Contributions to the reproductive biology of encrasicholina punctifer ...

Fisheries Research 44 (1999) 113±120 

Contributions to the reproductive biology of 

encrasicholina punctifer Fowler, 1938 

(engraulidae) from West Sumatra, Indonesia 

Gerd Maack a,* , Michael R. George b 

a ZMT Center for Tropical Marine Ecology, Bremen, Germany 

b German Oceanographic Museum, Museum for Marine Research and Fishery Aquarium, 

Katherinenberg 14/20, Stralsund 18439, Germany 

Received 6 January 1999; received in revised form 29 June 1999; accepted 17 July 1999 

Abstract 

Encrasicholina punctifer (Fowler, 1938) is economically by far the most important ®sh species in the coastal area of Padang 

(West Sumatra, Indonesia). In this study, the reproductive biology of E. punctifer is described for the ®rst time with different 

methods. The relationship between length and weight of E. punctifer in the coastal waters of west Sumatra can be described 

as W ˆ 6:310 6 L 3:125 

t …r 2 ˆ 0:96; n ˆ 2550†. The Encrasicholines are multiple spawners with asynchronous oocyte 

development. During one individual spawning season, oocyte development is a continuous process involving all stages of 

oocytes, clearly represented by an unimodal oocyte-size-frequency-distribution (OSFD). Before spawning a new batch can be 

identi®ed by its separation from the remaining oocytes, leaving a gap in the OSFD. There are postovulatory follicles inside the 

ovary after ovulation. From a gonosomatic index of 5.5 the ovaries contain hydrated oocytes, indicating a pre-spawning state. 

A certain proportion of the population is spawning at any time. The relative fecundity was estimated to be 985 ( 359) eggs 

per batch and gram female body weight. The oocyte development occurs simultaneously in all areas of the ovary. First 

maturity is reached at 57.5 mm L t . There is no dependence between ®sh condition and gonad weight. The necessary energy for 

the gonadal growth of the anchovies is not obtained from body fat, but most likely directly from forage. # 1999 Elsevier 

Science B.V. All rights reserved. 

Keywords: Anchovy; Encrasicholina punctifer; Reproductive biology; Fecundity; Oocyte development 

1. Introduction 

* Corresponding author. Present address: UFZ-Centre for Environmental 

Research, Department for Chemical Ecotoxicology, 

Permoserstraûe 15, 04318 Leipzig, Germany. Tel.: ‡‡49-341- 

2352740; fax: ‡‡49-341-2352401 

E-mail address: gm@.uoe.ufz.de (G. Maack) 

In many regions of Indonesia, ®sh is important for 

the human protein supply and at least 200 species are 

of commercial interest (Soesanto, 1985). Encrasicholina 

punctifer (Fowler, 1938) is by far the most 

economically important species in the coastal area 

of West Sumatra (Rohdenburg, 1995). It is a small 

0165-7836/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. 

PII: S 0165-7836(99)00084-3

114 G. Maack, M.R. George / Fisheries Research 44 (1999) 113±120 

pelagic schooling ®sh, with a total length of 10 cm 

(Paula e Silva, 1992) and a short life span of around a 

year (Rohdenburg, 1995). The species is commonly 

found in the coastal waters around the Indian Ocean 

and in the West Paci®c. 

From Delsman (1931) it is known, that Encrasicholines 

spawn virtually continuously. He described the 

species as a multiple spawning ®sh with asynchronous 

oocyte development, i.e. oocytes in all stages of 

development occurring simultaneously in reproductively 

active ovaries. According to Hunter et al. (1992) 

multiple spawning ®sh are called indeterminate serial 

or batch spawners, if the annual fecundity is not ®xed 

at the beginning of spawning and the standing stock of 

present oocytes in the ovary is continuously replaced 

by new developing oocytes during one spawning 

cycle. On the other hand, ®sh that have a ®xed 

fecundity prior to the onset of spawning, are called 

determinate serial spawners. Engraulis mordax is an 

example of an indeterminate serial spawner (Hunter 

and Goldberg, 1980; Hunter and Leong, 1981). In a 

determinate serial spawner, as for instance the Dover 

sole (Microstomus paci®cus), the standing stock of 

advanced oocytes-prior to the onset of spawning-is 

equivalent to the annual fecundity, whereas in an 

indeterminate serial spawner this is not the case 

(Hunter et al., 1992). In the latter case annual fecundity 

is much higher than the present standing stock of 

advanced oocytes. Determining the type of spawning 

is of great importance for estimating the potential 

annual fecundity of a species and its ability to recover 

from human ®shery impact. 

