JARB Journal of Animal Reproduction and Biotehnology

OPEN ACCESS pISSN: 2671-4639
eISSN: 2671-4663

Article Search

Original Article

Article Original Article
Split Viewer

Journal of Animal Reproduction and Biotechnology 2024; 39(1): 31-39

Published online March 31, 2024

https://doi.org/10.12750/JARB.39.1.31

Copyright © The Korean Society of Animal Reproduction and Biotechnology.

Reproductive biology of 58 fish species around La Réunion Island (Western Indian Ocean): first sexual maturity and spawning period

Kélig Mahé1,* , Julien Taconet1,2, Blandine Brisset2, Claire Gentil2, Yoann Aumond2, Hugues Evano2, Louis Wambergue2, Romain Elleboode1, Tévamie Rungassamie3 and David Roos2

1Unité HMMN, IFREMER, Laboratory of Fisheries, Boulogne-sur-Mer 62321, France
2Délégation Océan Indien, IFREMER Institute, La Réunion 97822, France
3Réserve Naturelle Marine de La Réunion, La Réunion 97822, France

Correspondence to: Kélig Mahé
E-mail: kelig.mahe@ifremer.fr

Received: January 19, 2024; Revised: February 14, 2024; Accepted: February 21, 2024

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background: The biological information of fish, which include reproduction, is the prerequisite and the basis for the assessment of fisheries.
Methods: The aim of this work was to know the reproductive biology with the first sexual maturity (TL50) and the spawning period for 58 mainly fish species in the waters around La Réunion Island (Western Indian Ocean). Twenty families belonging to the Actinopterygii were represented (acanthuridae, berycidae, bramidae, carangidae, cirrhitidae, gempylidae, holocentridae, kyphosidae, labridae, lethrinidae, lutjanidae, malacanthidae, monacanthidae, mullidae, polymixiidae, pomacentridae, scaridae, scorpaenidae, serranidae, sparidae; 56 species; n = 9,751) and two families belonging to the Elasmobranchii (squalidae, centrophoridae; 2 species; n = 781) were sampled. Between 2014 and 2022, 10,532 individuals were sampled covering the maximum months number to follow the reproduction periods of these species.
Results: TL50 for the males and the females, respectively, ranged from 103.9 cm (Acanthurus triostegus) to 1,119.3 cm (Thyrsitoides marleyi) and from 111.7 cm (A. triostegus) to 613.1 cm (Centrophorus moluccensis). The reproduction period could be very different between the species from the very tight peak to a large peak covered all months.
Conclusions: Most species breed between October and March but it was not the trend for all species around La Réunion Island.

Keywords: gonad observation, reproduction period, reproductive maturity stages, size at the first sexual maturity

The biological parameters (i.e. growth and reproduction) are essentially to management the fish population (Jakobsen et al., 2009). Fish reproductive biology is the necessary step to evaluate the reference points as spawning stock biomass and the maturity ogive, which are integrated in the stock assessment models (Jakobsen et al., 2009). The lack or scarcity of these biological information, can lead to over-exploitation of fisheries resources. The main commercial demersal tropical fishes, along with snappers (Lutjanidae), groupers (Serranidae), emperors (Lethrinidae), carangids (Carangidae), soldierfishes (Holocentridae) and goatfishes (Mullidae) support locally important artisanal fisheries throughout the Indo-Pacific region, but quantitative assessments of these species have been limited by a lack of adequate biological and fisheries data (Newman et al., 2016; Halim et al., 2020), including around La Réunion Island (Le Manach et al., 2015). Among 123 fish species followed around La Réunion Island (Roos et al., 2022), The main objective of this study was to provide the reproductive biology information with the first sexual maturity and the spawning period for 58 mainly fish species required for the management of fisheries resources.

Sampling

All fish sampled during scientific surveys, and some specimen were added from commercial landings to complete the length range or the months without surveys. During eight years (i.e. between 2014 and 2022), 10,532 individuals of 58 species were sampled. Twenty families belonging to the Actinopterygii were represented (acanthuridae, berycidae, bramidae, carangidae, cirrhitidae, gempylidae, holocentridae, kyphosidae, labridae, lethrinidae, lutjanidae, malacanthidae, monacanthidae, mullidae, polymixiidae, pomacentridae, scaridae, scorpaenidae, serranidae, sparidae; 56 species; n = 9,751) and two families belonging to the Elasmobranchii (squalidae, centrophoridae; 2 species; n = 781) were sampled (Table 1). All individuals were taken to the laboratory for accurate measurements. Each individual was measured to the nearest mm for total length (TL) and weighted to the grams for Total Weight (W). The gonads were observed macroscopically to determine the sex and this associated sexual maturity stage.

Table 1 . Sampling details (number and length by sex: males, M; females, F and immatures, I) with the first sexual maturity (TL50; p-value < 0.05 showed the significant sexual dimorphism) for 58 species around La Réunion Island (*protogynous hermaphroditism species)

