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Aquat Ecol (2020) 54:181–191 https://doi.org/10.1007/s10452-019-09735-y(0123456789().,-volV)(0123456789().,-volV) Assessing multiple predator, diurnal and search area effects on predatory impacts by ephemeral wetland specialist copepods . . . . Ross N. Cuthbert Tatenda Dalu Ryan J. Wasserman Cristia ´ n J. Monaco . . Amanda Callaghan Olaf L. F. Weyl Jaimie T. A. Dick Received: 16 August 2019 / Accepted: 22 November 2019 / Published online: 29 November 2019 The Author(s) 2019 Abstract Predator–prey interaction strengths can be of P. lamellatus under circadian and surface area highly context-dependent. In particular, multiple variations. Then, we assess the influence of a co- predator effects (MPEs), variations in predator sex occurring heterospecific predatory copepod, Lovenula and physical habitat characteristics may affect prey raynerae, on total predation rates. We demonstrate consumption rates and thus the persistence of lower MPEs on consumption, with antagonism between trophic groups. Ephemeral wetlands are transient conspecific P. lamellatus predatory units evident, ecosystems in which predatory copepods can be irrespective of prey density. Furthermore, we show numerically dominant. We examine the interaction differences between sexes in interaction strengths, strengths of a specialist copepod Paradiaptomus with female P. lamellatus significantly more voracious lamellatus towards mosquito prey in the presence of than males, irrespective of time of day and experi- conspecifics using a functional response approach. mental arena surface area. Predation rates by P. Further, we examine sex variability in predation rates lamellatus were significantly lower than the heterospecific calanoid copepod L. raynerae, whilst heterospecific copepod groups exhibited the greatest Handling Editor: Telesphore Sime-Ngando. R. N. Cuthbert (&) J. T. A. Dick T. Dalu R. J. Wasserman Institute for Global Food Security, School of Biological South African Institute for Aquatic Biodiversity (SAIAB), Sciences, Queen’s University Belfast, Makhanda 6140, South Africa Belfast BT9 5DL, Northern Ireland, UK e-mail: rossnoelcuthbert@gmail.com R. J. Wasserman Department of Biological Sciences and Biotechnology, R. N. Cuthbert O. L. F. Weyl Botswana International University of Science and DSI/NRF Research Chair in Inland Fisheries and Technology, Palapye, Botswana Freshwater Ecology, South African Institute for Aquatic Biodiversity (SAIAB), Makhanda 6140, South Africa C. J. Monaco School of Biological Sciences, University of Adelaide, R. N. Cuthbert A. Callaghan Adelaide 5005, Australia Ecology and Evolutionary Biology, School of Biological Sciences, University of Reading, Harborne Building, C. J. Monaco Reading RG6 6AS, England, UK Department of Zoology and Entomology, Rhodes University, Makhanda 6140, South Africa T. Dalu Ecology and Resource Management, University of Venda, Thohoyandou, Limpopo, South Africa 123 182 Aquat Ecol (2020) 54:181–191 predatory impact. Our results provide insights into the derivation of functional responses (FRs) (Solomon predation dynamics by specialist copepods, wherein 1949; Holling 1959). Functional responses quantify species density, diversity and sex affect interaction how resource intake changes with variations in strengths. In turn, this may influence population-level resource densities, and FR form and magnitude may persistence of lower trophic groups under shifting influence stability of lower trophic groups (Murdoch copepod predator composition. and Oaten 1975; Dick et al. 2014). Three common FR types have been categorised: the linear Type I, Keywords Paradiaptomus lamellatus Lovenula inversely density-dependent Type II and sigmoidal raynerae Calanoid copepod Multiple predator Type III (Hassell 1978). As Type II FRs are charac- effects Functional response terised by high proportional consumption rates at low densities, they may be particularly destabilising for resources, whilst Type III FRs are thought to be more stabilising through low-density refuge effects (Mur- Introduction doch and Oaten 1975). In Type II FRs, the attack rate parameter controls the initial slope of the curve whilst Predation is a fundamental biotic process which the handling time parameter controls the height of the profoundly affects ecosystem structure, stability and FR asymptote (i.e. maximum feeding rate). Empirical functioning (Brooks and Dodson 1965; Paine 1980; studies show that greater magnitude FRs (i.e. high Wasserman and Froneman 2013). Models applied to attack rates, low handling times, high maximum consumer–resource systems classically assumed func- feeding rates) produce higher ecological impact on tional equivalence of predators within populations prey populations (Bollache et al. 2008; Dick et al. (Volterra 1928; Lotka 1956; Rosenzweig and 2013; Taylor and Dunn 2018). Importantly, FRs offer MacArthur 1963), limiting comprehensive quantifica- a framework (Dick et al. 2014, 2017; Cuthbert et al. tions of interaction strengths under shifting biotic 2018a, b) to compare interaction strengths between contexts (e.g. predator sex or ontogenic stage). Yet, different consumers whilst deciphering context depen- more recent work has recognised the need to account dencies, such as multiple predator effects (MPEs; see for individual consumer variability within populations Sentis and Boukal 2018) and environmental change (e.g. Hassell 1978; Ebenman and Persson 1988; (e.g. Wasserman et al. 2016b). Murdoch et al. 2003; Thorp et al. 2018). Moreover, Ephemeral wetlands provide excellent model sys- as the effects of environmental change on species tems for testing ecological theory (De Meester et al. interactions are challenging to predict with certainty 2005), and in arid regions, these systems are partic- (Daufresne et al. 2009; Gilbert et al. 2014), quantify- ularly vulnerable to environmental change (see Dalu ing context dependencies for predation is imperative et al. 2017a). Their impermanency elicits fundamen- for inferences of trophic interactions in changing tally different food web structures to other aquatic environments (see Wasserman et al. 2016b). systems due to temporal variability in internal and Given that most ecological communities include external recruitment trends. In the early-mid stages of multiple predators which share common resources, hydroperiod, ephemeral ponds are dominated by predator–predator exchanges can profoundly alter internal recruits which hatch from dormant eggs in interaction strengths (Soluk 1993; Sih et al. 1998; the sediment (Greig et al. 2013; O’Neill et al. 2015). Bolker et al. 2003; Wasserman et al. 2016c). An Therefore, for much of the hydroperiod, drought- increasing body of work has examined the implica- adapted zooplankton groups such as calanoid cope- tions of multiple predators for prey risk (Schmitz pods are most prevalent within the species assemblage 2007; Vance-Chalcraft et al. 2007; Griffin et al. 2013), in many ephemeral wetlands (e.g. Wasserman et al. and understanding combined predator interactions 2018). However, despite their high prevalence and provides important insights for the implications of wide distribution (Dussart and Defaye 2001), the predator species loss for ecosystem function (Duffy trophic interaction strengths between copepods and et al. 2007). One classical ecological approach to their resources and their susceptibility to environmen- quantify consumer–resource (e.g. predator–prey) tal change remain poorly understood in biodiverse interactions under context dependencies is through ephemeral systems (though see Wasserman et al. 123 Aquat Ecol (2020) 54:181–191 183 2016a; Cuthbert et al. 2018c, d). Sex ratios are known research has found additive interactions among other to differ over the course of the hydroperiod in copepod species (Cuthbert et al. 2019b). We subse- ephemeral wetland specialist copepods due to selec- quently examine how predation rates vary between tive processes such as predation (Wasserman et al. sexes of this species and test whether circadian or 2018). In turn, this may intensify impacts by predatory surface area variations further influence consumption. zooplankton on lower trophic groups if sex ratios Copepod feeding rates have been shown previously to become biased, given that females can have higher be highest in gravid females (Laybourn-Parry et al. predatory impacts (Cuthbert et al. 2019a). However, 1988; Cuthbert et al. 2019a), and prey detection is these effects may also be dependent on the overall known to be reliant on hydromechanical cues (Hwang abundances of zooplankters, as offtake rates (product and Strickler 2001). Container dimensions have also of functional and numerical responses) under low been