Ontogenetic shift in diet of a large elapid snake is facilitated by allometric change in skull morphology

Abstract

As snakes are limbless, gape-limited predators, their skull is the main feeding structure involved in prey handling, manipulation and feeding. Ontogenetic changes in prey type and size are likely to be associated with distinct morphological changes in the skull during growth. We investigated ontogenetic variation in diet from stomach contents of n = 161 dugite specimens (Pseudonaja affinis, Elapidae) representing the full range of body size for the species, and skull morphology of 46 specimens (range 0.25–1.64 m snout-vent-length; SVL). We hypothesised that changes in prey type throughout postnatal ontogeny would coincide with distinct changes in skull shape. Dugites demonstrate a distinct size-related shift in diet: the smallest individuals ate autotomised reptile tails, medium-sized individuals predominantly ate small reptiles (as snakes grew larger there was an increased likelihood of feeding on reptiles head-first), and the largest individuals (> 0.8 m SVL) ate mammals and large reptiles. Morphometric analysis revealed that ~ 40% of the variation in skull shape was associated with body size (SVL). Through ontogeny, skulls changed from a smooth, bulbous cranium with relatively small trophic bones (upper and lower jaws and their attachments), to more rugous bones (as an adaption for muscle attachment) and relatively longer trophic bones that would extend gape. Individual shape variation in trophic bone dimensions was greater in larger adults and this likely reflects natural plasticity of individuals feeding on different prey sizes/types. Rather than a distinct morphological shift with diet, the ontogenetic changes were consistent, but positive allometry of individual trophic bones resulted in disproportionate growth of the skull, reflected in increased gape size and mobility of jaw bones in adults to aid the ingestion of larger prey and improve manipulation and processing ability. These results indicate that allometric scaling is an important mechanism by which snakes can change their dietary niche.

Fang shape varies with ontogeny and sex in the venomous elapid snake Pseudonaja affinis

“…Based on this, we find that from 60 cm onwards the PC1 change slows and plateaus, meaning the shift to a more slender shape is achieved. This finding agrees with that of Patterson et al (2021) where individuals were found to only incorporate mammalian prey after reaching a SVL of 60 cm. The change to a more slender fang over the course of their subadult life stage enables adult P. affinis (>60 cm) to effectively target and subdue ductile mammals as their dominant prey.…”

“…Given these differences in biomechanical properties of the prey integument, we predict that the fangs of P. affinis will exhibit differences in sharpness and overall shape to accommodate for their change in diet during life. Additionally, knowing that P. affinis displays an ontogenetic shift in diet at 60 cm SVL (Patterson et al, 2021), we expect to find an associated change in fang shape morphology either just before or at 60 cm SVL. We make two predictions on how the fang shape should differ based on the fact that lizards and mammals represent functionally distinct prey items.…”

“…P. affinis Günther, 1872 specimens (n = 40) were sourced from the Western Australian Museum (Table S1, n = 15) and also from opportunistic road-kill collections (n = 25) from the greater Perth region in WA between 2014 and 2018 (originally sourced for Wolfe et al (2018) and Patterson et al (2021) under the Department of Parks and Wildlife's Regulation 17 licence (#SF009895)). The data set consists of snakes of varying sizes ranging 25.7-158.8 cm SVL, with sexually immature juveniles (n = 5), males (n = 15), females (n = 17) and adults of unknown sex (n = 3).…”

“…In order to study the change in fang shape across ontogeny, postulated to be related to their ontogenetic diet shift, the SVL was collected for all individuals. The specimens were divided into three life stage groups: juvenile snakes that exclusively feed on small reptiles and reptile tails (20-39.9 cm) (Wolfe et al, 2018); sub-adults that feed on slightly larger reptiles (40-59.9 cm); and adults that have partially or completely shifted to a mammalian-based diet (60 cm and onwards) (Patterson et al, 2021;Wolfe et al, 2018).…”

“…Within Pseudonaja, all species except P. modesta experience an ontogenetic diet shift, where juveniles prey on lizards and adults show a partial and often complete shift to mammalian prey (Cipriani et al, 2017;Jackson et al, 2016;Shine, 1977). Recent work shows that Pseudonaja affinis starts incorporating mammalian prey when they reach a snout-vent length (SVL) of 60 cm and by the time they reach 80 cm mammals become their dominant prey (Patterson et al, 2021).…”