ArticlePDF Available

Foraging strategy mediates ectotherm predator–prey responses to climate warming

Wiley
Ecology
Authors:
Laura A Twardochleb at CA State Water Resources Control Board
Laura A Twardochleb
Tyler Treakle at Arizona State University
Tyler Treakle
Phoebe Lehmann Zarnetske at Michigan State University
Phoebe Lehmann Zarnetske
Download full-text PDF
Read full-text
Download citation

Abstract and Figures

Climate warming and species traits interact to influence predator performance, including individual feeding and growth rates. However, the effects of an important trait—predator foraging strategy—are largely unknown. We investigated the interactions between predator foraging strategy and temperature on two ectotherm predators: an active predator, the backswimmer Notonecta undulata, and a sit‐and‐wait predator, the damselfly Enallagma annexum. In a series of predator–prey experiments across a temperature gradient, we measured predator feeding rates on an active prey species, zooplankton Daphnia pulex, predator growth rates, and mechanisms that influence predator feeding: body speed of predators and prey (here measured as swimming speed), prey encounter rates, capture success, attack rates, and handling time. Overall, warming led to increased feeding rates for both predators through changes to each component of the predator’s functional response. We found that prey swimming speed strongly increased with temperature. The active predator’s swimming speed also increased with temperature, and together, the increase in predator and prey swimming speed resulted in twofold higher prey encounter rates for the active predator at warmer temperatures. By contrast, prey encounter rates of the sit‐and‐wait predator increased fourfold with rising temperatures as a result of increased prey swimming speed. Concurrently, increased prey swimming speed was associated with a decline in the active predator’s capture success at high temperatures, whereas the sit‐and‐wait predator’s capture success slightly increased with temperature. We provide some of the first evidence that foraging traits mediate the indirect effects of warming on predator performance. Understanding how traits influence species’ responses to warming could clarify how climate change will affect entire functional groups of species.
The Arrhenius equation provided the best fit for the relationship between temperature and swimming speed (cm/s) of Notonecta, with slope Ea (activation energy, eV ± 1 SE) = 0.10 (±0.05). A segmented model provided the best fit for Daphnia, with a breakpoint near 28°C, Ea = 0.11 (± 0.06) at temperatures below the breakpoint, and Ea = 1.04 (± 0.23) above the breakpoint. The 95% confidence intervals around the best‐fit line are represented by gray bands for Daphnia and broken red lines for Notonecta.
The Arrhenius equation provided the best fit for the relationship between temperature and swimming speed (cm/s) of Notonecta, with slope Ea (activation energy, eV ± 1 SE) = 0.10 (±0.05). A segmented model provided the best fit for Daphnia, with a breakpoint near 28°C, Ea = 0.11 (± 0.06) at temperatures below the breakpoint, and Ea = 1.04 (± 0.23) above the breakpoint. The 95% confidence intervals around the best‐fit line are represented by gray bands for Daphnia and broken red lines for Notonecta.
… 
Relationships between temperature, functional response components, and growth rates. (a) Best fit lines of the Arrhenius equation for encounters (per h 20 Daphnia per L ± 1 SE); (b) fit of the Arrhenius equation for capture success (number of successful attacks per encounter) of Enallagma, and the Arrhenius–quadratic equation for Notonecta; (c) Arrhenius fit for attack rates (L/h), (d) handling time (h), and (e) relative growth rates (mg mg0.34/d). Ea (eV ± 1 SE) is the activation energy, and Topt (°C ± 1 SE) is the thermal optimum. Broken lines represent 95% confidence intervals.
Relationships between temperature, functional response components, and growth rates. (a) Best fit lines of the Arrhenius equation for encounters (per h 20 Daphnia per L ± 1 SE); (b) fit of the Arrhenius equation for capture success (number of successful attacks per encounter) of Enallagma, and the Arrhenius–quadratic equation for Notonecta; (c) Arrhenius fit for attack rates (L/h), (d) handling time (h), and (e) relative growth rates (mg mg0.34/d). Ea (eV ± 1 SE) is the activation energy, and Topt (°C ± 1 SE) is the thermal optimum. Broken lines represent 95% confidence intervals.
… 
Functional responses at each temperature for (a) Notonecta and (b) Enallagma.
Functional responses at each temperature for (a) Notonecta and (b) Enallagma.
