Journal of Fish Biology (2000) 56, 552–576 doi: 10.1006/jfbi.1999.1182, available online at http://www.idealibrary.com on Abundance, distribution, morphometrics, reproduction and diet of the Izak catshark A. J. R*¶, G. M*, L. J. V. C†, R. W. L‡, D. A. E§ M. J. G* *Zoology Department, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa; †Shark Research Centre, South African Museum, P.O. Box 61, Cape Town 8000, South Africa; ‡Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa and §U.S. Abalone, P.O. Box 254, Davenport, CA 95017, U.S.A. (Received 19 August 1999, Accepted 19 October 1999) Holohalaelurus regani was caught in 38% of the 3314 bottom trawls conducted during routine demersal surveys off the South African west and south coasts from 1986 to 1999. An index of biomass for H. regani has increased on the west coast, from 1606 t in 1986–1993 to 3012 t in 1994–1999, despite c. 130 t being taken annually as by-catch in the demersal fishery. On the south coast, there has also been an increase over the same period, from 793 to 1350 t. Females and juveniles were generally found in shallower water (<300 m) than males, suggesting an inshore nursery area. Male H. regani become mature at 450–500 mm L T , whereas females become mature at 400–450 mm L T . There is reproductive activity throughout the year and fecundity appears to be high. This species is a generalist feeder, with the diet comprising teleosts, crustaceans and cephalopods. H. regani also scavenges offal opportunistically. Its high fecundity, the relative protection of females and juveniles in shallow water that is rarely trawled, its opportunistic diet and its robust nature that may allow it to survive after it has been discarded, have enabled H. regani to increase in numbers, despite indirect fishing pressure. 2000 The Fisheries Society of the British Isles Key words: chondrichthyans; catshark; by-catch; maturation; fecundity; diet; scavenging. INTRODUCTION Sharks are a common component of the demersal fish community off southern Africa, and are regularly landed as by-catch in the trawl fishery (Smale & Compagno, 1997). Sharks are generally slow growing and have low fecundity. Thus, they are highly susceptible to over-exploitation, even as a consequence of incidental fishing mortality. This has led to some concern about the effect that the demersal fishery in South Africa may have on chondrichthyans, resulting in a number of studies on the biology of these species (Smale, 1991; Ebert, 1994; Ebert et al., 1996; Smale & Compagno, 1997). Catsharks (Scyliorhinidae, Carcharhiniformes) are, along with dogfish (Squaliformes) and skates (Rajiformes), the most diverse component of the demersal chondrichthyan fauna in southern Africa. The family comprises c. 108 species world-wide (Compagno, 1984, 1988, 1999), with at least 18 species in southern African waters (Compagno et al., 2000). The Izak catshark ¶Author to whom correspondence should be addressed at present address: Oceanography Department, University of Cape Town, Rondebosch 7701, South Africa. Tel.: +27 21 650 3286; fax: +27 21 650 3979; email: [email protected]552 0022–1112/00/030552+25 $35.00/0 2000 The Fisheries Society of the British Isles
Transcript
Journal of Fish Biology (2000) 56, 552–576doi: 10.1006/jfbi.1999.1182, available online at http://www.idealibrary.com on
Abundance, distribution, morphometrics, reproduction anddiet of the Izak catshark
A. J. R*¶, G. M*, L. J. V. C†, R. W. L‡,D. A. E§ M. J. G*
*Zoology Department, University of the Western Cape, Private Bag X17, Bellville 7535,South Africa; †Shark Research Centre, South African Museum, P.O. Box 61,
Cape Town 8000, South Africa; ‡Marine and Coastal Management, Private Bag X2,Rogge Bay 8012, South Africa and §U.S. Abalone, P.O. Box 254, Davenport,
CA 95017, U.S.A.
(Received 19 August 1999, Accepted 19 October 1999)
Holohalaelurus regani was caught in 38% of the 3314 bottom trawls conducted during routinedemersal surveys off the South African west and south coasts from 1986 to 1999. An index ofbiomass for H. regani has increased on the west coast, from 1606 t in 1986–1993 to 3012 t in1994–1999, despite c. 130 t being taken annually as by-catch in the demersal fishery. On thesouth coast, there has also been an increase over the same period, from 793 to 1350 t. Femalesand juveniles were generally found in shallower water (<300 m) than males, suggesting aninshore nursery area. Male H. regani become mature at 450–500 mm LT, whereas femalesbecome mature at 400–450 mm LT. There is reproductive activity throughout the year andfecundity appears to be high. This species is a generalist feeder, with the diet comprisingteleosts, crustaceans and cephalopods. H. regani also scavenges offal opportunistically. Itshigh fecundity, the relative protection of females and juveniles in shallow water that is rarelytrawled, its opportunistic diet and its robust nature that may allow it to survive after it has beendiscarded, have enabled H. regani to increase in numbers, despite indirect fishing pressure.
