Structure and Development of the Parotoid Gland in … · 2015. 6. 30. · morphs (three females,...

American Society of Ichthyologists and Herpetologists (ASIH) is collaborating with JSTOR to digitize, preserve and extend access to Copeia.

http://www.jstor.org

Structure and Development of the Parotoid Gland in Metamorphosed and Neotenic Ambystoma gracile Author(s): Lawrence E. Licht and David M. Sever Source: Copeia, Vol. 1993, No. 1 (Feb. 11, 1993), pp. 116-123Published by: American Society of Ichthyologists and Herpetologists (ASIH)Stable URL: http://www.jstor.org/stable/1446302Accessed: 30-06-2015 16:06 UTC

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

This content downloaded from 147.174.85.132 on Tue, 30 Jun 2015 16:06:04 UTCAll use subject to JSTOR Terms and Conditions

http://www.jstor.org

http://www.jstor.org/action/showPublisher?publisherCode=asih

http://www.jstor.org/stable/1446302

http://www.jstor.org/page/info/about/policies/terms.jsp



116 COPEIA, 1993, NO. 1

S. H. Weitzman for their critiques of an earlier draft; D. J. Stewart for contributing literature and information concerning Neolebias; and G. G. Teugels and D. A. Hendrickson for the loan of museum specimens. Funding for field research was furnished by the United States Cen- ter for International Exchange of Scholars and the United States Information Service in the form of a Fulbright Research Grant to the first author.

LITERATURE CITED

BELL-CROSS, G., ANDJ. L. MINSHULL. 1988. The fishes of Zimbabwe. National Museums and Monu- ments of Zimbabwe, Harare, Zimbabwe.

HUBBS, C. L., AND K. F. LAGLER. 1958. Fishes of the Great Lakes region. Cranbrook Institute of Sci- ence, Bloomfield, Michigan.

KELLEY, D. W. 1968. Fishery development in the central Barotse flood plain. FAO Fish. UNDP(TA) Rep. FRi/UNDP(TA): 1-151.

LEVITON, A. E., R. H. GIBBS, JR., E. HEAL, AND C. E. DAWSON. 1985. Standards in herpetology and ichthyology: Part 1. Standard symbolic codes for in- stitutional resource collections in herpetology and ichthyology. Copeia 1985:802-832.

POLL, M. 1967. Contribution a la faune ichthyolo-

gique de l'Angola. Publication Culturais Compan- hia de Diamantes de Angola 75:1-381.

__---, AND J. P. GOSSE. 1963. Revision des genres Nannaethiops Giinther, 1871 et Neolebias Steindach- ner, 1894 et descriptuion de trois especies nouvelles (Pisces; Citharinidae). Annls. Mus. R. Afr. Centr. 116:5-40.

---, AND - . 1982. Rehabilitation des genres Congocharax Matthes, 1964 et Dundocharax Poll, 1967 (Pisces, Distichodontidae) mis en synonymie par R. P. Vari, 1979 avec Neolebias Steindachner. Bull. Inst. R. Sci. Nat. Belg. 54:1-8.

TEUGELS, G. G., AND T. R. ROBERTS. 1990. Descrip- tion of a small distinctively coloured new species of the characoid genus Neolebias from the Niger delta, West Africa (Pisces; Distichodontidae).J. Afr. Zool. 104:61-67.

VARI, R. P. 1979. Anatomy, relationships and clas- sification of the families Citharinidae and Disticho- dontidae (Pisces, Characoidea). Bull. Br. Mus. Nat. Hist. (Zool.) 36:261-344.

WINEMILLER, K. 0. 1991. Comparative ecology of Serranochromis species (Teleostei: Cichlidae) in the Upper Zambezi River. J. Fish Biol. 39:617-639.

DEPARTMENT OF WILDLIFE AND FISHERIES SCI-

ENCES, TEXAS A&M UNIVERSITY, COLLEGE

STATION, TEXAS 77843-2258. Submitted 22 Nov. 1991. Accepted 12 Feb. 1992. Section editor: R. Winterbottom.

