Journal of Fish Biology (2014) 84, 106–132 doi:10.1111/jfb.12258, available online at wileyonlinelibrary.com
Biology of the harlequin fish Othos dentex (Serranidae), with particular emphasis on sexual pattern and other reproductive characteristics B. French*, I. C. Potter*†, S. A. Hesp*‡, P. G. Coulson* and N. G. Hall*‡ *Centre for Fish and Fisheries Research, School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia and ‡Western Australian Fisheries and Marine Research Laboratories, 39 Northside Drive, Hillarys, WA 6025, Australia (Received 9 June 2013, Accepted 18 September 2013) Key biological characteristics of the harlequin fish Othos dentex , a representative of a monospecific genus of the Anthiinae (Serranidae), were determined from samples collected around reefs on the south coast of Western Australia. The females of this relatively long-lived species (maximum recorded age in this study = 37 years) attained only a slightly greater maximum total length and age than males and neither the length nor the age-frequency distributions showed a conspicuous sex-based bimodality. Furthermore, gonads from a wide size and age range of O. dentex were shown by histology, at several locations along their length, to always comprise exclusively either ovarian or testicular tissues. Thus, O. dentex is a gonochorist, a sexual pattern only previously recorded definitively for one other anthiine serranid, i.e. Epinephelides armatus, which also occurs in south-western Australia. Similar to E. armatus, O. dentex possesses ‘solid’ testes with a central sperm duct, thereby differing in structure from those typically found in serranids, in which there is a central membrane-bound ‘ovarian’ lumen and peripherally located sperm sinuses. The gonadal characteristics and sexual pattern of these two gonochoristic anthiines are not consistent with a recent proposal for the trends exhibited by the evolution of gonochorism and protogyny within the Serranidae. Othos dentex has indeterminate fecundity and a protracted spawning period (7 months) and, on the basis of underwater observations and a low gonado-somatic index (I G ) for males, is a pair spawner, which is unusual for a gonochorist of a serranid or member of a related family. While the large spots on the lower half of the body of O. dentex are shown quantitatively to be similarly yellow in juveniles and adult females, they then become blue in males at maturity and this intensifies during the spawning period, when they presumably play an important role in agonistic interactions among males and courtship with females. The attainment of maturity and rapid growth by O. dentex early in life may reflect selection pressures to reduce predation mortality during that period. Total mortality in the population is moderately low during later life, implying that the current fishing pressure on O. dentex is relatively light. © 2014 The Fisheries Society of the British Isles
Key words: Anthiine; gonadal characteristics; gonochorism; longevity; reproduction; sexual dichromatism.
†Author to whom correspondence should be addressed. Tel.: +61 08 9239 8801; email: i.potter@ murdoch.edu.au
106 © 2014 The Fisheries Society of the British Isles
BIOLOGY OF A GONOCHORISTIC ANTHIINE SERRANID
107
INTRODUCTION The Serranidae were traditionally regarded as comprising three subfamilies, i.e. the Anthiinae, Serraninae and Epinephalinae (Hoese et al., 2006; Nelson, 2006). More recently, however, a cladistic study by Smith & Craig (2007) demonstrated that this group is polyphyletic and the Epinephalinae was therefore separated into its own family, the Epinephalidae. The Serranidae sensu stricto, comprising the Serraninae and Anthiinae and commonly referred to as sea basses, basslets or hamlets, is a diverse teleost family that is widely distributed in tropical and temperate waters, where it typically lives around coral and rocky reefs (Hoese et al., 2006; Nelson, 2006). The Serraninae contains c. 13 genera and 75 species (Nelson, 2006) and the Anthiinae includes at least 21 genera and c. 170 species, with both of these subfamilies well represented in Australian waters (Allen et al., 2006; Hoese & Bray, 2006; Nelson, 2006). In terms of body size, the maximum lengths of serranid species sensu stricto range widely (Love et al., 1996; Dulˇci´c et al., 2007; Moore et al., 2007; Gomon et al., 2008). The majority of the ageing studies on serranids that have been based on validated ageing criteria, however, have typically yielded maximum ages of 0·05) and thus the data for these variables for the individuals of both sexes were pooled. The equation for the linear relationship between the ln of M and LT of both sexes combined is lnM = 3·125(lnLT ) − 11·954 (r 2 =0·98, mean square = 0·007, P < 0·05, n = 380). This relationship between the M and LT of intact fish was then used to estimate the mass of each O. dentex that had been filleted. The O. dentex that were sampled ranged from 183 to 605 mm in LT and their ages ranged from 2 to 37 years (Fig. 2). The females and males ranged in LT from 250 to 605 mm and 183 to 570 mm, and in age from 2 to 37 years and 3 to 31 years, respectively. The LT of the vast majority of both females (88%) and males (90%) was between 325 and 554 mm and those of both sexes produced an ill-defined modal LT class at 450–474 mm (Fig. 2). Both sexes were represented in each 5 year age class interval up to 30–34·9 years (Fig. 2). The r2 values for the von Bertalanffy growth curves fitted to the lengths at ages of females and males [Fig. 3(a), (b)] were relatively high (Table II). Although the curves for the two sexes were significantly different (P < 0·001), the difference between the predicted LT at age was II; ) gonads in sequential 25 mm total length (LT ) classes and sequential 2 year age classes. Logistic curves ( ) and their associated 95% c.l. ( ) were derived from the probability that a fish at a given LT or age is mature. Sample sizes are shown.