FamilleLatin mameNumberLength of adults (F+M)Length of MalesLength of FemalesTL50
TotalMalesFemalesImmaturesMeanSDRange
(min-max)
MeanSDRange
(min-max)
MeanSDRange
(min-max)
MalesFemalesAdultes
(F+M)
p-value
AcanthuridaeAcanthurus triostegus542214225103152.021.334-199154.618.099-199150.716.495-192103.91111.68108.300.21
Naso elegans6340185322.786.6167-469336.177.3208-459266.186.0167-426214.39204.65
Naso unicornis176986711299.694.9157-557322.893.4167-557266.591.8157-532247.76209.43231.65< 0.05
BerycidaeBeryx decadactylus4920272503.167.6350-610458.957.2350-550528.958.9388-610
BramidaeEumegistus illustris2369612713680.6135.1452-1,000661.3126.0470-910692.8142.2452-1,000628.56521.05575.550.09
CarangidaeCaranx melampygus6545200609.196.0433-838621.1100.2467-838582.081.9433-710
Decapterus tabl63232911266.926.0193-326267.023.7233-313264.629.9193-326215.05215.06
CentrophoridaeCentrophorus moluccensis6931380589.1309.00-876644.5182.60-741543.9379.20-876548.51613.07556.26< 0.05
CirrhitidaeCirrhitus pinnulatus6942243189.522.1140-252196.818.0168-252177.323.5140-223
GempylidaePromethichthys prometheus8628535381.177.0216-564356.068.3263-490401.873.4282-564386.05356.92361.93< 0.05
Rexea prometheoides135161154298.650.80-425257.421.1222-320306.743.00-425
Thyrsitoides marleyi3692431,092.4463.0222-1,8901,009.8342.0410-1,2801,223.3426.0320-1,8901,119.30
HolocentridaeMyripristis berndti12260557233.343.4126-308239.842.2126-308229.942.4127-292129.96
Myripristis chryseres8748372206.120.2150-255215.918.1182-255194.815.5150-215155.99159.95
Myripristis murdjan7323464200.529.5145-255198.225.1145-234205.430.0146-255
Ostichthys kaianus4016213283.243.7165-360291.043.4188-360282.838.4184-344
Sargocentron spiniferum3813223268.252.1181-371275.850.0220-361268.454.3196-371210.31212.85
KyphosidaeKyphosus bigibbus2714121317.427.6244-365326.116.9296-353308.735.4244-365289.89287.68
Kyphosus cinerascens3219130327.663.0205-470305.848.7205-360359.369.7271-470241.23240.18
Kyphosus vaigiensis251771306.749.4203-395292.948.9203-395347.023.5304-375
LabridaeCheilinus trilobatus79135610314.176.9184-477355.573.9184-473305.177.0200-477
LethrinidaeGnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Lethrinus rubrioperculatus*12536872339.666.5192-464401.117.5354-433315.161.7194-464208.62208.62
LutjanidaeAphareus rutilans16290648429.891.4211-786429.592.5211-786434.492.6319-769353.70381.76368.81< 0.05
Aprion virescens6540241443.1123.2212-893427.3106.2288-670477.5137.2323-893324.04320.30
Etelis carbunculus1,70088177742277.170.9139-1,250270.659.3164-980286.781.4153-1,250183.95183.46188.180.87
Etelis coruscans193859810455.6249.2206-1,155450.6240.2206-1,068480.0268.1220-1,155391.99394.25397.490.83
Lutjanus bengalensis256190177.219.3147-217166.514.3147-189180.619.7152-217
Lutjanus kasmira75336037320219.634.9110-336230.137.1150-336211.228.9110-281180.22147.11161.29< 0.05
Lutjanus notatus3972011951215.222.8143-277224.322.3155-277206.219.0143-247
Pristipomoides argyrogrammicus64731731713232.231.8122-317239.431.3162-316226.829.6140-317148.06149.34
Pristipomoides filamentosus3009817131262.851.1155-576273.361.1157-576264.442.3165-383326.90310.35317.370.18
Pristipomoides multidens2701401291501.8128.3270-865514.9132.0282-865487.6123.0270-815388.63346.15369.62< 0.05
MalacanthidaeBranchiostegus doliatus3316152342.742.9247-422356.136.2303-422326.748.0247-410
MonacanthidaeCantherhines dumerilii5625256279.935.2185-355274.427.6185-312292.838.5233-355240.00219.39
MullidaeMulloidichthys flavolineatus4214545331137.964.285-415197.179.495-319242.586.597-415185.17204.51207.040.37
Mulloidichthys pfluegeri5826311332.558.4193-452339.050.4215-429328.765.1193-452259.33240.43247.930.61
Parupeneus trifasciatus2699811358226.155.679-401255.761.7141-401213.137.3129-352218.90199.22212.920.63
PolymixiidaePolymixia berndti7217469230.463.8151-430248.289.2151-430226.057.7160-429
Polydactylus sexfilis107492533309.3148.870-519379.630.5311-457440.835.5366-519256.55
PomacentridaeAbudefduf septemfasciatus272061206.211.3180-227203.911.8180-227213.86.4207-224
ScaridaeCalotomus carolinus6726392354.555.3186-456384.055.4202-456334.047.4186-403245.72240.00240.000.81
Chlorurus enneacanthus16872879321.484.1175-765333.189.5175-765312.180.8182-560209.58200.53
Scarus psittacus11768445278.647.4121-364300.235.3198-364248.738.4137-326164.74154.02
ScorpaenidaePontinus nigerimum37121510275.651.8161-380311.328.6273-370241.947.1161-298
SerranidaeCephalopholis aurantia*2225415513228.535.8136-318259.925.2219-318220.432.3136-313160.39160.39
Cephalopholis nigripinnis*3110201167.427.4119-230178.823.3145-209162.128.8119-230
Cephalopholis spiloparaea*4720270170.024.9129-236176.825.3134-236165.023.9129-230
Epinephelus fasciatus*301332644230.754.2100-421273.966.3164-421225.850.1100-353130.28130.28
Epinephelus hexagonatus*3146320744166.027.9112-241181.125.2127-233158.828.0112-241
Epinephelus merra*1341610711181.129.0120-254188.128.2149-230180.329.9120-254166.20166.20
Epinephelus radiatus*1149996364.2108.1123-653392.795.8280-562368.3106.7187-653317.71317.71
Epinephelus tauvina*72223812267.767.7158-518256.970.5187-518285.265.1158-450268.72268.72
Gnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Variola albimarginata*152451061358.678.7185-555428.062.3257-555330.365.4185-494236.26236.26
Variola louti*7124470580.1136.7216-840649.3145.8392-840544.7118.4216-741363.01363.01
SparidaeArgyrops filamentosus6134225239.621.7195-290244.222.6198-290239.615.9214-270
SqualidaeSqualus megalops71230239713512.0190.20-820460.2187.60-683559.8171.40-820397.67500.00454.63< 0.05


First sexual maturity

Sex ratios as the percentage of females (F) in the samples, were calculated. The first sexual maturity, to separate juveniles and sexually mature individuals thus defining the spawning biomass (i.e. reference point for exploited marine fishes) (Thorson et al., 2012), was measured from TL50. This biological parameter was the total length at which 50% of individuals are mature for the first time.

Where m(l) is the proportion of mature individuals in

m(l)=exp(exp(a+b*l))
TL50=ln(ln(0.5))ab

each length class (%), a is intercept, b is slope, l is the fish total length (cm) and TL50 is the mean total length at sexual maturity (50%, cm), were used. Among the Actinopterygii, two families (serranidae and lethrinidae, 13 species; Table 1) showed the protogynous hermaphrodites (i.e. change sex from female to male). For these species, first sexual maturity was only estimated for females.

Reproduction period

Fish were assigned to the following maturity development stages as recommended at the international level (ICES, 2018): from (I) immature; (II) resting; (III) ripe and running; (IV) spent; to (V) post-spent. From the percentage of individuals per month and per maturity stages throughout the year, the reproduction period and intensity were identified. The adults are the sum of all fish of maturity stages III, IV and V.

Statistical analysis

Statistical analyses to identify the significant sex effect on the first sexual maturity (with significant effect at p < 0.05) were carried out from the CAR package (Fox and Weisberg, 2011). This sexual dimorphism was tested on all fish species without two protogynous hermaphrodites families. The figures were carried out from the ggplot2 (Wickham, 2016) and plyr (Wickham, 2011) packages in the R statistical environment (R Core Team, 2023).

Ethical statement

All species were sampled from scientific surveys or caught for the commercial landings. They are not in the IUCN red list as critically endangered, endangered or vulnerable species.

Among 10,532 individuals, there were 4,271 males, 5,346 females and 915 immatures. Summarised information for each species, by each sex or both males and females, is presented in Table 1 and Supplementary Table 1. Among 23 families, two were represented by a relatively high number of species, such as the Serranidae (11 species) and Lutjanidae (10 species). In the sameway, these two families showed the large number of individuals with 4,512 belonging to the Lutjanidae and 1,518 belonging to the Serranidae. According to the selected species, the distribution between the two sexes and the immatures can be very different. While the reproduction of protogynous hermaphrodites (i.e. for two families: serranidae and lethrinidae represented by 13 species) explained why males could be larger than females, for other species, there was no generalizable observable trend between males and females and it depends on the analysed species.

Among 58 analysed species, the mean total length of the first sexual maturity (TL50) could be modelled from individual in situ data for 40 species (Table 1). TL50 for the males and the females, respectively, ranged from 103.9 cm (Acanthurus triostegus) to 1,119.3 cm (Thyrsitoides marleyi) and from 111.7 cm (A. triostegus) to 613.1 cm (Centrophorus moluccensis) (Table 1). For ten hermaphrodites’ species, only TL50 for females was modelled. For 30 other species presenting the TL50 fitted on the data, this biological parameter was measured for the males and for the females for 16 species. Among these species, 10 a higher TL50 for females than for males and only 6 have the opposite trend. The significant different of TL50 between the males and the females were observed for 7 species among 16 species (Table 1).

