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Age and growth of angler-fish (Lophius piscatorius L.) in the north Irish Sea
Fisheries Research, 7 (1989)267-278 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
267
Age and G r o w t h of Angler-Fish (Lophius piscatorius L.) in the North Irish Sea W.W. CROZIER
Department of Agriculture for Northern Ireland, Fisheries Research Laboratory, 38 Castleroe Road, Coleraine (Gt. Britain) (Accepted for publication 21 November 1988)
ABSTRACT Crozier, W.W., 1989. Age and growth of angler-fish (Lophius piscatorius L.) in the north Irish Sea. Fish. Res., 7: 267-278. Age analysis was carried out on 3739 angler-fish taken from the north Irish Sea between May 1983 and June 1985. A variety of ossified structures were examined, including fin rays, teeth, vertebrae and otoliths; the latter proving suitable for routine ageing. Validation of ageing was obtained from the observation of seasonal changes in otolith marginal growth, growth of young fish and following of an identified year class through the fishery. Derived growth rates agreed well with the temporal progression of length/frequency modes through time. Growth rates were calculated from length-at-age data and von Bertalanffy parameters fitted yielding the equation; L = 105.555 [ 1 - exp ( - 0.1759 ( t - 0.380 ) ) ]. Growth in weight and weight/length relationships were also examined. The complex growth patterns of the otoliths are discussed in relation to feeding behaviour and difficulties in interpretation outlined. The results obtained are compared with other studies of Lophiid growth.
INTRODUCTION
The angler fish, Lophius piscatorius L., forms a small but significant component of the by-catch of the Northern IrelandNephrops fishery (Briggs, 1985 ), some 270 t being landed annually at Northern Ireland ports, with a first sale value in excess of £250 000 (Anon., 1986). Around 1800 t of angler-fish are caught annually in the Irish Sea (ICES Division VIIa), total allowable catches being based on historical landings rather than on biological data. Research is currently being carried out into the population biology of L. piscatorius in the north Irish Sea in order to provide background information upon which future management of this fishery can be based. This includes aspects of feeding ecology (Crozier, 1985), population genetics (Crozier, 1987) and commercial exploitation. This paper presents preliminary data on ageing, growth and weight/ 0165-7836/89/$03.50
© 1989 Elsevier Science Publishers B.V.
268 length relationships of angler-fish in the north Irish Sea, and should be suitable for incorporation into multi-species modelling of the mixed demersal fishery. Previous studies of growth in L. piscatorius have been carried out on samples from the Mediterranean (Tsimenidis and Ondrias, 1980; Tsimenidis, 1984) and the Biscay/Celtic Sea areas (Guillou and Njock, 1978; Dupouy et al., 1986). Growth of this species in the Irish Sea has not previously been examined. MATERIALSAND METHODS Monthly samples ofL. piscatorius were taken from the traditional Nephrops fishing grounds in the north-eastern part of the Irish Sea from May 1983 to June 1985 inclusive. A total of 3739 fish was examined, ranging in length from 9.1 to 133.1 cm. Most samples were taken at 50-100-m depth by commercial Nephrops trawls of 60-mm nominal mesh at the cod end, though a single sample in June 1984 was collected during an inshore juvenile fish survey at depths of < 50 m. Commercially caught angler-fish are usually discarded at lengths below ~ 26 cm as they are unmarketable, thus samples for age and lengthfrequency analysis were taken from total rather than landed catches. Samples were either examined fresh after landing, or were deep frozen for later examination. At the laboratory, measurements were made of total length (cm) and eviscerated weight (to the nearest 0.1 g below 1.0 kg, to the nearest 5 g above 1.0 kg); sex was determined and maturity stage classified by macroscopic examination of the gonads (Nikolsky, 1963). Both sagittal otoliths were taken for age determination, blotted dry and stored in multi-well plastic containers. In early samples, vertebrae, teeth and fin ray samples were also taken for age investigations. Following convention, a birth date of 1 January was assumed in assigning an age group to a fish. The actual birth date for Irish Sea anglerfish probably lies around 1 June. Age determination in Lophiidae presents considerable difficulties, especially in older fish. Tsimenidis and Ondrias (1980) used whole otoliths to age L. piscatorius and L. budegassa, but reported considerable problems in interpreting the ring structure, as did Griffiths and Hecht (1986) in L. upsicephalus. Dupouy et al. ( 1986 ) favoured the illicium for a study of growth in L. piscatorius and L. budegassa. In the present investigation, several ossified structures were examined using a variety of techniques. These included acid etching, burning, staining with methyl violet or silver nitrate, sectioning in a number of planes and immersion in a variety of high refractive index media. Although fin rays were easy to embed and section (Dupouy et al., 1986), the ring structure was difficult to interpret as the rings differed in number depending on the distance of the section from the fin ray origin. In some cases, rings did not circumscribe the section and contrast was poor. Vertebrae were examined whole and sectioned,
269
Fig. 1. Dorso/ventral section of a sagittal otolith of L. piscatorius from the Irish sea, displaying three annual zones, each comprising a complex series of opaque and hyaline bands; fish total length = 50.8 cm.