DISCUSSION S E X U A L PAT T E R N
The following results demonstrate that O. dentex is a gonochorist. (1) Lengthfrequency distributions for the females and males, which are based on data collected from many locations and different times of the year, exhibited no evidence of a marked overall bimodality that could be attributed to differences between the lengths of the two sexes. (2) As with length, the age-frequency distributions showed no underlying evidence of a sex-based bimodality. Indeed, apart from the oldest female, both sexes were represented in each age class, and the same two age classes, i.e.
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Table III. Estimates, and their associated 95% c.l., for the total lengths (LT ) and ages (A) at which 50 and 95% of the females and males of Othos dentex reach maturity, i.e. LT50 and LT95 , and A50 and A95
Female Estimate Lower Upper Male Estimate Lower Upper
LT50 (mm)
LT95 (mm)
A50 (years)
A95 (years)
345 333 357
412 391 433
6·3 5·2 7·1
9·7 8·3 11·2
356 341 369
408 388 428
6·3 5·0 7·3
9·6 6·5 11·3
5–9·9 and 10–14·9 years, were sequentially by far the most abundant in both sexes. (3) Histological examination of a large number of gonads from a wide length and age range of fish from different times of the year, representing individuals of both juveniles and adults and all stages in gonadal development, demonstrated that the gonads of each fish contained solely ovarian tissue or testicular tissue. Thus, while the smallest fish could not be obtained and thereby enable the characteristics of the gonads to be determined very early in life, the above findings satisfy the criteria of Sadovy & Shapiro (1987) for elucidating whether a species is an hermaphrodite or a gonochorist (Sadovy & Domeier, 2005; Sadovy de Mitcheson & Liu, 2008). The demonstration that O. dentex is a gonochorist parallels the finding of Moore et al. (2007) for E. armatus, another anthiine. While a third athiine, New Zealand orange perch Lepidoperca aurantia Roberts 1989, was recorded by Roberts (1989) as probably a gonochorist in his taxonomic review of a group of serranids in New Table IV. The total length at which 50% are mature (LT50 ) and maximum age (Amax ) determined for Othos dentex during this study, and estimates of the expected values for the life-history characteristics of O. dentex and their s.e. ranges, derived from the empirical relationships of Froese & Binohlan (2000) and Jari´c & Gaˇci´c (2012)
LT50 and Amax (this study) Females Males Females Males
345 mm 356 mm 37 years 31 years
LT50 from L∞ and Amax from A50 (Froese & Binohlan, 2000) Estimate
s.e. range
401 mm 303–531 mm 286 mm 204–402 mm 20·6 years 13·2–32·3 years 20·6 years 13·2–32·3 years Amax from A50 (Jari´c & Gaˇci´c, 2012) Estimate
Females Males
37 years 31 years
17·2 years 17·2 years
L∞ , asymptotic length; A50 , age at which 50% are mature.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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(a)
(b)
(c)
(d)
Fig. 8. Photographs showing variations in the colour of the large spots on the ventral body surface posterior to the pectoral fin of Othos dentex . (a) Immature female of 283 mm total length (LT ), (b) mature female of 438 mm LT , (c) immature male of 260 mm LT and (d) mature male of 480 mm LT .