For all 58 species, the reproduction period and intensity were analysed for each species including all adults’ individuals (Fig. 1) and by each sex (females Supplementary Fig. 1 and males Supplementary Fig. 2). There were three species including the two Elasmobranchii species (Squalus megalops and Centrophorus moluccesis) and one species of the mullidae family (Mulloidichthys flavolineatus) showed that the reproduction peak (i.e. high spawning period; Fig. 1) covered all months. Conversely, other species presented the reproduction peak very tightly spread over 3 months (Thyrsitoides marleyi; Kyphosus bigibbus; Aphareus rutilans; Pristipomoides filamentosus; Polymixia berndti; Cephalopholis nigripinnis; Epinephelus hexagonatus). However, for the species with the restricted reproduction period, most species breed between October and March but it was not the trend for all species. The reproduction activity may be concentrated in the winter months for a limited number of species as Argyrops filamentosus, Pristipomoides filamentosus, Kyphosus vaigiensis and Kyphosus bigibbus (Fig. 1).

Figure 1. Reproduction period and intensity (percentage of individuals actively breeding: No spawning: 0-25%; Low spawning: 25-50%; Medium spawning: 50-75%; High spawning: 75-100%) of species around La Réunion Island (*month without sampled individuals).

Reproductive process through the sexual maturity and the peak of reproduction are important elements prerequisite to realize the stock assessment with a good precision (Chen et al., 2022). However, for many fish species, the females and males and their maturity stage cannot be distinguished by only external characteristics. Consequently, for many cases of study, this information is lack, very old or partial. Moreover, for tropical species as around La Réunion Island, there may be conservation problems due to the high temperature after fishing which result in difficulties in observation internal organs such as the gonads. Consequently, this type of study aggregating reproductive information from organ observations in the laboratory for a very large number of species is necessary to provide reference points for each species, which can be used in fisheries resource monitoring as is done for other biological parameters such as the length-weight relationship (Roos et al., 2022).

Firstly, the length of the first sexual maturity (TL50) was measured for each species. Among fish species, there are two mainly sexual characteristics: hermaphrodites versus dioecious species. For the protogynous hermaphrodites, concerning two families (serranidae and lethrinidae, 13 species), the first sexual maturity of females is earlier than the sex change and consequently the length is not the same (Frisch et al., 2016). For the dioecious species, there are no clearly patterns between the TL50 for females and males. Some species show comparable TL50 between males and females, others show marked differences in favor of females or males. These differences between sexes within the same population or between several population in the length at the sexual maturity, can be caused by phenotypic changes, genetic adaptations or the interaction of both (Law, 2000; Trindade-Santos and Freire, 2015). TL50 is influenced by environmental conditions (Weatherley, 1990), but human activities could be the potential factors (i.e. fishing, pollution…). For example, a negative relationship between the length at sexual maturity and the level of fishing pressure was observed (ICES, 2012; Marty et al., 2014).

Secondly, the timing and intensity of the spawning were estimated for each species. For this reproductive trait, there are mainly difference among species with some species with a very large reproduction peak covered all months and conversely, others with very tight reproduction peak over 3 months. These results corroborate the same approach applied in the Mediterranean Sea (Tsikliras et al., 2010). Some species that breed strongly throughout the year may show two sexual strategies with some individuals breeding once a year and others at least twice (Bye, 1984; Cushing, 1990). The duration and the period of the year of the reproduction peak varies between the species and between the populations within the same species. The spawning season begin when the fish receive the environmental stimuli (Hoar, 1969; Liley, 1969). Lunar periodicity seems to be the influential external stimulus on reproductive characteristics of tropical coastal fish species (Harrison et al., 1984; Thresher, 1984). Another important factor to trigger the reproduction could be internal with the hormonal cascades leading to maturation and spawning and the gill surface area (Pankhurst, 2016; Pauly, 2019; Pauly, 2022). Finally, the reproduction biology could linked to the age class of the specimen with the ontogenic effect (Rijnsdorp, 1989; Trippel et al., 1997).

The reproductive biology information with the first sexual maturity and the spawning period were analyzed for 58 mainly fish species around the La Réunion Island in the Indian Ocean. For many species, these biological data were not available or were very old. The first sexual maturity length is essential to evaluate the reference point named the spawning stock biomass (SSB) (Thorson et al., 2012) used in the stock assessment and the reproduction period is important as proxy to explain the individuals movement (i.e. during reproduction period, the fish gather in groups) and/or to define temporal management rules. All biological data can be used in the future for natural resource management, which allows sustainable fishing. Moreover, another complementary analysis of the gonads through the histological approach could be realized in the future.

Conceptualization, D.R., K.M.; data curation, J.T., B.B., C.G., Y.A., H.E., L.W., R.E., T.R., D.R.; formal analysis, K.M., J.T., D.R.; investigation, K.M., J.T., D.R.; methodology, K.M., J.T., D.R.; project administration, K.M., D.R.; resources, D.R.; supervision, K.M., D.R.; writing - original draft, K.M., D.R.; writing - review & editing, K.M., J.T., B.B., C.G., Y.A., H.E., L.W., R.E., T.R., D.R.

This study was carried out with the financial support of the Data Collection Framework (DCF; EC Reg. 199/2008, 665/2008; Decisions 2008/949/EC and 2010/93/EU), the European Fisheries Fund (EFF 2007-2013; ANCRE-DMX2 project: Indicateurs biologiques et écologiques pour une gestion durable des stocks de poissons DéMersauX profonds d’intérêt halieutique à La Réunion), The European Maritime and Fisheries Fund (EMFF 2014-2020; IPERDMX project: Indicateurs Populationnels et Ecosystémiques pour une gestion durable des Ressources en poissons DéMersauX récifaux et profonds (1-500 m) à La Réunion), the Agence Française de Développement (AFD; AFD CZD1097; Accobiom project) and the French State. Another project ‘PECHTRAD’ (PECHe TRADitionnelle) funded by the reserve participated in this study.

