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Descriptions of rajid egg cases from southeastern Australian waters

Article in Zootaxa · June 2006

DOI: 10.11646/zootaxa.1231.1.3

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Accepted by M. de Carvalho: 4 Apr. 2006; published: 12 Jun. 2006 53

ZOOTAXAISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright © 2006 Magnolia Press

Zootaxa 1231: 53–68 (2006) www.mapress.com/zootaxa/

Descriptions of rajid egg cases from southeastern Australian waters

M.A. TRELOAR1, 2, L.J.B. LAURENSON1 & J.D STEVENS21School of Life and Environmental Sciences, Deakin University, PO Box 423, Warrnambool, Victoria, 3280, Australia

2CSIRO Marine and Atmospheric Research, GPO Box 1538, Hobart, Tasmania, 7001, Australia

Abstract

Egg cases from nine skate species occurring in Tasmanian waters were examined and measured. Aspecies-specific identification key is provided for eight of these species. The key was developedprimarily from fresh egg cases dissected from the oviduct, although specimens collected from theocean floor or found dried on the beach were also used to test the key. Egg cases for the ninthspecies could not be included because the only egg case pair recovered was partially formed. Adiagnosis of the posterior end of this egg case is provided.

Key Words: Rajid, egg case, fibroids, anterior, posterior, apron, lateral keel

Introduction

Skates (Family: Rajidae) are oviparous; a reproductive mode that enables females toencapsulate oocytes in morphologically structured shells that suit their environment.Generally, one oocyte from each ovary passes through the oviduct to the oviducal gland.The fertilised ovum then enters the egg case, which is generally one third to half formed.The remainder of the egg case then forms around the ovum. Two egg cases are produced(one in each oviduct) and deposited consecutively onto the substrate. The embryodevelops inside the egg case and is nourished from the nutrients of the yolk until most ofthe yolk is absorbed. The neonate is then strong enough to leave the egg case (Hamlett andKoob 1999). In Australia, there are at least 43 skate species (10 genera) with mostexhibiting a high level of endemicity (Last and Yearsley 2002). Several nomenclaturechanges have occurred in the Australian skate fauna recently with some species remainingundescribed. This may result from rajids forming one of the largest groups ofelasmobranchs and having a high species diversity along with morphological conservatism(McEachran and Dunn 1998).

TRELOAR ET AL.54 © 2006 Magnolia Press

1231ZOOTAXA To date, there are several published identification keys or descriptive morphological

studies on skate egg cases (Clark 1922; Breder and Nichols 1937; Breder and Atz 1938;Ishiyama 1958; Hitz 1964; Templeman 1982; Stehmann and Merrett 2001; Ebert 2005),although few exist for Australian species (Whitley 1938; Whitley 1944). DespiteWhitley’s studies, there is still confusion with identifications of most Australian skate eggcases.

Egg cases have specific characteristics that aid in species identification. Differencesbetween species have been widely noted, although generic characters may also exist.Identifying egg cases can lead to more knowledge about the adaptive differentiation of aspecies and may shed light on the taxonomic status of many species (Ishiyama 1958). Thepurpose of this study was to describe the specific morphological characters for egg casesof each skate species collected in southeastern Australia.

Material and methods

Nine species of skates were collected between 2002 and 2004 from various commercialand recreational fishers around Tasmania, Australia. Each specimen was identified tospecies using Last and Stevens (1994). Both partially and fully formed egg cases wereextracted from the oviduct and stored in 70% ethanol or fixed in formalin and transferredto 70% ethanol for later observation. Maximum width and body length (BL) of each fullyformed egg case were measured with vernier callipers (± 0.1 mm) and the egg case thenweighed using a top loading balance (±1 g). Other morphometrics taken after preservationincluded minimum width, keel width, posterior and anterior horn length and apron length(Fig. 1). Terminology of egg case morphology and methods of measurements wereadapted from Fitz and Daiber (1963) and Ishiyama and Ishihara (1977). Preservation inethanol caused a slight decrease in overall size. The average difference between the eggsin a pair was much less than the average difference between pairs in all species, thereforeone egg case from each pair was measured (Table 1).

