Antipredator Responses by Native Mosquitofish to Non-Native Cichlids: An Examination of the Role of Prey Naiveté

The strong impact of non-native predators in aquatic systems is thought to relate to the evolutionary naiveté of prey. Due to isolation and limited dispersal, this naiveté may be relatively high in freshwater systems. In this study, we tested this notion by examining the antipredator response of native mosquitofish, Gambusia holbrooki, to two non-native predators found in the Everglades, the African jewelfish, Hemichromis letourneuxi, and the Mayan cichlid, Cichlasoma urophthalmus. We manipulated prey naiveté by using two mosquitofish populations that varied in their experience with the recent invader, the African jewelfish, but had similar levels of experience with the longer-established Mayan cichlid. Specifically, we tested these predictions: (1) predator hunting modes differed between the two predators, (2) predation rates would be higher by the novel jewelfish predator, (3) particularly on the naive population living where jewelfish have not invaded yet, (4) antipredator responses would be stronger to Mayan cichlids due to greater experience and weaker and/or ineffective to jewelfish, and (5) especially weakest by the naive population. We assayed prey and predator behavior, and prey mortality in lab aquaria where both predators and prey were free-ranging. Predator hunting modes and habitat domains differed, with jewelfish being more active search predators that used slightly higher parts of the water column and less of the habitat structure relative to Mayan cichlids. In disagreement with our predictions, predation rates were similar between the two predators, antipredator responses were stronger to African jewelfish (except for predator inspections), and there was no difference in response between jewelfish-savvy and jewelfish-naive populations. These results suggest that despite the novelty of introduced predators, prey may be able to respond appropriately if non-native predator archetypes are similar enough to those of native predators, if prey rely on general antipredator responses or predation cues, and/or show neophobic responses.

Fight versus flight: the interaction of temperature and body size determines antipredator behaviour in tegu lizards

Ectotherm antipredator behaviour might be strongly affected both by body temperature and size: when environmental temperatures do not favour maximal locomotor performance, large individuals may confront predators, whereas small animals may flee, simply because they have no other option. However, integration of body size and temperature effects is rarely approached in the study of antipredator behaviour in vertebrate ectotherms. In the present study we investigated whether temperature affects antipredator responses of tegu lizards, Tupinambis merianae, with distinct body sizes, testing the hypothesis that small tegus (juveniles) run away from predators regardless of the environmental temperature, because defensive aggression may not be an effective predator deterrent, whereas adults, which are larger, use aggressive defence at low temperatures, when running performance might be suboptimal. We recorded responses of juvenile (small) and adult (large) tegu lizards to a simulated predatory attack at five environmental temperatures in the laboratory. Most differences between the two size classes were observed at low temperatures: large tegus were more aggressive overall than were small tegus at all temperatures tested, but at lower temperatures, the small lizards often used escape responses whereas the large ones either adopted a defensive posture or remained inactive. These results provide strong evidence that body size and temperature affect the antipredator responses of vertebrate ectotherms. We discuss the complex and intricate network of evolutionary and ecological parameters that are likely to be involved in the evolution of such interactions. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Conspecific and heterospecific alarm substance induces behavioral responses in piau fish Leporinus piau

In ostariophysan fish, the detection of alarm substance released from the skin of a conspecific or a sympatric heterospecific may elicit alarm reactions or antipredator behavioral responses. In this study, experiments were performed to characterize and quantify the behavioral response threshold of Leporinus piau, both individually and in schools, to growing dilutions of conspecific (CAS) and heterospecific skin extract (HAS). The predominant behavioral response to CAS stock stimulation was biphasic for fish held individually, with a brief initial period of rapid swimming followed by a longer period of immobility or reduced swimming activity. As the dilution of skin extract was increased, the occurrence and magnitude of the biphasic alarm response tended to decrease, replaced by a slowing of locomotion. Slowing was the most common antipredator behavior, observed in 62.5% of animals submitted to HAS stimulation. School cohesion, measured as proximity of fish to the center of the school, and swimming activity near the water surface significantly increased after exposure to CAS when compared with the control group exposed to distilled water. Histological analysis of the epidermis revealed the presence of Ostariophysi-like club cells. The presence of these cells and the behavioral responses to conspecific and heterospecific skin extract stimulation suggest the existence of a pheromone alarm system in L. piau similar to that in Ostariophysi, lending further support for the neural processing of chemosensory information in tropical freshwater fish.

