Macroscopic gonad staging and reproductive seasonality in the Gorean snapper, Lutjanus goreensis a gonochoristic West African Lutjanid Kafayat A. Fakoya1* and Martins A. Anetekha1 1Department of Fisheries, Faculty of Science, Lagos State University, Ojo, P.M.B. 0001 LASU Post Office, Ojo, Lagos State, Nigeria. *Corresponding Author: [email protected] Abstract In Nigeria, the Gorean snapper Lutjanus goreensis is an important component of artisanal fisheries and trawl landings although substantial gap exists on some aspects of the species’ reproductive biology in the entire Gulf of Guinea. The main objective of the study was to characterize the sexual differentiation and ratio, spawning seasonality and pattern through observation of three somatic indices: gonadosomatic index (IG), hepatosomatic index (IH) and the Relative Condition Factor (Krel), macroscopic staging and size at first sexual maturity of the species. Spawning seasonality and pattern were best determined from temporal trends of IG and macroscopic gonad stage frequencies. The fish is monogamous with sex ratio of 1 male: 1 female. Five distinct gonad maturity stages and lack of population synchrony in gonadal development were distinguished. Mean sizes at first sexual maturity were 34.61cm TL and 34.21 cm TL for females and males, respectively. Multiple spawning peaks reflected by high

IG occurred in December, May to June and August indicated protracted spawning while lowest IG occurred in March- April, denoted a resting phase. The species is a multiple spawner as evinced from asynchronous development of the gonads. It showed continuous reproduction throughout the year, particularly at higher intensity during the heavy rains (May to September). While these findings imply continuous recruitment into fishery, it is recommended that for optimal exploitation, minimum capture size has to be increased above sizes at sexual maturity.

Introduction species spawn year round with spawning peak Lutjanidae popularly known as snappers during moderate warm water temperature comprise a large family of the order (Thresher, 1984), and on the basis of spawning Perciformes, important in both tropical and periodicity, two distinct spawning populations subtropical waters. The family is represented are distinguished: a restricted spawning period by 4 subfamilies: Lutjaninae, Apsilinae, centered around summer for continental Etelinae and Paradicichthyninae. The first is populations and species, and a year-round the largest subfamily grouped into 6 genera: spawning period with pulses of activity in Lutjanus, Macolor, Pinjalo, Hoplopagrus, spring and autumn for insular populations and Ocyurus and Rhomboplites. Within the species (Grimes, 1987). family, Lutjanus represents, by far, the Gonadosonatic index (IG) and macroscopic most widespread genus and abundant, with staging have been used with relative success at least 70 species in the Atlantic, Pacific in determining the time of spawning in and Indian Oceans (Allen, 1985; Martinez- many snapper species. A five - stage scheme Andrade, 2003). Generally, the characteristic modified from Nikolsky (1963) consisting life-history traits of lutjanids implies low of: immature, maturing including recovery, productivity which culminates in a slow rate ripe, spawning and spent was used to classify of population increase and predisposes several gonad development and also determine species of shallow and deepwater stocks to time of spawning in the vermillion snapper, overfishing with serious consequences for Rhomboplites aurorubens (Manickhand- conservation and management (Grandcourt Heilemann and Phillip, 1996). The Red et al., 2006). Typically, most tropical snapper snapper, L. campechanus spawns in June

West African Journal of Applied Ecology, vol. 27(1), 2019: 1 - 22 2 West African Journal of Applied Ecology, vol. 27(1), 2019 with less peaks in July and August (Collins et 1976; El Habouz et al., 2011), with lipid al., 1996). Likely, L. fulviflamma in Kenyan content of marine fish increasing during the inshore waters and South Arabian sea, L. feeding period and gonad development (Lloret griseus and L. analis from different locations and Planes, 2003). A lower value indicates in Florida waters, Fort Pierce South, Cuba and decreased reproductive activity or the end of Puerto Rico also exhibited extended periods the spawning period, and suggests that the indicated by a main peak season and a shorter fish may decrease its feeding activity during season, laying eggs in batches (Domeier et reproduction (Simon et al., 2009). al., 1996; Kaunda-Arara and Ntiba, 1997; Size rather than age may be more closely Grandscourt et al., 2006; Faunce et al., 2008). linked with respect to the onset of sexual This spawning strategy was also observed maturity (Schaefer, 1987; Lowerre-Barbieri, in L. peru in Mexico with a main season in 2009). Functional statistical relationships or August, and a second period during February fitting of a logistic curve between proportion corresponding with the highest values of the mature and size and/or age is the traditional gonadosomatic index (Gallardo-Cabello et method of estimating sexual maturity al., 2010) and L. argentiventris from March to (Lowerre-Barbieri et al., 2011). In L. analis July with a peak in activity during April-June from Florida waters, fifty percent of females

(Garcia-Contreras et al., 2009). achieved sexual maturity at 353 mm TLmax Liver size is related to its lipid content and and 2.07 years of age (Faunce et al., 2008). is indicative of lipid accumulation during The red snapper, L. campechanus reaches favorable environmental conditions and sexual maturity at approximately two years of utilization to support gonad development age when they are about 26–27 cm in length or adverse conditions (Lloret and Planes, (Morans, 1988; Phelps et al., 2009; Brule et al.,

