Dining dichotomy: aquatic and terrestrial prey capture behavior in the Himalayan newtTylototriton verrucosus

Abstract

Transitions between aquatic and terrestrial prey capture are challenging. Trophic shifts demand a high degree of behavioral flexibility to account for different physical circumstances between water and air to keep performance in both environments. The Himalayan newt, Tylototriton verrucosus, is mostly terrestrial but becomes aquatic during its short breeding period. Nonetheless, it was assumed that it lacks the capability of trophic behavioral flexibility, only captures prey on land by its tongue (lingual prehension) and does not feed in water. This theory was challenged from stomach content analyses in wild populations that found a variety of aquatic invertebrates in the newts' stomachs during their breeding season. Accordingly, we hypothesized that T. verrucosus actively changes its terrestrial prey capture mechanism to hunt for aquatic prey at least during its aquatic stage. In fact, the kinematic analyses showed that T. verrucosus uses lingual prehension to capture prey on land but changes to suction feeding for aquatic strikes. The statistical analyses revealed that terrestrial and aquatic strikes differ significantly in most kinematic parameters while behavioral variability does not differ between both behaviors. In turn, the movement patterns in suction feeding showed a higher degree of coordination between jaw and hyoid movements compared to the putative primary feeding mode, namely lingual prehension. We conclude that T. verrucosus, though relatively slow compared to trophic specialists, benefits from a high degree of behavioral flexibility that allows exploiting food sources efficiently from two very different habitats.

Evolution of skull shape in the family Salamandridae (Amphibia: Caudata)

“…). Therefore, the changes in the morphology of the frontosquamosal arch in the Pleurodelinae could be related to skull kinetics and be regarded as an independently acquired adaptation related to various feeding performances (Deban & Wake, ; Wake & Deban, ; Heiss & De Vylder, ). However, we consider it unlikely that the reduction of the frontosquamosal arch and (presumed) convergences that we have reconstructed for the skull shape of salamandrid salamanders would represent adaptations to similar selective environments.…”

“…However, in Triturus ivanbureschi, a species with a partially reduced frontosquamosal arch, various types of skull kinetics, including a movable connection among the skull roof elements, were recently reported (Natchev et al 2016). Therefore, the changes in the morphology of the frontosquamosal arch in the Pleurodelinae could be related to skull kinetics and be regarded as an independently acquired adaptation related to various feeding performances Heiss & De Vylder, 2016). However, we consider it unlikely that the reduction of the frontosquamosal arch and (presumed) convergences that we have reconstructed for the skull shape of salamandrid salamanders would represent adaptations to similar selective environments.…”

Aquatic–terrestrial transitions of feeding systems in vertebrates: a mechanical perspective

“…Some salamanders go further, and, while they still use suction feeding in water, they change to lingual prehension on land and catch prey by their protractible tongue (Fig. 7) (Reilly and Lauder, 1989;Lauder and Gillis, 1997;Deban and Wake, 2000;Wake and Deban, 2000;Heiss and De Vylder, 2016). In contrast, turtles are less flexible and only the fully terrestrial tortoises make use of their tongue for initial food uptake on land, but unlike their turtle relatives, extant tortoises have lost any capacity to feed under water (Natchev et al, 2015).…”

“…White arrows indicate the test prey item. Images of T. verrucosus are modified from Heiss and De Vylder (2016), images of H. grandis feeding in water are modified from Lintner (2010) and images of H. grandis feeding on land are courtesy of P. Lemell, N. Natchev, C. Beisser and E. Heiss.…”

Functional morphology of terrestrial prey capture in salamandrid salamanders

“…Additionally, the semi-aquatic salamandrids L. vulgaris and I. alpestris can alter the surface of their tongue pad and mucous secretions in the mouth during seasonal breeding phases, developing slender lingual papillae and complex adhesive systems during the terrestrial phase to aid in tongue prehension (Heiss et al, 2017). Gape, hyobranchial and tongue movements vary between aquatic-and terrestrial-feeding events in terrestrial, semi-aquatic and aquatic salamandrids as well, further suggesting that whereas semi-aquatic and aquatic salamanders are able to feed in different environments, their kinematics and consequently their performance are less extreme compared with species that are specialized feeders for one environment (Heiss and De Vylder, 2016;Miller and Larsen, 1990;Stinson and Deban, 2017).…”