash194 doi1023073546560

Monadjem A (1997) Stomach contents of 19 species of small mammalsfrom Swaziland South African Journal of Zoology 32 23ndash26

Nel J Avenant N and PurvesM (1996)Mammals Final Report ContractNo 1008 Baseline Biology Survey and Reserve Development Phase1B (Afridev Consultants Darling South Africa)

New T R (1999) Untangling the web spiders and the challenges ofinvertebrate conservation Journal of Insect Conservation 3 251ndash256doi101023A1009697104759

Norrdahl K and Korpimaumlki E (1995) Effects of predator removal onvertebrate prey populations birds of prey and small mammalsOecologia103 241ndash248 doi101007BF00329086

Orgeas J and Andersen A N (2001) Fire and biodiversity responses ofgrass-layer beetles to experimental fire regimes in an Australian tropicalsavanna Journal of Applied Ecology 38 49ndash62 doi101046j1365-2664200100575x

Pearce J and Venier L (2005) Small mammals as bioindicators ofsustainable boreal forest management Forest Ecology andManagement 208 153ndash175 doi101016jforeco200411024

Pearson D L and Cassola F (1992) World-wide species richnesspatterns of tiger beetles (Coleoptera Cicindelidae) indicator taxon forbiodiversity and conservation studiesConservation Biology 6 376ndash391doi101046j1523-1739199206030376x

Pearson D E and Ruggiero L F (2003) Transect versus grid trappingarrangements for sampling small-mammal communities WildlifeSociety Bulletin 31 454ndash459

Petchey O L (2000) Species diversity species extinction and ecosystemfunction American Naturalist 155 696ndash702 doi101086303352

Petit S and Usher M B (1998) Biodiversity in agricultural landscapesthe ground beetle communities of woody uncultivated habitatsBiodiversity and Conservation 7 1549ndash1561 doi101023A1008875403868

Pocock M J O and Jennings N (2008) Testing biotic indicator taxa thesensitivity of insectivorous mammals and their prey to the intensificationof lowland agriculture Journal of Applied Ecology 45 151ndash160doi101111j1365-2664200701361x

Rainio J and Niemelauml J (2003) Ground beetles (Coleoptera Carabidae) asbioindicators Biodiversity and Conservation 12 487ndash506 doi101023A1022412617568

Rich T D (2002) Using breeding land birds in the assessment of westernriparian systems Wildlife Society Bulletin 30 1126ndash1139

Rodriacuteguez J P Pearson D L and Barrera R R (1998) A test for theadequacy of bioindicator taxa are tiger beetles (Coleoptera Cicindelidae)appropriate indicators formonitoring the degradation of tropical forests inVenezuela Biological Conservation 83 69ndash76 doi101016S0006-3207(97)00017-7

Rosenzweig M L (1995) lsquoSpecies Diversity in Space and Timersquo(Cambridge University Press Cambridge)

Rowe-Rowe D T (1995) Small-mammal recolonization of a fire-exclusioncatchment after unscheduled burning South African Journal of WildlifeResearch 25 133ndash137

Rowe-Rowe D T and Lowry P B (1982) Influence of fire on small-mammal populations in the Natal Drakensberg South African Journal ofWildlife Research 12 130ndash139

Rowe-Rowe D T and Meester J (1982) Habitat preferences andabundance relations of small mammals in the Natal DrakensbergSouth African Journal of Zoology 17 202ndash209

Seaman M T and Louw S vdM (1999) SAGraSS a biomonitoringmethod for grasslands In lsquoIAIAsarsquo99 Conference Proceedingsrsquopp 231ndash238 (University of the Free State Bloemfontein South Africa)

Skinner J D and Chimimba C T (2005) lsquoThe Mammals of the SouthernAfrican Subregionrsquo (Cambridge University Press Cape Town)

Tilman D (1982) lsquoResource Competition and Community Structurersquo(Princeton University Press Princeton)