2003). The hepatosomatic index (IH) is used 2010). Grandcourt et al. (2006) estimated the as an indicator of the reproductive period size at first maturity of Lutjanus fulviflamma and is related to the relocation of energy (blackspot snapper) to be 16.7cm and 18.7 resources from the liver to the vitellogenesis cm for males and females respectively, process (Veloso-Junior et al., 2009). In most while Pinon et al. (2009) reported 32.60 cm fish species including L. guttatus (Sarabia- total length at first maturity for the female Mendez et al., 2010) and O. chrysurus yellowtail snapper, L. argentiventris, from

(Trejo- Martínez et al., 2011), the IH has an the Southwest Gulf of California. Different inverse relationship with the gonadosomatic studies identified a minimum length of 25.45 index when a species has a definite spawning cm TL in female L. peru as first sexual maturity season. This is because the process of gonad for female in the state of Michoacan, but in development requires energy which is usually the State of Guerrero, higher values were drawn from the body reserves or visceral calculated (Gallardo-Cabello et al., 2010). tissues such as the liver (Wootton, 1998; Sexual maturity of L. jocu in the Abrolhos

Ekanem et al., 2004). A higher IG value is an Bank is attained at about 32 cm for females and indication of increased reproductive activity; 34 cm for males (Freitas et al., 2011), similar it shows that the gonads are developing and to conspecifics from the Caribbean. Also, increase feeding activity (Tyler and Dunn, similar values ranging between 29–31.50 cm K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 3 were calculated for L. guttatus from Mexico Nigeria and in the Gulf of Guinea. In addition, and Costa Rica (Sarabia-Mendez et al., 2010). there is no published data on any aspects of Teixeira et al. (2010) reported minimum the species’ reproductive biology in the entire maturity length of 28 cm fork length (FL) in Gulf of Guinea and little is known of the females and 35 cm FL in males of L. analis, recruitment and exploitation status. Therefore, respectively, while in L. alexandrei, the size of based on the general life-history traits of first sexual maturity was estimated at 17.1 cm snappers, it may be particularly vulnerable standard length (SL) for females and 16.8 cm to fishing and in need of information for SL for males (Fernandes et al., 2012). management. Hence, this study aims to Along the West African coast in the Gulf contribute basic knowledge on its reproductive of Guinea, four of six naturally occurring traits like gonadal development, spawning Lutjanid species widely distributed between pattern and season, length at first maturity Senegal and the Congo are morphologically which will be used for fishery management distinguished as red snappers. The Gorean and future artificial reproduction study in the snapper, Lutjanus goreensis is a red, medium study region. to large and deep-bodied species (over 350 mm TL) (Martinez-Andrade, 2003), common Materials and Methods to 50 cm but capable of attaining maximum Study Area total length of 80 cm (Allen, 1985) and easily The fishing grounds of Lagos coastal waters distinguished from co-existing species by a extend approximately from 6° 24’ 54’’ - 6° 25’ characteristic blue stripe or narrow blue band 30’’ N and 3° 23’ 06 - 3° 23’ 06’’ E covering or row of broken spots below the eye (Fisher the Nigerian – Benin Republic Border in the et al., 1981; Allen, 1985). The species is a West and to Lekki in the East. To the North, demersal fish of the subthermocline Lutjanid it is bounded by Five Cowrie Creek and to community in the Gulf of Guinea (Longhurst, the South by the vast Atlantic Ocean (Ediang 1969; Ssentongo et al., 1986). Adults are and Ediang, 2013). Prior to promulgation of marine forms inhabiting sandy, rocky or coral the 1971 Sea Fisheries Regulations, this area areas (Allen, 1985; Newman, 1995) while supported almost all of the industrial fishing juveniles are classified as estuarine-dependent activities in Nigeria in the 1960’s, which led (Martinez-Andrade, 2003). to the collapse of the fishery. The Lagos coast Snappers are among large-sized fish species is a narrow coastal shelf which lies between over-exploited in Nigerian inshore waters 14,816 km and 27,780 km with a total area of (Amiengheme, 1999). Red species of Lutjanus 41,000 km2 (Adebiyi, 2012). The continental are among the most appreciated fish species shelf is relatively narrow about 15 km and in regional and international markets due predominantly soft and muddy (Tobor, 1991). to their excellent flesh quality as food fish There is a range of clean sand in the turbulent (Blaber et al., 2005; Zhang et al., 2006; Fry waters behind the Lagos Harbour through a et al. 2009; Sustainable Fisheries Partnership, narrow belt of fine sand and clay in the quiet 2009). However, there is no major study for waters offshore (Ugwumba, 1984). Off Lekki, L. goreensis as substantial gaps exist for both there are rock outcrops and a sunken vessel systematic and biological information in at 15–20m. Bottom deposits consist primarily 4 West African Journal of Applied Ecology, vol. 27(1), 2019 of hard rock substrate (Wilson, 1983). Dead (whole body weight, to the nearest 0.1 g) with Holocene coral banks interrupt the middle an electronic balance (Mettler 400 PM). Each to outer continental shelf East and West of fish specimen was cut open and sex noted by Lagos (Awosika, 1990) and precisely around visual examination of the gonads. Both gonads Longitude 3° 55′ 00″ E and Latitude 6° 10′ and liver were removed from each specimen 99″N, the largest of the three major submarine and their wet weights weighed to the nearest canyons (the Avon deeps) also interrupts the 0.01 g. shelf (Awosika, 2008). Most demersal fish stocks off the Lagos Coast are concentrated in Sex Ratio an area of about 1,800 km2 which is located The proportion of the two sexes relative to one between the highwater mark on the shore and another was used to calculate the sex ratio and lower limit of the thermocline (Ssentongo et also to infer the mating system. al., 1986). Fishing season along the Nigerian coastline is affected by the eastward flowing Macroscopic Gonadal Staging warm Guinea current; oceanic fronts which Classification of ovaries and testes ona alter the characteristics of surface water macroscopic scale of gonadal development within a short period (a few days); southwest was initially accomplished according to monsoon, the equatorial undercurrent or south colour, texture, vascular irrigation and equatorial (Lomonosov current), the Benguela relative occupation in abdominal cavity. The and the Canary currents and possible extension classification was based on 5 maturity stages: of the coastal upwelling phenomenon to the immature, maturing (including recovery), coastal sector of the Bights of Benin and ripening, ripe and spent modified after Biafra (Ssentongo et al., 1986). gonadal staging of the mangrove snapper, L. argentimaculatus (Russell et al., 2003); black Sample and data collection spot or dory snapper, L. fulviflamma (Kaunda- Samples of L. goreensis were purchased Arara and Ntiba, 1997; Grandcourt et al., fortnightly from commercial catches of 2006). Newer and simplified terminologies licensed trawlers (cod-end with maximum for classifying gonad maturity phases adapted stretch mesh size of 76 mm), and also from after macroscopic criteria (Brown–Peterson artisanal fishermen using hook and line et al., 2011) corresponding to developmental operating in the marine coastal waters of stages I-V were incorporated into the study. Lagos from December 2008 to December 2010. The fish samples were transported in Estimation of size at first maturity a cooler packed with ice to the laboratory This is considered to be the length at onset where they were immediately analyzed fresh of its sexual maturity. For this analysis, fish or preserved in a deep freezer for examination. identified by macroscopic gonad stages II-V Frozen specimens were sufficiently thawed were used, because females can be considered and wiped to remove excess moisture. to be ‘‘sexually mature’’ or reaching maturity Samples were measured (total length, TL to from the ovarian stage II onwards or males the nearest 0.1 cm) using the traditional one- reach spermatogenesis (stage II) onwards meter fish measuring board, and weighed (Núñez and Duponchelle, 2009). The length K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 5 at which 50% of fish attain maturity or size Statistical analyses at first reproduction 50 (L ) was estimated by Data were analyzed using the IBM SPSS plotting the total length against distribution of statistical package (Version 20.0) and percentage cumulative frequency of DV/RT Microsoft Excel 2007 software. Data were (Stage II) and more advanced stages fish in the expressed as mean ± standard error of various size of 2 cm group classes (Russell et mean (SE). The sex ratio was tested for any al., 2003; Bhendarkar et al., 2013). deviation from the expected 1:1 ratio by using Chi Square analysis. A significance level of p Spawning Seasonality and Pattern < 0.05 was considered in the analysis. The timing and frequency of spawning were established by counting and estimating Results percentage of the proportion of sexually Sex Ratio mature fish in each reproductive phase and Sexes were best distinguished by dissection also the mean indices: gonadosomatic index of the gonads. A total of 189 male and 188