… 
Hypothesized combinations of temperature and prey density that should favor active or sit‐and‐wait strategies. (a) When prey speed increases with warming, active strategies could be advantageous at low temperatures when prey density is low. Sit‐and‐wait strategies could be advantageous at high temperatures when prey density is high. (b) When prey speed decreases with warming, active strategies could be favored at high temperatures when prey density is low. Sit‐and‐wait strategies could be favored at low temperatures when prey density is high.
Hypothesized combinations of temperature and prey density that should favor active or sit‐and‐wait strategies. (a) When prey speed increases with warming, active strategies could be advantageous at low temperatures when prey density is low. Sit‐and‐wait strategies could be advantageous at high temperatures when prey density is high. (b) When prey speed decreases with warming, active strategies could be favored at high temperatures when prey density is low. Sit‐and‐wait strategies could be favored at low temperatures when prey density is high.
… 
Figures - available from: Ecology
This content is subject to copyright. Terms and conditions apply.
Content uploaded by Laura A Twardochleb
Author content
All content in this area was uploaded by Laura A Twardochleb on Jul 30, 2020
Content may be subject to copyright.
A preview of the PDF is not available
A preview of this full-text is provided by Wiley.
Learn more
Content available from Ecology 
This content is subject to copyright. Terms and conditions apply.
... Using a system of periodically forced ordinary differential equations, we model changes throughout the growing season in zooplankton (resource) biomass (Z ), juvenile damselfly (consumer) body size (S) and damselfly abundance (C ) (figure 2). We define the growing season [54,55] as the period when pond temperature exceeds 10°C (electronic supplementary material, figure S1), since below 10°C damselfly and zooplankton activity levels are low [56,57]. We track emergence from the damselfly juvenile to adult stage during the growing season as discrete events within this continuous-time system. ...
... We assume the resource (zooplankton) Z grows logistically in the absence of the consumer (damselflies), with maximum growth rate r and carrying capacity K (figure 2); we add a small immigration term i to account for refugia and to prevent unrealistically large population cycles. Juvenile damselflies increase their body size S by ingesting zooplankton following a saturating type-II functional response [56], minus loss in growth potential owing to maintenance μ. Rates of resource consumption and maintenance increase linearly with juvenile body size. ...
... Here, a and h are the consumer attack rate and handling time on the resource, and e c is the conversion efficiency of the resource into growth in juvenile body size. Assuming that the temperature remains below the optimum, the rates r, a, h, μ and d are modelled as functions of temperature T (Kelvin) using the Arrhenius equation [3,56] ...
Life-history responses to temperature and seasonality mediate ectotherm consumer–resource dynamics under climate warming
Article
Full-text available
  • Apr 2023
Climate warming is altering life cycles of ectotherms by advancing phenology and decreasing generation times. Theoretical models provide powerful tools to investigate these effects of climate warming on consumer–resource population dynamics. Yet, existing theory primarily considers organisms with simplified life histories in constant temperature environments, making it difficult to predict how warming will affect organisms with complex life cycles in seasonal environments. We develop a size-structured consumer–resource model with seasonal temperature dependence, parameterized for a freshwater insect consuming zooplankton. We simulate how climate warming in a seasonal environment could alter a key life-history trait of the consumer, number of generations per year, mediating responses of consumer–resource population sizes and consumer persistence. We find that, with warming, consumer population sizes increase through multiple mechanisms. First, warming decreases generation times by increasing rates of resource ingestion and growth and/or lengthening the growing season. Second, these life-history changes shorten the juvenile stage, increasing the number of emerging adults and population-level reproduction. Unstructured models with similar assumptions found that warming destabilized consumer–resource dynamics. By contrast, our size-structured model predicts stability and consumer persistence. Our study suggests that, in seasonal environments experiencing climate warming, life-history changes that lead to shorter generation times could delay population extinctions.
View
... Thus, animals' reliance on food is linked to heatwaves-increased food consumption can offset the metabolic costs of elevated temperatures and promote heat tolerance [3][4][5]. However, foraging entails predation risks for many animals [6,7], and elevated temperatures can increase predation through improved capture efficiency and shifts in the functional response [8][9][10]. Therefore, foraging decision making plays a fundamental role in the ecology of fear-whereby the sub-lethal, fitness-related costs of avoiding predation may exceed the population-level costs of predation to prey [11,12] -in a warming world. ...
