Predation-risk effects of predator identity on the foraging behaviors of frugivorous bats

Predators directly and indirectly affect the density and the behavior of prey. These effects may potentially cascade down to lower trophic levels. In this study, we tested the effects of predator calls (playbacks of bird vocalizations: Tyto alba, Speotyto cunicularia, and Vanellus chilensis), predator visual stimuli (stuffed birds) and interactions of visual and auditory cues, on the behavior of frugivore phyllostomid bats in the field. In addition, we tested if the effects of predation risk cascade down to other trophic levels by measuring rates of seed dispersal of the tree Muntingia calabura. Using video recording, we found that bats significantly decreased the foraging frequency on trees when a visual cue of T. alba was present. However, no stimuli of potential predatory birds, including vocalization of T. alba, affected bat foraging frequency. There was a change in bat behavior during 7 min, but then their frequency of activity gradually increased. Consequently, the presence of T. alba decreased by up to ten times the rate of seed removal. These results indicate that risk sensitivity of frugivorous phyllostomid bats depends on predator identity and presence. Among the predators used in this study, only T. alba is an effective bat predator in the Neotropics. Sound stimuli of T. alba seem not to be a cue of predation risk, possibly because their vocalizations are used only for intraspecific communication. This study emphasizes the importance of evaluating different predator stimuli on the behavior of vertebrates, as well as the effects of these stimuli on trait-mediated trophic cascades. © 2013 Springer-Verlag Berlin Heidelberg.

Cytotoxic effects of neem oil in the midgut of the predator Ceraeochrysa claveri

Studies of morphological and ultrastructural alterations in target organs have been useful for evaluating the sublethal effects of biopesticides regarded as safe for non-target organisms in ecotoxicological analyses. One of the most widely used biopesticides is neem oil, and its safety and compatibility with natural enemies have been further clarified through bioassays performed to analyze the effects of indirect exposure by the intake of poisoned prey. Thus, this study examined the cellular response of midgut epithelial cells of the adult lacewing, Ceraeochrysa claveri, to neem oil exposure via intake of neem oil-contaminated prey during the larval stage. C. claveri larvae were fed Diatraea saccharalis eggs treated with neem oil at concentrations of 0.5%, 1% and 2% throughout the larval stage. The adult females obtained from these treatments were used at two ages (newly emerged and at the start of oviposition) in morphological and ultrastructural analyses. Neem oil was found to cause pronounced cytotoxic effects in the adult midgut, such as cell dilation, emission of cytoplasmic protrusions, cell lysis, loss of integrity of the cell cortex, dilation of cisternae of the rough endoplasmic reticulum, swollen mitochondria, vesiculated appearance of the Golgi complex and dilated invaginations of the basal labyrinth. Epithelial cells responded to those injuries with various cytoprotective and detoxification mechanisms, including increases in cell proliferation, the number of calcium-containing cytoplasmic granules, and HSP 70 expression, autophagic processes and the development of smooth endoplasmic reticulum, but these mechanisms were insufficient for recovery from all of the cellular damage to the midgut. This study demonstrates that neem oil exposure impairs the midgut by causing sublethal effects that may affect the physiological functions of this organ, indicating the importance of studies of different life stages of this species and similar species to evaluate the safe and compatible integrated use of biopesticides.

Provisioning Strategies of Antarctic Fur Seals and Chinstrap Penguins Produce Different Responses to Distribution of Common Prey and Habitat

Central-place foragers that must return to a breeding site to deliver food to offspring are faced with trade-offs between prey patch quality and distance from the colony. Among colonial animals, pinnipeds and seabirds may have different provisioning strategies, due to differences in their ability to travel and store energy. We compared the foraging areas of lactating Antarctic fur seals and chinstrap penguins breeding at Seal Island, Antarctica, to investigate whether they responded differently to the distribution of their prey (Antarctic krill and myctophid fish) and spatial heterogeneity in their habitat. Dense krill concentrations occurred in the shelf region near the colony. However, only brooding penguins, which are expected to be time-minimizers because they must return frequently with whole food for their chicks, foraged mainly in this proximal shelf region. Lactating fur seals and incubating penguins, which can make longer trips to increase energy gain per trip, and so are expected to be energy-maximizers, foraged in the more distant (>20 km from the island) slope and oceanic regions. The shelf region was characterized by more abundant, but lower-energy-content immature krill, whereas the slope and oceanic regions had less abundant but higher-energy-content gravid krill, as well as high-energy-content myctophids. Furthermore, krill in the shelf region undertook diurnal vertical migration, whereas those in the slope and oceanic regions stayed near the surface throughout the day, which may enhance the capture rate for visual predators. Therefore, we sug- gest that the energy-maximizers foraged in distant, but potentially more profitable feeding regions, while the time-minimizers foraged in closer, but potentially less profitable regions. Thus, time and energy constraints derived from different provisioning strategies may result in sympatric colonial predator species using different foraging areas, and as a result, some central-place foragers use sub- optimal foraging habitats, in terms of the quality or quantity of available prey.

