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BRIEF REPORT First Report of Albinism in the White- Spotted Bamboo Shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), With a Review of Reported Color Aberrations in Elasmobranchs Steven Clark n SeaWorld, Inc., Orlando, Florida Three albinistic, white-spotted bamboo sharks (Chiloscyllium plagiosum) (two males and one female) were hatched at SeaWorld parks. Due to their lack of integumentary and retinal pigments, all three animals were considered true albinos. The term ‘‘leucism,’’ more prominently used within the herpetological discipline, is suggested as a more apt description for previously reported color aberrations in elasmobranchs. Reports of color aberrations in other species of elasmobranchs, and a clarification of the terms used to describe these irregu- larities in pigmentation, are also presented. Zoo Biol 21:519–524, 2002. c 2002 Wiley-Liss, Inc. Key words: albinism; leucism; captivity; Hemiscyllidae INTRODUCTION As in other poikilothermic vertebrates, coloration in fishes is determined by chromatophores [Moyle and Cech, 1988; Bechtel, 1995], of which there are three basic types. Melanophores produce melanin, which is responsible for black and c 2002 Wiley-Liss, Inc. n Correspondence to: Steven Clark, Corporate Zoological Operations, SeaWorld, Inc., 7007 SeaWorld Drive, Orlando, FL 32821-8097. E-mail: [email protected] Received for publication July 5, 2001; Accepted March 6, 2002. DOI: 10.1002/zoo.10068 Published online in Wiley InterScience (www.interscience.wiley.com). Zoo Biology 21:519–524 (2002)

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Page 1: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

BRIEF REPORT

First Report of Albinism in the White-Spotted Bamboo Shark, Chiloscylliumplagiosum (Orectolobiformes:Hemiscyllidae), With a Reviewof Reported Color Aberrationsin ElasmobranchsSteven Clarkn

SeaWorld, Inc., Orlando, Florida

Three albinistic, white-spotted bamboo sharks (Chiloscyllium plagiosum) (twomales and one female) were hatched at SeaWorld parks. Due to their lack ofintegumentary and retinal pigments, all three animals were considered truealbinos. The term ‘‘leucism,’’ more prominently used within the herpetologicaldiscipline, is suggested as a more apt description for previously reported coloraberrations in elasmobranchs. Reports of color aberrations in other species ofelasmobranchs, and a clarification of the terms used to describe these irregu-larities in pigmentation, are also presented. Zoo Biol 21:519–524, 2002.�c 2002 Wiley-Liss, Inc.

Key words: albinism; leucism; captivity; Hemiscyllidae

INTRODUCTION

As in other poikilothermic vertebrates, coloration in fishes is determined bychromatophores [Moyle and Cech, 1988; Bechtel, 1995], of which there are threebasic types. Melanophores produce melanin, which is responsible for black and

�c 2002 Wiley-Liss, Inc.

nCorrespondence to: Steven Clark, Corporate Zoological Operations, SeaWorld, Inc., 7007 SeaWorld

Drive, Orlando, FL 32821-8097. E-mail: [email protected]

Received for publication July 5, 2001; Accepted March 6, 2002.

DOI: 10.1002/zoo.10068

Published online in Wiley InterScience (www.interscience.wiley.com).

Zoo Biology 21:519–524 (2002)

Page 2: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

brown pigments; xanthophores generate reds and yellows; and iridophores, althoughthey do not synthesize pigments, are iridescent chromatophores responsible for colorreflection. As in other animals, black and brown integumentary pigmentation of fishis a result of melanophores derived from the neural crest [Bechtel, 1995], while retinalpigmentation results from melanophores arising from the optic cup [Zhao et al.,1997]. Complete albinism is phenotypically expressed as a lack of integumentary andretinal melanin, indicating defects in the integumentary and retinal melanophores.Thus, true albinos lack any dark body pigments and are devoid of eye coloration.However, as other chromatophores may still be functional, albinistic specimens canexhibit integumentary coloration, such as yellows and reds.

Another color aberration, which is used primarily in the herpetologicalliterature and is known as ‘‘leucism,’’ describes a specimen with reduced or absentintegumentary pigment, but with pigmented retinas [Bechtel, 1995; Schmidt, 1999].These organisms have diminished or no body coloration, and darkly pigmented eyes.

This study provides initial documentation of albinism in Chiloscylliumplagiosum, as well as information and suggested descriptive terminology for reportedcolor aberrations in other species of elasmobranchs.