(IG), hepatosomatic index (IH) and the relative female L. goreensis were identified and condition factor (Krel) by month against the examined. Males ranged in total length and sample period. Changes in monthly IH was used body weight from 21.90 to 56.10 cm TL with as a proxy to study dynamics of lipid reserves a mean of 32.30 cm TL (SE ± 0.48) and 156.0 accumulation and depletion. Complemented to 2975.0 g with a mean of 622.83 g (SE ± with IG and Krel, it was used to assess role in 31.52), respectively. Females ranged in total gonad maturation. length and body weight from 22.60 to 47.60 cm TL with a mean of 33.47 cm TL (SE ±

Gonadosomatic Index (IG) 0.41) and 200.0 to 2000.0 g with a mean of

Temporal variation in the IG in all sexually 669.93 g (SE ± 26.15), respectively. Overall mature specimens was calculated using the sex ratio of male : female was balanced at 1.01 formula by Trejo-Martínez et al. (2011): : 1 (Chi- Square X2= 0. 003, d.f. = 1, n = 377, -1 IG = 100 · Mg · MG p >0.05) and did not differ significantly from Where: Mg is the gonad weight and MG is the the expected 1:1 ratio. body weight, both in grams.

Hepatosomatic Index (IH) Macroscopic Gonad Maturity Staging in L.

Similarly, temporal variation in the IH in all goreensis sexually mature specimens was calculated In the present study, five stages of gonadal using the formula by Trejo-Martinez et al. development were identified in male and (2011): female L. goreensis. The stages ranged -1 IH = 100 · ML · MG , from immature (IM); Developing (DV)/

Where: ML is the liver weight and MG is the Regenerating (RT); Spawning Capable (SC); body weight. Actively Spawning (AS) and Regressing (RG).