Population Growth of Antarctic Fur Seals: Limitation by a Top Predator, The Leopard Seal?

Antarctic fur seals (Arctocephalus gazella) in the South Shetland Islands are recovering from 19th-century exploitation more slowly than the main population at South Georgia. To document demographic changes associated with the recovery in the South Shetlands, we monitored fur seal abundance and reproduction in the vicinity of Elephant Island during austral summers from 1986/1987 through 1994/1995. Total births, mean and variance of birth dates, and average daily mortality rates were estimated from daily live pup counts at North Cove (NC) and North Annex (NA) colonies on Seal Island. Sightings of leopard seals (Hydrurga leptonyx) and incidents of leopard seal predation on fur seal pups were recorded opportunistically during daily fur seal research at both sites. High mortality of fur seal pups, attributed to predation by leopard seals frequently observed at NC, caused pup numbers to decline rapidly between January and March (i.e., prior to weaning) each year and probably caused a long-term decline in the size of that colony. The NA colony, where leopard seals were never observed, increased in size during the study. Pup mortality from causes other than leopard seal predation appeared to be similar at the two sites. The number of pups counted at four locations in the Elephant Island vicinity increased slowly, at an annual rate of 3.8%, compared to rates as high as 11% at other locations in the South Shetland Islands. Several lines of circumstantial evidence are consistent with the hypothesis that leopard seal predators limit the growth of the fur seal population in the Elephant Island area and perhaps in the broader population in the South Shetland Islands. The sustained growth of this fur seal population over many decades rules out certain predator–prey models, allowing inference about the interaction between leopard seals and fur seals even though it is less thoroughly studied than predator–prey systems of terrestrial vertebrates of the northern hemisphere. Top-down forces should be included in hypotheses for future research on the factors shaping the recovery of the fur seal population in the South Shetland Islands.

Using occupancy models to investigate space partitioning between two sympatric large predators, the jaguar and puma in central Brazil

Coexistence of sympatric species is mediated by resource partitioning. Pumas occur sympatrically with jaguars throughout most of the jaguar's range but few studies have investigated space partitioning between both species. Here, camera trapping and occupancy models accounting for imperfect detection were employed in a Bayesian framework to investigate space partitioning between the jaguar and puma in Emas National Park (ENP), central Brazil. Jaguars were estimated to occupy 54.1% and pumas 39.3% of the sample sites. Jaguar occupancy was negatively correlated with distance to water and positively correlated with the amount of dense habitat surrounding the camera trap. Puma occupancy only showed a weak negative correlation with distance to water and with jaguar presence. Both species were less often present at the same site than expected under independent distributions. Jaguars had a significantly higher detection probability at cameras on roads than at off-road locations. For pumas, detection was similar on and off-road. Results indicate that both differences in habitat use and active avoidance shape space partitioning between jaguars and pumas in ENP. Considering its size, the jaguar is likely the competitively dominant of the two species. Owing to its habitat preferences, suitable jaguar habitat outside the park is probably sparse. Consequently, the jaguar population is likely largely confined to the park, while the puma population is known to extend into ENP's surroundings. (C) 2011 Deutsche Gesellschaft fur Saugetierkunde. Published by Elsevier GmbH. All rights reserved.

Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters

Studies of consumer-resource interactions suggest that individual diet specialisation is empirically widespread and theoretically important to the organisation and dynamics of populations and communities. We used weighted networks to analyze the resource use by sea otters, testing three alternative models for how individual diet specialisation may arise. As expected, individual specialisation was absent when otter density was low, but increased at high-otter density. A high-density emergence of nested resource-use networks was consistent with the model assuming individuals share preference ranks. However, a density-dependent emergence of a non-nested modular network for core resources was more consistent with the competitive refuge model. Individuals from different diet modules showed predictable variation in rank-order prey preferences and handling times of core resources, further supporting the competitive refuge model. Our findings support a hierarchical organisation of diet specialisation and suggest individual use of core and marginal resources may be driven by different selective pressures.

