Oona M. Lönnstedt

Putting prey and predator into the CO2 equation – qualitative and quantitative effects of ocean acidification on predator–prey interactions

Little is known about the impact of ocean acidification on predator-prey dynamics. Herein, we examined the effect of carbon dioxide (CO(2)) on both prey and predator by letting one predatory reef fish interact for 24 h with eight small or large juvenile damselfishes from four congeneric species. Both prey and predator were exposed to control or elevated levels of CO(2). Mortality rate and predator selectivity were compared across CO(2) treatments, prey size and species. Small juveniles of all species sustained greater mortality at high CO(2) levels, while large recruits were not affected. For large prey, the pattern of prey selectivity by predators was reversed under elevated CO(2). Our results demonstrate both quantitative and qualitative consumptive effects of CO(2) on small and larger damselfish recruits respectively, resulting from CO(2)-induced behavioural changes likely mediated by impaired neurological function. This study highlights the complexity of predicting the effects of climate change on coral reef ecosystems.

Learn and live: predator experience and feeding history determines prey behaviour and survival

Determining how prey learn the identity of predators and match their vigilance with current levels of threat is central to understanding the dynamics of predator–prey systems and the determinants of fitness. Our study explores how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and survival in the field for a juvenile coral reef damselfish. We collected young fish immediately prior to their settlement to benthic habitats. In the laboratory, these predator-naïve fish were exposed to a high- or low-food ration and then conditioned to recognize the olfactory cues (odours) and/or visual cues from two common benthic predators. Fish were then allowed to settle on reefs in the field, and their behaviour and survival over 70 h were recorded. Feeding history strongly influenced their willingness to take risks in the natural environment. Conditioning in the laboratory with visual, olfactory or both cues from predators led fish in the field to display risk-averse behaviour compared with fish conditioned with sea water alone. Well-fed fish that were conditioned with visual, chemical or a combination of predator cues survived eight times better over the first 48 h on reefs than those with no experience of benthic predator cues. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.

Environmentally relevant concentrations of microplastic particles influence larval fish ecology

Microplastics triple threat The billions of tons of plastics that we release into the environment for the most part do not biodegrade. But they do degrade, breaking into ever smaller particles that end up in the oceans. Lönnstedt et al. show that the impacts of these microplastics are multifold (see the Perspective by Rochman). Eurasian perch larvae exposed to microplastics were less active, less responsive to predator cues, more likely to be eaten, and less likely to thrive—preferring to eat plastic rather than their natural prey. Science, this issue p. 1213; see also p. 1172 Microplastics alter the behavior and reduce the survival and growth of European perch. The widespread occurrence and accumulation of plastic waste in the environment have become a growing global concern over the past decade. Although some marine organisms have been shown to ingest plastic, few studies have investigated the ecological effects of plastic waste on animals. Here we show that exposure to environmentally relevant concentrations of microplastic polystyrene particles (90 micrometers) inhibits hatching, decreases growth rates, and alters feeding preferences and innate behaviors of European perch (Perca fluviatilis) larvae. Furthermore, individuals exposed to microplastics do not respond to olfactory threat cues, which greatly increases predator-induced mortality rates. Our results demonstrate that microplastic particles operate both chemically and physically on larval fish performance and development.

Reassessing the trophic role of reef sharks as apex predators on coral reefs

Apex predators often have strong top-down effects on ecosystem components and are therefore a priority for conservation and management. Due to their large size and conspicuous predatory behaviour, reef sharks are typically assumed to be apex predators, but their functional role is yet to be confirmed. In this study, we used stomach contents and stable isotopes to estimate diet, trophic position and carbon sources for three common species of reef shark (Triaenodon obesus, Carcharhinus melanopterus and C. amblyrhynchos) from the Great Barrier Reef (Australia) and evaluated their assumed functional role as apex predators by qualitative and quantitative comparisons with other sharks and large predatory fishes. We found that reef sharks do not occupy the apex of coral reef food chains, but instead have functional roles similar to those of large predatory fishes such as snappers, emperors and groupers, which are typically regarded as high-level mesopredators. We hypothesise that a degree of functional redundancy exists within this guild of predators, potentially explaining why shark-induced trophic cascades are rare or subtle in coral reef ecosystems. We also found that reef sharks participate in multiple food webs (pelagic and benthic) and are sustained by multiple sources of primary production. We conclude that large conspicuous predators, be they elasmobranchs or any other taxon, should not axiomatically be regarded as apex predators without thorough analysis of their diet. In the case of reef sharks, our dietary analyses suggest they should be reassigned to an alternative trophic group such as high-level mesopredators. This change will facilitate improved understanding of how reef communities function and how removal of predators (e.g., via fishing) might affect ecosystem properties.

Degraded environments alter prey risk assessment.

Elevated water temperatures, a decrease in ocean pH, and an increasing prevalence of severe storms have lead to bleaching and death of the hard corals that underpin coral reef ecosystems. As coral cover declines, fish diversity and abundance declines. How degradation of coral reefs affects behavior of reef inhabitants is unknown. Here, we demonstrate that risk assessment behaviors of prey are severely affected by coral degradation. Juvenile damselfish were exposed to visual and olfactory indicators of predation risk in healthy live, thermally bleached, and dead coral in a series of laboratory and field experiments. While fish still responded to visual cues in all habitats, they did not respond to olfactory indicators of risk in dead coral habitats, likely as a result of alteration or degradation of chemical cues. These cues are critical for learning and avoiding predators, and a failure to respond can have dramatic repercussions for survival and recruitment.

