Aquatic Feeding in Salamanders

CHAPTER 3

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 paedomorphosis, 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 larval 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 family. 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), mol- ing the tongue, the jaws, or water flow (i.e., suction). lusks, worms, fish, and amphibians (Martof and Scott, The prey is then transported into the mouth and ma- 1957; Peck, 1973; Joly, 1981; Petersen et al., 1989; Tum- nipulated by water flow or movements of the tongue. lison et al., 1990). Some forms (eg, cryptobranchids; Processing of prey is minimal and usually does not in- Nickerson and Mays, 1973) may occasionally scavenge. volve reduction or chewing, although this may occur Cannibalistic morphs of Ambystoma eat primarily other to some degree in large taxa (e.g., amphiumids). Swal- salamanders, including members of their own species lowing is the final stage of feeding in which the prey (e.g., Collins and Holomuzki, 1984). Terrestrial and enters the esophagus. aerial prey are occasionally eaten as they happen to Salamanders capture prey by rapid movements of fall or land in the water. The stomach contents of the body, jaws, and hyobranchial apparatus. A sala- aquatic salamanders are generally representative of the mander can cover the initial distance between itself prey available in the microhabitat, suggesting that little and the prey by (1) bringing the prey toward itself dietary specialization occurs (Duellman and Trueb, as in suction feeding, (2) extending an appendage to 1986). Avoidance of distasteful prey is more probable grasp the prey as in lingual prehension, or (3) moving than specialization, although salamanders may select its whole body toward the prey as in jaw prehension. prey based on various parameters such as size, move- A combination of these methods is often used to get the ment pattern, and nutrient value (Avery, 1968; see prey into the mouth. Suction feeding involves expand- Roth, 1987, for a review). Larvae of a given species of ing the buccal cavity during mouth opening and draw- salamander at different stages of growth may show dif- ing water and prey into the mouth while the gill slits ferences in diet due to prey capture abilities (Bell, 1975; are held closed. The buccal cavity is expanded by de- Brophy, 1980) or habitat partitioning (Leff and Bach- pression of the hyobranchial apparatus. Water is then mann, 1986), and diet may vary with seasonal changes expelled through the gill slits or mouth by elevation of in prey abundance (Burton, 1977). In general, the diet the hyobranchial apparatus. Suction feeding is also contains prey items of the appropriate size (White, called “gape-and-suck” feeding. Lingual prehension in- 1977) in the frequency that they are likely to be encoun- volves grasping prey with the tongue and also relies tered within the microhabitat. on movements of both the jaws and hyobranchial ap- Depending on prey density and prey type, salaman- paratus. The hyobranchial apparatus, with the sticky ders exhibit either active foraging in which they seek tongue pad at its rostral tip, is protruded from the out and pursue prey or sit-and-wait foraging where mouth toward the prey. The tongue pad adheres to they remain stationary and let prey come to them (An- the prey and the hyobranchial apparatus is then re- thony et al., 1992; Jaeger and Barnard, 1981; Uiblein tracted, bringing prey either between the jaws or en- et al., 1992); some salamanders have been shown to tirely into the buccal cavity. This behavior is also called switch between foraging modes in the course of larval tongue prehension, tongue flipping, tongue projection, 68 Stephen M. Deban and David B. Wake or tongue protrusion and is accomplished by forward sliding and folding movements of hyobranchial apparatus. Jaw prehension is simply closing the mouth around the prey item so that it is trapped between the upper and the lower jaws. The salamander brings the jaws near the prey by lunging forward or sweeping the head laterally. The hyobranchial apparatus plays little role in jaw prehension. While jaw and lingual prehension are performed both on land and in water, suction feeding can only be performed aquatically because it relies upon the incompressibility of water to create enough flow to entrain the prey. The additional term ram feeding denotes ingestion behavior in which the salamander lunges forward and engulfs the prey without grasping it between the jaws. Suction feeding is the most common mode of ingestion among aquatic salamanders-it is used by all larvae and most species of aquatic adult salamanders. In addition, it is used by most bony fish (Muller and Osse, 1984). The widespread use of suction feeding among aquatic vertebrates implies that it is an extremely effective way to capture prey in water (see also Chapter 16). Suction feeding is rapid; a large Cryptobranchus com- pletes the behavior in less than one-tenth of a second. Suction feeding is also forceful and can draw even large, elongate, or highly elusive prey entirely into the mouth. Most secondarily aquatic adult salamanders are paedomorphic and perennibranchiate, and suction feed as their larvae do. Many aquatic salamanders, such as aquatic salamandrids and some hynobiids, undergo metamorphosis and lose larval features, but continue to suction feed with their adult morphology. Some salamandrids, for example Puchytriton, do so with great proficiency (Miller and Larsen, 1989) (Fig. 3.2). Others, such as cryptobranchids and amphiumids, appear to undergo partial metamorphosis, developing unusual adult structures while retaining some larval features such as posterior branchial cartilages, labial lobes, gill slits, and external gills; these groups suc- FIGURE 3.2. Suction-feeding behavior of an adult Puchytviton sp., tion feed. a fully aquatic newt of the family Salamandridae. Note the rapid dis- Some metamorphosed aquatic and semiaquatic sal- appearance of the worm into the salamander’s mouth, the extensive amanders, including all plethodontids and rhyacotri- upper labial lobes occluding much of the lateral gape, and the pronounced buccal expansion and hyobranchial depression. The video tonids and some hynobiids, do not use suction to cap- frames are 8.3 msec apart, and the background is a 5-mm grid. ture prey in water. Instead they use ancestral terrestrial ingestion behaviors, lingual and jaw prehension, to capture aquatic prey (Deban and Marks, 1992; Schwenk ior, morphology, and function in both larval and adult and Wake, 1993; Larsen, personal communication).Be- salamanders will be emphasized in this chapter. cause lingual prehension and jaw prehension are performed more commonly by terrestrial forms and because they are performed in water in the same way 11. MORPHOLOGY they are on land, they will not be stressed here. Instead they will be discussed in the following chapter on ter- Morphology is one of the most completely known restrial feeding in salamanders. Suction feeding behav- aspects of the feeding biology of salamanders. Exten- 3. Aquatic Feeding in Salamanders 69 sive anatomical data have been gathered over the last and prominent labial lobes occlude the sides of the century and descriptions of head morphology exist mouth. for many salamander taxa (Parker, 1882; Driiner, 1901, The teeth of larval salamanders are sharply pointed, 1904; Francis, 1934; Edgeworth, 1935; Piatt, 1938; Schu- typically nonpedicellate, and monocuspid and consist macher, 1958; Severtsov, 1964). Still, all morphologi- of a cylindrical base fused to a conical apex. They lack cal data relevant to feeding are not available for every the suture plane of adult pedicellate teeth (Beneski and group. Larsen, 1989a,b). Dentition is generally homodont, Feeding behavior relies on morphological features and teeth are borne on the premaxilla, maxilla, vomer, of the skull, jaws, hyobranchial apparatus, tongue pad, and palatine or palatopterygoid of the upper jaw and gill slits, and labial lobes. Both larval and adult aquatic the dentary and coronoid of the lower jaw (Fig. 3.3). salamanders must feed in the same environment, and Teeth grow in size and number during larval life. New thus share many of these features. This section de- tooth loci are added with the enlargement of jaw bones scribes the general pattern of the feeding morphology (Bonebrake and Brandon, 1971). Teeth are added pos- of larval and adult salamanders. Most features of the teriorly along the maxillae and dentaries and postero- larval feeding system presented here persist in the laterally to the vomers (Parker and Dunn, 1964; Wor- adults of perennibranchiate forms, i.e., perennibran- thington and Wake, 1971). At metamorphosis, teeth of chiate adults retain an essentially larval morphology. the coronoid and palatopterygoid usually disappear Metamorphic forms lose many larval morphological with the disintegration of these bones, and vomerine features, but may retain the larval feeding behavior teeth extend onto the parasphenoid (Wilder, 1928). while supplementing it with terrestrial feeding behav- The tongue is usually absent or poorly developed in ior. Metamorphic forms are discussed in a later section larvae; if present, it possesses few of the glands or pa- on adult morphology. pillae of the tongue pad of postmetamorphic individuals. Larvae often possess a fold in the floor of the mouth just rostral and ventral to the anterior elements A. Larval Morphology of the hyobranchial apparatus, called a buccal fold or The head of larval salamanders is tapered anteri- anterior fold. This region of overlap is just beneath the orly with an anterior mouth opening and posterior gill tongue and it accommodates ventral expansion of the slits. Bushy external gills protrude posterolaterally and buccal floor during suction feeding. A ventral gular slit have up to four main branches, or rami, each with nu- is often present at the level of the external gills and ac- merous vascularized fimbriae. The eyes are lidless and commodates extension of the skin of the throat during do not protrude. Neuromasts of the lateral line system buccal expansion. are abundant around the mouth and sides of the head, Extensions of skin on the upper and lower jaws

premaxilla ethmoidal ,nasal premaxilla \ ossification /

I cm FIGURE 3.3. Larval skull of the aquatic hynobiid Butrachuperus musfersi in dorsal, lateral, and ventral views. Note the presence of maxillae, lacrimals, septomaxillae, and prefrontals, as well as separate prootic, opisthotic, and exoccipital ossifications. 70 Stephen M. Deban and David B. Wake called labial lobes block the sides of the mouth and di- The skull bones of larval salamanders are loosely ar- rect the gape anteriorly. Upper and lower lobes are ticulated and less robust than in the adult. Sutures be- fused posteriorly and interlock or simply overlap an- tween bones are lacking or incomplete, or gaps exist teriorly; in larvae the regions where upper and lower between bones. During growth, the bones increase in lobes meet are called labial folds. Labial lobes have relative size and their degree of overlap and fusion. long been recognized as important for effective suction Larval skull morphology appears more conservative feeding (Matthes, 1934). These interlocking lobes and taxonomically than that of adults, and the phyloge- their folds allow for expansion during mouth opening netic diversity of larval skull morphology is not as well and, at the same time, prevent water from entering the documented. mouth from the sides. During suction feeding, the la- The upper jaw consists of the paired or fused pre- bial lobes narrow the gape and direct it anteriorly, thus maxilla, vomer, palatopterygoid, and, in some cases, restricting, focusing, and accelerating water flow and the late-appearing paired maxilla, all of which bear increasing the likelihood that prey are captured. teeth. The maxilla, when present, is loosely attached to Two or three gill slits (also called gill apertures or the skull. The maxillae are absent in the larva of many gill clefts) are located on each side of the head below taxa and appear during metamorphosis. In some per- the external gill rami. The gill slits lie between the dis- ennibranchiate taxa the maxilla never forms (e+, Nec- tal elements (epibranchials) of the hyobranchial appa- ttln~sand Pseudobranchus) or appears late and remains ratus and open into the mouth. Water that enters the a small, free-floating element (e.g., Siren; Reilly and mouth during suction feeding is expelled through the Altig, 1996). In these, the palatine or palatopterygoid gill slits after the prey has been captured. Interlocking forms a robust, dentate component of the upper jaw. fingers of tissue or mineralized tooth-like elements In all taxa the medial parasphenoid forms the palate. called gill rakers are present on the pharyngeal sur- The lower jaw consists of Meckel’s cartilage invested faces of the gill bars of some taxa and help prevent prey by the tooth-bearing dentary, the prearticular (also from escaping as water is expelled. called the gonial), usually the toothed coronoid (also called the splenial), and the angular (in cryptobranchoids). The articular cartilage of the lower jaw forms 1. Larval Skull, Jaws, and Hyobranchial Apparatus a joint with the quadrate of the skull, which is posi- The larval skull consists of the posterior neurocra- tioned between the orbit and the otic capsule. The jaw nium and auditory capsules connected via parachord- joint is far anterior in most larvae and perennibran- als and trabeculae to the anterior nasal capsules, in- chiate forms, reducing the gape. vested by dermal bones dorsally and by palatal bones The hyobranchial apparatus of larval salamanders and attached ventrally to the suspensorium (Fig. 3.3). is composed of interconnected skeletal elements that Posterior ossifications include the prootic, opisthotic, lie in the floor of the mouth and throat and border the and exoccipital, which together comprise the occipito- gill slits. An unpaired medial element, the basibran- otic (Trueb, 1993). Dorsal bones include the paired chial (sometimes called the copula), forms the main frontals and parietals. Marginal tooth-bearing bones axis of the larval hyobranchial apparatus (Fig. 3.4) with are the paired maxillae and the premaxillae, which are which the remaining bilaterally paired elements articu- paired or fused medially. Bones of the palate include late. The basibranchial articulates rostrally with the the paired vomers, the single parasphenoid, and the ceratohyals and caudally with the first and second cer- paired palatines or palatopterygoids. Palatines are atobranchials. These elements are sometimes called hy- present as separate elements only in the Sirenidae, po- pobranchials (Reilly and Lauder, 1988b),but likely rep- sitioned caudal to the vomers and bearing many teeth. resent the fusion of the ancestral hypobranchial and Palatopterygoids are present caudal to the vomers in ceratobranchial, and here are called ceratobranchials. the Proteidae (where they articulate with the vomers A third ceratobranchial is present in cryptobranchoids, and quadrates to form robust components of the upper but does not meet the basibranchial (see Batrachuperus, jaw) and in larval plethodontids (where they are free- Fig. 3.4).The ceratobranchialsare in turn attached to the floating) and bear teeth on their rostrolateral edges. more distal epibranchials (sometimes called cerato- The orbitosphenoids form around the trabecular carti- branchials; Reilly and Lauder, 1988b), which number lages. The suspensorium, which connects the lower three or four on each side of the main axis and which jaw to the skull, consists of the cartilaginous palato- curve dorsally to border the gill slits and support the ex- quadrate and osseous quadrate invested by the bony ternal gills. An unpaired, medial element, the urohyal pterygoid (which is absent in all plethodontids) and (also called the second basibranchial or os thyroideum), squamosal. The quadrate articulates with the articular lies caudal to the basibranchial and is often continuous of the lower jaw. with it. Hypohyals lie between the ceratohyals and the 3. Aquatic Feeding in Salamanders 71