shown to influence consumer–resource interac- copepod abundances could be reduced. In addition, tion strength quantifications (Uiterwaal and DeLong physical habitat characteristics may alter interactions 2018). Lastly, we examine P. lamellatus feeding rates between predatory copepods and their prey. Owing to in the presence of the heterospecific calanoid copepod periodic wetting and drying cycles, the surface area of Lovenula raynerae Sua ´rez-Morales, Wasserman, Dalu ephemeral wetlands is highly dynamic spatiotempo- 2015 (Suarez-Morales et al. 2015), with which P. rally, and reductions in surface area may increase lamellatus commonly coexists. We thus seek to provide information into how predator–prey interac- predator encounter rates with prey. Indeed, in an experimental context, search area has been shown to tion strengths in ephemeral aquatic food webs are substantially alter the nature of consumer–resource modulated by emergent biotic and abiotic contexts. dynamics (Yas ¸ ar and Ozger 2005; Uiterwaal and We thus predict that: (1) conspecifics of P. lamellatus DeLong 2018; Dalal et al. 2019). Day/night cycles will interact independently and thus FRs will combine may also modify predatory impacts of species which additively; (2) consumption rates will be higher in rely on visual cues (e.g. Townsend and Risebrow females than males, reduced under higher surface 1982); however, temporary pond specialist copepods areas and unaffected by circadian variations and; (3) have been suggested to be more reliant on hydrome- overall feeding rates will be heightened in the presence chanical cues for prey detection (Cuthbert et al. of an additional heterospecific predatory copepod, 2018d). Nevertheless, little is known about how these given their tendency to occupy different parts of the environmental factors interact to influence ephemeral water column. wetland food webs, where copepods can be top predators. Paradiaptomus lamellatus Sars 1895 is a predatory Materials and methods calanoid copepod which hatches from dormant eggs in the sediment within arid ephemeral ecosystems (see Experimental organisms Wasserman et al. 2016a; Dalu et al. 2017b). This species has the potential to influence trophic dynamics Adult P. lamellatus (female: 4.23 ± 0.07 mm; male: in ephemeral ponds and particularly in the early-mid 3.85 ± 0.08 mm) and L. raynerae (female: stages of hydroperiod when such copepod groups 4.77 ± 0.14 mm; male: 4.40 ± 0.10 mm) were sam- dominate higher trophic levels (Brendonck and De pled from an ephemeral pond in Makhanda (Graham- 0 00 Meester 2003; Dalu et al. 2017b). Given the high stown), Eastern Cape, South Africa (3316 47.8 S, 0 00 densities of predators that hatch from the sediment in 2635 39.8 E) during the 2017–2018 austral summer these systems, predator–predator con/heterospecific by towing a 64-lm zooplankton net through the upper interactions, alongside physical habitat characteris- portion of the water column. Copepods were trans- tics, may have marked effects on interaction strengths ported in source water to a controlled environment towards focal prey species. Therefore, the present (CE) room at Rhodes University, Makhanda, main- study examines environmental context dependencies tained at 25 ± 2 C and under a 14:10 light/dark of consumer impact. Firstly, we use comparative FRs photoperiod regime. Copepods were housed in 25 L to quantify conspecific MPEs of P. lamellatus towards aquaria and starved in strained (20-lm filter) source surface-dwelling larval mosquito prey. The previous water. The prey, larvae of the Culex pipiens mosquito 123 184 Aquat Ecol (2020) 54:181–191 complex, were cultured in the CE room using egg rafts The Lambert W function was used to fit Eq. 1 (Bolker collected from artificial container-style habitats within 2008). A nonparametric bootstrapping procedure the Rhodes University campus on a diet of crushed (n = 2000) was followed to generate 95% confidence rabbit food pellets ad libitum (Agricol, Port intervals (CIs) around FR curves based on the attack Elizabeth). rate and handling time parameters. This process allows density-dependent visual differences in FRs to be Experiment 1: Functional responses (FRs) ascribed on the basis of CI con/divergence (e.g. and conspecific multiple predator effects (MPEs) Wasserman et al. 2016b). Using the attack rate and handling time parameter A factorial