Tilman D Wedin D and Knops J (1996) Productivity and sustainabilityinfluencedbybiodiversity in grassland ecosystemsNature379 718ndash720doi101038379718a0

Van Rooyen N (2002) Veld management in the savannas In lsquoGame RanchManagementrsquo (Ed J du P Bothma) pp 571ndash620 (Van SchaikPublishers Pretoria South Africa)

Vorster M (1982) The development of the ecological index method forassessing veld condition in the Karoo Proceedings of the GrasslandSociety of South Africa 17 84ndash89

Wang G Wang Z Zhou Q and Zhong W (1999) Relationship betweenspecies richness of small mammals and primary productivity of arid andsemi-arid grasslands in north China Journal of Arid Environments 43467ndash475 doi101006jare19990572

Wootton J T (1998) Effects of disturbance on species diversity amultitrophic perspective American Naturalist 152 803ndash825doi101086286210


wwwpublishcsiroaujournalswr

assessments typically sample several different groups oforganisms the development of an effective integratedmonitoring strategy for South African grassland ecosystems islong overdue A key step is the determination of informativeeasily assessed indicator groups Based on the success of theSASS and the River Health Program inmonitoring the ecologicalintegrity of South African rivers a grassland health programbased on insect assemblages was suggested (Seaman and Louw1999) However the proposed Southern African grasslandscoring system (SAGraSS) has proven time consuming anddifficult to implement and further refinement and testing ofthe system is essential (Kaiser et al 2009) In South Africathese environmental indicators lsquoform the basis of the state of theenvironment reportingrsquo (DEAT 2006) However when reportedon consistently over time they might also hold potential forassessing the effectiveness of management actions aimed atspecific environmental pressures

Small mammal communities have been investigated as bio-indicators in many different environmental contexts (Fox andFox 1984 Kirkland 1990 Carey and Wilson 2001 Ecke et al2002 Pearce and Venier 2005 Hoffmann and Zeller 2005Klinger 2006 Avenant and Cavallini 2007 Glennon andPorter 2007) This group offers multiple advantages as bio-indicators they typically are adapted for survival in relativelysmall areas most species reproduce rapidly and thus show goodresponse to successional changes in vegetation and theygenerally can be sampled using relatively quick easy andinexpensive methods (Ferreira and Avenant 2003 Avenantet al 2008) Compared with plants and invertebrates they arealso fairly easy to identify and for many there is a body ofnatural history information regarding their biology

In southern Africa variation in small mammal communitystructure is thought to reflect parameters such as habitat structureand complexity rainfall and primary productivity predationdisturbance history of the vegetation including firingtrampling and grazing patch size and the distance betweensimilar habitats and the presence of exotics (Avenant 2000a2000b) The impact of these factors on individual small mammalspecies can be expected to vary according to their physiologicalnutritional social and anti-predator requirements (see Birneyet al 1976) while the outcomes at a community level shouldreflect both the complex interplay of factors and the influence ofinter-specific competition Despite the inevitable complexity areasonable expectation is that prolonged or intense ecologicaldisturbancewill lead to a loss of ecosystem lsquointegrityrsquo associatedeither with invasion by exotic organisms with changes in soilfertility or structure or with loss of ecosystem function (egthrough removal of large mammals or predators) and that thiswill be reflected in a decline in small mammal species richness(Avenant 2000b 2005) A theoretical basis for this prediction isfound in Tilmanrsquos hump-shaped curve model (Tilman 1982Fig 1) which predicts an increase in the number of specieswith advancing successional stage after disturbance up to thepoint of ecological climax followed by a secondary decline inpost-climax contexts (also see Rosenzweig 1995) Tilmanrsquosmodel is supported by numerous empirical studies that havedemonstrated correlations between species diversity anddisturbance (eg Wootton 1998 Hastwell and Huston 2001)and between species diversity and declines in ecosystem