Dicamptodon ensatus (L) G;rinophilus porphyriticus (L) Batrachuperus mustersi (L)

Pseudobranchus striatus (A) Proteus anguinus (A) Amphiuma means (L) FIGURE 3.4. Hyobranchia (in ventral view) of larval and perennibranchiate salamanders of six families. Cartilage is shown in white and ossification or mineralization is shaded. Scale bars equal 3 mm. See Table 3.1 for abbreviations. Proteus drawing is adapted from Marche and Durand (1983), with permission. basibranchial in some taxa (e.g., Dicamptodon and Am- and elements are held together by shared membranes phiuma, Fig. 3.4). The basibranchial and ceratobranchi- rather than by ligaments. The ceratohyals, however, als are fused to form a branchial plate in some taxa (e.g., are linked at their midpoints to the mandibles by the plethodontids, see Gyrinophilus,Fig. 3.4). hyomandibular ligaments or at their caudal ends to the The shapes of the hyobranchial elements show varia- prearticulars or quadrates by hyoquadrate ligaments. tion among taxa (Fig. 3.4), but with some underlying A single branched ligament may be present in some common themes. The basibranchial is usually elongate taxa (Elwood and Cundall, 1994) or at some stages of and circular or triangular in cross section. The cerato- development (Reilly and Altig, 1996). hyals are flat and broad, and the ceratobranchials are The elements of the hyobranchial apparatus are often cylindrical. The epibranchials are triangular in mostly cartilaginous, although ossification or minerali- cross section and taper to points or terminate with zation occurs in some elements and is usually more ex- knobs at the posterior tips, which are attached by tensive in older larvae. The basibranchial and cerato- muscles to the skull and dorsolateral neck region. The hyals are entirely cartilaginous, whereas the urohyal is ceratohyals and first epibranchials are usually the usually the first element to ossify. The second and third largest elements of the larval hyobranchial apparatus; ceratobranchials may be ossified or calcified in crypto- more posterior elements are progressively smaller. branchoids, and the epibranchials are ossified in some Articulations between elements are generally loose, taxa (e.g., dicamptodontids and plethodontids). Adults 72 Stephen M. Deban and David B. Wake of perennibranchiate species may show the metamor- logues and synonyms, see Edgeworth, 1935; Francis, phic (i.e., adult) pattern of ossification, but a larval 1934). Only muscles likely to function in feeding are number and configuration of hyobranchial elements presented, and discussion of their functions is re- (e.g., Proteus and Pseudobranchus, Fig. 3.4). stricted to their expected actions when they contract. A later section on feeding function discusses in more detail the roles of various muscles in producing coor- 2. Larval Head Musculature dinated feeding movements. The muscles of the head can be divided into four Mouth opening and closing are performed by an- broad functional groups: jaw muscles, hyobranchial tagonistic sets of muscles: the depressors, which open muscles, skull muscles, and throat muscles. The gen- the mouth, and the levators, which close the mouth eral pattern of larval muscle morphology is presented (Fig. 3.5A). The mouth-opening muscle is the depres- in this section. Some taxa may not possess all of the sor mandibulae (DM), which is sometimes divided into muscles listed. Current names of muscles are used; two parts: depressor mandibulae anterior (DMA) and some synonyms are listed in parentheses and are not posterior (DMP) (see Table 3.1 for abbreviations). DM mentioned thereafter (for more thorough lists of homo- muscles originate on the skull in the vicinity of the

A n GH

SARl LME BH LMI AA DMA SAR 2-4 DMP

RC DT

LAB

SH IMP SAR

IOQ

RCP IHP

RCS

FIGURE 3.5. Larval (A) and adult (B) cranial muscles of the salamandrid Taricka granulosa in ventral and lateral-views. In ventral views, deep muscles are depicted on the left side and more superficial muscles are shown on the right side. See Table 3.1 for abbreviations and the text for descriptions of muscles. 3. Aquatic Feeding in Salamanders 73

TABLE 3.1 Abbreviations, Homologs and Synonyms of squamosal and quadrate (the DMP originates on the Skeletal Elements and Muscles ceratohyal in Siren) and insert on the ventrocaudal sur- Homologs and face of the articular or prearticular just beneath the jaw Synonyms joint. The branchiomandibularis (BM, also called ceratomandibularis or hyomandibularis) originates on the Skeletal elements A Angular distal tip of the first epibranchial and either merges BB Basibranchial (Copula) with the DMP to insert on the prearticular or inserts on BP Branchial plate Splits into BB and CBs on metamorphosis the hyomandibular ligament. In addition to depressing BH Basihyal the lower jaw, the BM is in a position to aid in hyobran- C Cornua chial depression by drawing the epibranchial tips dor- CB Ceratobranchial (Hypobranchial) CH Ceratohyal sorostrally. All exert dorsal and caudal components of co Coronoid (Splenial) force on the caudal side of the jaw joint. Contraction of D Dentary EB Epibranchial (Ceratobranchial); fused these muscles swings the lower jaw downward by ro- larval CB and EB in tating it about its articulation with the quadrate. some taxa HH Hypohyal In addition to those jaw depressors which span the L Lingual jaw joint, elongate ventral muscles may contribute to M Meckel's cartilage OG Otoglossal mouth opening by pulling the tip of the lower jaw pos- PA Prearticular (Gonial) teroventrally. These include the geniohyoideus [GH, R Radial R 1 formed from larval HH UH Urohyal (Second Basibranchial, also called the coracomandibularis (Lauder and Shaf- Os thyroideum) fer, 1985)l and the rectus cervicis superficialis and pro- Muscles fundus (RCS and RCP). The GH originates on the man- AA Adductores arcuum (Subarcualis obliquus, dibular symphysis and inserts on the urohyal. The RCS Transversus ventralis 1) BH Branchiohyoideus (Ceratohyoideus, (also called the sternohyoideus) originates from the Ceratohyoideus sternum and the RCS originates on the rectus abdomi- externus) CDSP Cephalodorsosubpharyngeus Formed from fusion of nus muscles, which in turn originate on the pelvis. The larval LAB and TV RCP (also called the abdominohyoideus) and RCS may BM Branchiomandibularis (Ceratomandibularis, Hyomandibularis) be indistinct from one another at their rostral ends, DM Depressor mandibulae where they insert on the basibranchial, first ceratobran- DMA Depressor mandibulae anterior DMP Depressor mandibulae posterior chials, or the branchial plate. These muscles can affect DT Dorsalis trunci mouth opening if the GH contracts simultaneously and G Gularis Formed from larval JHP the skull is prevented from flexing ventrally. The con- GG Genioglossus GGL Genioglossus lateralis Formed from larval GG nection between mandibles and ceratohyals by the hy- GH Geniohyoideus (Coracomandibularis) omandibular ligament may also affect mouth opening GHL Geniohyoideus lateralis Formed from larval GH GHM Geniohyoideus medialis Formed from larval GH as the hyobranchial apparatus is depressed (Reilly and HOYP Hebosteoypsiloideus Formed from larval RC Lauder, 1990). IMA Intermandibularis anterior (Submentalis) IMP Intermandibularis posterior Mouth-closing muscles include the levator (or ad- IH Interhyoideus ductor) mandibulae, which is divided into two main IHP Interhyoideus posterior (Sphincter colli, Interbranchialis) parts: the levator mandibulae externus (LME) and the IOQ Jn terossaquadrata Formed from larval IH levator mandibular internus (LMI). The internus is ITCS Intertransversarius capitis sometimes further divided into the internus anterior supe r io r IVE Intervertebral epaxial (LMIA) and internus posterior (LMIP).The LMIA and LAB Levatores arcuum branchiarum LME originate on the skull and the LMIP originates on LME Levator mandibulae externus LMI Levator mandibulae internus the atlas. All insert primarily on the prearticular, but LMIA Levator mandibulae internus also on the dentary of the lower jaw. These muscles are anterior LMIP Levator mandibulae internus positioned to produce primarily dorsal, but also medial posterior components of force on the rostral side of the jaw joint, LSV Lateral subvertebralis MSV Medial subvertebralis and swing the lower jaw upward or apply biting force. QP Quadratopectoralis Formed from larval JHP Suction feeding requires movements of the hyo- RC Rectus cervicis branchial apparatus in addition to movements of the RCP Rectus cervicis profundus (Abdominohyoideus) RCS Rectus cervicis superficialis (Stemohyoideus) jaws. Muscles of the hyobranchial apparatus are di- SAR Subarcualis rectus vided here into (1) hyobranchial depressors and leva- SH Subhyoideus Formed from larval IH TV Transversus ventralis tors, which produce primarily dorsoventral and ros-

~ ~ trocaudal movements, (2) branchial adductors and 'Synonyms are in parentheses. abductors, which produce lateral movements, and 74 Stephen M. Deban and David B. Wake