design was implemented with respect to estimates from single predator treatments (Eq. 1), we ‘predator group’ (2 levels) and ‘prey supply’ (5 levels) fit a population-dynamic model to predict consump- to decipher FRs and MPEs of single and multiple P. tion by multiple predators, following McCoy et al. lamellatus. Adult male P. lamellatus were supplied (2012) and Sentis and Boukal (2018): with C. pipiens larvae (2.51 ± 0.11 mm) at five dN densities (2, 4, 8, 16 and 32) in arenas of 5.6 cm ¼ fðÞ N P ð2Þ i i dt i¼1 diameter containing 80 mL strained source water following copepod starvation for 48 h. This range of where N is the prey density, P (i =1, 2, …, n) are the prey densities was informed from pilot studies, which population densities of predators i and f (N) is the FR indicated necessary numbers to decipher asymptotic of predator i. The population-dynamic model has been FR magnitudes. Following a 2-h period to allow larval shown to be more robust than other approaches, such prey acclimation within the experimental arenas, P. as the multiplicative risk model, for inferences of lamellatus were introduced either singularly or as a MPEs (Sentis and Boukal 2018). To generate prey conspecific unit comprised of two individuals. Cope- survival predictions (and thus consumption rates), pods were then allowed to feed undisturbed for 10 h initial values of N and P (i =1, 2, …, n) were set at the during light conditions, after which the remaining live experimental prey and predator densities, with prey prey were counted. Four replicates were conducted survival projected over the total experimental dura- within each treatment group, and controls comprised tion. We used a global sensitivity analysis that three replicates at each density in the absence of incorporated confidence intervals from single predator predators. Overall consumption was analysed using FR parameters via a Latin hypercube sampling generalised linear models (GLMs) assuming a Poisson algorithm (Soetaert and Petzoldt 2010). error distribution and log link with respect to the To deduce emergent MPEs, we used consumption ‘predator group’ and ‘prey supply’ treatments, and predictions from the population-dynamic model their interaction. We followed Crawley (2007) for all (Eq. 2) under each prey density (Sentis et al. 2017). models and removed insignificant terms and interac- The predicted interaction strengths were derived as the tions stepwise and performed post hoc tests using simulated proportion of available prey consumed at Tukey’s comparisons (Lenth 2018). each density. Likewise, we calculated experimentally Functional response analyses were undertaken observed interaction strengths for conspecific predator using the frair packages in R v3.4.4 (Pritchard et al. pairs. Given that the predicted interaction strengths 2017; R Core Development Team 2018). We used from the population-dynamic model are in the absence logistic regression to infer FR types, whereby a of non-trophic interactions, whilst experimentally significantly negative first-order term indicates a Type observed interaction strengths include these interac- II response. To account for prey depletion during the tions, we calculated non-trophic interaction strengths experiment, we fit Rogers’ random predator equation by subtracting the predicted estimates from those (Rogers 1972; Juliano 2001): experimentally observed. Thus, a negative non-trophic interaction strength indicates antagonistic MPEs, N ¼ NðÞ 1 expðÞ aNðÞ h T ð1Þ e 0 e whilst positive values indicate synergism. Owing to where N is the number of prey eaten, N is the initial e 0 assumptions of parametric testing being violated, a density of prey, a is the attack constant, h is the Kruskal–Wallis test was used to derive whether the handling time, and T is the total experimental period. 