¶Author to whom correspondence should be addressed at present address: Oceanography Department,University of Cape Town, Rondebosch 7701, South Africa. Tel.: +27 21 650 3286; fax: +27 21 650 3979;email: [email protected]
INTRODUCTION
Sharks are a common component of the demersal fish community off southernAfrica, and are regularly landed as by-catch in the trawl fishery (Smale &Compagno, 1997). Sharks are generally slow growing and have low fecundity.Thus, they are highly susceptible to over-exploitation, even as a consequence ofincidental fishing mortality. This has led to some concern about the effect thatthe demersal fishery in South Africa may have on chondrichthyans, resulting ina number of studies on the biology of these species (Smale, 1991; Ebert, 1994;Ebert et al., 1996; Smale & Compagno, 1997).
Catsharks (Scyliorhinidae, Carcharhiniformes) are, along with dogfish(Squaliformes) and skates (Rajiformes), the most diverse component of thedemersal chondrichthyan fauna in southern Africa. The family comprises c. 108species world-wide (Compagno, 1984, 1988, 1999), with at least 18 speciesin southern African waters (Compagno et al., 2000). The Izak catshark
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0022–1112/00/030552+25 $35.00/0 � 2000 The Fisheries Society of the British Isles
F. 1. (a) Adult male Holohalaelurus regani and (b) an egg case (bar=5 mm).
Holohalaelurus regani Gilchrist is a member of a genus endemic to southern andeast Africa [Fig. 1(a)]. H. regani itself may be confined to southern Africa, asH. regani-like sharks off east Africa are distinct (Compagno, 1988) and probablyrepresent a separate species (H. melanostigma, LJVC, unpubl. data). Bass et al.(1975) noted that H. regani off the kwaZulu-Natal coast of South Africa andsouthern Mozambique had a somewhat different colour pattern and were smallerthan typical H. regani from waters off the Cape coast of South Africa. Thepresent paper concerns typical H. regani, described from Cape Seas (Gilchrist,1922) and ranging from southern Namibia to the Eastern Cape coast of SouthAfrica.
Although H. regani is the most common demersal cartilaginous fish caught intrawls in the Cape region (Compagno et al., 1991), knowledge of its basic biologyis limited. Bass et al. (1975) reviewed its biology, but their data are mostly basedon specimens from kwaZulu-Natal and southern Mozambique. It is known thatmature females bear only one cased egg per oviduct (single oviparity; Nakaya,
1975; Compagno, 1988), unlike certain other scyliorhinids including the SouthAfrican tiger catshark Halaelurus natalensis (Regan) that have several cased eggsper oviduct (multiple oviparity). H. regani is found between 98 and 515 m depthsoff the Cape coast of South Africa and Namibia (Compagno et al., 1991), andeats (in order of importance) teleosts, crustaceans and cephalopods (Ebert et al.,1996). However, aside from these pieces of information, relatively little isknown.
The results of a study of the general biology of H. regani, including itsmorphometrics, reproduction and feeding are presented here, together with anassessment of the distribution, stock size and annual by-catch by the demersalfishery. It is likely that the most feasible conservation option for a whole suite ofby-catch species such as H. regani will be the implementation of open oceanmarine protected areas. Thus, knowledge of the biology, distribution andabundance of these species is crucial in the selection of such sites. This workrepresents the first detailed study of H. regani.
MATERIALS AND METHODS
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F. 2. H. regani distribution based on observed density (kg km�2) per trawl from all surveys. Trawlpositions shown as dots.
STUDY AREASamples were collected during routine hake biomass surveys conducted by the Chief
Directorate: Marine and Coastal Management using the research vessel FRS Africana offthe west and south coasts of South Africa between Port Elizabeth and the Orange River(Fig. 2) from 1986 to 1999. The detailed methodology for station selection anddescription of the gear deployed are given in Payne et al. (1985). Briefly, trawls wereconducted on a semi-random, depth-stratified basis during daylight hours. Each trawl
was designed to last for 30 min, but because of the irregular topography of the seabedsome were of shorter duration. Two regions were surveyed (Fig. 2):
(1) West Coast: The continental shelf and upper slope south of the internationalborder with Namibia (c. 29� S) and west of Cape Agulhas (20� E) out to the 500-misobath. There was one annual survey in summer and one in winter from 1986 to1990, but only an annual summer survey since then.
