Abstract.-The spawning seasonality, fecundity, and daily Reproductive biology and egg production of three species of short-lived c1upeids, the sardine egg production of three species of Amblygaster sirm, the herring Herklotsichthys quadrimaculatus, Clupeidae from Kiribati, and the sprat Spratelloides delicatulus were examined in Kiribati to assess whether vari tropical central Pacific able recruitment was related to egg production. All species were David A. Milton multiple spawners, reproducing throughout the year. Periods of Stephen J. M. Blaber increased spawning activity were Nicholas J. F. Rawlinson not related to seasonal changes in (SIRO Division of Fisheries, Marine Laboratories, the physical environment. Spawn ing activity and fish fecundity P.O. Box J20. Cleveland, Queensland 4 J63. Australia were related to available energy reserves and, hence, food supply. The batch fecundity ofA. sirm and S. delicatulus also varied inversely with hydrated oocyte weight. The maximum reproductive life The sprat Spratelloides delicatulus, Changes in abundance may be span of each species was less than the herring Herklotsichthys quadri related to variable or irregular re nine months and averaged two to maculatus, and the sardine Ambly cruitment, because many clupeoids three months. Each species had a gaster sirm are the dominant tuna (especially clupeids and engraulids) similar spawning frequency of three to five days, but this varied baitfish species in the Republic of have little capacity to compensate more in A. sirm and S. delica Kiribati (Rawlinson et aI., 1992). for environmental variation during tulus. Amblygaster sirm had the All three species inhabit coral reef the period ofpeak spawning and egg highest fecundity and potential lagoons and adjacent waters. production (Cushing, 1967, 1971). lifetime egg production, but the Sprats school in shallow water Most clupeids, including some number of eggs produced per ki logram of fish was highest in the around reefs and adjacent seagrass tropical species, are multiple small sprat S. delicatulus. during the day. Herring also form spawners (Alheit, 1989). Multiple Monthly estimates of the daily dense schools in shallow water spawning should be advantageous egg production of each species along the shoreline and among for short-lived species because it varied with the proportion of the reefs during the day (Williams and enables them to maintain rela population that was spawning. Estimates of egg production Clarke, 1983). Unlike the other tively stable population sizes in showed little similarity to the fre species, sardines school near the unpredictable environments quency distribution of birthdates bottom ofthe lagoon during the day (Armstrong and Shelton, 1990). back-calculated from length-fre (Conand, 1988). All species disperse Multiple spawning has been estab quency samples. The distribution into the mid and upper waters of lished for few tropical clupeids of back-calculated birthdates con firmed that fish spawned in all the lagoon during the night to feed (e.g., Sardinella brasiliensis; Isaac months, but the proportion born and become available to the com Nahum et aI., 1988). Of the three each month varied widely from mercial fishery. major baitfish species in Kiribati, species to species and year to year. A major source of lost fishing only S. delicatulus has been shown The reproductive strategy of these time by pole-and-line vessels in to be a multiple-spawner (Milton species ensures that successful spawning is likely, and so the Kiribati has been irregular baitfish and Blaber, 1991). All three species level of recruitment is more de catches (MacInnes, 1990). These are subject to high natural mortal pendent on post-hatching survival important tuna baitfish species ity in Kiribati (Rawlinson et aI., rates than on egg production. have shown large seasonal and 1992), thus lifetime egg production interannual fluctuations in abun dance since they were first re corded during the 1940's (McCar 1 McCarthy, D. 1985. Fishery dynamics and 1 biology of the major wild baitfish species thy, 1985 ; Rawlinson et aI., 1992). particulary Spratelloides delicatulus, from Both A. sirm and H. quadrima Tarawa, Kiribati. Kiribati Fisheries Div., culatus disappear from baitfish Tarawa, Kiribati, 53 p. catches for variable periods and 2 Kiribati Fisheries Division. 1989. Fisher ies Division 1989 Annual Rep., Ministry Manuscript accepted 24 September 1993 can be absent for months or years of Natural Resources Development, Fishery Bulletin 92:102-121 (1994) (Kiribati Fisheries Division, 19892). Tarawa, Kiribati, 38 p.
102 Milton et al.: Reproductive biology and egg production of three species of Clupeidae 103 may be increased ifthey spawned multiple batches In this study, we examined the variability in re of eggs. productive biology of the three major baitfishes in Egg production of multiple spawning species de Kiribati to determine the influence of adult repro pends on reproductive life span, the time between ductive variability on subsequent recruitment. Our spawnings, and the age structure ofthe population objective was to test the hypothesis that reproduc (Parrish et al., 1986). Batch fecundity ofS. delica tive biology of short-lived clupeids is adapted to tulus varies widely between sites, both within and maintaining relatively stable population sizes. We between countries (Milton et aI., 1990). In a short determined potential life-time egg production and lived species such as S. delicatulus «5 months; whether estimated egg production is related to the Milton et aI., 1991), reproductive life span may have frequency distribution ofback-calculated birthdates. an important influence on potential lifetime egg production. Batch fecundity of H. quadrimaculatus does not Methods and materials appear to vary throughout its distribution, and ranges from 4,000 to 10,000 eggs (Marichamy, 1971; Study areas Hida and Uchiyama, 1977; Williams and Clarke, The Republic of Kiribati covers an area of 3 x 106 1983; Moussac and Poupon, 1986; Conand, 1988). km2 in the central Pacific ocean and comprises three Fish mature at about 90 mm in length at six months main island groups (Gilbert, Phoenix, and Line Is of age (Williams and Clarke, 1983), and they sur lands) (see Inset Fig. 1). The Gilbert Island group vive for at least one year (Milton et aI., 1993). Little is the most populated, consisting of 16 coral reef is known offecundity and egg production ofA. sirm. islands. All islands in the group have a typical ocean Fecundity of the species is related to length and platform coral reefstructure and have been built up weight, with a mean of 20,000 eggs per batch, and by sc1eractinian corals and coralline algae on a sub individuals probably spawn more than one batch of merged mountain (Gilmour and Colman, 19903). eggs (Conand, 1988). Most atolls consist ofsmall islets lying on the east Temperate clupeids vary widely in life-history ern side of a lagoon with an open western side due parameters (e.g., Clupea spp., Jennings and to the prevailing easterly winds. Most typically have Beverton, 1991). Food availability and environmen passages between the islets through which water is tal conditions affect the size and number of eggs of exchanged. Pacific herring (Clupea pallasi) (Hay and Brett, The four study sites (Abaiang, Butaritari, Tarawa, 1988). Results of studies of temperate clupeoids and Abemema) were typical ofislands in the Gilbert suggest that they do not spawn during periods of Island group; all had narrow islets on their south high food abundance, but store energy as fat for ern and eastern sides, except Abaiang (Fig. 1). La later reproductive activity (Hunter and Leong, 1981; goons were mainly shallow (20-30 m deep), often lIes, 1984). There are no similar studies of tropical with large areas of intertidal seagrass or sand on clupeids. Encrasicholina heterolobus, a tropical their eastern sides. Bottom topography ofthe deeper engraulid, does not deplete energy reserves in the parts ofthe lagoon was generally smooth, with some liver or soma during spawning (Wright, 1990). Fish coral outcrops. Our study sites were similar to those with higher condition factor (K) also had higher described by Hobson and Chess (1978) in the fecundity. Marshall Islands. Stored energy or fish condition that may influence both spawning frequency and batch fecundity have Environmental parameters a marked influence on egg production and, hence, affect subsequent recruitment (Ricker, 1954; On each sampling occasion, we measured the time Beverton and Holt, 1957). Adult reproductive varia of collection, sea surface temperature (OC), cloud tion should strongly influence recruitment in short cover (okters), wind direction and speed. and moon lived tropical species that have short larval phases phase because these factors may be related to and rapid growth. An example is S. delicatulus spawning or recruitment (Dalzell, 1985, 1987; which, in the Solomon Islands, live a maximum of Peterman and Bradford, 1987; Milton and Blaber, five months and mature at about two months ofage 1991). For each site, monthly rainfall data for 1989 (Milton and Blaber, 1991; Milton et aI., 1991). Amblygaster sirm and H. quadrimaculatus live less than two years (Milton et aI., 1993) and mature in 3 Gilmour, A. J., and R. Colman. 1990. Report on a consultancy on a pilot environmental study ofthe outer island development 6-12 months (Williams and Clarke, 1983; Conand, program, Republic of Kiribati. Graduate School ofthe Environ 1988). ment, Macquarie Univ., Australia, 151 p. 104 Fishery Bulletin 92(1/. 1994
and January 1989 from Tarawa. Fish were caught by several methods at each site. Most samples were collected ~ from the commercial tuna baitfish ~ Butaritari catches each month at each site. Supplementary samples were ob tained by beach-seining (H. quadrimaculatus and S. delicatulus), cast-netting (H. quadrimaculatus) in ~ shallow water during the day, or gill ~Abaiang Gilbert Is netting (25- and 38-mm stretched ~Tarawa mesh) at night near baitfishing opera tions. All fish were preserved in 70% ethanol.