Copeia, 1993(1), pp. 116-123

Structure and Development of the Parotoid Gland in

Metamorphosed and Neotenic Ambystoma gracile

LAWRENCE E. LICHT AND DAVID M. SEVER

Structure and development of the parotoid gland were examined in larval, metamorphosed, and neotenic Ambystoma gracile. Larvae first show gland en-

largement when they are near 50 mm SVL, the size at metamorphosis. The gland is well developed in metamorphs and only partially developed in neotenes. In neotenes, gland height is reduced but histology and histochemistry do not differ from that in metamorphosed individuals. Lowering the head and positioning of the gland as part of defensive behavior first appears at metamorphosis, and such behavior is readily shown by most metamorphs. Larvae and neotenes do not show the same defensive behavior as metamorphs.

AT metamorphosis, larval salamanders undergo numerous morphological changes

involving skin texture, skull shape, tongue appearance, hyobranchial apparatus, and gill slit closure and loss (Lauder and Shaffer, 1986; Reilly, 1987; Reilly and Lauder, 1988). Some salamanders, however, may not metamorphose,

and neoteny, the attainment of sexual maturity with the retention of larval morphology, occurs in all families (Dent, 1968; Duellman and Trueb, 1986). Neoteny can be either complete or in- complete (Reilly, 1986, 1987). For example, in the family Salamandridae, neoteny is incom- plete, and many features such as gill structures

@ 1993 by the American Society of Ichthyologists and Herpetologists



LICHT AND SEVER-PAROTOID DEVELOPMENT IN AMBYSTOMA 117

remain larval, but skull morphology becomes adult. In the Ambystomatidae, there is com-

plete larval morphology in these characters

(Reilly, 1986, 1987), although at sexual matu-

rity, the cloacal glands in neotenes become adult (Licht and Sever, 1991).

Facultatively neotenic species are those in which some individuals of a population undergo metamorphosis and others remain larval (Duell- man and Trueb, 1986). The Northwestern Sal- amander, Ambystoma gracile, is unique among such species in having enlarged, raised parotoid glands on the head behind the eyes (Bishop, 1943; Stebbins, 1951). The general morphology of the gland, effects of glandular secretions, and use of the gland in defensive behavior in metamorphosed A. gracile have been described

by Brodie and Gibson (1969) and Williams (1983). Neither the ontogeny of gland development in metamorphs nor the extent of gland development in neotenic individuals has been studied in detail. Thus, we examined a series of A. gracile including larval, neotenic, and metamorphosed individuals to describe histological details of gland structure and to determine the extent of gland development in all life-history forms of the species. Moreover, because most

morphological features in neotenic A. gracile remain larval (Reilly, 1987), the comparative development of the parotoid gland in neotenes and metamorphs represents a useful character to establish a more complete description of het- erochronic characters in this species.

MATERIALS AND METHODS

Ambystoma gracile were collected from the Lit- tle Campbell River in Langley, British Colum- bia, and Hollyburn Mountain in West Vancou- ver, British Columbia. Some specimens, collected in 1969, 1984, or 1988, were used in other studies (Licht, 1975; Lowcock and Licht, 1990; Licht and Sever, 1991) and were preserved in 5% formalin. Voucher specimens are

deposited in the Canadian Museum of Nature, NMC 33903-1 to 33903-7. Three types of individuals were examined: juvenile larvae, metamorphs, and neotenes. Sexual maturity was es- tablished by the presence of enlarged testes and coiled, pigmented vasa deferentia in males and

yolk-filled, pigmented ova in females (Sem- litsch, 1985; Lowcock and Licht, 1990).

Parotoid gland dimensions.-The parotoid gland is visible as a dorsal swelling on either side of the head and extends from the neck to the eye. Gland length through its midline was measured in the metamorphs from the posterior margin

of the gland on the neck to the anterior margin at the eye. In branchiate individuals, because the gland was not conspicuously enlarged, this measurement was made at a point from the third

gill arch to the eye. The snout-vent length (SVL to nearest 1 mm) and length of gland site (nearest 0.5 mm) were measured in larvae, metamorphs, and neotenes. For visibly enlarged glands, gland height and width (at midpoint of the gland to nearest 0.5 mm) were measured by use of a dissecting microscope. All measurements were log transformed, and the relationship between SVL and gland dimensions was

analyzed by least-squares regression. Males and females (excluding juvenile larvae) were ana-

lyzed separately to test for sexual dimorphism in gland length. Measurements for metamorphs and neotenes were compared by analysis of co- variance (Zar, 1984). All statistical analyses were run on Statistical Analysis System computer programs (SAS, 1985).