yielding a complex array of concentric rings, but these proved difficult to in-. terpret in fish aged > 5 years, leading to overestimation of age relative to otolith ages. In the case of young fish, vertebral ring structure was more clearly identifiable. Vertebral ages agreed well with otolith-derived ages, an overall agreement of 90.6% being achieved in a trial comparison, despite the inclusion of some older fish. Teeth sections often displayed a clear ring structure if sec-tioned thinly enough to allow viewing by transmitted light. However, the number of rings discerned depended critically on the location of the section, proximal sections having more rings than distal sections, this leading to low agreement (32%) with otolith ages. Otoliths were finally chosen for routine ageing because they did not appear to have the limitations of interpretation present with the other structures examined. Although the examination of whole otoliths under high refractive index media yielded a clear ring pattern, it was difficult to resolve the nucleus region in older fish since the otolith thickens with increasing age (Tsimenidis, 1984). Accordingly, all otoliths were embedded in black-pigmented fibreglass resin and sectioned through the nucleus in the dorso-ventral plane using a lowspeed diamond saw (McCurdy, 1985). Resulting sections were mounted on
270
microscope slides in clear fibreglass resin and examined using transmitted and incident light. In general, the otolith growth pattern took the form of wide opaque zones between which occurred groups of much narrower opaque and hyaline bands (Fig. 1 ). This pattern of growth, similar to that reported for L. upsicephalus (Griffiths and Hecht, 1986), can be used to derive an age if it is assumed that each multi-banded zone separating the wide opaque zones represents a winter annulus. Interpretation of these zones is relatively easy in juvenile fish. However, in older fish, a decrease in growth rate leads to less well spaced rings and interpretation is very difficult in fish aged > 8-10 years. The age of these fish is possibly being underestimated. In ~ 1% of fish examined, the otoliths were crystalline and could not be aged.
Ageing validation In order to validate the otolith ages obtained in the present investigation, it was necessary to verify that the hyaline zones observed represent annulae and are consistent with the age of the fish. Several techniques of direct and indirect verification were tested. Marginal growth was examined microscopically in all otoliths aged during a 26-month continuous sampling period. Edge growth of 3357 otoliths was class-
60
°~
4Cp
P •
20
1983 M
J
J
A
S
1984 O
N
D
J
F
M
A
M
1985 J
J
A
S
O
N
D
J
F
M
A
M
J
Fig. 2. Percent of otoliths from Irish Sea angler-fish having opaque marginal growth during a 26month sampling period, 1983-1985.
271 58 56 54
52 5C 4E 46
~, 44
~- 40 E 38 36
li
34 32 0T
i J
i J
1i 9 8 3i A S
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[
i O
i N
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i A
i S
i O
i N
/[~
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i
i
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Fig. 3. Growth of the 1982 year class in the Irish Sea fishery. Points represent mean observed length at age for each month (vertical bars represent S.D.).
ified as opaque or hyaline, and the percentage having opaque growth was plotted against the month of capture (Fig. 2 ). A cycle of edge growth is evident in 1983, with the percentage of fish having opaque growth being highest during the summer period, then falling to a minimum during the winter months. The cycle was repeated in 1984 and the first half of 1985. If it is assumed, as for most temperate teleost species, that opaque growth represents the period of' active growth of the otolith (Panella, 1980), then the appearance of the complex hyaline zone on the margin in winter suggests that this zone represents a period of reduced or intermittent otolith growth and represents an annulus, as defined by Jearld (1984). The presence within the hyaline zone of multiple narrow opaque zones suggests that some intermittent growth does occur during winter. From Fig. 2, it can be seen that not all otoliths examined had hyaline growth during winter, a maximum of 18.2% having opaque growth in the winter of 1983/84. This probably results from a difference in the timing of annulus formation among fish of different ages, older fish having in some cases completed annulus formation by December/January. A further way of validating ageing is to follow the progress of a particular year class through the fishery. This method examines the increase in growth of a given aged group in succeeding years, i.e., Group I becomes Group II as the
272 28
25
o
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2o
15'
I S
i O Group
O
i N
1984 1 1 9 8 5 D
i J
I F
I M Group
f A
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i J
T
Fig. 4. Growth of Group 0 and Group I angler-fish in the Irish Sea, based on mean observed length at age (vertical bars represent S.D. ).
standardised birth date of I January is passed, and so on (Gordon, 1977; Macer, 1977). This was carried out for the 1982 year class of angler-fish in the present investigation (Fig. 3 ) which were examined as Group I in 1983, Group II in 1984 and Group III in 1985, respectively. The rate of growth of this year class matches growth increments observed between successive age groups present in the fishery at any one time (see Results). These results are confirmed by observations of the growth of young fish in the fishery, carried out for the progression from Group 0 to Group I of the 1984 year class (Fig. 4). No consistent seasonal slowing down of growth is evident in these data. Validation of the ageing technique was also obtained from a comparison of the growth of a particular age group with the observed progression of length/ frequency modes in the fishery over the same period (Campbell and Collins, 1975; Dupouy et al., 1986). This was carried out for the Group II angler-fish during 1984 (Fig. 5), where the observed mean length at age for each quarter is seen to match the progression of the length/frequency mode of Group II fish in the fishery. Similar observations have been used to validate Lophius ageing carried out by Tsimenidis and Ondrias (1980) and Dupouy et al. (1986).