Egg cases were either extracted from the oviduct (in utero) and referred to as ‘fresh’,recovered from the ocean, either hatched or soon to hatch and referred to as ‘wet’, orcollected from beaches around Tasmania and referred to as ‘dry’. Ten of the fresh/wetspecimens were air-dried in the laboratory to determine the degree of shrinkage and assistin the identification of dry egg cases. All photographs are of preserved fresh egg cases.

MorphologySkate egg cases are typically rectangular with elongated projections called horns that

extend from each of the four corners. The posterior and anterior horns may differ in length.The posterior end of the egg case is the end that is first to protrude from the cloaca, and iswhere the embryo emerges at hatching (Ishiyama 1958). A noticeable distinguishingfeature between the posterior and anterior ends is the shape of the posterior apron, which is

© 2006 Magnolia Press 55RAJID EGG CASES

1231ZOOTAXAtypically straighter than the anterior apron (Fig. 1).

In general, both the dorsal and ventral sides of the egg case are convex. However thedorsal side is unambiguously more convex as it is positioned along the dorsal side of thefemale’s body and thus follows the contour of the cavity allowing for smooth extraction ofthe egg cases from the cloaca of the mother (H. Ishihara, personal communication, TaiyoEngineering, Tokyo, Japan). The body of egg cases may be coated with filaments orfibroids and may have longitudinal striations that can be deeply or shallowly ridged. Mostskate egg cases have a series of loose fibres along the lateral keel edge called ‘attachmentfibres’ or fibres located near the horns that may aid in securing it to the substrate called‘tendrils’ (Cox et al., 1987). The degree of development of these attachment fibres mayalso be used to distinguish one species from another (Ishiyama 1958).

FIGURE 1. Egg case morphology, terminology and measurements.

Shrinkage, predation and dilapidation of dried egg cases can cause variations in size,shape and structure, which can lead to mis-identification. Egg case colour can varybetween fresh, wet and dried specimens. Several months after being laid, the egg case goesthrough a catechol oxidation process, darkening to almost black (Koob 1987); colour istherefore not useful when developing an identification key for both wet and dry egg cases(Koob 1987).


1231ZOOTAXA


1231ZOOTAXAEgg case size can be used as a distinguishing feature for species identification. Size

may vary considerably within a species, as a significant relationship exists betweenmaternal size and egg case size (Ishiyama 1958; Templeman 1982), although theproportions between measurements remain the same.

Results

Egg cases from most southeastern Australian species have been collected to date.However, the key will require regular updating as new data or species emerge.

Identification key for rajid egg cases collected from skates in southeastern Australian waters

1a Egg case small, ≤ 85 mm BL ........................................................................................ 2 1b Egg case medium to large, ≥ 90 mm BL....................................................................... 52a Lateral keel absent; dorsal and/or ventral surfaces of egg case covered with dense

fibroids .......................................................................................................................... 3 2b Lateral keel present; dorsal and ventral surfaces of egg case not covered with dense

fibroids ....................................................................................... Dipturus sp. A (Fig. 3)3a Posterior horns shorter than body width; egg case > 40 mm BL .................................. 43b Posterior horns at least 2.7 times maximum body width; egg case ≤ 40 mm BL .........

.................................................................................................Pavoraja nitida (Fig. 10)4a Ventral surface of egg case covered with dense fibroids; egg case narrow at posterior

end; posterior apron 1.5 times length of anterior apron .............Dipturus cerva (Fig. 6)4b Ventral surface of egg case not covered with dense fibroids; posterior apron length

almost 3 times the length of anterior apron..........................Dipturus lemprieri (Fig. 8)5a Dorsal and ventral surfaces of egg case covered with dense fibroids; posterior horns

shorter than body width................................................................................................. 65b Dorsal and ventral surfaces of egg case not covered with dense fibroids; posterior

horns at least 1.4 times maximum body width...........Amblyraja cf hyperborea (Fig. 2)6a Lateral keel prominent, > 18% of maximum body width; aprons fringed......................

................................................................................................ Dipturus whitleyi (Fig. 9)6b Lateral keel discrete, < 14% of maximum body width; aprons not fringed.................. 77a Egg case large, ≥ 160 mm BL; posterior horns enclosed in apron ..................................

............................................................................................ Dipturus cf gudgeri (Fig. 7)7b Egg case medium, ≤ 120 mm BL; posterior horns extending out of apron ....................