... Warming generally promotes insect reproduction, but its benefits can depend on food availability (this study; [50]). Warming may also increase mortality through its positive effects on predation [8][9][10]. Therefore, future work should investigate the combined effects of predation (rather than predation risk), food availability and heatwaves at the population or community level given the critical importance of insects to the functioning of terrestrial ecosystems (reviewed in [51]). ...
Hot and scared: how do heatwaves and predation risk impact resource acquisition and allocation?
Article
Full-text available
Heatwaves are increasingly prevalent and can constrain investment into important life-history traits. In addition to heatwaves, animals regularly encounter threats from other organisms in their environments, such as predators. The combination of these two environmental factors introduces a decision-making conflict—heat exposure requires more food intake to fuel investment into fitness-related traits, but foraging in the presence of predators increases the threat of mortality. Thus, we used female variable field crickets (Gryllus lineaticeps) to investigate the effects of heatwaves in conjunction with predation risk (exposed food and water sources, and exposure to scent from black widow spiders, Latrodectus hesperus) on resource acquisition (food intake) and allocation (investment into ovarian and somatic tissues). A simulated heatwave increased food intake and the allocation of resources to reproductive investment. Crickets exposed to high predation risk reduced food intake, but they were able to maintain reproductive investment at an expense to investment into somatic tissue. Thus, heatwaves and predation risk deprioritized investment into self-maintenance, which may impair key physiological processes. This study is an important step towards understanding the ecology of fear in a warming world.
View
... This is because with higher turbidity, detection distances will decrease between predator and prey [59], and in warmer water prey will spend more time swimming and engaging in predator inspection behaviours [42]. Regardless of the activity levels of the predator, increased activity in prey has been linked to higher encounter rates at high temperatures [60]. Therefore we hypothesize that the combined response to increased temperature and turbidity may be synergistic. ...
... However, as the activity (swimming speed) of the guppies increased in both the warm and interaction treatments, the predator and prey became closer. This is consistent with previous work demonstrating that increased activity increases encounter rates between predators and prey [60]. When only turbidity increased (i.e. in the turbid treatment), the predator-prey distance was also reduced, but in this instance activity levels of neither predator nor prey were significantly correlated with the predator-prey distance. ...
Temperature and turbidity interact synergistically to alter anti-predator behaviour in the Trinidadian guppy
Article
Full-text available
  • Jul 2023
Due to climate change, freshwater habitats are facing increasing temperatures and more extreme weather that disrupts water flow. Together with eutrophication and sedimentation from farming, quarrying and urbanization , freshwaters are becoming more turbid as well as warmer. Predators and prey need to be able to respond to one another adaptively, yet how changes in temperature and turbidity interact to affect predator-prey behaviour remains unexplored. Using a fully factorial design, we tested the combined effects of increased temperature and turbidity on the behaviour of guppy shoals (Poecilia reticulata) in the presence of one of their natural cichlid predators, the blue acara (Andinoacara pulcher). Our results demonstrate that the prey and predator were in closest proximity in warmer, turbid water, with an interaction between these stressors showing a greater than additive effect. There was also an interaction between the stressors in the inter-individual distances between the prey, where shoal cohesion increased with temperature in clear water, but decreased when temperature increased in turbid water. The closer proximity to predators and reduction in shoaling in turbid, warmer water may increase the risk of predation for the guppy, suggesting that the combined effects of elevated temperature and turbidity may favour predators rather than prey.
View
... Indirect effects of warming may pose a threat sooner than unavoidable prolonged exposure to critical temperatures. Indirect effects of climate change may be especially important for small-bodied ectotherms whose overall function and behavior vary in response to minute changes in the thermal landscape (Fucini et al., 2014;Twardochleb et al., 2020). ...
A Current Knowledge Gap and Documented Patterns in Body Temperature, Food Consumption, Daily Activity, and Growth Rate in Lizards
Article
  • Oct 2024
Warming temperatures are known to influence ectotherm life history and physiology. As climate change increases global temperatures, the consequences of direct and indirect effects of warming are becoming of high interest in biology. Warming temperatures could alter daily activity, change rates of food consumption, and influence allocation of energy, altering life history. Lizards are a taxon of concern regarding climate change, with documented thermal sensitivity in physiological performance and life history. The current study used a series of meta-analyses to examine how body temperature, food consumption, duration of daily activity, and growth rate influence lizards. The results indicated that warming temperatures increased food consumption but decreased growth rate. Meanwhile, increasing food consumption increases lizard growth rate. However, mechanistic studies are needed to determine the factors dictating identified trends, as the current approach is correlational. Overall, few data were available for the parameters of interest, with zero studies quantifying the influence of daily activity on food consumption. Restrictions in daily activity are a primary consideration with climate change models for lizards; however, empirical data quantifying the effects are lacking. The current study identified fruitful areas for future research, specifically on the effects of daily activity on energetics to understand indirect and direct effects of climate change.
