Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems.     

Foraging Ecology of the Tropical Giant Hunting Ant Dinoponera australis (Hymenoptera: Formicidae)—Evaluating Mechanisms for High Abundance

A central goal of ecology is to understand the mechanisms behind variation in the abundance of species. Food web theory predicts higher biomass for animals at lower trophic levels. However, some high trophic level species may reach great abundance via highly efficient foraging behaviors. We evaluated ecological and behavioral traits of the giant tropical ant Dinoponera australis related to these mechanisms. We determined its distribution and abundance, documented its foraging behavior, and measured its trophic position in a population at P.N. Iguazú, Argentina. We report that D. australis colonies are overdispersed, and the species reaches a wet biomass of more than 2.5 kg/ha at this site. Dinoponera australis foraging behavior is characterized by route fidelity of individual workers, with different individuals specializing on different areas around the nest. Finally, stable isotopic evidence and direct observation suggest these ants are among the top predators in this terrestrial invertebrate community. We interpret our findings in the context of how the behavior of an abundant top predator creates an exception to the usual trade‐off between biomass and trophic level. Together these data provide insight into the biology of one of the world's largest ants and why they may be able to attain such high densities where they occur.     

Characterization of postdive recovery using sound recordings and its relationship to dive duration,exertion, and foraging effort of southern elephant seals (Mirounga leonina)

It is notoriously difficult to measure physiological parameters in cryptic free‐ranging marine mammals. However, it is critical to understand how marine mammals manage their energy expenditure and their diving behavior in environments where the predation risks are low and where survival is mainly linked to capacities to maintain physiological homeostasis and energy budget balance. Elephant seals are top marine predators that dive deeply and continuously when at sea. Using acoustic recorders deployed on two postbreeding southern elephant seals (SES) females, we developed methods to automatically estimate breathing frequency at the surface. Using this method, we found that seals took successive identical breaths at high frequency (0.29 Hz) when recovering at the surface and that breath count was strongly related to postdive surfacing time. In addition, dive depth was the main factor explaining surfacing time through the effects of dive duration and total underwater swimming effort exerted. Finally, we found that recovery does not only occur over one dive timescale, but over a multidive time scale for one individual. The way these predators manage their recovery will determine how they respond to the change in oceanic water column structure in the future.     

食物链长度远因与近因研究进展综述

食物链长度是生态系统的基本属性,其变化决定着群落结构和生态系统功能。稳定同位素分析技术的进步推进了生态系统中食物链长度决定因子相关研究的开展。尽管近期的研究证明了食物链长度与资源可利用性、生态系统大小、干扰等远因之间的关系,但是对于食物网内部结构变化这一近因对食物链长度的影响作用关注较少。综述了边界明确和开放类型淡水生态系统中食物链长度的相关研究进展;探讨了远因和近因机制在决定食物链长度中的作用;给出了判断不同层次和尺度上决定食物链长度机制的概念框架;为今后更好的开展不同生态系统间食物链长度的比较研究提出了建议。     

Shark Predation on Migrating Adult American Eels (Anguilla rostrata) in the Gulf of St. Lawrence

In an attempt to document the migratory pathways and the environmental conditions encountered by American eels during their oceanic migration to the Sargasso Sea, we tagged eight silver eels with miniature satellite pop-up tags during their migration from the St. Lawrence River in Québec, Canada. Surprisingly, of the seven tags that successfully transmitted archived data, six were ingested by warm-gutted predators, as observed by a sudden increase in water temperature. Gut temperatures were in the range of 20 to 25°C—too cold for marine mammals but within the range of endothermic fish. In order to identify the eel predators, we compared their vertical migratory behavior with those of satellite-tagged porbeagle shark and bluefin tuna, the only endothermic fishes occurring non-marginally in the Gulf of St. Lawrence. We accurately distinguished between tuna and shark by using the behavioral criteria generated by comparing the diving behavior of these two species with those of our unknown predators. Depth profile characteristics of most eel predators more closely resembled those of sharks than those of tuna. During the first days following tagging, all eels remained in surface waters and did not exhibit diel vertical migrations. Three eels were eaten at this time. Two eels exhibited inverse diel vertical migrations (at surface during the day) during several days prior to predation. Four eels were eaten during daytime, whereas the two night-predation events occurred at full moon. Although tagging itself may contribute to increasing the eel''s susceptibility to predation, we discuss evidence suggesting that predation of silver-stage American eels by porbeagle sharks may represent a significant source of mortality inside the Gulf of St. Lawrence and raises the possibility that eels may represent a reliable, predictable food resource for porbeagle sharks.     