(2) South Coast: The continental shelf east of Cape Agulhas (20� E) to about PortElizabeth (26� E), out to the 200-m isobath. For some surveys the upper slope(200–500-m isobaths) was included. In general, there have been two surveys peryear, one in autumn (to the 200-m isobath) and one in spring (to the 500-misobath).
On both west and south coasts, ad hoc trawls at depths >500 m were madeoccasionally. This sampling strategy has led to some bias in the data, because differentmonths, areas and depths were sampled each year using a different number of trawls(Table I).
ABUNDANCE AND DISTRIBUTIONBiomass estimates of H. regani were calculated for 100-m depth strata from trawl data
using the areal-expansion method (Payne et al., 1985) separately for west and southcoasts. Mean density per stratum was calculated and extrapolated to the total area perdepth stratum. Biomass estimates were not calculated from Cruise 060 because the entirerange of H. regani was not covered, nor from Cruise 069 because the ship broke downafter only 25 stations (Table I).
The area swept by each trawl was estimated as the product of the width (mouthopening of the net assumed as a constant 26 m) and length (calculated as towing speed,3·5 kt, times trawl duration) of the trawl track. The density of H. regani (kg km�2) wasthen calculated by dividing the mass caught by the area swept by each trawl. Distributionmaps of H. regani based on the estimated density from each trawl were then constructedusing the kriging routine in Surfer (Golden Software Inc., U.S.A.).
MORPHOMETRICSSpecimens of H. regani were sexed, measured (L to �1 mm) and weighed (W to
�1 g). Measurements included pre-caudal length and total length (LT, with the tailextended in a straight line to provide maximum length; Compagno, 1984). For males, theouter left clasper length and the width at the base of the left clasper were also measured.The heart was weighed from nine specimens. Owing to time constraints after each trawl,not all H. regani caught could be processed (Table I), nor could all the biologicalinformation be collected from every specimen. However, the specimens that wereprocessed were chosen randomly.
REPRODUCTIONTo identify changes in sexual maturity with size, a number of pertinent variables were
measured. Testes of males and ovaries of females were removed, weighed and thegonadosomatic index (IG=100(gonad mass)(body mass)�1) was calculated. To obtain anestimate of lipid reserves, which may indicate sexual maturity, the liver of males andfemales was weighed and the hepatosomatic index (IH=(liver mass)(body mass)�1)calculated. A number of other measurements were also made to assess maturity,including for males the length and width of each testis, and for females the presence ofegg cases in the oviduct, the maximum egg size in the ovary, the number of eggs in theovary and the width of the shell gland. Length and width of 11 egg cases were alsomeasured.
DIET ANALYSISStomachs were removed by opening the body cavity and severing the gut at the
oesophagus and at the posterior margin of the duodenum. Watery fluid was allowed to
556 . . .
T I. The area (west coast=west of 20� E, south coast=east of 20� E), cruise details,the number of trawls and the number of H. regani collected for biological sampling from
the 38 cruises conducted by the Chief Directorate: Marine and Coastal Management
drain from the contents before weighing. Although prey fragments were sorted andidentified to the lowest possible taxon and then weighed (�1 g), the data were pooledsubsequently by major taxon (teleosts, crustaceans or cephalopods) because the stomachcontents were often too digested to allow consistent identification. Prey items were
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identified using a variety of guides (e.g. Barnard, 1950). The contribution of the majortaxonomic groups to the diet was assessed using standard quantitative measures (Hyslop,1980), namely numerical importance (%N), gravimetric importance (%M) and frequencyof occurrence (%F). The index of relative importance (IRI) was then calculated as%F(%N+%M). To investigate changes in diet associated with growth, H. regani weregrouped into four arbitrary size classes, namely <350, 350–450, 450–550 and >550 mmLT.
RESULTS
ABUNDANCE AND DISTRIBUTIONOn the west coast, the biomass of H. regani has increased from a mean of
1606 t (for the period 1986–1993) to a mean of 3012 t [1994–1999, Fig. 3(a)]. Theanomalously high biomass estimate in January 1990 is likely to be an overesti-mate, as this peak is also seen in other species such as hake Merluccius spp. andhorse mackerel Trachurus trachurus capensis Nekrasov 1978 (Chief Directorate:Marine and Coastal Management, unpublished data). It is more difficult toassess the trend in H. regani biomass on the south coast because only some ofthe surveys trawled deeper than 200 m (see Table I) and there was a large andvariable portion of the biomass from 200 to 500 m on the south coast(2·5–49·7%, mean 21·7%). However, biomass estimates for 0–200 m depth couldbe calculated from each survey and these were plotted separately from estimatesfor 0–500 m depth [Fig. 3(b)]. For the 0–200 m depth stratum, the biomassincreased from a mean of 516 t (for the period 1986–1993) to a mean of 840 t(1994–1999). Similarly, for the 0–500-m depth stratum, the biomass increasedfrom a mean of 793 t (1986–1993) to a mean of 1350 t [1993–1999, Fig. 3(b)].Therefore, the total biomass of H. regani in the two regions has increased by82%, from a mean of 2400 t (1986–1993) to a mean of 4360 t (1994–1999).