function resilience and resistance (Grime 1998 Cardinaleet al 2000 Chapin et al 2000 Johnson 2000 Loreau 2000McCann 2000 Petchey 2000 Fonseca and Ganade 2001)Although successional stage and lsquointegrityrsquo are not equivalentecological concepts (indeed natural disturbance regimes areundoubtedly essential in maintaining ecological integrity) inthe present context the level of historical and contemporarydisturbance is such as to expect that Tilmanrsquos model forsuccession can be applied to stages in ecosystem degradation(ie loss of integrity) and recovery (see also Avenant 2005)Application of the model to small mammal communities issupported by studies of rodents in Chinese grasslands (Wanget al 1999) and by several studies conducted on rodents in SouthAfrica (eg Rowe-Rowe and Lowry 1982 Rowe-Rowe 1995Ferreira and VanAarde 2000) and elsewhere (eg Abramsky andRosenzweig 1984 Abramsky 1988 Rosenzweig 1995)

In this paper I explore the utility of small mammals asindicators of habitat lsquointegrityrsquo in the grassland biome of theFree State of South Africa with a broader view to enhancing therole of this group of organisms in environmental assessment andmanagement Thedataset is a compilation of results obtainedoverthe past ~15 years (eg Avenant 1998 2002 2003b 2004 Nelet al 1996) and derives from many different short-term studiesand environmental assessments carried out for a variety ofreasons and with somewhat contrasting methodologies Whilea longer-term multi-organism project in one locality is inprogress this study uses all of the previously generated datafrom the Free State grassland biome to explore general aspects ofsmall mammal community structure and to provide a benchmarkagainst which future small mammal assessments and monitoringcan be measured

Materials and methodsStudy area

Table 1 and Fig 2 summarise the trapping history and effort atsix study areas ndash QwaQwa National Park (QQNP) WillemPretorius Nature Reserve (WPNR) Korannaberg Conservancy

SuccessionEcological integrity

Num

ber

of s

peci

es

Fig 1 Hypothesis for using small mammals as indicators of habitatintegrity in the South African grasslands tested in the current study







1A

2A

3A

4A

5A

6A

7A

8A

9A

10A

11A

12A

13A

14A

15A

16A

17A

306186120094534040226134080160054134026040080320374

43215233412212263

09370892034900001141063710280639124200000693050000000637045117920956

22572257128510002793300329591608500010000000166700103003140000003003

045807510475ndash

03550924077706450884ndash

10000715ndash

0924063410000851


18B

19B

20B

21B

22B

23B

24B

25B

294169067058098160243436

22322323

01180692097002710655103904240734

12762049269511821942282513532020

05060998075603660950063605920236


26C

27C

28C

29C

30C

411189072124381

75552

18371325130412510292

61733021349731851188

08650747053904520394


31C

32C

33C

34C

35C

36C

151110071408

541134

125811910000000009081119

300331851000100022423115

059107680513060306940709


37C (430)38C (548)39C (629)40C (878)

075019188294

2236

0562063707301235

1692300317612924

0813092405310403


41C (240)42C (424)43C (491)44C (593)