(3) hyobranchial stabilizers, which anchor or adjust the muscles are in a position to move the last epibranchial branchial tips. medially. Hyobranchial depressors swing the hyobranchial Branchial adductors move the epibranchial tips to- apparatus ventrally and caudally and are responsible ward one another. The BH may serve this function in for enlarging the buccal cavity during suction feed- some taxa. The subarcularis rectus 1 (SAR l), which ing. The RCS and RCP exert a caudal force on the originates on the ventral surface of the ceratohyal center of the hyobranchial apparatus. The branchiohy- and inserts on the first epibranchial, can adduct the oideus (BH, also called ceratohyoideus or ceratohyoi- epibranchial medially. Subarcualis rectus muscles 2 deus externus) originates on the ventral surface of the through 4 span the epibranchials and can move them ceratohyal, inserts on the tip of the first epibranchial, toward one another. The single or double adductores and may share fibers with the adjacent BM (Fig. 3.5A). arcuum (AA, also called the subarcualis obliquus or The BH pulls the epibranchial tip closer to the rostral transversus ventralis 1) runs from the ceratobranchial end of the ceratohyal, buckling the hyobranchial ap- or branchial plate to the second and third epibranchials paratus ventrad and pulling the epibranchial tip ven- and can adduct the epibranchials medially. This may trad. As mentioned previously, the BM may similarly close or open the gill slits, depending on the relative aid in hyobranchial depression. position of the first epibranchial, or may swing the Hyobranchial levators either cradle the hyobran- basibranchial relative to the epibranchial to return the chial apparatus or attach directly to it and function to hyobranchial apparatus to its resting position. compress the buccal cavity and return the hyobran- Hyobranchial stabilizers include the levatores ar- chial apparatus to its resting position. The geniohyoi- cuum branchiarum (LAB), which originate broadly on deus (GH) originates on the urohyal, inserts at the the dorsalis trunci muscles (DT) of the neck or on the mandibular symphysis, and pulls the center of the otic region of the skull and insert on the epibranchial hyobranchial apparatus rostrad. As mentioned earlier, tips (Fig. 3.5A). They are in a position to move the epi- because of its attachment to the mandibular symphy- branchial tips dorsally or rostrally or to anchor them sis, this muscle may also act as a mouth opener if the and prevent caudal excursion. hyobranchial apparatus is stabilized in its depressed The head is moved dorsally, ventrally, or laterally position. The intermandibularis posterior (IMP) origi- to direct the gape during suction feeding and to aid nates on the medial aponeurosis of the floor of the in prey manipulation and swallowing. Four sets of mouth and runs laterally to insert on the dentary and muscles can produce these movements. The dorsalis prearticular. A small intermandibularis anterior (IMA, trunci (DT) originates on the vertebrae and inserts on also called submentalis) is usually present, spanning the occipito-otic of the skull and can flex the head dor- the mandibular symphysis. The interhyoideus (IH) solaterally. The intervertebral epaxial muscle (IVE), originates with the IMP on the medial aponeurosis but sometimes not distinct from the DT, can also raise runs caudally as well as laterally to insert on the caudal the cranium. The intertransversarius capitis superior tip of the ceratohyal or on the hyoquadrate ligament. (ITCS) originates on the atlas, inserts on the occipito- An interhyoideus posterior (IHP, also called the inter- otic, and can deflect the cranium dorsolaterally. The branchialis or sphincter colli) is often distinct from the levator scapulae and cucullaris muscles originate on IH, lies just caudal to the IH, and runs from the dis- the pectoral girdle and insert on the skull and can flex tal tip of the first epibranchial medially to insert on the head laterally. The skull can be flexed ventrolater- the medial aponeurosis of the throat. The IMP, IH, and ally by the medial subvertebralis muscle (MSV),which IHP all raise the floor of the mouth, cradling and push- originates on the ribs of the first few vertebrae and in- ing the hyobranchial apparatus upward to its resting serts on the parasphenoid. The lateral subvertebralis position. The IHP may also function in branchial ad- (LSV) originates from the lateral body wall muscula- duction. ture, inserts in the otic region, and can flex the skull Branchial abductors move the epibranchials apart, laterally. opening the gill slits. The BH is in a position to abduct The IMP, IH, and IHP can raise the floor of the the first epibranchial laterally in some species (e.g., mouth and constrict the pharynx and may function in Ambystoma tigriunum), whereas in others (e.g., pletho- prey manipulation or swallowing. In addition to bran- dontids) it appears to move the epibranchial medially. chial adduction, the TV can constrict the pharynx and The tranversus ventralis (TV) muscles, which vary in aid in swallowing. The skull levators (DT, IVE, ITCS) number among taxa, originate at the midline on the and depressors (MSV, LSV), as well as the levator ventral surface of the pharynx and insert on or near the scapulae and cucullaris muscles, can aid in swallowing medial edge of the most medial epibranchial. The TV by moving the head. 3. Aquatic Feeding in Salamanders 75

B. Adult Morphology pad, whereas partially metamorphosing forms possess a raised glandular field in the floor of the mouth. Meta- Adult aquatic salamanders represent the full range morphosing species have tongues of various sizes and of metamorphic patterns, from completely larviform, degrees of complexity. Suction feeding forms tend to perennibranchiate species, such as the axolotl, to com- have smaller, simpler tongues, whereas those that use pletely metamorphosed forms, such as most newts. We tongue prehension in water have larger, more com- divide this spectrum of developmental patterns into plex tongues such as those of terrestrial species. Adult three groups, based on the overall degree of metamor- tongue morphologies of those species that use tongue phosis of the feeding system. (1)”Perennibranchiates” prehension will be presented in the next chapter. possess all or most larval features, including gill slits, The labial lobes of adult salamanders are of two external gills, posterior branchial elements, and inter- types: those that are essentially retained larval features locking labial lobes. They possess few adult features, and those that form after metamorphosis. Labial lobes such as maxillae and a tongue pad. This group includes of the larval type are found in all larval and perenni- all of the Sirenidae and Proteidae and some members branchiate salamanders and in many partially meta- of other families. (2) ”Partial metamorphs” possess a morphosing forms. Sirenids have by far the most ex- mixture of larval and adult features. They may lose extensive labial lobes of this type; the lateral gape is ternal gills and gill slits, but may retain labial lobes and entirely occluded and the mouth forms a small, rect- posterior branchial elements. They possess maxillae angular anterior opening. Cryptobranchus is unusual and a rudimentary tongue pad. This group includes all in that it retains larval labial lobes on the lower jaws, members of the Cryptobranchidae and Amphiumidae, but not on the upper jaws. The fully aquatic, suction as well as ambystomatids formerly placed in the ge- feeding ambystomatids formerly placed in the genus nus Rhyacosiredon. (3) “Metamorphs” have lost exter- Rhyacosiredon (now placed in Ambystoma) retain lar- nal gills, gill slits, posterior branchial elements, inter- val labial lobes and otherwise appear to be partially locking labial lobes, and have fully formed maxillae metamorphosed (Reilly and Brandon, 1994).The labial and tongue pads with intrinsic tongue muscles. This lobes of aquatic adult salamandrids and hynobiids are group includes the newts and all terrestrial and semi- of the second type and only form on the upper jaw. aquatic salamanders. The adult morphology of meta- These adult labial lobes are simple flaps and are not morphs and partial metamorphs is the focus of this sec- homologous to the more complex, interlocking larval tion. Perennibranchiate adults are considered here as lobes. well, but are emphasized in the previous section on lar- All perennibranchiate and many partially metamor- val morphology. phosing forms possess gill apertures. Cryptobranchus Unlike the heads of larval and perennibranchiate and Amphiuma possess one gill aperture, or spiracle on salamanders, which have pointed or tapered rostra, each side of the head. Andrias has no gill openings. Pe- the heads of metamorphosed and partially metamor- rennibranchiate forms may possess a gular slit, whereas phosed salamanders are more rounded and blunt. some partially or completely metamorphosing forms The external gills and tail fin are lost, the eyes pro- possess a fold in this location. Cryptobranchoids and trude, and eyelids form. In addition to these superficial the fully aquatic salamandrid, Pachytviton, are unusual changes, which occur at metamorphosis, deeper alter- in having longitudinal folds in the buccal floor that ac- ations are made in most components of the feeding sys- commodate ventral expansion. Cryptobranchids also tem, including the teeth, tongue, jaws, skull, hyobran- retain the larval anterior fold beneath the hyoid and chial apparatus, and many muscles of the head. are capable of perhaps the greatest increases in buccal The teeth of metamorphosed salamanders consist volume of any salamander. of a bony pedicel attached by fibrous connective tissue to an enamel-coated crown. Teeth of metamorphosed 1. Adult Skull, Jaws, and Hyobranchial Apparatus animals are either monocuspid or dicuspid, with various crown shapes, including clubs, discs, and spikes. Metamorphosis from the larval to adult form in- Older perennibranchiate and metamorphosing animals volves changes in the skull, jaws, and hyobranchial ap- possess biscupid, subpedicellate teeth. The dentition paratus. These changes are presented here in order to is generally monostichous and homodont (Beneski and introduce the adult form of these skeletal systems. Ele- Larsen, 1989a,b). Partially metamorphosing species ments that do not change substantially during meta- may possess bicuspid teeth (Erdman and Cundall, 1984; morphosis are not mentioned in this section. Elwood and Cundall, 1994). During metamorphosis, elements of the skull are Perennibranchiate forms generally lack a tongue lost, appear, or are remodeled, and further ossification 76 Stephen M. Deban and David 8. Wake and expansion occur. In addition to the bones pres- ing metamorphosis. Ligamentous and connective tis- ent in the larva, some of which enlarge and overlap, sue attachments to surrounding skeletal elements are prefrontals, lacrimals, nasals, and septomaxillae may variable. A hyoquadrate ligament or hyomandibular develop in the rostrum of the skull, paralleling the ligament persists or develops in adults of some taxa, developmental appearance of rostral elements in the such as plethodontids. This ligament may be replaced hyobranchial apparatus. Some taxa, particularly hy- in some of the Salamandridae (e.g., Taricka) by a nobiids, already possess many of these elements as lar- hyosuspensory ligament between the upper quadrate vae (Fig. 3.3). and the posterior tip of the ceratohyal (Findeis and During metamorphosis, the jaws are strengthened. Bemis, 1990). The hypohyals, when present in the larva, The maxilla appears or broadens its attachments to the may vanish entirely or give rise to adult elements, such skull. The vomer and premaxilla enlarge and reinforce as the radial cartilages found in the Ambystomati- their connections with the skull, and the orientation of dae, Rhyacotritonidae, Dicamptodontidae, and Hyno- vomerine tooth rows changes with the change in shape biidae. The ceratohyal loses its connection to the basi- of the vomer. Dentate extensions of the vomer mi- branchial, except in hynobiids, ambystomatids, and grate posteriorly onto the parasphenoid, and the tooth- dicamptodontids. In these taxa, the ceratohyals and bearing, palatine portion of the palatopterygoid is lost. basibranchial are connected by narrow radial carti- The dentaries become more heavily ossified and abut lages (see Batrachuperus, Fig. 3.6). In some hynobiids, at the symphysis, and the coronoid is lost (except in these cartilages form elongate loops, which cross in a Dicamptodon in which only the teeth are lost). Meckel's figure-eight fashion over the midline and connect the cartilage is reduced and the dentary and prearticular two ceratohyals (Cox and Tanner, 1989; Larsen et al., may fuse to one another. The jaw articulation is repos- 1996).The developmental appearance of new elements itioned posteriorly so that it comes to lie behind the at the rostral end of the hyobranchial apparatus is com- orbit as the squamosal and quadrate swing posteriorly, mon among salamanders, and these new elements may increasing the gape. articulate with the basibranchial, for example, the sec- The hyobranchial apparatus of perennibranchiate ond radii, otoglossal cartilage, or lingual plate of the species is essentially larval in configuration. In some Ambystomatidae and Dicamptodontidae (Krogh and taxa, such as Proteus, extensive ossification occurs, but Tanner, 1972) and Salamandridae (Ozeti and Wake, all larval elements are retained (Marche and Durand, 1969), or may lie adjacent to it, like the basihyals and 1983). In metamorphosing taxa, the transformation hypohyals of the Amphiumidae and Cryptobranchi- from the larval to the adult hyobranchial configuration dae. In some taxa, anterior projections of the basibran- involves loss, remodeling, and often ossification of ele- chial, called cornua, form and support the adult tongue ments. The posterior branchial arches are lost, typically pad (Fig. 3.6). In some plethodontids a separate lin- leaving two pairs of ceratobranchials and one or two gual cartilage forms at the tip of the basibranchial and pairs of epibranchials in the adult. Some terrestrial functions in rotation of the tongue pad (Lombard and members of the Salamandridae lack discrete first cera- Wake, 1977). tobranchials as adults, and the epibranchials appear The articulations between the basibranchial and cer- elongated. These adult elements are probably the prod- atobranchials are altered at metamorphosis. The bran- uct of fusion of the larval first ceratobranchials and chial plate of the larvae of some taxa gives rise to sepa- first epibranchials and are called the epibranchials. The rate basibranchial and ceratobranchials. The urohyal epibranchial and ceratobranchial persist as a separate loses its attachment to the basibranchial and may dis- element in all aquatic members of the Salamandridae. appear altogether, as in many salamandrids. In the Plethodontidae the larval epibranchials disin- Complete metamorphosis of the hyobranchial ap- tegrate completely and a new adult epibranchial de- paratus makes tongue protrusion possible. The cera- velops at metamorphosis from undifferentiated tissue tohyals are freed somewhat from the remaining ele- (Alberch and Gale, 1986).In the Hynobiidae, two pairs ments, allowing folding and forward movements of of epibranchials persist, the first cartilaginous and the the rest of the apparatus to which the tongue pad is second bony. The Cryptobranchidae show variation in attached. the degree of metamorphosis of the hyobranchial sys- The ossification pattern of the hyobranchial appara- tem. Cryptobranchus has a larval number of posterior tus varies taxonomically (Fig. 3.6). Only the urohyal, elements, but with more ossification and mineraliza- when present, is universally ossified. Aquatic pletho- tion than in the larva, whereas Andrias loses the more dontids, which do not suction feed, such as Desmog- posterior epibranchials (Cox and Tanner, 1989). natkus marmouatus, possess slender cartilaginous hyo- The ceratohyal becomes thinner and more blade-like branchia; only portions of the basibranchial are ossi- anteriorly and narrowed and elongate posteriorly dur- fied. In other taxa, the basibranchial, epibranchial tips, 3. Aquatic Feeding in Salamanders 77