Zealand, this view was not based on a demonstrated detailed analysis of a wide suite of biological characteristics and thus requires verification. The possible route taken by the evolution of gonochorism and protogyny in serranids has been considered by Sadovy & Domeier (2005) and Erisman & Hastings (2011), who drew on the pioneering work of several authors, including D’Ancona (1952), Smith (1965) and Reinboth (1970). Sadovy & Domeier (2005) stated that the central region of the testes of the adult serranids, including those of anthiines, 1·2 Colour ratio
1·0
1·2 15 10
1·1
11
17
19
20
0·8
13 August September October November December January February March
Colour ratio
0·7
0·8
0·6
Month
2
3 1
0·4
11
5
12
1·0 0·9
13 10
1
2
15 11
2 7
17
24 16
12
9
22
7
4
12
0·2 200
250
300
350 400 LT (mm)
450
500
550
Fig. 9. Mean ± s.e. ratio of blue to yellow colouring (colour ratio) of the spots on the lower half of the body and posterior to the pectoral fin of females ( ) and males ( ) in sequential 25 mm total length (LT ) classes of Othos dentex caught throughout the year. Sample sizes for the females and males of each class are shown above or below the mean values. Inset shows the mean monthly colour ratios during the spawning period. Monthly sample sizes are shown above the mean values.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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contains a central membrane-lined ‘ovarian’ lumen, which represents the retention of this structure from the gonads of its bisexual juvenile stage. The central location of this lumen accounts for the sperm sinuses being situated on the periphery of the testes of those species. This study has shown, however, that the central region of the testes of adults of the athiine O. dentex does not contain a membrane-bound ‘ovarian’ lumen and that this region is occupied instead by a conspicuous sperm duct. This arrangement parallels that recorded by Moore et al. (2007) for E. armatus from a different genus of the Anthiinae but found in the same geographical region as O. dentex . Furthermore, the gonads of all juveniles of O. dentex and E. armatus in the length and age ranges examined consisted exclusively of ovarian or testicular tissue and were thus not bisexual. While this contrasts with the situation in other gonochoristic serranids, such as Paralabrax species (Sadovy & Domeier, 2005), O. dentex and E. armatus might possess bisexual gonads very early in life, noting, however, that this was not the case even in individuals of the latter species whose LT was only 60 mm and whose gonads were very undeveloped (Moore et al., 2007). Thus, if bisexuality is present early in juvenile life, it disappears very early in gonadal development and long before the individuals of at least E. armatus reach maturity and some time before this is achieved in O. dentex . Sadovy & Domeier (2005) discussed the evolution of sexual patterns in serranids based on their possession of a non-functional bisexual phase in Paralabrax species, in which the male and female tissues are clearly separate. The phylogenetic relationships within the Serranidae, however, have since been modified and Paralabrax is no longer considered the ancestral genus (Smith & Craig, 2007). Recently, Erisman & Hastings (2011) superimposed the known sexual patterns of species of anthiines and serranines on a cladogram constructed using morphological and molecular data derived for those species. The trends on the cladogram imply that protogyny was the ancestral condition in the Serranidae sensu stricto and was retained by members of the Anthiinae at its base, with gonochorism subsequently being evolved by the serranid genus Paralabrax and followed by simultaneous hermaphroditism in other members of the Serranidae. A lack of requisite morphological and molecular data for E. armatus precluded the inclusion of this species by Erisman & Hastings (2011) in their cladistic analysis for the Serranidae. These authors were thus unable to apply the sexual pattern of E. armatus, and also that determined for O. dentex during this study, i.e. gonochorism, when using their cladogram to hypothesize the sequence of gonochorism and protogyny during the evolution of this family. Erisman & Hastings (2011) did note, however, that, as E. armatus and possibly L. pulchella were gonochorists, this sexual pattern had evolved at least once in the Anthinae. Furthermore, superimposition of sexual pattern on the species used by Erisman et al. (2009) for deriving a phylogenetic scheme for the Epinephelidae, a closely related family of the Serranidae, implies that gonochorism evolved on different occasions in this family. If the scheme of Erisman & Hastings (2011) for the evolution of sexual patterns in serranids is correct, O. dentex and E. armatus presumably represent an early offshoot or offshoots within the anthiines from ancestors in which protogyny had not yet evolved or they are derivatives of species that possessed the characteristics associated with protogynous hermaphroditism (as in other anthiines), but which then became lost. It thus follows that the collection of sound relevant morphological and molecular data for O. dentex and E. armatus, which could be incorporated with those