Relative Condition Factor, Krel for each Major macroscopic characteristic features of fish was calculated according to Le Cren’s each reproductive phase of ovaries and testes equation (1951): are shown in Table 1. Fish in all reproductive b Kn l= MG / a TL phases were found occurring throughout 6 West African Journal of Applied Ecology, vol. 27(1), 2019 the study period. In both sexes, there was Occurrence of adipose fats was most in IM lack of population synchrony in gonadal fish and least in SC specimens. Adipose fats development, that is, not all the breeders were also distributed among other parts such showed the same gonadal stage maturity as the stomach. in a month. IM and DV/RT fish were most predominant. Distinguishing between RT and Estimation of Size at First Maturity DV fish was difficult hence their synonymous Based on a 5-stage macroscopic scale, only classification under one phase. Individuals IM fish were excluded from the estimations of with ripe - running ovaries were not observed the maturity ogives while other reproductive

TABLE 1 Macroscopic characteristics used to describe the gonadal maturity stages of L. goreensis modified after Kaunda-Arara and Ntiba (1997), Russell et al. (2003) and Grandcourt et al. (2006) Maturity New Old Males Females Stage Terminology Terminology Stage I Immature (IM): Juvenile/ Testes appear as two long, Cylindrical, translucent, corresponds to a immature thin grayish – white or semi- slightly pink or glassy never-spawned transparent strings with fats ovary with a rounded end in fish attached to gonads. appearance. Fats attached to gonads Stage II Developing/ Maturing Testes showing increase in Increased size from Stage I. Regenerating virgin/resting/ size from Stage I. Grayish – Ovaries are compact, creamy (DV/RG): recovering white, opaque and strap-like yellow to light orange, well corresponds spent with thin lateral edges. No vascularized with small cream to fish going milt is expressed when cut. coloured eggs. Fats may be to finalize their Fats attached to gonads. attached to gonads. Ovaries of maturation by recovering spent individuals the forthcoming are soft, flattened and flabby to spawning season touch. Stage III Spawning Mature/ Creamy or white testes with Large orange coloured ovaries capable (SC): ripening wave-like lateral edges; milt with dense network of blood SC fish are is expressed when cut but not capillaries visible internally. developmentally free flowing.. Little or no fats Unovulated hyaline (clear) and may be attached to gonads. oocytes not free running. Little physiologically or no fats may be attached to able to spawn gonads. Stage IV Actively Ripe Testes are large, white with Ovaries are distended and spawning (AS): rounded lateral edges; milt fill most of the body cavity; corresponds on freely flowing when cut. Hyaline oocytes free running, spawning fish expressed when pressed. Stage V Regressing (RT): Spent Testes are flaccid, smaller Ovaries are flaccid, elongated fish in which in size from Stage IV and and appear bruised or dark in spawning has have a dark brown bruised colour. Few residual eggs may ceased appearance. A very small be present. amount of residual milt may be present when squeezed. and very few RG male and female individuals phases from the second to the fifth were were observed. Paired lobes of the testes considered. As a result, 119 males and 139 and ovaries were symmetrical with adipose females were considered as sexually mature. fats usually attached in IM to SC fishes. The L50 for males and females were roughly K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 7 equal. L50 for males was 34.21 cm while phase, 0.8% in AS phase and 5.9% in the RS that for females was 34.61 cm (Figure 1). phase. Males in SC phase did not occur in June Minimum sizes at maturity were 25.30 cm but were most abundant in February (53.8%), TL and 24.20 cm TL for males and females, April (36.4%), and July to October (33.3 – respectively (Figure 2). Largest male and 66.7%). The only male in the AS phase was female with maturing gonads were 56.10 cm present in August (12.5%). With the exception TL and 47.60 cm TL, respectively. of January, few males (7.1 – 14.3%) in RS

Figure 1 Size at first sexual maturity for 119 maleL. goreensis

Figure 2 Size at first sexual maturity for 139 femaleL.goreensis

Spawning Seasonality and Pattern in male L. phase were recorded from December to May goreensis and also occurred in September (8.3%). During the study period, 119 males were The proportion of mean somatic weight devoted identified as sexually mature. Males in DV/ to gonads was low (< 0.5) in all months. The

RG phases were found all year round and gonadosomatic index (IG) ranged from 0.04% consisted 64.7% of the gonads (Figure 3). to 1.87% while mean IG was 0.21%. There Advanced gonadal stages in SC to RT phases appeared to be a direct relationship between accounted for the remaining proportion the occurrence of individuals in SC phase and

(35.3%) and consisted of 28.6% in the SC high mean values IG in February (0.37%), May 8 West African Journal of Applied Ecology, vol. 27(1), 2019

(0.25%), July (0.26%) and August (0.27%). lowest in June (0.80%), rose to its peak in

Also, there was correlation between mean IG July (1.17%), declined in September (0.99%) and mean IH from February to May, although and maintained a uniform trend till November mean IH appeared to lag behind those of IG. (1.03%). From December to June, Krel showed

In contrast to mean IG, mean IH increased at inverse relationships with IH and with also IG a faster rate from May to August. Highest between March and May. However between monthly values of IH were observed in August June and November, it showed a parallel trend

(0.95%), January (0.92%) and July (0.91%). with IG and IH.