1219096911562219

4346

1293079109801385

3717208321323333

0684050106110464



Data collection






Results













0270027024002130

1122

0000000003500380

1000100012851333

ndash

ndash

04750517


0000027018700000

0120

0000000006000000

0000100019080000

ndash

ndash

0868ndash


0000080010700000

0220

0000064005600000

0000300320000000

ndash

09240813ndash


0000000013300000

0020

0000000005000000

0000000016670000

ndash

ndash

0715ndash


0270000002700270

1011

0000000000000000

1000000010001000

1000ndash

10001000


0000000018700530

0022

0000000006800690

0000000023310000

ndash

ndash

09871000


0000000017800800

0022

0000000005000640

0000000016673003

ndash

ndash

07150924


0000053021300000

0110

0000000000000000

0000100010000000

ndash

10000850ndash


4960365031304700

6557

1430143314741754

3891478554956369

0587071907840772


2220157032600520

4352

1232082411850562

3676212826112000

0681060205690813


0390052010400910

2333

0637104009740956

3003598831153003

0924093207820803


1830065010401430

3342

0980105513210474

2674500055871486

0866093209010672


3260261054803910

2212

0440019900000451

1230111110001403

0617027500000440


1750050020001750

3232

0796000010400683

2101100034972331

0773096209080987









1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890


0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962


1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678




Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References









































































































1A

2A

3A

4A

5A

6A

7A

8A

9A

10A

11A

12A

13A

14A

15A

16A

17A

306186120094534040226134080160054134026040080320374

43215233412212263

09370892034900001141063710280639124200000693050000000637045117920956

22572257128510002793300329591608500010000000166700103003140000003003

045807510475ndash

03550924077706450884ndash

10000715ndash

0924063410000851


18B

19B

20B

21B

22B

23B

24B

25B

294169067058098160243436

22322323

01180692097002710655103904240734

12762049269511821942282513532020

05060998075603660950063605920236


26C

27C

28C

29C

30C

411189072124381

75552

18371325130412510292

61733021349731851188

08650747053904520394


31C

32C

33C

34C

35C

36C

151110071408

541134

125811910000000009081119

300331851000100022423115

059107680513060306940709


37C (430)38C (548)39C (629)40C (878)

075019188294

2236

0562063707301235

1692300317612924

0813092405310403


41C (240)42C (424)43C (491)44C (593)

