Novel Predators and Naïve Prey: How Introduced Mammals Shape Behaviours and Populations of New Zealand Lizards

<p>Biotas that evolved in isolation from mammalian predators are susceptible to degradation due to recent human-mediated introductions of mammals. However, behavioural, morphological and life historical adaptations of prey to novel mammalian predators can allow prey to persist in mammal-invaded areas. Lizards in New Zealand are an ideal group for exploring the effects of invasive mammals on vertebrate prey because: (1) the ca. 80 endemic species evolved without mammals as a major influence for 80 my, (2) mammalian introductions during the past 2000 y have differentially affected lizard species, and (3) some species coexist with mammals on the mainland as well as occurring on mammal-free offshore islands. I tested three hypotheses: (1) lizard populations that have persisted on New Zealand’s mainland are no longer declining in the presence of introduced mammalian predators, (2) introduced mammals induce behavioural shifts in native lizards, and (3) lizard behavioural patterns and chemosensory predator detection abilities vary according to exposure to introduced mammals. Trends in capture rates of five sympatric native lizard populations over a 23 year (1984-2006) period demonstrate that not all lizard populations that have persisted thus far on New Zealand’s mainland have stabilised in numbers. Large, nocturnal and terrestrial species remain highly vulnerable at mainland sites. Introduced kiore, Rattus exulans, induce behavioural changes in Duvaucel’s geckos, Hoplodactylus duvaucelii. A radio telemetric study demonstrated that geckos start reverting to natural use of habitats within six months of kiore eradication. Activity patterns of common geckos, H. maculatus, and common skinks, Oligosoma nigriplantare polychroma, in laboratory trials are also correlated with their exposure to mammalian predators. Lizard activity (time spent moving) increases relative to freeze behaviour with greater exposure to mammals. However, specific antipredator behaviours are not elicited by chemical cues of either native (tuatara, Sphenodon spp) or introduced (ship rat, R. rattus) predators. Lizard populations may persist by changing their behaviours in the presence of invasive mammals. However, the continued declines of particularly vulnerable mainland lizard taxa suggest that mammal-induced behavioural shifts may only slow population declines rather than enabling long-term survival. Eradicating pest mammals from offshore islands has proven effective at restoring both populations and behaviours of native lizards, but lizard populations on the mainland also deserve conservation priority. Research directed at understanding the synergistic effects of invasive species that are causing continued lizard population declines and mammal-proof fencing to protect the most vulnerable mainland populations from extinction are both urgently required.</p>

Novel Predators and Naïve Prey: How Introduced Mammals Shape Behaviours and Populations of New Zealand Lizards

<p>Biotas that evolved in isolation from mammalian predators are susceptible to degradation due to recent human-mediated introductions of mammals. However, behavioural, morphological and life historical adaptations of prey to novel mammalian predators can allow prey to persist in mammal-invaded areas. Lizards in New Zealand are an ideal group for exploring the effects of invasive mammals on vertebrate prey because: (1) the ca. 80 endemic species evolved without mammals as a major influence for 80 my, (2) mammalian introductions during the past 2000 y have differentially affected lizard species, and (3) some species coexist with mammals on the mainland as well as occurring on mammal-free offshore islands. I tested three hypotheses: (1) lizard populations that have persisted on New Zealand’s mainland are no longer declining in the presence of introduced mammalian predators, (2) introduced mammals induce behavioural shifts in native lizards, and (3) lizard behavioural patterns and chemosensory predator detection abilities vary according to exposure to introduced mammals. Trends in capture rates of five sympatric native lizard populations over a 23 year (1984-2006) period demonstrate that not all lizard populations that have persisted thus far on New Zealand’s mainland have stabilised in numbers. Large, nocturnal and terrestrial species remain highly vulnerable at mainland sites. Introduced kiore, Rattus exulans, induce behavioural changes in Duvaucel’s geckos, Hoplodactylus duvaucelii. A radio telemetric study demonstrated that geckos start reverting to natural use of habitats within six months of kiore eradication. Activity patterns of common geckos, H. maculatus, and common skinks, Oligosoma nigriplantare polychroma, in laboratory trials are also correlated with their exposure to mammalian predators. Lizard activity (time spent moving) increases relative to freeze behaviour with greater exposure to mammals. However, specific antipredator behaviours are not elicited by chemical cues of either native (tuatara, Sphenodon spp) or introduced (ship rat, R. rattus) predators. Lizard populations may persist by changing their behaviours in the presence of invasive mammals. However, the continued declines of particularly vulnerable mainland lizard taxa suggest that mammal-induced behavioural shifts may only slow population declines rather than enabling long-term survival. Eradicating pest mammals from offshore islands has proven effective at restoring both populations and behaviours of native lizards, but lizard populations on the mainland also deserve conservation priority. Research directed at understanding the synergistic effects of invasive species that are causing continued lizard population declines and mammal-proof fencing to protect the most vulnerable mainland populations from extinction are both urgently required.</p>

Visual pursuit behavior in mice maintains the pursued prey on the retinal region with least optic flow

Mice have a large visual field that is constantly stabilized by vestibular ocular reflex (VOR) driven eye rotations that counter head-rotations. While maintaining their extensive visual coverage is advantageous for predator detection, mice also track and capture prey using vision. However, in the freely moving animal quantifying object location in the field of view is challenging. Here, we developed a method to digitally reconstruct and quantify the visual scene of freely moving mice performing a visually based prey capture task. By isolating the visual sense and combining a mouse eye optic model with the head and eye rotations, the detailed reconstruction of the digital environment and retinal features were projected onto the corneal surface for comparison, and updated throughout the behavior. By quantifying the spatial location of objects in the visual scene and their motion throughout the behavior, we show that the prey image consistently falls within a small area of the VOR-stabilized visual field. This functional focus coincides with the region of minimal optic flow within the visual field and consequently area of minimal motion-induced image-blur, as during pursuit mice ran directly toward the prey. The functional focus lies in the upper-temporal part of the retina and coincides with the reported high density-region of Alpha-ON sustained retinal ganglion cells.