Histology.-For histological studies, six metamorphs (three females, 71-80 mm, and three males, 74-79 mm SVL) and seven neotenes (three females, 63-76 mm, and four males, 65- 77 mm SVL) were examined. All specimens were

laboratory-reared individuals of the same age (13 months' posthatching). The parotoid gland region for three larvae (35-48 mm SVL) was also examined histologically. Parotoid glands were excised from specimens preserved in 5% formalin, rinsed in water, dehydrated in a grad- ed series of alcohol, cleared in toluene, and em- bedded in paraffin. Sections 10 ,m thick were cut on a rotary microtome and affixed to al- buminized slides. Some slides from each specimen were stained in hematoxylin-eosin whereas others were treated with the "histochemical quad stain" (Floyd, 1990), which contains stains and reactions diagnostic for proteins (naphthol yellow S), neutral carbohydrates (periodic acid/ base fuchsin Schiff-PAS), and acidic muco- substances (Alcian blue at pH 2.0).

The heights of 11 gland tubules selected at random from the midline of the parotoid gland cluster were measured to the nearest 0.01 mm with an ocular micrometer in a microscope at 100 x magnification.

Behavior.-As part of another study (Licht, 1992), a series of larvae of A. gracile were raised in the laboratory under constant temperature (19.5 ? 1 C) and food levels. After a number of months, some larvae metamorphosed, and other remained branchiate as neotenes. The neotenes were kept separately in glass bowls with one liter of dechlorinated water, and meta-



118 COPEIA, 1993, NO. 1

.'043

CB7

0 Fig. 1. Parotoid gland in Ambystoma gracile: (A) Gland enlargement in metamorphic (on left) compared to

neotenic individual, each 65 mm SVL; (B) cut parotoid gland showing depth (2 mm); (C) newly metamorphosed individual showing defensive behavior and parotoid gland directed toward probe.




morphs were held individually in plastic boxes lined with wet paper towels. All were kept at 19.5 (+1) C.

To assess salamander defensive behavior, especially as it related to the use of the head and parotoid gland area, 23 neotenes and 27 metamorphs were each touched with a glass probe on the tip of the snout or the gland. Twelve other individuals were tested as they completed metamorphosis and still retained gill stubs. All neotenic and metamorphosed individuals were over 55 mm SVL. Observations were made on the immediate response and general behavior of each individual, but results were not quan- tified.

RESULTS

Parotoid gland dimensions.-The gland is a kid- ney-shaped swelling on the head behind the eye (Fig. 1). Gland length, or the site for gland lo- cation, did not differ between metamorphosed males (n = 26) and females (n = 23) {F = 2.15, P > 0.20}, nor between neotenic males (n = 22) and females (n = 31) {F = 1.21, P > 0.20}. Gland length varied directly with SVL in larvae, metamorphosed and neotenic individuals [sexes combined (Table 1)]. The regression lines for gland length and SVL for metamorphosed and neotenic groups differ significantly (ANCOVA, F[1,981 = 60.25, P < 0.001).

The gland is conspicuously raised in metamorphosed individuals but not in either larvae or neotenes (Fig. 1 A-B). Mean gland height for 20 metamorphosed individuals (56-80 mm SVL) was 1.90 mm (SD = 0.20), and mean width was 6.15 mm (SD = 0.56). Gland width was significantly correlated with SVL (r = 0.868, df = 18, P < 0.001), but gland height was not (r = 0.222, df = 18, P > 0.20). Swelling of the gland was barely perceptible in neotenes, and neither height nor width was measured.

The gland first became visibly enlarged as larvae, from 50-55 SVL, began to metamorphose. By the time gills are resorbed, the gland was fully enlarged in length from neck to eye and was 1.5-2.0 mm high (n = 12). An individual (55 mm SVL) with gill stubs had enlarged glands (Fig. 1C).