METHODS

Three albinistic, white-spotted bamboo sharks (Chiloscyllium plagiosum) werehatched at SeaWorld parks in Orlando, Florida, and San Diego, California (date ofbirth, sex, and total length at birth, respectively, as follows: 16 August 2000, female,160mm; 3 October 2000, male, not recorded; and 16 March 2001, male, 165mm).The normally-pigmented parents of all offspring are part of the SeaWorld collection.All white-spotted bamboo sharks presently in the SeaWorld collection are descended

Fig. 1. Male, albinistic white-spotted shark (C. plagiosum) soon after hatching, March 2001,at SeaWorld, San Diego, California (total length at hatching: 165mm).

520 Clark

Page 3: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

TABLE

1.Reported

coloraberrationsin

elasm

obranchs

Totallength

Designation

Species

Sex

ordiscwidth

(mm)

Geographic

location

Eye

pigmentation

Original

Present

study

Reference

Rajiform

esDasyatidae

Dasyatisamericana

F243

NorthCarolina,USA

Present

Albinism

Leucism

SchwartzandSafrit[1977]

D.brevicaudatus

HaurakiGulf,New

Zealand

Notreported

Albinism

Reported

inTalent[1973]

D.pastinata

F46

GulfofGabes,Tunisia

Notreported

Albinism

CapapeandPantoustier[1975]

Myliobatidae

Myliobatiscalifornica

F735

Baja

California

Sur,Mexico

Absent

Albinism

Albinism

deJesus-Roldan[1990]

Rhinoptera

bonasusa

F971

Maryland,USA

Present

Notreported

Leucism

Schwartz[1959]

R.bonasus

FB890

ChesapeakeBay,USA

Present

Albinism

Leucism

Joseph[1961]

Rajidae

Raja

batis

F416

Notreported

Notreported

Albinism

Wilson[1951]

R.batis

M735

Aberdeen,Scotland

Notreported

Albinism

Wilson[1951]

R.clavata

F537

Scotland

Notreported

Partialalbinism

Traquair[1893]

R.naevus

F35

Aberdeen,Scotland

Notreported

Albinism

Wilson[1951]

Orectolobiform

esGinglymostomatidae

Nebriusconcolor

M2904

Wakayam

Prefecture,Japan

Present

Partialalbinism

Leucism

TaniuchiandYanagisawa

[1987]

Hem

iscyllidae

Chiloscyllium

plagiosum

bF

160

Florida,USA

Absent

Albinism

Presentstudy

C.plagiosum

bM

Embryo

Florida,USA

Absent

Albinism

Presentstudy

C.plagiosum

bM

165

Florida,USA

Absent

Albinism

Presentstudy

Orectolobidae

Orectolobus

japonicusc

F223

Okinawa

Notreported

Albinism

Iwamasa

andOkano[1982]

O.japonicusc

F225

Okinawa

Notreported

Albinism

Iwamasa

andOkano[1982]

Stegostomatidae

Stegostomafasciatum

F1850

IndianOcean

Present

Albinism

Leucism

Nakaya[1973] Continued

Page 4: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

TABLE

1.(C

ontinued

)

Totallength

Designation

Species

Sex

ordiscwidth

(mm)

Geographic

location

Eye

pigmentation

Original

Present

study

Reference

Carcharhiniform

esCarcharhinidae

Carcharhinusamboinensis

F743

Queensland,Australia

Absent

Albinism

Albinism

McK

ayandBeinssen

[1988]

Sphyrnalewini

M605

Georgia,USA

Absent

Albinism

Albinism

McK

enzie[1970]

Triakidae

Hem

itrakisjapanica

FDaiouzaki,Japan

Absent

Albinsim

Albinism

Furuta

[1984]

Musteluscalifornicus

M263

California,USA

Absent

Albinism

Albinism

Cohen

[1973]

M.californicus

M340

MontereyBay,USA

Notreported

Albinism

Herald

etal.[1960]

M.californicusd

FMontereyBay,USA

Absent

Albinism

Albinism

Talent[1973]

Triakissemifasciata

M600

California,USA

Absent

Albinism

Albinism

Follett[1976]

Hexanchiform

esHexanchidae

Notorynchusmaculatusn

M870

SanFranciscoBay,USA

Present

Partialalbinism

Herald

[1953]

Squaliform

esSqualidae

Squalusacanthias

F990

NorthSea,Norw

ay

Notreported

Albinism

Fr�iland[1975]

Lamniform

esCetorhinidae

Cetorhinusmaxim

us

B3000

Utrisa,Norw

ay

Notreported

Albinism

Fr�iland[1975]

Lamnidae

Carcharodoncarcharias

F1670

E.CapeProvince,S.Africa

Absent

Albinism

Albinism

Smale

andHeemstra

[1997]

Column‘‘Designation’’presents

descriptiveterm

sasoriginallyreported

andmysuggestedterm

inology.‘‘Albinism’’wasreserved

only

forthose

specim

enspossessingreducedorabsentbodyandretinalpigmentation,whiletheterm

‘‘leucism

’’referred

tothose

withreducedorabsentbody

pigmentation,yet

retainingeyeorretinalpigmentation.

aAuthorstatespigmentedeyerules‘‘...outanyalbinocondition.’’

bCaptive-born.

cEmbryosfrom

norm

allypigmentedfemale.

dFiveem

bryosfrom

norm

allypigmentedfemale.

eScattered

bodypigmentation.

n¼N.cepedianus.