123 Aquat Ecol (2020) 54:181–191 185 strength of non-trophic interactions was affected by (3.33 ± 0.13 mm) in arenas of 5.6 cm diameter initial prey density. containing 25 mL strained source water. Again, prey were allowed to settle for 2 h prior to the addition of Experiment 2: Diurnal predation variabilities predators. Predators were allowed to feed for 18 h, between sexes after which the remaining live prey were counted to quantify numbers killed. We conducted five replicates We conducted a factorial experiment to evaluate the per experimental group, whilst controls consisted of effects of ‘sex’ (2 levels), ‘time’ (2 levels) and ‘surface three replicates in the absence of predatory copepods. area’ (2 levels) on the predation efficacy of P. Generalised linear models (GLMs) assuming a quasi- lamellatus. Adult gravid female and male P. lamella- Poisson error distribution and with a log link were tus were starved for 72 h before being added individ- used to compare consumption rates between predator ually to arenas containing 30 C. pipiens larvae treatments, with Tukey’s comparisons used for mul- (2.42 ± 0.07 mm). The numbers of prey were tiple pairwise tests (Lenth 2018). selected to approximate maximal densities from Experiment 1. After prey had acclimated for 2 h as before, male or female copepods were added individ- Results ually to arenas containing 25 mL strained source water of either 3.5 or 5.6 cm diameter, with trials Experiment 1: Functional responses (FRs) either conducted during day or night conditions. and conspecific multiple predator effects (MPEs) Predatory copepods were allowed to feed for 10 h, after which they were removed and remaining live All control prey survived, indicating that all experi- mosquito prey counted. This duration aligned with the mental deaths were due to copepod predation, which current darkness regime of the CE room (see before). was also witnessed directly. Overall consumption did Five replicates were performed within each experi- not differ between single and multiple P. lamellatus mental group. Controls consisted of a replicate in each predator treatments (v = 0.18, df =1, p = 0.67), yet treatment group in the absence of predators. Gener- increased significantly under greater prey densities alised linear models (GLMs) assuming a quasi-Pois- (v = 25.21, df =4, p \ 0.001). There was no signif- son error distribution with a log link were used to icant ‘predator group 9 prey supply’ interaction analyse consumption with respect to ‘sex’, ‘time’ and (v = 0.80, df =4, p = 0.94). ‘surface area’ and their interactions, as residuals were Type II FRs were inferred under both single and found to be overdispersed. multiple predator treatments, as evidenced by signif- icantly negative first-order terms (Table 1). Confi- Experiment 3: Heterospecific predatory impacts dence intervals overlapped for single and multiple predator treatments, indicating a lack of significant We examined the predatory impacts of P. lamellatus difference in FRs across prey densities (Fig. 1). in the presence of L. raynerae by quantifying preda- Non-trophic interaction strengths were always tion in single (i.e. 1 P. lamellatus or 1 L. raynerae negative (Fig. 2) and were not significantly affected separately) and mixed groups (i.e. 1 of each species in by prey densities (v = 5.57, df =4, p = 0.23). combination). Adult males of L. raynerae and P. Accordingly, antagonistic multiple predator effects lamellatus were starved for 24 h prior to experimen- were evidenced by interacting conspecific P. lamella- tation before being presented to 50 C. pipiens larvae tus irrespective of prey density. Table 1 First-order terms derived from logistic regression of arising from Rogers’ random predatory equation for single and proportional prey consumption as a function of prey density, multiple Paradiaptomus lamellatus feeding on Culex pipiens alongside functional response parameter estimates and p values larvae Treatment First-order term, p Attack rate, p Handling time, p P. lamellatus 9 1 - 0.04, 0.02 0.47, 0.01 0.16, 0.01 P. lamellatus 9 2 - 0.05, 0.001 0.74, 0.04 0.26, \ 0.001 123 186 Aquat Ecol (2020) 54:181–191 prey were killed by female P. lamellatus than by males Pl overall (F = 48.71, p \ 0.001; Fig. 3). There was 1,38 Pl + Pl no significant difference in consumption rates during day or night (F = 0.49, p = 0.49) or between 1,36 different arena surface area treatments (F = 3.62, 1,37 p = 0.07). Further, the higher predation rates dis- played by females were robust to both diurnal and arena surface area variations, with all interaction terms in the model found to be non-significant (all p [ 0.05) (Fig. 3). Experiment 3: Heterospecific predatory impacts All control prey survived in predator-free treatments, 0 8 16 24 32 and thus, experimental deaths were attributed to Prey density (no. individuals) predation by copepods. Predation was significantly affected by the predator treatment group