Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

The impact of invasive predators on native prey has attracted considerable scientific attention, whereas the reverse situation (invasive species being eaten by native predators) has been less frequently studied. Such interactions might affect invasion success; an invader that is readily consumed by native species may be less likely to flourish in its new range than one that is ignored by those taxa. Invasive cane toads (Rhinella marina) in Australia have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds are more resistant to toad toxins. We quantified prey preferences of four species of wading birds (Nankeen night heron, purple swamphen, pied heron, little egret) in the wild, by offering cane toads and alternative native prey items (total of 279 trays offered, 14 different combinations of prey types). All bird species tested preferred the native prey, avoiding both tadpole and metamorph cane toads. Avoidance of toads was strong enough to reduce foraging on native prey presented in combination with the toads, suggesting that the presence of cane toads could affect predator foraging tactics, and reduce the intensity of predation on native prey species found in association with toads.

Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression

1. Apex predators can benefit ecosystems through top–down control of mesopredators and herbivores. However, apex predators are often subject to lethal control aimed at minimizing attacks on livestock. Lethal control can affect both the abundance and behaviour of apex predators. These changes could in turn influence the abundance and behaviour of mesopredators.

2. We used remote camera surveys at nine pairs of large Australian rangeland properties, comparing properties that controlled dingoes Canis lupus dingo with properties that did not, to test the effects of predator control on dingo activity and to evaluate the responses of a mesopredator, the feral cat Felis catus.

3. Indices of dingo abundance were generally reduced on properties that practiced dingo control, in comparison with paired properties that did not, although the effect size of control was variable. Dingoes in uncontrolled populations were crepuscular, similar to major prey. In populations subject to control, dingoes became less active around dusk, and activity was concentrated in the period shortly before dawn.

4. Shifts in feral cat abundance indices between properties with and without dingo control were inversely related to corresponding shifts in indices of dingo abundance. There was also a negative relationship between predator visitation rates at individual camera stations, suggesting cats avoided areas where dingoes were locally common. Reduced activity by dingoes at dusk was associated with higher activity of cats at dusk.

5. Our results suggest that effective dingo control not only leads to higher abundance of feral cats, but allows them to optimize hunting behaviour when dingoes are less active. This double effect could amplify the impacts of dingo control on prey species selected by cats. In areas managed for conservation, stable dingo populations may thus contribute to management objectives by restricting feral cat access to prey populations.

6. Synthesis and applications. Predator control not only reduces indices of apex predator abundance but can also modify their behaviour. Hence, indicators other than abundance, such as behavioural patterns, should be considered when estimating a predator's capacity to effectively interact with lower trophic guilds. Changes to apex predator behaviour may relax limitations on the behaviour of mesopredators, providing enhanced access to resources and prey.

Predator behaviour and predation risk in the heterogeneous Arctic environment

1. Habitat heterogeneity and predator behaviour can strongly affect predator–prey interactions but these factors are rarely considered simultaneously, especially when systems encompass multiple predators and prey.

2. In the Arctic, greater snow geese Anser caerulescens atlanticus L. nest in two structurally different habitats: wetlands that form intricate networks of water channels, and mesic tundra where such obstacles are absent. In this heterogeneous environment, goose eggs are exposed to two types of predators: the arctic fox Vulpes lagopus L. and a diversity of avian predators. We hypothesized that, contrary to birds, the hunting ability of foxes would be impaired by the structurally complex wetland habitat, resulting in a lower predation risk for goose eggs.

3. In addition, lemmings, the main prey of foxes, show strong population cycles. We thus further examined how their fluctuations influenced the interaction between habitat heterogeneity and fox predation on goose eggs.

4. An experimental approach with artificial nests suggested that foxes were faster than avian predators to find unattended goose nests in mesic tundra whereas the reverse was true in wetlands. Foxes spent 3·5 times more time between consecutive attacks on real goose nests in wetlands than in mesic tundra. Their attacks on goose nests were also half as successful in wetlands than in mesic tundra whereas no difference was found for avian predators.

5. Nesting success in wetlands (65%) was higher than in mesic tundra (56%) but the difference between habitats increased during lemming crashes (15%) compared to other phases of the cycle (5%). Nests located at the edge of wetland patches were also less successful than central ones, suggesting a gradient in accessibility of goose nests in wetlands for foxes.