  1. Bye VJ. 1984. The role of environmental factors in the timing of reproductive cycles. In: Potts GW and Wootton RJ, (Eds.), Fish Reproduction: Strategies and Tactics. Academic Press, New York, pp. 187-205.
  2. Chen X, Fang Z. 2022. Age and growth of fish. In: Chen X and Liu B, (Eds.), Biology of Fishery Resources. Springer, Singapore, pp. 71-111.
    CrossRef
  3. Cushing DH. 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26:249-293.
    CrossRef
  4. Fox J and Weisberg S. 2011. An R Companion to Applied Regression. 2nd ed, Sage, Thousand Oaks, pp. 1-608.
  5. Frisch AJ, Cameron DS, Pratchett MS, Williamson DH, Williams AJ, Reynolds AD, Hoey AS, Rizzari JR, Evans L, Kerrigan B, Muldoon G, Hobbs JPA. 2016. Key aspects of the biology, fisheries and management of Coral grouper. Rev. Fish Biol. Fish. 26:303-325.
    CrossRef
  6. Halim A, Loneragan NR, Wiryawan B, Hordyk AR, Yulianto I. 2020. Evaluating data-limited fisheries for grouper (Serranidae) and snapper (Lutjanidae) in the Coral Triangle, eastern Indonesia. Reg. Stud. Mar. Sci. 38:101388.
    CrossRef
  7. Harrison PL, Babcock RC, Bull GD, Oliver JK, Willis BL. 1984. Mass spawning in tropical reef corals. Science 223:1186-1189.
    Pubmed CrossRef
  8. Hoar WS. 1969. Reproduction. Fish Physiol. 3:1-72.
    Pubmed CrossRef
  9. ICES. 2012. Marine Strategy Framework Directive - Descriptor 3+. ICES CM 2012/ACOM 62. ICES, Copenhagen, pp. 1-172.
  10. ICES. 2018. Report of the Workshop for Advancing Sexual Maturity Staging in Fish (WKASMSF). ICES CM/EOSG 38. ICES, Copenhagen, pp. 1-75.
  11. Jakobsen T, Fogarty M, Moksness E. 2009. Fish Reproductive Biology: Implications for Assessment and Management. Blackwell, Oxford, pp. 1-429.
    CrossRef
  12. Law R. 2000. Fishing, selection, and phenotypic evolution. ICES J. Mar. Sci. 57:659-668.
    CrossRef
  13. Le Manach F, Bach P, Barret L, Guyomard D, Fleury PG, Pauly D. 2015. Reconstruction of the domestic and distant-water fisheries catch of la réunion (France), 1950-2010. Fish. Cent. Res. Rep. 23:83-98.
  14. Liley NR. 1969. Hormones and reproductive behavior in fishes. Fish Physiol. 3:73-116.
    CrossRef
  15. Marty L, Ernande B. 2014. Temporal trends in age and size at maturation of four North Sea gadid species: cod, haddock, whiting and Norway pout. Mar. Ecol. Prog. Ser. 497:179-197.
    CrossRef
  16. Newman SJ, Williams AJ, Wakefield CB, Nicol SJ, O'Malley JM. 2016. Review of the life history characteristics, ecology and fisheries for deep-water tropical demersal fish in the Indo-Pacific region. Rev. Fish Biol. Fish. 26:537-562.
    CrossRef
  17. Pankhurst NW. 2016. Reproduction and development. Fish Physiol. 35:295-331.
    Pubmed KoreaMed CrossRef
  18. Pauly D. 2019. Gasping Fish and Panting Squids: Oxygen, Temperature and the Growth of Water-Breathing Animals. 2nd ed, Excellence in Ecology 22, International Ecology Institute, Oldendorf, pp. 1-216.
  19. Pauly D. 2022. Why do fish reach first maturity when they do? J. Fish Biol. 101:333-341.
    Pubmed CrossRef
  20. R Core Team. 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
  21. Rijnsdorp AD. 1989. Maturation of male and female North Sea plaice (Pleuronectes platessa L). )ICES J. Mar. Sci. 46:35-51.
    CrossRef
  22. Roos D, Taconet J, Gentil C, Brisset B, Evano H, Aumond Y, Huet J, Lepetit C, Boymond-Morales R, Rungassamy T, Mahé K. 2022. Variation of the relationships between lengths and weights applied to 123 fish species observed at Réunion Island (Indian Ocean). Afr. J. Mar. Sci. 44:171-180.
    CrossRef
  23. Thorson JT, Cope JM, Jensen OP. 2012. Spawning biomass reference points for exploited marine fishes, incorporating taxonomic and body size information. Can. J. Fish. Aquat. Sci. 69:1556-1568.
    CrossRef
  24. Thresher RE. 1984. Reproduction in Reef Fishes. T.F.H. Publications, Neptune City, pp. 1-399.
    CrossRef
  25. Trindade-Santos I and Freire KMF. 2015. Analysis of reproductive patterns of fishes from three Large Marine Ecosystems. Front. Mar. Sci. 2:38.
    CrossRef
  26. Trippel EA, Solemdal P. 1997. Effects of adult age and size structure on reproductive output in marine fishes. In: Chambers RC and Trippel EA, (Eds.), Early Life History and Recruitment in Fish Populations. Chapman & Hall, London, pp. 31-62.
    CrossRef
  27. Tsikliras AC, Stergiou KI. 2010. Spawning period of Mediterranean marine fishes. Rev. Fish Biol. Fish. 20:499-538.
    CrossRef
  28. Weatherley AH. 1990. Approaches to understanding fish growth. Trans. Am. Fish. Soc. 119:662-672.
    CrossRef
  29. Wickham H. 2011. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40:1-29.
    CrossRef
  30. Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. 2nd ed, Springer, Cham, pp. 1-260.
    CrossRef

Article

Original Article

Journal of Animal Reproduction and Biotechnology 2024; 39(1): 31-39

Published online March 31, 2024 https://doi.org/10.12750/JARB.39.1.31

Copyright © The Korean Society of Animal Reproduction and Biotechnology.

Reproductive biology of 58 fish species around La Réunion Island (Western Indian Ocean): first sexual maturity and spawning period

Kélig Mahé1,* , Julien Taconet1,2, Blandine Brisset2, Claire Gentil2, Yoann Aumond2, Hugues Evano2, Louis Wambergue2, Romain Elleboode1, Tévamie Rungassamie3 and David Roos2

1Unité HMMN, IFREMER, Laboratory of Fisheries, Boulogne-sur-Mer 62321, France
2Délégation Océan Indien, IFREMER Institute, La Réunion 97822, France
3Réserve Naturelle Marine de La Réunion, La Réunion 97822, France

Correspondence to:Kélig Mahé
E-mail: kelig.mahe@ifremer.fr

Received: January 19, 2024; Revised: February 14, 2024; Accepted: February 21, 2024

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background: The biological information of fish, which include reproduction, is the prerequisite and the basis for the assessment of fisheries.
Methods: The aim of this work was to know the reproductive biology with the first sexual maturity (TL50) and the spawning period for 58 mainly fish species in the waters around La Réunion Island (Western Indian Ocean). Twenty families belonging to the Actinopterygii were represented (acanthuridae, berycidae, bramidae, carangidae, cirrhitidae, gempylidae, holocentridae, kyphosidae, labridae, lethrinidae, lutjanidae, malacanthidae, monacanthidae, mullidae, polymixiidae, pomacentridae, scaridae, scorpaenidae, serranidae, sparidae; 56 species; n = 9,751) and two families belonging to the Elasmobranchii (squalidae, centrophoridae; 2 species; n = 781) were sampled. Between 2014 and 2022, 10,532 individuals were sampled covering the maximum months number to follow the reproduction periods of these species.
Results: TL50 for the males and the females, respectively, ranged from 103.9 cm (Acanthurus triostegus) to 1,119.3 cm (Thyrsitoides marleyi) and from 111.7 cm (A. triostegus) to 613.1 cm (Centrophorus moluccensis). The reproduction period could be very different between the species from the very tight peak to a large peak covered all months.
Conclusions: Most species breed between October and March but it was not the trend for all species around La Réunion Island.

Keywords: gonad observation, reproduction period, reproductive maturity stages, size at the first sexual maturity

INTRODUCTION

The biological parameters (i.e. growth and reproduction) are essentially to management the fish population (Jakobsen et al., 2009). Fish reproductive biology is the necessary step to evaluate the reference points as spawning stock biomass and the maturity ogive, which are integrated in the stock assessment models (Jakobsen et al., 2009). The lack or scarcity of these biological information, can lead to over-exploitation of fisheries resources. The main commercial demersal tropical fishes, along with snappers (Lutjanidae), groupers (Serranidae), emperors (Lethrinidae), carangids (Carangidae), soldierfishes (Holocentridae) and goatfishes (Mullidae) support locally important artisanal fisheries throughout the Indo-Pacific region, but quantitative assessments of these species have been limited by a lack of adequate biological and fisheries data (Newman et al., 2016; Halim et al., 2020), including around La Réunion Island (Le Manach et al., 2015). Among 123 fish species followed around La Réunion Island (Roos et al., 2022), The main objective of this study was to provide the reproductive biology information with the first sexual maturity and the spawning period for 58 mainly fish species required for the management of fisheries resources.

MATERIALS AND METHODS

Sampling

All fish sampled during scientific surveys, and some specimen were added from commercial landings to complete the length range or the months without surveys. During eight years (i.e. between 2014 and 2022), 10,532 individuals of 58 species were sampled. Twenty families belonging to the Actinopterygii were represented (acanthuridae, berycidae, bramidae, carangidae, cirrhitidae, gempylidae, holocentridae, kyphosidae, labridae, lethrinidae, lutjanidae, malacanthidae, monacanthidae, mullidae, polymixiidae, pomacentridae, scaridae, scorpaenidae, serranidae, sparidae; 56 species; n = 9,751) and two families belonging to the Elasmobranchii (squalidae, centrophoridae; 2 species; n = 781) were sampled (Table 1). All individuals were taken to the laboratory for accurate measurements. Each individual was measured to the nearest mm for total length (TL) and weighted to the grams for Total Weight (W). The gonads were observed macroscopically to determine the sex and this associated sexual maturity stage.