overall Fig. 1 Functional responses of Paradiaptomus lamellatus (Pl) (F = 27.01, p \ 0.001; Fig. 4). Lovenula raynerae 2,12 feeding on Culex pipiens larvae individually and in predatory units of two individuals. Shaded areas are bootstrapped 95% consumed significantly more prey than P. lamellatus confidence intervals individually (z = 3.96, p \ 0.001). There was no significant difference between L. raynerae individual predation and mixed multiple predator predation 0.50 (z = 2.21, p = 0.07), whilst, conversely, predation by single P. lamellatus was significantly lower than that of mixed copepod species groups (z = 4.88, 0.25 p \ 0.001). Nevertheless, predatory impact tended to be highest under heterospecific treatment groups (Fig. 4). 0.00 Discussion −0.25 The integration of biotic context is imperative for robust quantifications of predatory impact within −0.50 ecosystems. In particular, prey species seldom expe- 2 4 8 16 32 rience single predators in nature, and so thus under- Prey density (no. individuals) standing predator–predator interactions is pertinent to decipher overall interaction strengths towards lower Fig. 2 Non-trophic interaction strengths of conspecific pairs of Paradiaptomus lamellatus feeding on Culex pipiens larvae trophic groups (Sih et al. 1998; Schmitz 2007; Vance- across prey densities. The solid black line indicates neutral non- Chalcraft et al. 2007; Griffin et al. 2013; Wasserman trophic interactions, whilst negative values indicate antagonistic et al. 2016c). The present study demonstrates context- interactions. Means are ± SE (n = 4 per experimental group) dependent interaction strengths by copepods in ephemeral wetlands. Specifically, using FRs, we Experiment 2: Diurnal predation variabilities demonstrate that MPEs arising from conspecific between sexes copepod predatory units of P. lamellatus are antago- nistic, resulting in risk reductions for basal prey Control survival in predator-free treatments was compared to predictions in the absence of non-trophic 100%, and so experimental deaths were assumed to interactions. Further, our results display differences in be due to predation by copepods. Significantly more predatory impact based on sex, with female P. Non−trophic interaction strength (± SE) No. prey eaten Aquat Ecol (2020) 54:181–191 187 Day Night Predator sex Female Male 3.5 5.6 3.5 5.6 Arena diameter (cm) Fig. 3 Effect of Paradiaptomus lamellatus sex, diurnal regime and experimental arena surface area on consumption of Culex pipiens larvae. Means are ± SE (n = 5 per experimental group) lamellatus exerting significantly higher predation pressure on lower trophic groups than smaller-sized males. These effects were robust to abiotic effects surrounding diurnal cycling and aquatic surface area, which are both highly variable spatiotemporally in ephemeral aquatic habitats. Moreover, when P. lamel- latus were within a heterospecific predatory unit alongside the controphic calanoid copepod L. rayn- erae, predation pressure tended to be heightened. This suggests that increasing predator diversity may increase ecological impacts on basal prey; however, whether other conspecific antagonisms balance this effect requires further investigation. The outcomes of predator–predator interactions can manifest in a variety of ways for basal resources. Pl Lr Pl + Lr Predator Broadly, interactions can elicit either additive, antag- onistic or synergistic outcomes (Soluk 1993; Losey Fig. 4 Individual and multiple predator consumption by and Denno 1998; Sih et al. 1998; Vance-Chalcraft and Paradiaptomus lamellatus (Pl) and Lovenula raynerae (Lr) Soluk 2005; Barrios-O’Neill et al. 2014a; Wasserman towards larval Culex pipiens. Means are ± SE (n = 5 per treatment group) et al. 2016c). Our results demonstrate that per capita prey risk reductions may result when multiple P. lamellatus are present. Such antagonism has No. prey eaten (± SE) No. prey eaten (± SE) 188 Aquat Ecol (2020) 54:181–191 additionally been displayed in other study systems in associated with their larger size coupled with require- respect to both heterospecific (e.g. Soluk 1993; ments for progeny development (e.g. Laybourn-Parry Barrios-O’Neill et al. 2014a) and conspecific (e.g. et al. 1988; Cuthbert et al. 2019a). Paradiaptomus Wasserman et al. 2016c) predator groups. Yet, there lamellatus was shown here to be able to handle larval has been