H. regani were found in 38% of the 3314 trawls over the entire survey area,from 29� S to 26� E, although its abundance decreased east of Cape Agulhas(Fig. 2). Within this geographic range, H. regani occupied a broad band thatextended to greater depths along the south (46–910 m) than the west (50–500 m)coasts. H. regani were rarely found shallower than 100 m depth. Patches of highdensity were found where the shelf was broad. Highest densities were 338·2 kgkm�2 at 230 m depth on the west coast and 261·1 kg km�2 at 292 m depth onthe south coast.
The relationship between H. regani biomass and depth was similar on both thewest and south coasts. Biomass was generally low inshore and on the slope, andpeaked at intermediate depths. The majority (56%) of the biomass of H. reganialong the west coast was distributed between 200 and 300 m depth [Fig. 4(a)],and more than 75% of the biomass on the south coast was located between 100and 200 m depth [Fig. 4(b)].
There was little seasonal change in the distribution of H. regani on the westcoast over the 1986–1993 period [Fig. 5(a) and (b)], although densities did appearto be slightly higher during summer. Neither was there any major change in thesummer distribution of H. regani on the west coast between the period of lowbiomass [1986–1993, Fig. 5(b)] and the period of high biomass [1994–1999, Fig.5(c)]. The increase in the biomass on the west coast was a result of a generalincrease in estimated density over the entire reported range, not to a change in
558 . . .
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F. 3. Biomass (in t, mean�CV) of H. regani from 1986 to 1999 on (a) west and (b) south coasts.(b) �, 0–200 m (generally spring); �, 0–500 m (generally autumn).
the distribution or to extended range. There was also no clear seasonal changein the distribution of H. regani on the south coast (Fig. 6). However, there is asuggestion of a seasonal migration to the southern tip of the Agulhas Bankduring autumn.
There was a marked shift in the ratio of males to females in the populationwith increasing depth (Fig. 7). Populations were dominated by females(0·60 : 1) in water <200 m depth [Fig. 7(a)], but became progressively more
559
male dominated with increasing depth; at depths >400 m, the sex ratio was 10 : 1[Fig. 7(d)]. The frequency histograms in Fig. 7 also show that juveniles(<300 mm LT) and large females were generally found inshore (<300 m).
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MORPHOMETRICSA total of 1819 specimens of H. regani was examined. Males were significantly
longer (mean LT 485·1 mm, range 84–685, n=957) than females (401·2 mm,range 110–520, n=838; t=16·23, d.f.=1793, P<0·0001). The modal size classfor males was 550–600 mm LT, whereas the modal class for females was450–500 mm LT. It is noteworthy that the size distribution of both males andfemales was skewed towards larger individuals (Fig. 7). The mean mass of males(364·9 g, range 3–1060) was greater than that of females (199·1 g, range 3–470).
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F. 6. Holohalaelurus regani distribution on the south coast based on observed density (kg km�2) for (a)spring and (b) autumn surveys. Trawl positions shown as dots.
562 . . .
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F. 7. Length–frequency histograms for males ( ) and females ( ) for depths of (a) <200 m (n=700, sexratio 0·60 : 1), (b) 200–300 m (n=889; sex ratio 1·37 : 1), (c) 300–400 m (n=150; sex ratio 6·50 : 1)and (d) >400 m (n=55; sex ratio 10 : 1).
563
There was a very strong relationship between body mass (W) and LT for bothsexes, with the equations for males and females given by:
males: W=5·063�10�7L3·264T , r2=0·98; n=541;
females: W=1·997�10�7L3·426T , r2=0·96; n=449;
The slope of the curve was significantly steeper for females than males(ANCOVA, F=17·8, d.f.=986, P<0·0001), implying females were bulkier thanmales for a given size.
There was no significant difference in the slopes of the sex-specific linearrelationships between LT and pre-caudal length (LPC, mm; ANCOVA, F=0·45,d.f.=988, P>0·05), and the combined equation is given by:
LPC=0·804LT�8·741 (r2=0·998, n=545, P<0·0001).