~Abemama Reproductive biology ~c(J Laboratory st~dies All fish collected from commercial baitfish sampling were measured (standard length in millimetres), and a subsample of20 to 60 specimens weighed (±0.005 g). Go nads, otoliths, liver, and viscera were removed and the amount ofvisible fat subjectively estimated. Both ovaries from the first 20 females ofeach spe- o, 100, kms cies at each site for each month were 2°5 dried of surface moisture, weighed 110° llll"w (±0.001 g) and stored in 4% formalin seawater fo:r histology. Testes, ovaries ofother fish, liver, and the soma were dried at 60·C to a constant weight. Otoliths were used to estimate the age (in days) of each fish by methods AlIItralia outlined in Milton et a1. (1993). Addi tional samples offish caught by other Figure 1 methods were treated separately, but Map of Gilbert Islands, Kiribati showing the four study sites in a similar way. We report only on (Butaritari, Abaiang, Tarawa, and Abemama). Inset shows the ter results ofstudies offish collected from ritorial boundary of Kiribati, the Gilbert Islands, and their posi commercial samples unless otherwise tion in the Pacific. stated. For histological preparations, go- nads were embedded in paraffin, sec tioned at 9 mm, and stained with Ehrlich's and 1990 were obtained from the Kiribati Govern haemotoxylin and eosin (McManus and Mowry, ment Meteorological Division. 1964). Gonad maturation stages were defined follow ing Cyrus and Blaber (1984) and Hunter and Sampling Goldberg (1980), and were similar to those of Fifty to 1,000 Amblygaster sirm, Herklotsichthys Moussac and Poupon (1986) for H. quadrimaculatus quadrimaculatus, and Spratelloides delicatulus were from the Seychelles. We staged each gonad accord collected monthly at one or more of four sites in ing to the relative numbers ofcells at each develop Kiribati (Butaritari, Abaiang, Tarawa, and mental stage (Young et aI., 1987; Table 1), and the Abemama; Fig. 1) between August 1989 and May presence of any post-ovulatory follicles was noted. 1991. Additional samples of A. sirm and H. The percentage ofeach histological section that cor quadrimaculatus were collected in November 1988 responded to each developmental stage was subjec- Milton et al.: Reproductive biology and egg production of three species of Clupeidae 105
examine the fecundity of fish with any empty fol Table 1 licles. An advanced modal size group ofoocytes could Criteria used for staging female gonads of tropi be distinguished in ripe fish. We separated a cal clupeids stained with haematoxylin and eosin. subsample of between half (A. sirm) and all (8. delicatulus) of the ovary and weighed it. The num Stage Histology ber ofeggs in the advanced mode was counted and (1) Immature Chromatin nucleolar stage the fecundity was estimated by multiplying the prefollicle cells surround each number ofeggs in the subsample by the ratio oftotal oocyte gonad weight to subsample weight. Fecundity esti (2) Developing/resting Perinucleolar stage mates were made within three to four days after the uniform staining cytoplasm ovary was removed from the fish to minimize the (3) Maturing Yolk vesicle formation; some non-staining yolk (lipid) potential bias of differential absorption of fixative (4) Ripe Vitellogenic stage - red by oocytes and surrounding somatic tissue. staining yolk; developed We used hydrated oocytes from fish caught be chorion tween 2000 and 2330 hours to estimate egg weight. (5) Running ripe Globular red-staining yolk; Oocyte weights were estimated from hydrated 00 (spawning) oocytes hydrated; develop ment complete cytes in ovaries that were almost ready to spawn (6) Spent Presence of post-ovulatory (late Stage 5; Table 1). We measured oocyte dry follicles; cortical alveoli weight by counting 10 samples of 10 oocytes from present and/or atresian of each ovary, drying the oocytes at 50· C to a constant remaining ripe oocytes mass and weighing each subsample separately. We scored visceral fat on a five-point scale. If a fish had less than 25% of the intestine covered in tively estimated. Post-ovulatory follicles were aged fat deposits, it was scored as (1); 25-50%, (2); 50 according to stages found in other multiple-spawning 75%, (3); and 75-100%, (4). A fish scored (5) when clupeoids (Hunter and Goldberg, 1980; Goldberg et al., all intestine was covered with fat and deposits were 1984; Isaac-Nahum et al., 1988). Gonosomatic indices also present around the stomach (Nikolsky, 1963). (GSI) were calculated as the ratio ofwet gonad weight The proportion offemales examined histologically to somatic weight (total weight minus gonad weight), each month that had post-ovulatory follicles (POF; expressed as a percentage. Similarly, we calculated a Stage 6) was used to evaluate reproductive season hepatosomatic index (HSI) as the ratio of liver dry ality. We detennined that these fish had spawned weight to somatic dry weight (total weight minus en within the previous 15-48 hours, because these tire viscera), expressed as a percentage. structures decompose and cannot be recognised af Length and age at sexual maturity were defined ter that time (Hunter and Goldberg, 1980; Clarke, as the minimum size and age at which fish had ripe 1989). In samples where no fish had POF's, we used oocytes (Stage 4), detennined by histological exami the proportion of fish in the histological subsample nation. Fish that had running-ripe oocytes (Stage 5) whose sections had greater than 85% running-ripe were recorded as in spawning condition. We defined oocytes (Milton and Blaber, 1991). We used this the length and age at first spawning as the small proportion to calculate monthly estimates of mean est size where the proportion ofrunning-ripe oocytes daily oocyte production and the number ofbatches of in the section exceeded 85% for more than 50% of oocytes spawned each month (Parrish et aI., 1986). the fish of that length or age. We chose this crite We estimated daily oocyte production (nJkg of rion after examining large numbers of histological adults; egg production index) for samples collected sections with running-ripe oocytes. In these sections from commercial baitfishing, because these samples they always represented more than 85% of the sec were assumed to be most representative ofthe popu tion area. Our results were similar to that found in lation. Our methods were similar to those ofParker other tropical clupeoids (Milton and Blaber, 1991). (1980, 1985), which have been used to estimate the The reproductive life span ofthe population ofeach spawning biomass of a number of multiple spawn species at each site each month was determined ers (Armstrong et aI., 1988; Pauly and Palomeres, from the oldest fish (Milton et aI., 1993) in each 1989; Somerton, 1990). However, our methods dif sample minus the age at first spawning. fered because we used commercial catch per unit of We estimated batch fecundity for each species effort (CPUE) as an index of adult abundance. from fish that had been examined histologically and had oocytes that were starting to hydrate (ripe-early running ripe; Stages 4--5; Table 1), but we did not 106 Fishery Bulletin 92(1I. 1994
where f i is the proportion of females in the ith ofthe two approaches were compared. Ifthe variable length class, p is the proportion of the sample most related to fecundity in the stepwise regression spawning, Fi is the fecundity of a fish ofthat length was not the one most related to fecundity in the par taken from the fecundity-length regression, SRi is tial-eorrelation analysis, the stepwise regression model the sex-ratio of the ith length class and Wi is the was discarded and no relationship was assumed. total weight of fish in the ith sample. CPUE was In order to estimate egg production (Eq. 1), we estimated from the monthly catch returns of the estimated the proportion of females in each 5-mm commercial fleet. We chose this method of estimat length class from the total sample of each species. ing egg production because S. delicatulus have de The variance of these estimates was calculated by mersal eggs (Leis and Trnski, 1989) and the eggs of using the normal approximation to the binomial dis A. sirm and H. quadrimaculatus are difficult to tribution (Walpole, 1974). We assessed whether the sample adequately in the large areas of suitable monthly percentage of annual egg production was habitat in each lagoon. related to the proportion of annual recruitment in For comparison with adult spawning data, we the same month by rank-correlations (Conover, back-calculated the distribution ofbirthdates offish 1980). collected in each length-frequency sample by using The average age of the potential spawning popu