265
Q2
,
254
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~3
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~6
~
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~
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~
~Tlooia~,ol,o.
length (cm'~
Fig. 5. Comparison of length/frequency distributions of angler-fish in the Irish Sea fishery for each quarter in 1984 with observed mean length of Group II fish, (arrowed). Sample sizes are given for each quarter.
274 RESULTS
Growth in length of L. piscatorius was examined by calculating von Bertalanffy parameters based on observed length-at-age data for Ages 1-6 inclusive. Older fish were excluded because their observed length at age varies considerably, possibly due to age assignment errors from otolith reading. The author has found that angler-fish 7 or 8 years old and above contribute little in numbers or biomass to the commercial fishery. Mean length-at-age data are given in Fig. 6, together with the fitted von Bertalanffy growth curve. Sexes were combined for this analysis as no significant difference was found in observed mean length at age in comparisons between the sexes (Age 1, t = 1.253, d.f. = 150, P > 0.2; Age 2, t--0.719, d.f. = 141, P>0.4; Age 3, t=0.597, d.f.=90, P > 0 . 5 ; Age 4, t=0.026, d.f.=20, P > 0 . 9 ) . The equation describing the growth curve is of the form
80 ~
70
60
~, so
40
30
2o
I I
3 age (years)
Fig. 6. Plot of observed mean length at age of Irish Sea angler-fish derived from otolith sections together with fitted von Bert~lanffy growth curve (vertical bars represent S.D.).
275 TABLE 1 Growth in weight of angler-fish in the north Irish Sea, from Ages 1 to 6, based on mean observed weight at age (n=420) Age (years)
Mean weight (g)
S.D.
1 2 3 4 5 6
158.2 661.8 1695.7 2203.0 3166.8 4934.2
111.441 229.478 535.852 642.788 527.174 945.169
Lt=L~ [1-exp(-k(t-to)
)]
where Lt is length at age t, L~ is asymptotic length (cm), k is the coefficient of growth and to the hypothetical time at which the fish would be zero length. For angler-fish, the curve best fitting the data is
L = 105.555 [1 - e x p ( - 0.1759 ( t - 0.380) ) ] The calculated L~ matches well the length of the oldest fish observed in the present investigation (typically 100-110 cm, exceptionally 133.1 cm). If Age 7 fish are included in the growth curve, L~ becomes 168.4 cm, though this cannot be considered as reliable as the original estimate. Growth in weight data are given in Table 1 for Lophius examined in the present investigation and are based on observed weights at age. Weight/length relationships were calculated separately for each sex. These were
W=O.O17771L 2"91s156 (males, n = 1 9 0 , r=0.988) W=O.O2144L 2"ss°1~3 (females, n = 2 3 5 , r=0.993) Covariance tests indicated that the slope fl of the weight/length regressions did not differ significantly between sexes (F= 3.698; d.f.= 1, 421; P > 0.05). Elevations (~) were not significantly different (F= 0.498; d.f. = 1,423; P > 0.4 ). Accordingly, a combined weight/length regression was calculated:
W = 0.019772L 2's95° (sexes combined, n = 425, r = 0.992 ) In both sexes, fl differed significantly from 3 (males, t=2.098, d.f.=188, P < 0.05; females, t= 2.913, d.f. = 233, P < 0.0001 ), indicating allometric growth. DISCUSSION
The growth patterns observed in otoliths of L. piscatorius examined in the present investigation indicate that a complex annulus is laid down each year.
276 Growth in this species seems to be a discontinuous irregular feature rather than a regular pattern of alternating slow and fast growth. Possible reasons for this have been identified by Griffiths and Hecht (1986), who described similar growth patterns in L. upsicephalus. They suggested that feeding periodicity was a major contributory factor overriding more regular temperature- or reproduction-related cycles of growth. Irregular feeding behaviour has been shown to affect otolith growth patterns (Bilton, 1974; Simkiss, 1974). It has been observed in L. piscatorius in aquaria (Bigelow and Schroeder, 1953; Field, 1966) and has been inferred from analysis of stomach fullness data from commercially caught angler-fish (Crozier, 1985). The growth pattern as described here for L. piscatorius makes age analysis more difficult than usual, especially in older fish where the multi-ring appearance of the annulus is compacted as annuli become progressively closer together. Thus, the author does not recommend that otoliths can be reliably used for the age analysis of angler-fish > 6 years old. The oldest fish observed in the present investigation was aged as 16 years old (133.1 cm), but this is likely to be an underestimate. Nevertheless, it has been demonstrated here that otolith ageing is valid for angler-fish ~<6 years old. The interpretation of growth patterns was supported by seasonal changes in otolith marginal growth, observations of rates of growth of young fish and by following the progression of an identified year class through the fishery. In addition, derived growth rates agreed 100
80
60 E
~ 40 E
20
I 1
I 2
I 3 age
I 4
i 5
i 6
[years)
Fig. 7. Comparisonof growthofL. piscatorius in the presentstudywith resultsfromother studies: O=Crozier (this study); O=Tsimenidis and Ondrias (1980); E]=Dupouy et al. {1986); • = GuiUouand Njock (1978). Verticalbars representS.D.