Lowest mean values of IG and IH were observed from March to April and in November. Though Spawning Seasonality and Pattern in female mean IG values were also low in January and L. goreensis

May their mean IH values were contrastingly A total of 139 females were sexually mature high (Figure 4). Mean Krel was dome - shaped, of which approximately 66.9% were in DV indicating relative stability with marginal / RT phases during the study period (Figure increments between January and June. Krel 5). Sexually mature females in the DV or RT appeared relatively stable between March phases were most abundant (66.9%) all year (1.01%) and May (1.00%). However, it was round with the highest percentages observed

Figure 3 Monthly trend of reproductive phases (macroscopic stages II –V) in 119 male L.goreensis

Figure 4 Mean monthly trends in IG, IH and Krel in 119 male L. goreensis K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 9

between January and April. Females in SC May. Initially, mean IG exhibited a slower pace to RG phases presented a lower proportion than the corresponding mean IH (Figure 6). of 33.1% of gonadal stages. Females in SC Thereafter, the relationship appeared inverse phase were most abundant in May (33.3%), when mean IH appeared to lag behind mean IG

July (38.5%), August (41.7%), October till September. Mean IG peaked in December (50.0%) and November (60.0%). The only (1.37%), June (1.34%), August (1.34%), four females in AS phase coincided with October (1.88%) and November (2.41%). IH mean high GSI in December (1.37 %), June peaked in December (0.95%), July (1.03%) (1.34%), July ( ̴̴̴1.00%) and a lower GSI in and increased through October (0.97%) to May (0.85%). Also, very few females in the November (0.99%). Lowest mean values of

RG phase were recorded in December ( 6.2% IG and IH occurred simultaneously between ), January (7.1%) , March (6.2%) and August March (0.56%; 0.73%) and April (0.53%; (16.7%). 0.65%), respectively. Low mean values of

IG ranged from 0.04% to 4.42% while mean IG IG were also observed in January (0.59 %), was 0.96%. Highest individual IG values were February (0.61%) and September (0.74%)

4.42 % in November, 4.15% in June and 4.11% while a low mean IH was recorded in June

December. Mean IG and mean IH followed (0.77 %) in contrast to a high mean IG (1.34%). similar parallel trend between December and Krel appeared relatively stable throughout

Figure 5 Monthly trend of reproductive phases (macroscopic stages II –V) in 139 female L.goreensi

Figure 6: Mean monthly trends in IG, IH and Krel in 139 female L. goreensis 10 West African Journal of Applied Ecology, vol. 27(1), 2019 the period of study showing slight increases snappers convey different interpretations which were barely discernible in June and of mating systems and also could provide