Ultimate predators : lionfish have evolved to circumvent prey risk assessment abilities

Invasive species cause catastrophic alterations to communities worldwide by changing the trophic balance within ecosystems. Ever since their introduction in the mid 1980s common red lionfish, Pterois volitans, are having dramatic impacts on the Caribbean ecosystem by displacing native species and disrupting food webs. Introduced lionfish capture prey at extraordinary rates, altering the composition of benthic communities. Here we demonstrate that the extraordinary success of the introduced lionfish lies in its capacity to circumvent prey risk assessment abilities as it is virtually undetectable by prey species in its native range. While experienced prey damselfish, Chromis viridis, respond with typical antipredator behaviours when exposed to a common predatory rock cod (Cephalopholis microprion) they fail to visibly react to either the scent or visual presentation of the red lionfish, and responded only to the scent (not the visual cue) of a lionfish of a different genus, Dendrochirus zebra. Experienced prey also had much higher survival when exposed to the two non-invasive predators compared to P. volitans. The cryptic nature of the red lionfish has enabled it to be destructive as a predator and a highly successful invasive species.

Chemical alarm cues inform prey of predation threat: the importance of ontogeny and concentration in a coral reef fish

Prey that respond to inappropriate cues in their assessment of predation risk spend more time performing defensive behaviours and less time undertaking behaviours that promote fitness. Hence, prey should respond to cues that are the best predictors of predation risk relevant to the prey individual. Many fish undergo ontogenetic shifts in habitat and resource use during their lifetime; consequently, prey fish are exposed to a variety of predators at different stages of their development. Also, as relative concentration of the alarm cue represents both spatial and temporal information about a predation event, prey should adjust the intensity of their antipredator response in a threat-sensitive manner. We found that the ambon damselfish, Pomacentrus amboinensis, exhibited a threat-sensitive response to damage-released cues of conspecifics, with the magnitude of the response dependent on the cue concentration. Higher cue concentrations (suggesting a greater threat) elicited a stronger avoidance response, while low cue concentrations (weak threats) elicited a weak antipredator response. Moreover, the nature of the response depended on the ontogenetic stage of the cue donor. Reef-naive recruit individuals exhibited consistent antipredator behaviours when exposed to alarm cue concentrations from individuals of the same ontogenetic stage, modest antipredator responses to juvenile skin extracts, and no antipredator behaviours when exposed to cues from adult fish. Individuals that alter their avoidance response in a manner that reflects the magnitude of risk successfully balance the trade-off between defensive and risky or fitness-promoting behaviours, and natural selection would presumably favour these individuals.

Well-informed foraging: damage-released chemical cues of injured prey signal quality and size to predators.

Predators use a variety of information sources to locate potential prey, and likewise prey animals use numerous sources of information to detect and avoid becoming the meal of a potential predator. In freshwater environments, chemosensory cues often play a crucial role in such predator/prey interactions. The importance of chemosensory information to teleost fish in marine environments is not well understood. Here, we tested whether coral reef fish predators are attracted to damage-released chemical cues from already wounded prey in order to find patches of prey and minimize their own costs of obtaining food. Furthermore, we tested if these chemical cues would convey information about status of the prey. Using y-maze experiments, we found that predatory dottybacks, Pseudochromis fuscus, were more attracted to skin extracts of damselfish, Pomacentrus amboinensis, prey that were in good condition compared to prey in poor body condition. Moreover, in both the laboratory and field, we found that predators could differentiate between skin extracts from prey based on prey size, showing a greater attraction to extracts made from prey that were the appropriate size to consume. This suggests that predators are not attracted to any general substance released from an injured prey fish instead being capable of detecting and distinguishing relatively small differences in the chemical composition of the skin of their prey. These results have implications for understanding predator foraging strategies and highlights that chemical cues play a complex role in predator–prey interactions in marine fish.

Predator-induced changes in the growth of eyes and false eyespots

The animal world is full of brilliant colours and striking patterns that serve to hide individuals or attract the attention of others. False eyespots are pervasive across a variety of animal taxa and are among natures most conspicuous markings. Understanding the adaptive significance of eyespots has long fascinated evolutionary ecologists. Here we show for the first time that the size of eyespots is plastic and increases upon exposure to predators. Associated with the growth of eyespots there is a corresponding reduction in growth of eyes in juvenile Ambon damselfish, Pomacentrus amboinensis. These morphological changes likely direct attacks away from the head region. Exposure to predators also induced changes in prey behaviour and morphology. Such changes could prevent or deter attacks and increase burst speed, aiding in escape. Damselfish exposed to predators had drastically higher survival suffering only 10% mortality while controls suffered 60% mortality 72 h after release.

Degrading habitats and the effect of topographic complexity on risk assessment

Topographic complexity is a key component of habitats that influences communities by modulating the interactions among individuals that drive population processes such as recruitment, competition, and predation. A broad range of disturbance agents affect biological communities indirectly through their modifications to habitat complexity. Individuals that best judge the threat of predation within their environment and can trade-off vigilance against behaviors that promote growth will be rewarded with the highest fitness. This study experimentally examined whether topographic habitat complexity affected the way a damselfish assessed predation risk using olfactory, visual, or combined cues. Fish had higher feeding rates in the low complexity environment. In a low complexity environment, damage-released olfactory cues and visual cues of predators complemented each other in the preys assessment of risk. However, where complexity was high and visual cues obscured, prey had lower feeding rates and relied more heavily on olfactory cues for risk assessment. Overall, fish appear to be more conservative in the high complexity treatment. Low complexity promoted extremes of behavior, with higher foraging activity but a greater response to predation threats compared with the high complexity treatment. The degree of flexibility that individuals and species have in their ability to adjust the balance of senses used in risk assessment will determine the extent to which organisms will tolerate modifications to their habitat through disturbance.