The ecology of fear and inverted biomass pyramids

In inverted biomass pyramids (IBPs) prey are outnumbered by their predators when measured by biomass. We investigate how prey should behave in the face of danger from higher predator biomass, and how anti-predator behavior (in the form of vigilance) can, in turn, affect the predator–prey system. In this study, we incorporate anti-predator behaviors into a Lotka–Volterra predator–prey model in the form of fixed and facultative vigilance. Facultative vigilance models behavior as a dynamic foraging game, allowing us to assess optimal behavioral responses in the context of IBPs using a dynamical fitness optimization approach. We model vigilance as a tradeoff between safety and either the prey's maximum growth rate or its carrying capacity. We assess the population dynamics of predators and prey with fear responses, and investigate the role fear plays on trophic structure. We found that the ecology of fear plays an important role in predator–prey systems, impacting trophic structure and the occurrence of IBPs. Fixed vigilance works against IBP structure by always reducing the predator–prey biomass ratio at equilibrium with increasing levels of vigilance. Facultative vigilance can actually promote IBPs, as prey can now adjust their vigilance levels to cope with increased predation and the costs associated with vigilance. This is especially true when the effectiveness of vigilance is low and predators are very lethal. In general, these trends are true whether the costs of vigilance are felt on the prey's maximum growth rate or its carrying capacity. Just as the ecology of fear, when first introduced, was used to explain why top carnivores are rare in terrestrial systems, it can also be used to understand how big fierce predators can be common in IBPs.     

Partitioning mechanisms of Predator Interference in different Habitats

Prey are often consumed by multiple predator species. Predation rates on shared prey species measured in isolation often do not combine additively due to interference or facilitation among the predator species. Furthermore, the strength of predator interactions and resulting prey mortality may change with habitat type. We experimentally examined predation on amphipods in rock and algal habitats by two species of intertidal crabs, Hemigrapsus sanguineus (top predators) and Carcinus maenas (intermediate predators). Algae provided a safer habitat for amphipods when they were exposed to only a single predator species. When both predator species were present, mortality of amphipods was less than additive in both habitats. However, amphipod mortality was reduced more in rock than algal habitat because intermediate predators were less protected in rock habitat and were increasingly targeted by omnivorous top predators. We found that prey mortality in general was reduced by (1) altered foraging behavior of intermediate predators in the presence of top predators, (2) top predators switching to foraging on intermediate predators rather than shared prey, and (3) density reduction of intermediate predators. The relative importance of these three mechanisms was the same in both habitats; however, the magnitude of each was greater in rock habitat. Our study demonstrates that the strength of specific mechanisms of interference between top and intermediate predators can be quantified but cautions that these results may be habitat specific. An erratum to this article can be found at     

Does a top predator suppress the abundance of an invasive mesopredator at a continental scale?