View
... Recent theoretical developments provide a framework to investigate how complex processes emerge from species' individual metabolic responses to new thermal conditions using mechanistic models linking metabolism to locomotion to search rates. While some empirical data have emerged over the last decade to test these theoretical predictions [36][37][38] , both lab and field data remain scarce 39 . ...
Metabolic plasticity drives mismatches in physiological traits between prey and predator
Article
Full-text available
  • May 2024
Metabolic rate, the rate of energy use, underpins key ecological traits of organisms, from development and locomotion to interaction rates between individuals. In a warming world, the temperature-dependence of metabolic rate is anticipated to shift predator-prey dynamics. Yet, there is little real-world evidence on the effects of warming on trophic interactions. We measured the respiration rates of aquatic larvae of three insect species from populations experiencing a natural temperature gradient in a large-scale mesocosm experiment. Using a mechanistic model we predicted the effects of warming on these taxa’s predator-prey interaction rates. We found that species-specific differences in metabolic plasticity lead to mismatches in the temperature-dependence of their relative velocities, resulting in altered predator-prey interaction rates. This study underscores the role of metabolic plasticity at the species level in modifying trophic interactions and proposes a mechanistic modelling approach that allows an efficient, high-throughput estimation of climate change threats across species pairs.
View
... The inclusion of both environmental history and temporal variability is therefore an important frontier for such studies (Thompson et al. 2001). Finally, although climatic differences affect the availability of resources throughout the seasons, increasing temperature also has a direct effect on the foraging activity of animals, especially ectotherms (Roslin et al. 2017;Twardochleb et al. 2020), thus affecting the resource consumptions. Yet previous field studies of nutrient preferences have rarely considered the effects of time, climate and habitat simultaneously. ...
Different feeding preferences for macronutrients across seasons and sites indicate temporal and spatial nutrient limitation in the black bog ant
Article
Full-text available
  • Apr 2024
  • OECOLOGIA
How the resource use by consumers vary in different environments and time scales is one of the fundamental ecological questions. Replicated field studies are rare, however; so the extent to which nutrient use varies and why is uncertain. We studied an endangered tyrphobiotic species, the black bog ant (Formica picea), and its feeding preferences in temperate peatlands. We conducted a baiting experiment at three different sites with high nest densities, repeated over three years and three periods of growing season. Preferences for three main macronutrients (carbohydrates, proteins and lipids) were assessed. We hypothesised that if nutrient limitation plays a role, ants will have an increased need for proteins and lipids in early seasons when brood is raised, while carbohydrates use will increase in late seasons. We also expected that site identity would influence nutrient preferences, but not year. Our results supported the nutrient limitation hypothesis for proteins that were consumed more in the early season. In contrast, preference for carbohydrates was rather high and did not increase consistently through season. Although the occupancy of lipid baits was low overall, it increased at colder temperatures, in contrast to carbohydrate and protein baits. Nutrient preferences varied more among sites than years, with the lowest nutrient use observed in a diverse fen-meadow, consistent with the nutrient limitation hypothesis. Year affected ant abundance, but not bait occupancy. Our results suggest that black bog ants flexibly adapt their diet to environmental conditions and that an interplay between nutrient limitation and climate determines their feeding behaviour.
View
... Optimal foraging theory recognizes two basic types of strategies used by predators to find their prey: ambush (also called sit-and-wait) and active (or 'widely foraging') strategy (Bell, 1991). Moreover, a predator may also use a combination of these two strategies (Twardochleb et al., 2020;Zoroa et al., 2011). A typical sit-and-wait predator remains immobile for long periods in order to capture its prey via ambush, while active-searching predators wander throughout the habitat to locate their prey. ...