Batrachuperus mustersi Cryptobranchus alleganiensis Leurognathus mannoratus J

Rhyacosiredon rivularis Pachytriton sp. Pleurodeles waltl

FIGURE 3.6. Hyobranchia (in ventral view) of adults of metamorphosing and partially metamorphosing salamanders from five families. Bone or mineralization is shaded and cartilage is unshaded. Some elements are cut away to reveal underlying elements or the outlines of underlying elements are shown as dashed lines. Scale bars equal 1 cm. See Table 3.1 for abbreviations. Cryptobranchus drawing is adapted from Elwood and Cundall (1994). 1. Morph. 220, 47-70. Copyright 0 1994. Reprinted by permission of Wiley-Liss, Inc., a sub- sidiary of John Wiley & Sons, Inc. and posterior portion of the ceratohyal are frequently In partially metamorphosing taxa, such as crypto- ossified. Almost the entire apparatus may ossify in branchids and amphiumids, the hyobranchial appara- suction-feeding members of the Salamandridae, such tus of the adult retains some larval features. Hypohyals, as Puchytriton, with only the rostral portion of the as well as basihyals, are present in the adult. Articula- ceratohyal remaining cartilaginous (Ozeti and Wake, tions between hyobranchial elements are strengthened 1969). Rhyacosiredon has a more robust hyobranchial during development. The anterior hyobranchial ele- apparatus than other ambystomatids and shows exten- ments of cryptobranchids remain cartilaginous, even in sive ossification of the epibranchials and ceratohyal, as large animals, and are extremelybroad, filling the space well as ossification of the first ceratobranchial.Crypto- between the mandibles (Cox and Tanner, 1989; Elwood branchoids show an unusual, but consistent pattern of and Cundall, 1994). The hypohyals of Rhyacosiredon ossification of the second ceratobranchial and epibran- have a morphology intermediate between the larval chial, which may be indicative of an unusual method configuration and that of the adults of fully metamor- of force transmission during feeding (see Section 111,D). phosing ambystomatids (Reilly and Brandon, 1994). 78 Stephen M. Deban and David B. Wake

Posterior epibranchials persist in amphiumids, as well morphosis and are known as the DM thereafter. In as in Cryptobrunchus in which the third epibranchial desmognathine plethodontids, the tendon associated calcifies. The first epibranchial and ceratobranchial with the LMIP is enlarged at metamorphosis, forming fuse to one another to form a single element, the epi- the distinctive atlanto-mandibular ligament (Schwenk branchial, in amphiumids, cryptobranchids, and some and Wake, 1993). hynobiids (Fig. 3.6). In amphiumids, the second cera- The BH is lost at metamorphosis in metamorphos- tobranchial is absent, even in larvae. ing and partially metamorphosing taxa. The SAR 1 en- In sirenids and proteids, the anterior ceratohyal, the larges, often forming a muscular bulb around the first basibranchial, and ceratobranchials ossify. In sirenids epibranchial (or ceratobranchial in those species that the basibranchial is particularly unusual: the anterior lack a separate epibranchial), and shifts its function to tip is bulbous where it meets the ceratohyals (Cope, tongue protrusion. In partially metamorphosing forms 1889).In proteids the epibranchials also ossify (Fig.3.4). (i.e., cryptobranchids and amphiumids) and in many Some taxa show divergent skull and jaw morpholo- newts, the SAR 1 replaces the BH in position and func- gies. Sirenids, amphiumids, and Proteus have elong- tion (Fig. 3.5B). The remaining SAR muscles are lost. In ate, tapered heads and jaws, whereas cryptobranchids plethodontids, a geniohyoideus lateralis (GHL) arises have broad, rounded heads and jaws. Amphiumids from the GH, which then becomes known as the ge- have enlarged jaws, teeth, and jaw musculature and niohyoideus medialis (GHM). The GHL originates on are capable of a powerful bite; they can bite violently the mandible lateral to the symphysis and inserts on when handled. Members of the Salamandridae have the lateral edge of the ceratohyal. The GHM retains its particularly robust skulls; many possess a bony arch larval origin and insertion, but the urohyal separates joining the frontal and squamosal and some have from the basibranchial before metamorphosis is com- the maxilla and pterygoid abutting. Cryptobranchoids plete. The posterior attachment of the GH shifts to the possess an ossified angular element in the lower jaw RCS in those taxa lacking a urohyal. The GHM loses its (Noble, 1931), and the mandibular symphysis forms a function in drawing the hyobranchial apparatus ante- joint consisting of cartilaginous pads and collagen lig- riorly and becomes a buccal stabilizer in plethodon- aments, allowing the mandibles to flex considerably tids. In other taxa, the GH similarly loses its attachment ventrally and dorsally with respect to one another to the basibranchial and acts as a sling that can stabi- (Cundall et ul., 1987; Elwood and Cundall, 1994). This lize or raise the hyobranchial apparatus. The rectus unilateral jaw depression is possible only because the cervicis (RC) muscles become more distinct as pro- mandibles are unusually strongly curved. Their cur- fundus (RCP) and superficialis (RCS). A superficialis vature allows them to swing independently of one lateralis (RCSL) slip may form in plethodontids. The another, producing an anterolateral gape when one entire group of RC muscles functions in tongue reside is depressed relative to the other. Desmognathine traction or hyobranchial depression. A hebosteoy- plethodontids have specializations associated with a psiloideus (HOYP) muscle, the function of which is strong bite, including stalked occipital condyles, modi- unknown, becomes distinct from the RC group at fied anterior vertebrae, and robust skulls (see Schwenk metamorphosis in plethodontids, originating on the and Wake, 1993, and references therein). urohyal (or basibranchial) and inserting on the RCP near the sternum (Lombard and Wake, 1977). Among the dorsal muscles of the head and neck, 2. Adult Head Musculature only the IVE changes significantly at metamorphosis, Muscles change in size, orientation, and function becoming distinct from the DT. This new muscle func- during metamorphosis and may be lost, form, or give tions in cranial elevation. rise to new muscles. In general, more muscles are lost The metamorphic fate of the superficial throat than appear, mostly those associated with gill and epi- muscles varies among taxa and has been the source branchial movements, including the SAR muscles (ex- of much nomenclatural confusion. In plethodontids, cept SAR l), AA, and LAB (Fig. 3.5B). Those feeding the IHP of the larva gives rise to both the quadrato- muscles that typically change during metamorphosis pectoralis (QP) and the gularis (G) of the adult. The G are emphasized here. is the only remnant of the IHP to persist in most adult The BM is lost or shifts its posterior attachment from plethodontids. The desmognathines and Axeides pos- the epibranchial tip to merge with the DMP and fan sess both; the QP becomes a strong head depressor, out posteriorly onto the fascia cephalodorsalis, thereby shifting its dorsal attachment from the epibranchial to losing its role in hyobranchial depression. The new the quadrate, and shifting its caudal attachment to the combined muscle is called the DMP. In some taxa the pectoral fascia. The G in these taxa is a small strap DMA and DMP become indistinguishable at meta- muscle that lies against the QP. In adults of all other 3. Aquatic Feeding in Salamanders 79 salamander taxa (i.e., nonplethodontids), the IHP re- they use a particular modality. Larvae and perenni- tains its general larval position or shifts its origin to the branchiate forms typically rely on mechanical, electri- fascia cephalodorsalis, but is still called the IHP (Piatt, cal, and olfactory senses, but can use vision as well 1940). (Luthardt-Laimer, 1983; Besharse and Brandon, 1974). In the Salamandridae and Hynobiidae, the IH of the Adults of metamorphosing forms rely to a lesser de- larva splits to give rise to the anterior subhyoideus gree on olfactory and lateral line stimuli; they use pri- (SH) and the posterior interossaquadrata (IOQ). The marily vision and have well-developed eyes. SH originates from the posterior end of the ceratohyal The eyes of salamanders have all the components of and inserts anteriorly on the dorsal fascia of the IMP or typical vertebrate eyes, including a cornea, lens, iris on the mandible near the symphysis, and upon con- and pupil, and multilayered retina of cells and fibers. traction draws the ceratohyal rostrally (Fig. 3.5B). The The retina includes photoreceptors (rods and cones), IOQ may shift its insertion from the ceratohyal to the horizontal cells, bipolar cells, amacrine cells, and gan- quadrate. In adults of all other families, the IH retains glion cells. The cornea is flat and the lens is spherical, its larval position (Krogh and Tanner, 1972) and name. suited for an aquatic environment in which only the The cephalodorsosubpharyngeus (CDSP) forms from lens and not the cornea is responsible for focusing the the fusion of the posterior larval TV and LAB muscles image (Roth, 1987). Salamanders are capable of color and is in a position to constrict the pharynx and aid in vision, and larvae and aquatic adults are more sensi- swallowing. tive to longer wavelengths of light (which predominate A genioglossus (GG) forms or is elaborated during in water) than terrestrial adults (Himstedt, 1973a,b). metamorphosis, originating on the mandibular sym- Focusing on near objects such as prey is accomplished physis and fanning out into the tongue pad. The GG by contraction of the protractor lentis muscle, which draws the tongue pad toward the mandibular symphy- moves the lens away from the retina. The eyes are re- sis. In Cryptobranchus, this muscle inserts on the hyo- duced and covered with skin in many cave-dwelling pohyals and acts as a hyobranchial levator (Elwood salamanders, many of which are perennibranchiate. and Cundall, 1994). In ambystomatids, the GG gives These species show a decrease in overall eye size and a rise to the genioglossus lateralis (GGL), which inserts degeneration of the retina and optical structures. Eye- on or in the vicinity of the lateral edge of the ceratohyal lids are lacking in larval and perennibranchiate sala- (such as the GHL in plethodontids) (Larsen and Guth- manders, cryptobranchids and amphiumids; they are rie, 1975). Rhyacotritonids may possess both SH and reduced in some fully aquatic salamandrids and hy- GGL (Krogh and Tanner, 1972). These muscles and the nobiids, and Rkyacosiredon, and are present in fully intrinsic tongue muscles, which also form at metamor- metamorphosed salamanders. phosis, function primarily in tongue prehension and The optic nerve, which consists of the axons of the will therefore be discussed in the next chapter. retinal ganglion cells, crosses the optic nerve of the Feeding muscles are divided into two series, bran- contralateral eye at the optic chiasm and enters the di- chiomeric and hypobranchial, based on developmental encephalon from below. Fibers terminate in, or project origin and innervation. The branchiomeric (branchial) to, various parts of the diencephalon (e.g., thalamus series includes the majority of the feeding muscles, and pretectum), the optic tectum in the dorsal por- is innervated by visceral motor components of the tion of the mesencephalon, and the tegmentum in the nervous system, and forms from the embryonic myo- ventral portion. Most fibers of the optic nerve travel meres. Branchiomeric feeding muscles include IM, to the contralateral side of the thalamus, pretectum, IMP, IH, SH, IHP, LM, DM, BH, LAB, and SAR. The and tectum; however, some ipsilateral projections hypobranchial series forms from rostral growths of exist (Fig. 3.7). The proportion of ipsilateral projec- myotomes behind the branchial area, is innervated by tions varies among taxa and developmental stages. somatic motor components of the nervous system (i.e., Proportionally more ipsilateral projections are present the hypoglossal nerve), and includes the GH, GHL, after metamorphosis in those taxa with larvae. Ipsilat- GG, GGL, RCP, and RCS and the intrinsic muscles of eral projections are most abundant in completely ter- the tongue pad. restrial forms, especially those with greatly overlapping visual fields and binocular vision, such as bolitoglossine plethodontids (Roth, 1987). Information C. Sensory and Motor Systems from the optic tectum is relayed through three de- Larval and adult salamanders foraging in water are scending tecto-bulbar tracts to the brain stem where presented with the same array of sensory stimuli and motor nuclei controlling feeding muscles reside (Dicke generally use the same set of sensory modalities to de- and Roth, 1994). tect and localize prey, but differ in the degree to which Salamanders possess two olfactory systems: the 80