Aim We examined evidence for the mesopredator release hypothesis at a subcontinental scale by investigating the relationship between indices of abundance of the dingo Canis lupus dingo (top‐order predator) and the invasive red fox Vulpes vulpes (mesopredator) in three large regions across mainland Australia. The red fox is known to be one of the major threats to the persistence of small and medium‐sized native vertebrates across the continent. Location Australia. Methods Indices of abundance were calculated from three independently collected datasets derived from bounty returns and field surveys. Data were analysed using univariate parametric, semi‐parametric and nonparametric techniques. Results Predator abundance indices did not conform to a normal distribution and the relationships between dingo and fox abundance indices were not well described by linear functions. Semi‐parametric and nonparametric techniques revealed consistently negative associations between indices of dingo and fox abundance. Main conclusions The results provide evidence that mesopredator suppression by a top predator can be exerted at very large geographical scales and suggest that relationships between the abundances of top predators and mesopredators are not linear. Our results have broad implications for the management of canid predators. First, they suggest that dingoes function ecologically to reduce the activity or abundance of red foxes and thus are likely to dampen the predatory impacts of foxes. More generally, they provide support for the notion that the mesopredator‐suppressive effects of top predators could be incorporated into broad‐scale biodiversity conservation programmes in many parts of the world by actively maintaining populations of top predators or restoring them in areas where they are now rare. Determining the population densities at which the interactions of top predators become ecologically effective will be a critical goal for conservation managers who aim to maintain or restore ecosystems using the ecological interactions of top predators.     

Do the antipredator strategies of shared prey mediate intraguild predation and mesopredator suppression?

Understanding the conditions that facilitate top predator effects upon mesopredators and prey is critical for predicting where these effects will be significant. Intraguild predation (IGP) and the ecology of fear are hypotheses used to describe the effects of top predators upon mesopredators and prey species, but make different assumptions about organismal space use. The IGP hypothesis predicts that mesopredator resource acquisition and risk are positively correlated, creating a fitness deficit. But if shared prey also avoid a top predator, then mesopredators may not have to choose between risk and reward. Prey life history may be a critical predictor of how shared prey respond to predation and may mediate mesopredator suppression. We used hierarchical models of species distribution and abundance to test expectations of IGP using two separate triangular relationships between a large carnivore, smaller intraguild carnivore, and shared mammalian prey with different life histories. Following IGP, we expected that a larger carnivore would suppress a smaller carnivore if the shared prey species did not spatially avoid the large carnivore at broad scales. If prey were fearful over broad scales, we expected less evidence of mesopredator suppression. We tested these theoretical hypotheses using remote camera detections across a large spatial extent. Lagomorphs did not appear to avoid coyotes, and fox detection probability was lower as coyote abundance increased. In contrast, white‐tailed deer appeared to avoid areas of increased wolf use, and coyote detection probability was not reduced at sites where wolves occurred. These findings suggest that mesopredator suppression by larger carnivores may depend upon the behavior of shared prey, specifically the spatial scale at which they perceive risk. We further discuss how extrinsic environmental factors may contribute to mesopredator suppression.     

Defensive Behavior in Primary- and Secondary-Host Generations of the Soldier-Producing Aphid, Pemphigus bursarius (Hemiptera: Aphididae)

The genus Pemphigus comprises several species that produce soldiers (defensive morphs) in galls on the primary host. At the moment, it is unclear if host-alternating species also produce defenders on their secondary host. We therefore examined how P. bursarius morphs of the secondary host generations respond to predators to test whether they show defensive behavior. We further examined how this response compares with the antipredator behavior of soldiers in P. bursarius and P. spyrothecae occurring on the primary host. We performed two manipulative experiments using two predatory species to quantify the behavior of the different morphs in response to predators. In both experiments, secondary host morphs of P. bursarius showed no attacking behavior and antipredator behavior in these morphs was limited to escaping natural enemies by walking away. In contrast, the first instars of the primary host generations in both Pemphigus species showed attacking behavior and were capable of killing the predators.     

Slow, fast and in between: habitat distribution and behaviour of larvae in nine species of libellulid dragonfly

1. Activity and microhabitat use are important factors determining species performance in habitats that differ in permanence and species composition of top predators. This study examined the relationship between the distribution across a gradient of habitat permanence and an associated transition in the composition of top predators and the behaviour of species of larval dragonflies. It also assessed the relationship between larval behaviour, body size and the duration of the larval stage. In laboratory mesocosms the mobility of the different species was measured, as was the extent to which they associated with artificial vegetation. 2. Species mobility was positively related to their natural occurrence in habitats in which invertebrates or small‐bodied fish were the top predators, and negatively related with the frequency with which species co‐existed with large‐bodied fish, the permanence of the habitat and the length of the larval stage. 3. Rather than falling into strict low and high mobility categories, habitat generalists that occurred across the habitat gradient, co‐existing with different top predators, had variable mobility levels. In these generalists, mobility was positively related to how frequently they were found in natural habitats in which invertebrates were the top predators. 4. The extent to which species utilized the artificial vegetation in mesocosms was associated with the length of the larval period but was not associated with mobility or species habitat distribution in the field.     