The mean heart mass was 0·62 g (range 0.1–2.1, n=9), corresponding to 0·17%of the body mass.
MATURATION AND REPRODUCTION: MALESThe relationship between outer clasper length of males and LT was positive
and sigmoid in form [Fig. 8(a)]. The greatest rate of change in clasper lengthoccurred in individuals between 400 and 450 mm LT. Basal clasper widthbroadened with increasing LT [Fig. 8(b)]. The dimensions of the testes (lengthand width) increased with LT [Fig. 8(c)], although the rate of increase in lengthtapered off after c. 600 mm LT. There was no difference in the width of the rightand left testis, but the left testis was consistently longer than the right one from400 mm LT. There was a rapid increase in gonad weight with body size[Fig. 9(a)]. However, IG reached a maximum of 0·6% at 500 mm LT, and thenremained relatively constant [Fig. 9(c)]. Liver mass increased with body size[Fig. 10(a)]. Although IH of males remained constant (3·5%) in individuals up to450 mm LT, it increased to reach a peak of 4.5% at 550 mm LT, before decreasingagain [Fig. 10(b)].
MATURATION AND REPRODUCTION: FEMALESMaturation of females was characterized by enlargement of the shell gland.
The relationship between shell gland width and LT followed a sigmoid curve[Fig. 11(a)], with the most rapid increase in gland width for individuals between400 and 450 mm LT. This LT corresponded to a shell gland width of 10 mm, andcoincided with an increase in the maximum diameter of eggs in the uterus[Fig. 11(b)] and a rapid decline in the number of eggs in the ovary [Fig. 11(c)].The gonad mass also increased with LT [Fig. 9(b)], with IG reaching a maximumof c. 3% at 450 mm LT [Fig. 9(d)]. Liver mass increased with LT [Fig. 10(a)] andIH increased to 5·5% at 350 mm LT and then declined [Fig. 10(b)].
Egg cases of H. regani are light brown in colour, have a velvety covering withlongitudinal striations and long tendrils from each corner [Fig. 1(b)]. The meanlength of 11 egg cases was 39·7 mm (range 36–43) and the mean width was13·3 mm (range 12–15). Female H. regani began to produce cased eggs between
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F. 8. Changes in (a) outer clasper length and (b) basal clasper width with LT. (c) The increase in testesdimensions with LT. Lines were fitted using the distance-weighted least squares smoothingprocedure. (c) Right testis (——): �, length; �, width; left testis (. . . .): �, length; , width.
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380 and 400 mm LT, with the proportion of females with cased eggs increasing toc. 50% from 440 to 460 mm LT. A study conducted in January and July 1986revealed that 30·1% of the 83 individuals examined that did not have cased eggsnevertheless had uncased eggs within the oviduct. There was no significantdifference in the proportion of mature females that had cased eggs duringsummer (45%, n=183), autumn (53%, n=17), winter (51%, n=71) and spring(52%, n=56, �2=1·42, d.f.=3, P>0·05).
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F. 9. The increase in gonad weight with size for (a) males and (b) females, and the relationship betweenthe gonadosomatic index (IG) and LT for (c) males and (d) females. Lines were fitted using thedistance-weighted least squares smoothing procedure.
DIETStomach contents of 378 H. regani specimens were examined. There was no
evidence of stomach eversion and only 0.8% (three out of the 378 stomachs) wereempty. Twenty-five prey groups could be positively identified (Table II). Therewere six species of teleosts, nine groups of crustaceans and five species ofcephalopods found in the stomach contents, with polychaetes, hydrozoans andgastropods constituting an insignificant component of the diet. Overall, teleosts
566 . . .
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I H
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400 600
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er m
ass
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F. 10. The increase in (a) liver mass with total length for males (. . . .�. . . .) and females (—�—). Therelationship between (b) hepatosomatic index (IH) and LT for males and females. Lines were fittedusing the distance-weighted least squares smoothing procedure.
(IRI=4706) were the most important prey item, followed by crustaceans(IRI=1980) and then cephalopods (IRI=800, Fig. 12). Cephalopods generallyhad high %N, but their %M was very low.
The order of importance of the three major prey groups in the diet was thesame for all size classes of H. regani (Table III). However, as H. regani increased
567
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Shell gland width (mm)
Nu
mbe
r of
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s
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6 10 12 1684
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ize
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)
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Sh
ell g
lan
d w
idth
(m
m)
4
16
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200 400300
(a)
12
4
F. 11. Changes in (a) shell gland width with LT, (b) maximum egg size in the ovary with shell glandwidth and (c) number of eggs in the ovary with shell gland width. Lines were fitted using thedistance-weighted least squares smoothing procedure.
in size, teleosts became relatively less important and crustaceans becamerelatively more important. There was no consistent trend in the preference forcephalopods with increasing H. regani size.