FIGURE 3.7. Sensory-motor schematic of the feeding system of a generalized salamander, showing both larval and adult features. Sensory information entering the eyes, nostrils, and lateral line organs is integrated in the telencephalon, diencephalon, and mesencephalon. These centers activate motor nuclei (numbered ovals) in the brain stem, which control the contraction of muscles (striped gray) through cranial nerves (black lines) and consequently produce feeding movements of the jaws and hyobranchial apparatus (solid light gray). Nerves and brain tracts are solid black lines or gray channels and muscle innervations are shown as black dots, and sense organs and parts of the brain are shown in white or dark gray. Motor nuclei are numbered according to the cranial nerves they supply. See Table 3.1 for muscle abbreviations. 3. Aquatic Feeding in Salamanders 81 primary olfactory system and the vomeronasal organ are represented as a topographical map (Bartels et aZ., or accessory olfactory system. The main olfactory sys- 1990). Salamanders use lateral line information to de- tem includes the nasal epithelium with chemosensory tect predators as well as to localize and orient to mov- olfactory cells, each of which has many filaments ex- ing prey and to direct the predatory strike (Himstedt posed to the nasal chamber which are capable of re- et al., 1982). sponding to molecules in the environment. Axons of Salamanders are capable of detecting prey using vi- olfactory cells form the first cranial nerve, which pro- sual, olfactory, tactile, and lateral line receptors and are jects to the olfactory bulbs of the forebrain (Fig. 3.7). most responsive to live, active prey. Aquatic salaman- The vomeronasal system opens into the nasal chamber ders use olfactory and visual cues for initial orientation and has receptors in a separate sac, lateral to those of to prey and to direct the prey-capture strike (Martin the main olfactory system (Dawley, 1988), and has et al., 1974), but also use mechanoreception and elec- a separate accessory bulb in the brain (Eisthen et al., troreception (Joly,1981; Himstedt,l967; Griffiths, 1993). 1994). Plethodontids possess the additional feature of Cave salamanders may have slender, elongate legs, nasolabial grooves, which form at metamorphosis and which are used during foraging to lift the body above which conduct substrate-borne molecules to the the substrate and enhance mechanoreception by ex- vomeronasal sac. This vomeronasal system is impor- posing more of the lateral line system to water move- tant in courtship behavior and may be used in prey ments (Peck, 1973).Blind urodeles, such as Proteus, are tracking. sensitive to olfactory stimuli and will respond readily Taste buds on the tongue and pharynx are used to to immobile, dead prey, whereas salamanders that use reject distastful or noxious prey. The glossopharyngeal vision are less responsive to dead prey and olfactory nerve (cranial nerve IX) conducts impulses from the cues and rely on prey movement (Durand et al., 1982; taste buds to the brain. Additional taste buds are pres- Uiblein et aZ., 1992). In light, vision dominates prey ent on the skin and may be used to locate prey. localization and inhibits olfactory detection; darkness The lateral line system is present in all aquatic sal- (or blindness) appears to release this inhibition (Roth, amanders and is used to detect water currents and 1987). electrical charges. The lateral line system is closely as- Feeding movements are controlled by clusters of sociated with the auditory system and the two are col- motor neurons or motor nuclei of the brain stem (Roth lectively called the acousticolateralis system. Lateral et al., 1990).Motor nuclei of the feeding muscles are ar- line detectors form series of small depressions or raised ranged in two columns along each side of the brain "stitches" on the head and along the body, containing stem from the medulla oblongata to the second spinal ampullary organs, neuromasts, or pit organs. Ampul- nerve (Fig. 3.7). The motor nuclei supply axons to the lary organs are present on the head and function as cranial and first and second spinal nerves, which inner- electroreceptors, which can detect the tiny electrical vate the feeding muscles (Piatt, 1938). The trigeminal fields generated by the muscle contractions of prey up (cranial nerve V) innervates the IMP and LM. The fa- to a few centimeters away (Bartels et al., 1990). Neuro- cial (VII) innervates the IH, SH, BH, and DM. The glos- masts and pit organs extend down the head, body, and sopharyngeal (IX) innervates the SAR 1. The vagus (X) tail and are mechanoreceptive, containing sensory hair innervates the AA, LAB, SAR 2-SAR 4, TV, CDSP, and cells that are responsive to water movements and pres- the SAR 1 of adults of some taxa (e.g., plethodontids). sure changes. Larval salamanders possess all three The accessory (XI) serves the cucullaris. The hypoglos- types of receptors, as do some aquatic adult salaman- sus (XII, formed from first and second spinal nerves) ders (Fritzsch and Wahnschaffe, 1983). Lateral line or- innervates the GG, GGL, GHM, GHL, RCP, RCS, and gans become covered with epidermis in salamanders muscles of the tongue pad. that spend time out of water, such as Notopkthalrnus Salamanders must gather sensory information about and Siren, but become exposed to the skin surface and their prey and produce the appropriate behavior to become functional again when the salamander returns make a successful capture. Information is perceived by to water (Dawson, 1936; Reno and Middleton, 1973). the sense organs and is processed in the brain, which Axons of sensory cells of the lateral line system enter then activates motor nuclei in the brain stem, contract- the brain through five separate nerves in the vicinity of ing muscles in the proper sequence to generate coor- the auditory nerve (VIII) and project to the acoustico- dinated movements of the body, head, jaws, and throat. lateral area of the somatic sensory column of the me- Most if not all of the sensory and motor components of dulla (Northcutt and Brandle, 1995). Lateral line in- the feeding system are known. However, the specific formation is relayed to the tectum of the midbrain, nuclei and connections of the brain that are involved where it is processed and where the lateral line sensors in integrating the various sensory inputs (olfaction, 82 Stephen M. Deban and David B. Wake lateral line, vision) and in producing the appropriate cavity. Salamanders that lack or have a reduced num- activation of motor nuclei are as yet undetermined. ber of gill slits expel water slowly out of the mouth, Sensory-motor integration in amphibians in general re- which is held ajar. Gill rakers or teeth prevent the prey mains a rich area of research. from escaping during water expulsion. Suction feeding requires special morphology to be successful, including a robust hyobranchial apparatus 111. FUNCTION and associated musculature to generate rapid and forceful buccal expansion and labial lobes or other A. Ingestion Behavior and Kinematics means of restricting water flow to the front of the mouth. The coordination of buccal expansion and The feeding behavior of salamanders has been di- mouth opening is also important for successful suction vided into four stages: orientation, approach, fixation, feeding, although some variation in these two behav- and snapping (Roth, 1987).Orientation involves lifting iors exists. the head from the substrate and directing it toward the Variation in suction feeding behavior across taxa or prey item. Approach involves walking or swimming developmental stages involves changes in the extent, toward the prey item until it is within reach. Fixation timing, and duration of jaw and hyobranchial move- is a period during which the salamander assesses the ments during the prey-capture strike. Comparative prey, usually while the prey is stationary. Snapping, or studies of feeding behavior make use of kinematic striking, is the ingestion behavior: suction feeding or analysis of the movements of the jaws and throat dur- tongue or jaw prehension, sometimes combined with a ing prey capture. These movements are confined pri- lunge. Snapping is typically triggered, or "released," marily to the sagittal plane, so are best visualized in by prey movement. Snapping usually occurs so rapidly lateral view, and are typically rapid and must be cap- that it is effectively invisible to the eye and has been tured by high-speed videography or cine. Gape cycle difficult to describe or analyze until recent technologi- durations for some representative taxa are as fol- cal advances in high-speed cinematography and vi- lows: 17-30 msec in larval Desmognathus quadramacu- deography. The other stages occur at a speed that is latus (Deban, personal observation), 35-47 msec in observable to the unaided eye. The four stages are of- larval Salamandra salamandra (Reilly, 1995), 40 to over ten discrete, but some may be absent or blend together. 80 msec in adult Cryptobranchus (Elwood and Cundall, For example, if the prey is already within reach, the 1994) and Amphiuma tridactylum (Erdmann and Cun- approach may be omitted, or if the prey is moving con- dall, 1984), and 80-110 msec in larval Ambystoma mexi- tinuously the fixation period may be skipped. Sala- canurn (Lauder and Shaffer, 1985). manders may also perform an olfactory test, in which Quantification of the strike by kinematic analysis in- the snout is pressed downward onto or near the prey, volves recording the positions of various anatomical after the fixation stage but before striking at stationary points throughout the course of the behavior (i.e., on Prey. each frame of a video sequence). Displacements, distances, angles, and velocities can be calculated from 1. Suction Feeding these position data, as can the timing and duration of Snapping in most aquatic salamanders involves gen- events. Quantification of behavior in this way facili- erating intraoral suction to capture prey, During suc- tates comparisons across taxa or developmental stages. tion feeding, the mouth is opened while the buccal Such data can then be visualized by kinematic pro- cavity is expanded. This expansion creates a drop in files, which depict distances or the positions of points buccal pressure relative to ambient pressure, causing through time (Fig. 3.8). Two measures typically made water and prey to flow into the mouth. The gill slits are on suction feeding salamanders are gape distance, or closed and labial lobes restrict the mouth opening to the distance between the tips of the jaws, and hyobran- the front. The head is raised during mouth opening. chial depression distance, or the distance between the This allows for ventral excursion of the lower jaw and top of the neck and the ventralmost point on the throat. also serves to aim the gape at the prey. The buccal Gape distance and hyobranchial depression distance cavity continues expanding as the mouth is closed and both increase and then decrease during the suction the head is lowered, resulting in continuous water flow feeding behavior. The kinematic profile of gape dis- throughout the gape cycle. The gill slits open before tance (the gape profile) typically appears as a bell- mouth closure and before maximum buccal expansion. shaped curve (Fig. 3.8). The hyobranchial profile ap- After the mouth closes, water is expelled slowly pears as a skewed curve, showing a rapid increase and through the open gill slits by compression of the buccal a slower decrease. By plotting both kinematic profiles 3. Aquatic Feeding in Salamanders 83

