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Can Large Branchiopods Shape Microcrustacean Communities in Mediterranean Temporary Wetlands?

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Can Large Branchiopods Shape Microcrustacean Communities in Mediterranean Temporary Wetlands? CSIRO PUBLISHING Marine and Freshwater Research, 2011, 62, 46–53 www.publish.csiro.au/journals/mfr Can large branchiopods shape microcrustacean communities in Mediterranean temporary wetlands? Aline WaterkeynA,B,D, Patrick GrillasB, Maria Anton-PardoC, Bram VanschoenwinkelA and Luc BrendonckA ALaboratory of Aquatic Ecology and Evolutionary Biology, Katholieke Universiteit Leuven, Charles Deberiotstraat 32, 3000 Leuven, Belgium. BTour du Valat, Research Center for Mediterranean Wetlands, Le Sambuc, 13200 Arles, France. CDepartment of Microbiology and Ecology, University of Valencia, Dr. Moliner 50, 46100 Burjassot, Valencia, Spain. DCorresponding author. Email: [email protected] Abstract. It was recently suggested that large branchiopods may play a keystone role in temporary aquatic habitats. Using a microcosm experiment manipulating microcrustacean communities of Mediterranean temporary wetlands (Camargue, Southern France), we tested the following hypotheses: (i) large branchiopods (the notostracan Triops cancriformis and the anostracan Chirocephalus diaphanus) can limit microcrustacean densities through both competition and predation; (ii) notostracans create high suspended-matter concentrations through bioturbation, which can negatively impact microcrustaceans; and (iii) the outcome of these biotic interactions is more detrimental at high salinities. We found a strong predatory impact of T. cancriformis on active microcrustacean populations, but also on dormant populations through the consumption of resting eggs. They also preyed on anostracans and their conspecifics and can indirectly have a negative effect on microcrustaceans through bioturbation, probably by impeding filtering capacities. The presence of C. diaphanus also limited most microcrustacean groups, probably through competition and/or predation. We did not find a significant effect of the tested salinity range (0.5–2.5 g LÀ1) on the biotic interactions. Our study shows that large branchiopods can shape microcrustacean communities under a wide range of environmental conditions and confirms their potential for a keystone role, especially one of notostracans as top predators. Additional keywords: Anostraca, bioturbation, interference competition, predation, Triops. Introduction of competition in structuring of zooplankton communities Predation and competition are recognised as strong community- (Bengtsson 1993; Jocque´ et al. 2010). structuring forces (Sih et al. 1985), often mediated by keystone Large branchiopods have long been recognised as being a species. The presence or absence of such keystone species distinctive group of temporary waters. Their role as a keystone may therefore severely alter the characteristics of a community group, shaping invertebrate communities in temporary wetlands, (Power et al. 1996). In permanent aquatic environments, this has only been suggested more recently (Yee et al. 2005; regulatory role is often attributed to fish (Zaret 1980). As a result Jocque´ et al. 2010; Waterkeyn et al. 2010). The predatory role of periodic drying, fish are usually excluded from temporary of notostracans (tadpole shrimps) has long been under- aquatic habitats. This does not mean, however, that these estimated, mostly because of controversy about their diet habitats are ‘enemy free’ (Brendonck et al. 2002). On the con- (Dumont and Negrea 2002). Additionally, their role in modify- trary, they often exhibit high predation pressures (Boix et al. ing wetland environments by disturbing sediments leading 2006). A whole range of predators have been suggested to to increased turbidity of the water column has largely been play an important role in temporary freshwater systems, such neglected. Similarly, the influence of anostracans (fairy as turbellarians, notonectids, diving beetles, dragonfly larvae, shrimps) on zooplankton in temporary wetlands, through Chaoborus spp. larvae, notostracans, and amphibian larvae competition (both resource and interference competition) and (e.g. Brendonck et al. 2002; De Roeck et al. 2005; Boix et al. predation, remains largely unknown (Sa´nchez and Angeler 2006). By contrast, competition has often been underestimated 2007; Jocque´ et al. 2010). The high degree of environmental in temporary aquatic systems, mostly because frequent dis- variability among wetlands often compromises the detect- turbance as a result of drying was thought to truncate competi- ion of such structuring roles (Sa´nchez and Angeler 2007). tive interactions. However, the limited research on competitive Therefore, experimental studies based on manipulative designs interactions in temporary waters has confirmed the importance are more appropriate to test for the keystone role of large Ó CSIRO 2011 10.1071/MF10147 1323-1650/11/010046 Large branchiopods shape microcrustacean communities Marine and Freshwater Research 47 branchiopods in temporary wetland food webs (Sa´nchez and 2-L sample was filtered through a 64-mm net and preserved in Angeler 2007). 