It is widely accepted that predator recognition and avoidance are important behaviors in allowing prey to mitigate the impacts of their predators. However, while prey species generally develop anti-predator behaviors through coevolution with predators, they sometimes show accelerated adoption of these behaviors under strong selection pressure from novel species. We used a field manipulation experiment to gauge the ability of the common ringtail possum (Pseudocheirus peregrinus), a semi-arboreal Australian marsupial, to recognize and respond to olfactory cues of different predator archetypes. We predicted that ringtails would display stronger anti-predator behaviors to cues of the invasive European red fox (Vulpes vulpes) in areas where fox impacts had been greatest, and to cues of the native lace monitor (Varanus varius) in areas of sympatry compared with allopatry. We found that ringtails fled quickly and were more alert when exposed to the fecal odors of both predators compared to neutral and pungent control odors, confirming that predator odors are recognized and avoided. However, these aversive responses were similar irrespective of predator presence or level of impact. These results suggest that selection pressure from the fox has been sufficient for ringtails to develop anti-predator behaviors over the few generations since foxes have become established. In contrast, we speculate that aversive responses by ringtails to the lace monitor in areas where this predator is absent reflect recent coexistence of the two species. We conclude that rapid evolution of anti-predator behaviors may occur when selection is strong. The maintenance of these behaviors should allow re-establishment of predator-prey relationships if the interactants regain sympatry via range shifts or management actions to reintroduce them to their former ranges.
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.
Glucocorticoid hormone profiles are increasingly used as physiological markers to infer the strength of species interactions that can influence fitness and ensuing population dynamics of animals. Here we investigated two aims. First, we measured the effect of a 90-min capture stress protocol on the plasma corticosterone responses of a large native Australian lizard, the lace monitor (Varanus varius). Second, we compared the basal and postcapture stress corticosterone responses of lace monitors in habitats where they were exposed to high or low densities of the European red fox (Vulpes vulpes), an introduced competitor. Lace monitors responded to the capture stress protocol by significantly increasing plasma levels of corticosterone above basal at 45- and 90-min-postcapture blood-sampling intervals. In habitats with high fox densities, lace monitors produced a significantly greater basal and capture-stress-induced corticosterone response compared to individuals in low-fox density habitat. A significant interaction among fox density, time postcapture, and body condition was also found to influence plasma corticosterone values. These results suggest competition with red fox, perhaps via nutritional stress and increased hypersensitivity of the adrenocortical axis in lizards. At present, without further research, we do not understand whether such responses mediate lizard fitness or whether they have adaptive or maladaptive consequences for lizard populations in response to red fox competition. Nevertheless, our results help broaden understanding of the physiological implications arising from species interactions and specifically how introduced competitors could mediate diverse impacts on native biodiversity.
Habitat loss and invasive predators increasingly threaten global biodiversity. Here we use a landscape-scale experimental approach to explore the individual and synergistic eff ects of logging and an invasive predator, the red fox Vulpes vulpes on two common native arboreal vertebrates (a predator and prey species) in south-eastern Australia. We used site occupancy methods to evaluate diff erent models evaluating the eff ects of site specifi c forest logging disturbance, lethal fox baiting and forest structural elements for explaining variation in site occupancy of a large monitor lizard Varanus varius , and a marsupial prey, the common ringtail possum Pseudocheirus peregrinus across a complex forest landscape. Site occupancy of ringtail possum was infl uenced by habitat resources and the structural complexity of forest, which indirectly mediated predation risk. Presence of fox baiting had no direct eff ect on the ringtail site occupancy. In contrast, access to prey resources and fox baiting appeared to best explain site occupancy variation in monitor lizards across the landscape. While these species are aff ected primarily by separate disturbances, synergistic interactions between the processes may intensify their eff ects. Our results demonstrate that species susceptibility to disturbance processes are highly idiosyncratic. Th is approach makes effi cient use of integrated modelling to aid conservation management at both local and landscape levels.
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