Sit-and-wait foraging is not enough in food-deprived environments: evidence from groundwater and salamanders
Article
Full-text available
  • Dec 2023
  • ANIM BEHAV
Keywords: activity ambush freshwater interaction optimal foraging predatoreprey sit-and-wait wide active foraging Foraging strategies are fundamental traits that characterize predators, with strong differences between sit-and-wait predators and active-searching predators. Optimal foraging theory predicts that environmental conditions affect the efficiency of these strategies, with active predators being favoured when prey are scarce and difficult to detect. Subterranean habitats are ideal models to study the effectiveness of foraging strategies. Laboratory studies on fish and salamander predators showed that active foraging often characterizes cave-adapted species, but field studies demonstrating the advantages of active foraging for growth and survival are lacking. In this study, we assessed how predators displaying a sit-and-wait strategy can cope with the variable costs of foraging under different ecological contexts, such as cave and surface environments. We performed a cross-environment experiment that was repeated in 3 years by rearing salamander, Salamandra salamandra, larvae from caves and surface streams in cages placed in both surface and cave environments. We measured larval growth (weight and total length) repeatedly every 10e20 days, from March to July, and assessed water temperature variation, prey availability and metamorphosis achievement in the rearing sites. Larvae in stream cages grew larger than larvae in subterranean cages, which showed negative growth. Our results suggest that the sit-and-wait strategy does not provide enough prey for development in cave environments, irrespective of larvae origin. In food-deprived environments, active foraging is necessary to obtain the energy required for the basic functions of the organisms exploiting them.
View
... The impact of climate change-induced stressors on trophic interactions is a complex research topic, triggering various degrees of effects in marine species across different trophic levels, even in ones with close phylogenetic links (i.e., same genus) (Parmesan, 2006). Climate change can also lead to population decline (IPCC, 2019), local extinction (Hofmann et al., 2010;IPCC, 2019;Twardochleb et al., 2020), and overall range shifts (Beukema et al., 2009;Howard et al., 2013;Lefort et al., 2015), creating novel interactions within a community. Predation is crucial among interspecific interactions, as a driver of both abundance and diversity of species, via prey consumption or behavior shifts (e.g., Sanford, 1999;Laws, 2017), with cascading effects through lower trophic levels that shapes community composition and ecosystem functioning (Sanford, 1999;Laws, 2017;Estes et al., 2011;Harley, 2011;Miller et al., 2014;Draper and Weissburg, 2019). ...
Impacts of ocean warming and acidification on predator-prey interactions in the intertidal zone: A research weaving approach
Article
  • Sep 2023
  • J EXP MAR BIOL ECOL
The effect of ocean warming and acidification on predator-prey interactions in the intertidal zone is a topic of growing concern for the scientific community. In this review, we aim to describe how scientists have explored the topic via research weaving, a combination of a systematic review, and a bibliometric approach. We assess articles published in the last decade exploring the impact of both stressors on predation in the intertidal zone, via experimental or observational techniques. Several methods were used to delve into how climate change-induced stress affected intertidal predation, as the study design leaned toward single-based driver trials to the detriment of a multi-driver approach. Mollusks, echinoderms, and crustaceans have been extensively used as model organisms , with little published data on other invertebrates, vertebrates, and algae taxa. Moreover, there is a strong web of co-authoring across institutions and countries from the Northern Hemisphere, that can skew our understanding towards temperate environments. Therefore, institutions and countries should increase participation in the southern hemisphere networking, assessing the problems under a global outlook. Our review also addresses the various impacts of ocean acidification, warming, or their interaction with predation-related variables, affecting organisms from the genetic to a broader ecological scope, such as animal behaviour or interspecific interactions. Finally, we argue that the numerous synonyms used in keywording articles in the field, possibly hurting future reviews in the area, as we provide different keyword standardizations. Our findings can help guide upcoming approaches to the topic by assessing what has been already done and revealing gaps in emerging themes, like a strong skew towards single-driver (specially acidification) lab experiments of northern hemisphere organisms and a lack of field multi-stressor experiments.