568 . . .
DISCUSSION
T II. List of species identified in the stomach contents of H. regani; a study duringJanuary 1997 revealed that 55% of the stomachs had nematode parasites and 17·5% of the
*Not recorded in the diet previously by Ebert et al. (1996).
ABUNDANCE AND DISTRIBUTIONH. regani is ubiquitous around the South African west and south coasts at
depths between 100 and 500 m. This study extends the depth range of H. reganifrom 98 to 515 m in Cape and Namibian waters (Compagno et al., 1991) to40–910 m. Based on data for 1986–1990, Compagno et al. (1991) postulated aslight northward extension of H. regani in summer. The additional datapresented here do not support this hypothesis.
The best estimate of the current biomass of H. regani off the west and southcoasts of South Africa is c. 4360 t. This estimate should be used with caution,however, because the two assumptions implicit in the swept area method havenot been verified. First, it is assumed that everything in front of the net is caught.This may not always be true, as the net opening extends only 2 m off the bottomand some fish may go over the net. One possible explanation for the few smallindividuals in the length–frequency plots is that juveniles may move up into thewater column (and avoid capture) and are thus under-sampled. Second, it isassumed that the density of a species on untrawlable grounds (rocky substrates)
F. 12. Numerical importance (%N), gravimetric importance (%M) and frequency of occurrence (%F)of teleosts, crustaceans and cephalopods in the diet. The index of relative importance,IRI=%F(%N+%M), for each dietary item is represented by the area of the square.
is the same as that calculated for the trawl grounds, which may be violated if aspecies has a substrate preference. Long tendrils on H. regani egg cases suggestthat they are attached to a rocky substrate, as are the egg cases of otherscyliorhinids (Castro et al., 1988). Moreover, the dark colour of young(<230 mm LT) H. regani that Bass et al. (1975) suggested was an adaptation todeep water may actually provide camouflage on rocky substrate. Therefore,biomass estimates could be biased because many juveniles and few adults may befound on rocky substrates.
Despite the caveats associated with the biomass estimates, the increasing trendin biomass on both the west and south coasts should be unaffected by theassumptions in the swept area method, as any biases should be constantthroughout the time series. It is useful to place the biomass estimate of H. reganiin context of the amount that may be taken as by-catch by the demersal fishery.From data collected during 402 commercial trawls on the west coast, H. reganirepresented 0·13% of the hake biomass caught (S. Hart, coordinator SANCORObserver Programme, pers. comm.). For an annual hake quota of 100 000 t onthe west coast, this equates to 130 t of H. regani or c. 4% of the biomass index peryear. However, some individuals caught in demersal trawls may survive, asH. regani are relatively robust, often swimming away when returned to the seaafter being caught in a trawl.
To interpret the increasing trend in H. regani biomass, it is necessary to takecognizance of the changes in the pattern of fishing effort by the demersal fleetsince 1986. On the west coast, there has been a shift in the fishing effort to deeper
F. 13. Total fishing effort (in days) for the demersal fleet for (a) west and (b) south coasts. Effortstatistics for the south coast include the estimated effort from the inshore fleet, which is known tobe very imprecise and is not used routinely for hake management.
waters, with the total effort remaining relatively constant [Fig. 13(a)]. Bycontrast, on the south coast there has not been a shift in the effort, but areduction in the effort in the 101–200-m depth stratum [Fig. 13(b)]. It ishypothesized that the increase in H. regani biomass during the 1990s could be aconsequence of the reduced effort not only on areas of maximum concentrationof H. regani (compare Figs 4 and 13), but on females and juveniles, which arefound more commonly inshore (Fig. 7). This inshore region could be a nurseryarea, as migration of pregnant females into areas to give birth is a common traitamong sharks (Springer, 1967).
572 . . .
MORPHOMETRICSIn H. regani, males attain a larger size than females, an unusual situation in
sharks. However, males are also larger than females for the kwaZulu-Natal andMozambique form of H. regani, for Holohalaelurus punctatus (Gilchrist &Thompson) and possibly for Scyliorhinus capensis (Smith, in Muller & Haenle)(Bass et al., 1975; Compagno, 1984, 1988), although this is not a generalcharacteristic of scyliorhinids.
The liver of H. regani (5% by body weight) is relatively small compared withpelagic and slope-dwelling sharks, which have a lot of oil to maintain buoyancy(Bone & Roberts, 1969; Baldridge, 1970). For instance, the liver of the tigershark Galeocerdo cuvier (Peron & Lesueur) is 20% of its body weight and that ofthe more sedentary ragged-tooth shark Carcharias taurus Rafinesque is over 8%(Crile & Quiring, 1940).