2.0 I I I I I I I I I I I I Hyobranchial Depression h E 1.5 I I I E I v ;.----e.- E 1.0 - I I c CU cm 0 0.5

0.0

-4

-8 0 4 8 12 16 20 24 28 32 36 40 44 Time (ms) FIGURE 3.8. Kinematic profiles of jaw, hyobranchial, and head movements through the course of a single suction-feeding event in a larval Desrnognathus quaduumaculatus (snout-vent length is 30 mm). Hyobranchial depression that continues into mouth closing is typical of suction feeding. The head angle increases as the head is raised during mouth opening, directing the gape at the prey, and later decreases as the head is tucked during and after mouth closing. against the same time axis, the temporal relationship of 2. Tongue Prehension the two movements can be seen. Figure 3.8 shows the Tongue prehension is used to capture prey by all typical pattern for suction feeding: mouth opening and terrestrial salamanders and by several aquatic sala- closing occur much more rapidly than hyobranchial de- manders (e.g., some plethodontids and rhyacotrito- pression and elevation, and maximum gape is reached nids) (Schwenk and Wake, 1988; personal observation). before maximum hyobranchial depression. Kinematic The behavior involves forward movement of the hyob- profiles of this type are used to examine how the re- ranchial apparatus which propels the tongue out of the lationship between the two movements might vary mouth. The SAR and SH muscles protract the tongue, among taxa or with different prey types. In addition to and the RCS and RCP muscles retract it. Several gape and hyobranchial distance, other kinematic vari- muscles of the tongue tip rotate and shape the tongue ables differ among suction feeding salamanders, in- pad. The gape profile is usually not bell shaped as in cluding the angle between head and body (Fig. 3.8) suction feeding, but often has a plateau region of con- and the distance of forward lunging. For example, stant gape corresponding with tongue protrusion. Cryptobrunchus shows especially large buccal expan- Gape increases to its maximum not as the tongue is sion for its size, and both Cvyptobvanchus and Am- protruded, but rather as the tongue returns with the phiumu display pronounced head dipping on mouth prey to the mouth, producing a three- or four-part closing (Reilly and Lauder, 1992).Cryptobranchids are gape profile. unique in that they often display asymmetrical kinematics during capture and intraoral transport in which 3. Jaw Prehension one side of the lower jaw or hyobranchial apparatus is abducted more rapidly or farther than the other side Prey capture by jaw prehension is used in both aqua- (Elwood and Cundall, 1994). tic and terrestrial feeding and involves movements of 84 Stephen M. Deban and David B. Wake the jaws and little movement of the hyobranchial ap- traction of the eyeballs, and movements of the head. paratus. A forward lunge of the body or lateral turn of The tongue may be used as well in salamanders that the head is used to bring the jaws to the prey. The gape possess it. Swallowing is similar in both terrestrial cycle produces a bell-shaped profile similar to suction and aquatic salamanders, involving contraction of the feeding, but the hyobranchial apparatus shows ex- transverse throat musculature (IM, IH, G, QP, CDSP, tremely small excursions relative to those seen during TV) and retractor bulbi, which squeeze prey down suction feeding. the esophagus. The dilator and constrictor laryngis muscles open and close the larynx and glottis except B. Prey Processing in plethodontids, which lack these muscles. Peristaltic contractions of the smooth muscles of the esophagus After prey is captured, it must be prepared for then move prey to the stomach. swallowing. Salamanders usually swallow their prey whole, without chewing or reducing it, although there C. Functional Morphology are some exceptions, such as cryptobranchids and amphiumids. Processing prey usually involves only posi- Prey capture, intraoral transport, and processing tioning it in the oral cavity and lubricating it with mu- are accomplished by movements of the jaws and hyo- cus. Occasionally, prey that protrudes from the mouth branchial apparatus. The type of hyobranchial move- after capture is pushed against the substrate to orient ments and relative timing of jaw and hyobranchial it or to move it into the mouth. The head is sometimes movements differ among the various feeding behav- thrashed laterally to orient the prey, to reduce it, or to iors (suction feeding, tongue prehension, and jaw pre- break it free from the substrate. Prey is sometimes hension). The hyobranchial apparatus is thrust for- moved into and out of the mouth across the teeth re- ward (tongue prehension), swung backward (suction peatedly by water flow to center it; this may have the feeding), or held relatively stationary (jaw prehension) effect of macerating the prey. The forelimbs are not by different patterns of muscle activity. The muscles in- used in prey manipulation. Like prey capture, intraoral volved in each of these behaviors, as well as their hy- transport of prey involves coordinated movements of pothesized roles in producing feeding movements, are the jaws and hyobranchial apparatus and can be ac- discussed in this section. Feeding movements are dis- complished by suction or tongue movements. cussed as though they are symmetrical, although some Suction-based transport of prey within the mouth to taxa, such as cryptobranchids, are known to move the esophagus is achieved by movements similar to asymmetrically (e.g., Cundall et al., 1987). Again, suc- suction-feeding movements (Gillis and Lauder, 1994). tion feeding is emphasized over tongue and jaw pre- Prey is moved toward the esophagus by currents of in- hension; the latter behaviors are covered in the next flowing water and held with the teeth or pressed to the chapter . roof of the mouth until the next cycle of intraoral trans- The buccal expansion of suction feeding is produced port. This process is repeated until the prey is in a po- by the hyobranchial apparatus and its associated mus- sition to be swallowed. culature (Fig. 3.5). The hyobranchial apparatus at rest Lingual-based prey transport (hyolingual transport) is folded and lies in the floor of the mouth and the is accomplished by rapid cyclical movements of the throat and rather close to the palate. During buccal ex- hyobranchial apparatus and tongue. The prey adheres pansion, it is swung ventrally and caudally about its to the tongue pad and is moved caudally and ventrally attachments to the lower jaw, skull, and neck. The at- in the mouth. As the tongue is moved forward for the tachments of the ceratohyal to the jaw joint and of the next cycle, the teeth and jaws prevent the prey from epibranchials to the neck and skull form the dorsal being pushed forward. This ratchet-like process slowly points of rotation for this hyobranchial depression. The moves prey toward the esophagus. Movements of the basibranchial retains its horizontal orientation, but is cranium, for example, head tucking in desmognathine translated downward and backward. In addition to ro- plethodontids (Schwenk and Wake, 1993), may assist tation around joints, elasticity of the cartilaginous ele- in forcing prey toward the rear of the throat. The ments has been proposed to play a role in some move- tongue is first moved forward in the mouth, pressed ments of the hyobranchial apparatus, such as opening against the prey, and then retracted rapidly, producing and closing of the gill slits (Severtsov, 1966).The entire a drop in the floor of the buccal cavity similar to that apparatus may move slightly dorsoventrally as well seen in suction feeding. This process is repeated until because the points of rotation at the jaw joint and neck the prey is swallowed. are somewhat mobile. Also, the distal tips of the cera- Swallowing involves forcing prey down the esopha- tohyals and epibranchials may move laterally during gus by contraction of the pharyngeal musculature, re- buccal expansion, broadening the pharynx. Both the 3. Aquatic Feeding in Salamanders 85 dorsoventral shifting of the hyobranchial apparatus can depress the mandibles asymmetrically, opening and the lateral expansion of the pharynx contribute only one-half of the mouth at a time, a behavior ob- only slightly to buccal expansion, and will not be dis- served most often during prey manipulation. This be- cussed further; ventrocaudal rotation of the hyobran- havior may serve the same function as labial lobes in chial apparatus is considered the primary movement other taxa, restricting the gape and accelerating water producing buccal expansion. As the hyobranchial ap- flow. Cryptobranchids can also depress the hyobran- paratus rotates and drops, it applies a downward force chial apparatus asymmetrically during prey capture to the buccal lining and the skin of the throat, which and manipulation (Cundall et al., 1987). The ability of unfold and expand ventrally to produce the volume cryptobranchids to move the jaws and hyobranchial change that draws water, and usually prey, into the apparatus unilaterally indicates that muscles may not mouth. When the buccal cavity has expanded fully, it be functioning symmetrically during feeding, as many begins to compress by elevation of the hyobranchial functional studies tend to assume. apparatus, which is accomplished like hyobranchial The gill slits of many aquatic salamanders have also depression, only in reverse and much more slowly. been proposed to contribute to suction-feeding perfor- Water is expelled through the gill slits or mouth and mance (Lauder and Shaffer, 1986; Reilly and Lauder, prey is retained by the gill rakers or teeth. 1988a).Gill slits have been shown to open during suc- Mouth opening and closing must be coordinated tion feeding before maximum buccal expansion. This with hyobranchial depression and elevation to ensure timing of gill slit opening would allow the momentum capture and prevent subsequent escape of the prey. of the primary flow to carry water posteriorly out the The mouth is opened and closed simply by rotation of gill slits, preventing turbulence that could disrupt flow the mandible about its articulation with the skull. The into the mouth (Muller and Osse, 1984). Alternatively, mouth is opened and begins to close during buccal ex- the momentum of the primary water flow can be ab- pansion and is kept closed or ajar during buccal com- sorbed by a relatively enormous buccal expansion, in pression. If a prey item is not brought entirely into the which water is stored for later expulsion during buccal mouth during the initial strike, it is gripped by the op- compression. This latter mechanism likely operates in posing teeth of the dentary on the lower jaw and the Cryptobranchids, which have no gill slits or only a tiny premaxilla and maxilla (when present) on the upper spiracle, and in metamorphosed newts, which lack gill jaw. Some large salamanders, such as amphiumids and slits. The exact biomechanical role of gill slits in suction cryptobranchids, have robust jaws and teeth that can feeding remains to be determined and likely differs in be used for crushing or tearing prey. taxa with different morphologies. Gill slits are clearly Labial lobes are critical for effective suction feeding not always necessary for successful suction feeding (Matthes, 1934; Miller and Larsen, 1989). They effec- in salamanders, given the suction-feeding prowess of tively prevent water from entering the sides of the some postmetamorphic salamandrids that lack gill mouth and restrict water flow to the front. By reducing slits, many of which suction feed as effectively as lar- the area of the aperture through which a given volume vae (Miller and Larsen, 1989). of water must flow in a certain period of time, labial lobes increase the velocity of the flow and thus increase D. Biomechanics the probability that elusive prey will be entrained. La- bial lobes are so frequently present in suction feeders Analyses of feeding kinematics and anatomy of the that the presence of these structures in the absence of feeding system can be combined to produce a model behavioral data is evidence that the salamander suc- of the biomechanical events of suction feeding. This tion feeds. Salamanders that lack labial lobes may, section presents such a model for salamanders, which however, use suction when feeding in water, for exis intended to be used as a heuristic device to identify ample, breeding Ambystoma (Miller and Larsen, 1986). developmental and evolutionary transitions in hyo- The importance of labial lobes in suction feeding is re- branchial function. It is to be used as a foundation on flected in the poor prey-capture success of these sala- which to build hypotheses of functional transforma- manders that lack them (Reilly and Lauder, 1988a). tion, rather than as a precise representation of all of the Other morphological and functional features may events occurring during suction feeding. also enhance suction-feeding ability. In amphiumids, The skeletal elements of the skull and hyobranchial the maxillae are attached loosely to the rest of the skull apparatus of larval salamanders form a system of rigid and undergo medial displacement during suction feed- elements on which the muscles act to produce moving, consequently reducing frontal gape and poten- ments. Suction feeding involves primarily rotational tially improving capture success (Erdmann and Cun- movements of the jaws and hyobranchial apparatus dall, 1984). Cryptobranchids are unique in that they (Fig. 3.9A) and can be modeled as a system of levers. 86 Stephen M. Deban and David B. Wake

FIGURE 3.9. Mechanics of hyobranchial depression during suction feeding, showing hyobranchial apparatus and jaws in the elevated position on the left and the depressed position on the right. Larval skull, jaws, and hyobranchial elements, shown in lateral view (A), are modeled as systems of levers (B). Muscles (black lines) contract to produce movements of the levers. Muscles shown on figures on the left produce movements that place the elements in the positions shown on the right, and vice versa. Oblique views (C) show displacements of the hyobranchial apparatus in three dimensions, including twisting of vertical elements about their long axes.