6. Our study shows that the structural complexity of wetlands decreases predation risk from foxes but not avian predators in arctic-nesting birds. Our results also demonstrate that cyclic lemming populations indirectly alter the spatial distribution of productive nests due to a complex interaction between habitat structure, prey-switching and foraging success of foxes.

Influence of sea-ice structure on minke whale and other krill-predator distribution

This thesis investigated the extent to which sea-ice structure and complexity could be measured to identify suitable feeding habitat for krill-eating predators such as the Antarctic minke whale (Balaenoptera bonaerensis). The results of this study suggest that the distribution and movement of minke whales is limited by the structure of the sea ice and that the sea ice influences minke whales' habitat use more than their overall distribution. Similar relationships were found for other krill predators such as Adelie penguins and crabeater seals.

Flocking and feeding in the fiddler crab (UCA tangeri): prey availability as risk-taking behaviour

For a full understanding of prey availability, it is necessary to study risk-taking behaviour of the prey. Fiddler crabs are ideally suited for such a study, as they have to leave their safe burrow to feed on the surface of the intertidal flats during low tide, thereby exposing themselves to avian predators. A study in an intertidal area along the coast of Mauritania showed that small crabs always stayed in the vicinity of their burrow, but large crabs wandered in large flocks (also referred to as droves) to feed on sea-grass beds downshore. Transplanting downshore feeding substrate to the burrowing zone of the small crabs proved that they too preferred to feed on it. Since small crabs can be preyed upon by more species of birds, this suggests that the decision not to leave the burrowing zone might be related to the risk of being fed upon by birds. We calculated predation risk from measurements on the density and feeding activity of the crabs, as well as the feeding density, the intake rate and the size selection of the avian predators. Per hour on the surface, crabs in a flock were more at risk than crabs feeding near their burrow. Thus, though flocking crabs may have benefited from ‘swamping the predator’ by emerging in maximum numbers during some tides only, this did not reduce their risk of predation below that of non-flocking crabs. Furthermore we found that irrespective of activity, large crabs suffered a higher mortality per tide from avian predators than small crabs. This suggests that large crabs could not sufficiently reduce their foraging time to compensate for the increased risk while foraging in a flock, even though they probably experienced better feeding conditions than small crabs staying near their burrow. The greater energy demands of large crabs were reflected in a greater surface area grazed. Thus, with increasing size a fiddler crab has to feed further away from its burrow and so may derive less protection from staying near to it. It seems that growing big does not reduce the risk of predation for fiddler crabs, as it does in many other species with indeterminate growth. As in such species, the most probable advantage of growing big is increased mating success. Ultimately, therefore, prey availability must be understood from the life-history decisions of the prey species.

Restricting prey dispersal can overestimate the importance of predation in trophic cascades

Predators can affect prey populations and, via trophic cascades, predators can indirectly impact resource populations (2 trophic levels below the predator) through consumption of prey (density-mediated indirect effects; DMIEs) and by inducing predator-avoidance behavior in prey (trait-mediated indirect effects; TMIEs). Prey often employ multiple predator-avoidance behaviors, such as dispersal or reduced foraging activity, but estimates of TMIEs are usually on individual behaviors. We assessed direct and indirect predator effects in a mesocosm experiment using a marine food chain consisting of a predator (toadfish--Opsanus tau), prey (mud crab--Panopeus herbstii) and resource (ribbed musse--Geukensia demissa). We measured dispersal and foraging activity of prey separately by manipulating both the presence and absence of the predator, and whether prey could or could not disperse into a predator-free area. Consumption of prey was 9 times greater when prey could not disperse, probably because mesocosm boundaries increased predator capture success. Although predator presence did not significantly affect the number of crabs that emigrated, the presence of a predator decreased resource consumption by prey, which resulted in fewer resources consumed for each prey that emigrated in the presence of a predator, and reduced the overall TMIE. When prey were unable to disperse, TMIEs on mussel survival were 3 times higher than the DMIEs. When prey were allowed to disperse, the TMIEs on resource survival increased to 11-times the DMIEs. We found that restricting the ability of prey to disperse, or focusing on only one predator-avoidance behavior, may be underestimating TMIEs. Our results indicate that the relative contribution of behavior and consumption in food chain dynamics will depend on which predator-avoidance behaviors are allowed to occur and measured.

