Copeia, 2004(4), pp. 903–907

Ontogeny of Feeding in the Asian Glassfish, Chanda nama (Ambassidae)

ARCHIS R. GRUBH AND KIRK O. WINEMILLER

Dietary analysis of a population of the glassfish Chanda nama from a wetland in southwestern India revealed facultative scale feeding (lepidophagy). In addition to fish scales, microcrustacea and aquatic insects were consumed by all size classes, with juvenile diets containing larger fractions of invertebrates. More scales were consumed during the wet season, the period when abundance of juvenile fishes was greatest. Aquarium observations revealed how the glassfish uses stealth and ambush tactics. Scales are dislodged by raking the extended lower jaw, distally armed with four curved conical teeth, across the flanks of prey.

PECIALIZED scale feeding, or lepidophagy, (Major, 1973; Sazima and Uieda, 1980; Sazima, S is defined as the ingestion of scales without 1983). bones or flesh (Sazima, 1983). Lepidophagy has Roberts (1989) briefly described the denti- been described for seven Neotropical characid tion of two Asian glassfishes (Ambassidae, Per- genera (Roberts, 1970; Sazima, 1983; Vari, ciformes), Chanda nama from India and Para- 1986), three Neotropical trichomycterid genera doxodacna piratica from the Malay Peninsula and (Baskin et al., 1980), at least six African Western Borneo, presumed to feed on scales. genera (Fryer et al., 1955; Eccles and Lewis, Although the were described as scale 1976; Liem and Stewart, 1976), an Australian feeders, no assessment of the degree of lepido- ariid catfish (Roberts, 1978), an Australian ter- phagy was provided for either species. Here we aponid (Whitfield and Blaber, 1978), two caran- report for the first time ontogenetic diet shifts gid genera (Major, 1973; Sazima and Uieda, involving scale feeding in C. nama from a fresh- 1980), and two ambassid genera (Roberts, water wetland in the western Ghats region of 1989). Lepidophagous Neotropical characids India. have morphological and behavioral specializa- tions for removing scales (Sazima, 1977, 1983; MATERIALS AND METHODS Sazima and Machado, 1990). Catoprion mento has everted teeth and a long lower jaw that opens From August 2000 to July 2001, fishes were to a Ͼ 90Њ angle to rake scales from the flanks collected from a natural wetland (approximate- of fishes (Sazima, 1983; Nico and Taphorn, ly 40 ha) at Manavalakurichy (8Њ10Ј12ЉN, 1988). Exodon paradoxus, Roeboexodon guyanensis, 77Њ18Ј24ЉE) in southern region of the western Serrabrycon magoi, and Roeboides species possess Ghats, Tamil Nadu, India. Annual rainfall in the external teeth on the snout that are used to dis- region is 1.2–1.5 m, with a period of relatively lodge scales (Roberts, 1970; Sazima, 1983; Vari, low rainfall from December through March 1986). Morphological and behavioral mecha- (mean monthly rainfall 35 mm) and high rain- nisms for scale feeding are less apparent in most fall from April through November (mean rain- noncharacid fishes (but see Hori, 1993). fall 134 mm). During most years, low rainfall in In lepidophagous characids (Catoprion mento September (53 mm rainfall during 2000) briefly and Roeboides spp.), the juvenile diet shifts from interrupts the long rainy season. Manipulation microcrustacea to aquatic insects before switch- of inlet and outlet sluice gates maintains rela- ing to scales in the adult diet (Sazima and Ma- tively constant water level. Water level increases chado, 1982; Nico and Taphorn, 1988; Peterson during unusually wet periods. The wetland con- and Winemiller, 1997). Frequency of scales in tains 28 fish species (ARG, unpubl. data) and stomachs of Reoboides dayi and Reoboides affinis in lacks exotic (e.g., Catla catla, Labeo rohita, the Venezuelan llanos was greater during the Chirrhina mrigala) commonly introduced into dry season when aquatic insect abundance is surface waters of the country. were cap- lower and fish densities are higher (Peterson tured with seines (6 ϫ 2 m, 3 mm mesh), cast and Winemiller, 1997; Peterson and MacIntyre, nets (3 m radius, 10 mm mesh) and experimen- 1998). Among most marine lepidophagous fish- tal gill nets (150 ϫ 3 m, with 2, 3.5, 5, 8, and es, scale is performed by juveniles and 15 cm mesh). Sampling was conducted from ceases during later ontogeny in association with 0600–1400 h. All aquatic habitats were surveyed modification of jaw structure and dentition (i.e., vegetation, open water, edge, and mid-

