An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Predator‐induced selection on urchin activity level depends on urchin body size

Temporally consistent individual differences in behavior impact many ecological processes. We simultaneously examined the effects of individual variation in prey activity level, covering behavior, and body size on prey survival with predators using an urchin–lobster system. Specifically, we tested the hypothesis that slow‐moving purple sea urchins (Strongylocentrotus purpuratus) and urchins who deploy extensive substrate (pebbles and stones) covering behavior will out‐survive active urchins that deploy little to no covering behavior when pitted against a predator, the California spiny lobster (Panulirus interruptus). We evaluated this hypothesis by first confirming whether individual urchins exhibit temporally consistent differences in activity level and covering behavior, which they did. Next, we placed groups of four urchins in mesocosms with single lobster and monitored urchin survival for 108 hr. High activity level was negatively associated with survival, whereas urchin size and covering behavior independently did not influence survival. The negative effect of urchin activity level on urchin survival was strong for smaller urchins and weaker for large urchins. Taken together, these results suggest that purple urchin activity level and size jointly determine their susceptibility to predation by lobsters. This is potentially of great interest, because predation by recovering lobster populations could alter the stability of kelp forests by culling specific phenotypes, like foraging phenotypes, from urchin populations.     

The influence of landscape features on nest predation rates of grassland‐breeding waders

In Europe, lowland wet grasslands have become increasingly fragmented, and populations of waders in these fragments are subject to unsustainably high levels of nest predation. Patches of taller vegetation in these landscapes can support small mammals, which are the main source of prey for many predators. Providing such patches of habitat could potentially reduce levels of nest predation if predators preferentially target small mammals. However, predator attraction to patches of taller vegetation for foraging, shelter, perching and/or nesting could also result in local increases in predation rates, as a consequence of increased predator densities or spill‐over foraging into the surrounding area. Here we assess the influence of taller vegetation on wader nest predation rates, and the feasibility of managing vegetation structure to alter predator impacts. Between 2005 and 2011, the nest distribution and hatching success of Northern Lapwings Vanellus vanellus, which nest in the open, and Common Redshanks Tringa totanus, which conceal their nests in vegetation, were measured on a 487‐ha area of wet grassland in eastern England that is primarily managed for breeding waders. Predation rates of Lapwing nests increased significantly with distance from patches of taller vegetation, and decreased with increasing area of taller vegetation within 1 km of the nest, whereas neither variable influenced Redshank nest predation probability. These findings suggest that the distribution and activity of nest predators in lowland wet grassland landscapes may be influenced by the presence and distribution of areas of taller vegetation. For Lapwings at least, there may therefore be scope for landscape‐scale management of vegetation structure to influence levels of predation in these habitats.     

Detection of earthworm prey by Ruff Philomachus pugnax

Ruff Philomachus pugnax staging in the Netherlands forage in agricultural grasslands, where they mainly eat earthworms (Lumbricidae). Food intake and the surface availability of earthworms were studied in dairy farmland of southwest Friesland in March–April 2011. Daily changes in earthworm availability were quantified by counting visible earthworms. No earthworms were seen on the surface during daytime, but their numbers sharply increased after sunset and remained high during the night. Nevertheless, intake rates of individual Ruff in different grasslands measured during daytime showed the typical Holling type II functional response relationship with the surfacing earthworm densities measured at night. Radiotagging of Ruff in spring 2007 revealed that most, if not all, feeding occurs during the day, with the Ruff assembling at shoreline roosts at night. This raises the question of why Ruff do not feed at night, if prey can be caught more easily than during daytime. In March–May 2013 we experimentally examined the visual and auditory sensory modalities used by Ruff to find and capture earthworms. Five males were kept in an indoor aviary and we recorded them individually foraging on trays with 10 earthworms mixed with soil under various standardized light and white noise conditions. The number of earthworms discovered and eaten by Ruff increased with light level, but only when white noise was played, suggesting that although they can detect earthworms by sight, Ruff also use auditory cues. We suggest that although surfacing numbers of earthworms are highest during the night, diurnal intake rates are probably sufficient to avoid nocturnal foraging on a resource that is more available but perhaps less detectable at that time.     

