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Three different hermaphroditic sexual patterns on the Balearic Islands shelf (north-western Mediterranean sea) Alexandre Alonso-Fernández 1 , Josep Alós 2 , Amalia Grau 3  ,Rosario Domínguez-Petit 1 , and Fran Saborido-Rey 1 1 Instituto de Investigaciones Marinas, IIM (CSIC). C/Eduardo Cabello, 6.  Vigo, Pontevedra, Spain. Corresponding author:  [email_address] 2 Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB). C/ Miquel Marqués 21, 07190, Esporles, Illes Balears, Spain 3 Direcció General de Pesca, Govern de les Illes Balears, C/ Foners 10, 07006, Palma, Spain. Institute of Marine Research (CSIC) Vigo, Spain Fisheries Ecology http://pesquerias.iim.csic.es
[object Object],Simultaneous hermaphrodite Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
Protandry ,[object Object],4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
[object Object],Protogyny 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
Rudimentary Hermaphroditism   (late gonochorism) juvenil bisexual phase functional gonochorist ,[object Object],4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
[object Object],[object Object],Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
In this study the three species selected to illustrate the coexistence of different hermaphroditic strategies in the same ecosystem were:  the rainbow wrasse,   Coris julis , the painted comber,  S erranus scriba  and the annular seabream,  Diplodus annularis . These three fishes are the main  recreational target species  in the Balearic Islands, NW Mediterranean, and they have been recently reported that are vulnerable to the impact of some recreational angling activities.   Coris julis S erranus scriba Diplodus annularis Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
The purpose of this study was to delineate  the  seasonal cycle  of sexual maturation,  timing and rhythm of spawning ,  ovarian development organization  and establish the  functional   sexual pattern  for each species under a  histological approach .   Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Introduction
[object Object],[object Object],Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Material and Methods
Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Material and Methods
[object Object],[object Object],[object Object],[object Object],Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Material and Methods
Coris julis  exhibit an  asynchronous ovarian development  organization.  This asynchrony was reflected also by the continuous oocyte size-frequency distribution.  There were several modes within the continuous oocyte size frequency distribution (several different batches of oocytes).   Theme session 1:  Female and male reproductive strategies Primary growth Cortical alveoli advanced-VIT early-VIT 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Study of ultrastructure of the testes showed  unrestricted spermatogonial testicular type .  Spermatogenesis  is  cystic  in this species.  Grier (1981) Theme session 1:  Female and male reproductive strategies Unrestricted Restricted 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Study of ultrastructure of the testes showed  unrestricted spermatogonial testicular type .  Spermatogenesis  is  cystic  in this species.  Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Intersexual  individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of  degenerating ovarian tissue .  Spermatogonial nest spreads  within the gonad. The highly prevalence of  eosinophils  in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Intersexual  individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of  degenerating ovarian tissue .  Spermatogonial nest spreads  within the gonad. The highly prevalence of  eosinophils  in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Intersexual  individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of  degenerating ovarian tissue .  Spermatogonial nest spreads  within the gonad. The highly prevalence of  eosinophils  in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Bimodal frequency distribution  by length and age is clear, with smaller and younger modal for females than secondary males. Primary males also were younger and smaller than secondary males. Modal size and age of intersexual individuals is located in the middle of size and age range distribution.   Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
“ […] In monandric species, all males are derived exclusively from functional females through sex change (i.e. secondary male). Diandric species undergo two male developmental pathways; some males differentiate directly from juveniles through sexual differentiation (i.e. primary male), while others are secondary, as in monandry.[…]” Liu and Sadovy (2004) primary secondary
Diandric protoginy  was identified for  Coris julis , estimation of length and age at sex change was conducted excluding primary males and intersexual individuals ( GLM, link function=binomial) .  Length-at-sex-change  and  age-at-sex-change  were 132 mm and 4 years respectively  Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Reproductive cycle was evaluated using monthly variation of mean estimated  GSI  values and monthly  maturity stage frequency . The seasonal variability in mean GSI values and the high proportion of females in actively spawning condition showed that the  spawning season  extends from late spring through early summer.   Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
In  Serranus scriba ,  gonads revelled that ovary and testis are present and mature at the same time,  enough evidence for  simultaneous   hermaphoditism  diagnosis.  Asynchronous  ovarian development organization was present and testes are characterized by  cystic   spermatogenesis and  unrestricted  spermatogonial testicular type.  Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June.  Attending to the proportion of mature stage the  spawning   season  extends from late spring through mid summer.  Theme session 1:  Female and male reproductive strategies Rivulus marmoratus Serranus tabacarius Serranus triginus 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June.  Attending to the proportion of mature stage the  spawning   season  extends from late spring through mid summer.  Theme session 1:  Female and male reproductive strategies Rivulus marmoratus 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June.  Attending to the proportion of mature stage the  spawning   season  extends from late spring through mid summer.  Theme session 1:  Female and male reproductive strategies Serranus tabacarius Serranus triginus 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Regarding ovarian development  Diplodus annularis   showed  asynchronous  organization and testes are of  unrestricted  spermatogonial testicular type and  cystic  spermatogenesis.   Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
When  ovotestis  were clearly identified only one of the tissues was functional,  no intersexual  individuals with degenerating tissue were found. Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
Although the sex ratio was slightly biased to females, except for smaller sizes, the  size and age frequency distribution  for both sex were basically the same like in gonochoristic species.  Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
May and June showed the highest reproductive activity during the year with a sharply decrease in July,  stating the spawning season in late spring-early summer. Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Results
[object Object],[object Object],[object Object],[object Object],Theme session 1:  Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes  16-19 June 2009 -  El Puerto de Santa María, Cádiz, Spain Conclusions
Thank You

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hermaphroditic_fish_species

  • 1. Three different hermaphroditic sexual patterns on the Balearic Islands shelf (north-western Mediterranean sea) Alexandre Alonso-Fernández 1 , Josep Alós 2 , Amalia Grau 3 ,Rosario Domínguez-Petit 1 , and Fran Saborido-Rey 1 1 Instituto de Investigaciones Marinas, IIM (CSIC). C/Eduardo Cabello, 6. Vigo, Pontevedra, Spain. Corresponding author: [email_address] 2 Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB). C/ Miquel Marqués 21, 07190, Esporles, Illes Balears, Spain 3 Direcció General de Pesca, Govern de les Illes Balears, C/ Foners 10, 07006, Palma, Spain. Institute of Marine Research (CSIC) Vigo, Spain Fisheries Ecology http://pesquerias.iim.csic.es
  • 2.