the growth equations of Milton et a1. (1993). Fre lation in each sample was compared by a nested quencies in each age class were adjusted for mor analysis ofvariance with month ofsampling nested tality by using the estimates of Rawlinson et a1. within year. Significant differences between treat (1992). The distribution ofbirthdates was also back ments were identified from comparison ofthe least calculated for H. quadrimaculatus and S. delica squares means of each treatment, as sample sizes tulus length-frequency samples from previous stud differed between cells (Sokal and Rohlf, 1981). ies at one site (Tarawa) January 1976 to February 1977 (R. Cross, 19784) and May 1983 to April 1984 (McCarthy, 19851). We used age distribution in these Results earlier studies and those ofthe present study to ex amine seasonal, annual, and site-related differences Environmental parameters in the reproductive life span of each species. Sea-surface temperature in Kiribati varied little throughout the year. During the study period, tem Statistical analyses Inter- and intra-specific differ peratures varied between 29°C and 32°C (Table 2). ences in fat index, HSI and K were examined with Rainfall varied along the Gilbert Island group; rain Fisher's t-tests to account for unequal sample sizes. fall was higher in Butaritari than at the other sites. Seasonal and site-related differences in fecundity Some rain fell throughout the study period but was (expressed as oocytes per gram) were examined by more intense during 1990 at all sites. Rainfall dur analysis ofcovariance with weight as the covariate. ing 1989 was below the long-term average at all Hydrated oocyte weight and reproductive life span sites and was 16-50% that of 1990. The highest were examined by one-way analysis of variance. rainfall fell during the north-east monsoon (Decem We examined the relative influence of exogenous ber-April) at all sites. Winds were mostly light, and and endogenous factors on the fecundity of each varied in direction seasonally, blowing from the east species at each site by stepwise regression (Sokal during the monsoon, but from the south-south-west and Rohlf, 1981). We included the following: length, for the rest of the year (Table 2). weight, age, sea-surface temperature (OC), wind speed (in knots), moon phase (expressed by fitting Reproductive biology a sin/cosin curve to the number ofdays since the last full moon before the sample was taken divided by Maturation The length and age at first maturity the number of days in a lunar month (29.5) (Milton of A. sirm varied between sites (Table 3). Ambly and Blaber, 1991), fish condition (K: weightllength3), gaster sirm matured younger and smaller in Kiribati fat, and HSI(%). We retained only those variables than elsewhere. Length and age at first spawning that significantly improved the fit of the model were much greater than the length or age when fish (P<0.05). Because several of these variables were reached sexual maturity, but this size was similar correlated, we did a partial-correlation analysis be to that of fish from northern Australia (Table 3). tween these variables and fecundity, and the results Herklotsichthys quadrimaculatus matured and were capable of spawning at 70 mm length and 4 months
4 Cross, R. 1978. Fisheries research notes. Fisheries Division, of age (Table 3). The relative size and age at which Ministry of Commerce and Inductry, Tarawa, Kiribati, 58 p. fish matured (as a proportion ofmaximum size and Milton et al.; Reproductive biology and egg production of three species of C1upeidae 107 age) did not differ among fish from the four sites. In Kiribati, Table 2 S. delicatulus become sexually Mean water temperature rc I, wind speed (kn), cloud cover, and monthly mature at 40 mm and two rainfall (mm) at four sites in Kiribati from November 1988 to May 1991. months of age and spawn shortly afterwards. Compared Parameter Butaritari Abaiang Tarawa Abemama to the other species, the length Water temperature ('Cl 30.2 ± 0.3 30.2 ± 0.4 29.5 ± 0.1 29.9 ± 0.2 and age at maturity and first Range 28-32 27-33 29-30 29-31 spawning varied less among Wind speed (knl 2.2 ± 0.6 4.2 ± 0.9 5.4 ± 1.2 2.2 ± 0.2 sites (Table 3). The three spe Range 0-7 0-10 1-15 1-5 cies differed in the length and Prevailing direction East East East East age at sexual maturity and Cloud cover (okters) 2 ± 0.6 5 ± 0.6 3 ± 0.5 1 ± 0.4 first spawning. However, as a Range 0-6 1-7 0-7 0-4 proportion oftheir maxima, the Monthly rainfall (mm) (1945-88) 263 ± 35 181 ± 35 165 ± 35 128 ± 33 Range 7-908 0-761 0-824 0-728 three species were similiar (t Monthly rainfall 1989 (mm) 184 ± 29 42 ± 10 77 ± 23 36 ± 10 test; p>o.n All matured and Range 51-351 0-108 6--235 3-102 spawned at about 70% ofmaxi Monthly rainfall 1990 (mm) 404 ± 37 298 ± 51 202 ± 31 mum size and 50% of maxi Range 195-614 19-643 93-402 mum age (Table 3). Months sampled 14 12 18 13
Timing of spawning We iden- tified recent spawning by the presence of post-ovu lation spawned each month (Fig. 3). Female condi latory follicles in the ovaries. In A. sirm, follicles tion, fat index, and HSI all followed a similar pat were detected in samples collected between 0100 to tern during the study but did not appear to be di 1630 hours, and new post-ovulatory follicles (iden rectly related to spawning activity. Fish in spawn tified as day-O [<24 hr]; Hunter and Goldberg, 1980; ing condition had the highest HSI, fat, and condi Goldberg et aI., 1984) were observed in fish collected tion values, but these were only significantly greater between 0100 and 0510 hours. Female H. than those of spent fish (P<0.05; Table 4). quadrimaculatus with post-ovulatory follicles were Spratelloides delicatulus spawned almost continu collected between 2130 and 1630 hours and day-O ously throughout the study period but spawning follicles were found in samples collected between varied in intensity (Fig. 4). Peak spawning occurred 2130 to 0300 hours. In female H. quadrimaculatus during different periods in each of the years caught after 0300 hours, follicles could not be dis sampled. Female HSI and fat index showed a simi tinguished from day-1 type POF's, as the follicles de lar pattern during the study but monthly changes generated rapidly. Similarly, we detected post-ovu in these parameters or fish condition did not follow latory follicles in female S. delicatulus collected from the spawning cycle. We found no significant differ 2210 to 1930 hours, and follicles of all females col ences in HSI or fat index for females with ovaries lected earlier than 0845 hours were identified as in different stages of development (P>O.l; Table 4). day-O. Those in females of the single sample col Fish condition was lower among spent fish than in lected later in the day (1930) were assigned as day-I. ripe or spawning fish (P<0.05; Table 4). Females with ripe ovaries had higher mean HSI, fat, and Spawning season There was protracted spawning condition than those in other stages ofdevelopment, in A. sirm with periods of intense spawning activ but these differences were not significant (Table 4). ity (Fig. 2). During both 1989 and 1990, fish spawned August to October and also during May Fecundity The relative fecundity ofA. sirm and H. June in 1990. Condition, fat index, and HSI were quadrimaculatus did not differ among sites or sea less during spawning periods and reached a peak in sonally within sites in Kiribati (ANCOVA with March-April 1990, i.e., before spawning (Fig. 2). We weight as covariate; overall P>0.07; Table 5). How found less fat deposits in spent fish and the fish ever, the relative fecundity of H. quadrimaculatus were in poorer condition than fish with gonads in was significantly different between fish from Tarawa other stages of development (P<0.05; Table 4). We andAbemama (t-test;P<0.05). Batch fecundity ofboth noted no significant differences in HSI among fish species did not differ among sites in Kiribati. Within with gonads at the same stage of development. their respective species groups, both species had simi Herklotsichthys quadrimaculatus spawned lar batch fecundities to the other species listed, al throughout the study period: 20 to 50% ofthe popu- though their relative fecundities were lower (Table 5). lOB Fishery Bulletin 92(1 I. 1994
Table 3 Length and age at sexual maturity and first spawning ofAmblygaster sirm, Herklotsichthys quadrimaculatus, and Spratelloides delicatulus from various populations throughout their range. (L mat = length at maturity, ~BP = = mat = = length at first spawning, Lrruu; maximum size, T age at maturity, TrBP age at first spawning, rruu; = maximum age, K = Kiribati, I = India, SI = Solomon Islands).