Habitat complexity dampens selection on prey activity level

Conspecific prey individuals often exhibit persistent differences in behavior (i.e., animal personality) and consequently vary in their susceptibility to predation. How this form of selection varies across environmental contexts is essential to predicting ecological and evolutionary dynamics, yet remains currently unresolved. Here, we use three separate predator–prey systems (sea star–snail, wolf spider–cricket, and jumping spider–cricket) to independently examine how habitat structural complexity influences the selection that predators impose on prey behavioral types. Prior to conducting staged predator–prey interaction encounters, we ran prey individuals through multiple behavioral assays to determine their average activity level. We then allowed individual predators to interact with groups of prey in either open or structurally complex habitats and recorded the number and individual identity of prey that were eaten. Habitat complexity had no effect on overall predation rates in any of the three predator–prey systems. Despite this, we detected a pervasive interaction between habitat structure and individual prey activity level in determining individual prey survival. In open habitats, all predators imposed strong selection on prey behavioral types: sea stars preferentially consumed sedentary snails, while spiders preferentially consumed active crickets. Habitat complexity dampened selection within all three systems, equalizing the predation risk that active and sedentary prey faced. These findings suggest a general effect of habitat complexity that reduces the importance of prey activity level in determining individual predation risk. We reason this occurs because activity level (i.e., movement) is paramount in determining risk within open environments, whereas in complex habitats, other behavioral traits (e.g., escape ability to a refuge) may take precedence.     

Temperature dependency of predation: Increased killing rates and prey mass consumption by predators with warming

Temperature dependency of consumer–resource interactions is fundamentally important for understanding and predicting the responses of food webs to climate change. Previous studies have shown temperature‐driven shifts in herbivore consumption rates and resource preference, but these effects remain poorly understood for predatory arthropods. Here, we investigate how predator killing rates, prey mass consumption, and macronutrient intake respond to increased temperatures using a laboratory and a field reciprocal transplant experiment. Ectothermic predators, wolf spiders (Pardosa sp.), in the lab experiment, were exposed to increased temperatures and different prey macronutrient content (high lipid/low protein and low lipid/high protein) to assess changes in their killing rates and nutritional demands. Additionally, we investigate prey mass and lipid consumption by spiders under contrasting temperatures, along an elevation gradient. We used a field reciprocal transplant experiment between low (420 masl; 26°C) and high (2,100 masl; 15°C) elevations in the Ecuadorian Andes, using wild populations of two common orb‐weaver spider species (Leucauge sp. and Cyclosa sp.) present along the elevation gradient. We found that killing rates of wolf spiders increased with warmer temperatures but were not significantly affected by prey macronutrient content, although spiders consumed significantly more lipids from lipid‐rich prey. The field reciprocal transplant experiment showed no consistent predator responses to changes in temperature along the elevational gradient. Transplanting Cyclosa sp. spiders to low‐ or high‐elevation sites did not affect their prey mass or lipid consumption rate, whereas Leucauge sp. individuals increased prey mass consumption when transplanted from the high to the low warm elevation. Our findings show that increases in temperature intensify predator killing rates, prey consumption, and lipid intake, but the responses to temperature vary between species, which may be a result of species‐specific differences in their hunting behavior and sensitivity to temperature.     

To feed or not to feed? Bioenergetic impacts of fear‐driven behaviors in lactating dolphins

In mammals, lactation can be the most energetically expensive part of the reproductive cycle. Thus, when energy needs are compromised due to predation risk, environmental disturbance, or resource scarcity, future reproductive success can be impacted. In marine and terrestrial environments, foraging behavior is inextricably linked to predation risk. But quantification of foraging energetics for lactating animals under predation risk is less understood. In this study, we used a spatially explicit individual‐based model to study how changes in physiology (lactating or not) and the environment (predation risk) affect optimal behavior in dolphins. Specifically, we predicted that an adult dolphin without calf would incur lower relative energetic costs compared to a lactating dolphin with calf regardless of predation risk severity, antipredator behavior, or prey quality consumed. Under this state‐dependent analysis of risk approach, we found predation risk to be a stronger driver in affecting total energetic costs (foraging plus locomotor costs) than food quality for both dolphin types. Further, contrary to our hypothesis, after accounting for raised energy demands, a lactating dolphin with calf does not necessarily have higher relative‐to‐baseline costs than a dolphin without calf. Our results indicate that both a lactating (with calf) and non‐lactating dolphin incur lowered energetic costs under a risk‐averse behavioral scheme, but consequently suffer from lost foraging calories. A lactating dolphin with calf could be particularly worse off in lost foraging calories under elevated predation risk, heightened vigilance, and increased hiding time relative to an adult dolphin without calf. Further, hiding time in refuge could be more consequential than detection distance for both dolphin types in estimated costs and losses incurred. In conclusion, our study found that reproductive status is an important consideration in analyzing risk effects in mammals, especially in animals with lengthy lactation periods and those exposed to both biological and nonbiological stressors.     