Fight versus flight: the interaction of temperature and body size determines antipredator behaviour in tegu lizards

Ectotherm antipredator behaviour might be strongly affected both by body temperature and size: when environmental temperatures do not favour maximal locomotor performance, large individuals may confront predators, whereas small animals may flee, simply because they have no other option. However, integration of body size and temperature effects is rarely approached in the study of antipredator behaviour in vertebrate ectotherms. In the present study we investigated whether temperature affects antipredator responses of tegu lizards, Tupinambis merianae, with distinct body sizes, testing the hypothesis that small tegus (juveniles) run away from predators regardless of the environmental temperature, because defensive aggression may not be an effective predator deterrent, whereas adults, which are larger, use aggressive defence at low temperatures, when running performance might be suboptimal. We recorded responses of juvenile (small) and adult (large) tegu lizards to a simulated predatory attack at five environmental temperatures in the laboratory. Most differences between the two size classes were observed at low temperatures: large tegus were more aggressive overall than were small tegus at all temperatures tested, but at lower temperatures, the small lizards often used escape responses whereas the large ones either adopted a defensive posture or remained inactive. These results provide strong evidence that body size and temperature affect the antipredator responses of vertebrate ectotherms. We discuss the complex and intricate network of evolutionary and ecological parameters that are likely to be involved in the evolution of such interactions. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Cortisol influences the antipredator behavior induced by chemical alarm cues in the Frillfin goby

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Antipredator defences of young are independently determined by genetic inheritance, maternal effects and own early experience in mouthbrooding cichlids.

1. Predation is a prime force of natural selection. Vulnerability to predation is typically highest early in life, hence effective antipredator defences should work already shortly after birth. Such early defences may be innate, transmitted through non-genetic parental effects or acquired by own early experience. 2. To understand potential joint effects of these sources of antipredator defences on pheno- typic expression, they should be manipulated within the same experiment. We investigated innate, parental and individual experience effects within a single experiment. Females of the African cichlid Simochromis pleurospilus were exposed to the offspring predator Ctenochromis horei or a benign species until spawning. Eggs and larvae were hand-reared, and larvae were then exposed to odour cues signalling the presence or absence of predators in a split-brood design. 3. Shortly after independence of maternal care, S. pleurospilus undergo a habitat shift from a deeper, adult habitat to a shallow juvenile habitat, a phase where young are thought to be par- ticularly exposed to predation risk. Thus, maternal effects induced by offspring predators pres- ent in the adult habitat should take effect mainly shortly after independence, whereas own experience and innate antipredator responses should shape behaviour and life history of S. pleurospilus during the later juvenile period. 4. We found that the manipulated environmental components independently affected different offspring traits. (i) Offspring of predator-exposed mothers grew faster during the first month of life and were thus larger at termination of maternal care, when the young migrate from the adult to the juvenile habitat. (ii) The offspring’s own experience shortly after hatching exerted lasting effects on predator avoidance behaviour. (iii) Finally, our results suggest that S. pleuro- spilus possess a genetically inherited ability to distinguish dangerous from benign species. 5. In S. pleurospilus, maternal effects were limited to a short but critical time window, when young undergo a niche shift. Instead, own environmental sampling of predation risk combined with an innate predisposition to correctly identify predators appears to prepare the young best for the environment, in which they grow up as juveniles.

Multiple predator effects and native prey responses to two non-native Everglades cichlids

Non-native predators may have negative impacts on native communities, and these effects may be dependent on interactions among multiple non-native predators. Sequential invasions by predators can enhance risk for native prey. Prey have a limited ability to respond to multiple threats since appropriate responses may conflict, and interactions with recent invaders may be novel. We examined predator–prey interactions among two non-native predators, a recent invader, the African jewelfish, and the longer-established Mayan cichlid, and a native Florida Everglades prey assemblage. Using field enclosures and laboratory aquaria, we compared predatory effects and antipredator responses across five prey taxa. Total predation rates were higher for Mayan cichlids, which also targeted more prey types. The cichlid invaders had similar microhabitat use, but varied in foraging styles, with African jewelfish being more active. The three prey species that experienced predation were those that overlapped in habitat use with predators. Flagfish were consumed by both predators, while riverine grass shrimp and bluefin killifish were eaten only by Mayan cichlids. In mixed predator treatments, we saw no evidence of emergent effects, since interactions between the two cichlid predators were low. Prey responded to predator threats by altering activity but not vertical distribution. Results suggest that prey vulnerability is affected by activity and habitat domain overlap with predators and may be lower to newly invading predators, perhaps due to novelty in the interaction.

Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non-consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non-native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non-native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non-consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non-native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter-related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non-native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non-native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.