Length at Length at first Age at first maturity (mm) spawning (mm) Age at maturityCd) spawning (d) 1 Species Site (Lmo'ILmaz) (Lf.pl Lmaz ) CTmo,lTmaz) (Tfop ITmaz) Source A.8irm Kiribati 110 CO.50) 180 (0.80) 150 (0.29) 330 (0.65) (1) New Caledonia 132 (0.72) 295 (0.40) (2) N. Australia 174 (0.79) 193 (0.88) (3) Sri Lanka 166 (0.88) -330 (0.80) (4) Mean 146 (0.72)
B. quadrimaculatu8 Hawaii 80 (0.63) 90 (0.70) 160 (0.53) 190 (0.63) (5) Marshall Is. 90 CO.82) 190 (0.72) (6) Fiji 95 (0.78) 98 (0.80) 275 (-) 294 (-) (7), (8) Butaritari CK) 65 (0.68) 70 (0.74) 125 (0.50) 135 (0.53) (l) Abaiang (K) 70 (0.74) 70 (0.74) 125 (0.37) 125 (0.37) (l) Tarawa (K) 69 (0.72) 70 CO.73) 138 (0.45) 150 CO.(8) (1) Abemama (K) 70 CO.64) 72 <0.65) 140 (0.34) 150 CO.36) (1) New Caledonia 91 CO.64) 244 (-) (9) Andaman Is. CI) 99 (0.81) 104 (0.85) (10) Seychelles 97 CO.71) 150 (0.30) (11) Mean 83 (0.72) 82 (0.74) 172 (0.46) 174 CO.(7)
S. delicatulu8 Fiji 35 (0.56) 39 (0.63) 52 (0.43) 61 (0.51) (7), (8) Butaritari (K) 40 (0.68) 40 <0.68) 65 CO.51) 68 CO.54) (l) Abaiang (K) 45 (0.75) 53 (0.88) 62 CO.51) 80 (0.64) (1) Tarawa (K) 45 (0.68) 50 (0.76) 77 CO.50) 90 (0.57) (1) Munda (SI) 37 CO.58) 37 CO.58) 72 (0.47) 78 (0.51) (12), (13) Vona Vona CSI) 37 CO.66) 37 (0.66) 68 (0.53) 72 CO.56) (12), (13) Tulagi CSI) 38 CO.60) 38 (0.60) 73 (0.55) 75 (0.57) (12), (13) Maldives 38 CO.69) 40 (0.73) 90 CO.60) 97 (0.65) (13), (14) India 42 (0.71) (15) Mean 40 (0.66) 42 CO.69) 70 (0.51) 78 (0.57)
1 Sources: (1) present study, (2) Conand (1991), (31 Okera (1982), (4) Dayaratne and Gjosaeter (1986), (5) Williams and Clarke (1983), (6) Hida and Uchiyama (1977), (7) Lewis et aJ. ll983), (8) Dalzell et aJ. (1987). (9) Conand (1988), llO) Marichamy (1971), (11) Moussac anf Poupon (1986), (12) Milton and Blaber (1991), ll3) Milton et aJ. (1991), (14) Milton et aJ. (1990), (15) Mohan and Kunhikoya (1986).
Using stepwise linear regression, we found that fecundity of S. delicatulus was highest in New fecundity was related to weight in all species (Table Caledonia - significantly higher than at all other 6; Fig. 5). Fecundity of A. sirm was significantly sites except Butaritari in Kiribati (Table 5). How correlated with HSI and fish condition. Fish condi ever, the relative fecundity of S. delicatulus was tion, HSI, and fat index were all correlated with lower than its congeners, S. gracilis and S. lewisi, fecundity in H. quadrimaculatus (Table 6). Fecun at sites where they co-occurred (Table 5). dity was significantly correlated with weight and We found that the fecundity ofS. delicatulus cor condition at two of the four sites. Although, when related strongly with fish weight (Fig. 5). The only data from all sites were combined, weight and fat other factor related to fecundity in S. delicatulus index were the only significant correlates. was HSI. There was a significant relationship be Fecundity of S. delicatulus varied widely among tween fecundity and HSI at Butaritari and Tarawa sites, both within Kiribati and among countries and when all data were combined. Spawning fish (Table 5). In Kiribati, relative fecundity was higher had a higher HSI at Butaritari than at other sites at Butaritari than atAbaiang (P<0.05), but differed (2.24 ± 0.13 vs. 1.41 ± 0.08; P
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0 o J FMAMJ J ASONDJ FMAMJ J ASO 1989 1990
Figure 2 Figure 3 Monthly variation (±95% confidence limits) in (A) Monthly variation (±95% confidence limits) in (A) condition, (B) visceral fat index, (C) hepatosomatic condition, (B) visceral fat index, (C) hepatosomatic index and (D) proportion spawning of female index and (D) proportion spawning of female Amblygaster sirm from Kiribati between January Herklotsichthys quadrimaculatus from Kiribati be 1989 and October 1990. tween November 1988 and April 1991.