Table 1. Sampling details (number and length by sex: males, M; females, F and immatures, I) with the first sexual maturity (TL50; p-value < 0.05 showed the significant sexual dimorphism) for 58 species around La Réunion Island (*protogynous hermaphroditism species).

FamilleLatin mameNumberLength of adults (F+M)Length of MalesLength of FemalesTL50
TotalMalesFemalesImmaturesMeanSDRange
(min-max)
MeanSDRange
(min-max)
MeanSDRange
(min-max)
MalesFemalesAdultes
(F+M)
p-value
AcanthuridaeAcanthurus triostegus542214225103152.021.334-199154.618.099-199150.716.495-192103.91111.68108.300.21
Naso elegans6340185322.786.6167-469336.177.3208-459266.186.0167-426214.39204.65
Naso unicornis176986711299.694.9157-557322.893.4167-557266.591.8157-532247.76209.43231.65< 0.05
BerycidaeBeryx decadactylus4920272503.167.6350-610458.957.2350-550528.958.9388-610
BramidaeEumegistus illustris2369612713680.6135.1452-1,000661.3126.0470-910692.8142.2452-1,000628.56521.05575.550.09
CarangidaeCaranx melampygus6545200609.196.0433-838621.1100.2467-838582.081.9433-710
Decapterus tabl63232911266.926.0193-326267.023.7233-313264.629.9193-326215.05215.06
CentrophoridaeCentrophorus moluccensis6931380589.1309.00-876644.5182.60-741543.9379.20-876548.51613.07556.26< 0.05
CirrhitidaeCirrhitus pinnulatus6942243189.522.1140-252196.818.0168-252177.323.5140-223
GempylidaePromethichthys prometheus8628535381.177.0216-564356.068.3263-490401.873.4282-564386.05356.92361.93< 0.05
Rexea prometheoides135161154298.650.80-425257.421.1222-320306.743.00-425
Thyrsitoides marleyi3692431,092.4463.0222-1,8901,009.8342.0410-1,2801,223.3426.0320-1,8901,119.30
HolocentridaeMyripristis berndti12260557233.343.4126-308239.842.2126-308229.942.4127-292129.96
Myripristis chryseres8748372206.120.2150-255215.918.1182-255194.815.5150-215155.99159.95
Myripristis murdjan7323464200.529.5145-255198.225.1145-234205.430.0146-255
Ostichthys kaianus4016213283.243.7165-360291.043.4188-360282.838.4184-344
Sargocentron spiniferum3813223268.252.1181-371275.850.0220-361268.454.3196-371210.31212.85
KyphosidaeKyphosus bigibbus2714121317.427.6244-365326.116.9296-353308.735.4244-365289.89287.68
Kyphosus cinerascens3219130327.663.0205-470305.848.7205-360359.369.7271-470241.23240.18
Kyphosus vaigiensis251771306.749.4203-395292.948.9203-395347.023.5304-375
LabridaeCheilinus trilobatus79135610314.176.9184-477355.573.9184-473305.177.0200-477
LethrinidaeGnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Lethrinus rubrioperculatus*12536872339.666.5192-464401.117.5354-433315.161.7194-464208.62208.62
LutjanidaeAphareus rutilans16290648429.891.4211-786429.592.5211-786434.492.6319-769353.70381.76368.81< 0.05
Aprion virescens6540241443.1123.2212-893427.3106.2288-670477.5137.2323-893324.04320.30
Etelis carbunculus1,70088177742277.170.9139-1,250270.659.3164-980286.781.4153-1,250183.95183.46188.180.87
Etelis coruscans193859810455.6249.2206-1,155450.6240.2206-1,068480.0268.1220-1,155391.99394.25397.490.83
Lutjanus bengalensis256190177.219.3147-217166.514.3147-189180.619.7152-217
Lutjanus kasmira75336037320219.634.9110-336230.137.1150-336211.228.9110-281180.22147.11161.29< 0.05
Lutjanus notatus3972011951215.222.8143-277224.322.3155-277206.219.0143-247
Pristipomoides argyrogrammicus64731731713232.231.8122-317239.431.3162-316226.829.6140-317148.06149.34
Pristipomoides filamentosus3009817131262.851.1155-576273.361.1157-576264.442.3165-383326.90310.35317.370.18
Pristipomoides multidens2701401291501.8128.3270-865514.9132.0282-865487.6123.0270-815388.63346.15369.62< 0.05
MalacanthidaeBranchiostegus doliatus3316152342.742.9247-422356.136.2303-422326.748.0247-410
MonacanthidaeCantherhines dumerilii5625256279.935.2185-355274.427.6185-312292.838.5233-355240.00219.39
MullidaeMulloidichthys flavolineatus4214545331137.964.285-415197.179.495-319242.586.597-415185.17204.51207.040.37
Mulloidichthys pfluegeri5826311332.558.4193-452339.050.4215-429328.765.1193-452259.33240.43247.930.61
Parupeneus trifasciatus2699811358226.155.679-401255.761.7141-401213.137.3129-352218.90199.22212.920.63
PolymixiidaePolymixia berndti7217469230.463.8151-430248.289.2151-430226.057.7160-429
Polydactylus sexfilis107492533309.3148.870-519379.630.5311-457440.835.5366-519256.55
PomacentridaeAbudefduf septemfasciatus272061206.211.3180-227203.911.8180-227213.86.4207-224
ScaridaeCalotomus carolinus6726392354.555.3186-456384.055.4202-456334.047.4186-403245.72240.00240.000.81
Chlorurus enneacanthus16872879321.484.1175-765333.189.5175-765312.180.8182-560209.58200.53
Scarus psittacus11768445278.647.4121-364300.235.3198-364248.738.4137-326164.74154.02
ScorpaenidaePontinus nigerimum37121510275.651.8161-380311.328.6273-370241.947.1161-298
SerranidaeCephalopholis aurantia*2225415513228.535.8136-318259.925.2219-318220.432.3136-313160.39160.39
Cephalopholis nigripinnis*3110201167.427.4119-230178.823.3145-209162.128.8119-230
Cephalopholis spiloparaea*4720270170.024.9129-236176.825.3134-236165.023.9129-230
Epinephelus fasciatus*301332644230.754.2100-421273.966.3164-421225.850.1100-353130.28130.28
Epinephelus hexagonatus*3146320744166.027.9112-241181.125.2127-233158.828.0112-241
Epinephelus merra*1341610711181.129.0120-254188.128.2149-230180.329.9120-254166.20166.20
Epinephelus radiatus*1149996364.2108.1123-653392.795.8280-562368.3106.7187-653317.71317.71
Epinephelus tauvina*72223812267.767.7158-518256.970.5187-518285.265.1158-450268.72268.72
Gnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Variola albimarginata*152451061358.678.7185-555428.062.3257-555330.365.4185-494236.26236.26
Variola louti*7124470580.1136.7216-840649.3145.8392-840544.7118.4216-741363.01363.01
SparidaeArgyrops filamentosus6134225239.621.7195-290244.222.6198-290239.615.9214-270
SqualidaeSqualus megalops71230239713512.0190.20-820460.2187.60-683559.8171.40-820397.67500.00454.63< 0.05


First sexual maturity

Sex ratios as the percentage of females (F) in the samples, were calculated. The first sexual maturity, to separate juveniles and sexually mature individuals thus defining the spawning biomass (i.e. reference point for exploited marine fishes) (Thorson et al., 2012), was measured from TL50. This biological parameter was the total length at which 50% of individuals are mature for the first time.