Black sea urchins evaluate predation risk using chemical signals from a predator and injured con- and heterospecific prey

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)

Effects of ocean acidification on visual risk assessment in coral reef fishes

1. With the global increase in CO2 emissions, there is a pressing need for studies aimed at understanding the effects of ocean acidification on marine ecosystems. Several studies have reported that exposure to CO2 impairs chemosensory responses of juvenile coral reef fishes to predators. Moreover, one recent study pointed to impaired responses of reef fish to auditory cues that indicate risky locations. These studies suggest that altered behaviour following exposure to elevated CO2 is caused by a systemic effect at the neural level. 2. The goal of our experiment was to test whether juvenile damselfish Pomacentrus amboinensis exposed to different levels of CO2 would respond differently to a potential threat, the sight of a large novel coral reef fish, a spiny chromis, Acanthochromis polyancanthus, placed in a watertight bag. 3. Juvenile damselfish exposed to 440 (current day control), 550 or 700 µatm CO2 did not differ in their response to the chromis. However, fish exposed to 850 µatm showed reduced antipredator responses; they failed to show the same reduction in foraging, activity and area use in response to the chromis. Moreover, they moved closer to the chromis and lacked any bobbing behaviour typically displayed by juvenile damselfishes in threatening situations. 4. Our results are the first to suggest that response to visual cues of risk may be impaired by CO2 and provide strong evidence that the multi-sensory effects of CO2 may stem from systematic effects at the neural level.

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO2 predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO2 effects, whereby some individuals are unaffected at particular CO2 concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO2 (current day levels) or 850 µatm CO2, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO2 failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO2 fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO2 exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO2 exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO2-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO2 may alter the cognitive ability of juvenile fish and render learning ineffective.

The `club` cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia

The alarm response to skin extract has been well documented in fish. In response to skin extract, there is a decline in both locomotion activity and aggressive interactions. Our observation herein of these responses in the cichlid Nile tilapia, Oreochromis niloticus, confirmed the existence of the alarm response in this species. However, so far there has been a paucity of information on the autonomic correlates of this response. In this study, the ventilatory change in response to the chemical alarm cue was evaluated. This parameter was measured 4 min before and 4 min after exposure to 1 mL of either conspecific skin extract or distilled water (extract vehicle). Skin extract induced an increase in the ventilation rate, which suggested an anticipatory adjustment to potentially harmful stimuli. The chemical cue (alarm substance) also interfered with the prioritisation of responses to different environmental stimuli (stimuli filtering); this was suggested by the observation that the Nile tilapia declined to fight after exposure to a cue that indicates a risk of predation. Furthermore, histological analysis of the Nile tilapia skin revealed the presence of putative alarm substance-producing (club) cells.

Effects of algal turbidity on foraging and antipredator behaviour of the three-spined stickleback (Gasterosteus aculeatus)

The aim of this thesis was to examine how aquatic organisms, such as fish, behave in an altered environmental condition. Many species of fish use vision as their primary tool to gain information about their surrounding environment. The visual conditions of aquatic habitats are often altered as a result of anthropogenic disturbance, such as eutrophication that initiates algal turbidity. In general, turbidity reduces the visibility and can be hypothesized to have an influence on the behaviour of fish. I used the three-spined stickleback (Gasterosteus aculeatus) as a model species and conducted four studies in the laboratory to test how algal turbidity affects its behaviour. In this thesis, two major behavioural aspects are discussed. The first is antipredator behaviour. In study I, the combined effects of turbidity and shoot density on habitat choice (shelter vs open) behaviour was tested on a group of sticklebacks (20 fish) in the presence and absence of piscivorous perch (Perca fluviatilis). In study II, I examined the behavioural responses of feeding sticklebacks when they were exposed to the sudden appearance of an avian predator (the silhouette of a common tern, Sterna hirundo). The study was done in turbid and clear water using three different groups sizes (1, 3 and 6 fish). The second aspect is foraging behaviour. Study III & IV focused on the effects of algal turbidity on the foraging performance of sticklebacks. In study III, I conducted two separate experiments to examine the effects of turbidity on prey consumption and prey choice of sticklebacks. In this experiment turbidity levels and the proportion of large and small prey (Daphnia spp.) were manipulated. In study IV, I studied whether a group of six sticklebacks can distribute themselves according to food input at two feeding stations in a way that provided each fish with the same amount of food in clear and turbid water. I also observed whether the fish can follow changes in resource distribution between the foraging patches. My results indicate an overall influence of algal turbidity on the antipredator and foraging behaviour of sticklebacks. In the presence of a potential predator, the use of the sheltered habitat was more pronounced at higher turbidity. Besides this, sticklebacks reduced their activity levels with predator presence at higher turbidity and shoot density levels, suggesting a possible antipredator adaptation to avoid a predator. When exposed to a sudden appearance of an avian predator, sticklebacks showed a weaker antipredator response in turbid water, which suggests that turbidity degrades the risk assessment capabilities of sticklebacks. I found an effect of group size but not turbidity in the proportion of sticklebacks that fled to the shelter area, which indicates that sticklebacks are able to communicate among group members at the experimental turbidity levels. I found an overall negative effect of turbidity on food intake. Both turbidity and changes in the proportion of prey sizes played a significant role in a stickleback’s prey selection. At lower turbidity levels (clear <1 and 5 NTU) sticklebacks showed preferences for large prey, whereas in more turbid conditions and when the proportion of large to small prey increased sticklebacks became increasingly random in their prey selection. Finally, my results showed that groups of sticklebacks disperse themselves between feeding stations according to the reward ratios following the predictions of the ideal free distribution theory. However, they took a significantly longer time to reach the equilibrium distribution in turbid water than in clear water. In addition, they showed a slower response to changes in resource distribution in a turbid environment. These findings suggest that turbidity interferes with the information transfer among group foragers. It is important to understand that aquatic animals are often exposed to a degraded environment. The findings of this thesis suggest that algal turbidity negatively affects their behavioural performance. The results also shed light on the underlying behavioural strategies of sticklebacks in turbid conditions that might help them adapt to an altered environmental situation and increase their survival. In conclusion, I hold that although algal turbidity has detrimental effects on the antipredator and foraging behaviour of sticklebacks, their behavioural adjustment might help them adapt to a changing environment.