higher at Butaritari (1.41 ± 0.06; N=57) than at Table 7). We found no significant differences among other sites (Abaiang HSI=1.07 ± 0.11; N=7; Tarawa sites for oocyte weights ofH. quadrimaculatus. HSI=0.81 ± 0.09; N=14). The proportion of male S. delicatulus that had GSI greater than 5% was also Sex ratio The sex-ratio of A. sirm, H. quadrima higher at Butaritari (36%) than at other sites culatus, and S. delicatulus changed as fish grew but (Abaiang 17.5%; Tarawa 20%). only among the largest length classes of each spe Oocyte weights ofA. sirm and S. delicatulus dif cies were there significant deviations from a ratio fered significantly from site to site (Table 7). In S. of 1:1. In all three species, females dominate the delicatulus, we found the greatest oocyte weight at largest length classes (Fig. 6). In our samples, we Abemama andAbaiang - significantly higher than found significantly more female A. sirm and S. at Butaritari and Tarawa (P<0.01). Oocyte weights delicatulus among fish larger than the length at first in A. sirm were also higher at Abaiang (P<0.001; spawning (180 and 45 mm respectively). With H. J J0 Fishery Bulletin 92(1). J994
higher lifetime egg production Table 4 at all sites than did co-occur Mean hepatosomatic index (HSI: %), visceral fat index (Fat) and condi ring S. delicatulus. The num tion (K: dry weight/length3 ) of Amblygaster sirm, Herklotsichthys ber of days between successive uadrimaculatus and Spratelloides delicatulus at different stages ofgonadal spawnings influenced esti development (SE =standard error ± N =number of females examined). mates of lifetime egg produc tion. Although longer in A. Species Stage HSI ± SE Fat ± SE K (x 10-6) ±SE N sirm, the difference was not A. Birm maturing 0.38 ± 0.06 3.4 ± 0.6 4.05 ± 0.25 8 significant (Table 8), ripe 0.43 ± 0.04 3.2 ± 0.3 4.14 ± 0.07 30 spawning 0.39 ± 0.06 2.6 ± 0.4 4.03 ± 0.13 16 Recruitment Amblygaster spent 0.42 ± 0.05 1.7 ± 0.2 2.77 ± 0.13 6 sirm recruited from a single H. quadrimacUlatUB maturing 0.87 ± 0.08 1.4 ± 0.1 3.89 ± 0.05 45 protracted period in Kiribati ripe 0.96 ± 0.06 1.6 ± 0.1 3.81 ± 0.05 127 during 1989 (March to October; spawning 1.04 ± 0.07 1.8 ± 0.1 3.91 ± 0.05 95 Fig. 8). We found a greater pro spent 0.69 ± 0.04 1.7 ± 0.1 3.53 ± 0.06 40 portion of survivors had been born between March and July S. delicatuluB maturing 1.41 ± 0.19 1.3 ± 0.2 2.36 ± 0.06 15 ripe 1.98 ± 0.10 1.6 ± 0.1 2.51 ± 0.04 41 than in all other months except spawning 1.84 ± 0.15 1.3 ± 0.1 2.46 ± 0.04 35 September (P<0.05L There spent 1.46 ± 0.10 1.2 ± 0.1 2.28 ± 0.04 55 were insufficient data to com pare monthly egg production with recruitment, but the pe riod of highest recruitment corresponded with the quadrimaculatus, females dominated among fish times of greatest spawning activity. However, this over 80 mm (Fig. 6). did not appear to be directly related to the absolute number of oocytes produced (Fig. 7). Egg production The number of spawnings per The proportion ofH. quadrimaculatus born each month and the daily egg production of all species month differed over the four years
30000 A ~ A 3.5L F =180.5W1.0 20000 l=O.48 ~ ::f..""",\,,,~, N=32 10000
Or------r----r----,----.-----, o 50 100 150
8000 B F = 367.5W - 299.8 00 6000 go 2 o ~ r =O.54 N=167 c 4000 ~ o i ~'''' ,,~"" ,~, 2000 J O+-"""-.....--..---~-,.__-~___, o 5 10 15 100 D
80 3000 C o F = 699.9W 1.1 ~ 60 l=O.74 o ~ 2000 'c N=87 ~ 40 /J; 1000 20 o
O¥=---.....--..---~-...__-~____. o 2 3
Figure 4 Monthly variation (±95% confidence limits) in (AI Figure 5 condition, (B) visceral fat index, (C) hepatosomatic The relationship between batch fecundity and index and (D) proportion spawning of female fish weight for (A) Amblygaster sirm, (Bl Spratelloides delicatulus from Kiribati between Herklotsichthys quadrimaculatus and (C) November 1988 and May 1991. Spratelloides delicatulus from Kiribati.
Discussion and S. delicatulus from Kiribati agree with previ ous reproductive studies of these species in tropical The reproductive cycles of A. sirm, H. quadrima areas (McCarthy, 19851; Moussac and Poupon, 1986; culatus, and S. delicatulus in Kiribati are similar to Milton and Blaber, 1991). In the tropics, both spe that reported for temperate multiple-spawning cies spawn throughout the year, but have periods clupeoids (Hunter and Goldberg, 1980; Gil and Lee, when spawning activity is greater. In more temper 1986; Shelton, 1987; Alheit, 1989). Most studies on ate parts of their range, the reproductive season of multiple spawning clupeoids have been on both H. quadrimaculatus and S. delicatulus is engraulids; these species spawn many batches of shorter and coincides with increases in water tem eggs each year and have variable batch fecundity perature in early summer (Williams and Clarke, (Alheit, 1989). Our results for H. quadrimaculatus 1983; Lewis et a1., 1983; Conand, 1988). 112 Fishery Bulletin 92(11. 1994
Table 5 Mean length (mm), age (years), fecundity, relative fecundity (eggs g-l) ofAmblygaster sirm, Herklotsichthys quadrimaculatus, and Spratelloides delicatulus and other tropical and subtropical clupeids (sardines, her- rings, and sprats) (K =Kiribati, SI =Solomon Islands, I =India, P.N.G. =Papua New Guinea, UK =United Kingdom, SU =Soviet Union, G =Germany).
Length Age Fecundity ReI. fecundity Species Site ± SE ± SE ± SE ± SE N Source
Sardines Amblygaster sirm Abaiang (K) 189 ± 5 0.97 ± 0.03 18789 ± 2757 187.1 ± 25.3 7 11) Tarawa (K) 194 ± 1 1.04 ± 0.03 20327 ± 1391 192.0 ± 12.0 25 (1) New Caledonia 139-177 0.90-2.2 8000-27780 300.0 ± 16.9 24 (2), (3) Sardinella brasiliensis Brazil 162 ± 2 23318 ± 2065 356 ± 37 23 (4) S. marquesensis Marquesas Is. 109 ± 6 4150 ± 1000 6 (5) S. zunasi Korea 75-142 1-3 8800-58800 31 (6)
Berrings Herklotsichthys uadrimaculatus Hawaii 807 121 1155-6296 160-311 46 (7) Marshall Is. 100 ± 2 0.59 ± 0.02 4755 ± 380 7 (8) Butaritari (K) 75 ± 1 0.45 ± 0.01 1844 ± 108 295.5 ± 12.1 44 11) Abaiang (K) 75 ± 1 0.45 ± 0.02 1975 ± 133 317.4 ± 19.3 27 11) Tarawa (K) 76 ± 1 0.44 ± 0.02 2353 ± 110 344.1 ± 10.2 63 (1) Abemama (K) B4 ± 2 0.61 ± 0.04 300B ± 207 319.1 ± 22.7 33 (1) Andaman Is. (Il 95-115 8353 ± - 19 (9) Seychelles 8B-127 4500-8000 24 (101 Opisthonema libertate Mexico 142 ± 1 57125 ± 1850 553 ± 14 115 (11)
Sprats Spratelloides delicatulus Butaritari (K) 52 ± 2 0.27 ± O.oI 1359 ± 143 B67 ± 55 19 (1) Abaiang (K) 52 ± 1 0.21 ± 0.02 973 ± 43 667 ± 35 7 (1) Tarawa (K) 54 ± 1 0.29 ± 0.01 1255 ± 54 735 ± 25 49 11) Abemama (K) 41 ± 1 0.20 ± 0.02 524 ± 95 702 ± 75 12 (1) Munda (SIl 48 ± 1 0.26 ± 0.01 799 ± 45 554 ± 25 57 (12) Vona Vona (SIl 49 ± 1 0.26 ± 0.01 925 ± 102 717 ± 45 28 (12) Tulagi (SII 46 ± 1 0.21 ± 0.01 926 ± 93 567 ± 49 28 (12) New Caledonia 45 710 B83 ± 14 20 (2) India 40 ± 3 60B ± 54 15 (13)
S. gracilis Munda (SI) 50 0.19 514 504 1 (14) Vona Vona (SI) 37 ± 1 0.15 ± 0.01 505 ± 51 BB2 ± 68 13 (12) P.N.G. 53 ± 2 2592 ± 313 1690 ± 96 18 (15) Maldives 59 ± 1 0.29 ± 0.02 1998 ± 137 1073 ± 54 33 (12) India 40 ± 5 790 ± 71 962 ± 53 15 (13)
S. lewisi Munda (SI) 44 ± 1 0.18 ± 0.01 887 ± 20 925 ± 16 219 (14) Vona Vona (SI) 42 ± 1 0.14 ± 0.01 930 ± 51 1032 ± 36 62 (14) Tulagi (SIl 49 ± 1 0.28 ± 0.02 1290 ± 84 1230 ± 69 29 (14) Sprattus sprattus Scotland lUK) 108 3 2729 187 64 (16) Baltic Sea (SUI 121 1.9 2174 232 46 (17) North Sea (G) 2 413 (17)
Sources: (1) present study, (2) Conand (1988). (3) Conand (1991), (4) Isaac-Nahum et al. (1988), (5) Nakamura and Wilson (1970), (6) Gil and Lee (1986), (7) Williams and Clarke (19831, (8) Hida and Uchiyama (977). (9) Marichamy (1971). (0) Moussac and Poupon (986), (11) Torres-Villegas and Perezgomez (1988), (12) Milton et al. (1990), (13) Mohan and Kunhikoya (1986), (14) Milton unpubl. data, (15) Dalzell (1985), (16) De Silva (1973), (17) Alheit (1988 I.