Histology.-The parotoid gland is composed of numerous granular glands in the dermis (Wil- liams, 1983). No sexual dimorphism in gland cytology was observed. In metamorphosed individuals, the granular glands are tightly packed, columnar, and filled with granules of two sorts (Fig. 2A). The most numerous granules are eosinophilic and about 5

tsm in diameter. These

are separate from small groups of larger granules, about 20 Ctm in diameter, that vary from basophilic to eosinophilic. Both types of granules stain positively for proteins and give a slightly positive PAS reaction for neutral carbohydrates.

Nuclei are flattened and are limited to the periphery of the gland. Usually a distinction between cytoplasm and luminal contents was not resolved, especially in the most full glands. Where the luminal-epithelial borders are ap- parent, the epithelial layer is a narrow, simple band of cells, cuboidal toward the epidermis and squamous distally. Thus, the bulk of each gland is composed of granules in the lumen.

At the junction between each gland and the basal surface of the epidermis is a narrow duct that leads from the granular gland lumen to the surface of the epidermis (Fig. 2B). A demilune containing PAS-positive granules is near the base of the duct. Superficial to the epithelial cells is a thick sheath that contains melanin and PAS+ collagen fibers. As noted by Williams (1983), a superficial collar of smooth muscle surrounds the base of the excretory duct. Alcian blue-positive mucous glands also occur in the dermis, and the epidermis is composed of three layers of cuboidal epithelial cells covered by a superficial squamous keratinized layer.

The main difference between the granular glands in metamorphosed compared to neotenic individuals is gland height. In metamorphosed individuals, mean gland height is 1.11 mm (SD = 0.19); in neotenes, mean gland height is 0.54 mm (SD = 0.19). No difference in gland height exists between sexes of either neotenes or metamorphs. Otherwise, metamorphosed and neotenic individuals differ only in skin anatomy (Fig. 2C). In the neotenes, the outer keratinized layer of the epidermis is absent, and Leydig cells, containing PAS-positive and naphthol yellow-positive granules, are numerous in the epidermis. As in metamorphs, mucous glands are abundant in the dermis of neotenes.

Evidence of dermal gland development was seen in only one immature larval specimen, 47 mm SVL, that possessed flattened granular glands 0.10-0.18 mm in diameter (Fig. 2D). These glands contain small granules that give slightly positive reactions to PAS and naphthol yellow and large vacuoles containing a floccu- lent substance that reacts positively to naphthol yellow. Mucous glands are absent in this individual. No glands occur in the dermis in the other immature larvae.

Behavior.-Larvae and neotenes responded to a touch on their snout or neck from a glass



120 COPEIA, 1993, NO. 1

Ai '" , ? A , -j•:

" ?-.,: ? -,. .

. .7 . . . .H.. .• .

Sg _ N u

. .: - r1* a

.. ,. . S m ... . - .L.g.,./

•. F

,." ..,"

.. .: Y~fif W4

'Nu -S c Sg '

m g

AK .WO..ro

• ,,,,• - 4.1

L c S9

C ;-c" 5g L~s' ? ?;?.,np

•. .• .'..• :•;•":, - • •-.•. "-= ••'- • '-:'. ,•' ? 2 ... = . - .

• ,.• l "-" . ,. .* ,.' -. " --. .. .•,•,,'' '.

:

So * :?.?~ ::a :. - • • -... •/

? t"S

~~...? .. .. .. .1?. cp ?r

.-:. .. •.' " m• "

- • - •.