View
Differential metabolic responses in bold and shy sea anemones during a simulated heatwave
Article
Full-text available
  • Jan 2024
  • J EXP BIOL
As climate change-induced heatwaves become more common, phenotypic plasticity at multiple levels is a key mitigation strategy by which organisms can optimise selective outcomes. In ectotherms, changes to both metabolism and behaviour can help alleviate thermal stress. Nonetheless, no study in any ectotherm has yet empirically investigated how changing temperatures affect among-individual differences in the associations between these traits. Using the beadlet anemone (Actinia equina), an intertidal species from a thermally heterogeneous environment, we investigated how individual metabolic rates, linked to morphotypic differences in A. equina, and boldness were related across changing temperatures. A crossed-over design and a temporal control was used to test the same individuals at a non-stressful temperature, 13oC, and under a simulated heatwave at 21oC. At each temperature, short-term repeated measurements of routine metabolic rate (RMR) and a single measurement of a repeatable boldness-related behaviour, immersion response-time (IRT), were made. Individual differences, but not morphotypic differences, were highly predictive of metabolic plasticity, and the plasticity of RMR was associated with IRT. At 13oC, shy animals had the highest metabolic rates, while at 21oC this relationship was reversed. Individuals that were bold at 13oC also exhibited the highest metabolic rates at 21oC. Additional metabolic challenges during heatwaves could be detrimental to fitness in bold individuals. Equally, lower metabolic rates at non-stressful temperatures could be necessary for optimal survival as heatwaves become more common. These results provide novel insight into the relationship between metabolic and behavioural plasticity, and its adaptive implications in a changing climate.
View
Metabolic plasticity drives mismatches in physiological traits between prey and predator
Preprint
Full-text available
  • Oct 2023
Metabolic rate, the rate of energy use, underpins key ecological traits of organisms, from development and locomotion to interaction rates between individuals. A warming world, acting through the temperature-dependence of metabolic rate, is expected to alter predator-prey dynamics. Yet, there is very little real-world empirical evidence on the effects of warming on trophic interactions. We measured the respiration rates of the aquatic larvae of three insect species, from populations experiencing a natural gradient of temperatures in a large-scale mesocosm experiment. Using a mechanistic model we predicted the effects of warming on predator-prey interaction rates among these taxa. We found that differences in metabolic plasticity of the three species likely lead to mismatches in the temperature-dependence of their relative velocities, resulting in altered predator-prey interaction rates. We conclude that species-level differences in metabolic plasticity likely plays a key role in changing trophic interactions and food web dynamics in a warming world.
View
Functional responses are maximized at intermediate temperatures
Article
Full-text available
Functional responses describe how consumer foraging rates change with resource density. Despite extensive research looking at the factors underlying foraging interactions, there remains ongoing controversy about how temperature and body size control the functional response parameters space clearance (or attack) rate and handling time. Here, we investigate the effects of temperature, consumer mass, and resource mass using the largest compilation of functional responses yet assembled. This compilation contains 2,083 functional response curves covering a wide range of foragers and prey types, environmental conditions, and habitats. After accounting for experimental arena size, dimensionality of the foraging interaction, and consumer taxon, we find that both space clearance rate and handling time are optimized at intermediate temperatures (a unimodal rather than monotonic response), suggesting that the response to global climate change depends on the location of the consumer’s current temperature relative to the optimum. We further confirm that functional responses are higher and steeper for large consumers and small resources, and models using consumer and resource masses separately outperformed models using consumer:resource mass ratios, suggesting that consumer and resource body mass act independently to set interaction strengths. Lastly, we show that the extent to which foraging is affected by temperature or mass depends on the taxonomic identity of the consumer and the dimensionality of the consumer–resource interaction. We thus argue that although overall body size and temperature effects can be identified, they are not universal, and therefore food web and community modeling approaches could be improved by considering taxonomic identity along with body size and unimodal temperature effects.
View
Consistent temperature dependence of functional response parameters and their use in predicting population abundance
Article
Full-text available
Global warming is one of the greatest threats to the persistence of populations: increased metabolic demands should strengthen pairwise species interactions, which could destabilize food webs at the higher organizational levels. Quantifying the temperature dependence of consumer–resource interactions is thus essential for predicting ecological responses to warming. We explored feeding interactions between different predator–prey pairs in controlled‐temperature chambers and in a system of naturally heated streams. We found consistent temperature dependence of attack rates across experimental settings, though the magnitude and activation energy of attack rate were specific to each predator, which varied in mobility and foraging mode. We used these parameters along with metabolic rate measurements to estimate energetic efficiency and population abundance with warming. Energetic efficiency accurately estimated field abundance of a mobile predator that struggled to meet its metabolic demands, but was a poor predictor for a sedentary predator that operated well below its energetic limits. Temperature effects on population abundance may thus be strongly dependent on whether organisms are regulated by their own energy intake or interspecific interactions. Given the widespread use of functional response parameters in ecological modelling, reconciling outcomes from laboratory and field studies increases the confidence and precision with which we can predict warming impacts on natural systems.