Although we found A. sirm also had an extended lasted two to five months during early summer spawning season in Kiribati, the species may not (Conand, 1991) or the monsoon period (Rosa and spawn throughout the year. Our result differs from Laevastu, 1960; Dayaratne and Gjosaeter, 1986). previous studies that found the spawning season Neither temperature nor rainfall appear to be the Milton et al.: Reproductive biology and egg production of three species of C1upeidae 113 proximate stimuli for spawning ofA. sirm in Kiribati. Tempera Table 6 ture was constant throughout Stepwise regression of the relationship between various endogenous the year and rainfall was factors and fish fecundity from sites in Kiribati. (Cr; = partial higher at all sites in Kiribati correlation coefficient; r 2 =overall correlation coefficeint; P =signifi between December and April, cance level; N = sample size; HSI = hepatosomatic index; All = data when spawning activity was from each site combined). lowest. Most spawning activity Species Site Factor r 2 r2 p N in this species occurred during p the second half of the year AmblYllaBter 8irm Tarawa Weight 0.24 0.44 <0.05 25 when the prevailing wind di HSI 0.20 rection changed from east to All Weight 0.38 0.64 <0.001 32 west, associated with the north- Condition 0.28 west monsoon that starts at Herklot8ichthY8 Butaritari Weight 0.36 0.43 <0.001 44 this time (Burgess, 19875). Our quadrimaculatu8 Condition 0.07 limited wind and rainfall data Abaiang Weight 0.28 0.39 <0.01 27 did not indicate that increased HSI 0.11 spawning activity in A. sirm Tarawa Length 0.58 0.63 <0.001 63 was related to the shift in Condition 0.03 weather pattern. Age 0.02 Gonad maturation and Abemama Weight 0.62 0.72 <0.001 33 spawning were also linked to Fat 0.10 changes in fish liver-weight All Weight 0.54 0.57 <0.001 167 (HSl), visceral fat, and condi- Fat 0.03 tion ofeach species. Either HSI Spratelloide8 Butaritari Weight 0.70 0.76 <0.001 19 or fat index and condition were delicatulu8 HSI 0.06 all significantly reduced in Abaiang no factor 7 postspawning fish. Amblygas- Tarawa Weight 0.37 0.52 <0.001 49 ter sirm stores energy in the HSI 0.15 viscera rather than in the liver. Abemama Weight 0.87 0.87 <0.001 12 Other multiple-spawning c1up- eoids also transfer energy from All Weight 0.59 0.66 <0.001 87 stored fat to reproductive tis- HSI 0.07 sue (Dahlberg, 1969; Okera, 1974; Hunter and Leong, 1981). In contrast, spent H. quadrimaculatus and S. delicatulus had reduced HSI, which suggests that Table 7 the liver is the energy store utilized during repro Mean hydrated oocyte dry weight ofAmblygaster duction (Diana and MacKay, 1979; Smith et aI., sirm, Herklotsichthys quadrimaculatus, and 1990). Energy stored in this organ would be readily Spratelloides delicatulus from four sites in Kiribati (N = number of females examined). available for rapid assimilation; hence, fish could spawn multiple batches of eggs rapidly. Hydrated oocyte Studies of temperate herring, Clupea harengus, weight ± SE have shown that gonad maturation is linked to food Species Site (x 10-4 g) N availability and fat storage (Linko et aI., 1985; A. sirm Abaiang 4.4 ± 0.5 7 Henderson and Almatar, 1989; Rajasilta, 1992). Tarawa 1.5 ± 0.1 16 Ovaries of all three species in Kiribati and of S. delicatulus in the Solomon Islands (Milton and H. quadrimaculatus Butaritari 2.0 ± 0.2 36 Abaiang 1.8 ± 0.1 12 Blaber, 1991) vary in a similar way to herring. Tarawa 1.6 ± 0.2 19 Milton and Blaber (1991) did not find a direct rela Abemama 1.9 ± 0.2 26 tion between spawning and prey availability. This S. delicatulus Butaritari 0.7 ± 0.1 11 suggests that while gonad maturation in these clu- Abaiang 1.4 ± 0.2 12 Tarawa 0.8 ± 0.04 27 5 Burgess, S. M. 1987. The climate of western Kiribati. New Zealand Meterological Service, Wellington, NZ. Miscellaneous Abemama 2.2 ± 0.2 10 publ. 188, part 7. 114 Fishery Bulletin 9211). 1994
co;; 5 .... A
<100110120130140150160170180190200>200 Length (mm) 100 B 80
~ 60 CD Time J 40 B 20
<30 40 50 60 70 80 90 >90 Length (mm)
100
80
60
40 1989 1990 1991 20 Time O-'--.----r-.....-,-----y---,.---...,---.-- <30 35 40 45 50 55 60 >60 Length (mm) c
Figure 6 6 Ontogenetic change in the proportion female of (A) Amblygaster sirm, (B) Herklotsichthys quad rimaculatus and (C) Spratelloides delicatulus (±95% 4 confidence limits) from Kiribati. 2
O-rrr-r,.,.-n-r""-TTTT1""'rrTTT1r-tAr"TT'"rrT"T""1 peids is probably linked to cycles in prey abundance, fat storage may reduce the effects of short-term fluc Time tuations in prey abundance on reproduction. Diel timing ofspawning events was similar for all Figure 7 species. We found new post-ovulatory follicles (day Monthly estimates of daily egg production of (A) 0) in females collected from 2130 hours onwards Amblygaster sirm, (B) Herklotsichthys quadrima with the greatest proportion detected after 0100. culatus and (C) Spratelloides delicatulus from This indicates that these species spawn during the Kiribati during the study period. early part of the night, probably prior to midnight. Our results are consistent with previous studies that found high densities ofA. sirm eggs in the plank cal clupeoids (Clarke, 1987) also showed that spawn ton after midnight (Delsman, 1926; Lazarus, 1987). ing peaked before midnight. Studies of other sardines (Goldberg et aI., 1984; Length and age at sexual maturity ofA. sirm and Isaac-Nahum et aI., 1988; Re et al., 1988) and tropi- H. quadrimaculatus in Kiribati differed from those Milton et al.: Reproductive biology and egg production of three species of C1upeidae 115
Table 8 Mean reproductive life span (in days) and days between spawning of Amblygaster sinn. Herklotsichthys quadrimaculatus, and Spratelloides delicatulus from four sites in Kiribati (N = number of length-frequency samples; No. = number of months examined).