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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used by Erisman & Hastings (2011), would enable a more up-to-date cladogram to be constructed for the relationships among the species of Serranidae and thus be invaluable in refining views on the evolution of sexual patterns in this family. M A X I M U M L E N G T H , L O N G E V I T Y A N D G ROW T H
The maximum LT of 605 mm recorded for O. dentex caught on the south coast of Western Australia during this study was similar to the corresponding value of c. 600 mm LT recorded in a preliminary study in South Australia (Saunders et al., 2010). It is thus surprising that these maximum lengths were both far less than the 750 mm standard length (= c. 860 mm LT ) recorded by Gomon et al. (2008) for this species in their treatise on the fishes of Southern Australia. The maximum LT recorded for O. dentex in this study is still large for a species of serranid sensu stricto, with the above values of c. 600 mm being exceeded only by species such as barred sea bass Paralabrax nebulifer (Girard 1854), for which a maximum LT of 620 mm has been recorded (Love et al., 1996). The use of marginal increment analysis demonstrated that the number of opaque zones in the otoliths of O. dentex could be used to determine the ages of the individuals of this species. Thus, the maximum age of 42 years recorded for O. dentex in South Australian waters (Saunders et al., 2010), as well as the 37 years recorded in this study for populations on the south coast of Western Australia, demonstrate that this species is long-lived. These two similar values are the greatest yet recorded for a serranid sensu stricto, most of which are serranines (Table V). The maximum age for the Western Australian population of O. dentex provides another example of a reef-dwelling species from the south coast of this part of Australia having considerable longevity but it is not as great as the 68, 70 and 78 years recorded for S. aequipinnis, A. gouldii and B. frenchii , respectively, from that environment (Coulson et al., 2009, 2012; Cossington et al., 2010). Although small O. dentex , i.e.
Biology of the harlequin fish Othos dentex (Serranidae), with particular emphasis on sexual pattern and other reproductive characteristics B. French*, I. C. Potter*†, S. A. Hesp*‡, P. G. Coulson* and N. G. Hall*‡ *Centre for Fish and Fisheries Research, School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia and ‡Western Australian Fisheries and Marine Research Laboratories, 39 Northside Drive, Hillarys, WA 6025, Australia (Received 9 June 2013, Accepted 18 September 2013) Key biological characteristics of the harlequin fish Othos dentex , a representative of a monospecific genus of the Anthiinae (Serranidae), were determined from samples collected around reefs on the south coast of Western Australia. The females of this relatively long-lived species (maximum recorded age in this study = 37 years) attained only a slightly greater maximum total length and age than males and neither the length nor the age-frequency distributions showed a conspicuous sex-based bimodality. Furthermore, gonads from a wide size and age range of O. dentex were shown by histology, at several locations along their length, to always comprise exclusively either ovarian or testicular tissues. Thus, O. dentex is a gonochorist, a sexual pattern only previously recorded definitively for one other anthiine serranid, i.e. Epinephelides armatus, which also occurs in south-western Australia. Similar to E. armatus, O. dentex possesses ‘solid’ testes with a central sperm duct, thereby differing in structure from those typically found in serranids, in which there is a central membrane-bound ‘ovarian’ lumen and peripherally located sperm sinuses. The gonadal characteristics and sexual pattern of these two gonochoristic anthiines are not consistent with a recent proposal for the trends exhibited by the evolution of gonochorism and protogyny within the Serranidae. Othos dentex has indeterminate fecundity and a protracted spawning period (7 months) and, on the basis of underwater observations and a low gonado-somatic index (I G ) for males, is a pair spawner, which is unusual for a gonochorist of a serranid or member of a related family. While the large spots on the lower half of the body of O. dentex are shown quantitatively to be similarly yellow in juveniles and adult females, they then become blue in males at maturity and this intensifies during the spawning period, when they presumably play an important role in agonistic interactions among males and courtship with females. The attainment of maturity and rapid growth by O. dentex early in life may reflect selection pressures to reduce predation mortality during that period. Total mortality in the population is moderately low during later life, implying that the current fishing pressure on O. dentex is relatively light. © 2014 The Fisheries Society of the British Isles
Key words: Anthiine; gonadal characteristics; gonochorism; longevity; reproduction; sexual dichromatism.