• .. . ' See

Fig. 2. Sagittal sections through granular glands in the parotoid region of Ambystoma gracile. (A) Overview of several granular glands in a metamorphosed male, 79 mm SVL. (B) Higher magnification of same specimen used in (A), showing details of the excretory pore and surrounding structures. (C) Neotenic female, 65 mm SVL. (D) Immature larva, 47 mm SVL. Scale bar in lower right corner-120 gm for (A), 4 4m for (B), and 6 gm for (C) and (D). Ep = epidermis; Fs = fibrous sheath surrounding each granular gland; Lc = Leydig cells in the epidermis; Lg = large granules; Mg = mucous gland in dermis; Nu = nucleus of granular gland epithelial cell; Po = excretory pore of a granular gland; Sc = stratum compactum of the dermis; Sg = small

granules; Sk = skeletal muscle; Sm = smooth muscle around neck of excretory duct; and Va = vacuoles in larval granular gland.

probe by quickly swimming away. Flight was immediate and no individual appeared to twist its head or neck region nor butt or press against the probe. In contrast, 23 of 27 metamorphs bent their heads and arched the parotoid gland toward the probe (Fig. 1C); 22 individuals lifted their tails and tilted their bodies toward the probe when they were touched on the side of the head. The behavioral response shown by most postmetamorphic animals was also shown

by all 12 individuals tested that were losing tail fins and gills and at the beginning of metamorphosis.

DISCUSSION

The parotoid gland is characteristic of the toad genus Bufo, and, in that taxon, the gland structure and secretions have been well studied (e.g., Noble, 1931; Low, 1972; Cannon and Hostetler, 1976). Among salamanders, the glands are known from species in several fam-

ilies including Plethodontidae, Salamandridae, and Ambystomatidae (Anderson, 1961; Stew- ard, 1970; Brodie, 1977).

In A. gracile, the fully enlarged gland is found only in metamorphosed individuals, and gland enlargement begins at metamorphosis. Where- as other features, such as gill structure and skull

morphology, remain larval in neotenic A. gracile (Reilly, 1986, 1987), the parotoid gland can be considered intermediate in development. In neotenes, the gland enlarges but not to the full extent seen in metamorphosed individuals. The skin of neotenes remains larval, retaining com- ponents such as Leydig cells (Dodd and Dodd, 1976), but the slight enlargement of the parotoid represents a tendency toward metamorphosis. Thyroxine influences the development of skin glands at metamorphosis (Dodd and Dodd, 1976), and, thus, the partial enlargement of the parotoid gland in neotenes likely indicates increase in levels of thyroxine or other hormones. In A. gracile and other neotenic am-




TABLE 1. COEFFICIENTS FOR LEAST-SQUARES REGRESSION OF LOG GLAND LENGTH (G)* AGAINST LOG SVL (S) FOR LARVAL, NEOTENIC, AND METAMORPHOSED Ambystoma gracile. The straight line is log G = log A + b log

S; log A and b are intercept and slope, respectively, with standard error (SE).

Gland SVL length

Form n a (mm) x (mm) b (SE) log A (SE) r P

Larval 52 29.8 5.93 1.8246 (0.0922) -1.9363 (0.1350) 0.942 <0.001 Neotenic 54 68.1 14.05 0.9828 (0.0809) -0.6553 (0.1482) 0.860 <0.001 Metamorphosed 48 69.8 12.25 0.9037 (0.1112) -0.5792 (0.2049) 0.768 <0.001

* G is distance from neck to eye and length of visibly enlarged gland in metamorphosed individuals, undeveloped gland site in larvae, and partially enlarged gland in neotenes.

bystomatids, neotenes show increased thyroid activity at the time when metamorphosis would normally occur, but levels of thyroid hormones are lower than in metamorphs and not high enough to induce transformation (Norris and Platt, 1973; Eagleson and McKeown, 1978). The parotoid glands begin to enlarge in larvae of about 50 mm SVL, the size when metamorphosis usually occurs (Licht, 1992). Likely changes in levels of hormones in neotenes are also re- flected by the full development of the cloacal glands and the synchrony of sexual maturity in neotenes and metamorphs (Licht and Sever, 1991).

The distance from neck to eye represents ac- tual length of enlarged glands in metamorphs and site of the partially developed gland in neotenes. Gland length and width vary directly with SVL, and the significantly shorter gland length in metamorphs compared to neotenes (Table 1) is a consequence of the presence of eyelids in metamorphs only (Fig lA). Height of the gland is nearly the same for all metamorphosed individuals and does not vary with SVL.