Anti-Aversive Effects of Cannabidiol on Innate Fear-Induced Behaviors Evoked by an Ethological Model of Panic Attacks Based on a Prey vs the Wild Snake Epicrates cenchria crassus Confrontation Paradigm

Several pharmacological targets have been proposed as modulators of panic-like reactions. However, interest should be given to other potential therapeutic neurochemical agents. Recent attention has been given to the potential anxiolytic properties of cannabidiol, because of its complex actions on the endocannabinoid system together with its effects on other neurotransmitter systems. The aim of this study was to investigate the effects of cannabidiol on innate fear-related behaviors evoked by a prey vs predator paradigm. Male Swiss mice were submitted to habituation in an arena containing a burrow and subsequently pre-treated with intraperitoneal administrations of vehicle or cannabidiol. A constrictor snake was placed inside the arena, and defensive and non-defensive behaviors were recorded. Cannabidiol caused a clear anti-aversive effect, decreasing explosive escape and defensive immobility behaviors outside and inside the burrow. These results show that cannabidiol modulates defensive behaviors evoked by the presence of threatening stimuli, even in a potentially safe environment following a fear response, suggesting a panicolytic effect. Neuropsychopharmacology (2012) 37, 412-421; doi:10.1038/npp.2011.188; published online 14 September 2011

Prey digestion in the midgut of the predatory bug Podisus nigrispinus (Hemiptera: Pentatomidae)

Pre-oral digestion is described as the liquefaction of the solid tissues of the prey by secretions of the predator. It is uncertain if pre-oral digestion means pre-oral dispersion of food or true digestion in the sense of the stepwise bond breaking of food polymers to release monomers to be absorbed. Collagenase is the only salivary proteinase, which activity is significant (10%) in relation to Podisus nigrispinus midgut activities. This suggests that pre-oral digestion in P. nigrispinus consists in prey tissue dispersion. This was confirmed by the finding of prey muscles fibers inside P. nigrispinus midguts. Soluble midgut hydrolases from P. nigrispinus were partially purified by ion-exchange chromatography, followed by gel filtration. Two cathepsin L-like proteinases (CAL1 and CAL2) were isolated with the properties: CAL1 (14.7 kDa, pH optimum (pHo) 5.5, km with carbobenzoxy-Phe-Arg-methylcoumarin, Z-FR-MCA, 32 mu M); CAL2 (17 kDa, pHo 5.5, km 11 mu M Z-FR-MCA). Only a single molecular species was found for the other enzymes with the following properties are: amylase (43 kDa, pHo 5.5, km 0.1% starch), aminopeptidase (125 kDa, pHo 5.5, km 0.11 mM L-Leucine-p-nitroanilide), alpha-glucosidase (90 kDa, pHo 5.0, km 5 mM with p-nitrophenyl alpha-D-glucoside). CAL molecular masses are probably underestimated due to interaction with the column. Taking into account the distribution of hydrolases along P. nigrispinus midguts, carbohydrate digestion takes place mainly at the anterior midgut, whereas protein digestion occurs mostly in middle and posterior midgut, as previously described in seed- sucker and blood-feeder hemipterans. (C) 2012 Elsevier Ltd. All rights reserved.

What ethologically based models have taught us about the neural systems underlying fear and anxiety

Classical Pavlovian fear conditioning to painful stimuli has provided the generally accepted view of a core system centered in the central amygdala to organize fear responses. Ethologically based models using other sources of threat likely to be expected in a natural environment, such as predators or aggressive dominant conspecifics, have challenged this concept of a unitary core circuit for fear processing. We discuss here what the ethologically based models have told us about the neural systems organizing fear responses. We explored the concept that parallel paths process different classes of threats, and that these different paths influence distinct regions in the periaqueductal gray - a critical element for the organization of all kinds of fear responses. Despite this parallel processing of different kinds of threats, we have discussed an interesting emerging view that common cortical-hippocampal-amygdalar paths seem to be engaged in fear conditioning to painful stimuli, to predators and, perhaps, to aggressive dominant conspecifics as well. Overall, the aim of this review is to bring into focus a more global and comprehensive view of the systems organizing fear responses.

The loss of indirect interactions leads to cascading extinctions of carnivores

Species extinctions are biased towards higher trophic levels, and primary extinctions are often followed by unexpected secondary extinctions. Currently, predictions on the vulnerability of ecological communities to extinction cascades are based on models that focus on bottom-up effects, which cannot capture the effects of extinctions at higher trophic levels. We show, in experimental insect communities, that harvesting of single carnivorous parasitoid species led to a significant increase in extinction rate of other parasitoid species, separated by four trophic links. Harvesting resulted in the release of prey from top-down control, leading to increased interspecific competition at the herbivore trophic level. This resulted in increased extinction rates of non-harvested parasitoid species when their host had become rare relative to other herbivores. The results demonstrate a mechanism for horizontal extinction cascades, and illustrate that altering the relationship between a predator and its prey can cause wide-ranging ripple effects through ecosystems, including unexpected extinctions.