Where m(l) is the proportion of mature individuals in

m(l)=exp(exp(a+b*l))
TL50=ln(ln(0.5))ab

each length class (%), a is intercept, b is slope, l is the fish total length (cm) and TL50 is the mean total length at sexual maturity (50%, cm), were used. Among the Actinopterygii, two families (serranidae and lethrinidae, 13 species; Table 1) showed the protogynous hermaphrodites (i.e. change sex from female to male). For these species, first sexual maturity was only estimated for females.

Reproduction period

Fish were assigned to the following maturity development stages as recommended at the international level (ICES, 2018): from (I) immature; (II) resting; (III) ripe and running; (IV) spent; to (V) post-spent. From the percentage of individuals per month and per maturity stages throughout the year, the reproduction period and intensity were identified. The adults are the sum of all fish of maturity stages III, IV and V.

Statistical analysis

Statistical analyses to identify the significant sex effect on the first sexual maturity (with significant effect at p < 0.05) were carried out from the CAR package (Fox and Weisberg, 2011). This sexual dimorphism was tested on all fish species without two protogynous hermaphrodites families. The figures were carried out from the ggplot2 (Wickham, 2016) and plyr (Wickham, 2011) packages in the R statistical environment (R Core Team, 2023).

Ethical statement

All species were sampled from scientific surveys or caught for the commercial landings. They are not in the IUCN red list as critically endangered, endangered or vulnerable species.

RESULTS

Among 10,532 individuals, there were 4,271 males, 5,346 females and 915 immatures. Summarised information for each species, by each sex or both males and females, is presented in Table 1 and Supplementary Table 1. Among 23 families, two were represented by a relatively high number of species, such as the Serranidae (11 species) and Lutjanidae (10 species). In the sameway, these two families showed the large number of individuals with 4,512 belonging to the Lutjanidae and 1,518 belonging to the Serranidae. According to the selected species, the distribution between the two sexes and the immatures can be very different. While the reproduction of protogynous hermaphrodites (i.e. for two families: serranidae and lethrinidae represented by 13 species) explained why males could be larger than females, for other species, there was no generalizable observable trend between males and females and it depends on the analysed species.

Among 58 analysed species, the mean total length of the first sexual maturity (TL50) could be modelled from individual in situ data for 40 species (Table 1). TL50 for the males and the females, respectively, ranged from 103.9 cm (Acanthurus triostegus) to 1,119.3 cm (Thyrsitoides marleyi) and from 111.7 cm (A. triostegus) to 613.1 cm (Centrophorus moluccensis) (Table 1). For ten hermaphrodites’ species, only TL50 for females was modelled. For 30 other species presenting the TL50 fitted on the data, this biological parameter was measured for the males and for the females for 16 species. Among these species, 10 a higher TL50 for females than for males and only 6 have the opposite trend. The significant different of TL50 between the males and the females were observed for 7 species among 16 species (Table 1).

For all 58 species, the reproduction period and intensity were analysed for each species including all adults’ individuals (Fig. 1) and by each sex (females Supplementary Fig. 1 and males Supplementary Fig. 2). There were three species including the two Elasmobranchii species (Squalus megalops and Centrophorus moluccesis) and one species of the mullidae family (Mulloidichthys flavolineatus) showed that the reproduction peak (i.e. high spawning period; Fig. 1) covered all months. Conversely, other species presented the reproduction peak very tightly spread over 3 months (Thyrsitoides marleyi; Kyphosus bigibbus; Aphareus rutilans; Pristipomoides filamentosus; Polymixia berndti; Cephalopholis nigripinnis; Epinephelus hexagonatus). However, for the species with the restricted reproduction period, most species breed between October and March but it was not the trend for all species. The reproduction activity may be concentrated in the winter months for a limited number of species as Argyrops filamentosus, Pristipomoides filamentosus, Kyphosus vaigiensis and Kyphosus bigibbus (Fig. 1).

Figure 1.Reproduction period and intensity (percentage of individuals actively breeding: No spawning: 0-25%; Low spawning: 25-50%; Medium spawning: 50-75%; High spawning: 75-100%) of species around La Réunion Island (*month without sampled individuals).

DISCUSSION

Reproductive process through the sexual maturity and the peak of reproduction are important elements prerequisite to realize the stock assessment with a good precision (Chen et al., 2022). However, for many fish species, the females and males and their maturity stage cannot be distinguished by only external characteristics. Consequently, for many cases of study, this information is lack, very old or partial. Moreover, for tropical species as around La Réunion Island, there may be conservation problems due to the high temperature after fishing which result in difficulties in observation internal organs such as the gonads. Consequently, this type of study aggregating reproductive information from organ observations in the laboratory for a very large number of species is necessary to provide reference points for each species, which can be used in fisheries resource monitoring as is done for other biological parameters such as the length-weight relationship (Roos et al., 2022).

Firstly, the length of the first sexual maturity (TL50) was measured for each species. Among fish species, there are two mainly sexual characteristics: hermaphrodites versus dioecious species. For the protogynous hermaphrodites, concerning two families (serranidae and lethrinidae, 13 species), the first sexual maturity of females is earlier than the sex change and consequently the length is not the same (Frisch et al., 2016). For the dioecious species, there are no clearly patterns between the TL50 for females and males. Some species show comparable TL50 between males and females, others show marked differences in favor of females or males. These differences between sexes within the same population or between several population in the length at the sexual maturity, can be caused by phenotypic changes, genetic adaptations or the interaction of both (Law, 2000; Trindade-Santos and Freire, 2015). TL50 is influenced by environmental conditions (Weatherley, 1990), but human activities could be the potential factors (i.e. fishing, pollution…). For example, a negative relationship between the length at sexual maturity and the level of fishing pressure was observed (ICES, 2012; Marty et al., 2014).

Secondly, the timing and intensity of the spawning were estimated for each species. For this reproductive trait, there are mainly difference among species with some species with a very large reproduction peak covered all months and conversely, others with very tight reproduction peak over 3 months. These results corroborate the same approach applied in the Mediterranean Sea (Tsikliras et al., 2010). Some species that breed strongly throughout the year may show two sexual strategies with some individuals breeding once a year and others at least twice (Bye, 1984; Cushing, 1990). The duration and the period of the year of the reproduction peak varies between the species and between the populations within the same species. The spawning season begin when the fish receive the environmental stimuli (Hoar, 1969; Liley, 1969). Lunar periodicity seems to be the influential external stimulus on reproductive characteristics of tropical coastal fish species (Harrison et al., 1984; Thresher, 1984). Another important factor to trigger the reproduction could be internal with the hormonal cascades leading to maturation and spawning and the gill surface area (Pankhurst, 2016; Pauly, 2019; Pauly, 2022). Finally, the reproduction biology could linked to the age class of the specimen with the ontogenic effect (Rijnsdorp, 1989; Trippel et al., 1997).

CONCLUSION

The reproductive biology information with the first sexual maturity and the spawning period were analyzed for 58 mainly fish species around the La Réunion Island in the Indian Ocean. For many species, these biological data were not available or were very old. The first sexual maturity length is essential to evaluate the reference point named the spawning stock biomass (SSB) (Thorson et al., 2012) used in the stock assessment and the reproduction period is important as proxy to explain the individuals movement (i.e. during reproduction period, the fish gather in groups) and/or to define temporal management rules. All biological data can be used in the future for natural resource management, which allows sustainable fishing. Moreover, another complementary analysis of the gonads through the histological approach could be realized in the future.

SUPPLEMENTARY MATERIALS

Supplementary material can be found via https://doi.org/10.12750/JARB.39.1.31

jarb-39-1-31-supple.pdf

Acknowledgements

We thank all fishers and colleagues who helped us in the field, and the anonymous reviewers for their comments and suggestions.