᭧ 2004 by the American Society of Ichthyologists and Herpetologists 904 COPEIA, 2004, NO. 4 pool). Specimens were preserved in 15% for- malin, then rinsed in freshwater prior to ex- amination in the lab. Of 3361 C. nama captured, 3034 were mea- sured for standard length (SL) to the nearest 0.1 mm, and 382 individuals representing all size classes (grouped by 5 mm intervals), months, and habitats were dissected for stom- ach contents. Food items in the anterior half of gut were examined under a dissecting micro- scope and identified to (invertebrates), species (fishes), or general category (e.g., algae, , scales) yielding a total of 22 prey cat- egories. Food items were blotted dry on paper Fig. 1. Volumetric percentages of three major re- source categories in diets of size classes of Chanda towel, and their volumes measured by water dis- nama (values in parentheses are sample sizes). placement in graduated cylinders. Resolution for the smallest food items was approximately 1 ␮l. To estimate the approximate size of matu- ration, gonads of dissected specimens were ex- wasϪ0.30 (Spearman’s rho, df ϭ 355, P Ͻ amined under a dissecting microscope, and ova- 0.0001), between SL and the volume of aquatic ries were staged as immature (lacking visible oo- insects in the diet wasϪ0.26 (P Ͻ 0.0001), and cytes or oocytes within 0.10 mm of the maxi- the correlation between SL and the volume of mum diameter observed for the population) or scales in the diet was 0.86 (P Ͻ 0.0001). Con- mature (containing at least some oocytes of the sumption of scales was facultative, with no size maximum diameter). class averaging more than 50% scales in the diet by volume. Nonetheless, scales were the most RESULTS important diet category for adult size classes ϭ Chanda nama were captured during each (average volumetric percentage 38%, range ϭ monthly survey (average sample ϭ 110, range among size-class averages 35–50%). The ϭ 15–892). Approximately half of all males and mean number of scales in individual stomachs females had mature gonads by 25 mm SL; thus was 8.15 for juveniles (n ϭ 114) and 13.94 for we consider this the size at maturation. In every adults (n ϭ 242). The maximum number of monthly sample, females Ͼ 26.4 mm SL con- scales in individual stomachs was 32 for juve- tained ripe ovaries. Ripe ovaries contained mul- niles and 65 for adults. Only eight juveniles and tiple oocyte cohorts, and juveniles were present 17 adults in our sample had empty stomachs. in every sample, which suggests that some seg- Diets of both juveniles and adults varied sea- ment of the population probably spawns during sonally (Fig. 2). Juveniles (SL Ͻ 25 mm) fed any given month. March through July (early wet predominantly on aquatic insects from late wet season) samples were dominated by juveniles to early dry seasons (October to January). Mi- (10–25 mm SL) and probably reflect peak crocrustacea were the most important dietary spawning during this period. component for juveniles during other periods, Analysis of volumetric percentages of major the only exception being July (middle wet sea- diet categories for different size classes of C. son) when scales were the dominant item in ju- nama revealed a strong pattern of ontogenetic venile diets. Scales were significant dietary ele- diet shift (Fig. 1). Juveniles fed heavily on aquat- ments for adults throughout the year, compris- ic insects (mostly Ephemeroptera but including ing from 15–90% of the monthly mean volume Odonata and Coleoptera) and microcrustacea of adult stomach contents (Fig. 2). Greatest con- (calanoid copepods, Cladocera, Isopoda, and Amphipoda). Terrestrial insects appeared in the sumption of scales by adults was during the pe- diet at 25 mm SL and remained a minor dietary riod April to August (end of dry season–early component (5–17%) for all subsequent size wet season). Microcrustacea (zooplankton) classes. Scale feeding was observed among in- comprised the greatest percentage of the adult dividuals as small as 15 mm, and the volume of diet during the period November to February scales in stomachs increased gradually with size (end of wet season–early dry season). Aquatic until reaching an asymptote at approximately and terrestrial insects were important diet ele- 35 mm (Fig. 1). The correlation between SL ments for adults during the late dry season and the volume of microcrustacea in the diet (March to April). GRUBH AND WINEMILLER—SCALE FEEDING IN CHANDA 905