†Author to whom correspondence should be addressed. Tel.: +61 08 9239 8801; email: i.potter@ murdoch.edu.au
106 © 2014 The Fisheries Society of the British Isles
BIOLOGY OF A GONOCHORISTIC ANTHIINE SERRANID
107
INTRODUCTION The Serranidae were traditionally regarded as comprising three subfamilies, i.e. the Anthiinae, Serraninae and Epinephalinae (Hoese et al., 2006; Nelson, 2006). More recently, however, a cladistic study by Smith & Craig (2007) demonstrated that this group is polyphyletic and the Epinephalinae was therefore separated into its own family, the Epinephalidae. The Serranidae sensu stricto, comprising the Serraninae and Anthiinae and commonly referred to as sea basses, basslets or hamlets, is a diverse teleost family that is widely distributed in tropical and temperate waters, where it typically lives around coral and rocky reefs (Hoese et al., 2006; Nelson, 2006). The Serraninae contains c. 13 genera and 75 species (Nelson, 2006) and the Anthiinae includes at least 21 genera and c. 170 species, with both of these subfamilies well represented in Australian waters (Allen et al., 2006; Hoese & Bray, 2006; Nelson, 2006). In terms of body size, the maximum lengths of serranid species sensu stricto range widely (Love et al., 1996; Dulˇci´c et al., 2007; Moore et al., 2007; Gomon et al., 2008). The majority of the ageing studies on serranids that have been based on validated ageing criteria, however, have typically yielded maximum ages of 0·05) and thus the data for these variables for the individuals of both sexes were pooled. The equation for the linear relationship between the ln of M and LT of both sexes combined is lnM = 3·125(lnLT ) − 11·954 (r 2 =0·98, mean square = 0·007, P < 0·05, n = 380). This relationship between the M and LT of intact fish was then used to estimate the mass of each O. dentex that had been filleted. The O. dentex that were sampled ranged from 183 to 605 mm in LT and their ages ranged from 2 to 37 years (Fig. 2). The females and males ranged in LT from 250 to 605 mm and 183 to 570 mm, and in age from 2 to 37 years and 3 to 31 years, respectively. The LT of the vast majority of both females (88%) and males (90%) was between 325 and 554 mm and those of both sexes produced an ill-defined modal LT class at 450–474 mm (Fig. 2). Both sexes were represented in each 5 year age class interval up to 30–34·9 years (Fig. 2). The r2 values for the von Bertalanffy growth curves fitted to the lengths at ages of females and males [Fig. 3(a), (b)] were relatively high (Table II). Although the curves for the two sexes were significantly different (P < 0·001), the difference between the predicted LT at age was II; ) gonads in sequential 25 mm total length (LT ) classes and sequential 2 year age classes. Logistic curves ( ) and their associated 95% c.l. ( ) were derived from the probability that a fish at a given LT or age is mature. Sample sizes are shown.
DISCUSSION S E X U A L PAT T E R N
The following results demonstrate that O. dentex is a gonochorist. (1) Lengthfrequency distributions for the females and males, which are based on data collected from many locations and different times of the year, exhibited no evidence of a marked overall bimodality that could be attributed to differences between the lengths of the two sexes. (2) As with length, the age-frequency distributions showed no underlying evidence of a sex-based bimodality. Indeed, apart from the oldest female, both sexes were represented in each age class, and the same two age classes, i.e.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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B. FRENCH ET AL.