Author Contributions

Conceptualization, D.R., K.M.; data curation, J.T., B.B., C.G., Y.A., H.E., L.W., R.E., T.R., D.R.; formal analysis, K.M., J.T., D.R.; investigation, K.M., J.T., D.R.; methodology, K.M., J.T., D.R.; project administration, K.M., D.R.; resources, D.R.; supervision, K.M., D.R.; writing - original draft, K.M., D.R.; writing - review & editing, K.M., J.T., B.B., C.G., Y.A., H.E., L.W., R.E., T.R., D.R.

Funding

This study was carried out with the financial support of the Data Collection Framework (DCF; EC Reg. 199/2008, 665/2008; Decisions 2008/949/EC and 2010/93/EU), the European Fisheries Fund (EFF 2007-2013; ANCRE-DMX2 project: Indicateurs biologiques et écologiques pour une gestion durable des stocks de poissons DéMersauX profonds d’intérêt halieutique à La Réunion), The European Maritime and Fisheries Fund (EMFF 2014-2020; IPERDMX project: Indicateurs Populationnels et Ecosystémiques pour une gestion durable des Ressources en poissons DéMersauX récifaux et profonds (1-500 m) à La Réunion), the Agence Française de Développement (AFD; AFD CZD1097; Accobiom project) and the French State. Another project ‘PECHTRAD’ (PECHe TRADitionnelle) funded by the reserve participated in this study.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent to Publish

Not applicable.

Availability of Data and Materials

Not applicable.

Conflict of Interest

Conflicts of Interest: No potential conflict of interest relevant to this article was reported.

Fig 1.

Figure 1.Reproduction period and intensity (percentage of individuals actively breeding: No spawning: 0-25%; Low spawning: 25-50%; Medium spawning: 50-75%; High spawning: 75-100%) of species around La Réunion Island (*month without sampled individuals).
Journal of Animal Reproduction and Biotechnology 2024; 39: 31-39https://doi.org/10.12750/JARB.39.1.31

Table 1 . Sampling details (number and length by sex: males, M; females, F and immatures, I) with the first sexual maturity (TL50; p-value < 0.05 showed the significant sexual dimorphism) for 58 species around La Réunion Island (*protogynous hermaphroditism species).

FamilleLatin mameNumberLength of adults (F+M)Length of MalesLength of FemalesTL50
TotalMalesFemalesImmaturesMeanSDRange
(min-max)
MeanSDRange
(min-max)
MeanSDRange
(min-max)
MalesFemalesAdultes
(F+M)
p-value
AcanthuridaeAcanthurus triostegus542214225103152.021.334-199154.618.099-199150.716.495-192103.91111.68108.300.21
Naso elegans6340185322.786.6167-469336.177.3208-459266.186.0167-426214.39204.65
Naso unicornis176986711299.694.9157-557322.893.4167-557266.591.8157-532247.76209.43231.65< 0.05
BerycidaeBeryx decadactylus4920272503.167.6350-610458.957.2350-550528.958.9388-610
BramidaeEumegistus illustris2369612713680.6135.1452-1,000661.3126.0470-910692.8142.2452-1,000628.56521.05575.550.09
CarangidaeCaranx melampygus6545200609.196.0433-838621.1100.2467-838582.081.9433-710
Decapterus tabl63232911266.926.0193-326267.023.7233-313264.629.9193-326215.05215.06
CentrophoridaeCentrophorus moluccensis6931380589.1309.00-876644.5182.60-741543.9379.20-876548.51613.07556.26< 0.05
CirrhitidaeCirrhitus pinnulatus6942243189.522.1140-252196.818.0168-252177.323.5140-223
GempylidaePromethichthys prometheus8628535381.177.0216-564356.068.3263-490401.873.4282-564386.05356.92361.93< 0.05
Rexea prometheoides135161154298.650.80-425257.421.1222-320306.743.00-425
Thyrsitoides marleyi3692431,092.4463.0222-1,8901,009.8342.0410-1,2801,223.3426.0320-1,8901,119.30
HolocentridaeMyripristis berndti12260557233.343.4126-308239.842.2126-308229.942.4127-292129.96
Myripristis chryseres8748372206.120.2150-255215.918.1182-255194.815.5150-215155.99159.95
Myripristis murdjan7323464200.529.5145-255198.225.1145-234205.430.0146-255
Ostichthys kaianus4016213283.243.7165-360291.043.4188-360282.838.4184-344
Sargocentron spiniferum3813223268.252.1181-371275.850.0220-361268.454.3196-371210.31212.85
KyphosidaeKyphosus bigibbus2714121317.427.6244-365326.116.9296-353308.735.4244-365289.89287.68
Kyphosus cinerascens3219130327.663.0205-470305.848.7205-360359.369.7271-470241.23240.18
Kyphosus vaigiensis251771306.749.4203-395292.948.9203-395347.023.5304-375
LabridaeCheilinus trilobatus79135610314.176.9184-477355.573.9184-473305.177.0200-477
LethrinidaeGnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Lethrinus rubrioperculatus*12536872339.666.5192-464401.117.5354-433315.161.7194-464208.62208.62
LutjanidaeAphareus rutilans16290648429.891.4211-786429.592.5211-786434.492.6319-769353.70381.76368.81< 0.05
Aprion virescens6540241443.1123.2212-893427.3106.2288-670477.5137.2323-893324.04320.30
Etelis carbunculus1,70088177742277.170.9139-1,250270.659.3164-980286.781.4153-1,250183.95183.46188.180.87
Etelis coruscans193859810455.6249.2206-1,155450.6240.2206-1,068480.0268.1220-1,155391.99394.25397.490.83
Lutjanus bengalensis256190177.219.3147-217166.514.3147-189180.619.7152-217
Lutjanus kasmira75336037320219.634.9110-336230.137.1150-336211.228.9110-281180.22147.11161.29< 0.05
Lutjanus notatus3972011951215.222.8143-277224.322.3155-277206.219.0143-247
Pristipomoides argyrogrammicus64731731713232.231.8122-317239.431.3162-316226.829.6140-317148.06149.34
Pristipomoides filamentosus3009817131262.851.1155-576273.361.1157-576264.442.3165-383326.90310.35317.370.18
Pristipomoides multidens2701401291501.8128.3270-865514.9132.0282-865487.6123.0270-815388.63346.15369.62< 0.05
MalacanthidaeBranchiostegus doliatus3316152342.742.9247-422356.136.2303-422326.748.0247-410
MonacanthidaeCantherhines dumerilii5625256279.935.2185-355274.427.6185-312292.838.5233-355240.00219.39
MullidaeMulloidichthys flavolineatus4214545331137.964.285-415197.179.495-319242.586.597-415185.17204.51207.040.37
Mulloidichthys pfluegeri5826311332.558.4193-452339.050.4215-429328.765.1193-452259.33240.43247.930.61
Parupeneus trifasciatus2699811358226.155.679-401255.761.7141-401213.137.3129-352218.90199.22212.920.63
PolymixiidaePolymixia berndti7217469230.463.8151-430248.289.2151-430226.057.7160-429
Polydactylus sexfilis107492533309.3148.870-519379.630.5311-457440.835.5366-519256.55
PomacentridaeAbudefduf septemfasciatus272061206.211.3180-227203.911.8180-227213.86.4207-224
ScaridaeCalotomus carolinus6726392354.555.3186-456384.055.4202-456334.047.4186-403245.72240.00240.000.81
Chlorurus enneacanthus16872879321.484.1175-765333.189.5175-765312.180.8182-560209.58200.53
Scarus psittacus11768445278.647.4121-364300.235.3198-364248.738.4137-326164.74154.02
ScorpaenidaePontinus nigerimum37121510275.651.8161-380311.328.6273-370241.947.1161-298
SerranidaeCephalopholis aurantia*2225415513228.535.8136-318259.925.2219-318220.432.3136-313160.39160.39
Cephalopholis nigripinnis*3110201167.427.4119-230178.823.3145-209162.128.8119-230
Cephalopholis spiloparaea*4720270170.024.9129-236176.825.3134-236165.023.9129-230
Epinephelus fasciatus*301332644230.754.2100-421273.966.3164-421225.850.1100-353130.28130.28
Epinephelus hexagonatus*3146320744166.027.9112-241181.125.2127-233158.828.0112-241
Epinephelus merra*1341610711181.129.0120-254188.128.2149-230180.329.9120-254166.20166.20
Epinephelus radiatus*1149996364.2108.1123-653392.795.8280-562368.3106.7187-653317.71317.71
Epinephelus tauvina*72223812267.767.7158-518256.970.5187-518285.265.1158-450268.72268.72
Gnathodentex aureolineatus*6013389234.337.2155-303241.927.8182-273241.634.8173-303187.70187.70
Variola albimarginata*152451061358.678.7185-555428.062.3257-555330.365.4185-494236.26236.26
Variola louti*7124470580.1136.7216-840649.3145.8392-840544.7118.4216-741363.01363.01
SparidaeArgyrops filamentosus6134225239.621.7195-290244.222.6198-290239.615.9214-270
SqualidaeSqualus megalops71230239713512.0190.20-820460.2187.60-683559.8171.40-820397.67500.00454.63< 0.05