View
Metabolic asymmetry and the global diversity of marine predators
Article
Full-text available
  • Jan 2019
Cold is better for polar predators Generally, biodiversity is higher in the tropics than at the poles. This pattern is present across taxa as diverse as plants and insects. Marine mammals and birds buck this trend, however, with more species and more individuals occurring at the poles than at the equator. Grady et al. asked why this is (see the Perspective by Pyenson). They analyzed a comprehensive dataset of nearly 1000 species of shark, fish, reptiles, mammals, and birds. They found that predation on ectothermic (“cold-blooded”) prey is easier where waters are colder, which generates a larger resource base for large endothermic (“warm-blooded”) predators in polar regions. Science , this issue p. eaat4220 ; see also p. 338
View
Warming drives higher rates of prey consumption and increases rates of intraguild predation
Article
Full-text available
  • Jul 2018
  • OECOLOGIA
Warming due to climate change is expected to alter species interactions. These interactions are shaped by components of individual behavior, particularly foraging behaviors. However, few studies consider species’ behavioral responses to warming to predict how species interactions will be affected by warming. We chose two complementary approaches to examine how climate warming may affect the behavior and interactions of aquatic intraguild predators. First, we measured behavioral responses to warming in six larval dragonfly species, expecting that feeding rate and activity would increase with temperature. Secondly, we conducted intraguild predation (IGP) trials with three species to understand how temperature affects IGP, and if species’ behavioral responses to warming are indicative of the outcome of IGP interactions. Warming increased feeding rates by 42% on average across species but had no effect on activity rate. The magnitude of change in feeding rate was positively correlated with the maximum temperatures species experience across their ranges. Lastly, warming increased rates of IGP twofold, however, species’ behavioral responses alone were not predictive of their susceptibility to become IG prey of other larvae at warmer temperatures. Our results provide evidence that IGP interactions may be greatly affected by future increases in temperature; however, activity responses to warming alone are weak predictors of the outcomes of these interactions. Future studies should consider other species’ traits when forecasting the effects of climate change on species interactions.
View
Smell or vision? The use of different sensory modalities in predator discrimination
Article
Full-text available
  • Sep 2017
  • BEHAV ECOL SOCIOBIOL
Theory predicts that animals should adjust their escape responses to the perceived predation risk. The information animals obtain about potential predation risk may differ qualitatively depending on the sensory modality by which a cue is perceived. For instance, olfactory cues may reveal better information about the presence or absence of threats, whereas visual information can reliably transmit the position and potential attack distance of a predator. While this suggests a differential use of information perceived through the two sensory channels, the relative importance of visual vs. olfactory cues when distinguishing between different predation threats is still poorly understood. Therefore, we exposed individuals of the cooperatively breeding cichlid Neolamprologus pulcher to a standardized threat stimulus combined with either predator or non-predator cues presented either visually or chemically. We predicted that flight responses towards a threat stimulus are more pronounced if cues of dangerous rather than harmless heterospecifics are presented and that N. pulcher, being an aquatic species, relies more on olfaction when discriminating between dangerous and harmless heterospecifics. N. pulcher responded faster to the threat stimulus, reached a refuge faster and entered a refuge more likely when predator cues were perceived. Unexpectedly, the sensory modality used to perceive the cues did not affect the escape response or the duration of the recovery phase. This suggests that N. pulcher are able to discriminate heterospecific cues with similar acuity when using vision or olfaction. We discuss that this ability may be advantageous in aquatic environments where the visibility conditions strongly vary over time. Significance statement The ability to rapidly discriminate between dangerous predators and harmless heterospecifics is crucial for the survival of prey animals. In seasonally fluctuating environment, sensory conditions may change over the year and may make the use of multiple sensory modalities for heterospecific discrimination highly beneficial. Here we compared the efficacy of visual and olfactory senses in the discrimination ability of the cooperatively breeding cichlid Neolamprologus pulcher. We presented individual fish with visual or olfactory cues of predators or harmless heterospecifics and recorded their flight response. When exposed to predator cues, individuals responded faster, reached a refuge faster and were more likely to enter the refuge. Unexpectedly, the olfactory and visual senses seemed to be equally efficient in this discrimination task, suggesting that seasonal variation of water conditions experienced by N. pulcher may necessitate the use of multiple sensory channels for the same task. Electronic supplementary material The online version of this article (10.1007/s00265-017-2371-8) contains supplementary material, which is available to authorized users.
