Teasing apart the factors that influence prey choice and foraging tactics in the wild poses formidable logistical challenges because of multiple confounding features. For example, a particular type of prey may be rarely consumed not because of predator aversion, but because that prey type is more difficult to find or to capture than some other kind of prey22. Similarly, predators may key in on specific types of prey based on dietary preferences, prey size, or abundance23,24,25. The method of bait deployment that we adopted circumvents many of those problems, by standardising prey abundance, observability, and ease of capture by the predator. Under these conditions, free-ranging crocodiles from toad-sympatric versus toad-naïve populations showed substantial differences in foraging tactics and bait choice. In toad-naïve populations, crocodiles took equal numbers of treatment (toad) baits and control (chicken) baits, and frequently took baits located on land as well as over water. In contrast, crocodiles in toad-sympatric populations generally avoided toad baits in all locations and foraged primarily in the water rather than on land. Both of these shifts—in prey types and foraging locations—conceivably reduce the vulnerability of crocodiles to fatal ingestion of highly toxic cane toads.
The relatively rapid (< 8 years) development of aversion towards cane toads as prey, reflected both in the decreased proportion of toad baits consumed and by active rejections on camera, is unsurprising. Research on captive freshwater crocodiles reported rapid aversion learning in response to an initial non-fatal encounter with cane toads as prey26. Studies of other vulnerable predators (e.g., red-bellied blacksnakes, Pseudechis porphyriacus; common planigales, Planigale maculata; yellow-spotted monitors, Varanus panoptes) have shown that toad colonisation can induce a rapid and long-sustained aversion to their consumption as prey1,27,28. At least two mechanisms may underpin the elimination of cane toads from diets of these predators: behavioural plasticity (conditioned taste aversion) and natural selection (higher mortality of individuals with a genetically based propensity to consume toads1,9). Studies on newly hatched, and hence, toad-naïve, offspring of freshwater crocodiles from a range of sites (including locations where toad-induced mortality was high and others where it was not) did not reveal any geographic variation in their propensity to consume cane toads26. Thus, the ability to rapidly learn taste-aversion to cane toads may explain the shift in prey preferences of crocodiles following the arrival of toads.
The divergence in foraging behaviour of crocodiles between our two regions (toad invaded versus uninvaded) is more novel and may support the hypothesis that crocodiles experience a higher risk of fatality when they forage for toads on land. Our video analysis of prey handling behaviour confirms that crocodiles do “wash” recently seized toads, more often and for longer than occurred with non-toxic (chicken) baits. Presumably then, crocodiles recognise the unpalatability of toads and attempt to eliminate potential toxicity by flushing their mouths with water. This option is not immediately accessible to a predator that seizes its prey on land, and even a few seconds’ delay in returning to the water might be enough to increase susceptibility to this fast-acting poison8. In our study, 25% of crocodiles that took baits on land did not return to the water to consume them; and this behaviour may be especially risky. Interestingly, consuming prey in the water is not the default foraging behaviour for larger crocodilian species such as C. johnstoni, that often consume prey on land29, even with aquatic items such as fish (Fig. 5). This comparison further supports the idea that naïve crocodiles perceive toads as unpalatable and return to the water to compensate for this.
Freshwater crocodiles feeding on adult cane toads in the water (A,B) and on land (C,D). It is common for C. johnstoni crocodiles to consume prey on land, even if the prey is captured in the water (E: a catfish; F: a small barramundi). Photographs by R. Somaweera.
Other species of predators also employ behavioural mechanisms akin to ‘washing’ when consuming toxic prey16. For example, the slender loris sneezes, slobbers and urinates on poisonous invertebrates prior to consumption30. Similarly, otters detect the toxins of novel prey Bufo spinosus and avoid dermal toxin glands by skinning and washing carcasses prior to consumption (despite never having encountered amphibians previously)31. Toxins are often bitter and unpalatable, facilitating detection by predators16.
