Crustacean species richness in temporary pools: relationships

with habitat traits

Avi Eitam1,4,*, Leon Blaustein1, Kay Van Damme2, Henri J. Dumont2 & Koen Martens2,31Community Ecology Laboratory, Institute of Evolution, University of Haifa, 31905 Haifa, Israel2Department of Biology, Animal Ecology, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium3Institute of Biodiversity and Ecosytem Dynamics, University of Amsterdam, Mauritskade 57,1092 AD Amsterdam, The Netherlands4Present address: Department of Entomology, University of Kentucky, S-225 Ag. Science Center North,

Lexington, KY 40546-0091, U.S.A.(*Author for correspondence: Tel.: +859-257-2513, Fax: +859-323-1120, E-mail: eitam@yahoo.com)

Received 23 August 2003; in revised form 13 January 2004; accepted 27 January 2004

Key words: Cladocera, hydroperiod, Ostracoda, species–area, temporary ponds

Abstract

We examined species richness separately for cladocerans and ostracods in 52 temporary pools in a smallgeographical area, relating species richness with habitat traits using multiple regressions. Habitat traitsconsidered included surface area, water depth, permanence and sediment depth. Permanence was animportant predictor of species richness of both cladocerans and ostracods. Additionally, variation inostracod species richness was significantly explained by water depth (negative relationship) and sedimentdepth (positive relationship). Surface area was not a statistically significant factor in any of our analyses.The importance of permanence supports the hypothesis that extinction due to pool drying is a majordriving force behind the structuring of microcrustacean communities in temporary pools.

Introduction

Variation in species richness in temporary waterbodies can often be explained by pool size (Ward& Blaustein, 1994; March & Bass, 1995; Spenceret al., 1999) or permanence (Holland & Jenkins,1998; Spencer et al., 1999; Bilton et al., 2001;Eason & Fauth, 2001; Therriault & Kolasa, 2001).Larger pools are more likely to be colonized (Roth& Jackson, 1987; Pearman, 1995; Wilcox, 2001;Kiflawi et al., 2003). Invasion is more likely to besuccessful in larger pools because they can supportlarge populations, they contain a greater numberof microhabitats (March & Bass, 1995), and theyexperience temperature fluctuations of smalleramplitude (Bronmark & Hansson, 1998). Perma-nence, or hydroperiod, can influence the proba-bility to complete the reproductive cycle prior to

drying of the pool (Wellborn et al., 1996), thusaffecting the probability of extinction. On theother hand, pools with longer hydroperiods attractmore predator species (Spencer et al., 1999) andpredators may cause local extinctions of preferredprey species (e.g., Scott & Murdoch, 1984).

Many species richness studies consider a widetaxonomic range within a single analysis (e.g.,Spencer et al., 1999; Boix et al., 2001; Kiflawi et al.,2003).However,major taxamaydiffer in themannerin which they are influenced by various pool prop-erties (Hershey et al., 1999). For example, taxa thatexhibit microhabitat specialization, e.g., turbellari-ans, should be more influenced by pool size (Eitamet al., in press), while those with longer generationtimes would be more affected by permanence.

Hydrobiologia 525: 125–130, 2004.� 2004 Kluwer Academic Publishers. Printed in the Netherlands. 125

Here, we examine species richness separatelyfor cladocerans and ostracods in 52 temporarypools in a small geographical area, relatingrichness of each order with habitat traits in mul-tiple regression models. Traits considered includetwo components of pool size (surface area andwater depth), pool permanence and depth ofsediment, an important repository for resting eggs(Bronmark & Hansson, 1998). We compare ourresults with those for turbellarians derived fromthe same set of pools (Eitam et al., in press).Differences or similarities between these two or-ders of crustaceans, and between them and tur-bellarians, could elucidate the relative importanceof factors influencing their communities in tem-porary pools.

Materials and methods

The study site was located on the southern slope ofMt. Kabul and the adjacent northern slope of Mt.Shekhanya, Lower Galilee, Israel (32� 51¢ N,35� 14¢ E, elevation 340–390 m). The habitat is acombination of natural oak and planted pine for-est, greatly depressed by overgrazing; thus, themajority of the surface area is covered by bushessuch as Pistacia lentiscus L., with much exposedrock or soil.