.....................................................................................................Dipturus sp. B (Fig. 4)

Note: Dipturus sp. L was not included in this key as only partially formed egg cases were examined.


1231ZOOTAXA Descriptions of egg cases

Amblyraja cf hyperborea—Boreal skate (Fig. 2)

DistributionWidely distributed throughout temperate parts of the Atlantic, Pacific and Indian

Oceans. Occurs in depths to 2500 m. Fairly common in southern Australian (particularlyoff Tasmania) and New Zealand waters, occurring in depths of 1300–1500 m (Last andStevens 1994).

FIGURE 2. Ventral and dorsal view of the egg cases of Amblyraja cf hyperborea

DescriptionEgg case large, broad, rectangular (Table 1); colour dark brown; narrower at posterior

end. Ventral side fairly flat; dorsal and ventral sides covered with fine fibroids. Lateral


1231ZOOTAXAkeel > 20% maximum width. Attachment fibres absent; posterior horns depressed, > BL,

tapering out to fine hairs. Anterior horns short; posterior apron length > 25% BL. Anteriorapron length < posterior apron length.

Dipturus sp. A (sensu Last and Stevens, 1994 as Raja sp. A)—Longnosed skate (Fig. 3)

DistributionFound in New South Wales, Victoria and Tasmania in depths from 40–250 m (Last and

Stevens 1994).

FIGURE 3. Ventral and dorsal view of the egg cases of Dipturus sp. A (Last and Stevens 1994).

DescriptionSmall, squat/broad, round in shape (Table 1); colour brown/yellow, transparent;

ventral surface almost flat, dorsal surface convex. Ventral surface smooth with very fewfine fibroids; dorsal surface with fine fibroids. Lateral keel broad, ≥ 5 mm in width on


1231ZOOTAXA each side. Attachment fibres very fine, located on lateral margin; posterior and anterior

horns depressed, short; both aprons short, posterior apron length slightly > anterior apronlength.

Dipturus sp. B ( sensu Last and Stevens, 1994 as Raja sp. B)—Grey skate (Fig. 4)

DistributionFound in waters off New South Wales, Tasmania, South Australia, and Western

Australia. Most abundant at depths of 450–600 m, but recorded over depths of 330–950 m(Last and Stevens 1994).

FIGURE 4. Ventral and dorsal view of the egg cases of Dipturus sp. B (Last and Stevens 1994).

DescriptionEgg case medium to large, slightly rounded in shape (Table 1); colour golden, may


1231ZOOTAXAhave a green tinge. Fibroids thick, present on both dorsal and ventral surfaces; lateral keel

> 9% maximum body width. Attachment fibres prominent on lateral margin; tendrilsextending from posterior horns. Anterior horns slightly longer than posterior horns, hornsdepressed, narrow. Anterior and posterior aprons fully extended, similar in length (> 15%of BL).

Dipturus sp. L ( sensu Last and Stevens, 1994 as Raja sp. L)—Maugean skate (Fig. 5)

DistributionRecorded from two separate estuaries on the west coast of the Tasmanian land-mass

(Bathurst Harbour and Macquarie Harbour). Most common in waters of about 5 m depth(Last and Stevens 1994).

FIGURE 5. Ventral and dorsal view of the egg cases of Dipturus sp. L (Last and Stevens 1994).


1231ZOOTAXA Description

Egg case medium to large, rectangular (Table 1); colour green or brown, almosttransparent; dorsal and ventral surfaces with few fine fibroids; lateral keel > 15%maximum width; attachment fibres absent. Anterior region not described as specimenscollected were only three quarters developed; body length of a complete specimen wouldpossibly be > 90 mm. Posterior horns relatively long, length > 30 mm; posterior apronlong, sub-equal in size to posterior horns; apron fringed, delicate.

Dipturus cerva Whitley, 1939—White-spotted skate (Fig. 6)

DistributionFound in New South Wales, Victoria, Tasmania, South Australia and Western

Australia, in depths of 20–470 m (Last and Stevens 1994).

FIGURE 6. Ventral and dorsal view of the egg cases of Dipturus cerva.


1231ZOOTAXADescription

Egg case small, round in shape (Table 1); colour fawn/brown. Dorsal and ventralsurfaces with thick fibroids; lateral keel absent. Attachment fibres prominent on lateralmargin; horns fairly short, roundish, similar in length at both posterior and anterior ends.As egg case becomes narrower, apron becomes more pronounced at posterior end.