In the coastal area of West Sumatra, there is no 

management for the artisanal ®shery and the impact on 

the standing stock is rising, because more and more 

people try to earn their living with artisanal ®shery. In 

this study the reproductive biology of E. punctifer is 

described to place basic information on this species at 

®shery management agencies' disposal. Different 

methods were used for a cross-check of the results. 

2. Material and methods 

E. punctifer was collected twice a week from 

artisanal ®shermen, operating the traditional Bagan 

®shery at the coast of Padang (Fig. 1). By this method, 

®sh are attracted by arti®cial light and caught with lift 

nets during the night. Samples for this study were 

taken from different boats and pooled each week from 

April to July 1994. For length±weight relationship, 

total length L t (to 1 mm) and body weight (g) of 2550 

individuals were measured. For fecundity studies, 780 

individuals ranging from 43 to 95 mm L t were 

sampled. In the laboratory, wet weight, length and 

gonad weight of the ®sh were measured. Subsamples 

were preserved in 4% buffered formalin for histological 

investigations. 

2.1. Gonosomatic index 

The gonosomatic index (GSI) was determined as 

follows: 

GSIˆgonad weight …gonad-free body weight† 1 100: 

2.2. Condition factor 

The condition factor (CF) was determined as 

follows by using the total length L t of the ®sh: 

CF ˆ gonad-free wet weight L 3:125 

t 100: 

Instead of the theoretical coef®cient of b ˆ 3, the 

actual coef®cient of the length±weight regression was 

used. 

2.3. Size at sexual maturity 

Size at sexual maturity was determined with the 

GSI-method after Grimes (1976). This method was 

used to determine the 50% maturity length by calculating 

the mean GSI per 5 mm length-class. 

100xGSI …n† 

100 ˆ proportional increase in GSI: 

GSI …n1† 

The resulting values showed the proportional 

increase or decrease of mean GSI in comparison to 

the previous length-class. The highest proportional 

increase of GSI of all classes corresponded to the 

mean length, where 50% of this species reached 

maturity. 

2.4. Analysis of ovaries 

For counting and measuring the oocytes, the ovary 

tissue was preserved in Gilson's ¯uid (Bagenal, 1978)

G. Maack, M.R. George / Fisheries Research 44 (1999) 113±120 115 

Fig. 1. Location where E. punctifer was collected off the coast of Padang-City (hatched field). 

for three months. Oocytes from the ®xed tissue were 

then separated from the ovigerous folds (ovarian 

lamellae) and measured to the nearest 0.01 mm on 

their longest axis under a binocular microscope on a 

digitizer. Ripe ovaries were identi®ed from their 

external appearance and the extent to which they ®lled 

the body cavity. The most advanced group of oocytes 

was counted and the relative batch fecundity (oocytes 

per g body weight) of each female was estimated. 

Standard method of Methyleneblue (Gerrits, 1985) 

was used to stain the ovaries. The ovaries of 30 

specimens were examined histologically and classi- 

®ed using Wright's method for E. heteroloba (Wright, 

1992). 

3. Results 

The length±weight relationship of E. punctifer off 

the coast of West Sumatra is 

Weight ˆ 6:310 6 L 3:125 

t ; r 2 ˆ 0:96; n ˆ 2550: 

No correlation was found between the GSI and the 

condition factor (r 2 ˆ 0.0017) for immature females 

and for mature females. 

The progression of maturing oocytes was evident 

when the upper mode of the oocyte size frequency in 

the ovaries was plotted against the gonosomatic index 

(Fig. 2). The maximum mode of the oocyte is constant 

except when the GSI is between 5 and 9. All oocytes of 

the spawning batch are fully grown. Furthermore, the 

scatter of the points suggests, that there is a rapid 

increase in the oocyte size at maturity. 

In this study E. punctifer reached sexual maturity at 

a total length of 55±59 mm. The same length was 

estimated using histological measures. At a total 

length of 60 mm postovulatory follicles (POFs) were 

found in the ovaries. Vitellogenesis appeared in 

females larger than 57 mm L t . The relation of size 

at sexual maturity to maximal length was 0.504.


Fig. 2. Relationship between the diameter of the most advanced mode of oocytes in the ovary and gonosomatic index (GSI) of E. punctifer. 

3.1. Fecundity 

Relative batch fecundity of E. punctifer was 985 

(359) eggs per g body weight. To ®nd potential 

differences between the two ovaries of single females, 

both ovaries of 13 specimens were counted separately 

and results compared. There was no signi®cant difference 

in the distribution (p < 0.1) between the left 

and right ovary of single females. Oocytes of the four 

different maturity classes were distributed evenly over 

the entire ovary. 

