Sacrificial males: the potential role of copulation and predation in contributing to copepod sex‐skewed ratios

Abstract

Predation is thought to play a selective role in the emergence of behavioural traits in prey. Differences in behaviour between prey demographics may, therefore, be driven by predation with select components of the population being less vulnerable to predators. While under controlled conditions prey demography has been shown to have consequences for predation success, investigations linking these implications to natural prey population demographics are scarce. Here we assess predator–prey dynamics between notonectid predators (backswimmers) and Lovenula raynerae (Copepoda), key faunal groups in temperate ephemeral pond ecosystems. Using a combination of field and experimental approaches we test for the development and mechanism of predation‐induced sex‐skewed ratios. A natural population of L. raynerae was tracked over time in relation to their predator (notonectid) and prey (Cladocera) numbers. In the laboratory, L. raynerae sex ratios were also assessed over time but in the absence of predation pressure. Predation success and prey performance experiments evaluating differences between L. raynerae male, female, gravid female and copulating pairs exposed to notonectid predation were then examined. Under natural conditions, a female dominated copepod population developed over time and was correlated to predation pressure, while under predator‐free conditions non sex‐skewed prey population demographics persisted. Predator–prey laboratory trials showed no difference in vulnerability and escape performance for male, female and gravid female copepods, but pairs in copula were significantly more vulnerable to predation. This vulnerability was not shared by both sexes, with only female copepods ultimately escaping from successful predation on a mating pair. These results suggest that contact periods during copula may contribute to the development of sex‐skewed copepod ratios over time in ecosystems dominated by hexapod predators. This is discussed within the context of vertebrate and invertebrate predation and how these dissimilar types of predation are likely to have acted as selective pressures for copepod mating systems.

Lack of prey switching and strong preference for mosquito prey by a temporary pond specialist predator

“…Also, as larval mosquito prey proportions increased, positive selectivity for this prey type intensified, while there was very little low‐density refuge for the mosquito. Importantly, these prey selectivity patterns were largely consistent across predator sexes, with sex ratios previously shown to differ temporally and alter interaction strengths in temporary ponds (Wasserman et al ., ; Cuthbert et al ., ). Given the documented development of sex‐skewed demographics in favour of female copepods in these systems (Wasserman et al ., ), similarities in prey preferences may facilitate sustained top‐down pressure on larval mosquitoes irrespective of sex demographics over the hydroperiod.…”

“…Importantly, these prey selectivity patterns were largely consistent across predator sexes, with sex ratios previously shown to differ temporally and alter interaction strengths in temporary ponds (Wasserman et al ., ; Cuthbert et al ., ). Given the documented development of sex‐skewed demographics in favour of female copepods in these systems (Wasserman et al ., ), similarities in prey preferences may facilitate sustained top‐down pressure on larval mosquitoes irrespective of sex demographics over the hydroperiod. Indeed, predatory paradiaptomid copepods have recently been identified as important natural enemies for mosquitoes that vector pathogens and parasites (Cuthbert et al ., 2018b).…”

“…Ephemeral aquatic ecosystems are characterised by atypical trophic structuring, with community dynamics contingent on patterns of internal recruitment (i.e. resting egg hatching) and external recruitment via colonisation from other environments during wet phases (Brendonck & De Meester, 2003;Wasserman et al, 2016Wasserman et al, , 2018. In these habitats, top-down pressure is often driven by predaceous crustaceans which hatch from egg banks at the start of the wet phase (Wasserman et al, 2016).…”

Combined impacts of warming and salinisation on trophic interactions and mortality of a specialist ephemeral wetland predator

“…Moreover, in other study systems, the effects of salinisation have synergised with additional factors, such as higher order predation, with implications for the persistence of lower trophic groups (Hintz & Relyea, ; Hintz et al., ). Given that higher‐order predation in ephemeral wetlands is often imported via aerial colonisation (Wasserman, Weston, et al., ), the effects of salinity increases on predatory impacts from external colonists such as notonectids requires assessment. Indeed, if these predatory colonists are more tolerant to salinisation than resident zooplankters, predatory impacts and cascade effects on prey groups could be intensified.…”

“…Calanoid copepods are often numerically dominant in ephemeral wetlands during the early and middle stages of the hydroperiod and can occupy top trophic levels (Dalu, Wasserman, Froneman, & Weyl, ; Wasserman, Weston, et al., ). Such zooplankton groups are internally recruited from dormant eggs within egg banks in the substrate, which hatch following rainfall events which initiate the hydroperiod (Wasserman, Alexander, Barrios‐O'Neill, et al., ).…”