Switching from mesopredator to apex predator: how do responses vary in amphibians adapted to cave living?

Abstract

The effective detection of both prey and predators is pivotal for the survival of mesopredators. However, the condition of being a mesopredator is strongly context dependent. Here we focus on two aquatic caudate species that have colonised caves: the Pyrenean newt (Calotriton asper) and the olm (Proteus anguinus). The former maintains both surface and subterranean populations, while only cave-adapted populations of the latter exist. Both species are apex predators in underground waterbodies, while the Pyrenean newt is a mesopredator in surface waterbodies. Shifting to a higher level of the trophic web through colonising caves may promote the loss of anti-predator response against surface apex predators, and an increase in the ability to detect prey. To test these two non-exclusive hypotheses, we integrated classical behavioural characterisations with a novel approach: the assessment of lateralisation (i.e. preference for one body side exposure). Behavioural experiments were performed using laboratory-reared individuals. We performed 684 trials on 39 Pyrenean newts and eight olms. Under darkness and light conditions, we tested how exposure to different chemical cues (predatory fish, prey and unknown scent) affected individuals’ activity and lateralisation. Both cave and surface Pyrenean newts responded to predator cues, while olms did not. In Pyrenean newts, predator cues reduced the time spent in movement and time spent in lateralisation associated with hunting. Our results show that predator recognition is maintained in a species where recently separated populations inhabit environments lacking of higher predators, while such behaviour tends to be lost in populations with longer history of adaptation. Significance statement Predator recognition can be maintained in animals adapted to predator free habitats, but varies with their history of adaptation. Species that are not at the apex of the food web can become top predators if they colonise subterranean environments. We compared the behavioural responses of the olm, a strictly cave species with a long underground evolutionary history, and of the Pyrenean newt, a facultative cave species that also has stream-dwelling populations. Moreover, we integrated a classical behavioural characterisation, such as movement detection, with a novel approach: the assessment of lateralisation. While olms do not respond to external predators scent, cave-dwelling newts still recognise it. This clearly indicates that predator recognition is still maintained in species that have colonised predator-free environments more recently.

Updating salamander datasets with phenotypic and stomach content information for two mainland Speleomantes

“…Nonetheless, subterranean environments also may be chosen by Speleomantes because predator pressure is lower if compared to epigean ones 6 , 7 . Indeed, Speleomantes likely represent one of the apex predators in these environments 8 , preying on a wide array of taxa 9 . Speleomantes ’ narrow eco-physiological requirements, combined with their limited distributions and high site fidelity 1 , 10 , make these species very sensitive to human-induced effects and susceptible to extinction 11 , 12 ; all Speleomantes species are therefore strictly protected 13 , 14 .…”

Collecting eco‐evolutionary data in the dark: Impediments to subterranean research and how to overcome them

“…The history of subterranean biology teaches us that a quasi in-situ approach-that is, to bring the laboratory into the target species' Vandel (1894Vandel ( -1980. Since its foundation in 1948, this semi-natural experimental setting has aided generations of subterranean biologists in the challenging task of shedding light on the natural history and behavior of a wide range of elusive subterranean life forms (Clergue-Gazeau, 1974;Durand, 1970;Juberthie, 1985;Juberthie et al, 1996;Manenti et al, 2020). For aquifers, the equivalent would be to lower sediment, substrate cages, bags into groundwater wells (Schmidt et al, 2004), which, however, would still have to be retrieved every time to study the organisms.…”

Conservation Studies on Groundwaters’ Pollution: Challenges and Perspectives for Stygofauna Communities

“…Caves, especially in temperate areas, show strong differences in abundance and in diversity of both predator and trophic resources if compared to superficial habitats [76,77]. Caves, even if the availability of prey is reduced, can be safe habitats for typical surface mesorpedator species that become the apex predators there [78,79]. How can groundwater pollution promote the shift of an epigean mesopredator into a subterranean top predator?…”