Available data on heart weights of large sharks (LJVC, unpubl. data) suggeststhat H. regani has a relative heart weight (0·17% of body weight) approachinglarge and active species of sharks. Individuals of the highly active andwarm-blooded white shark Carcharodon carcharias (L.) and shortfin mako sharkIsurus oxyrinchus Rafinesque between 1 and 3 m long have heart weightsaveraging about 0·19 and 0·23% of body weight. Less active large sharks havesmaller hearts, including a 3-m ragged-tooth shark with a heart about 0·11% ofbody weight and a 4-m sleeper shark Somniosus antarcticus (Bloch & Schneider,1801) with a heart about 0·09% of body weight. Further evidence for H. reganibeing more active than previously thought is provided by the direct observationof four separate individuals during dives aboard the Jago submersible at 300 mdepth (dive numbers 502 and 507 off Child’s Bank, sponsored by De Beer’sMarine). One individual remained motionless on the bottom as the submersiblepassed. The other three individuals were seen swimming actively across the fieldof view about 1 m off the bottom.
REPRODUCTIONFemale H. regani become mature at 400–450 mm LT. This conclusion is based
on a number of lines of evidence. The first appearance of cased eggs in the uteruscoincided with a widening of the uterus, a rapid expansion in the width of theshell gland and the greatest IG. There was also a concomitant increase in themaximum egg size in the ovary (from 2 to 10 mm) and a decrease in the numberof eggs in the ovary (from 80 to 20). Ovulation in female H. regani occurs oncean egg is 11 mm in size. The greater IG of females (3%) compared with males(0·6%) probably contributes towards the slightly bulkier build of females thanmales of the same size, and accounts for the steeper slope of their length–weightrelationship.
A high proportion of mature females carry egg cases (c. 48%) and almostone-third of the remaining mature females without cased eggs have uncased eggsin utero. In terms of the seasonality of spawning, the most parsimoniousconclusion is that female reproduction is continuous throughout the year(although not all months were sampled). Although the batch frequency ofH. regani was not measured, another scyliorhinid, the chain dogfish Scyliorhinusretifer (Garman), can lay one egg pair every 15 days over a 2-year period (Castroet al., 1988). Therefore, reproduction by female H. regani is probably high and
continuous throughout the year, a strategy that would help to maintain highnumbers, even if many are taken as by-catch.
In female H. regani between 350 and 450 mm LT, IH decreased sharply as IG
increased. This may be attributable to the diversion of energy reserves toreproduction, as lipids are stored in the liver of chondrichthyans (Bone &Roberts, 1969; Craik, 1978). Interestingly, IH did not continue to decrease oncefemales reached full maturity (450 mm LT), despite a high proportion of thesefemales being reproductively active. This contrasts with the situation for sharksthat are live-bearers, where pregnant females show a decrease in IH (King, 1984;Smale & Compagno, 1997).
Male H. regani become mature from 450 to 500 mm total length (LT). Thisconclusion is based on the rapid elongation of the claspers and the size at whichIG has reached a maximum. For mature males, the rate of elongation of theclaspers decreases after 550 mm LT, but the basal width continues to broaden.Thus, for mature males there is continual stiffening of the claspers withincreasing size.
It is difficult to interpret the fluctuations in male IH. If considerable lipidresources are used in sperm production, then the decrease in IH after 550 mm LT
may suggest the onset of sperm production. This may be despite males beingmorphologically mature at 450–500 mm LT. More data on lipid reserves and theonset of sperm production are needed to solve this problem.
DIETH. regani consume a wide range of prey items, suggesting that it is a generalist
feeder. This is in accordance with the results of Ebert et al. (1996) who foundthat H. regani, together with other catsharks Apristurus microps (Gilchrist) andScyliorhinus capensis, were less specialized in their feeding than Apristurussaldanha (Barnard), Apristurus spp. and Galeus polli Cadenat. In this study, fourspecies of fish, four species of cephalopods and various smaller items wereidentified from the stomach contents that have not been recorded in the diet ofH. regani previously (Table II).