The skull and jaws form a single lever system. The and caudal elements, anchored by the dorsal element hyobranchial apparatus, together with the skull and and linked by the ventral element, which undergoes neck, can be represented in simplified form as a four- ventrocaudal translation without rotation. The rostral bar mechanism (Fig. 3.9B) in which rotation of any one and caudal elements are bilaterally paired, but articu- element causes equal rotation of the parallel element. late with the single, medial ventral and dorsal ele- The skull and neck, taken together, can be considered ments. The entire system thus resembles two four-bar a single component, which forms the dorsal element of linkages functioning in parallel, sharing some compo- the mechanism. The basibranchial forms the ventral nents (Fig. 3.9C). The jaw and hyobranchial lever sys- element. These two horizontal elements are linked by tems act in concert to produce the movements of suc- the paired ceratohyals and a pair of epibranchials (ei- tion feeding. ther the first or the second pair), which form the rostral Movement of the skeletal levers is accomplished by and caudal elements, respectively. Each of the four ele- contraction of the associated musculature. In the case ments of the mechanism articulates with neighboring of the jaws, the DM and LM act as antagonists to open elements and rotates with respect to them. The buccal and close the mouth, respectively. The GH is in a posi- cavity is expanded by parallel rotation of the rostral tion to open the mouth as well, via its attachment to 3. Aquatic Feeding in Salamanders 87 the mandible (Fig. 3.98). The mechanical advantage of the ventral element, as in the branchial plate of pletho- the GH in mouth opening is increased when the hyo- dontids, or to the caudal element as in amphiumids, in branchial apparatus is depressed. The muscles of the which they are fused with the epibranchials. Some lar- neck direct the gape dorsally, ventrally, or laterally, val salamanders possess additional skeletal elements, and some (the DT and ITCS) are in a position to pro- which lie between components of the linkage, but these vide resistance to skull depression when the GH is act as part of one of the elements of the system and used in mouth opening. The hyobranchial apparatus is do not alter its mechanical function as proposed here. swung ventrocaudally by the RCP, RCS, and BH and Adult salamanders may lack one or more connections is swung dorsorostrally by the GH, IMP, IH, and IHP. in the linkage, making the system a series of levers. The RCP is attached to the basibranchial and pulls that Some aquatic salamandrids, for example, lack a tight ventral element caudally, forcing it to pivot about its connection between the ceratohyals (rostral element) attachments to the rostral and caudal elements, which, and the basibranchial (ventral element). Adults also in turn, pivot about their attachments to the skull and lack the BH, which pulls diagonal corners toward one neck. The BH is attached to the tip of the first epibran- another; however, the SAR enlarges at metamorphosis chial and to the rostral tip of the ceratohyal and con- to replace the BH in both position and function. All tracts to pull the diagonal corners of the mechanism adults retain the primary muscle of the system, the toward one another, forcing the basibranchial ventro- RCP, which alone can swing the entire linkage ven- caudally. The BH and RCP both contribute to the same trocaudally. resultant force vector and produce the same ventrocau- In many larvae both the first epibranchial and the dal movement of the basibranchial. These two muscles ceratohyal are equally robust and probably bear com- are likely to be coactive during feeding, together pro- parable loads during buccal expansion. However, the ducing a powerful expansion of the buccal cavity. In relative robustness of these elements is variable among addition to forcing the hyobranchial apparatus ventro- taxa and across developmental stages, reflected in the caudally, the BH has two further roles in buccal expan- extent of ossification of the elements or the cross- sion. It is in a position to pull the tips of the epibran- sectional shape and area. In some groups, the cerato- chials ventrally and to rotate the flat ceratohyals about hyals are more robust than the epibranchials, whereas their long axes so that their medial edges are directed in others the reverse is true. During development and ventrally when the hyobranchial apparatus is fully de- evolution, the primary axis of the linkage system may pressed. This latter action brings the broad surfaces shift from one set of skeletal elements to another or of the ceratohyals into contact with the buccal walls, from the rostral to the caudal components. Crypto- supporting the buccal lining and aiding in expansion. branchoids, for example, are unusual in having the During the first part of buccal expansion the gill slits caudal component of the linkage be the second cerato- are held closed by the SAR muscles, which adduct the branchial and epibranchial, rather than the first as epibranchials. in other taxa. This caudal component is ossified and Acting in direct opposition to the RCP is the GH, forms the main load-bearing component; the rostral which draws the basibranchial rostrally via its attach- component, the ceratohyal, is flattened and cartilagi- ment to the urohyal. In adults in which the urohyal nous. In larval salamandrids, the ceratohyal is more ro- loses its attachment to the basibranchial, the GH re- bust than the epibranchials and is thus likely to bear tains its larval role but functions by cradling the hyo- more load, whereas in adults that feed aquatically, the branchial apparatus rather than pulling directly on it. epibranchials form the primary load-bearing axis of The IMP, IH, and IHP also do not attach directly to the system and are more fully ossified than the cerato- the linkage, but all cradle the ventral and caudal ele- hyal. In taxa that also feed on land using tongue pro- ments and exert dorsal components of force, moving traction, the rostral portions of the hyobranchial ap- the basibranchial rostrodorsally and reducing buccal paratus are generally more flexible and less capable of volume. The LAB muscles are in a position to pull the bearing compressive loads, whereas the caudal com- epibranchial tips dorsally, further compressing the buc- ponents are more robust, bearing loads during both cal cavity. suction feeding and tongue protraction. The lever system of the jaws is common to all salamanders, whereas the four-bar linkage system of the E. Metamorphosis hyobranchial apparatus is present in its purest form in larval salamanders. The first epibranchial is usually the Following metamorphosis, many salamanders leave most robust element of the larval hyobranchial appa- the water to forage on land. Suction feeding, the pri- ratus and forms the caudal component of the linkage mary mode of aquatic salamanders, relies on the in- system. The ceratobranchials may contribute either to compressibility of water to move prey into the mouth 88 Stephen M. Deban and David B. Wake and therefore must be abandoned and replaced by a of attempts, respectively. The absence of gill slits in the mode that can operate in air. Terrestrial salamanders adult newts does not affect their suction-feeding per- must capture prey by either tongue or jaw prehension, formance (Miller and Larsen, 1988; Reilly and Lauder, behaviors that make use of many of the same morpho- 1988a). logical components as suction feeding. The jaws are strengthened at metamorphosis and assume more im- G. Variation portance in prey capture. The hyobranchial apparatus is remodeled extensively for propelling the tongue Larger suction-feeding salamanders show consider- from the mouth, but in many cases can continue to able variation in the relative timing of events dur- function in buccal expansion. In general, the skull and ing prey capture. This variation across prey type and jaws begin a gradual metamorphosis before the hyo- among individuals can be due to the salamander ac- branchial apparatus, which undergoes a more abrupt tively modulating its behavior or selecting from a rep- transformation (Rose, 1996). Suction-feeding perfor- ertoire of stereotyped behaviors based on an assess- mance can thus be maintained at a high level late into ment of conditions before initiating a predatory strike. larval life in those taxa that make a developmental The high speed of suction-feeding movements is likely transition to tongue or jaw prehension. In some taxa, to preclude any adjustments via sensory feedback dur- such as plethodontids, suction-feeding function is lost ing the strike. Cryptobranchus and Amphiuma show completely as the hyobranchial apparatus transforms variation in the timing of movements of the hyo- and tongue function is emphasized. Even completely branchial apparatus, jaws, and body. When capturing aquatic adult plethodontids lack the ability to suction slowly moving or stationary prey, they show little for- feed and use tongue or jaw prehension to capture prey ward movement and mouth opening occurs before buc- in water (Deban and Marks, 1992). cal expansion begins. When feeding on elusive prey, these salamanders exhibit forward lunging and syn- chronous mouth opening and buccal expansion. Mouth F. Performance opening and buccal expansion are greater when feed- Many of the changes that occur during metamor- ing on elusive prey compared to sluggish prey (Erd- phosis can potentially affect suction-feeding perfor- man and Cundall, 1984; Elwood and Cundall, 1994). mance, including the loss of labial lobes, transforma- Slight individual variation in muscle activity patterns tion of the hyobranchial apparatus, development of has been recorded in larval Ambystoma feeding on the the tongue, reduction in buccal volume, and closure of substrate, but variation due to prey type was not de- the gill slits. Larvae and perennibranchiate salaman- tected (Reilly and Lauder, 1989). Ambystoma larvae ders, which undergo few of these changes, are the most have been observed to forage in the water column and adept at suction feeding. Larval Notophtkalmus virides- strike at prey from a distance (Hoff et al., 1985), sug- cens capture worms in up to 99% of their attempts gesting that additional variation in prey-capture be- (Reilly and Lauder, 1988a), larval Salamandra salarnan- havior remains to be investigated in some taxa. Explicit dra up to 91% of attempts (Reilly, 1995), and larval studies of variation are few (Erdmann and Cundall, Amybstoma tigrinum capture worms in 93% of attempts 1984; Shaffer and Lauder, 1985a,b; Elwood and Cun- and can catch even highly elusive prey such as fish 33% dall, 1994), however, leading to the impression that of the time (Lauder and Shaffer, 1986). Partially meta- salamander prey-capture is an invariant, stereotyped morphosing taxa such as amphiumids and cryptobran- behavior. This notion is gradually being dispelled as chids perform as well as larvae, even though they may more incidental kinematic evidence of variation is lack some larval features. The suction-feeding perfor- gathered. Nonetheless, studies directly examining the mance of aquatic adult salamandrids is variable but taxonomic and developmental diversity of both prey- comparable to that of larvae and is correlated with capture performance and variation are needed. the degree of head tapering and hyobranchial ossification, and the size of the labial lobes (Miller and Larsen, 1989). Adult semiaquatic newts with rounded heads IV. DIVERSITY AND EVOLUTION and modest labial lobes (Taricha, Cynops, Notophthal- mus, Paramesotriton, and Pleurodeles) capture earth- The preceding sections have presented the general worm pieces 90-97% of attempts, fairy shrimp 38- pattern of morphology, function, and behavior of the 58% of attempts, and fish 13-23% of attempts, whereas feeding systems of aquatic salamanders. Characters the fully aquatic Pachytriton, with a strongly tapered have been emphasized over taxa. The following sec- snout, fully ossified hyobranchial apparatus, and large tions are designed to place these characters in the con- labial lobes, captures these same prey 100,90, and 65% text of taxa that possess them. Unique features of each 3. Aquatic Feeding in Salamanders 89

family, common patterns of evolution (convergence ever, and many are aquatic or semiaquatic. Little is and homoplasy) within the Caudata, as well as syn- known of their feeding behavior. The semiaquatic Sala- apomorphies of larger clades (above the family level) mandrella keyserlingii and Batrachuperus persicus use jaw are discussed. Features common to most families have prehension in water (Deban, personal observation), already been covered. whereas the fully aquatic Batrachuperus and Packyhy- nobius possess pronounced labial lobes and a pleated buccal lining, morphology that is consistent with suc- A. Features of Salamander Families tion feeding. Hynobiids possess complex skulls and Each of the 10 families of salamanders possesses un- hyobranchia, with more elements than the other sala- usual or unique features of feeding biology. In the fol- manders (Fig. 3.3), a condition that has led, in part, to lowing accounts the developmental patterns (i.e., pe- the conclusion that they are basal within the Caudata rennibranchiate, paedomorphic, metamorphic) of each (with the cryptobranchids) after the Sirenidae (Fig. family is discussed as well as its bearing on feeding 3.1). Two epibranchials are present in adults, com- form and function. pared to one in all other metamorphosing taxa. The second ceratobranchials and epibranchials are ossified whereas the first are cartilaginous, a feature shared 1. Sirenidae with the Cryptobranchidae. Free radii are completely Sirenids are dwarf (Pseudobranchus, two species) or lacking, but unusual, elongate, radial cartilages con- giant (Siren, two species) paedomorphic, perennibran- nect the ceratohyals to one another or to the basi- chiate, fully aquatic salamanders that are elongate and branchial. lack hindlimbs entirely. They possess a fundamentally larval skull and hyobranchial configuration, which are 3. Cryptobranchidae unusual in many respects (Reilly and Altig, 1996). They possess premaxillae and robust tooth-bearing The Cryptobranchidae is a small family with two palatines in the upper jaw. The frontal processes of genera and three species, all aquatic. Cryptobranchids the premaxillae border the nasals laterally rather than possess unusual behavioral and morphological fea- medially as in most other salamanders. The skull is tures related to aquatic feeding. Not only do they reach strongly tapered rostrally, and the lower jaw is nearly enormous size as adults (up to 75 cm in Cryptobranchus triangular and rather small, bearing teeth only on the and 150 cm in Andrias), but they also have the largest coronoid (in Siren) and with the unusual ball-and- buccal expansion relative to body size of any salaman- socket jaw joint far anterior. Maxillae are lacking in der, due in part to the broad, flat head and pleated buc- Pseudobranchus but are present in Siren as tiny, free- cal lining. As a consequence they are supreme suction- floating elements (Parker, 1882; Larsen, 1963; Duell- feeders and are unique in that they can direct their man and Trueb, 1986). The hyobranchial apparatus is strike to the side using unilateral jaw and hyobran- extensively ossified and the anterior tip of the basi- chial depression (Elwood and Cundall, 1994). This branchial is bulbous where it articulates with the cera- behavior is facilitated by the loose mandibular sym- tohyals. Three epibranchials are present in Pseudobran- physis, strongly curved mandibles, and broad hyo- ckus and four in Siren. The labial lobes are the largest branchial elements. The pattern of hyobranchial ossifi- of any salamander, larval or adult, with upper lobes cation is unusual and shared with the Hynobiidae: the overlapping the lower jaw to such a degree that they first ceratobranchial and epibranchial (which are fused almost meet ventrally. Sirenids are powerful suction to one another) are cartilaginous and the second are feeders, due to the combination of the robust hyobran- bony. This second set acts as the primary lever in hyo- chial apparatus and the entirely frontal gape afforded branchial depression, as compared to the first set in by the immense labial lobes. The Sirenidae is the sister most other salamanders. Cryptobranchids are essen- taxon to all other salamanders (Fig. 3.1), but its mor- tially metamorphic in their skull morphology, but re- phology is unsual and not representative of the ances- tain other larval features, such as lidless eyes, a poorly tral condition. developed tongue pad, lower labial lobes, posterior branchial elements, and spiracles; the last two features 2. Hynobiidae are present in Cryptobranchus and absent in Andrius. Cryptobranchids will scavenge, but can also capture The sister group of the Cryptobranchidae, the Hy- elusive prey such as fish and can handle aggressive nobiidae, is a large family with about 39 species in prey such as crayfish. They are unusual among suc- seven genera. Some perennibranchiate populations of tion-feeding salamanders in that they can modulate Hynobius exist. Most species are metamorphic, how- their feeding behavior (the timing and extent of jaw 90 Stephen M. Deban and David B. Wake and hyobranchial movements), depending on the elu- are perhaps the most proficient suction feeders of all siveness of the prey. metamorphic salamanders. Taxa that use both suction feeding and tongue protraction (e.g., Taricha and Noto- 4. Proteidae phthalmus) possess an intermediate hyobranchial mor- The Proteidae includes the genera Necturus (five spe- phology. This morphology must play two disparate cies) and Proteus (one species), completely aquatic pae- feeding roles and represents a functional compromise domorphic perennibranchiates with an essentially lar- (Findeis and Bemis, 1990). Salamandrids that feed val morphology including labial lobes and two gill slits. aquatically after metamorphosis develop labial lobes The hyobranchial apparatus is heavily ossified and re- on the upper jaws that are functionally similar to larval tains the larval configuration throughout life. Proteids lobes (Ozeti and Wake, 1969) and increase suction- have only three epibranchials, a feature shared only feeding performance. Those that return to the water to with some plethodontid larvae and Pseudobranchus breed develop these lobes temporarily but resorb them (Fig. 3.4). The upper jaw lacks maxillae but contains rapidly (within 48 hr) on resuming a terrestrial exis- massive, dentate palatopterygoids that replace them in tence (Matthes, 1934). A terrestrial eft stage is present function. Proteids are strong suction feeders. Proteus is after metamorphosis in many taxa that are aquatic as elongate, blind, and cavernicolous and is adept at lo- adults (e.g., Notophthalmus), during which time prey is cating prey in complete darkness by olfactory and lat- captured with the tongue. A particularly unsual situ- eral line senses (Durand et al., 1982; Uiblein and Par- ation occurs in Pachytriton, in which adults have a tiny zefall, 1993). tongue pad and completely lack tongue protraction ability as do their larvae. However, a terrestrial eft 5. Amphiumidae stage occurs after metamorphosis in which tongue prehension presumably is used (Thiesmeier and Hornberg The Amphiumidae is a small family with three spe- 1997),suggesting that a secondary loss of tongue struc- cies, all aquatic, elongate, and with four tiny limbs and tures accompanies the return to a permanently aquatic a reduced number of toes. Amphiumids resemble lifestyle. The only viviparous salamanders are in this cryptobranchids in behavior and in their degree and family. The fetuses of these species feed on unfertilized pattern of paedmorphosis, despite marked differences ova or smaller embryos in utero and are born as larvae in morphology and ecology. They retain some larval or metamorphs; the terrestrial juveniles and adults do features (lidless eyes, small tongue pad, interlocking la- not feed in water. Chioglossa is unusual in that it pos- bial lobes, spiracles, and posterior branchial elements) sesses a slender hyobranchial apparatus specialized for but have solid and robust skulls with some metamor- tongue protraction, suggesting that it does not suction phic features. Amphiumids are strong suction feeders feed. It is known, however, to spend time in water and, like cryptobranchids, can modulate their behavior (Arntzen, 1981) and may capture aquatic prey using depending on prey type (Erdmann and Cundall, 1984). tongue or jaw prehension. They have powerful jaws and teeth and can capture and crush formidable prey, and can bite viciously (Co- 7. Rhyacotritonidae nant and Collins, 1991). The skull is elongate and tapered anteriorly, quite unlike the rounded, flattened The Rhyacotritonidae contains four species of one skull of cryptobranchids. genus, Rhyacotriton, all semiaquatic and metamorphic with reduced lungs. Adults possess a generalized hy- 6. Salamandridae obranchial morphology similar to the Ambystomati- dae and modest tongue protraction, which they use on The Salamandridae is a large and diverse family land and in water (Larsen, personal communication). with 14 genera and about 45 species, most of which They suction feed only as larvae. are aquatic or semiaquatic. The majority of species are fully metamorphic and possess the adult configura- 8. Dicamptodontidae tion of hyobranchial elements, although some populations are perennibranchiate. Salamandrids possess the The Dicamptodontidae contains four species of one full range of hyobranchial morphologies, from almost genus, Dicamptodon, three metamorphic and one pe- entirely cartilaginous, slender apparati that are used rennibranchiate (D.copei). The larvae and perennibran- in long-distance tongue protraction (e.g., Salamandrina chiate adults suction feed in a typical manner. No in- and Chioglossa) to the almost fully ossified, robust ap- formation is available on aquatic feeding in adults, parati used for powerful suction feeding (e.g., Pachy- which are essentially terrestrial but which return to the triton and Cynops). Salamandrids of the latter type water to breed and guard their eggs (Nussbaum, 1969). 3. Aquatic Feeding in Salamanders 91