Estimating Trans-Seasonal Variability in Water Column Biomass for a Highly Migratory,Deep Diving Predator

The deployment of animal-borne electronic tags is revolutionizing our understanding of how pelagic species respond to their environment by providing in situ oceanographic information such as temperature, salinity, and light measurements. These tags, deployed on pelagic animals, provide data that can be used to study the ecological context of their foraging behaviour and surrounding environment. Satellite-derived measures of ocean colour reveal temporal and spatial variability of surface chlorophyll-a (a useful proxy for phytoplankton distribution). However, this information can be patchy in space and time resulting in poor correspondence with marine animal behaviour. Alternatively, light data collected by animal-borne tag sensors can be used to estimate chlorophyll-a distribution. Here, we use light level and depth data to generate a phytoplankton index that matches daily seal movements. Time-depth-light recorders (TDLRs) were deployed on 89 southern elephant seals (Mirounga leonina) over a period of 6 years (1999–2005). TDLR data were used to calculate integrated light attenuation of the top 250 m of the water column (LA₂₅₀), which provided an index of phytoplankton density at the daily scale that was concurrent with the movement and behaviour of seals throughout their entire foraging trip. These index values were consistent with typical seasonal chl-a patterns as measured from 8-daySea-viewing Wide Field-of-view Sensor (SeaWiFs) images. The availability of data recorded by the TDLRs was far greater than concurrent remotely sensed chl-a at higher latitudes and during winter months. Improving the spatial and temporal availability of phytoplankton information concurrent with animal behaviour has ecological implications for understanding the movement of deep diving predators in relation to lower trophic levels in the Southern Ocean. Light attenuation profiles recorded by animal-borne electronic tags can be used more broadly and routinely to estimate lower trophic distribution at sea in relation to deep diving predator foraging behaviour.     

被动式电子标签用于花鼠种群动态研究的可行性

在野生动物研究过程中经常需要对动物个体进行标记。传统的标记方法存在着标记物易脱落、可能影响被标记动物的生理和行为、难于进行个体识别等缺点。被动式电子标签(passive integrated transponder, PIT)是基于射频识别技术的电子标签,可用于体内标记,具有不易脱落消失且能够进行个体识别的优点。我们在凉水国家级自然保护区以PIT标签为标记物,采用标志重捕技术开展花鼠(Eutamias sibiricus)的种群动态研究,同时对应用PIT标签的可靠性进行了研究。2011年秋季至2012年春季共标记花鼠个体140只,其中86只被重捕至少1次。2011年秋季标记的72只个体中有38只在2012年春季被重捕。重捕的花鼠个体注射口愈合完好,体重无明显降低。结果表明PIT标签是一种安全可靠、识别迅速、数据准确、不易丢失、可循环使用的体内标记电子标签,适用于基于个体识别的小型哺乳动物生态学研究。     

Evaluating the effects of trophic complexity on a keystone predator by disassembling a partial intraguild predation food web