New Perspectives on beta-Adrenergic Mediation of Innate and Learned Fear Responses to Predator Odor

In the present study, we investigated the role of noradrenergic transmission in unconditioned and conditioned responses to predatory threats. First, we examined the effects of systemically injected beta-blockers on unconditioned and contextual conditioned response to cat odor. The centrally acting beta-blocker (propranolol) was able to impair unconditioned responses, as well as the acquisition of the contextual fear to cat odor; however, the peripherally acting (nadolol) was not effective. Next, we examined the neural substrate underlying the noradrenergic modulation of the defensive response to cat odor and focused on the dorsal premammillary nucleus (PMd), because it represents the hypothalamic site most responsive to predatory threats and, at the same time, presents a dense plexus of noradrenergic fibers. We were able to see that propranolol significantly reduced PMd-Fos expression in response to cat odor and that beta-adrenoceptor blockade in the PMd, before cat odor exposure, reduced defensive responses to the cat odor and to the cat odor-related environment. We have also shown that beta-adrenoceptor blockade in the PMd, before the exposure to cat odor-related context, impaired the contextual conditioned responses. Overall, the present results provide convincing evidence suggesting that central noradrenergic mediation is critical for the expression of unconditioned and contextual conditioned antipredatory responses. We have further shown that the PMd appears to be an important locus to mediate these beta-adrenoceptor effects.

Physical environment modulates the behavioral responses induced by chemical stimulation of dorsal periaqueductal gray in mice

In order to investigate the relationship between behaviors elicited by chemical stimulation of the dorsal periaqueductal gray (dorsal PAG) and spontaneous defensive behaviors to a predator, the excitatory amino acid D,L-homocysteic acid (5 nmol in 0.1 mu l), was infused into the dorsal PAG and behavioral responses of mice were evaluated in two different situations, a rectangular novel chamber or the Mouse Defense Test Battery (MDTB) apparatus. During a 1-min period following drug infusion, more jumps were made in the chamber than in the MDTB runway but running time and distance traveled were significantly higher in the runway. Animals were subsequently tested using the standard MDTB procedure (anti-predator avoidance, chase and defensive threat/attack). No drug effects on these measures were significant. In a further test in the MDTB apparatus, the pathway of the mouse during peak locomotion response was blocked 3 times by the predator stimulus (anesthetized rat) to determine if the mouse would avoid contact. Ninety percent of D,L-homocysteic treated animals made direct contact with the stimulus (rat), indicating that D,L-homocysteic-induced running is not guided by relevant (here, threat) stimuli. These results indicate that running as opposed to jumping is the primary response in mice injected with D,L-homocysteic into the dorsal PAG when the environment enables flight. However, the lack of responsivity to the predator during peak locomotion suggests that D,L-homocysteic-stimulation into the dorsal PAG does not induce normal antipredator flight. (c) 2006 Published by Elsevier B.V.