277 well with t h e p r o g r e s s i o n of l e n g t h / f r e q u e n c y m o d e s in the p o p u l a t i o n t h r o u g h a year. G r o w t h rates d e r i v e d h e r e can be c o m p a r e d with t h o s e for L. piscatorius o b t a i n e d b y o t h e r a u t h o r s (Fig. 7). G r o w t h r a t e s c a l c u l a t e d h e r e are lower t h a n those for L. piscatorius in t h e M e d i t e r r a n e a n ( T s i m e n i d i s a n d Ondrias, 1980 ), t h o u g h such a difference m i g h t be e x p e c t e d b e t w e e n samples f r o m e x t r e m e s of the range of a fish species. T h e g r o w t h rates derived f r o m fin ray ageing by D u p o u y et al. (1986) for Celtic Sea L. piscatorius are low c o m p a r e d with the p r e s e n t study. T h i s m i g h t reflect a t r u e difference in growth rate; however, fin ray ageing was c o n s i d e r e d u n r e l i a b l e in the p r e s e n t investigation. T h e growth curve o b t a i n e d b y Guillou a n d N j o c k (1978) suggests a very slow growth rate c o m p a r e d with o t h e r studies, with a n average i n c r e m e n t of only 5.2 cm being c a l c u l a t e d b e t w e e n Ages 1 a n d 8. T h e i r L ~ is u n r e a s o n a b l y high at 260 cm and suggests t h a t t h e i r use of whole u n s e c t i o n e d o t o l i t h s led t h e m to seriously und e r e s t i m a t e age. D u p o u y et al. (1986) c a l c u l a t e d L~, for L. piscatorius f r o m the Celtic Sea to range f r o m 117 to 167 cm. ACKNOWLEDGEMENTS I t h a n k Mr. M.L.R. M c K a y for assistance in o b t a i n i n g samples, a n d Drs. R.P. Briggs a n d D.J.A. Agnew for helpful c o m m e n t s on t h e m a n u s c r i p t . T h e p r o v i s i o n of a r e s e a r c h g r a n t b y t h e J e f f r e y s Association Ltd. is gratefully acknowledged.
REFERENCES Anonymous, 1986. Report on the sea and inland fisheries of Northern Ireland 1986. H.M.S.O., Belfast, 26 pp. Bigelow, H.B. and Schroeder, W.C., 1953. Fishes of the Gulf of Maine. Fish. Bull., Wash., No. 53, 577 pp. Bilton, A.T., 1974. Effects of starvation and feeding on circulus formation on scales of young sockeye salmon of four racial origins and of one race of young kokanee coho and chinook salmon. In: T.B. Bagenal (Editor), Proceedings of an International Symposium on the Ageing of Fish, July 1973, at Reading, U.K., Unwin, Old Woking, pp. 40-70. Briggs, R.P., 1985. Catch composition in the Northern Ireland Nephrops fishery. Fish. Res., 3: 47-60. Campbell, G. and Collins, R.A., 1975. The age and growth of the Pacific bonito Sarda chiliensis, in the eastern North Pacific. Calif. Fish Game, 61: 181-200. Crozier, W.W., 1985. Observations on the food and feeding of the angler-fish, Lophius piscatorius L., in the northern Irish Sea. J. Fish Biol., 27: 655-665. Crozier, W.W., 1987. Biochemical genetic variation and population structure in angler-fish Lophius piscatorius L., from the Irish Sea and west of Scotland. J. Exp. Mar. Biol. Ecol., 106: 125-136. Dupouy, H., Pajot, R. and Kergoat, B., 1986. ]~tude de la croissance des baudroies Lophius pis
278
catorius et L. budegassa, de L'Atlantic nord-est obtenue ~ partir de l'illicium. Rev. Trav. Inst. Peches Marit., 48: 107-131. Field, J.G., 1966. Contributions to the functional morphology of fishes. 2. The feeding mechanism of the angler fish, L. piscatorius Linnaeus. Zool. Aft., 2: 45-67. Gordon, J.D.M., 1977. The fish populations in inshore waters of the west of Scotland. The biology of the Norway pout (Trisopterus esmarkii). J. Fish Biol., 10: 417-430. Griffiths, M.H. and Hecht, T., 1986. A preliminary study of age and growth of the monkfish Lophius upsicephalus (Pisces: Lophiidae) on the Agulhas Bank, South Africa. S. Afr. J. Mar. Sci., 4: 51-60. GuiUou, A. and Njock, J.C., 1978. Analyse des structure de la p~che dans les ports de la c6te atlantic franqaise de 1961 ~ 1975 et des incidences due chalutage sur les stocks des principles esp~ces concern~es par cette activit$ dans les mers adjacentes. Rev. Trav. Inst. P~ches Marit., 42: 17164. Jearld, A., 1984. Age determination. In: L.A. Nielson and D.L. Johnston (Editors), Fisheries Techniques. American Fisheries Society, Maryland, pp. 301-324. Macer, C.T., 1977. Some aspects of the biology of the horse mackerel [Trachurus trachurus (L.) ] in waters around Britain. J. Fish Biol., 10: 51-62. McCurdy, W.J., 1985. A low speed alternative method for cutting otolith sections. J. Cons. Int. Expl., Mer, 42: 186-187. Nikolsky, G.V., 1963. The Ecology of Fishes. Academic Press, New York, 352 pp. Panella, G., 1980. Growth patterns in fish sagittae. In: D.C. Rhoads and R.A. Lutz (Editors), Skeletal Growth of Aquatic Organisms. Plenum, New York, pp. 519-560. Simkiss, K., 1974. Calcium metabolism of fish in relation to ageing. In: T.B. Bagenal (Editor), Proceedings of an Inernational Symposium on the Ageing of Fish, July 1973, at Reading, U.K., Unwin, Old Woking, pp. 1-12. Tsimenidis, N.C., 1984. The growth pattern of otoliths of Lophius piscatorius L., 1758 and Lophius budegassa Spinola, 1807 in the Aegean Sea. Cybium, 8: 35-42. Tsimenidis, N.C. and Ondrias, J.C., 1980. Growth studies on the angler fishes Lophiuspiscatorius L. 1758 and L. budegassa Spinola 1807 in Greek waters. Thalassographica, 3: 63-94.