Predatory strategies and behaviours in cephalopods are altered by elevated CO2

There is increasing evidence that projected near‐future carbon dioxide (CO₂) levels can alter predator avoidance behaviour in marine invertebrates, yet little is known about the possible effects on predatory behaviours. Here we tested the effects of elevated CO₂ on the predatory behaviours of two ecologically distinct cephalopod species, the pygmy squid, Idiosepius pygmaeus, and the bigfin reef squid, Sepioteuthis lessoniana. Both species exhibited an increased latency to attack and altered body pattern choice during the attack sequence at elevated CO₂. I. pygmaeus also exhibited a 20% decrease in predation rate, an increased striking distance, and reduced preference for attacking the posterior end of prey at elevated CO₂. Elevated CO₂ increased activity levels of S. lessoniana comparable to those previously shown in I. pygmaeus, which could adversely affect their energy budget and increase their potential to be preyed upon. The effects of elevated CO₂ on predatory behaviours, predation strategies and activity levels of cephalopods reported here could have far‐reaching consequences in marine ecosystems due to the ecological importance of cephalopods in the marine food web.     

Effects of prey abundance,distribution, visual contrast and morphology on selection by a pelagic piscivore

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Learned Recognition of Novel Predator Odour by Zebra Danios, Danio Rerio, Following Time-shifted Presentation of Alarm Cue And Predator Odour

Fishes in the superorder ostariophysi possess specialized epidermal cells that contain an alarm cue. Fish associate novel odours, such as the odour of a predator, with predation risk after a single, simultaneous exposure to the novel odour and alarm cue. Thereafter, the novel cue is recognized as an indicator of risk and its presence induces antipredator behaviour. Two common antipredator behaviours are reduction in activity and movement to the bottom. This phenomenon has been demonstrated many times in the laboratory setting for a variety of aquatic taxa. In nature however, the detection of novel predator odour may be time-shifted with respect to the detection of alarm cues. Is there a critical period immediately upon the detection of alarm cue in which associative learning can occur? We presented zebra danios, Danio rerio, with the odour of northern pike, Esox lucius, 5?min after presenting them with either alarm cue or water (control). During a predation event, 5?min is a long time. When later retested with pike odour alone, zebra fish conditioned with alarm cue significantly increased antipredator behaviour in terms of decreased activity and movement towards the bottom. Control fish did not recognize pike odour as dangerous when retested. These data show that learned recognition of predation risk is sufficiently robust to accommodate ecologically realistic temporal shifts in stimulus presentation.     

Revolution in food web analysis and trophic ecology: diet analysis by DNA and stable isotope analysis

Characterization of energy flow in ecosystems is one of the primary goals of ecology, and the analysis of trophic interactions and food web dynamics is key to quantifying energy flow. Predator‐prey interactions define the majority of trophic interactions and food web dynamics, and visual analysis of stomach, gut or fecal content composition is the technique traditionally used to quantify predator‐prey interactions. Unfortunately such techniques may be biased and inaccurate due to variation in digestion rates ( Sheppard & Hardwood 2005 ); however, those limitations can be largely overcome with new technology. In the last 20 years, the use of molecular genetic techniques in ecology has exploded ( King et al. 2008 ). The growing availability of molecular genetic methods and data has fostered the use of PCR‐based techniques to accurately distinguish and identify prey items in stomach, gut and fecal samples. In this month’s issue of Molecular Ecology Resources, Corse et al. (2010) describe and apply a new approach to quantifying predator‐prey relationships using an ecosystem‐level genetic characterization of available and consumed prey in European freshwater habitats ( Fig. 1a ). In this issue of Molecular Ecology, Hardy et al. (2010) marry the molecular genetic analysis of prey with a stable isotope (SI) analysis of trophic interactions in an Australian reservoir community ( Fig. 1b ). Both papers demonstrate novel and innovative approaches to an old problem – how do we effectively explore food webs and energy movement in ecosystems?