Dipturus cf gudgeri (Whitley, 1940)—Bight skate (Fig. 7)

DistributionFound in New South Wales, Tasmania, South Australia and Western Australia, in

depths of 160–700 m, although most common in waters 400–550 m (Last and Stevens1994).

FIGURE 7. Ventral and dorsal view of the egg cases of Dipturus cf gudgeri.

DescriptionEgg case very large, slightly round in shape (Table 1); colour gold/brown. Egg case

narrows at anterior end; dorsal and ventral surfaces with thick fibroids, both sides convex.Attachment fibres present on lateral margin; posterior horns enclosed in apron with tips ofeach horn extending from apron; posterior apron slightly arch shaped.


1231ZOOTAXA Dipturus lemprieri Richardson, 1845—Thornback skate

(Fig. 8)

DistributionFound in New South Wales, Victoria, Tasmania, and South Australia from the shore to

about 170 m but usually in shallow waters less than 40 m (Last and Stevens 1994).

DescriptionEgg case small, narrow, very slightly rounded in shape; colour fawn or brown (Table

1). Ventral surface almost flat, dorsal surface convex; dorsal surface with felty densefibroids, ventral surface smooth with very fine fibroids; lateral keel absent. Attachmentfibres evident on lateral margin; posterior and anterior horns flat, similar in length;posterior apron 2–3 times longer than anterior apron.

FIGURE 8. Ventral and dorsal view of the egg cases of Dipturus lemprieri.


1231ZOOTAXADipturus whitleyi Iredale, 1938—Melbourne/Whitley’s skate

(Fig. 9)

DistributionFound in New South Wales, Victoria, Tasmania, South Australia and Western

Australia in shallow waters to 170 m (Last and Stevens 1994).

DescriptionEgg case very large and broad, rectangular in shape (Table 1); colour gold or fawn.

Anterior end slightly narrower than posterior end; dorsal surface very convex in shape,covered with thick fibroids. Ventral surface fairly flat; smooth with fine fibroids; lateralkeel broad, > 20% maximum width. Attachment fibres more common on aprons, alsopresent on lateral keel. Posterior and anterior horns short, narrow, flat; aprons long,although posterior apron is longer. Aprons fringed, posterior apron arch shaped.

FIGURE 9. Ventral and dorsal view of the egg cases of Dipturus whitleyi.


1231ZOOTAXA Pavoraja nitida (Günther, 1880)—Peacock skate

(Fig. 10)

DistributionFound in New South Wales, Victoria, Tasmania and South Australia in depths from

30–390 m (Last and Stevens 1994).

FIGURE 10. Ventral and dorsal view of the egg cases of Pavoraja nitida.

DescriptionEgg case very small (Table 1), round in shape; colour fawn/brown. Dorsal and ventral

surfaces with fine fibroids; lateral keel absent; attachment fibres present on lateral edge.


1231ZOOTAXAHorns very long at posterior end, length > 5 cm, taper to fine hairs; anterior horns short,

curving at tips. Anterior apron very short may be up to one third smaller than posteriorapron.

Discussion

This key is suitable for identifying both wet and dry skate egg cases from southeasternAustralia. The key was developed using fresh (extracted from the uteri) egg cases,where correct species identification was assured and egg cases were undamaged. Howeverdrying identified fresh specimens showed that the key would still work on dried egg cases.When dry, the keratin-like substance of the egg case becomes brittle and is prone todamage. At room temperature, dried egg cases shrink by about 30% of their original size.This key was also used on previously unknown specimens collected from the beach. It wasfound if the egg cases were relatively undamaged, identification was possible. Heavilydamaged and predated egg cases were unidentifiable.

The egg case of the different species had a variety of characteristics which allowedthem to be distinguished. Although egg case body size sometimes overlapped betweenspecies, other features could be used to distinguish them, including horn and apronlengths, shape, and presence/absence of a lateral keel and attachment fibres (irrespectiveof whether the egg case was fresh or not).