August. With respect to both IG and IH, Krel anecdotal evidence of spawning aggregations showed similar temporal trend from January offshore. Thus, on the basis of maximum to April with IG and beyond June with IH. size compositions of many species in sub- family Lutjaninae, the Gorean snapper can be Discussion classified as a medium to large snapper with maximum total lengths (TL) of 35.0 cm. Size Sexual differentiation, size distribution by sex distribution data from the present study showed and sex ratio that approximately 31.6% of the specimens In this study, secondary sexual characters were above 35 cm TL. Furthermore, in the which suggest sexual dimorphism and enable Gulf of Guinea, this species is common to 50 identification of sexes were not observed. cm TL and is capable of attaining a size of Hence, sexes were differentiated into males 80 cm (Allen, 1985). Therefore, the sex ratio and females by primary sexual characters. observed in the Gorean snapper is indicative of Absence of sexual dimorphism is not such monogamous pairing systems. Fernandes uncommon in snappers except in 2 species et al. (2012) reported paired sex ratios in large of genus Pristipomoides from the Indo-West lutjanids as suggestive of such monogamy Pacific (Grimes, 1987). Examination of gonads systems. showed that specimens of L. goreensis sampled Although there has been no published report are sexually dioecious and gonochorists. of spawning aggregation in L. goreensis, the Gonochorism is a characteristic of snappers paired sex ratio presented in this study is a (Grimes, 1987) attributed to factors such as strong indication of spawning aggregation. To similar sizes of sexual maturation of the sexes buttress this hypothesis, Martinez–Andrade and absence of individuals undergoing sexual (2003) posited that large lutjanids migrate transition (Domeier et al., 1996). offshore during the spawning season. Domeier L. goreensis presented a sex ratio which did et al. (1996) opined spawning migration of not differ from unity, meaning that there was snapper species from inshore to offshore to no statistical difference in the number of males be a strategy to increase the survival of the and females. There are several interpretation offspring. They suggested that spawning for the unity sex ratio observed in the species, migration of snappers to be borne out of the which can suggest monogamous mating need for more spatial and nutritional resources systems. Secondly, it is the ratio expected to survive than smaller fish, in order to for species in the family Lutjanidae (Texeira overcome the difficulty of finding mates during et al., 2010). Thirdly, a unity sex ratio is the spawning season as a result of increased associated with gonochorism and also being space. Therefore in view of this, large sexually sexually dioecious (Allen, 1985; Sadovy and mature L. goreensis may aggregate to spawn. Shapiro, 1987; Grandcourt et al., 2006; Trejo- Carter and Perrine (1994); Domeier and Martínez et al., 2012) and this was proven Colin (1997) also stated paired sex ratio as from examination of the gonads. Fourthly, common in snapper species which spawn size distributions coupled with sex ratios in in offshore aggregation. Caveriviere (1996) K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 11 reported spawning aggregations of 2500 To corroborate this view, Kaunda-Arara and large African red snappers (L. agennes), Ntiba (1997) did not find any fish in the RS caught accidentally by tuna purse seiners phase or spent condition in their samples of L. in surface waters off the Guinea Gulf coast fulviflamma. on western Africa. The African red snapper In this study, the occurrence of adipose fats is a congeneric or sympatric species to the attached to gonads in the Gorean snapper had Gorean snapper, L. goreensis in the Gulf of been previously reported in L. campechanus, Guinea with striking similarities in common L . argentimaculatus, Lutjanus carponotatus, and maximum sizes observed. Therefore, this L. griseus and L. fulviflamma (Collins et al., portends that the two snapper species may 1996; Domeier et al., 1996; Russell et al., also exhibit similar reproductive behaviours 2003; Kritzer, 2004; Kamukuru and Mgaya, inclusive of migration, and also supports the 2004). They were also observed attached to the postulation that the Gorean snapper forms stomachs. Adipose fats in these fishes could spawning aggregations. imply that they are used for gametogenesis and spawning of sexually mature fish during Macroscopic Gonadal Staging the spawning season (Domeier et al., 1996; Females with small, glassy ovaries and those Kamukuru and Mgaya, 2004). Declining with slightly bigger, pinkish ovaries were amounts of adipose fats noted in specimens categorized as sexually immature. This is of L. goreensis from IM to SC phases most a classic instance of continuous gonadal probably indicate progressive mobilization development and the artificial nature of gonadal of stored energy reserves primarily lipids staging in fishes (King, 2007). A lack of to support a gradual increase in gonad population synchrony in gonadal development development and maturation. Therefore, this was observed in both sexes. This was also also suggests that the species relies on stored noted in L. argentiventris where possibly energy reserves, one of which is the adipose individuals breed at different times of the year fat to develop gonads. with the consequence of gonads with different macroscopic stages and varied gonad weights Estimation of Size at First Maturity which could result in significant differences in In both sexes, fishes macroscopically classified the values of gonadosomatic index (Bonilla- as DV/RT(developing/ recovering spent), SC Gomez et al., 2013). Trejo–Martínez et al. (ripening), AS (ripe) and RS (spent) according (2011) also noted that the occurrence of RG/ to schemes of Kaunda-Arara and Ntiba (1997); DV fish year - round suggested that females Russell et al., (2003) and Grandcourt et al., did not mature synchronously. The occurrence (2006) were treated as sexually mature adults. of very few female L. goreensis in the RS L. goreensis attains a maximum size of 80 phase were probably because an individual cm TL in the Gulf of Guinea (Allen, 1985) fish would quickly release its eggs in several while mean sizes at first sexual maturity in the batches at the end of which the ovary quickly study were estimated at 34.61 TL and 34.21 recovers to regenerating stage. According to cm TL for females and males, respectively. Macer (1974), spawning process in fish is rapid Populations and species associated with which can obscure certain maturity stages. continents mature at a relatively smaller 12 West African Journal of Applied Ecology, vol. 27(1), 2019 size (43% of maximum length) than those August break. Presence of high number of SC associated with islands (51%), while deep- males and females for most part of the year water species and populations mature at a indicated possibility of year-round spawning. significantly higher percentage of maximum Fish of both sexes in the AS phases observed size (49%) than shallow-water species (43%) in December, May to August/ September (Allen, 1985; Martinez-Andrade, 2003; suggested that a period of peak spawning took Fernandes et al., 2012). Consequently, this place between May and August. sampled population of L. goreensis attained Tropical species spawn almost continuously sexual maturity at ̴ approximately 43% of the because longevity of the reproductive period reported maximum size. Hence, L. goreensis shortens with increasing latitude (Miller and in this study conformed to the sexual maturity Kendall 2009). Several previous studies have pattern observed for populations and species demonstrated that gonadal development and/ associated with a continental margin and or spawning for lutjanid species occurs over shallow - water, i.e. they matured at a smaller a period of several months (Nanami et al., size than island populations and deep - water 2010). Over time, reproductive cycles and species. time of spawning in marine fishes have been The minimum sizes of mature fish individuals studied by macroscoping staging of gonads in this study indicated that coastal samples and the relative size or weight of gonads could attain sexual maturity at sizes as low as (King, 2007). In Rhomboplites aurorubens, 25 cm TL. Sexual maturity has been reported to fish with gonads in all reproductive phases or occur from this length in some snapper species stages of development from mature to spent such as L. argentiventris, L. griseus, and L. (i.e. SC to RS) throughout the year indicated apodus of marine habitats (Aburto-Oropeza et year-round spawning while increase in al., 2009; Jaxion-Harm et al,. 2012) in contrast frequency of spawning (AS ) fish during some to individuals from estuarine environments months suggested peak period of spawning which are sexually immature and remain as (Manickhand- Heilemann and Phillip, 1999). functional juveniles regardless of the size they This aligns with the view that spawning for attain in the estuarine environments (Sheaves, some tropical snappers may take year round 1995). (Thresher, 1984).