267
Age and G r o w t h of Angler-Fish (Lophius piscatorius L.) in the North Irish Sea W.W. CROZIER
Department of Agriculture for Northern Ireland, Fisheries Research Laboratory, 38 Castleroe Road, Coleraine (Gt. Britain) (Accepted for publication 21 November 1988)
ABSTRACT Crozier, W.W., 1989. Age and growth of angler-fish (Lophius piscatorius L.) in the north Irish Sea. Fish. Res., 7: 267-278. Age analysis was carried out on 3739 angler-fish taken from the north Irish Sea between May 1983 and June 1985. A variety of ossified structures were examined, including fin rays, teeth, vertebrae and otoliths; the latter proving suitable for routine ageing. Validation of ageing was obtained from the observation of seasonal changes in otolith marginal growth, growth of young fish and following of an identified year class through the fishery. Derived growth rates agreed well with the temporal progression of length/frequency modes through time. Growth rates were calculated from length-at-age data and von Bertalanffy parameters fitted yielding the equation; L = 105.555 [ 1 - exp ( - 0.1759 ( t - 0.380 ) ) ]. Growth in weight and weight/length relationships were also examined. The complex growth patterns of the otoliths are discussed in relation to feeding behaviour and difficulties in interpretation outlined. The results obtained are compared with other studies of Lophiid growth.
INTRODUCTION
The angler fish, Lophius piscatorius L., forms a small but significant component of the by-catch of the Northern IrelandNephrops fishery (Briggs, 1985 ), some 270 t being landed annually at Northern Ireland ports, with a first sale value in excess of £250 000 (Anon., 1986). Around 1800 t of angler-fish are caught annually in the Irish Sea (ICES Division VIIa), total allowable catches being based on historical landings rather than on biological data. Research is currently being carried out into the population biology of L. piscatorius in the north Irish Sea in order to provide background information upon which future management of this fishery can be based. This includes aspects of feeding ecology (Crozier, 1985), population genetics (Crozier, 1987) and commercial exploitation. This paper presents preliminary data on ageing, growth and weight/ 0165-7836/89/$03.50
© 1989 Elsevier Science Publishers B.V.
268 length relationships of angler-fish in the north Irish Sea, and should be suitable for incorporation into multi-species modelling of the mixed demersal fishery. Previous studies of growth in L. piscatorius have been carried out on samples from the Mediterranean (Tsimenidis and Ondrias, 1980; Tsimenidis, 1984) and the Biscay/Celtic Sea areas (Guillou and Njock, 1978; Dupouy et al., 1986). Growth of this species in the Irish Sea has not previously been examined. MATERIALSAND METHODS Monthly samples ofL. piscatorius were taken from the traditional Nephrops fishing grounds in the north-eastern part of the Irish Sea from May 1983 to June 1985 inclusive. A total of 3739 fish was examined, ranging in length from 9.1 to 133.1 cm. Most samples were taken at 50-100-m depth by commercial Nephrops trawls of 60-mm nominal mesh at the cod end, though a single sample in June 1984 was collected during an inshore juvenile fish survey at depths of < 50 m. Commercially caught angler-fish are usually discarded at lengths below ~ 26 cm as they are unmarketable, thus samples for age and lengthfrequency analysis were taken from total rather than landed catches. Samples were either examined fresh after landing, or were deep frozen for later examination. At the laboratory, measurements were made of total length (cm) and eviscerated weight (to the nearest 0.1 g below 1.0 kg, to the nearest 5 g above 1.0 kg); sex was determined and maturity stage classified by macroscopic examination of the gonads (Nikolsky, 1963). Both sagittal otoliths were taken for age determination, blotted dry and stored in multi-well plastic containers. In early samples, vertebrae, teeth and fin ray samples were also taken for age investigations. Following convention, a birth date of 1 January was assumed in assigning an age group to a fish. The actual birth date for Irish Sea anglerfish probably lies around 1 June. Age determination in Lophiidae presents considerable difficulties, especially in older fish. Tsimenidis and Ondrias (1980) used whole otoliths to age L. piscatorius and L. budegassa, but reported considerable problems in interpreting the ring structure, as did Griffiths and Hecht (1986) in L. upsicephalus. Dupouy et al. ( 1986 ) favoured the illicium for a study of growth in L. piscatorius and L. budegassa. In the present investigation, several ossified structures were examined using a variety of techniques. These included acid etching, burning, staining with methyl violet or silver nitrate, sectioning in a number of planes and immersion in a variety of high refractive index media. Although fin rays were easy to embed and section (Dupouy et al., 1986), the ring structure was difficult to interpret as the rings differed in number depending on the distance of the section from the fin ray origin. In some cases, rings did not circumscribe the section and contrast was poor. Vertebrae were examined whole and sectioned,
269
Fig. 1. Dorso/ventral section of a sagittal otolith of L. piscatorius from the Irish sea, displaying three annual zones, each comprising a complex series of opaque and hyaline bands; fish total length = 50.8 cm.