1. Many taxa can be found in food webs that differ in trophic complexity, but it is unclear how trophic complexity affects the performance of particular taxa. In pond food webs, larvae of the salamander Ambystoma opacum occupy the intermediate predator trophic position in a partial intraguild predation (IGP) food web and can function as keystone predators. Larval A. opacum are also found in simpler food webs lacking either top predators or shared prey. 2. We conducted an experiment where a partial IGP food web was simplified, and we measured the growth and survival of larval A. opacum in each set of food webs. Partial IGP food webs that had either a low abundance or high abundance of total prey were also simplified by independently removing top predators and/or shared prey. 3. Removing top predators always increased A. opacum survival, but removal of shared prey had no effect on A. opacum survival, regardless of total prey abundance. 4. Surprisingly, food web simplification had no effect on the growth of A. opacum when present in food webs with a low abundance of prey but had important effects on A. opacum growth in food webs with a high abundance of prey. Simplifying a partial IGP food web with a high abundance of prey reduced A. opacum growth when either top predators or shared prey were removed from the food web and the loss of top predators and shared prey influenced A. opacum growth in a non-additive fashion. 5. The non-additive response in A. opacum growth appears to be the result of supplemental prey availability augmenting the beneficial effects of top predators. Top predators had a beneficial effect on A. opacum populations by reducing the abundance of A. opacum present and thereby reducing the intensity of intraspecific competition. 6. Our study indicates that the effects of food web simplification on the performance of A. opacum are complex and depend on both how a partial IGP food web is simplified and how abundant prey are in the food web. These findings are important because they demonstrate how trophic complexity can create variation in the performance of intermediate predators that play important roles in temporary pond food webs.     

Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic

Tiger sharks (Galeocerdo cuvier) are a wide ranging, potentially keystone predator species that display a variety of horizontal movement patterns, making use of coastal and pelagic waters. Far less, however, is known about their vertical movements and use of the water column. We used pop‐up satellite archival tags with two data sampling rates (high rate and standard rate tags) to investigate the vertical habitat use and diving behavior of tiger sharks tagged on the Puerto Rico–Virgin Islands platform and off Bermuda between 2008 and 2009. Useable data were received from nine of 14 sharks tagged, tracked over a total of 529 days. Sharks spent the majority of their time making yo‐yo dives within the upper 50 m of the water column and considerable time within the upper 5 m of the water column. As a result, sharks typically occupied a narrow daily temperature range (~2°C). Dives to greater than 200 m were common, and all sharks made dives to at least 250 m, with one shark reaching a depth of 828 m. Despite some similarities among individuals, a great deal of intraspecific variability in vertical habit use was observed. Four distinct depth distributions that were not related to tagging location, horizontal movements, sex, or size were detected. In addition, similar depth distributions did not necessitate similar dive patterns among sharks. Recognition of intraspecific variability in habitat use of top predators can be crucial for effective management of these species and for understanding their influence on ecosystem dynamics.     

Managing predators: The influence of kangaroo rat antipredator displays on sidewinder rattlesnake hunting behavior

Upon sensing predators in their vicinity, many prey species perform antipredator displays that are thought to provide information to the predator that deters it from attacking (predator‐deterrent signals). These displays can be complex, incorporating a variety of signaling elements as well as direct physical harassment of the predator. Although the display behaviors in these communication systems are often well characterized, evidence of the efficacy of these displays in deterring predators is limited due to the challenges associated with studying free‐ranging predators. Here, we examine how the anti‐snake signals of the desert kangaroo rat (Dipodomys deserti) influence the ambush hunting behaviors of sidewinder rattlesnakes (Crotalus cerastes). We found that, although desert kangaroo rats incorporate a number of signal elements into their antipredator display, only sand kicking behavior was a significant factor in motivating sidewinder rattlesnakes to cease hunting: high rates of sand kicking led to early abandonment of ambush coils. These results indicate that anti‐snake displays of small mammals may be especially effective at mitigating the threat posed by rattlesnakes when those displays incorporate physical harassment as well as signaling.     