a lack of work considering predatory culicid prey at consistent levels across diurnal and zooplankters (Cuthbert et al. 2019b). Multiple P. surface area variations, with the higher predation rates lamellatus were shown to interact antagonistically in of females in comparison with males robust to these the present study, thus alleviating prey risk. Non- abiotic differences. These intraspecific differences in trophic interactions were always negative here, irre- predation rate may be driven by body size or spective of prey density, in contrast to other studies reproductive energy demands. However, the effects where a unimodal relationship has been demonstrated of surface area for other abiotic factors that may (Sentis et al. 2017). Moreover, there were no signif- influence predation rates, such as temperature, require icant differences in single and multiple predator further elucidation given the observed effects of consumption rates by P. lamellatus in the present warming for interaction strengths in temporary ponds study, and there were no differences in FR form (Wasserman et al. 2016b; Cuthbert et al. 2019c). The exhibited between predator treatments towards culicid lack of response to day/night differences suggests a prey. Whilst attack rates tended to be higher in reliance on hydromechanical cues to capture prey in P. lamellatus, as with other copepods (Hwang and conspecific as compared to single copepod treatments, handling times were longer and thus maximum Strickler 2001; Cuthbert et al. 2018d). Contrastingly, feeding rates were generally reduced. This corrobo- other studies have demonstrated species-specific rates our finding of negative non-trophic interactions, responses to diurnal regime which affect feeding rates with multiple predators tending to reduce rather than (e.g. Barrios-O’Neill et al. 2014b) and shown search increase feeding rates. Nevertheless, as Type II FRs area implications for FR parameterisation (e.g. Uiter- are characterised by high per capita rates of resource waal and DeLong 2018). Therefore, in ephemeral acquisition at low prey densities, both single and wetlands, predation pressures by calanoid copepods multiple predator treatments could be destabilising to likely remain high across daily photoperiod undula- mosquito prey populations. Conversely, towards tions and throughout the various spatial stages of daphniid prey, Wasserman et al. (2016a) demonstrated hydroperiod. Empirically, this may corroborate with that P. lamellatus displays a more sigmoidal FR, the temporal constraints which characterise ephemeral which may impart greater stability to this prey type. systems and necessitate sustained resource intake rates Therefore, the FR form of ephemeral wetland spe- in the ‘race against time’ to reproduce in zooplankters cialist copepod species appears to be variable depend- in these systems (De Meester et al. 2005). ing on species-level compositional differences within In contrast to the antagonism displayed by con- lower trophic groups. In turn, these interspecific specific units of P. lamellatus, the present study shows differences may contribute to prey species extirpations that predatory interactions can be enhanced when this within temporary aquatic systems, with the FR type species is in the presence of heterospecifics. Combined known to directly influence population stability (Dick feeding rates were significantly elevated in the pres- et al. 2014). Here, this may indicate that larval ence of the controphic calanoid copepod L. raynerae. mosquitoes are impacted to a greater degree than This seeming lack of predator–predator interference daphniids by P. lamellatus. may be driven by differences in spatial occupancy In the present study, interaction strengths of female between the species, with P. lamellatus mainly P. lamellatus were shown to be significantly greater benthic, whilst L. raynerae occupies the water column. than male conspecifics. Many copepod species display Given that these calanoids often coexist in ephemeral marked sexual dimorphism (e.g. Oktsuka and Huys wetlands, with both species recruited internally from 2001) alongside behavioural variation (e.g. Wasser- dormant, drought-resistant eggs (Wasserman et al. man et al. 2018), and this in turn can manifest in 2016a), our results suggest that variations in predator variable feeding rates (see Cuthbert et al. 2019a). diversity