The granular glands of the parotoid gland are not different in cytology from those else- where in the dermis of the skin (Williams, 1983), except for their relatively larger size in metamorphosed individuals. Granular glands in the dorsal tail base, however, also may be enlarged, at least in well-fed individuals, and these caudal granular glands function in nutrient storage as well as predator defense (Williams and Larsen, 1986).

Williams (1983) also noted two types of granules in the granular glands of A. gracile. At the ultrastructural level, the larger granules are membrane bound and separated from the more numerous (70% of the secretion) small granules by unit membrane. As found here, he also reported that both types of granules give positive reactions to protein stains; presumably both form part of the excreted product. Viewed with transmission electron microscopy, the granular gland epithelia form a syncytium, and myoepi-

thelial cells occur in the sheath surrounding each gland. These features were not observed in the parotoid gland cluster, but they may not be resolved by light microscopy.

Brodie and Gibson (1969) reported that the gland first appeared about one month after metamorphosis. In contrast, we found the gland already enlarged by the completion of gill re- sorption (Fig. 1C). Gland appearance may de- pend on the size and condition of the individual at metamorphosis and subsequent growth rate. For example, in toads, the parotoid gland becomes fully formed 3-4 weeks after metamorphosis in laboratory-raised animals (Licht, 1967), but larger, wild-caught individuals show enlarged glands 7-10 days earlier (LEL, pers. obs.).

Observed use of the gland in defensive behavior by metamorphosed individuals is the same as that described by Brodie and Gibson (1969). A metamorphosed individual does not flee but rather lifts its body, may raise its tail also containing skin glands, and directs the parotoid gland toward a potential threat (Fig. IC). In this way, maximal gland surface area is exposed to an attacker. This posture and positioning of the gland are exhibited only by metamorphosing animals, and such behavior is acquired at the same time as the gland is structurally enlarged. The gland may also be useful in intraspecific interactions. Metamorphosed A. gracile emit sounds that may function to reduce intraspecific aggression (Licht, 1973), and vocalization cou- pled with defensive positioning of the parotoid glands could function to prevent bites and wounds during agonistic encounters. Larvae and neotenes flee rapidly if provoked and show no tendency to confront a potential threat; neither makes the sounds emitted by the metamorphs (LEL, pers. obs.).

The parotoid gland is probably more effective in a terrestrial setting and may not be useful for larvae or neotenes in the aquatic environ- ment. Gland secretions are water insoluble, highly viscous and adhesive, and very effective in adhering to the mouth and eyes of potential



122 COPEIA, 1993, NO. 1

mammalian predators (Brodie and Gibson, 1969). On land, the metamorphs face a large variety of vertebrate predators likely sensitive to the bitter taste and toxic effects of the secretions. In contrast, neotenes face few predators except fishes: for example, large trout are

reported to prey on A. gracile (Efford and Ma- thias, 1969). Those fishes large enough to cap- ture neotenes may swallow them whole and are not as prone to chew their prey as do mammalian predators. Thus, the adhesive quality and distasteful properties of gland secretions

may not be effective on aquatic predators, and the insolubility of secretions in water may reduce transmission of secretions. Of relevance is the fact that neotenic populations of A. gracile predominate in high altitude, permanent, typ- ically fish-free lakes (Sprules, 1974), and, except as small larvae prone to insect predation, larger neotenes apparently face little predation.

ACKNOWLEDGMENTS

We thank M. Stasiuk for help with manuscript preparation. This research was supported by the Natural Sciences and Engineering Research Council of Canada Grant 3142 to LEL and Na- tional Sciences Foundation Grant BSR 87-15341 to DMS.

LITERATURE CITED

ANDERSON, J. D. 1961. The life history and system- atics of Ambystoma rosaceum. Copeia 1961:371-377.

BISHOP, S. C. 1943. Handbook of salamanders. Com- stock Publishing, Ithaca, New York.

BRODIE, E. D., JR. 1977. Salamander antipredator postures. Copeia 1977:523-535.

--, AND L. S. GIBSON. 1969. Defensive behavior and skin glands of the northwestern salamander, Ambystoma gracile. Herpetologica 25:187-194.