Days Max. lifetime Reproductive between egg production Species Site Year life span ± SE Range N spawning Range No. (x 104 )
A. sirm Abaiang 1989-1990 19.0 ± 6.4 0-66 12 20.0 Tarawa 1989-1990 60.1 ± 15.4 0-127 7 41.6 Abemama 1989-1990 3.2 ± 3.1 0-19 6 Overall 1989-1990 26.7 ± 6.8 0-127 25 6.2 ± 2.3 1.5-25.9 10 38.7 H. quadrimacUlatu8 Butaritari 1989-1991 47.3 ± 15.0 0-201 14 11.9 Abaiang 1989-1991 73.9 ± 15.6 0-201 17 12.8 Tarawa 1976/83/89-91 84.1 ± 7.8 0-254 64 19.3 Abemama 1989-1991 141.8 ± 30.9 0-286 12 27.7 Overall 1989-1991 80.6 ± 8.6 0-286 74 3.1 ± 0.3 1.3-4.7 15 21.1 S. delicatulus Butaritari 1989-1991 53.6 ± 4.6 24-74 15 1.9 Abaiang 1989-1991 49.2 ± 5.1 21-80 11 1.5 Tarawa 1989-1991 66.9 ± 10.6 0-144 16 3.5 Tarawa 1976 76.6 ± 10.5 45-129 7 3.1 Tarawa 1983/84 84.3 ± 9.5 34-152 16 3.7 all 1989 90.0 ± 13.4 53-144 7 3.2 all 1990/91 51.0 ± 4.1 0-109 35 2.5 Overall 1989-1991 57.5 ± 4.6 0-144 42 5.2 ± 1.8 1-30 16 3.2
gested these differences were consistent with the 20 hypothesis of Longhurst and Pauly (1987) that fish 1989 ofany species living in cooler water will grow to and (n = 717) mature at a larger size through the interaction of oxygen supply and demand. Our data on H. quadrimaculatus is consistent with this hypothesis - the other studies were all at sites at higher lati tudes than Kiribati, where the water temperature is lower. Also, the proportion of maximum size at which fish matured was similar at all locations, o J FMAM JJ A SON D despite the absolute differences in size at maturity Time in Kiribati. By comparison, A. sirm matured at a smaller size Figure 8 and grew to a larger size in Kiribati than at other The proportion of Amblygaster sirm (±95% locations (Milton et aI., 1993). The proportion of confidence limits) sampled between August maximum size at which fish matured was also lower 1989 and July 1990 born each month in 1989, than found in previous studies and was less than the backcaleulated from length-frequency samples. proportion common to a wide range of clupeoids (70%; Beverton, 1963). In response to severe fishing pressure, the size and age at sexual maturity of in other parts oftheir range (Table 3). We found few several sardine species have been found to decline differences within Kiribati, but both species became (Murphy, 1977). Presumably, this is because any sexually mature and spawned at much shorter body density-dependent effects are reduced during early lengths than at other locations. Herklotsichthys growth (Beverton and Holt, 1957; Ware, 1980). quadrimaculatus did not grow as large in Kiribati Amblygaster sirm can have high or variable adult as elsewhere (Milton et aI., 1993), but the propor mortality in Kiribati (Rawlinson et aI., 1992), tion ofmaximum size at which this species matured favouring early maturation (Stearns and Crandall, was similar throughout its range. Milton and Blaber 1984). (1991) found regional differences in length at sexual Length at first spawning was a similar proportion maturity in other small tropical clupeoids; they sug- of maximum size for the three species and was con- 116 Fishery Bulletin 92( I), 1994
50 1976 30 1976 (n = 3002) 40 (n =13131) 20 30
20 10 10 o 0'-"'-'" 50 1983 30 1983 (n = 1705) 40 (n = 9198) 30 20 ~20 o ~ 10 :;:- 10 !!.... c: ~ 0 ,-.,.--,.--,.-,.-,.-,. 5l 0 E "250 1989 '2 30 1989 o (n 4745) ~ 40 = &l (n =2014) II: 20 30 20 10 10 0'-""""'" 0'-""""'" 50 1990 30 1990 (n = 2747) 40 (n =16419) 30 20 20 10 10 o o J FMAM JJ A SON D J FMAM JJ A SON D Time Time Figure 9 Figure 10 The proportion of Herklotsichthys qua.d The proportion of Spratelloides delicatulus rimaculatus born each month in 1976, 1983, born each month in 1976, 1983, 1989. and 1989, and 1990. back-calculated from length 1990, back-calculated from length-frequency frequency samples (95% confidence limits of samples (95% confidence limits of all propor all proportions are all less than 1.5%), tions are all less than 1.5%). sistent with the close relation with maximum size study period and suggests that adult food resources found by Blaxter and Hunter (1982 l for other and larval survival are predictable or relatively con clupeoids. These authors also noted a latitudinal stant (Sibly and Calow, 1983 l. effect; fish from lower latitudes spawned at a In comparison to other species, S. delicatulus had smaller proportion of maximum size. a higher relative fecundity that was also correlated Temperate clupeids (especially herrings, Clupea with HSI. Females in spawning condition also had spp.) show a great plasticity in the number and size a higher HSI at Butaritari. Commercial CPUE was of eggs produced; many species show seasonal, and highest at this site (Rawlinson et aI., 1992) and S. inter-annual, as well as geographic, variation in delicatulus spawned more, smaller eggs than at their reproductive outputs (Alheit, 1989; Jennings other sites where relative fecundity was lower. and Beverton, 1991) reflecting energetic resources These data suggest that the fecundity of S. and environmental conditions (Hay and Brett, 1988; delicatulus may be influenced by the amount of Henderson and Almatar, 1989>. By comparison, the energy stored in the liver. This energy store would tropical herring, H. quadrimaculatus, spawned be important in a small multiple-spawning species; throughout the year and showed negligible tempo it would enable the fish to continue spawning dur ral or spatial variation in fecundity, egg weight, or ing short periods of reduced food supply (Hay and inter-spawning interval. This indicates that egg Brett, 1988). The length of the inter-spawning in production was almost constant throughout the terval has been shown experimentally to be related Milton et al.: Reproductive biology and egg production of three species of C1upeidae 117 to food supply in other fish species (Townshend and The reproductive life span ofthe smallest species, Wootton, 1984). Fish at Butaritari may experience S. delicatulus, was intermediate between the other a more predictable environment that enables them species and varied little among sites during 1989 to produce more eggs of smaller size than fish in and 1990. Unlike H. quadrimaculatus, the reproduc more variable environments. tive life span ofS. delicatulus varied between years, In contrast, A. sirm delayed spawning beyond the which suggests that survival rates are not as con size and age at sexual maturity and did not spawn stant or as predictable as those of H. until one year old. As fecundity was related to quadrimaculatus. Potential lifetime egg production weight, delayed spawning enabled A. sirm to grow ofeach female was only one tenth that ofother spe faster than the other species (Milton et aI., 1993) cies, but, because of the larger number of females, and have a higher batch fecundity when spawning monthly estimates of daily egg production were started. Murphy (1968) hypothesized that delayed higher. The distribution of back-calculated spawning and longer reproductive life span would birthdates varied between years, but a greater pro evolve in response to variable reproductive success. portion ofbirths fell in May-August, irrespective of However, Armstrong and Shelton (1990) demon the pattern of egg production. Annual CPUE of S. strated that, even with a short reproductive life delicatulus (Rawlinson et aI., 1992) was similar in span, multiple spawners had a high probability of 1989 and 1990, which suggests that fishing mortal successful reproduction when subject to random ity had not contributed to the increased mortality environmental fluctuations over time. Thus, delay that reduced the reproductive life span in 1990. ing spawning would be of adaptive advantage if The reproduction and abundance ofS. delicatulus mortality was low (Roff, 1984) because batch fecun may be more directly influenced by its environment dity and lifetime egg production would be increased. than are the other species. Adult survival is vari Our