ultative, and adults also consume insects and microcrustacea. In a manner similar to Neo- tropical characids in the Roeboides, C. nama undergoes an ontogenetic diet shift from feeding primarily on invertebrates as juveniles to scale feeding as adults. Roeboides dayi in streams of the Venezuelan llanos fed extensively on seasonally abundant microcrustacea and aquatic insects during the wet season (Peterson and Winemiller, 1997). In contrast, Roeboides prognathus from the Cuiaba´ River in ap- pears to have a diet largely restricted to scales (Sazima, 1983). Seasonal resource fluctuations could have been associated with temporal vari- ation in the degree of lepidophagy observed in C. nama in the Manavalakurichy wetlands. Daily operation of sluice gates maintains a fairly con- stant water level in this ecosystem. Nonetheless, environmental parameters, such as tempera- ture, pH, DO, turbidity and conductivity, vary in response to seasonal rainfall. During the dry Fig. 2. Volumetric percentages of three major re- season, temperature, conductivity and turbidity source categories in diets of juvenile (top graph) and are higher, and DO is lower. Both adults and adult (bottom graph) Chanda nama at Manavalakuri- juveniles consumed relatively large fractions of chy wetland during different months (2000–2001). aquatic insects and microcrustacea during this period. Juveniles that consumed scales did so mostly during the early wet season. Scales were DISCUSSION major components of the adult diet throughout Chanda nama and P. piratica are the only the year, but scale consumption was relatively freshwater fishes in Asia reported to consume greater during the early wet season. During the scales (Roberts, 1989). Other freshwater and es- early wet season, fish recruitment is high, such tuarine ambassid species have been document- that large populations of young fishes yield high ed to feed on aquatic invertebrates and in a few availability of scales as a potential food resource. cases fishes (Nair and Nair, 1981, 1983; Merrick Chanda nama does not possess external snout and Schmida, 1984; Martin, 1989). Scales pro- teeth as observed in several genera of lepido- vide lepidophagous consumers an abundant phagous Neotropical characids. We examined and rapidly renewable resource (Nico and Ta- head morphology of three C. nama specimens phorn, 1988). scales have substantial en- measuring 33.6, 54.2, and 64.1 mm SL. In ad- ergy content (van Oosten, 1957; Whitfield and dition to having numerous rows of tiny conical Blaber, 1978; Nico and De Morales, 1994), but teeth embedded on both jaws, each specimen their nutritional value has not been investigated possessed two enlarged conical teeth in the an- extensively. Nico and De Morales (1994) found teriolateral region of both mandibular tooth little variation in energy and protein content of pads (Fig. 3). These teeth are curved anteriorly scales from several different Neotropical fish and presumably are used to dislodge scales. The species. The energy content per unit dry mass jaws open to create an approximate 90Њ angle of fish scales is about two-thirds that of whole with the long lower jaw protruding further than fish (Nico and De Morales, 1994). In his study the premaxillae. Presumably, C. nama, with jaws of the cleaner Labroides phthirophagus, fully extended, rakes its enlarged mandibular Gorlick (1980) suggested the mucus layer asso- teeth across the flanks of prey to dislodge scales ciated with ingested scales is an important en- in a manner similar to that used by Catoprion ergy source rich in proteins (Wessler and Wer- mento as described and illustrated by Sazima ner, 1957) and lipids (Lewis, 1970). Juveniles of (1983). Both upper and lower jaws have a de- several cichlid species (e.g., Symphysodon spp.) gree of bilateral asymmetry (overtly, the anteri- feed heavily on their parents’ mucus, and the or projection of lower jaw is skewed either to Neotropical catfish Ochmacanthus alternus (Ti- the right or left side), which suggests popula- chomycteridae) is a specialized mucus feeder tions might have ‘‘left-handed’’ and ‘‘right- (Winemiller and Yan, 1989). handed’’ morphs that attack from only one side, Scale feeding in C. nama appears to be fac- a phenomenon described for a lepidophagous 906 COPEIA, 2004, NO. 4