Physiological ecology in the 21st century: advancements in biologging science

Top pelagic predators such as tunas, sharks, marine turtlesand mammals have historically been difficult to study due totheir large body size and vast range over the oceanic habitat.In recent years the development of small microprocessor-baseddata storage tags that are surgically implanted or satellite-linkedprovide marine researchers a novel avenue for examining themovements, physiology and behaviors of pelagic animals in thewild. When biological and physical data obtained from the tagsare combined with satellite derived sea surface temperatureand ocean color data, the relationships between the movements,behaviors and physical ocean environment can be examined. Tag-bearingmarine animals can function as autonomous ocean profilers providingoceanographic data wherever their long migrations take them.The biologging science is providing ecological physiologistswith new insights into the seasonal movements, habitat utilization,breeding behaviors and population structures in of marine vertebrates.In addition, the data are revealing migration corridors, hotspots and physical oceanographic patterns that are key to understandinghow organisms such as bluefin tunas use the open ocean environment.In the 21st century as ecosystem degradation and global warmingcontinue to threaten the existence of species on Earth, thefield of physiological ecology will play a more pivotal rolein conservation biology.     

Quantifying insect predation with predator exclusion cages: the role of prey antipredator behavior as a source of bias

There are limitations imposed by current methodologies to detect and quantify insect predation. However, there has been relatively little effort to experimentally document the sources of biases associated with the various methodologies. In this study, we examined how predation estimates in the field using predator exclusion cages may be biased when one fails to account for antipredator behavioral responses. To do this, we did the usual comparison of the number of insects missing from plants where predators were allowed access to the number missing from plants where predators were excluded, but also determined how many of the missing insects reacted to predators by dropping from plants and how many were actually preyed upon. Our results provide evidence that estimates of insect mortality in the field are significantly reduced if prey antipredator behavior is taken into account. As it is commonly assumed that prey missing in the field are predated, documenting the incidence of predator‐mediated ‘disappearance’ and capturing insect prey before they escape can provide with a relevant estimate of bias.     

A novel use of passive integrated transponder (PIT) tags as nest markers

ABSTRACT.   Double-observer methodology requires independent collection of data to accurately estimate population parameters. Use of visual nest markers to facilitate matching, relocating, and monitoring nests as part of a double-observer study violates this assumption, but few reliable alternatives exist, especially when working with cryptic nests and high nest densities in homogeneous habitat. We used passive integrated transponder (PIT) tags to nonvisually mark the nests of ground-nesting birds at the Yukon Delta National Wildlife Refuge in western Alaska in a double-observer study of nest density. We marked 70 nests with PIT tags and naïve observers subsequently detected tags at 44 of 50 re-scanned nests (88% correct identification). Failed detections were likely due to either suboptimal tag orientation or tags falling through nest material, and such failures may be an inherent, but uncommon, feature of this nest-marking technique. PIT tags facilitated nest monitoring among independent observers, uniquely and reliably marked nests, provided a minimum of cues to potential nest predators, and allowed us to estimate densities in a double-observer framework while not violating assumptions. These tags should be useful in other studies of nesting birds where nonvisual, reliable nest markers are needed, and they provide a new tool for double-observer studies.     

Archival electronic tagging of a predatory sea star — Testing a new technique to study movement at the individual level

Sea stars are important marine predators, and their feeding often controls the distribution of associated species. Therefore, quantifying their activity at an individual level is important in further understanding how they structure marine communities. Sea stars are difficult to tag, so there is little information on activity of sea stars in their natural environment over extended periods of days to weeks. We tagged the New Zealand sea star Coscinasteriasmuricata with small archival electronic tags that recorded water temperate and depth every 5 min for up to 2 weeks. The tagging was undertaken to test the viability of using electronic tags in research on the ecology of the sea stars in a New Zealand fiord, where their vertical distribution is influenced by the presence of low-salinity layers. The effects of the tagging were tested in the laboratory and in the field, with tagging having no detectable influence on invitro survival, feeding rate, and righting time, or on their insitu movement and depth distribution. Laboratory experiments testing the salinity tolerance of C.muricata showed they could tolerate salinities as low as 25 PSU for at least a 20-day period. Tagging of sea stars in their natural environment provided information on depth distributions, vertical migrations and the influence of the physical environment on their behaviour. The tagging also revealed a large variation in activity at the individual level. This study represents one of the first to utilise electronic tagging to study the ecology of a mobile invertebrate such as a sea star. The success of this initial study suggests that we could gain valuable quantitative insight into the ecology of these animals in future tag deployments.