yielding a complex array of concentric rings, but these proved difficult to in-. terpret in fish aged > 5 years, leading to overestimation of age relative to otolith ages. In the case of young fish, vertebral ring structure was more clearly identifiable. Vertebral ages agreed well with otolith-derived ages, an overall agreement of 90.6% being achieved in a trial comparison, despite the inclusion of some older fish. Teeth sections often displayed a clear ring structure if sec-tioned thinly enough to allow viewing by transmitted light. However, the number of rings discerned depended critically on the location of the section, proximal sections having more rings than distal sections, this leading to low agreement (32%) with otolith ages. Otoliths were finally chosen for routine ageing because they did not appear to have the limitations of interpretation present with the other structures examined. Although the examination of whole otoliths under high refractive index media yielded a clear ring pattern, it was difficult to resolve the nucleus region in older fish since the otolith thickens with increasing age (Tsimenidis, 1984). Accordingly, all otoliths were embedded in black-pigmented fibreglass resin and sectioned through the nucleus in the dorso-ventral plane using a lowspeed diamond saw (McCurdy, 1985). Resulting sections were mounted on
270
microscope slides in clear fibreglass resin and examined using transmitted and incident light. In general, the otolith growth pattern took the form of wide opaque zones between which occurred groups of much narrower opaque and hyaline bands (Fig. 1 ). This pattern of growth, similar to that reported for L. upsicephalus (Griffiths and Hecht, 1986), can be used to derive an age if it is assumed that each multi-banded zone separating the wide opaque zones represents a winter annulus. Interpretation of these zones is relatively easy in juvenile fish. However, in older fish, a decrease in growth rate leads to less well spaced rings and interpretation is very difficult in fish aged > 8-10 years. The age of these fish is possibly being underestimated. In ~ 1% of fish examined, the otoliths were crystalline and could not be aged.
Ageing validation In order to validate the otolith ages obtained in the present investigation, it was necessary to verify that the hyaline zones observed represent annulae and are consistent with the age of the fish. Several techniques of direct and indirect verification were tested. Marginal growth was examined microscopically in all otoliths aged during a 26-month continuous sampling period. Edge growth of 3357 otoliths was class-
60
°~
4Cp
P •
20
1983 M
J
J
A
S
1984 O
N
D
J
F
M
A
M
1985 J
J
A
S
O
N
D
J
F
M
A
M
J
Fig. 2. Percent of otoliths from Irish Sea angler-fish having opaque marginal growth during a 26month sampling period, 1983-1985.
271 58 56 54
52 5C 4E 46
~, 44
~- 40 E 38 36
li
34 32 0T
i J
i J
1i 9 8 3i A S
Group
[
i O
i N
D
i F
i M
I A
i M
19s4 ,
Group
J
J
II
i A
i S
i O
i N
/[~
I J
I F
19s~ M
Group
A
i
i
M
J
II[
Fig. 3. Growth of the 1982 year class in the Irish Sea fishery. Points represent mean observed length at age for each month (vertical bars represent S.D.).
ified as opaque or hyaline, and the percentage having opaque growth was plotted against the month of capture (Fig. 2 ). A cycle of edge growth is evident in 1983, with the percentage of fish having opaque growth being highest during the summer period, then falling to a minimum during the winter months. The cycle was repeated in 1984 and the first half of 1985. If it is assumed, as for most temperate teleost species, that opaque growth represents the period of' active growth of the otolith (Panella, 1980), then the appearance of the complex hyaline zone on the margin in winter suggests that this zone represents a period of reduced or intermittent otolith growth and represents an annulus, as defined by Jearld (1984). The presence within the hyaline zone of multiple narrow opaque zones suggests that some intermittent growth does occur during winter. From Fig. 2, it can be seen that not all otoliths examined had hyaline growth during winter, a maximum of 18.2% having opaque growth in the winter of 1983/84. This probably results from a difference in the timing of annulus formation among fish of different ages, older fish having in some cases completed annulus formation by December/January. A further way of validating ageing is to follow the progress of a particular year class through the fishery. This method examines the increase in growth of a given aged group in succeeding years, i.e., Group I becomes Group II as the
272 28
25
o
E
2o
15'
I S
i O Group
O
i N
1984 1 1 9 8 5 D
i J
I F
I M Group
f A
I M
i J
T
Fig. 4. Growth of Group 0 and Group I angler-fish in the Irish Sea, based on mean observed length at age (vertical bars represent S.D. ).
standardised birth date of I January is passed, and so on (Gordon, 1977; Macer, 1977). This was carried out for the 1982 year class of angler-fish in the present investigation (Fig. 3 ) which were examined as Group I in 1983, Group II in 1984 and Group III in 1985, respectively. The rate of growth of this year class matches growth increments observed between successive age groups present in the fishery at any one time (see Results). These results are confirmed by observations of the growth of young fish in the fishery, carried out for the progression from Group 0 to Group I of the 1984 year class (Fig. 4). No consistent seasonal slowing down of growth is evident in these data. Validation of the ageing technique was also obtained from a comparison of the growth of a particular age group with the observed progression of length/ frequency modes in the fishery over the same period (Campbell and Collins, 1975; Dupouy et al., 1986). This was carried out for the Group II angler-fish during 1984 (Fig. 5), where the observed mean length at age for each quarter is seen to match the progression of the length/frequency mode of Group II fish in the fishery. Similar observations have been used to validate Lophius ageing carried out by Tsimenidis and Ondrias (1980) and Dupouy et al. (1986).
