Crustacea: Ostracoda) in Three Temporary Ponds
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Hydrobiologia (2009) 636:219–232 DOI 10.1007/s10750-009-9952-0 PRIMARY RESEARCH PAPER Dynamics of sexual and parthenogenetic populations of Eucypris virens (Crustacea: Ostracoda) in three temporary ponds Maria Joa˜o Fernandes Martins • Jochen Vandekerkhove • Francesc Mezquita • Olivier Schmit • Juan Rueda • Giampaolo Rossetti • Tadeusz Namiotko Received: 20 May 2009 / Revised: 13 September 2009 / Accepted: 15 September 2009 / Published online: 19 October 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Eucypris virens is a freshwater ostracod This renders the species a potentially valuable in which both sexual reproduction and partheno- model organism to study the ‘queen of evolutionary genesis occur. Sympatric coexistence of both problems’, i.e. why sex is so successful despite its reproductive modes is known in zones of overlap. costs (paradox of sex). In order to maximally exploit this potential, a broad knowledge of the species’ ecology is essential, including an under- standing of its life history and population dynam- ics. Here, the phenology of the species was Electronic supplementary material The online version of followed in three temporary ponds through monthly this article (doi:10.1007/s10750-009-9952-0) contains (Spain) or fortnightly (Poland) samplings, through- supplementary material, which is available to authorized users. out an inundation period. This study confirms the wide ecological tolerances of E. virens. Although Handling editor: K. Martens the species is generally assumed to be univoltine, M. J. F. Martins (&) Á J. Vandekerkhove Á T. Namiotko two hatching periods were observed in the Spanish Laboratory of Limnozoology, Department of Genetics, sites. Biotic interactions, especially predation, University of Gdan´sk, Kładki 24, 80-822 Gdan´sk, Poland appear to be the important determinants of popu- e-mail: [email protected] lation dynamics in long-hydroperiod sites. Abiotic M. J. F. Martins Á J. Vandekerkhove Á O. Schmit Á conditions may influence population dynamics G. Rossetti through their impact on egg hatching. In the site Department of Environmental Sciences, University with male presence, the initially female-biased sex of Parma, Viale G. P. Usberti 33/A, 43100 Parma, Italy ratio evolved towards a balanced sex ratio through M. J. F. Martins the season. No consistent differences in limb EAWAG Swiss Federal Institute of Aquatic Sciences morphology were observed between females orig- and Technology, U¨ berlandstrasse 133, 8600 Du¨bendorf, inating from the three study sites. On the other Switzerland hand, valve size of adult females varied among M. J. F. Martins sites, possibly influenced by local environmental Institute of Integrative Biology (IBZ), ETH-Zu¨rich, conditions (mainly salinity and pH) as well as the Universita¨tsstrasse 16, 8092 Zu¨rich, Switzerland expected genetic diversity. J. Vandekerkhove Á F. Mezquita Á O. Schmit Á J. Rueda Department of Microbiology and Ecology, University of Keywords Ostracoda Á Phenology Á Vale`ncia, Av. Doctor Moliner 50, 46100 Burjassot, Spain Temporary ponds Á Ecological preferences 123 220 Hydrobiologia (2009) 636:219–232 Introduction specific adaptations, such as the capacity to produce resting eggs, rather than features associated with the Ostracods are small bivalve crustaceans abundant in mode of reproduction determine the population nearly all freshwater and marine habitats, but found dynamics of freshwater ostracods. also in interstitial and semi-terrestrial environments We monitored population dynamics in three tem- (Horne et al., 2002). The group exhibits a high porary ponds of sexual and/or asexual lineages of the taxonomic diversity (ca. 10000–15000 extant species; freshwater ostracod Eucypris virens (Jurine 1820). Kempf, 1980–2006, 1986–2008), an extensive fossil High clonal diversity within sites and regions (Scho¨n record (Horne & Martens, 1998; Martens et al., 2008) et al., 2000; Rossi et al., 2008) and substantial and an extraordinary diversity of life history strate- morphological variability (Te´tart, 1982; Martens gies (Chaplin et al., 1994; Butlin et al., 1998; Geiger, et al., 1992; Baltana´s et al., 2000; Baltana´s, 2002) 1998). This in combination with their relatively short have been reported in E. virens. Recent molecular generation time and the high frequency of transitions analyses show evidence of multiple origins of from sexuality to asexuality observed in certain asexuality from genetically distant sexual lineages. genera (Chaplin et al., 1994; Butlin et al., 1998) These sexual populations are characterized by deep denotes the Ostracoda as valuable model organisms phylogenetically divergence, enough to