Chapter Six – Individual Trait Variation and Diversity in Food Webs

In recent years, there has been a renewed interest in the ecological consequences of individual trait variation within populations. Given that individual variability arises from evolutionary dynamics, to fully understand eco-evolutionary feedback loops, we need to pay special attention to how standing trait variability affects ecological dynamics. There is mounting empirical evidence that intra-specific phenotypic variation can exceed species-level means, but theoretical models of multi-trophic species coexistence typically neglect individual-level trait variability. What is needed are multispecies datasets that are resolved at the individual level that can be used to discriminate among alternative models of resource selection and species coexistence in food webs. Here, using one the largest individual-based datasets of a food web compiled to date, along with an individual trait-based stochastic model that incorporates Approximate Bayesian computation methods, we document intra-population variation in the strength of prey selection by different classes or predator phenotypes which could potentially alter the diversity and coexistence patterns of food webs. In particular, we found that strongly connected individual predators preferentially consumed common prey, whereas weakly connected predators preferentially selected rare prey. Such patterns suggest that food web diversity may be governed by the distribution of predator connectivity and individual trait variation in prey selection. We discuss the consequences of intra-specific variation in prey selection to assess fitness differences among predator classes (or phenotypes) and track longer term food web patterns of coexistence accounting for several phenotypes within each prey and predator species.

9-28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse(Ctenolabrus rupestris)

Most studies on the impact of near-future levels of carbon dioxide on fish behaviour report behavioural alterations, wherefore abnormal behaviour has been suggested to be a potential consequence of future ocean acidification and therefore a threat to ocean ecosystems. However, an increasing number of studies show tolerance of fish to increased levels of carbon dioxide. This variation among studies in susceptibility highlights the importance of continued investigation of the possible effects of elevated pCO2. Here, we investigated the impacts of increased levels of carbon dioxide on behaviour using the goldsinny wrasse (Ctenolabrus rupestris), which is a common species in European coastal waters and widely used as cleaner fish to control sea lice infestation in commercial fish farming in Europe. The wrasses were exposed to control water conditions (370 µatm) or elevated pCO2 (995 µatm) for 1 month, during which time behavioural trials were performed. We investigated the possible effects of CO2 on behavioural lateralization, swimming activity, and prey and predator olfactory preferences, all behaviours where disturbances have previously been reported in other fish species after exposure to elevated CO2. Interestingly, we failed to detect effects of carbon dioxide for most behaviours investigated, excluding predator olfactory cue avoidance, where control fish initially avoided predator cue while the high CO2 group was indifferent. The present study therefore shows behavioural tolerance to increased levels of carbon dioxide in the goldsinny wrasse. We also highlight that individual fish can show disturbance in specific behaviours while being apparently unaffected by elevated pCO2 in other behavioural tests. However, using experiments with exposure times measured in weeks to predict possible effects of long-term drivers, such as ocean acidification, has limitations, and the behavioural effects from elevated pCO2 in this experiment cannot be viewed as proof that these fish would show the same reaction after decades of evolution.

The contribution of trait-mediated indirect effects to the net effects of a predator

Many prey modify traits in response to predation risk and this modification of traits can influence the prey's resource acquisition rate. A predator thus can have a “nonlethal” impact on prey that can lead to indirect effects on other community members. Such indirect interactions are termed trait-mediated indirect interactions because they arise from a predator's influence on prey traits, rather than prey density. Because such nonlethal predator effects are immediate, can influence the entire prey population, and can occur over the entire prey lifetime, we argue that nonlethal predator effects are likely to contribute strongly to the net indirect effects of predators (i.e., nonlethal effects may be comparable in magnitude to those resulting from killing prey). This prediction was supported by an experiment in which the indirect effects of a larval dragonfly (Anax sp.) predator on large bullfrog tadpoles (Rana catesbeiana), through nonlethal effects on competing small bullfrog tadpoles, were large relative to indirect effects caused by density reduction of the small tadpoles (the lethal effect). Treatments in which lethal and nonlethal effects of Anax were manipulated independently indicated that this result was robust for a large range of different combinations of lethal and nonlethal effects. Because many, if not most, prey modify traits in response to predators, our results suggest that the magnitude of interaction coefficients between two species may often be dynamically related to changes in other community members, and that many indirect effects previously attributed to the lethal effects of predators may instead be due to shifts in traits of surviving prey.