The proximate mechanisms underlying the apparent shift to aquatic rather than terrestrial foraging remain unclear. As for dietary preference, a shift in foraging tactics might be either learned or genetically based. Tests on captive-raised crocodiles from different populations could address this question but would be challenging logistically. Crocodiles show strong ontogenetic shifts in their choice of foraging sites19 and thus, offspring from captive-raised clutches would need to be maintained for several years in captivity before their choice of foraging sites was assessed. However, other behavioural traits that correlate with terrestrial foraging might be easier to explore. We might expect that ‘bolder’ individuals would be more likely to leave the water to forage, if boldness is associated with increased exploration and willingness to forage in the open32. Previous studies have explored the link between predator boldness and cane-toad induced mortality. Not only do bolder varanid lizards forage in different locations33, they are more likely to eat novel prey types such as invasive cane toads and have poorer learning responses to taste aversion trials10. Although we did not test this aspect directly, behavioural traits of freshwater crocodiles could influence their (i) foraging locations, (ii) propensity to eat a cane toad and (iii) ability to learn from non-lethal interactions with cane toads. Standardised trials could assess behavioural syndromes relatively early in life34. In-situ behavioural assays of crocodiles across a larger spatial scale (in toad invaded versus uninvaded areas) may document wider intraspecific variation and clarify whether underlying ‘personality’ traits are indeed corelated with foraging behaviour. Such studies could investigate the propensity to forage terrestrially, and to return to the water with prey, both of which have implications for predator vulnerability. Interestingly, strong selection against specific foraging behaviours may have ecological ramifications, if shifts lead to higher rates of predation on aquatic and semi-aquatic species, and less on terrestrial species. When populations of apex predators change numerically or behaviourally, trophic cascades can ensue, with unpredictable impacts on meso-predators and prey species35,36.
As well as learned or genetically-based factors, environmental differences between study sites (such as bank steepness or availability of alternative prey) may deter crocodiles from climbing out of the water in search of prey. However, there was no overt variation in site topography among the waterbodies selected (data not shown). Furthermore, terrestrial prey was more abundant in the toad-invaded region than the uninvaded region (unpublished data), the opposite pattern to what we would expect if prey availability was driving crocodile foraging tactics.
Other potential influences on bait uptake could be differences in densities of crocodiles at toad-naïve versus toad-sympatric sites, and/or a disproportionate influence of a small number of individuals that consumed multiple baits. However, animals were given ample opportunities to access baits (multiple locations, multiple bait stations, bait replenishment twice a day), such that there were always many more baits available than there were crocodiles. Although we could not identify individual predators, our video analysis confirmed that crocodiles of a wide range of body sizes visited stations at each location. Generally, toad-naïve sites had higher densities of crocodiles, potentially increasing rates of bait consumption based on numbers, or via increased competitive foraging. Nonetheless, the rate of bait uptake was low in toad-sympatric populations even with high densities of crocodiles. These patterns may reflect toad impact in two ways: (a) densities of crocodiles have decreased in toad-sympatric sites due to toad-induced mortality of crocodiles; and (b) the crocodiles most likely to survive the toad invasion are shy, neophobic, water-foraging individuals. Such animals may be less likely to engage with the novel apparatus that we set up, thereby decreasing uptake of baits. Irrespective of overall uptake, however, we found robust evidence of toad aversion in the toad-sympatric populations: the relative offtake of chicken baits increased relative to offtake of toad baits. This comparison of responses to the two types of bait confirms the influence of toads in these areas.
Our spatial sampling for the present study was not ideal, for logistical reasons. Ideally, we would use a Before-After-Control-Impact design, sampling multiple sites before and after the arrival of cane toads. Future research could replicate our work, at that larger spatial and temporal scale. However, if the impact of toads on crocodile foraging behaviour does not manifest until a few years after invasion, considerable logistical challenges will need to be overcome. For the present, we can confidently conclude that freshwater crocodiles within a toad-sympatric region foraged on land less frequently than did conspecifics in a toad-naïve region.
In summary, our data on foraging responses of crocodiles to standard baits revealed both of the patterns that we predicted. Following invasion by toxic toads, crocodiles tended to eliminate toads from their diet, and foraged less often in a habitat (on land) where consuming a toad was most likely to be fatal for the predator. Although we cannot confidently infer either causation or mechanisms for that divergence, our results suggest that further work on this topic would be of value.
Our data highlights the potential for an invasive species to modify multiple behavioural attributes of vulnerable native taxa. In the case of freshwater crocodiles, toad invasion has potentially induced shifts in foraging locations as well as prey selection. Other behavioural traits that affect foraging tactics, such as overall boldness, or prey-handling, such as washing, may have also been modified. Research on other taxa affected by invasive cane toads have shown comparable changes in predator behaviour. For example, native fish that benefit from discriminating toxic cane toads from non-toxic frogs may have evolved enhanced learning ability3. Dasyurid marsupials have switched their use of sensory modalities for stimulating prey-attack from purely visually based cues to chemical and visual signals27. Clarke et al.37 suggested that other aspects of encounters in the wild between toads and crocodiles (i.e., the part of the toad’s body that is grasped first) may affect opportunities for natural aversion learning and hence, modify demographic impact. Our research supports this inference. More generally, the arrival of a toxic alien taxa can impose strong pressure on native wildlife to adapt in ways that reduce rates of encounter with the invader, rates of consumption of the invader, or cause more subtle shifts in the contexts in which such encounters occur.
Source: Ecology - nature.com