  • 3.
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  • 5.
  • 6.
  • 7. In this study the three species selected to illustrate the coexistence of different hermaphroditic strategies in the same ecosystem were: the rainbow wrasse, Coris julis , the painted comber, S erranus scriba and the annular seabream, Diplodus annularis . These three fishes are the main recreational target species in the Balearic Islands, NW Mediterranean, and they have been recently reported that are vulnerable to the impact of some recreational angling activities. Coris julis S erranus scriba Diplodus annularis Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Introduction
  • 8. The purpose of this study was to delineate the seasonal cycle of sexual maturation, timing and rhythm of spawning , ovarian development organization and establish the functional sexual pattern for each species under a histological approach . Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Introduction
  • 9.
  • 10. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Material and Methods
  • 11.
  • 12. Coris julis exhibit an asynchronous ovarian development organization. This asynchrony was reflected also by the continuous oocyte size-frequency distribution. There were several modes within the continuous oocyte size frequency distribution (several different batches of oocytes). Theme session 1: Female and male reproductive strategies Primary growth Cortical alveoli advanced-VIT early-VIT 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 13. Study of ultrastructure of the testes showed unrestricted spermatogonial testicular type . Spermatogenesis is cystic in this species. Grier (1981) Theme session 1: Female and male reproductive strategies Unrestricted Restricted 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 14. Study of ultrastructure of the testes showed unrestricted spermatogonial testicular type . Spermatogenesis is cystic in this species. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 15. Intersexual individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of degenerating ovarian tissue . Spermatogonial nest spreads within the gonad. The highly prevalence of eosinophils in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 16. Intersexual individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of degenerating ovarian tissue . Spermatogonial nest spreads within the gonad. The highly prevalence of eosinophils in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 17. Intersexual individuals were clearly identified after histological examination. The first evidence of sex-change was the presence of degenerating ovarian tissue . Spermatogonial nest spreads within the gonad. The highly prevalence of eosinophils in intersexual individuals could indicate a kind of association of this cells with sex-change process. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 18. Bimodal frequency distribution by length and age is clear, with smaller and younger modal for females than secondary males. Primary males also were younger and smaller than secondary males. Modal size and age of intersexual individuals is located in the middle of size and age range distribution. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 19. “ […] In monandric species, all males are derived exclusively from functional females through sex change (i.e. secondary male). Diandric species undergo two male developmental pathways; some males differentiate directly from juveniles through sexual differentiation (i.e. primary male), while others are secondary, as in monandry.[…]” Liu and Sadovy (2004) primary secondary
  • 20. Diandric protoginy was identified for Coris julis , estimation of length and age at sex change was conducted excluding primary males and intersexual individuals ( GLM, link function=binomial) . Length-at-sex-change and age-at-sex-change were 132 mm and 4 years respectively Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 21. Reproductive cycle was evaluated using monthly variation of mean estimated GSI values and monthly maturity stage frequency . The seasonal variability in mean GSI values and the high proportion of females in actively spawning condition showed that the spawning season extends from late spring through early summer. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 22. In Serranus scriba , gonads revelled that ovary and testis are present and mature at the same time, enough evidence for simultaneous hermaphoditism diagnosis. Asynchronous ovarian development organization was present and testes are characterized by cystic spermatogenesis and unrestricted spermatogonial testicular type. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 23. Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June. Attending to the proportion of mature stage the spawning season extends from late spring through mid summer. Theme session 1: Female and male reproductive strategies Rivulus marmoratus Serranus tabacarius Serranus triginus 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 24. Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June. Attending to the proportion of mature stage the spawning season extends from late spring through mid summer. Theme session 1: Female and male reproductive strategies Rivulus marmoratus 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 25. Monthly variation in GSI values clearly shown a peak of reproductive activity in May and June. Attending to the proportion of mature stage the spawning season extends from late spring through mid summer. Theme session 1: Female and male reproductive strategies Serranus tabacarius Serranus triginus 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 26. Regarding ovarian development Diplodus annularis showed asynchronous organization and testes are of unrestricted spermatogonial testicular type and cystic spermatogenesis. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 27. When ovotestis were clearly identified only one of the tissues was functional, no intersexual individuals with degenerating tissue were found. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 28. Although the sex ratio was slightly biased to females, except for smaller sizes, the size and age frequency distribution for both sex were basically the same like in gonochoristic species. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 29. May and June showed the highest reproductive activity during the year with a sharply decrease in July, stating the spawning season in late spring-early summer. Theme session 1: Female and male reproductive strategies 4th Workshop on Gonadal Histology of Fishes 16-19 June 2009 - El Puerto de Santa María, Cádiz, Spain Results
  • 30.