Out of sight but not out of mind: corvids prey extensively on eggs of burrow-nesting penguins

Context Egg depredation is a major cause of reproductive failure among birds and can drive population declines. In this study we investigate predatory behaviour of a corvid (little raven; Corvus mellori) that has only recently emerged, leading to widespread and intense depredation of eggs of a burrow-nesting seabird (little penguin; Eudyptula minor). Aims The main objective of this study was to measure the rate of penguin egg depredation by ravens to determine potential threat severity. We also examined whether penguin burrow characteristics were associated with the risk of egg depredation. Ravens generally employ two modes of predatory behaviour when attacking penguin nests; thus we examined whether burrow characteristics were associated with these modes of attack. Methods Remote-sensing cameras were deployed on penguin burrows to determine egg predation rates. Burrow measurements, including burrow entrance and tunnel characteristics, were measured at the time of camera deployment. Key results Overall, clutches in 61% of monitored burrows (n≤203) were depredated by ravens, the only predator detected by camera traps. Analysis of burrow characteristics revealed two distinct types of burrows, only one of which was associated with egg depredation by ravens. Clutches depredated by ravens had burrows with wider and higher entrances, thinner soil or vegetation layer above the egg chamber, shorter and curved tunnels and greater areas of bare ground and whitewash near entrances. In addition, 86% were covered by bower spinach (Tetragonia implexicoma), through which ravens could excavate. Ravens used two modes to access the eggs: they attacked through the entrance (25% of burrow attacks, n≤124); or dug a hole through the burrow roof (75% of attacks, n≤124). Burrows that were subject to attack through the entrance had significantly shorter tunnels than burrows accessed through the roof. Conclusions The high rates of clutch loss recorded here highlight the need for population viability analysis of penguins to assess the effect of egg predation on population growth rates. Implications The subterranean foraging niche of a corvid described here may have implications for burrow-nesting species worldwide because many corvid populations are increasing, and they exhibit great capacity to adopt new foraging strategies to exploit novel prey. Journal compilation

Monitoring the ungulate prey of the Komodo dragon Varanus komodoensis: distance sampling or faecal counts?

Monitoring the abundances of prey is important for informing the management of threatened and endangered predators. We evaluated the usefulness of faecal counts and distance sampling for monitoring the abundances of rusa deer Rusa timorensis, feral pig Sus scrofa and water buffalo Bubalus bubalis, the three key prey of the Komodo dragon Varanus komodoensis, at 11 sites on five islands in and around Komodo National Park, eastern Indonesia. We used species-specific global detection functions and cluster sizes (i.e. multiple covariates distance sampling) to estimate densities of rusa deer and feral pig, but there were too few observations to estimate densities of water buffalo. Rusa deer densities varied from from 2.5 to 165.5 deer/km2 with coefficients of variation (CVs) of 15-105%. Feral pig densities varied from 0.0 to 25.2 pigs/km 2 with CVs of 25-106%. There was a positive relationship between estimated faecal densities and estimated population densities for both rusa deer and feral pig: the form of the relationship was non-linear for rusa deer, but there was similar support for linear and non-linear relationships for feral pig. We found that faecal counts were more useful when ungulate densities were too low to estimate densities with distance sampling. Faecal count methods were also easier for field staff to conduct than distance sampling. Because spatial and temporal variation in ungulate density is likely to influence the population dynamics of the Komodo dragon, we recommend that annual monitoring of ungulates in and around Komodo National Park be undertaken using distance sampling and faecal counts. The relationships reported here will also be useful for managers establishing monitoring programmes for feral pig, rusa deer and water buffalo elsewhere in their native and exotic ranges.

Stress triangle: do introduced predators exert indirect costs on native predators and prey?