Mean monthly IG values of 0.5 or more Spawning Seasonality throughout the year suggested that oocytes in Spawning season in L. goreensis was identified ovaries of L. goreensis were being continuously by mean IG and maturity stage or reproductive recruited in preparation for maturation and phase frequencies rather than by mean IH and spawning. In many asynchronous spawners, mean Krel. The season extended year round the gonadosomatic index of a mature or SC with multiple spawning peaks reflected by high female is not very high because the ovary mean IG in December, February, May/June, contains eggs in various states of maturity.

August/September, October and November. Mean IG values above 0.5 in the red snapper, Spawning pattern showed a peak in the early L. campechanus from the Gulf of Mexico part of the year coinciding with the dry season; corresponded approximately to the onset of in the major rainy season and during the short vitellogenesis (Fitzhugh et al., 2004). Hence, K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 13 the species investigated in this study is greater food production for early life stages. indicated to have a protracted spawning season Monthly variations of gonadosomatic index provided the process of oocyte maturation is in Serra Spanish mackerel also showed that not interrupted and leads to skipped spawning. peak breeding coincided with rainy season

In L. goreensis, IG values were low in females and possibly better environmental conditions and even lower (less than 0.5%) in males. Low (Chellappa et al., 2010). In tropical regions,

IG of less than 0.5% have been reported in rainfall plays an important role in determining brown meagre male (Grau et al., 2009). Lower the reproductive cycles of fishes and collective

IG values in males suggests that energy invested reproduction occurs during the time when for gamete production or spermatogenesis is environmental conditions are favorable for the probably less than that invested by females survival of juveniles and when adequate food which could be due to physiological and is available, besides protection from predators hormone effects on the gonadal development (Grimes, 1987). These periods are coincident of fish (Abdallah et al., 2013). Similarly, in L. for some lutjanids that inhabit continental and fulviflamma, ovaries were heavier than testes large islands (Andrade-Rodriguez, 2003). in gonad maturity stages II-V or DV to RS Collins et al. (1996) estimated the peak of phases (Kaunda-Arara and Ntiba, 1997). gonadosomatic index in red snapper (L. Mature eggs were found in the ovaries of campechenus) to be in June with less peaks female red snapper, when IG was 1 or more in July and August. In L. fulviflamma from in the northern Gulf of Mexico from May to Kenyan inshore marine waters, a prolonged September (Phelps et al., 2009). Similarly in period of weight loss in gonads or decline the present study, mean IG values of 1 or more in gonadosomatic index from a peak in recorded in December, June, August, October November/December to April/ May, indicated and November indicated that there were an extended spawning period during which mature eggs in the ovaries of the female L. several batches of eggs and sperm were goreensis and spawning imminent. Although released (Kaunda–Arara and Ntiba, 1997).

IG in December was high, occurrence of higher Grandscourt et al. (2005) estimated a spawning mean IG and peaks in IG in the second half of the season from highest values of gonadosomatic year from May- August connotes that a peak index for Lutjanus fulviflamma in the southern breeding season occurs during the heavy rains Arabian Gulf to be in May to September and possibly better environmental conditions. while a shorter season from April to July was Between 2008 and 2010, peak precipitation determined from maturity stage frequencies. months (>200 mm) for the Lagos Marine Area In L. peru, the main spawning period occurred were between May and October while the peak during August, and a second period during months for higher values of gonadosomatic February corresponding with the highest index were December and from May to values of the gonadosomatic index (Gallardo- August. The latter months appear to be linked Cabello et al., 2010). Based on gonadosomatic to maximum rainfall and minimum water index and the presence of gonad macroscopic temperatures during times of increased river stages 3 and 4 females, the reproductive flood in the rainy season leading to increased season for L. argentiventris spanned March to productivity in surface waters supporting July with a peak in activity during April-June 14 West African Journal of Applied Ecology, vol. 27(1), 2019

(Garcia-Contreras et al., 2009). In L. griseus, IG and Krel between January and May can be spawning began in late May and continued interpreted as a period of depletion in energy into early September (Domeier et al., 1996). reserves primarily proteins and lipids from the liver towards ovarian growth and maturation. Dynamics of lipid reserve storage and interplay Reproductive activity in females was low of Hepatosomatic Index (IH), Gonadosomatic between January and April and high between

Index (IG) and Relative Condition Factor (Krel) May and August; November/December as in gonad maturation. indicated by the values of IG. From June, there Liver and muscles are main organs responsible was a buildup of energy reserves in the liver for lipid reserve storage (Abdallah et al., which peaked in July followed by mobilization 2013). However in L. goreensis lipid reserves of the reserves to the ovaries for vitellogenesis were distributed among other parts such as till September. Vitellogenesis is linked to the gonads and stomach besides the liver. liver size as the precursors of the yolk are Similarly, the occurrence of more than one synthesized in the liver (Albieri et al., 2010) lipid reservoir was also reported in demersal and the liver might enlarge during the female fishes such as brown meagre, Sciaena umbra reproductive season in response to vitellogenin and the red drum, Sciaenops ocellatus (Craig needs (Plaza et al., 2007). Increase in storage et al., 2000). of energy reserve in liver was repeated during