be considered to study the fundamental evolutionary questions. as a cryptic species complex (Bode et al., in press). Reproduction in freshwater ostracods displays a Most ponds have been colonized repeatedly, as variety of forms: the ‘ancient asexuals’ with unknown assessed by the presence of multiple more or less sexual relatives, genera and/or species with related parthenogenetic lineages within one pond co-occurring parthenogenetic lineages (asexuals) (Adolfsson et al., submitted). Prior to these findings, and sexual lineages (sexuals) and obligatory sexual E. virens was regarded as a single species on the populations (Chaplin et al., 1994; Judson & Normark, basis of morphology. Laboratory studies suggest that 1996; Butlin et al., 1998). Evolutionary questions coexistence of E. virens lineages may be enhanced by have so far been tackled mainly by studying the differences in hatching phenologies and developmen- (palaeo)geography and the phylogeny of ostracods tal rates (Otero et al., 1998; Martins et al., 2008), but with different modes of reproduction (Griffiths & so far field evidence is lacking. We followed the Horne, 1998; Horne et al., 1998; Scho¨n et al., 2000). dynamics of two parthenogenetic populations and one Chaplin et al. (1994) found that asexual ostracod taxa bisexual population (coexistence of sexually and are relatively more successful in freshwater habitats asexually reproducing lineages) throughout one inun- of recent origin, whereas sexuals are commonly dation period. The importance of environment and found in marine environments and post-glacial lakes. mode of reproduction for the short-term dynamics of This points to the supreme colonization potential of these E. virens populations was assessed in a qual- asexuals and to their vulnerability to local displace- itative way by linking hatching patterns and changes ment by sexuals in the absence of environmental in the population structure and density with variations change (Bell, 1982). observed in the abiotic and biotic environments. Theory predicts a twofold advantage for asexual populations compared to their sexual relatives, because the latter suffer from the cost of male Materials and methods production (Maynard Smith, 1978). Still, sexual populations persist and compete directly with their Study species asexual relatives, at times even within the same pond (e.g. Scho¨n et al., 2000). A straightforward approach Eucypris virens is a freshwater ostracod species to study the ecological and evolutionary significance complex, traditionally regarded as a morphospecies. of sex is to compare life history traits and population Parthenogenetic populations are present throughout dynamics between sexuals and asexuals. Geiger Europe, North Africa, North America and Asia (1998) conducted a comparative analysis involving (Baltana´s, 1994; Meisch, 2000; Semenova, 2005) life history traits of sexual and asexual freshwater and are also known from Australia (Radke et al., ostracod species. His analysis suggested that species- 2003), New Zealand (Barclay, 1968; Eagar, 1971) 123 Hydrobiologia (2009) 636:219–232 221 and some Sub-Antarctic islands (Te´tart, 1982; Pugh a region where males had been previously recorded et al., 2002). Males are recorded from the circum- [pond Monfragu¨e 4 (MF4), Extremadura, Spain: N Mediterranean area and central Asia only (Meisch, 39°5403900,W6°0304800, 432 m asl]. As such, the 2000). The species is common in temporary ponds, selection of ponds allowed us to uncouple the effects but has been recorded in a wider variety of habitats of climate/latitude and reproductive mode. The (Meisch, 2000), with salinity ranges from 0 to 5% Spanish sites are isolated ponds, located in a natural (Hiller, 1972). It is a thermoeuryplastic species park and along cattle pathways, respectively. The (Nu¨chterlein, 1969) with tolerance for eutrophic Polish site JAB is composed of a temporary pond waters (Mezquita et al., 2001; Gifre et al., 2002). connected to a few disused ditches in a former The few published population density records indi- agricultural land bordering a heavily used road on the cate relatively low population densities (compared to outskirts of Gdan´sk city limits. other ostracod species) ranging from 13 to Sampling was carried out from the first (ice free) 200 ind. m-2 (Baltana´s, 1994). The growing and water presence until the site was recorded as dry (at reproductive periods are winter and spring (Alm, the end of the rainy season). Ponds were visited 1915; Baltana´s, 1994; Mezquita et al., 1999) but more monthly (Spain) or fortnightly (Poland), at approxi- eurychronic populations, present throughout the year, mately the same time of the day (late morning), to may also occur (Altinsac¸li, 2001). Although the avoid major