265
Q2
,
254
m
~3
,o
Is
L
175
1
1,
iD u
m
i.
li
.4
~7 ,o
273
4,
a
..
la
u .
i,
...7
~o ~
~6
~
,2
~
..
I,
~
~Tlooia~,ol,o.
length (cm'~
Fig. 5. Comparison of length/frequency distributions of angler-fish in the Irish Sea fishery for each quarter in 1984 with observed mean length of Group II fish, (arrowed). Sample sizes are given for each quarter.
274 RESULTS
Growth in length of L. piscatorius was examined by calculating von Bertalanffy parameters based on observed length-at-age data for Ages 1-6 inclusive. Older fish were excluded because their observed length at age varies considerably, possibly due to age assignment errors from otolith reading. The author has found that angler-fish 7 or 8 years old and above contribute little in numbers or biomass to the commercial fishery. Mean length-at-age data are given in Fig. 6, together with the fitted von Bertalanffy growth curve. Sexes were combined for this analysis as no significant difference was found in observed mean length at age in comparisons between the sexes (Age 1, t = 1.253, d.f. = 150, P > 0.2; Age 2, t--0.719, d.f. = 141, P>0.4; Age 3, t=0.597, d.f.=90, P > 0 . 5 ; Age 4, t=0.026, d.f.=20, P > 0 . 9 ) . The equation describing the growth curve is of the form
80 ~
70
60
~, so
40
30
2o
I I
3 age (years)
Fig. 6. Plot of observed mean length at age of Irish Sea angler-fish derived from otolith sections together with fitted von Bert~lanffy growth curve (vertical bars represent S.D.).
275 TABLE 1 Growth in weight of angler-fish in the north Irish Sea, from Ages 1 to 6, based on mean observed weight at age (n=420) Age (years)
Mean weight (g)
S.D.
1 2 3 4 5 6
158.2 661.8 1695.7 2203.0 3166.8 4934.2
111.441 229.478 535.852 642.788 527.174 945.169
Lt=L~ [1-exp(-k(t-to)
)]
where Lt is length at age t, L~ is asymptotic length (cm), k is the coefficient of growth and to the hypothetical time at which the fish would be zero length. For angler-fish, the curve best fitting the data is
L = 105.555 [1 - e x p ( - 0.1759 ( t - 0.380) ) ] The calculated L~ matches well the length of the oldest fish observed in the present investigation (typically 100-110 cm, exceptionally 133.1 cm). If Age 7 fish are included in the growth curve, L~ becomes 168.4 cm, though this cannot be considered as reliable as the original estimate. Growth in weight data are given in Table 1 for Lophius examined in the present investigation and are based on observed weights at age. Weight/length relationships were calculated separately for each sex. These were
W=O.O17771L 2"91s156 (males, n = 1 9 0 , r=0.988) W=O.O2144L 2"ss°1~3 (females, n = 2 3 5 , r=0.993) Covariance tests indicated that the slope fl of the weight/length regressions did not differ significantly between sexes (F= 3.698; d.f.= 1, 421; P > 0.05). Elevations (~) were not significantly different (F= 0.498; d.f. = 1,423; P > 0.4 ). Accordingly, a combined weight/length regression was calculated:
W = 0.019772L 2's95° (sexes combined, n = 425, r = 0.992 ) In both sexes, fl differed significantly from 3 (males, t=2.098, d.f.=188, P < 0.05; females, t= 2.913, d.f. = 233, P < 0.0001 ), indicating allometric growth. DISCUSSION
The growth patterns observed in otoliths of L. piscatorius examined in the present investigation indicate that a complex annulus is laid down each year.
276 Growth in this species seems to be a discontinuous irregular feature rather than a regular pattern of alternating slow and fast growth. Possible reasons for this have been identified by Griffiths and Hecht (1986), who described similar growth patterns in L. upsicephalus. They suggested that feeding periodicity was a major contributory factor overriding more regular temperature- or reproduction-related cycles of growth. Irregular feeding behaviour has been shown to affect otolith growth patterns (Bilton, 1974; Simkiss, 1974). It has been observed in L. piscatorius in aquaria (Bigelow and Schroeder, 1953; Field, 1966) and has been inferred from analysis of stomach fullness data from commercially caught angler-fish (Crozier, 1985). The growth pattern as described here for L. piscatorius makes age analysis more difficult than usual, especially in older fish where the multi-ring appearance of the annulus is compacted as annuli become progressively closer together. Thus, the author does not recommend that otoliths can be reliably used for the age analysis of angler-fish > 6 years old. The oldest fish observed in the present investigation was aged as 16 years old (133.1 cm), but this is likely to be an underestimate. Nevertheless, it has been demonstrated here that otolith ageing is valid for angler-fish ~<6 years old. The interpretation of growth patterns was supported by seasonal changes in otolith marginal growth, observations of rates of growth of young fish and by following the progression of an identified year class through the fishery. In addition, derived growth rates agreed 100
80
60 E
~ 40 E
20
I 1
I 2
I 3 age
I 4
i 5
i 6
[years)
Fig. 7. Comparisonof growthofL. piscatorius in the presentstudywith resultsfromother studies: O=Crozier (this study); O=Tsimenidis and Ondrias (1980); E]=Dupouy et al. {1986); • = GuiUouand Njock (1978). Verticalbars representS.D.