Using the t-test, there was no signi®cant (p < 0.05) 

difference in the distribution regarding the proportion 

of the maturity stages in each of the four divisions of 

the ovary (Fig. 3). All developmental stages of oocytes 

occurred in the entire ovary at the same time. The 

oocytes did not move to the cranial end of the ovary 

during maturation. 

3.2. Oocyte-size-frequency-distribution and 

histological analysis 

To examine the primary maturation stages, one 

representative female was selected to show the typical 

oocyte-size-frequency-distribution (OSFD) (50 mm 

size classes) and the histological cross section 

(Fig. 4a±c). The enormous increase of size and volume 

of the advanced oocytes is obvious. In a reproductively 

Fig. 3. Frequency of oocytes in different maturity-classes in the entire ovary in comparison to the frequency in a single quarter of the ovary 

(1st quarter: caudal end; 4th quarter: cranial end).


Fig. 4. Combined representation of OSFD, GSI and histological cross section of different maturity stages in the ovary of E. punctifer: 

(a) immature ovary with unyolked oocytes; (b) maturing ovary with vitellogenic oocytes; (c) ripe ovary with hydrated oocytes shortly 

before spawning, the batch is clearly visible. U ˆ unyolked oocytes; V ˆ vitellogenic oocytes; H ˆ hydrated oocytes. 

active ovary, there is no gap in the OSFD. This means 

the oocyte development is continuous (Fig. 4a and b). 

The maturation of the oocyte and the growing GSI 

are also re¯ected in the increasing average oocyte 

diameter of the different gonads. The average oocyte 

diameter is 0.25, 0.3 and 0.5 mm, respectively. Shortly 

before spawning, the most advanced group of oocytes 

forms a new batch of hydrated oocytes, clearly separated 

in the OSFD from the developing oocytes cohort 

with sizes up to 0.5 mm (Fig. 4c). The diameter of


hydrated oocytes range from 0.8 to 1.2 mm …x ˆ 

0:95 mm†; whereas the average oocyte diameter of 

the ®rst cohort is 0.31 mm. 

In the cross section of an immature ovary, only 

small unyolked oocytes can be detected (Fig. 4a) 

usually within a size range of 0.05±0.25 mm. In a 

maturing ovary, oocytes in different vitellogenic 

stages are present, (Fig. 4b) while a hydrated ovary 

contains oocytes in all different developmental stages 

(Fig. 4c). The three histological photos (Fig. 4a±c): 

reveal the sequence of oogenesis of E. punctifer: (a) 

from small cells with basophilic cytoplasm; (b) the 

intermediate stage of maturing oocytes in different 

phases of vitellogenesis; and (c) the largest size with 

dissolving nucleus and fusion of yolk globules during 

hydration. As shown for other pelagic ®sh species 

(George, 1998), vitellogenesis in E. punctifer also 

starts at the cytoplasm periphery of the oocyte. 

The oocytes do not move to the cranial end of the 

ovary during maturation (Fig. 3). The oocytes develop 

simultaneously in all parts of the ovary. In the histological 

cross sections postovulatory follicles were 

detected, indicating that the referring specimen had 

recently spawned. Postovulatory follicles-if presentalways 

occur together with vitellogenic oocytes. The 

follicles consist of two cell layers: the internal granulosa 

and the very thin external thecal layer. Only a 

few single atretic (degenerating) oocytes occurred 

during this study. 

4. Discussion 

The absence of a correlation of the mean CF and the 

GSI of E. punctifer, as also shown for other pelagic 

®sh species (George, 1996, 1998), con®rmed the 

suggestion of Wright (1989): the condition of the 

anchovies is not dependent on gonadal weight. The 

necessary energy for gonad growth is not obtained 

from body fat, but most likely directly from food. The 

basic energy requirement is needed for swimming, 

body function, etc. and only a surplus of energy can be 

used for oocyte development. Hunter and Leong 

(1981) estimate 13% of the body weight for Engraulis 

mordax is necessary for a single batch. That means a 

change in prey density would have a direct in¯uence 

on the fecundity of E. punctifer. 

The high variability of the batch fecundity found for 

E. punctifer (Table 1) is similar to that of E. heteroloba 

(Dalzell, 1987) and E. purpurea (Clarke, 1987). 