estimates of the reproductive lifespan of A. able and low (Tiroba et aI., 1990); egg production sirm indicate that this species spawns fewer times varies, probably in response to food supply, and sur in their lifetime than other species and thus would vival to recruitment is unpredictable. Yet the poten also have less chance of successful spawning than tial for successful reproduction with this strategy other species. Given that this is the longest-lived of may still be relatively high (Armstrong and Shelton, the species examined, our estimate of overall mean 1990). In contrast, H. quadrimaculatus appears to lifespan may be biased by the small number of be able to offset environmental variability to produce months sampled. Large fish may be under-repre a relatively constant supply of eggs. sented in small catches and may contribute to un The distribution pattern of back-calculated derestimating the reproductive potential ofA. sirm. birthdates ofeach species was not consistent among Herklotsichthys quadrimaculatus had a longer species. Months when a higher proportion survived reproductive life span and spawned more frequently differed for each species during all years; months than did the other species. Reproductive life span with highest mean survival were not the same for varied little among sites (except Abemama) and any species. This suggests that the effects of envi there was no significant temporal variation, which ronmental conditions such as seasonal food avail suggests that survival rates of large adult H. ability or favorable physical conditions are not the quadrimaculatus are fairly constant in Kiribati. same for each species. Alternatively, other factors This is reflected in their life-history parameters, such as predation (Rawlinson et aI., 1992) may have which varied little among sites or over time. In con greater influence on survival to recruitment. Egg trast, the frequency distribution of back-calculated production by S. delicatulus was positively corre birthdates indicated that overall survival was vari lated to survival rates in 1989 and negatively cor able both between and within years, and was not related in 1990. This seems unrelated to fish abun related to monthly egg production. We have no es dance as catch rates were higher in 1989 than in timates ofadult abundance during the study period, 1990 (Rawlinson et aI., 1992). and so population egg production could not be as Large variations in recruitment, reflected in catch sessed. However, the annual CPUE and abundance rates of the main baitfishes do not appear to be di ofH. quadrimaculatus in the baitfishery were simi rectly linked with variations in egg production. All lar in the three years for which both data sets were spawn in the lagoon for most of the year, and dis available (Rawlinson et aI., 1992). This suggests that tribution ofbirthdates indicated recruitment in most population size was relatively constant during this months. Although the absolute level of recruitment period. Ifso, then variation in. post-hatching survival varied throughout the year, multiple spawning re probably has an important influence on recruitment duces fluctuations in population size due to environ in this species (Smith, 1985). mental variability and should ensure that relatively 118 Fishery" Bulletin 92( 1I, 1994
stable population sizes are maintained. Earlier stud Conand, F. ies of A. sirm and H. quadrimaculatus in Tarawa 1988. Biology and ecology ofsmall pelagic fish from lagoon suggested that these species spend at least the lagoon of New Caledonia usable as bait for part oftheir life outside the lagoon (R. Cross, 19784; tuna fishing. Thesis Studies, ORSTOM, Paris, 239 p. McCarthy, 19851). Ifthis is the case, fluctuations in the relative abundances of these species may be re 1991. Biology and phenology of Amblygaster sirm (Clupeidae) in New Caledonia, a sardine of the lated to migrations; a better understanding ofthe fac coral environment. Bull. Mar. Sci. 48:137-149. tors causing large-scale movements is necessary Conover, W. J. before predicting the potential yield of this fishery. 1980. Practical nonparametric statistics, 2nd ed. J. Wiley & Sons, NY, 493 p. Cushing, D. H. Acknowledgments 1967. The grouping of herring populations. J. Mar. BioI. Assoc. U.K. 47:193-208. We thank staffofthe Kiribati Fisheries Division for 1971. The dependence of recruitment on parent assistance with fieldwork during the project. Peter stock in different groups of fishes. J. Cons. into Crocos and Jock Young and three anonymous re Explor. Mer 33:340-362. Cyrus, D. P., and S. J. M. Blaber. viewers made constructive comments on earlier 1984. The reproductive biology of Gerres in Natal drafts. This work formed part of the baitfish re estuaries. J. Fish. BioI 24:491-504. search project PN 9003 funded by the Australian Dahlberg, M. D. Centre for International Agricultural Research. 1969. Fat cycles and condition factors of two spe cies of menhaden, Brevoortia (Clupeidae), and natural hybrids from the Indian river of Literature cited Florida. Am. MidI. Nat. 82:117-126. Dalzell, P. Alheit, J. 1985. Some aspects of the reproductive biology of 1988. Reproductive biology of sprat (Sprattus Spratelloides gracilis (Schlegel) in the Ysabel sprattus): factors determining annual egg Passage, Papua New Guinea. J. Fish. BioI. production. J. Cons. into Explor. Mer 44:162-168. 27:229-237. 1989. Comparative spawning biology ofanchovies, Dalzell, Po, S. Sharma, and J. Prakash. sardines, and sprats. Rapp. P.-v. Reun. Cons. into 1987. Preliminary estimates of the growth and Explor. Mer 191:7-14. mortality fo three tuna baitfish species, Herklot Armstrong, M. J., and P. A. Shelton. sichthys quadrimaculatus, Spratelloides deli 1990. Clupeoid life-history styles in variable catulus and Rhabdamia gracilis from Fijian environments. Envir. BioI. Fish 28:77-85. waters. Tuna Billfish Assessment Programme Armstrong, M. J., P. A. Shelton, I. Hampton, G. Tech. Rep. 20:1-15. Jolly, and Y. Melo. Dayaratne, P., and J. Gjosaeter. 1988. Egg production estimates of anchovy biom 1986. Age and growth of four Sardinella species ass in the southern Benguela system. Calif. from Sri Lanka. Fish. Res. 4:1-33. Coop. Oceanic Fish. Invest. Rep. 26:3040. Delsman, H. C. Beverton, R. J. H. 1926. Eggs and larvae from the Java Sea: 7. The 1963. Maturation, growth and mortality ofclupeid genus Clupea. Treubia 8:218-239. and engraulid stocks in relation to fishing. Rapp. De Silva, S. S. P-v. Heun. Cons. into Explor. Mer 154:44-67. 1973. Aspects of the reproductive biology of the Beverton, R. J. H., and S. J. Holt. sprat, Sprattus sprattus in inshore waters of the 1957. On the dynamics of exploited fish west coast of Scotland. J. Fish BioI. 5:689-705. populations. Fish Invest., Ser. 2, Mar. Fish. GB Diana, J. S., and W. C. MacKay. Minist. Agric. Fish. Food 19:1-533. 1979. Timing and magnitude of energy deposition Blader, J. S. H., and J. R. Hunter. and loss in the body, liver and gonads of northern 1982. The biology of the clupeoid fishes. Adv. in pike (Esox lucius). J. Fish. Res. Board. Can. Mar. BioI. 20:1224. 36:481--487. Clarke, T. A. Gil, J. W., and T. W. Lee. 1987. Fecundity and spawning frequency of the 1986. Reproductive ecology of the scaled sardine, Hawaiian anchovy or Nehu, Encrasicholina Sardinella zunasi (Family Clupeidae), in Cheonsu purpurea. Fish. Bull. 85:127-138. Bay of the Yellow sea, Korea. In T. Uyeno, R. 1989. Seasonal differences in spawning, egg size, Arai, T. Taniuchi. and K. Matsuura (eds.), Indo and early development time of the Hawaiian an Pacific fish biology: proceedings of the second in chovy or nehu, Encrasicholina purpurea. Fish. ternational conference on Indo-Pacific fishes, p. Bull. 87:593-600. 818-829. Ichthyological Society ofJapan, Tokyo. Milton et al.: Reproductive biology and egg production of three species of C1upeidae J 19
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