Further identifications of other Australian skate egg cases are necessary to elucidateany phylogenic relationships between a skate’s genus and its egg cases. It is interestingthat Dipturus cf gudgeri egg cases have horns that are almost fully enclosed in the apron.This feature may be an attribute of a subgenus in the genus Dipturus (Ishiyama 1958). Anegg case with enclosed horns was also found in a Japanese species that belonged to thegenus Dipturus. Ishiyama (1958) and H. Ishihara (Taiyo Engineering, Tokyo, Japan,personal communication) reported some phylogenetic differences in egg cases betweengenera in Japanese species. This suggests that egg case morphology may help indetermining phylogenetic relationships in rajid species, although further work on egg caseassemblages is required both in Australia and worldwide.

Acknowledgements

We wish to acknowledge the following persons and organisations for making this researchpossible. CSIRO Marine and Atmospheric Research and Deakin University for theirsupport, Peter Last who helped with identifications, Louise Conboy for her expertphotography skills, Justin Hulls for editing and etching, Sarah Irvine for editing and RossDaley for assisting with the key.


1231ZOOTAXA References

Breder, C.M., Jr & Nichols, J.T. (1937) The eggs of Raja eglanteria Bosc, with a key to the shellsof New York species. Copeia, 3, 181–184.

Breder, C.M., Jr. & Atz, J.W. (1938) Further notes on the eggs of Raja eglanteria Bosc. Ichthyolog-ical Notes, (3), 145–146.

Clark, R.S. (1922) Skates and Rays (Raiae) No. 1 egg capsules and young. Journal of Marine Bio-logical Association U.K. 12,577–643.

Cox, D.L., Mecham, R.P. and Koob, T.J. (1987) Site-specific variation in amino acid compositionof skate egg capsule (Raja erinacea Mitchell, 1825). Journal of Experimental Marine Biologyand Ecology, 107, 71–74.

Ebert, D.A. (2005) Reproductive biology of skates, Bathraja (Ishiyama), along the eastern BeringSea continental slope. Journal of Fish Biology, 66, 618–649.

Fitz, J., S.E. & Daiber, F.C. (1963) An introduction to the biology of Raja eglanteria Bosc 1802 andRaja erinacea Mitchill 1825 as they occur in Delaware Bay. Bingham Oceanographic Collec-tion Bulletin, 18, 69.

Hamlett, W.C. & Koob, T.J. (1999) Female reproductive system. Sharks, skates, and rays; the biol-ogy of elasmobranch fishes. USA, The Johns Hopkins University Press, pp. 398–443.

Hitz, C. R. (1964). Observations on egg cases of the big skate (Raja binoculata Girard) found inOregon coastal waters. Journal of the Fisheries Research Board of Canada. 21: 851–854.

Ishiyama, R. (1958) Observations on the egg-capsules of skates of the family Rajidae, found inJapan and its adjacent waters. Bulletin of the Museum of Comparative Zoology 118 (1): 1–24.

Ishiyama, R. & Ishihara, H. (1977) Five new species of skates in the genus Bathyraja from thewestern North Pacific, with reference to their interspecific relationships. Japanese Journal ofIchthyology 24 (2): 71–90.

Koob, T.J. (1987). Effects of oxidation and reduction on the spectral properties of the egg capsulesof Raja erinacea Mitchill. Journal of Experimental Marine Biology and Ecology 113:155–166.

Last, P.R. & Stevens, J.D. (1994) Sharks and Rays of Australia. CSIRO Australia, 513 PP.Last, P.R. & Yearsley, G.K. (2002) Zoogeography and relationships of Australasian skates (Chon-

dricthyes: Rajidae). Journal of Biogeography, 29, 1627–1641.McEachran, J. D. & Dunn, K.A. (1998). Phylogenetic analysis of skates, a morphologically conser-

vative clade of elasmobranchs (Chondrichthyes: Rajidae). Copeia, 2, 271–290.Stehmann, M. & Merrett, N.R. (2001) First records of advanced embryos and egg capsules of

Bathyraja skates from the deep north-eastern Atlantic. Journal of Fish Biology, 59,338–349.Templeman, W. (1982) Development, occurrence and characteristics of egg capsules of the Thorny

skate, Raja radiata, in the Northwest Atlantic. Journal of Northwest Atlantic Fish Science, 3,47–56.

Whitley, G.P. (1938). The eggs of Australian sharks and rays. The Australian Museum Magazine, 6,372–382.

Whitley, G. P. (1944) Interesting Sharks’ Eggs. The Australian Museum Magazine, 260–261.

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