The three most important prey groups of H. regani were, in order ofimportance, teleosts, crustaceans and cephalopods. Teleosts were also the mostimportant prey item in the diet study of H. regani by Ebert et al. (1996), althoughit is difficult to compare IRI values directly between studies, because IRI valuescan vary depending on taxonomic resolution (Hansson, 1998). By contrast, Basset al. (1975) found that cephalopods were the most important prey group ofH. regani and cephalopods are known to be an important component of the dietof the dogfish Scyliorhinus retifer (Castro et al., 1988). In the present study andthat by Ebert et al. (1996), cephalopods generally had a high %N and a low %M.Thus, the contribution of cephalopods to the diet of H. regani may be eitherunder-estimated if cephalopod soft tissue is digested more rapidly than that ofteleosts and crustaceans, or over-estimated if their beaks remain in the stomachfor a long time after the soft tissue has been digested.
It is difficult to ascertain the relative importance of scavenged food to activelycaught prey in the diet of H. regani, as all the fish and squid noted in the dietcould be discards from demersal and pelagic fisheries operations. It is likely thatH. regani capture live crustaceans such as hermit crabs because they are
relatively robust and probably survive being returned to the sea after beingcaught in a trawl. In addition, crustaceans are known to be the majorcomponent of the diet of other catshark species in the Mediterranean (Carrasonet al., 1992). However, a number of lines of evidence suggest that H. reganiscavenges at least part of the teleost and cephalopod component of its diet.First, it is unlikely that H. regani could catch live highly mobile animals such assome of the pelagic fish (e.g. anchovy Engraulis capensis Gilchrist and sardineSardinops sagax (Jenyns), some demersal fish (e.g. ribbonfish Lepidopus and hakeMerluccius spp.), and active cephalopods (e.g. Sepia australis). Second, some ofthe food items are rarely found close to the bottom in deep water, such as thepelagic fish and the cephalopod Argonauta spp. Last, many of the teleostremains in the diet were fish heads. Cephalopods commonly remove the heads ofpelagic fish during feeding (Lipinski, 1987), and the heads of larger fish (Capehakes) are removed during cleaning at sea by fisheries operations (Smale &Compagno, 1997). Thus, it is likely that H. regani cruise the sea bottomscavenging fish and squid offal, and seizing any live crustaceans, fish and squidthat it can subdue. Should much of the teleost and cephalopod component ofthe diet be scavenged, it is interesting to note the absence of some species that arecommonly discarded at sea. These include dragonets Paracallionymus costatusBoulenger, 1898 and rattails Caelorinchus spp. and Malacocephalus laevis(Lowe). Further work is needed to ascertain the relative contribution of live preyand offal to the diet of H. regani.
There was a change in the diet of H. regani with increasing size, withcrustaceans becoming more important and teleosts less important. This may bebecause small H. regani could have more difficulty capturing protectedcrustaceans such as hermit crabs than do large individuals. Lyle (1983) foundthat as Scyliorhinus canicula (L.) increased in size, its consumption of hermitcrabs increased. Ontogenetic changes in diet are common among marinecarnivores (Steven, 1930), and are thought to minimize intra-specific competitionfor food. This has been noted for a number of other sharks around southernAfrica (Smale, 1991; Ebert, 1994; Smale & Compagno, 1997). However,ontogenetic changes in diet could also simply reflect the ambient organismspresent. If H. regani scavenge fisheries offal, then more is likely to be availableinshore where juveniles are found, as the pelagic fleet works only over thecontinental shelf. By contrast, large H. regani, which are predominantly adultmales, inhabit deep water where crustaceans are likely to be more common thanare fish discards.
It is hypothesized that the increase in abundance of H. regani despite indirectfishing pressure is a consequence of its relatively high fecundity, the reducedeffort of the demersal fishery in areas of maximum density of H. regani, therelative protection of females and juveniles in inshore areas that are rarelytrawled, its opportunistic diet that includes offal and its robust nature. It isimperative that the general biology of other demersal by-catch species is alsoinvestigated, to ascertain whether they have traits similar to those of H. reganiwhich have allowed it to succeed. For example, if other demersal by-catchspecies have inshore nursery areas, then the most feasible conservation option forthese species will be marine protected areas located inshore (say <200 m depth).These may have little impact on the demersal fishery, as most of the trawling on
the west coast is currently in water deeper than 300 m, although the south coastfishery could be impacted. However, it is unlikely that the fecundity of mostdemersal chondrichthyans in the region is as high as that of H. regani (with thepossible exception of smaller species of skates) and they may not be activescavengers. In fact, H. regani may be doing well at the expense of other membersof the demersal community.
We thank the Zoology Department of the University of the Western Cape (UWC) andthe National Research Foundation for the provision of funds to AJR and GM; theNational Research Foundation for the support of research by LJVC; M. Lipinski andM. Smale for assistance in the identification of cephalopods; S. Daniels (UWC) for helpidentifying the crustaceans; and the officers and crew of the FRS Africana for help in thecollection of specimens.
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