Herpetology Notes, volume 8: 455-457 (published online on 12 August 2015)

Observation of predation by a lycosid on a captive-reared larva (Ambystoma annulatum)

Adam Crane1,* and Alicia Mathis2

Salamanders in the family oviposit development in some species (Warkentin, in ponds where their offspring hatch and develop as 2011; Boone et al., 2002). The egg mass was placed in aquatic larvae for a period of weeks to years before a 19 L bucket containing 6 L of pond water. An airstone metamorphosizing and moving onto land (Wells, 2010). provided aeration at the surface of the water from a During their larval stage, individuals face a variety of battery powered pump. The eggs were transported by predators such as diving beetle larvae, wading birds, vehicle to our laboratory (Fig. 1A) where they were and other (Duellman and Trueb, 1986). held in an aerated plastic container (31×17.5×10.5 cm). Wolf (Lycosidae) are known predators of some Upon hatching, larvae were fed by adding pond water frogs (Formanowicz et al., 1981) and terrestrial eggs of containing daphnia. As larvae grew over the winter, some salamanders (Villa et al., 1982). In experimental we switched their diet to live bloodworms (3 feedings trials, Rubbo et al. (2003) found that wolf spiders would of 5-10 worms per week) and moved larvae into feed on terrestrial spotted salamanders (Ambystoma individual plastic containers (10×10×9 cm; Fig. 1B) to maculatum) by envenomation with their chelicerae. prevent cannibalism. Water changes with dechlorinated However, we are not aware of any literature reporting tap water were also conducted three times per week. predation of ambystomatid salamanders by any spider During the spring, these larvae were used in behavioural in the wild. Herein, we report a novel observation of experiments where they were exposed to snake odours, predation by a on a larval ringed salamander and their movement was quantified to assess innate (Ambystoma annulatum, Cope 1886) in its home pond predator recognition. Throughout their time in the after being raised in captivity (details below). Previously laboratory, the larvae were apparently healthy, showing known predators of this species include dragonfly larvae no signs of chytrid (Batrachochytrium dendrobatidis) (Crane et al., 2012) and cannibalistic conspecifics infection (e.g., redness, skin sloughing), while growing (Mathis et al., 2003). without deformity and feeding readily. During October 2010, we collected a clutch of On the afternoon of 11 May 2011, we released 20 ringed salamander eggs from a pond (36.5619°N, individual larvae (~8 cm in total length) back into 93.0802°W, WGS 84) at Bull Shoals Field Station in their home pond. This release was approved by the southwestern Missouri, U.S.A. The eggs were laid on local conservation authority (Missouri Department a small twig that we completely removed in order to of Conservation) because this salamander species is a minimize mechanical disturbance to the eggs which species of local conservation concern, being endemic to can affecting the timing of hatching and morphological the Ozarks region of Missouri, , and Oklahoma, U.S.A. Following the release, we observed the larvae for about 20 min. In contrast to wild individuals, these larvae were much more active at the surface of the water (Fig. 1C), similar to their behaviour in the laboratory when expecting food. Within five minutes one individual was 1 Department of Biology, University of Saskatchewan, 112 ambushed by a wolf spider (Dolomedes sp.) that moved Science Place, Saskatoon, Saskatchewan S7N 5E2, Canada 2 Biology Department, Missouri State University, 901 S. out onto the water’s surface to envenomate the larva in National, Springfield, Missouri 65897, USA the neck (Fig. 1D). * Corresponding author e-mail: [email protected] Because these salamanders were collected from the 456 Adam Crane & Alicia Mathis

Figure 1. The collected clutch of Ambystoma annulatum (A), and a larva housed in the laboratory (B). Larval surface behaviour (C) might result in predation risk from lycosid spiders (D).

pond as embryos, they had no larval experience in their from captivity may become easy targets because they natural habitat, although we cannot address the extent fail to recognize predation risk and have not learned to which this predation event resulted from the lack of critical antipredator responses (Gall and Mathis, 2010). experience of this individual. The naiveté of released A few programs have begun rearing salamanders for is of much interest to captive-rearing programs. release into the wild. In one study, 5-yr old salamanders Indeed, captive-reared animals can be poorly prepared (Cryptobranchus alleganiensis) were released and for challenges in their natural habitats (Huntingford, monitored with radio-telemetry, but overall survivorship 2004). Hatchery-raised fish have shown maladaptive after one year was lower than that estimated for wild behaviours such as poor motivation to feed (Crane et al., conspecifics (Bodinof et al., 2012). This was attributed 2015) and insufficient antipredator behaviour (Jackson to a variety of factors including naiveté. In our et al., 2011). While the idea of missing antipredator experimental work with this species (Crane and Mathis, behaviour is not new (Darwin, 1839), animals released 2011), and numerous studies on other taxa, captive- Predation by a lycosid spider on a captive-reared salamander larva 457 reared prey have been trained to recognize predators rearing conditions for the behaviour of cultivated fishes. Journal via classical conditioning (i.e., exposure to pairings of of Fish Biology 65: 122-142. novel predator cues with attack-released cues). While Formanowicz, D.R., Stewart, M.M., Townsend, K., Pough, F.H. , Brussard, P.F. (1981): Predation by giant crab spiders on the little research on released animals has been conducted, puerto rican frog Eleutherodactylus coqui. Herpetologica 37: predator training can increase post-release survival 125-129. (Shier and Owings, 2007; Polo-Cavia and Gomez- Gall, B.G. , Mathis, A. (2010): Innate predator recognition and the Mestre, 2014). problem of introduced trout. Ethology 116: 47-58. This report of the predation event upon a captive- Jackson, C.D., Brown, G.E. , Fleming, I. (2011): Differences in released salamander is a novel observation, but antipredator behaviour between wild and hatchery-reared determining whether it resulted from a deficiency in juvenile atlantic salmon (Salmo salar) under seminatural conditions. Canadian Journal of Fisheries and Aquatic Sciences captive rearing (developmental, morphological or 68: 2157-2166. behavioural) or is a typical occurrence for A. annulatum Mathis, A., Murray, K.L. , Hickman, C.R. (2003): Do experience in the wild would require controlled experimentation. and body size play a role in responses of larval ringed Captive-release programs should consider monitoring salamanders, Ambystoma annulatum, to predator kairomones? individuals that are raised under different hatchery Laboratory and field assays. Ethology 109: 159-170. conditions (e.g., predator trained or untrained) to Polo-Cavia, N. , Gomez-Mestre, I. (2014): Learned recognition pinpoint methods for improving post-release survival. of introduced predators determines survival of tadpole prey. Functional Ecology 28: 432-439. Rubbo, M.J., Townsend, V.R., Smyers, S.D. , Jaeger, R.G. Acknowledgements. We thank Brian Gall for critically reading (2003): An experimental assessment of invertebrate/vertebrate the manuscript. 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