CANNON, M. S., AND J. R. HOSTETLER. 1976. The anatomy of the parotoid gland in Bufonidae with some histochemical findings. J. Morph. 148:137- 160.

DENT, J. N. 1968. Survey of amphibian metamor-

phosis, p. 271-311. In: Metamorphosis. A problem in developmental biology. W. Etkin and L. I. Gil- bert (eds.). Appleton-Century-Crofts, New York, New York.

DODD, M. H. I., AND J. M. DODD. 1976. The biology of metamorphosis, p. 467-599. In: Physiology of the Amphibia. B. A. Lofts (ed.). Academic Press, New York, New York.

DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of

amphibians. McGraw-Hill, New York, New York. EAGLESON, G. W., AND B. A. MCKEOWN. 1978.

Changes in thyroid activity of Ambystoma gracile (Baird) during larval, transforming, and postmetamorphic phases. Can. J. Zool. 56:1377-1381.

EFFORD, I. E., AND J. A. MATHIAS. 1969. A compar-

ison of two salamander populations in Marion Lake, British Columbia. Copeia 1969:723-736.

FLOYD, A. D. 1990. Morphology and the art of tissue

analysis. LabLeader 5:3,6. Shandon-Lipshaw, Pitts-

burgh, Pennsylvania. LAUDER, G. V., AND H. B. SHAFFER. 1986. Functional

design of the feeding mechanism in lower verte- brates: unidirectional and bidirectional flow systems in the tiger salamander. Zool. J. Linn. Soc. 88:277-290.

LICHT, L. E. 1967. Initial appearance of the parotoid gland in three species of toads (genus Bufo). Her-

petologica 23:115-118. . 1973. Sound production and behaviour in

the northwestern salamander, Ambystoma gracile. Can. J. Zool. 51:1055-1056. -. 1975. Growth and food of larval Ambystoma

gracile from a lowland population in southwestern British Columbia. Ibid. 53:1716-1722.

- . 1992. The effect of food level on growth rate and frequency of metamorphosis and paedomor- phosis in Ambystoma gracile. Ibid. 70:87-93.

- , AND D. M. SEVER. 1991. Cloacal anatomy of metamorphic and neotenic salamanders. Ibid. 69: 2230-2233.

Low, B. S. 1972. Evidence from parotoid-gland secretions, p. 244-264. In: Evolution in the genus Bufo. W. F. Blair (ed.). Univ. of Texas Press, Austin.

LOWCOCK, L. A., AND L. E. LICHT. 1990. Natural

autotriploidy in salamanders. Genome 33:674-678. NOBLE, G. K. 1931. The biology of the Amphibia.

McGraw-Hill, New York, New York. NORRIS, D. O., AND J. E. PLATT. 1973. Effects of

pituitary hormones, melatonin, and thyroid inhib- itors on radio-iodide uptake by the thyroid glands of larval and adult tiger salamanders, Ambystoma tigrinum (Amphibia: Caudata). Gen. Comp. Endo- crinol. 25:368-376.

REILLY, S. M. 1986. Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens, and its relationship to metamorphosis and neoteny. J. Morph. 188:315-326.

- . 1987. Ontogeny of the hypobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): the ecological morphology of two neotenic strategies. Ibid. 191:205-214.

-, AND G. V. LAUDER. 1988. Ontogeny of aquatic feeding performance in the eastern newt, Noto- phthalmus viridescens (Salamandridae). Copeia 1988: 87-91.

SAS INSTITUTE INC. 1985. SAS users guide: statistics, Ver. 5 ed. Statistical Analysis Systems Institute, Inc., Cary, North Carolina.

SEMLITSCH, R. D. 1985. Reproductive strategy of a facultatively paedomorphic salamander Ambystoma talpoideum. Oecologia 65:305-313.

SPRULES, W. G. 1974. Environmental factors and the incidence of neoteny in Ambystoma gracile (Baird) (Amphibia: Caudata). Can. J. Zool. 53:1545-1552.

STEBBINS, R. C. 1951. Amphibians of western North America. Univ. California Press, Berkeley.

STEWARD, I. W. 1970. The tailed amphibians of Eu- rope. Taplinger Publ., New York, New York.