1219096911562219

4346

1293079109801385

3717208321323333

0684050106110464



Data collection






Results













0270027024002130

1122

0000000003500380

1000100012851333

ndash

ndash

04750517


0000027018700000

0120

0000000006000000

0000100019080000

ndash

ndash

0868ndash


0000080010700000

0220

0000064005600000

0000300320000000

ndash

09240813ndash


0000000013300000

0020

0000000005000000

0000000016670000

ndash

ndash

0715ndash


0270000002700270

1011

0000000000000000

1000000010001000

1000ndash

10001000


0000000018700530

0022

0000000006800690

0000000023310000

ndash

ndash

09871000


0000000017800800

0022

0000000005000640

0000000016673003

ndash

ndash

07150924


0000053021300000

0110

0000000000000000

0000100010000000

ndash

10000850ndash


4960365031304700

6557

1430143314741754

3891478554956369

0587071907840772


2220157032600520

4352

1232082411850562

3676212826112000

0681060205690813


0390052010400910

2333

0637104009740956

3003598831153003

0924093207820803


1830065010401430

3342

0980105513210474

2674500055871486

0866093209010672


3260261054803910

2212

0440019900000451

1230111110001403

0617027500000440


1750050020001750

3232

0796000010400683

2101100034972331

0773096209080987









1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890


0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962


1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678




Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References




































































































Data collection






Results













0270027024002130

1122

0000000003500380

1000100012851333

ndash

ndash

04750517


0000027018700000

0120

0000000006000000

0000100019080000

ndash

ndash

0868ndash


0000080010700000

0220

0000064005600000

0000300320000000

ndash

09240813ndash


0000000013300000

0020

0000000005000000

0000000016670000

ndash

ndash

0715ndash


0270000002700270

1011

0000000000000000

1000000010001000

1000ndash

10001000


0000000018700530

0022

0000000006800690

0000000023310000

ndash

ndash

09871000


0000000017800800

0022

0000000005000640

0000000016673003

ndash

ndash

07150924


0000053021300000

0110

0000000000000000

0000100010000000

ndash

10000850ndash


4960365031304700

6557

1430143314741754

3891478554956369

0587071907840772


2220157032600520

4352

1232082411850562

3676212826112000

0681060205690813


0390052010400910

2333

0637104009740956

3003598831153003

0924093207820803


1830065010401430

3342

0980105513210474

2674500055871486

0866093209010672


3260261054803910

2212

0440019900000451

1230111110001403

0617027500000440


1750050020001750

3232

0796000010400683

2101100034972331

0773096209080987









1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890


0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962


1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678




Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References








































































































0270027024002130

1122

0000000003500380

1000100012851333

ndash

ndash

04750517


0000027018700000

0120

0000000006000000

0000100019080000

ndash

ndash

0868ndash


0000080010700000

0220

0000064005600000

0000300320000000

ndash

09240813ndash


0000000013300000

0020

0000000005000000

0000000016670000

ndash

ndash

0715ndash


0270000002700270

1011

0000000000000000

1000000010001000

1000ndash

10001000


0000000018700530

0022

0000000006800690

0000000023310000

ndash

ndash

09871000


0000000017800800

0022

0000000005000640

0000000016673003

ndash

ndash

07150924


0000053021300000

0110

0000000000000000

0000100010000000

ndash

10000850ndash


4960365031304700

6557

1430143314741754

3891478554956369

0587071907840772


2220157032600520

4352

1232082411850562

3676212826112000

0681060205690813


0390052010400910

2333

0637104009740956

3003598831153003

0924093207820803


1830065010401430

3342

0980105513210474

2674500055871486

0866093209010672


3260261054803910

2212

0440019900000451

1230111110001403

0617027500000440


1750050020001750

3232

0796000010400683

2101100034972331

0773096209080987









1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890


0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962


1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678




Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References










































































































1000025022501000

2141

0562000011490000

2000100032681000

0896100007800850


1500050012500750

1111

0000000000000000

1000100010001000

0757096208010905


0500000017500500

1011

0000000000000000

1000000010001000

0962ndash

07190962


1750050020001250

2222

0410069306620673

1401000021552500

0738100008200916


0250075010001250

1223

0000063705620950

1000300320003333

1000095808960890


0250025007501750

1111

0000000000000000

1000100010001000

1000100009050719


0250000002500250

1011

0000000000000000

1000000010001000

1000ndash

10001000


0500025065000250

2131

0000000006440000

1000100016261000

0962100004631000


02500500

105000500

1141

0000000011160000

1000100026811000

1000096203440962


1625525033752250

2343

0500095012831099

2500250039373745

0819082805780900


2500125003751125

1132

0000000006550349

2000100018451486

0813100004090672


0125062506250375

1233

0000063706870800

1000200021231736

0850089605330386


0375175005000125

4444

1332127207011221

5587467318623247

0913067702830678




Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References






































































































Species richness










30

25

20

15

10

05

Season

Trap

succ








TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References








































































































TN

Rha

bdom

yspu

milio

Mastomys

coucha

Micaelamys

namaquensis

Taterabrantsi

Tateraleucog

aster

Mus

minutoides

Otomys

irroratus

Otomys

saundersiae

Dendrom

usmelanotis

Graphiurusmurinus

Malacothrix

typica

Saccostomus

campestris

Mystrom

ysalbicaud

atus

Myosorexvarius

Crocidu

racyan

ea

Eleph

antulusmyurus










































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References




































































































Discussion

Sampling issues










6

5

4

3

2

1

0

18 20 22 24 26 28 30 32 34 36 38 40 42 44Transect number

Spe

cies

ric

hnes

s








4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References









































































































4

3

2

1

0


Season

Spe

cies

ric

hnes

s

Winter


80

70

60

50

40

30


o

f tot

al s

peci

es r

ichn

ess

Winter



18

16

14

12

10

08

04

02

00

ndash02

ndash04

ndash06

18 20 22 24 26 28 30 32 34

Sha

nnon

div

ersi

ty


06


25

20

15

10

05


Div

ersi

ty

SeasonWinter


Simpson (1D) H3 110 = 7454 p gt 005









Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References










































































































Conclusions




095

090

085

080

075

070

065

060


Season

Eva

r

Winter

H3 91 = 12176 p lt 001






References







































































































References




































































































the potential utility of rodents and other small mammals...

Documents