Table III. Estimates, and their associated 95% c.l., for the total lengths (LT ) and ages (A) at which 50 and 95% of the females and males of Othos dentex reach maturity, i.e. LT50 and LT95 , and A50 and A95
Female Estimate Lower Upper Male Estimate Lower Upper
LT50 (mm)
LT95 (mm)
A50 (years)
A95 (years)
345 333 357
412 391 433
6·3 5·2 7·1
9·7 8·3 11·2
356 341 369
408 388 428
6·3 5·0 7·3
9·6 6·5 11·3
5–9·9 and 10–14·9 years, were sequentially by far the most abundant in both sexes. (3) Histological examination of a large number of gonads from a wide length and age range of fish from different times of the year, representing individuals of both juveniles and adults and all stages in gonadal development, demonstrated that the gonads of each fish contained solely ovarian tissue or testicular tissue. Thus, while the smallest fish could not be obtained and thereby enable the characteristics of the gonads to be determined very early in life, the above findings satisfy the criteria of Sadovy & Shapiro (1987) for elucidating whether a species is an hermaphrodite or a gonochorist (Sadovy & Domeier, 2005; Sadovy de Mitcheson & Liu, 2008). The demonstration that O. dentex is a gonochorist parallels the finding of Moore et al. (2007) for E. armatus, another anthiine. While a third athiine, New Zealand orange perch Lepidoperca aurantia Roberts 1989, was recorded by Roberts (1989) as probably a gonochorist in his taxonomic review of a group of serranids in New Table IV. The total length at which 50% are mature (LT50 ) and maximum age (Amax ) determined for Othos dentex during this study, and estimates of the expected values for the life-history characteristics of O. dentex and their s.e. ranges, derived from the empirical relationships of Froese & Binohlan (2000) and Jari´c & Gaˇci´c (2012)
LT50 and Amax (this study) Females Males Females Males
345 mm 356 mm 37 years 31 years
LT50 from L∞ and Amax from A50 (Froese & Binohlan, 2000) Estimate
s.e. range
401 mm 303–531 mm 286 mm 204–402 mm 20·6 years 13·2–32·3 years 20·6 years 13·2–32·3 years Amax from A50 (Jari´c & Gaˇci´c, 2012) Estimate
Females Males
37 years 31 years
17·2 years 17·2 years
L∞ , asymptotic length; A50 , age at which 50% are mature.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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BIOLOGY OF A GONOCHORISTIC ANTHIINE SERRANID
(a)
(b)
(c)
(d)
Fig. 8. Photographs showing variations in the colour of the large spots on the ventral body surface posterior to the pectoral fin of Othos dentex . (a) Immature female of 283 mm total length (LT ), (b) mature female of 438 mm LT , (c) immature male of 260 mm LT and (d) mature male of 480 mm LT .
Zealand, this view was not based on a demonstrated detailed analysis of a wide suite of biological characteristics and thus requires verification. The possible route taken by the evolution of gonochorism and protogyny in serranids has been considered by Sadovy & Domeier (2005) and Erisman & Hastings (2011), who drew on the pioneering work of several authors, including D’Ancona (1952), Smith (1965) and Reinboth (1970). Sadovy & Domeier (2005) stated that the central region of the testes of the adult serranids, including those of anthiines, 1·2 Colour ratio
1·0
1·2 15 10
1·1
11
17
19
20
0·8
13 August September October November December January February March
Colour ratio
0·7
0·8
0·6
Month
2
3 1
0·4
11
5
12
1·0 0·9
13 10
1
2
15 11
2 7
17
24 16
12
9
22
7
4
12
0·2 200
250
300
350 400 LT (mm)
450
500
550
Fig. 9. Mean ± s.e. ratio of blue to yellow colouring (colour ratio) of the spots on the lower half of the body and posterior to the pectoral fin of females ( ) and males ( ) in sequential 25 mm total length (LT ) classes of Othos dentex caught throughout the year. Sample sizes for the females and males of each class are shown above or below the mean values. Inset shows the mean monthly colour ratios during the spawning period. Monthly sample sizes are shown above the mean values.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
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B. FRENCH ET AL.