Figure 1 Open in figure viewer PowerPoint The aquatic habitats used for two studies of diet and trophic interactions that employed molecular genetic and stable isotope analyses. Panel a: Example of Rhone basin habitat (France) where fish diet was determined using PCR to classify prey to a series of ecological clades (photo by Emmanuel Corse). Panel b: A weir pool on the lower Murray River (Australia) where food web and prey use was evaluated using a combination of advanced molecular genetic and stable isotope analyses (photo credit: CSIRO).     

Consistent size‐independent harvest selection on fish body shape in two recreationally exploited marine species

Harvesting wild animals may exert size‐independent selection pressures on a range of morphological, life history, and behavioral traits. Most work so far has focused on selection pressures on life history traits and body size as morphological trait. We studied here how recreational fishing selects for morphological traits related to body shape, which may correlate with underlying swimming behavior. Using landmark‐based geometric morphometrics, we found consistent recreational fishing‐induced selection pressures on body shape in two recreationally exploited marine fish species. We show that individuals with larger‐sized mouths and more streamlined and elongated bodies were more vulnerable to passively operated hook‐and‐line fishing independent of the individual's body size or condition. While the greater vulnerability of individuals with larger mouth gapes can be explained by the direct physical interaction with hooks, selection against streamlined and elongated individuals could either involve a specific foraging mode or relate to underlying elevated swimming behavior. Harvesting using passive gear is common around the globe, and thus, size‐independent selection on body shape is expected to be widespread potentially leaving behind individuals with smaller oral gapes and more compact bodies. This might have repercussions for food webs by altering foraging and predation.     

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

1. Behavioural adaptations to avoid and evade predators are common. Many studies have investigated population divergence in response to changes in predation regime within species, but studies exploring interspecific patterns are scant. Studies on interspecific divergence can infer common outcomes from evolutionary processes and highlight the role of environmental constraints in shaping species traits. 2. Species of the dragonfly genus Leucorrhinia underwent well‐studied shifts from habitats being dominated by predatory fish (fish lakes) to habitat being dominated by predatory invertebrates (dragonfly lakes). This change in top predators resulted in a set of adaptive trait modifications in response to the different hunting styles of both predator types: whereas predatory fish actively search and pursue prey, invertebrate predator follow a sit‐and‐wait strategy, not pursuing prey. 3. Here it is shown that the habitat shift‐related change in selection regime on larval Leucorrhinia caused species in dragonfly lakes to evolve increased larval foraging and activity, and results suggest that they lost the ability to recognise predatory fish. 4. The results of the present study highlight the impact of predators on behavioural trait diversification with habitat‐specific predation regimes selecting for distinct behavioural expression.     

The Biology of Tiger Sharks, Galeocerdo Cuvier, in Shark Bay, Western Australia: Sex Ratio, Size Distribution, Diet, and Seasonal Changes in Catch Rates

Tiger sharks, Galeocerdo cuvier, are apex predators in a variety of nearshore ecosystems throughout the world. This study investigates the biology of tiger sharks in the shallow seagrass ecosystem of Shark Bay, Western Australia. Tiger sharks (n = 252) were the most commonly caught species (94%) compared to other large sharks. Tiger sharks ranged from 148–407cm TL. The overall sex ratio was biased towards females (1.8:1), but the sex ratio of mature animals (> 300cm TL) did not differ from 1:1. Contrary to previous accounts, tiger sharks were caught more often in all habitats during daylight hours than at night. Tiger shark catch rates were highly correlated with water temperature and were highest when water temperatures were above 19°C. The seasonal abundance of tiger sharks is correlated to both water temperature and the occurrence of their main prey: sea snakes and dugongs, Dugong dugon. Stomach contents analysis indicated that sea turtles and smaller elasmobranchs were also common prey. The importance of major seagrass grazers (dugongs and green sea turtles, Chelonia mydas) in the diet of tiger sharks suggests the possibility that these sharks are keystone predators in this ecosystem.     

Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey

Prey organisms reduce predation risk by altering their behavior, morphology, or life history. Avoiding or deterring predators often incurs costs, such as reductions in growth or fecundity. Prey minimize costs by limiting predator avoidance or deterrence to situations that pose significant risk of injury or death, requiring them to gather information regarding the relative threat potential predators pose. Chemical cues are often used for risk evaluation, and we investigated morphological responses of oysters (Crassostrea virginica) to chemical cues from injured conspecifics, from heterospecifics, and from predatory blue crabs (Callinectes sapidus) reared on different diets. Previous studies found newly settled oysters reacted to crab predators by growing heavier, stronger shells, but that adult oysters did not. We exposed oysters at two size classes (newly settled oyster spat and juveniles ~2.0 cm) to predation risk cue treatments including predator or injured prey exudates and to seawater controls. Since both of the size classes tested can be eaten by blue crabs, we hypothesized that both would react to crab exudates by producing heavier, stronger shells. Oyster spat grew heavier shells that required significantly more force to break, an effective measure against predatory crabs, when exposed to chemical exudates from blue crabs as compared to controls. When exposed to chemical cues from injured conspecifics or from injured clams (Mercenaria mercenaria), a sympatric bivalve, shell mass and force were intermediate between predator treatments and controls, indicating that oysters react to injured prey cues but not as strongly as to cues released by predators. Juvenile oysters of ~ 2.0 cm did not significantly alter their shell morphology in any of the treatments. Thus, newly settled oysters can differentiate between predatory threats and adjust their responses accordingly, with the strongest responses being to exudates released by predators, but oysters of 2.0 cm and larger do not react morphologically to predatory threats.     

Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies in a tri‐trophic system

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Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Behavioural response evoked by conspecific distress calls in two neotropical treefrogs

Anurans emit distress calls when attacked by predators as a defensive mechanism. As distress calls may trigger antipredator behaviour even in individuals that are not under attack, we tested whether this defensive behaviour induced behavioural changes in neighbouring conspecifics. We compared the behavioural responses of two species of Neotropical hylid frogs (genus Boana) to conspecific distress calls and white noise. Individuals of both species interrupted their vocal activity and decreased call rate after hearing the distress call. Natural variation on signal intensity calibrated among the nearest neighbours did not influence the response and we did not observe negative phonotaxis after any acoustic stimulus. Despite the fact that many predators are acoustically oriented, we could not determine if such response (reduced call rate) was induced by risk assessment or by the masking effect on advertisement calls. Boana faber responded similarly to white noise and distress calls, while B. bischoffi responded more intensely to distress calls. Duration of silence after playbacks in B. faber was longer than B. bischoffi. We suggest that, if the signals are interpreted as a risk cue by neighbouring conspecifics, each species may be preyed upon by different predators, as they may have led to distinct defensive strategies and different responses to distress calls. If risk assessment information is included in distress calls, it triggers behavioural responses only in the nearest neighbours, as we did not observe responses on the vocal activity of the interspecific chorus. Our results add relevant data about acoustic communication and interpretations by anurans, highlighting the importance of considering cues within common and widespread signals.     

Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators

1. Realized trophic niches of predators are often characterized along a one‐dimensional range in predator–prey body mass ratios. This prey range is constrained by an “energy limit” and a “subdue limit” toward small and large prey, respectively. Besides these body mass ratios, maximum speed is an additional key component in most predator–prey interactions.
2. Here, we extend the concept of a one‐dimensional prey range to a two‐dimensional prey space by incorporating a hump‐shaped speed‐body mass relation. This new “speed limit” additionally constrains trophic niches of predators toward fast prey.
3. To test this concept of two‐dimensional prey spaces for different hunting strategies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial mammalian predator–prey interactions, their body masses, and maximum speeds.
4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flexible. Group hunters and ambushers have evolved different strategies to occupy a similar trophic niche that avoids competition with pursuit predators. Moreover, our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro‐lions”) or mega‐carnivores (referred to as “mega‐cheetahs”).
5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic understanding of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions.

     

Diversity and coexistence are influenced by time‐dependent species interactions in a predator–prey system

Although numerous studies show that communities are jointly influenced by predation and competitive interactions, few have resolved how temporal variability in these interactions influences community assembly and stability. Here, we addressed this challenge in experimental microbial microcosms by employing empirical dynamic modelling tools to: (1) detect causal interactions between prey species in the absence and presence of a predator; (2) quantify the time‐varying strength of these interactions and (3) explore stability in the resulting communities. Our findings show that predators boost the number of causal interactions among community members, and lead to reduced dynamic stability, but higher coexistence among prey species. These results correspond to time‐varying changes in species interactions, including emergence of morphological characteristics that appeared to reduce predation, and indirectly facilitate growth of predator‐susceptible species. Jointly, our findings suggest that careful consideration of both context and time may be necessary to predict and explain outcomes in multi‐trophic systems.