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Aquatic Feeding in Salamanders

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Aquatic Feeding in Salamanders CHAPTER 3 Aquatic Feeding in Salamanders STEPHEN M. DEBAN AND DAVID B. WAKE Museum of Vertebrate Zoology and Department oflntegrative Biology University of California Berkeley, California 94720 I. INTRODUCTION canum. Some undergo partial metamorphosis and pos- A. Systematics sess both adult and larval features when reproductive, B. Natural History such as the fully aquatic Cryptobranchus. Others are C. Feeding Modes and Terminology primarily terrestrial and become secondarily aquatic 11. MORPHOLOGY as metamorphosed adults, notably during the breed- A. Larval Morphology ing season. The family Salamandridae contains the B. Adult Morphology most representatives of this type, known commonly C. Sensory and Motor Systems as newts. 111. FUNCTION A. Ingestion Behavior and Kinematics Salamanders covered in this chapter may be terres- B. Prey Processing trial, semiaquatic, or fully aquatic. They may return to C. Functional Morphology the water only periodically and may feed on both land D. Biomechanics and in water. Discussion here focuses on the aquatic E. Metamorphosis feeding biology of these taxa. Terrestrial feeding of F. Performance semiaquatic and terrestrial salamanders is discussed G. Variation in the next chapter. Here we describe the various feed- IV. DIVERSITY AND EVOLUTION ing behaviors: foraging, ingestion (prey capture), prey A. Features of Salamander Families processing, intraoral prey transport, and swallowing. B. Phylogenetic Patterns of Feeding Form and Function We review the relevant morphology and function of V. OPPORTUNITIES FOR FUTURE RESEARCH the sensory and motor systems and analyze the bio- References mechanical function of the feeding apparatus. Finally, we consider the evolution of aquatic feeding systems within and among the major taxa of salamanders. I. INTRODUCTION A. Systematics Aquatic feeding is widespread among salamanders. In this chapter and the next we use a recent phylo- All 10 families include members that are aquatic dur- genetic hypothesis (Fig. 3.1) based on combined mor- ing part of their lives and all have members that are phological and molecular data (Larson and Dimmick, aquatic or semiaquatic as adults. Aquatic feeding be- 1993). The suborder Sirenoidea (Duellman and Trueb, havior, morphology, and function in salamanders are 1986) is the basal clade in this phylogeny, containing accordingly diverse. Most aquatic adult salamanders only the Sirenidae, followed by a split between the are perennibranchiate or paedomorphic forms that Cryptobranchoidea (which contains the families Cryp- forego metamorphosis and function as larvae when tobranchidae and Hynobiidae, both of which are exter- sexually mature, such iis the axolotl, Ambystoma mexi- nal fertilizers) and the Salamandroidea (which has Copyright 0 2000 by Academic Press. FEEDING (K. ScJiromk, d) 65 All rights of reproduction in any form reserved. 66 Stephen M. Deban and David B. Wake Sirenidae 2 Sirenoidea departure from the ancestral life history is paedomor- phosis, in which sexual maturity occurs while larval Cryptobranchidae morphology is retained. This pattern is present in most Cryptobranchoidea Hynobiidae families of salamanders in varying degrees of expres- sion. It is most apparent in the Sirenidae and Protei- Amphiumidae dae, where it is termed perennibranchiation because of the retention of external gills and posterior gill bars, Plethodontidae and less apparent in the Amphiumidae and Crypto- Rhyacotritonidae branchidae, whose members possess a mixture of lar- val and adult features. Both perennibranchiate forms Salamandridae Salamandroidea and those with the ancestral life history are found in Ambystomatidae the Hynobiidae, Ambystomatidae, Dicamptodontidae, w Plethodontidae, and Salamandridae. A second com- 'Dicamptodontidae mon departure from the ancestral life history is direct Proteid ae development, in which the terrestrial adult lays eggs \ on land, the larval stage remains encapsulated or is by- FIGURE 3.1. Phylogenetic hypothesis of the relationships of the passed altogether, and a terrestrial juvenile emerges salamander families, from Larson and Dimmick (1993). This tree is from the egg. Direct development is found only in based on a combined set of morphological and molecular data. Plethodontidae, but has evolved repeatedly in this fam- ily. This life history characterizes most plethodontids (i.e., all members of the tribes Plethodontini and Boli- internal fertilization). The interrelationships of the toglossini) and thus over half of all salamanders. The three main clades within the Salamandroidea are un- third departure is viviparity, in which embryonic de- certain. The first clade contains the Rhyacotritonidae, velopment occurs inside the oviducts