70% ethanol to serve as reference for the starting condition, thus Water quality plays an important role shaping communities accounting for variation in microcrustacean densities during the in temporary wetlands, directly by selecting for tolerant species, inoculation process. Afterwards, for each of the large branchio- and indirectly by influencing biotic interactions. Salinity is one pod treatments, ten adult T. cancriformis (average Æ s.d. size: of the factors that play an important role in determining diversity 23 Æ 9 mm from head to base of furca) and/or ten adult and community structure in wetlands (Brendonck and Williams C. diaphanus (average Æ s.d. size: 32 Æ 8 mm from head to base 2000; Brock et al. 2005; Brucet et al. 2010), particularly in of furca) were added (one individual per L). The aquaria were the Mediterranean coastal temporary wetlands of the Camargue given an inoculum of phytoplankton from the outdoor meso- (Waterkeyn et al. 2008, 2009). Coping with osmotic stress can cosms (from which the experimental microcrustacean com- trade off with other traits, such as the performance of organisms munity was taken), combined with a daily addition of 2 mL of in their interactions with other species, and can therefore change Scenedesmus obliquus (2 Â 108 cells mLÀ1) and 2 mL of yeast the outcome of competition (e.g. Sarma et al. 2002) or predation (1 g of dried baker’s yeast in 100 mL of distilled water) during rates (e.g. Chandramohan et al. 2008). However, the impact the first four days. Afterwards, feeding was stopped to ensure of salinity on the structuring role of large branchiopods on limiting food conditions enabling the detection of competition. the microcrustacean communities of Mediterranean temporary During the experiment, temperature was kept between 138C wetlands remains unknown. Using a microcosm experiment, and 168C and lights were turned on between 0830 hours and we tested the following hypotheses: (1) large branchiopods can 1830 hours. The chosen treatments reflect natural conditions. effectively limit microcrustacean densities through both com- The salinities reflect the natural gradient in which microcrusta- petition and predation; (2) notostracans create high suspended ceans co-occur with large branchiopods (the latter being less matter concentrations through bioturbation, which can in turn tolerant), whereas their densities reflect rather high, but negatively impact microcrustaceans; and (3) the outcome of natural densities found in some Camargue ponds in the field these biotic interactions is more detrimental at high salinities. (A. Waterkeyn, unpubl. data; Pont and Vaquer 1986). The aquaria were sampled 1, 4, 8, and 11 days after the start of the exposure to large branchiopods, except for the T. cancri- Materials and methods formis and sediment treatments, which were stopped after Biotic interactions across a salinity gradient 8 days because by that time most of the microcrustaceans This experiment was carried out in December 2008 in the were already eaten in the T. cancriformis treatments. Salinity Research Centre of the Tour du Valat (438300N, 48400E). At (g LÀ1) was measured with a WTW conductivity meter three different salinities (0.5 g LÀ1, 1.0 g LÀ1, and 2.5 g LÀ1), 330i (Wissenschaftlich-Technische Werksta¨tten, Welheim, microcrustacean communities were exposed in 10-L aquaria Germany). On the first three sampling events, a 1-L microcrus- to six different treatments: (a) control, (b) Chirocephalus tacean sample was taken after mixing the water to homogenize diaphanus, (c) Triops cancriformis, (d) sediment, (e) T. can- the community. The sample was filtered through a 64-mm net and criformis þ sediment, and (f) T. cancriformis þ C. diaphanus þ preserved in 70% ethanol. During the last sampling event, the sediment. Each treatment was replicated four times for a total of whole content of the aquaria was filtered through a 64-mm net. 72 aquaria. The experiment lasted for 11 days. The filtered water was used to measure total suspended solids The aquaria for treatments (d), (e), and (f) were inoculated (TSS in mg LÀ1) using a portable Hach spectrophotometer with a 0.5-cm layer of sterilised sediment collected from a DR2800 (Hach Co., Loveland, CO, USA) and chlorophyll a freshwater temporary wetland on the estate of Tour du Valat. concentration using a methanol extraction method (Talling and The sediment was put in a drying oven at 2008C for three days Driver 1963). All microcrustacean samples were processed to kill any viable resting stages. The organisms used
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