277 well with t h e p r o g r e s s i o n of l e n g t h / f r e q u e n c y m o d e s in the p o p u l a t i o n t h r o u g h a year. G r o w t h rates d e r i v e d h e r e can be c o m p a r e d with t h o s e for L. piscatorius o b t a i n e d b y o t h e r a u t h o r s (Fig. 7). G r o w t h r a t e s c a l c u l a t e d h e r e are lower t h a n those for L. piscatorius in t h e M e d i t e r r a n e a n ( T s i m e n i d i s a n d Ondrias, 1980 ), t h o u g h such a difference m i g h t be e x p e c t e d b e t w e e n samples f r o m e x t r e m e s of the range of a fish species. T h e g r o w t h rates derived f r o m fin ray ageing by D u p o u y et al. (1986) for Celtic Sea L. piscatorius are low c o m p a r e d with the p r e s e n t study. T h i s m i g h t reflect a t r u e difference in growth rate; however, fin ray ageing was c o n s i d e r e d u n r e l i a b l e in the p r e s e n t investigation. T h e growth curve o b t a i n e d b y Guillou a n d N j o c k (1978) suggests a very slow growth rate c o m p a r e d with o t h e r studies, with a n average i n c r e m e n t of only 5.2 cm being c a l c u l a t e d b e t w e e n Ages 1 a n d 8. T h e i r L ~ is u n r e a s o n a b l y high at 260 cm and suggests t h a t t h e i r use of whole u n s e c t i o n e d o t o l i t h s led t h e m to seriously und e r e s t i m a t e age. D u p o u y et al. (1986) c a l c u l a t e d L~, for L. piscatorius f r o m the Celtic Sea to range f r o m 117 to 167 cm. ACKNOWLEDGEMENTS I t h a n k Mr. M.L.R. M c K a y for assistance in o b t a i n i n g samples, a n d Drs. R.P. Briggs a n d D.J.A. Agnew for helpful c o m m e n t s on t h e m a n u s c r i p t . T h e p r o v i s i o n of a r e s e a r c h g r a n t b y t h e J e f f r e y s Association Ltd. is gratefully acknowledged.
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278
catorius et L. budegassa, de L'Atlantic nord-est obtenue ~ partir de l'illicium. Rev. Trav. Inst. Peches Marit., 48: 107-131. Field, J.G., 1966. Contributions to the functional morphology of fishes. 2. The feeding mechanism of the angler fish, L. piscatorius Linnaeus. Zool. Aft., 2: 45-67. Gordon, J.D.M., 1977. The fish populations in inshore waters of the west of Scotland. The biology of the Norway pout (Trisopterus esmarkii). J. Fish Biol., 10: 417-430. Griffiths, M.H. and Hecht, T., 1986. A preliminary study of age and growth of the monkfish Lophius upsicephalus (Pisces: Lophiidae) on the Agulhas Bank, South Africa. S. Afr. J. Mar. Sci., 4: 51-60. GuiUou, A. and Njock, J.C., 1978. Analyse des structure de la p~che dans les ports de la c6te atlantic franqaise de 1961 ~ 1975 et des incidences due chalutage sur les stocks des principles esp~ces concern~es par cette activit$ dans les mers adjacentes. Rev. Trav. Inst. P~ches Marit., 42: 17164. Jearld, A., 1984. Age determination. In: L.A. Nielson and D.L. Johnston (Editors), Fisheries Techniques. American Fisheries Society, Maryland, pp. 301-324. Macer, C.T., 1977. Some aspects of the biology of the horse mackerel [Trachurus trachurus (L.) ] in waters around Britain. J. Fish Biol., 10: 51-62. McCurdy, W.J., 1985. A low speed alternative method for cutting otolith sections. J. Cons. Int. Expl., Mer, 42: 186-187. Nikolsky, G.V., 1963. The Ecology of Fishes. Academic Press, New York, 352 pp. Panella, G., 1980. Growth patterns in fish sagittae. In: D.C. Rhoads and R.A. Lutz (Editors), Skeletal Growth of Aquatic Organisms. Plenum, New York, pp. 519-560. Simkiss, K., 1974. Calcium metabolism of fish in relation to ageing. In: T.B. Bagenal (Editor), Proceedings of an Inernational Symposium on the Ageing of Fish, July 1973, at Reading, U.K., Unwin, Old Woking, pp. 1-12. Tsimenidis, N.C., 1984. The growth pattern of otoliths of Lophius piscatorius L., 1758 and Lophius budegassa Spinola, 1807 in the Aegean Sea. Cybium, 8: 35-42. Tsimenidis, N.C. and Ondrias, J.C., 1980. Growth studies on the angler fishes Lophiuspiscatorius L. 1758 and L. budegassa Spinola 1807 in Greek waters. Thalassographica, 3: 63-94.