The ultrasound guide: katydid ear pinnae code for bat call detection

Early predator detection is a key component of the predator-prey arms race, and has driven the evolution of multiple animal hearing systems. Katydids (Insecta) have a sophisticated ear consisting of paired tympana on each foreleg that receive sound externally and internally, creating a pressure-time difference receiver system capable of sensitive and accurate directional hearing, despite the small size of katydids. Some katydid species have pinnae of unknown function, which form cavities around the outer tympanal surfaces and have been hypothesised to influence the external sound paths. Combining experimental biophysics and numerical modelling on 3D ear geometries, we investigated pinna function in the katydid Copiphora gorgonensis. Pinnae induced large sound-pressure gains that enhanced sound detection at high ultrasonic frequencies (>60 kHz), matching the echolocation range of their nocturnal insectivorous bat predators. Comparing pinna resonances of sympatric katydid species supported these findings, and suggests that pinnae may have evolved for enhanced predator detection.

Avoiding costly mistakes in groups: The evolution of error management in collective decision making

Balancing the costs of alternative decisions is a fundamental challenge for decision makers. This is especially critical in social situations, where the choices individuals face are often associated with highly asymmetric error costs---such as pedestrian groups crossing the street, police squads holding a suspect at gunpoint, or animal groups evading predation. While a broad literature has explored how individuals acting alone adapt to asymmetric error costs, little is known about how individuals in groups cope with these costs. Here we investigate adaptive decision strategies of individuals in groups facing asymmetric error costs, modeling scenarios where individuals aim to maximize group-level payoff (‘‘cooperative groups’’) or individual-level payoff (‘‘competitive groups’’). We extended the drift--diffusion model to the social domain in which individuals first gather personal information independently; they can then either wait for additional social information or decide early, thereby potentially influencing others. We combined this social drift--diffusion model with an evolutionary algorithm to derive adaptive behavior. Under asymmetric costs, small cooperative groups evolved response biases to avoid the costly error. Large cooperative groups, however, did not evolve response biases, since the danger of response biases triggering false information cascades increases with group size. We show that individuals in competitive groups face a social dilemma: They evolve higher response biases and wait for more information, thereby undermining group performance. Our results have broad implications for understanding social dynamics in situations with asymmetric costs, such as crowd panics and predator detection.

Freely-moving mice visually pursue prey using a retinal area with least optic flow

Mice have a large visual field that is constantly stabilized by vestibular ocular reflex driven eye rotations that counter head-rotations. While maintaining their extensive visual coverage is advantageous for predator detection, mice also track and capture prey using vision. However, in the freely moving animal quantifying object location in the field of view is challenging. Here, we developed a method to digitally reconstruct and quantify the visual scene of freely moving mice performing a visually based prey capture task. By isolating the visual sense and combining a mouse eye optic model with the head and eye rotations, the detailed reconstruction of the digital environment and retinal features were projected onto the corneal surface for comparison, and updated throughout the behavior. By quantifying the spatial location of objects in the visual scene and their motion throughout the behavior, we show that the image of the prey is maintained within a small area, the functional focus, in the upper-temporal part of the retina. This functional focus coincides with a region of minimal optic flow in the visual field and consequently minimal motion-induced image blur during pursuit, as well as the reported high density-region of Alpha-ON sustained retinal ganglion cells.

Cutaneous tactile sensitivity before and after tail loss and regeneration in the leopard gecko (Eublepharis macularius)

Amongst tetrapods, mechanoreceptors on the feet establish a sense of body placement and help to facilitate posture and biomechanics. Mechanoreceptors are necessary for stabilizing the body while navigating through changing terrains or responding to a sudden change in body mass and orientation. Lizards such as the leopard gecko (Eublepharis macularius) employ autotomy – a voluntary detachment of a portion of the tail, to escape predation. Tail autotomy represents a natural form of significant (and localized) mass loss. Semmes-Weinstein monofilaments were used to investigate the effect of tail autotomy (and subsequent tail regeneration) on tactile sensitivity of each appendage of the leopard gecko. Prior to autotomy, we identified site-specific differences in tactile sensitivity across the ventral surfaces of the hindlimbs, forelimbs, and tail. Repeated monofilament testing of both control (tail-intact) and tail loss geckos had a significant sensitization effect (i.e., decrease in tactile threshold, maintained over time) in all regions of interest except the palmar surfaces of the forelimbs in post-autotomy geckos, compared to baseline testing. Although the regenerated tail is not an exact replica of the original, tactile sensitivity is shown to be effectively restored at this site. Re-establishment of tactile sensitivity on the ventral surface of the regenerate tail points towards a (continued) role in predator detection.