will have implications for basal prey, Feeding rates of gravid female copepods are often wherein higher densities of L. raynerae may intensify elevated due to heightened energetic demands predation pressure. Indeed, L. raynerae has also been 123 Aquat Ecol (2020) 54:181–191 189 Barrios-O’Neill D, Dick JTA, Ricciardi A, MacIsaac HJ, shown to demonstrate a destabilising Type II FR Emmerson MC (2014b) Deep impact: in situ functional towards various basal prey types (Wasserman et al. responses reveal context–dependent interactions between 2016a; Cuthbert et al. 2018c). vertically migrating invasive and native mesopredators and Overall, we show that biotic context relating to shared prey. Freshw Biol 59:2194–2203 Bolker BM (2008) emdbook: ecological models and data in R. predator–predator interactions and predator sexes can Princeton University Press, Princeton have marked, species-specific implications for inter- Bolker B, Holyoak M, Kr ˇivan V, Rowe L, Schmitz O (2003) action strengths in ephemeral wetlands, whilst abiotic Connecting theoretical and empirical studies of trait-me- effects were negligible. The ephemeral pond specialist diated interactions. Ecology 84:1101–1114 Bollache L, Dick JTA, Farnsworth KD, Montgomery WI (2008) copepod P. lamellatus interacted antagonistically with Comparison of the functional responses of invasive and conspecifics, yet positive multiple predator interac- native amphipods. Biol Lett 4:166–169 tions were indicated in the presence of the heterospeci- Brendonck L, De Meester L (2003) Egg banks in freshwater fic specialist copepod L. raynerae. Copepod predation zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84 was robust to variations in experimental surface area, Brooks JL, Dodson SI (1965) Predation, body size, and com- and predatory efficiencies were not altered by shifting position of plankton. Science 150:28–35 day/night regimes. Accordingly, predatory impact by Crawley MJ (2007) The R book. Wiley, Chichester these copepods is likely unaffected by habitat hetero- Cuthbert RN, Dick JTA, Callaghan A, Dickey JWE (2018a) Biological control agent selection under environmental geneity over the hydroperiod in ephemeral wetlands, change using functional responses, abundances and yet is affected by predator–predator exchanges and fecundities; the Relative Control Potential (RCP) metric. heightened in female copepods. Whilst little is known Biol Control 121:50–57 about trophic interactions driven by specialist cope- Cuthbert RN, Callaghan A, Dick JTA (2018b) Interspecific variation, habitat complexity and ovipositional responses pods in ephemeral wetlands within arid regions, this modulate the efficacy of cyclopoid copepods in disease study provides important insights into such interaction vector control. Biol Control 121:80–87 strengths under key environmental contexts. Cuthbert RN, Dalu T, Wasserman RJ, Callaghan A, Weyl OLF, Dick JTA (2018c) Calanoid copepods: an overlooked tool Acknowledgements This study forms part of a Ph.D. in the biocontrol of disease vector mosquitoes. J Med studentship provided by the Department for the Economy, Entomol 55:1656–1658 Northern Ireland. We thank Rhodes University for the provision Cuthbert RN, Dalu T, Wasserman RJ, Coughlan NE, Callaghan of laboratory facilities. This study was partially funded by the A, Weyl OLF, Dick JTA (2018d) Muddy waters: effica- National Research Foundation—South African Research Chairs cious predation of container-breeding mosquitoes by a Initiative of the Department of Science and Innovation (Inland newly-described calanoid copepod across differential Fisheries and Freshwater Ecology, Grant No. 110507). water clarities. Biol Control 127:25–30 Cuthbert RN, Dalu T, Wasserman RJ, Coughlan NE, Weyl OLF, Compliance with ethical standards Callaghan A, Froneman PW, Dick JTA (2019a) Sex- skewed trophic impacts in ephemeral wetlands. Freshw Conflict of interest The authors declare that they have no Biol 64:359–366 conflicts of interest. Cuthbert RN, Callaghan A, Sentis A, Dalal A, Dick JTA (2019b) Additive multiple predator effects can reduce mosquito Open Access This article is distributed under the terms of the populations. Ecol Entomol https://doi.org/10.1111/een. 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Aquatic Ecology – Springer Journals
Published: Mar 29, 2020
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