in clear water, but water of wetlands in southern India frequently has low transparency caused by high densities of phytoplankton. Presumably, stealth tactics of C. nama would be enhanced in moderately turbid water. The body of C. nama is highly transparent (hence the common name ‘‘glassfish’’), which undoubtedly reduces its de- tection by potential prey. The general body plan, body size, and stealth attack behavior of Roeboides species, another group of lepidopha- gous freshwater fishes, are similar to those of C. nama, and the two groups (Neotropical chara- ciform and Asian perciform) exemplify conver- gence in a trophic specialization. Considerable interspecific variation in body transparency and lepidophagy is observed in both groups (Sazi- ma, 1983; Roberts, 1989), but the degree of cor- relation between these traits is unknown. Fig. 3. Chanda nama (64.1 mm SL) head mor- phology showing jaws open to a right angle and ACKNOWLEDGMENTS curved conical teeth on the mandible. ARG thanks the U.S. Fish and Wildlife Service and its International Coordinator, D. Ferguson cichlid from (Hori, 1993). No for financial support of international travel, R. bilateral asymmetry of dentition was observed and S. Grubh of the Institute for Restoration of in C. nama. Natural Environment provided funding and fa- To observe scale-feeding behavior directly, we cilities for field and lab research in India. The introduced three adult C. nama, five adult Sal- Tamil Nadu Forest Department assisted with ac- mostoma bacaila (Cyprinidae), 10 individuals rep- cess to the study site. Assistance in the field and resenting three Puntius species (Cyprinidae), lab was provided by K. Grubh, A. Rajesh, S. Ve- and six subadult Oreochromis mossambicus (Cich- lappan, S. Kiruba, S. Jeeva, P. Ajitha, and J. Jul- lidae) into a 90-liter aquarium containing aquat- ian. S. Akin and D. A. Arrington assisted with ic vegetation and rocks. The feeding behavior statistical analysis of the data. This work was of C. nama was similar to that described for Ca- conducted under approved Texas A&M Univer- toprion mento (Characidae) by Sazima (1983). sity Use Protocol 2000–190. Typically, the attacker hovered near vegetation or rocks then dashed out to attack passing prey. LITERATURE CITED During an attack, the jaws were opened and held agape as the lower jaw was raked across the BASKIN, J. N., T. A. ZARET, AND F. MAGO-LECCIA. 1980. flank of the prey. Typically, only 1–2 scales were Feeding of reportedly parasitic catfishes (Tricho- dislodged then consumed as they sank in the mycteridae and Cetopsidae) in the Rio Portuguesa water column. Salmostoma bacaila and Puntius Basin, . Biotropica 12:182–186. species were attacked more frequently than O. ECCLES, D. H., AND D. S. C. LEWIS. 1976. A revision of the genus Docimodus Boulenger (Pisces: Cichlidae), mossambicus, the latter preventing many attacks a group of fishes with unusual feeding habits from by facing or evading its attacker. The cyprinids Lake Malawi. Zool. J. Linn. Soc. 58:165–172. were clearly distressed by repeated attacks by C. FRYER, G., P. H. GREENWOOD, AND F. TREWAVAS. 1955. nama, ultimately hovering at the surface in the Scale-eating habits of African cichlid fishes. Nature corner of the aquarium. Sazima (1977) de- 175:1089–1090. scribed a similar response by characids attacked GORLICK, D. L. 1980. Ingestion of host fish surface by Probolodus heterostomus in aquaria, and con- mucus by the Hawaiian cleaning wrasse, Labroides cluded the behavior was an artifact of confine- phthirophagus (Labridae), and its effects on host ment. Individual fish seemed to attack consis- species preference. Copeia 1980:863–868. tently from only one side, but we did not at- HORI, M. 1993. Frequency-dependent natural selec- tion in the handedness of scale-eating cichlid fish. tempt to quantify the phenomenon given our Science 260:216–219. small sample size. The question of ‘‘handed- LEWIS, R. W. 1970. Fish cutaneous mucus: a new ness’’ and bilateral asymmetry in C. nama war- source of skin surface lipids. Lipids 5:947–949. rants further study. LIEM,K.F.,AND D. J. STEWART. 1976. Evolution of the Our aquarium observations were conducted scale-eating cichlid fishes of Lake Tanganyika: a ge- GRUBH AND WINEMILLER—SCALE FEEDING IN CHANDA 907

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