Non-consumptive effects of predators on each other and on prey populations often exceed the effects of direct predation. These effects can arise from fear responses elevating glucocorticoid (GC) hormone levels (predator stress hypothesis) or from increased vigilance that reduces foraging efficiency and body condition (predator sensitive foraging hypothesis); both responses can lead to immunosuppression and increased parasite loads. Non-consumptive effects of invasive predators have been little studied, even though their direct impacts on local species are usually greater than those of their native counterparts. To address this issue, we explored the non-consumptive effects of the invasive red fox Vulpes vulpes on two native species in eastern Australia: a reptilian predator, the lace monitor Varanus varius and a marsupial, the ringtail possum Pseudocheirus peregrinus. In particular, we tested predictions derived from the above two hypotheses by comparing the basal glucocorticoid levels, foraging behaviour, body condition and haemoparasite loads of both native species in areas with and without fox suppression. Lace monitors showed no GC response or differences in haemoparasite loads but were more likely to trade safety for higher food rewards, and had higher body condition, in areas of fox suppression than in areas where foxes remained abundant. In contrast, ringtails showed no physiological or behavioural differences between fox-suppressed and control areas. Predator sensitive foraging is a non-consumptive cost for lace monitors in the presence of the fox and most likely represents a response to competition. The ringtail's lack of response to the fox potentially represents complete naiveté or strong and rapid selection to the invasive predator. We suggest evolutionary responses are often overlooked in interactions between native and introduced species, but must be incorporated if we are to understand the suite of forces that shape community assembly and function in the wake of biological invasions.

Stop jumping the gun : a call for evidence-based invasive predator management

Invasive mammalian predators are major drivers of species extinctions globally. To protect native prey, lethal control is often used with the aim of reducing or exterminating invasive predator populations. The efficacy of this practice, however, is often not considered despite multiple practical and ecological factors that can limit success. Here, we summarize contemporary knowledge regarding the use and challenges of both lethal control and alternative approaches for reducing invasive predator impacts. As the prevailing management approach, we outline four key issues that can compromise the effectiveness of lethal control: release of herbivore and mesopredator populations, disruption of predator social systems, compensatory predator immigration, and ethical concerns. We then discuss the relative merits and limitations of four alternative approaches that may enhance conservation practitioner's ability to effectively manage invasive predators: top-predator conservation or reintroduction, maintaining habitat complexity, exclusion fencing, and behavioral and evolutionary ecology. Considerable uncertainty remains regarding the effectiveness of management approaches in different environmental contexts. We propose that the deficiencies and uncertainties outlined here can be addressed through a combination of adaptive management, expert elicitation, and cost-benefit analyses. Improved management of invasive predators requires greater consideration and assessment of the full range of management approaches available.

A new method for resolving uncertainty of energy requirements in large water breathers: The 'mega-flume' seagoing swim-tunnel respirometer

Body size is a key determinant of metabolic rate, but logistical constraints have led to a paucity of energetics measurements from large water-breathing animals. As a result, estimating energy requirements of large fish generally relies on extrapolation of metabolic rate from individuals of lower body mass using allometric relationships that are notoriously variable. Swim-tunnel respirometry is the 'gold standard' for measuring active metabolic rates in water-breathing animals, yet previous data are entirely derived from body masses <10 kg - at least one order of magnitude lower than the body masses of many top-order marine predators. Here, we describe the design and testing of a new method for measuring metabolic rates of large water-breathing animals: a c. 26 000 L seagoing 'mega-flume' swim-tunnel respirometer. We measured the swimming metabolic rate of a 2·1-m, 36-kg zebra shark Stegostoma fasciatum within this new mega-flume and compared the results to data we collected from other S. fasciatum (3·8-47·7 kg body mass) swimming in static respirometers and previously published measurements of active metabolic rate measurements from other shark species. The mega-flume performed well during initial tests, with intra- and interspecific comparisons suggesting accurate metabolic rate measurements can be obtained with this new tool. Inclusion of our data showed that the scaling exponent of active metabolic rate with mass for sharks ranging from 0·13 to 47·7 kg was 0·79; a similar value to previous estimates for resting metabolic rates in smaller fishes. We describe the operation and usefulness of this new method in the context of our current uncertainties surrounding energy requirements of large water-breathing animals. We also highlight the sensitivity of mass-extrapolated energetic estimates in large aquatic animals and discuss the consequences for predicting ecosystem impacts such as trophic cascades.