WILLIAMS, T. A. 1983. Structure and function of the granular skin glands of the salamanders of the family Ambystomatidae (Amphibia: Urodela). Unpubl. Ph.D. diss., Washington State Univ., Pullman.

--, AND J. H. LARSEN, JR. 1986. New function for the granular skin glands of the eastern long- toed salamander, Ambystoma macrodactylum colum- bianum. J. Exp. Zool. 239:329-333.

ZAR,J. H. 1984. Biostatistical analysis. Prentice Hall, Englewood Cliffs, New Jersey.

(LEL) DEPARTMENT OF BIOLOGY, YORK

UNIVERSITY, 4700 KEELE STREET, TORONTO, ONTARIO M3J 1P3 CANADA; AND (DMS) DE- PARTMENT OF BIOLOGY, SAINT MARY'S

COLLEGE, NOTRE DAME, INDIANA 46556. Sub- mitted 19 Aug. 1991. Accepted 1 Feb. 1992. Section editor: D. G. Buth.

Copeia, 1993(1), pp. 123-133

Phylogenetic Relationships of the Sternoptychid Argyropelecus (Teleostei: Stomiiformes)

ANTONY S. HAROLD

The seven valid species of Argyropelecus are the subject of a phylogenetic analysis. Selected aspects of osteological and photophore anatomy were surveyed for these taxa and the outgroups Argyripnus, Polyipnus, Sonoda, and Sternoptyx. Argyropelecus and Sternoptyx are corroborated as sister groups and Polyipnus as their sister group. Of Argyropelecus species, affinis and gigas form a clade which is the sister group to the remaining members of the genus. Those five species are united by eight synapomorphic aspects of pelvic girdle, anal-fin pterygio- phore, pleural rib, and parasphenoid form. The three species lychnus, olfersi, and sladeni form a clade which is sister group to aculeatus and hemigymnus. These last two species are highly disparate in overall form, but that is inferred to be due mainly to paedomorphic features, including small adult body size and body shape little modified from postlarvae, in hemigymnus. Five synapomorphies, notable among them highly compressed supraneural shafts, support this relationship of aculeatus and hemigymnus.

T HE Sternoptychidae, according to the phylogenetic analysis of Weitzman (1974),

comprises the 10 genera Araiophos, Thorophos, Maurolicus, Danaphos, Valenciennellus, Argyrip- nus, Sonoda, Polyipnus, Sternoptyx, and Argyrope- lecus. Among the many synapomorphies uniting these taxa are the presence of Type Alpha pho- tophores and their occurrence in glandular clusters, only three branchiostegal rays associ- ated with the posterior ceratohyal, parietals separated by the supraoccipital bone, lack of a ba- sihyal, and absence of mesopterygoid teeth. The last three genera, the hatchetfishes, are deep- bodied, their name referring to the apomorphic abdominal keel structure and highly compressed body. To date, there is little under- standing of relationships within any sternoptychid genus nor has any explicitly been demonstrated to be monophyletic. To develop

reliable classifications at higher levels the in- tegrity of recognized genera should be probed. My research on Polyipnus, to be published separately, indicates that the genus is monophyletic. This conclusion is vital to the interpreta- tion of characters occurring among Argyropelecus species that bear some resemblance to conditions in derived members of Polyipnus.

Argyropelecus hemigymnus Cocco, 1829, was the first member of the genus to be described, and it remains the smallest species, not known to exceed 40 mm standard length. Several similar nominal species have been described, A. durvilli Cuvier and Valenciennes, 1849, A. intermedius Clarke, 1877, and A. heathi Harvey, 1952; but these were justifiably synonymized by Baird (1971) with A. hemigymnus. Argyropelecus olfersi (Cuvier, 1829), originally ascribed to the genus Sternoptyx, is one of the larger, very deep-bodied

? 1993 by the American Society of Ichthyologists and Herpetologists



Date post:	08-Oct-2020
Category:	Documents
Upload:	others
View:	4 times
Download:	0 times

Structure and Development of the Parotoid Gland in … · 2015. 6. 30. · morphs (three females,...

Documents