Dinâmica de interações intraguilda em Chrysoperla externa (Neuroptera: Chrysopidae), Harmonia axyridis (Coleoptera: Coccinellidae) com Diaphorina citri (Hemiptera: Psyllidae)

A necessidade por recursos alimentares move os insetos predadores na busca por presas, para garantir a sobrevivência. Existem vários fatores que podem influenciar o comportamento de busca e escolha por presas e, sob determinadas circunstâncias, o inseto pode escolher se alimentar de presas não alvo, como, por exemplo, inimigos naturais e assim prejudicar a população de organismos benéficos. Garantir a estabilidade do agroecossistema é uma forma de manter as populações de pragas em níveis compatíveis com a ação de inimigos naturais e, consequentemente obter o sucesso no controle biológico. Programas bem sucedidos de manejo de pragas requerem previamente a realização de estudos sobre comportamento de insetos. Com o intuito de compreender os fatores que governam o comportamento predatório e as interações ecológicas entre Harmonia axyridis e Chrysoperla externa, considerando a presença de Diaphorina citri como presa, objetivou-se estudar o efeito de interações intraguilda sobre a predação de D. citri, experimentalmente e utilizando modelos estatísticos para compreender a dinâmica de interações tróficas no contexto de potenciais guildas presentes em citros. Três experimentos distintos foram realizados para investigar o comportamento dos insetos predadores. Foram realizados testes com escolha entre larvas dos predadores C. externa e H. axyridis e testes com e sem escolha comparando machos e fêmeas do predador H. axyridis, a fim de investigar padrões de escolha de presas. O segundo experimento foi realizado para investigar o comportamento predatório entre larvas de segundo instar dos predadores sob diferentes densidades de D. citri como presa. As combinações foram: sem escolha de presas intraguilda, combinações com escolha de presas intraguilda e combinações com a presença de dois predadores da mesma espécie para possibilitar o canibalismo. As densidades de D. citri utilizadas foram 5, 10, 15, 30, 60, 80. No último experimento avaliou-se a interação entre larvas de C. externa e H. axyridis, ao longo do desenvolvimento, simulando a existência de apenas uma presa, como fonte de alimento. O desenvolvimento dos predadores foi avaliado e comparado utilizando-se duas presas diferentes, ninfas de D. citri e ovos de Ephestia kuehniella para cada larva de primeiro instar dos predadores C. externa e H. axyridis. As combinações de predadores foram as mesmas citadas no experimento anterior. Observou-se a duração do desenvolvimento larval nas diferentes combinações de predadores e presa, bem como o percentual de predações intraguilda e canibalismos ocorridos. Nem a densidade de presas, nem o tipo de presa ofertada influenciou o comportamento das larvas dos predadores para a realização de predação intraguilda ou canibalismo. O principal fator foi a diferença de idade que reflete no tamanho dos predadores, podendo direcionar a predação intraguilda ou o canibalismo e até mesmo acelerar o ciclo de desenvolvimento do predador intraguilda envolvido. Predadores em estágio inicial de vida buscaram por qualquer tipo de presa para garantir sua sobrevivência, não demonstrando qualquer padrão em suas escolhas. No caso dos adultos de H. axyridis, há diferença de comportamento entre os sexos, dependendo da densidade de presas disponíveis, fêmeas poderão ser mais ágeis na busca e consumo de presas.

Predator-specific changes in the morphology and swimming performance of larval Rana lessonae

1. We investigated the morphological responses of larval Rana lessonae to the presence of two predators with substantially different prey-detection and capture techniques; larval dragonflies (Aeshna cyanea) and the Pumpkinseed Sunfish (Lepomis gibossus). 2. We also examined the functional implications of any predator-induced morphological variation on their swimming ability by assessing performance during the initial stages of a startle response. 3. We found the morphological responses of larval R. lessonae were dependent on the specific predator present. Tadpoles raised in the presence of dragonfly larvae preying upon conspecific tadpoles developed total tail heights 5.4% deeper and tail muscles 4.7% shallower than tadpoles raised in a non-predator environment, while tadpoles raised with sunfish possessed tails 2% shallower and tail muscles 2.5% higher than non-predator-exposed tadpoles. 4. Predator-induced morphological variation also significantly influenced swimming performance. Tadpoles raised with sunfish possessed swimming speeds 9.5 and 14.6% higher than non- and dragonfly predator groups, respectively. 5. Thus, the expression of these alternative predator-morphs leads to a functional trade-off in performance between the different environments.