View
View
Searching for Biotic Multipliers of Climate Change
Article
  • Jul 2017
  • INTEGR COMP BIOL
Synopsis: As climates change, biologists need to prioritize which species to understand, predict, and protect. One way is to identify key species that are both sensitive to climate change and that disproportionately affect communities and ecosystems. These "biotic multipliers" provide efficient targets for research and conservation. Here, we propose eight mechanistic hypotheses related to impact and sensitivity that suggest that top consumers might often act as biotic multipliers of climate change. For impact, top consumers often affect communities and ecosystems through strong top-down effects. For sensitivity, metabolic theory and data suggest that photosynthesis and respiration differ in temperature responses, potentially increasing the sensitivity of consumers relative to plants. Larger-bodied organisms are typically more thermally sensitive than smaller ones, suggesting how large top consumers might be more sensitive than their smaller prey. In addition, traits related to predation are more sensitive than defensive traits to temperature. Top consumers might also be more sensitive because they often lag behind prey in phenological responses. The combination of low population sizes and demographic traits of top consumers could make them more sensitive to disturbances like climate change, which could slow their recovery. As top consumers are positioned at the top of the food chain, many small effects can accumulate from other trophic levels to affect top consumers. Finally, top consumers also often disperse more frequently and farther than prey, potentially leading to greater sensitivity to climate-induced changes in ranges and subsequent impacts on invaded communities. Overall, we expect that large, ectothermic top consumers and mobile predators might frequently be biotic multipliers of climate change. However, this prediction depends on the particular features of species, habitats, and ecosystems. In specific cases, herbivores, plants, or pathogens might be more sensitive than top consumers or have greater community impacts. To predict biotic multipliers, we need to compare sensitivities and impacts across trophic groups in a broader range of ecosystems as well as perform experiments that uncouple proposed mechanisms. Overall, the biotic multiplier concept offers an alternative prioritization scheme for research and conservation that includes impacts on communities and ecosystems.
View
View
Temperature and consumer type dependencies of energy flows in natural communities
Article
  • Dec 2017
  • OIKOS
With the world continuously warming, a mechanistic understanding of how temperature affects interaction strengths, which are fundamental to food-web stability, is needed. As interaction strengths are determined by the flows of energy from resources to consumers, we investigated effects of temperature on animal energetics. We used newly compiled datasets on respiration rates and assimilation efficiencies to assess how temperature affects the energy use (respiration rates) and the efficiency of energy gain (assimilation efficiency) for different consumer types. Furthermore, we incorporated our findings in a simulation of temperature effects on maintenance feeding rates (i.e. energy consumption necessary to sustain life). Our analysis revealed a generally positive temperature dependence of assimilation efficiencies across consumer types thus implying a net energy gain with warming. The temperature scaling of respiration rates did not differ between consumer types. Based on these parameters we calculated maintenance feeding rates and compared them to empirically measured (realized) feeding rates. This comparison revealed that detritivores and herbivores have the potential to increase their biomasses under warming as their maintenance feeding rates increase less strongly than their realized feeding rates. For carnivores, however, we found a stronger increase of their maintenance feeding rates compared to their realized feeding rates, which should lead to decreased population sizes under warming. Overall, our results increase the understanding of climate change effects on ecosystems as they suggest profound energetic consequences for natural communities. This article is protected by copyright. All rights reserved.
View
Frair: an R package for fitting and comparing consumer functional responses
Article
Consumer‐resource interactions (i.e. the functional response) underpin decades of ecological advancements. However, selecting, fitting and comparing functional response models using appropriate methods remains a non‐trivial endeavour. The R package frair provides tools for selecting and differentiating various forms of consumer functional response models, a consistent interface for fitting and visualising response curves, and a selection of statistically robust methods for comparing fitted parameters. Using real data from crustacean predator‐prey systems, we demonstrate the utility of frair , highlighting best practice and common analytical mistakes.
View