IG and IH displayed similar temporal trends another period of high reproductive activity which were not inversely related and such from October to November/December. patterns have been observed in L. peru Fish species differ in their ways of utilizing (Gallardo-Cabello et al., 2010) and in L. food reserves in reproduction and generally argentiventris (Pinon et al., 2009). The gonad development in many fish lead to combined increase in Krel, IH, and IG from June a high drain of energy from other tissues to August suggested that increased feeding such as the liver in the case of L. goreensis activities could be a major source of energy in the present study. Similar trends in IH, primarily for testicular maturation during and IG were replaced by a divergence from peak spawning period. A positive correlation May to September during which the indices between IH and IG suggest that the liver reserves exhibited opposite trends and also a smaller may not be used in the final maturation stages divergence in December. The divergence

(Sousa et al., 2003). Decline in Krel, IH, and represents an inverse relationship between

IG from September to November may be the gonadosomatic index and hepatosomatic interpreted as increased mobilization of energy index suggesting a definite spawning season reserves to testes for maturation during low (Ekanem et al., 2004). Prior to reproduction, reproductive activity while feeding activities increase in liver weight is associated with also supply some of the energy needed for the synthesis of lipids and proteins necessary gonad maturation. Concomitant increases in for gonad development (Palazón-Fernández, the three indices have been reported in the 2007). Inverse relationship between IH, and female sciaenid, Menticirrhus littoralis in IG was also reported in Ocyurus chrysurus southern Brazil (Braun and Fontoura, 2004). (Trejo-Martínez et al., 2011) and in L. guttatus

In female of L. goreensis, the interplay of IH, (Sarabia-Méndez et al., 2010). K. A. Fakoya and M. A. Anetekhai: Reproductive seasonality in the Gorean snapper, Lutjanus goreensis 15

Maintenance of a constantly low Krel conformed more to the extended spawning during periods of decreased and increased pattern characteristics of insular species and reproductive activity may be explained by the population. Continental populations of L. fact that energy reserves are also drawn from campechanus from Campeche Bank (Brule fish muscles and there is some level of feeding et al., 2010) and Ocyurus chrysurus from activity to replenish the energy reserves. In Mexico (Trejo-Martínez et al., 2011) also many fish species, minimal values in condition exhibited continuous year-round spawning, factor during spawning season are interpreted typical of insular species and populations. as the result of mobilization of somatic Observations on the protracted spawning energy reserves needed for reproductive pattern throughout the year may be as a development and energy in spawned fish, consequence of: (i) individuals of both sexes influenced by reduced feeding (Zin et al., had gonads at different macroscopic stages 2011). Development of gonads limits the size and varied gonad weights indicating lack of of the digestive tract which in turn limits fish population synchrony in gonadal development feeding (Valinassab et al., 2011). Therefore, during the study period which is suggestive of condition of the sexually mature fish might a multiple spawning species and (ii) longer be little influenced by reproductive effort warmer season in the equatorial region than even in the peak of spawning period; on the at higher latitudes. Protracted seasons are other hand, there may be little interpretation typical of tropical regions because of duration of Krel on reproduction because sampled fish of suitable temperatures and food availability were at various phases of the reproductive for survival of juveniles (Schaefer, 1987). For cycle. In both sexes, coincidence of very coastal lutjanids in northeastern of Brazil, low mean IG and IH from March to April and all year round warm water and increment in implied a resting period or period of very low richness from estuaries on food web appeared reproduction. A resting period of March - May to account for a long spawning season, like was also noted in the vermillion snapper, insular populations (Fernandes et al., 2012). Rhomboplites aurorubens in Trinidad and The Nigerian coast is basically warm with Tobago (Manickchand-Heileman and Phillip, temperature generally greater than 24oC. 1999). Therefore it is not impossible that being in the tropics, the rather long spawning period of Spawning Pattern L. goreensis may be caused by the prevalent The population in this study consisted of warm temperatures of more than 20oC. a coastal/marine species associated with L. goreensis showed continuous reproduction continental Nigeria. Snapper species exhibit throughout the year, particularly at higher protracted spawning seasons during summer intensity during the heavy rains (May to while insular populations tend to reproduce September). The species is a multiple spawner throughout the year (Grandcourt et al., with a protracted spawning season as evinced 2006; Fernandes et al., 2012). The spawning from asynchronous gonadal development. season of L. goreensis was however longer Findings could imply continuous recruitment than the restricted season expected of a into fishery. However to ensure optimal continental population of lutjanids and exploitation, minimum capture size has to 16 West African Journal of Applied Ecology, vol. 27(1), 2019 be increased above sizes at sexual maturity planning meeting of fisheries scientists calculated in this study. on Nationally Co-coordinating Resource Programme (NCRP) of the National Acknowledgments Agricultural Research Programmes (NCRP) The authors thank the Fisheries Laboratory of the National Agricultural Research Division of the Department of Fisheries Project (NARP). 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