We sampled from 52 pools, all within 2 km2.The urodele predator larval Salamandra salaman-dra L. was found in five of the larger and morepermanent pools; this predator can have largeimpacts on the structure of crustacean communi-ties (Blaustein et al., 1996; Blaustein, 1997; Eitamet al., unpublished). The pools ranged in surfacearea from 0.01 to 166 m2 (0.01–1.0 m2 for the 47pools without Salamandra), in water depth from0.1 to 80 cm (0.1–21 cm for pools without Sal-amandra), in permanence (hydroperiod) from 50 to173 days (50–165 days for pools without Salam-andra), and in sediment depth from 0.1 to 37 cm(0.1–37 cm for pools without Salamandra). Weestimated maximal surface area by measuring thelength and width with a tape measure, and mea-sured maximal water and sediment depth with agraduated stick. The index of permanence usedwas an estimate of the total number of days thatpools contained water during the season (details inEitam et al., in press).

Rainfall in Israel is restricted mainly to winter,with the majority of precipitation occurring be-tween December and February. Average annualrainfall in the area of our study site is approxi-mately 700 mm. To increase the probability of arepresentative sample of species richness, wesampled twice during a single season, on 30 Jan-uary and 18 March 2001. We performed singlesweeps with a 15 · 11 cm plankton net (mesh size:250 lm), collecting both from the sediment andthe water column. In large pools, we swept alength of approximately one meter; in poolssmaller than one meter in length, we swept theentire length of the pool. Preliminary samplingindicated that with this sampling regime we couldcollect the majority of crustacean species present inthese pools. We preserved the samples in 95% ethylalcohol and identified crustaceans under a stereo-microscope. Representative specimens were deter-mined to species in most cases by K. Van Damme(cladocerans) and K. Martens (ostracods).

We examined relationships between variouspool characteristics and species richness usingmultiple linear regression. We performed separateanalyses for cladocerans and ostracods, chosen forexamination because they were the most species-rich taxa in the pools besides turbellarians (seeEitam et al., in press). Statistically significant(p < 0.05) factors were added using the stepwiseselection procedure by order of their influence innature: maximal surface area (which should berelated to probability of colonization), maximalwater depth (successful colonization due to habitatheterogeneity), permanence (life cycle completion)and maximal sediment depth (avoidance of death/extinction). As we could not separate the effects ofthe presence of Salamandra and pool size/perma-nence, we repeated the analysis, first consideringall pools, and then excluding the five pools thatcontained Salamandra.

Results

Cladocera. Six species were identified (Table 1).One species, Alona cf. diaphana (allocated to thegenus Leberis by Sinev et al., in press) has notpreviously been reported from Israel (Bromley,1993). With all pools considered, pool permanence(p < 0.0001), but not surface area (p ¼ 0.99),

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Table 1. Cladocerans and ostracods collected in pools with (n ¼ 5) and without (n ¼ 47) larvae of the urodele predator Salamandra

salamandra

Order Species Number of pools

With Salamandra Without Salamandra

Cladocera Ceriodaphnia quadrangula Muller 4 2

Daphnia similis Claus 0 12

Alona cf. diaphana (King) 5 16

Macrothrix hirsuticornis Norman & Brady 0 5

Moina brachiata (Jurine) 3 2

Pleuroxus letourneuxi (Richard) 0 15

Ostracoda Eucyprinotus rostratus (Sywula) 5 4

Heterocypris spp. 0 36

Ilyocypris spp. 5 31

Potamocypris arcuata (Sars) 4 10

Tonnacypris lutaria (Koch) 2 8

Figure 1. Relationships between permanence and species richness in pools with (black) and without (white) Salamandra larvae: (a)

cladoceran species richness; (b) ostracod species richness. Regression lines are for data from all 52 pools.

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water depth (p ¼ 0.45) or sediment depth(p ¼ 0.78), was significantly related with speciesrichness, explaining 56% of the variance (Table 2,Fig. 1a). When excluding pools containing Sal-amandra, water depth (p ¼ 0.0026) and perma-nence (p ¼ 0.0062) but not surface area (p ¼ 0.59)or sediment depth (p ¼ 1.00), were significantlyrelated with species richness, together explaining60% of the variance (Table 2).

Ostracoda. Five taxa were identified (Table 1).Both Heterocypris and Ilyocypris spp. likely com-prise more than one species but were not dis-criminated to the species level. With all poolsconsidered, pool permanence (positive relation-ship, p < 0.0001), water depth (negative relation-ship, p ¼ 0.0014) and sediment depth (positiverelationship, p ¼ 0.0002), but not surface area

(p ¼ 0.076), were significantly related with speciesrichness, together explaining 60% of the variance(Table 3, Fig. 1b). Excluding pools containingSalamandra produced similar results (Table 3).