Page 5: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

from an initial group of seven animals purchased from overseas collectorsapproximately 13 years ago.

RESULTS

All three sharks possessed considerably reduced body pigmentation through-out, as well as a lack of retinal pigment (Fig. 1). Detection of albinism in the second-born shark occurred prior to hatching (the absence of normal pigmentation wasapparent through the egg case). Faint vertical bars (indicative of the color patternthat emerges in adults) against an almost completely white or cream-coloredbackground were evident on all animals. The first-born animal also possessedscattered patches of darker spots especially on the pectoral fins, the upper lobe of thecaudal fin, and at the base of the first dorsal fin. The combination of a lack ofintegument and retinal pigments indicates that all of the animals were completealbinos.

DISCUSSION

These animals represent the first documented report of color aberrations withinthis family. Because they were born of normal-colored parents, these albinos were aresult of the typical Mendelian autosomal recessive gene inheritance pattern seenbetween heterozygous parents. Other than albinism, these animals appeared normalin all other respects when compared to other normally-pigmented neonates of similarage. The oldest neonate died at 17 days of age. There were no obvious findings froman immediate necropsy to substantiate the cause of death. As of this writing, thesecond and third animals are still alive and appear to be developing normally.Since melanophore anatomy and physiology in amphibians, reptiles, and fish aresimilar, the term leucism, as described by Bechtel [1995], may be applicable toichthyological studies as well. Hence, reports of color aberrations such as albinism orpartial albinism among chondrichthyian fishes reported from a number of orders(Table 1) require closer examination. In keeping with the previously presenteddefinition, specimens with little or no darker body pigments, but with fullypigmented retinas may be described as leucistic [e.g., Nakaya, 1973; Taniuchi andYanagisawa, 1987]. This redefinition, then, reserves the term ‘‘albinism’’ for thoseanimals devoid of both integumentary and retinal melanin pigmentation.

ACKNOWLEDGMENTS

Appreciation is extended to the aquarium staffs at the SeaWorld parks inFlorida and California for providing photographs, information, and husbandry ofthese animals. This is SeaWorld technical contribution 2001-06-F.

REFERENCES

Bechtel HB. 1995. Reptile and amphibian variants:colors, patterns, and scales. Malabar, FL:Krieger Publishing Co. p 206.

Capape C, Pantoustier G. 1975. Anomalies chezquelque salachiens de cotes tunisiennes. ArchInstitut Pasteur Tunis 52:251–62.

Cohen JL. 1973. An albino grey smoothhoundMustelus californicus. Calif Fish Game 59:210–1.

de Jesus-Roldan M. 1990. An albino bat ray,Myliobatis californica, from the Pacific coast ofBaja California Sur, Mexico. Calif Fish Game76:126–7.

White-Spotted Bamboo Shark Albinism 523

Page 6: First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum (Orectolobiformes: Hemiscyllidae), with a review of reported color aberrations in elasmobranchs

Follett W. 1976. First record of albinsim in theleopard shark, Triakis semifasciata Girard. CalifFish Game 62:163–4.

Fr�iland Ø. 1975. Albinisme hos hai. Fauna Oslo28:170–3.

Furuta M. 1984. Sharks of Mie Prefecture.Reports Mie Zool Soc 7:11–3.

Herald E. 1953. The 1952 shark dervies atElkhourn Slough, Monterey Bay and at CoyotePoint, San Francisco. Calif Fish Game 39:237–43.

Herald ES, Schneebeli W, Green N, Innes K. 1960.Catch records for seventeen shark derbies held atElkhorn Slough, Monterey Bay. Calif Fish Game46:59–67.

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McKenzie M. 1970. First record of albinism in thehammerhead shark, Sphyrna lewini (Pisces:Sphyrnidae). J Elisha Mitchell Sci Soc 86:35–7.

Moyle PB, Cech Jr JJ. 1988. Fishes: an introduc-tion to ichthyology. Englewood Cliffs, NJ:Prentice Hall, Inc. p 559.

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comments on albinism in elasmobranchs. Jpn JIchthyol 20:120–2.

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524 Clark