of the mother, and the second the Plethodontidae and Amphiumidae and is present only in the genera Salamandra and Mer- as sister taxa. Within the third clade, the Proteidae is fensiella of the Salamandridae. the outgroup to the Salamandridae, Dicamptodonti- In taxa with the ancestral life history, the aquatic dae, and Ambystomatidae, with the last two being sis- larva ingests and manipulates prey using suction gen- ter taxa. erated in the mouth, whereas the terrestrial adult uses the tongue. Perennibranchiate forms which retain the larval morphology also retain the larval suction feed- B. Natural History ing behavior. Direct developers either pass through Intimately tied to the form and function of the feed- a nonfeeding larval stage while encapsulated or by- ing systems of salamanders is their life history. The pass the larval stage altogether and emerge as tongue- ancestral life history of salamanders is complex, like flipping terrestrial juveniles. Viviparous salamandrids that of many frogs and caecilians, and includes an give birth either to larvae, which suction feed, or to aquatic larval stage and a terrestrial or semiterrestrial metamorphosed, terrestrial juveniles, which use tongue adult stage, separated by a period of concentrated protrusion. During development in the oviducts of the postembryonic development known as metamorpho- mother, larvae and metamorphs feed on unfertilized sis. Throughout this biphasic life history a salamander eggs or smaller developing siblings (Alcobendas et al., must capture and subdue living prey, first in water and 1996); the intraoviductal feeding behavior remains un- then on land, and uses different means in these two en- described. vironments. Aquatic salamanders typically ingest prey Aquatic salamanders inhabit diverse freshwater en- by rapidly expanding the mouth and throat, drawing vironments, including lakes, ephemeral ponds, bogs, prey in by suction, whereas terrestrial salamanders swamps, drainage ditches, springs, rivers, streams, project a sticky tongue from the mouth to ensnare prey. and mountain brooks. Larvae can be divided into three These behaviors are performed rapidly, in a fraction of types based on external morphology (Valentine and a second, ensuring that even highly evasive prey are Dennis, 1964): pond type, stream type, and mountain- captured. brook type. Pond-type larvae have large, bushy gills, Six families of extant salamanders have members deep tail fin that extends onto the body, peculiar paired with the ancestral life history: Hynobiidae, Salaman- organs called balancers protruding from the head dur- dridae, Rhyacotritonidae, Dicamptodontidae, Ambys- ing early larval development, and are found in stand- tomatidae, and Plethodontidae. The most frequent ing or slowly flowing water where they float and swim 3. Aquatic Feeding in Salamanders 67 in the water column. Stream-type larvae generally development (Leff and Bachmann, 1986).Salamanders, have small external gills and a shallow tail fin that does as ectotherms, do not require much food to sustain not extent onto the back, are found in quickly flowing themselves. A larval or adult salamander can be main- water, and locomote by walking on the substrate and tained in captivity on little food, and some remain swim in short bursts. Mountain brook types have tiny healthy after months without eating. Simply obtaining gills and a shallow tail fin that does not extend onto the enough food to stay alive is probably not a challenge body and live in torrents and steep, cold mountain for most salamanders; however, salamanders living in streams. Both stream and mountain brook types may marginal conditions such as caves probably experi- be associated with a stream habitat, making use of ence a scarcity of prey. The amount eaten influences different microhabitats. Most larval and perennibran- growth rate and energy stores, and body size and the chiate salamanders can be classified into one of these amount of stored fat are directly related to reproduc- groups, although intermediates do exist. These three tive output. These relationships make competition for types of salamander larvae do not differ markedly in prey and, more generally, the trophic ecology of sala- feeding biology. manders potentially important in understanding sala- The literature on salamander diet is enormous and mander feeding and may help explain the outstanding cannot be reviewed here in any detail, however, some prey-capture abilities of some species. generalizations are presented. Salamanders are car- nivorous in all stages of life, eating primarily live prey, C. Feeding Modes and Terminology including arthropods (mostly insects: Diptera, Ephem- eroptera, and Trichoptera; as well as crustaceans: Iso- Aquatic salamanders capture or ingest prey by us- poda, Ostracoda, Amphipoda, and Decapoda),
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