References

  1. Bye VJ. 1984. The role of environmental factors in the timing of reproductive cycles. In: Potts GW and Wootton RJ, (Eds.), Fish Reproduction: Strategies and Tactics. Academic Press, New York, pp. 187-205.
  2. Chen X, Fang Z. 2022. Age and growth of fish. In: Chen X and Liu B, (Eds.), Biology of Fishery Resources. Springer, Singapore, pp. 71-111.
    CrossRef
  3. Cushing DH. 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv. Mar. Biol. 26:249-293.
    CrossRef
  4. Fox J and Weisberg S. 2011. An R Companion to Applied Regression. 2nd ed, Sage, Thousand Oaks, pp. 1-608.
  5. Frisch AJ, Cameron DS, Pratchett MS, Williamson DH, Williams AJ, Reynolds AD, Hoey AS, Rizzari JR, Evans L, Kerrigan B, Muldoon G, Hobbs JPA. 2016. Key aspects of the biology, fisheries and management of Coral grouper. Rev. Fish Biol. Fish. 26:303-325.
    CrossRef
  6. Halim A, Loneragan NR, Wiryawan B, Hordyk AR, Yulianto I. 2020. Evaluating data-limited fisheries for grouper (Serranidae) and snapper (Lutjanidae) in the Coral Triangle, eastern Indonesia. Reg. Stud. Mar. Sci. 38:101388.
    CrossRef
  7. Harrison PL, Babcock RC, Bull GD, Oliver JK, Willis BL. 1984. Mass spawning in tropical reef corals. Science 223:1186-1189.
    Pubmed CrossRef
  8. Hoar WS. 1969. Reproduction. Fish Physiol. 3:1-72.
    Pubmed CrossRef
  9. ICES. 2012. Marine Strategy Framework Directive - Descriptor 3+. ICES CM 2012/ACOM 62. ICES, Copenhagen, pp. 1-172.
  10. ICES. 2018. Report of the Workshop for Advancing Sexual Maturity Staging in Fish (WKASMSF). ICES CM/EOSG 38. ICES, Copenhagen, pp. 1-75.
  11. Jakobsen T, Fogarty M, Moksness E. 2009. Fish Reproductive Biology: Implications for Assessment and Management. Blackwell, Oxford, pp. 1-429.
    CrossRef
  12. Law R. 2000. Fishing, selection, and phenotypic evolution. ICES J. Mar. Sci. 57:659-668.
    CrossRef
  13. Le Manach F, Bach P, Barret L, Guyomard D, Fleury PG, Pauly D. 2015. Reconstruction of the domestic and distant-water fisheries catch of la réunion (France), 1950-2010. Fish. Cent. Res. Rep. 23:83-98.
  14. Liley NR. 1969. Hormones and reproductive behavior in fishes. Fish Physiol. 3:73-116.
    CrossRef
  15. Marty L, Ernande B. 2014. Temporal trends in age and size at maturation of four North Sea gadid species: cod, haddock, whiting and Norway pout. Mar. Ecol. Prog. Ser. 497:179-197.
    CrossRef
  16. Newman SJ, Williams AJ, Wakefield CB, Nicol SJ, O'Malley JM. 2016. Review of the life history characteristics, ecology and fisheries for deep-water tropical demersal fish in the Indo-Pacific region. Rev. Fish Biol. Fish. 26:537-562.
    CrossRef
  17. Pankhurst NW. 2016. Reproduction and development. Fish Physiol. 35:295-331.
    Pubmed KoreaMed CrossRef
  18. Pauly D. 2019. Gasping Fish and Panting Squids: Oxygen, Temperature and the Growth of Water-Breathing Animals. 2nd ed, Excellence in Ecology 22, International Ecology Institute, Oldendorf, pp. 1-216.
  19. Pauly D. 2022. Why do fish reach first maturity when they do? J. Fish Biol. 101:333-341.
    Pubmed CrossRef
  20. R Core Team. 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
  21. Rijnsdorp AD. 1989. Maturation of male and female North Sea plaice (Pleuronectes platessa L). )ICES J. Mar. Sci. 46:35-51.
    CrossRef
  22. Roos D, Taconet J, Gentil C, Brisset B, Evano H, Aumond Y, Huet J, Lepetit C, Boymond-Morales R, Rungassamy T, Mahé K. 2022. Variation of the relationships between lengths and weights applied to 123 fish species observed at Réunion Island (Indian Ocean). Afr. J. Mar. Sci. 44:171-180.
    CrossRef
  23. Thorson JT, Cope JM, Jensen OP. 2012. Spawning biomass reference points for exploited marine fishes, incorporating taxonomic and body size information. Can. J. Fish. Aquat. Sci. 69:1556-1568.
    CrossRef
  24. Thresher RE. 1984. Reproduction in Reef Fishes. T.F.H. Publications, Neptune City, pp. 1-399.
    CrossRef
  25. Trindade-Santos I and Freire KMF. 2015. Analysis of reproductive patterns of fishes from three Large Marine Ecosystems. Front. Mar. Sci. 2:38.
    CrossRef
  26. Trippel EA, Solemdal P. 1997. Effects of adult age and size structure on reproductive output in marine fishes. In: Chambers RC and Trippel EA, (Eds.), Early Life History and Recruitment in Fish Populations. Chapman & Hall, London, pp. 31-62.
    CrossRef
  27. Tsikliras AC, Stergiou KI. 2010. Spawning period of Mediterranean marine fishes. Rev. Fish Biol. Fish. 20:499-538.
    CrossRef
  28. Weatherley AH. 1990. Approaches to understanding fish growth. Trans. Am. Fish. Soc. 119:662-672.
    CrossRef
  29. Wickham H. 2011. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40:1-29.
    CrossRef
  30. Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. 2nd ed, Springer, Cham, pp. 1-260.
    CrossRef

Article Tools

PDF print Article
Export to Citation Open Access
Google Scholar Send to Email

Share this article on :

Stats or Metrics

Supplementary

Related articles in JARB

more

JARB Journal of Animal Reproduction and Biotehnology

qr code

OPEN ACCESS pISSN: 2671-4639
eISSN: 2671-4663