Discussion

Due to accelerated human development, tempo-rary pool habitats are disappearing at an alarmingrate worldwide (Williams, 2002) and in Israel inparticular. While temporary pools often supporthigh levels of crustacean biodiversity (Williams,2002), much remains unknown regarding biodi-versity of these habitats (King et al., 1996). Iden-tification of crustacean species in temporary poolsare sparse in Israel, particularly in mountainous

Table 3. Multiple linear regression models of factors explaining among-pool variance in ostracod species richness

Pools Model R2 Predictor variable Slope SS F p

Including 0.60 Surface area* 2.27 3.29 0.076

Salamandra Water depth )0.05 7.97 11.59 0.0014

Pools Permanence 0.03 30.03 43.66 <0.0001

Sediment depth 0.07 10.87 15.81 0.0002

Excluding 0.63 Surface area* 1.14 2.25 0.14

Salamandra Water depth )0.07 4.99 7.76 0.008

Pools Permanence 0.03 24.71 38.44 <0.0001

Sediment depth 0.07 9.86 15.34 0.0003

Analyses were conducted separately for all pools (n = 52) and only for pools that did not contain larvae of the urodele predator

Salamandra salamandra (n = 47). The R2 values are for models including only the statistically significant (p < 0.05) variables in each

group of pools.

*Natural log-transformed.

Table 2. Multiple linear regression models of factors explaining among-pool variance in cladoceran species richness

Pools Model R2 Predictor variable Slope SS F p

Including 0.48 Surface area* 0.0003 0.0003 0.99

Salamandra Water depth 0.69 0.57 0.45

Pools Permanence 0.03 23.43 19.34 <0.0001

Sediment depth 0.10 0.08 0.78

Excluding 0.60 Surface area* 0.29 0.30 0.59

Salamandra Water depth 0.09 9.84 10.25 0.0026

Pools Permanence 0.02 8.00 8.33 0.0062

Sediment depth 0.00 0.00 1.00

Analyses were conducted separately for all pools (n = 52) and only for pools that did not contain larvae of the urodele predator

Salamandra salamandra (n = 47). The R2 values are for models including only the statistically significant (p < 0.05) variables in each

group of pools.

*Natural log-transformed.

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regions of the Galilee (Bromley, 1993). Thus, thedocumentation of crustaceans from a large num-ber of small to medium-sized temporary pools inthe Lower Galilee represents a relatively uniqueaddition to our knowledge of freshwater poolbiodiversity.

Three of six cladocerans, Daphnia similis,Macrothrix hirsuticornis and Pleuroxus leto-urneuxi, and one of five ostracod taxa, Hetero-cypris spp., were not found in any of the poolscontaining Salamandra. The absence of Daphnia inSalamandra pools is not surprising; previousstudies show that Daphnia (Eitam et al., unpub-lished) and other large cladocerans (Blausteinet al., 1996) are highly vulnerable to predation bythis urodele. The possibility that Macrothrix,Pleuroxus and Heterocypris may also be excludedby Salamandra should be confirmed with con-trolled experiments.

Many studies suggest that pool permanence isone of the most important factors affecting com-munity structure in temporary pools (e.g., Holland& Jenkins, 1998; Bilton et al., 2001; Eason &Fauth 2001; Therriault & Kolasa, 2001). In thecurrent study, permanence was an important pre-dictor of species richness of both cladocerans andostracods, while surface area was not a statisticallysignificant factor in any of our analyses.

Sediment depth was also a significant predictorof ostracod species richness. This may be related tothe ability of some adult ostracods to go intotorpor in the sediment and resume activity shortlyafter inundation (Delorme & Donald, 1969). Theeffects of water depth on species richness are lessclear: the negative relationship for ostracods ispuzzling. A positive relationship between cladoc-eran richness and water depth occurred whenSalamandra pools were excluded, but not whenthey were included. Because Salamandra may re-duce species richness (Blaustein et al., 1996) andbecause they are found in the larger pools, waterdepth and Salamandra are likely confoundingvariables.

In contrast with the overall importance of poolpermanence for two orders of crustaceans, for thesame data set, turbellarian species richness wassignificantly related with surface area, but not withpermanence (Eitam et al., in press). This suggests afundamental difference between crustaceans andturbellarians in their natural history characteris-

tics. Eitam et al. (in press) suggested that theimportance of surface area for turbellarians maybe related to their propensity for microhabitatspecialization; such specialization is apparentlyless prevalent among crustaceans (Rundle &Ormerod, 1991). Conversely, the importance ofpermanence for both cladocerans and ostracodssupports the hypothesis that extinction due to pooldrying is a major driving force behind the struc-turing of microcrustacean communities in tempo-rary pools (Rundle et al., 2002).

Acknowledgements

We thank Moshe Kiflawi for field assistance andReuven Ortal for fruitful discussion. This studywas supported by a Vataat Postdoctoral Fellow-ship awarded to A. Eitam, and US-Israel Bina-tional Science Foundation grant 98-390 awardedto L. Blaustein and M. Mangel.

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