9. Ambystomatidae of the tongue protraction system that followed on the loss of robust hyobranchial elements that can function The Ambystomatidae, the sister taxon of the Di- as a mechanism for expanding the buccal cavity. Instead camptodontidae, is a large family with one genus, they use terrestrial feeding behaviors in water. The Ambystoma, and 31 species. Most are metamorphic and completely terrestrial bolitoglossines have a unique terrestrial, but some species (e.g., the axolotl A. mexi- pattern of one embryonic epibranchial. All plethodon- canum) and populations of other species (e.g., A. ti- tids are lungless and possess nasolabial grooves, a fea- grinum) are perennibranchiate. Larvae and perenni- ture unique to the family. branchiate adults suction feed. Adults may use suction (although poorly) to capture prey when returning to the water to breed. Species formerly placed in the B. Phylogenetic Patterns of Feeding genus Rhyacosiredon are partially metamorphic; the Form and Function adults inhabit mountain streams and retain larval fea- Many features of the feeding morphology and be- tures such as labial lobes, lidless eyes, and a small havior of salamanders have evolved convergently. Pae- tongue pad. They possess a midmetamorphic hyobran- domorphosis, or the retardation of development rela- chial configuration, with broader, more heavily ossi- tive to the ancestral condition, is a common pattern fied elements than other adult ambystomatids and among sah-hen taken to the extreme, re- less elaboration of anterior lingual elements (Fig. 3.6) sults in perennibranchiation. Perennibranchiation ap- (Reilly and Brandon, 1994). These features strongly pears in 7 of the 10 salamander families and has evolved suggest they are suction feeders, although behavioral more than once in some of these (notably the Ambysto- information is lacking. matidae and Plethodontidae). Extensive ossification of the hyobranchial apparatus has evolved independently 10. Plethodontidae in the Sirenidae, Proteidae, Salamandridae, Amphi- The Plethodontidae is the largest family of sala- umidae, and Cryptobranchidae and contributes to the manders, with over 275 species in 28 genera. Most of strong suction-feeding abilities of these taxa. Free hy- these species are members of the tribes Plethodontini pohyals in larvae and first radii of adults (which we and Bolitoglossini of the subfamily Plethodontinae consider homologues) have been lost independently and are completely terrestrial and direct developing. in the Sirenidae, Proteidae, and Plethodontidae, but Two basal clades within the family, the subfamily Des- are present at some stage of development in the other mognathinae and the tribe Hemidactyliini (within the families. Four larval epibranchials appear to be the an- subfamily Plethodontinae), have members that retain cestral condition for salamanders, and the presence of the ancestral life history of metamorphosis from an only three has evolved at least three times: in Pseudo- aquatic suction-feeding larva. Direct development has branchus, the Proteidae, and in the Hemidactyliini (and also evolved two to three times within the Desmogna- in the embryos of the Plethodontini). A composite first thinae. Morphologically, plethodontid larvae are typi- epibranchial representing the fusion of the first cerato- cal in most respects, but possess dentate palatoptery- branchial to the first epibranchial has evolved conver- goids and lack maxillae and ossified pterygoids. Most gently in the Amphiumidae and some members of the hemidactylines possess only three epibranchials as Cryptobranchoidea and Salamandridae. The presence larvae and many are perennibranchiate and suction of a third larval ceratobranchial is unique to the Cryp- feed as adults with their larval morphology. Two of tobranchoidea, as is the functioning of the second set these taxa, Haideotriton and Typhlomolge, are blind cave of branchial elements as the primary lever in hyobran- salamanders with one and two species, respectively. chial depression. Metamorphic plethodontids that feed in the water use Free-living larvae, and thus suction feeding, have tongue or jaw prehension, even the fully aquatic des- been lost numerous times, at least twice with the evo- mognathine Desmognafhus mavmorafus (Schwenk and lution of viviparity among salamandrids that give Wake, 1988; Deban and Marks, 1992; note that pre- birth to metamorphosed young and at least three times vious studies refer to D. marmoratus as Leurognathus with the evolution of direct development in pletho- marmoratus; however, we follow the recommendation dontids. Suction feeding has been lost at least three of Titus and Larson, 1996, based on their recent mo- times in adult salamanders that feed in water: among lecular study of desmognathine relationships). Suc- semiaquatic and aquatic rhyacotritonids, plethodon- tion feeding has not been documented in metamor- tids, and hynobiids, which have exapted the terrestrial phosing adult plethodontids. They have probably lost ingestion behaviors of tongue or jaw prehension to the ability to suction feed as a result of the elaboration capture aquatic prey. 92 Stephen M. Deban and David B. Wake

V. OPPORTUNITIES FOR areas. Taxonomic and developmental diversity among FUTURE RESEARCH salamanders remain to be exploited by researchers of biomechanics, physiology, development, and neu- The fundamental structure, function, and natural roethology. As long as representatives of most of the history of feeding in salamanders are well known. major groups of salamanders can be obtained, techno- Studies of foraging behavior have been conducted on a logical advances in high-speed imaging, electromyog- number of species, and diet is known for many more raphy, muscle physiology, and neurophysiology will taxa. Cranial anatomy has been described for many continue to provide opportunities to explore the form species from most of the major groups, although more and function of the feeding systems of salamanders at detailed morphological studies are needed for a num- multiple levels. ber of taxa, including the Sirenidae (especially Pseudob- ranchus), Dicamptodontidae, and Rhyacotritonidae. Acknowledgments The Rhyacotritonidae, which possesses a generalized and perhaps ancestral morphology, is particularly in- We thank members of the Wakelunch group and Marvalee Wake teresting because of its phylogenetic position. There for providing constructive comments on the manuscript. Karen Klitz rendered Figs. 3.4 and 3.6. are some groups for which scant morphological information is available, such as the Hynobiidae. The basic function of the suction-feeding system References common to most aquatic salamanders is fairly well understood, but the functional significance, if any, of Alberch, P., and E. A. Gale (1986) Pathways of cytodifferentiation the great morphological diversity of salamanders re- during the metamorphosis of the epibranchial cartilage in the salamander Eurycea bislineata. Dev. Biol. 117:233-244. mains largely uninvestigated. Feeding function of only Alcobendas, M., H. Dopazo, and P. Alberch (1996) Geographic varia- a handful of the approximately 400 species of salaman- tion in allozymes of populations of Salamandra salamandra (Am- ders has been studied in any detail, and even fewer phibia: Urodela) exhibiting distinct reproductive modes. J. Evol. species have been examined at more than one level of Biol. 9:83-102. biological organization. Studies of prey-capture behav- Anthony, C. D., D. R. Formanowicz, Jr., and E. D. Brodie, Jr. (1992) The effect of prey availability on the search behavior of two spe- ior and kinematics among the aquatic taxa have fo- cies of Chinese Salamanders. Herpetologica 48 :287-292. cused on the families Ambystomatidae and Salaman- Arntzen, J. W. (1981) Ecological observations on Chioglossa lusitanica dridae, and little information is available for the other (Caudata, Salamandridae). Amph.-Rept. 1: 187-203. families (Terrestrial taxa are more fully studied; see Avery, R. A. (1968) Food and feeding relation of three species of Tri- Chapter 4). Physiological studies of in vivo muscle turus (Amphibia: Urodela) during the aquatic phases. Oikos 19: 408-412. function (i.e., electromyography) have been under- Bartels, M., H. Miinz, and B. Claas (1990) Representation of lateral taken in only seven species of aquatic salamanders rep- line and electrosensory systems in the midbrain of the axolotl, resenting half of the families. Clearly more diversity Ambystoma mexicanum. J. Comp. Physiol. A. 167:347-356. remains to be explored, including those taxa that show Bell, G. (1975) The diet and dentition of smooth newt larvae (Triturus pronounced modulation or asymmetry of movement, vulgaris). J. Zool. Lond. 176:411-424. Beneski, J. T., Jr., and J. H. Larsen, Jr. (1989a) Interspecific,ontogenetic, such as Cyptobranchus and Amphiuma. and life history variation in the tooth morphology of mole sala- The development of feeding behavior and function manders (Amphibia, Urodela, and Ambystomatidae). J. Morph. has been studied in only two species of salamanders, 199:53-70. and early development of larval feeding remains com- Beneski, J. T., Jr., and J. H. Larsen, Jr. (198913) Ontogenetic altera- pletely unstudied. Little information is available on the tions in the gross tooth morphology of Dicamptodon and Rhyaco- triton (Amphibia, Urodela, and Dicamptodontidae). J. Morph. feeding behavior and function in larvae of the unusual 199~165-174. Cryptobranchoidea, particularly the Hynobiidae. The Besharse, J. C., and R. A. Brandon (1974) Postembryonic eye de- diversity of life histories among aquatically feeding generation in the troglobitic salamander Typhlotriton spelaeus. J. salamanders has not yet been exploited. 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