contains a central membrane-lined ‘ovarian’ lumen, which represents the retention of this structure from the gonads of its bisexual juvenile stage. The central location of this lumen accounts for the sperm sinuses being situated on the periphery of the testes of those species. This study has shown, however, that the central region of the testes of adults of the athiine O. dentex does not contain a membrane-bound ‘ovarian’ lumen and that this region is occupied instead by a conspicuous sperm duct. This arrangement parallels that recorded by Moore et al. (2007) for E. armatus from a different genus of the Anthiinae but found in the same geographical region as O. dentex . Furthermore, the gonads of all juveniles of O. dentex and E. armatus in the length and age ranges examined consisted exclusively of ovarian or testicular tissue and were thus not bisexual. While this contrasts with the situation in other gonochoristic serranids, such as Paralabrax species (Sadovy & Domeier, 2005), O. dentex and E. armatus might possess bisexual gonads very early in life, noting, however, that this was not the case even in individuals of the latter species whose LT was only 60 mm and whose gonads were very undeveloped (Moore et al., 2007). Thus, if bisexuality is present early in juvenile life, it disappears very early in gonadal development and long before the individuals of at least E. armatus reach maturity and some time before this is achieved in O. dentex . Sadovy & Domeier (2005) discussed the evolution of sexual patterns in serranids based on their possession of a non-functional bisexual phase in Paralabrax species, in which the male and female tissues are clearly separate. The phylogenetic relationships within the Serranidae, however, have since been modified and Paralabrax is no longer considered the ancestral genus (Smith & Craig, 2007). Recently, Erisman & Hastings (2011) superimposed the known sexual patterns of species of anthiines and serranines on a cladogram constructed using morphological and molecular data derived for those species. The trends on the cladogram imply that protogyny was the ancestral condition in the Serranidae sensu stricto and was retained by members of the Anthiinae at its base, with gonochorism subsequently being evolved by the serranid genus Paralabrax and followed by simultaneous hermaphroditism in other members of the Serranidae. A lack of requisite morphological and molecular data for E. armatus precluded the inclusion of this species by Erisman & Hastings (2011) in their cladistic analysis for the Serranidae. These authors were thus unable to apply the sexual pattern of E. armatus, and also that determined for O. dentex during this study, i.e. gonochorism, when using their cladogram to hypothesize the sequence of gonochorism and protogyny during the evolution of this family. Erisman & Hastings (2011) did note, however, that, as E. armatus and possibly L. pulchella were gonochorists, this sexual pattern had evolved at least once in the Anthinae. Furthermore, superimposition of sexual pattern on the species used by Erisman et al. (2009) for deriving a phylogenetic scheme for the Epinephelidae, a closely related family of the Serranidae, implies that gonochorism evolved on different occasions in this family. If the scheme of Erisman & Hastings (2011) for the evolution of sexual patterns in serranids is correct, O. dentex and E. armatus presumably represent an early offshoot or offshoots within the anthiines from ancestors in which protogyny had not yet evolved or they are derivatives of species that possessed the characteristics associated with protogynous hermaphroditism (as in other anthiines), but which then became lost. It thus follows that the collection of sound relevant morphological and molecular data for O. dentex and E. armatus, which could be incorporated with those
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 106–132
BIOLOGY OF A GONOCHORISTIC ANTHIINE SERRANID
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used by Erisman & Hastings (2011), would enable a more up-to-date cladogram to be constructed for the relationships among the species of Serranidae and thus be invaluable in refining views on the evolution of sexual patterns in this family. M A X I M U M L E N G T H , L O N G E V I T Y A N D G ROW T H
The maximum LT of 605 mm recorded for O. dentex caught on the south coast of Western Australia during this study was similar to the corresponding value of c. 600 mm LT recorded in a preliminary study in South Australia (Saunders et al., 2010). It is thus surprising that these maximum lengths were both far less than the 750 mm standard length (= c. 860 mm LT ) recorded by Gomon et al. (2008) for this species in their treatise on the fishes of Southern Australia. The maximum LT recorded for O. dentex in this study is still large for a species of serranid sensu stricto, with the above values of c. 600 mm being exceeded only by species such as barred sea bass Paralabrax nebulifer (Girard 1854), for which a maximum LT of 620 mm has been recorded (Love et al., 1996). The use of marginal increment analysis demonstrated that the number of opaque zones in the otoliths of O. dentex could be used to determine the ages of the individuals of this species. Thus, the maximum age of 42 years recorded for O. dentex in South Australian waters (Saunders et al., 2010), as well as the 37 years recorded in this study for populations on the south coast of Western Australia, demonstrate that this species is long-lived. These two similar values are the greatest yet recorded for a serranid sensu stricto, most of which are serranines (Table V). The maximum age for the Western Australian population of O. dentex provides another example of a reef-dwelling species from the south coast of this part of Australia having considerable longevity but it is not as great as the 68, 70 and 78 years recorded for S. aequipinnis, A. gouldii and B. frenchii , respectively, from that environment (Coulson et al., 2009, 2012; Cossington et al., 2010). Although small O. dentex , i.e.