Clarke (1987) explained seasonal differences in terms 

of water temperature, the temperature in summer in 

the study area being 58C higher than in winter. Wright 

(1989) suggested the availability of food as the main 

reason for regional and temporal differences of the 

batch fecundity in the genus Encrasicholina. Tiews et 

al. (1970) observed a spawning peak of E. punctifer, 

E. heteroloba and E. devisi in Manila Bay during the 

south-west monsoon, while primary production was 

very high. Parrish et al. (1986) found an age-speci®c 

fecundity in E. mordax. Variation of mean batch 

fecundity for a standardised female weight is 

described for Sardinops sagax, where batch fecundity 

increased with ovary-free body weight and length of a 

female (George, 1998). A comparative study of sardines, 

anchovies and sprats (Alheit, 1989) revealed a 

higher variability of batch fecundity within a spawning 

season, than interannual variations of batch 

fecundity. Additionally, Adrianov et al. (1996) found 

a marked daily cycle of oocyte development in the 

Black Sea Anchovy (Engraulis encrasicholus ponticus). 

The relationship of size at sexual maturity to maximal 

length with 0.504 ®ts very well to L max /L 1 ratio 

Beverton (1963) found for other Engraulidae. He 

showed, that the size at sexual maturity is proportional 

to maximal length. Smaller species reach size at 

sexual maturity, in proportion to their maximal length, 

Table 1 

Relative batch fecundity and length at sexual maturity (L t mm) of E. punctifer from the Indo-Pacific 

Country 

Mean relative 

batch fecundity 

S.D. Range N Sexual maturity 

(L t mm) 

Author 

West Sumatra 985 359 375±1851 35 55±59 Present study 

Papua-New- Guinea 875 301 713±1336 9 ± 1 Dalzell (1987) 

India ± ± 1236±8971 ± 45±49 Luther (1989) 

Philippines ± ± ± ± 65 Tiews et al. (1970)


faster than larger species (Blaxter and Hunter, 1982). 

One explanation for the different sizes at sexual 

maturity found by other authors (Table 1) is that they 

determined the sexual maturity macroscopically. In a 

multiple spawning ®sh with asynchronous oocyte 

development, without histological analysis it is critical 

to distinguish developing ovaries from those which 

®nished the individual spawning season and mature 

ovaries from those which are already partially spent. 

Important physiological processes like starting of the 

vitellogenesis and the beginning of the hydration are 

not macroscopically visible. In a serial spawner the 

identi®cation of postovulatory follicles is the only way 

to ®nd a partially spawned ovary. All this is only 

possible after histological analysis of the ovaries. 

The contemporary occurrence of postovulatory follicles 

and vitellogenic oocytes together in one ovary 

indicates that the studied species is a batch spawner. 

The high proportion of reproductive active females, 

their presence over the whole study time and the 

demonstrated OSFD of females indicate that E. punctifer 

is an indeterminate batch spawner. An extended 

spawning period of several months, or during the 

whole year, with possible bimodal intensity (not obligatory) 

is a character of an indeterminate serial spawning 

®sh (George, 1998). Any time of the year a 

particular percentage of the anchovies is able to 

spawn. For this ability a constant biotic environment 

is necessary, which is the case in tropical coastal 

waters off West Sumatra. Serial spawners produce 

more eggs than a comparable (in size) total spawner. 

Small ®sh like anchovies usually do not have enough 

space in the body cavity, that would be necessary to 

keep the total amount of oocytes produced per year at 

the same time. The hydration of the oocytes has to be 

divided into portions (Lozan, 1985). 

The results of this study could be used as a contribution 

for estimating the stock biomass, using the 

egg-production-biomass (EPM), developed under the 

guidance of Lasker (1985) and brie¯y reviewed by 

Alheit (1993). 

Additional knowledge about the spawning grounds 

is important to quantify the effect of variation in prey 

density to spawning biomass and indirectly to recruitment. 

Tzeng and Wang (1992) found spawning areas 

for E. punctifer in a mangrove estuary in Taiwan. 

Their study gave a ®rst link that the standing stock of 

E. punctifer is affected not only by the ®shery impact, 

but also by the human utilisation of the mangrove 

estuaries and the variation in prey density. 

Acknowledgements 

We would like to thank Dr. A. Kunzmann for the 

support at the Bung Hatta University of Padang, West- 

Sumatra. Special thanks go to Dr. W. Ekau and two 

unknown reviewers for the critical review of the 

manuscript. Very special thanks go to the people of 

Pasir Kandang, without whose generosity and cooperation 

the entire work would not have been possible. 

References 

Alheit, J., 1989. Comparative spawning biology of anchovies, 

sardines, sardines and sprats. Rapp. P.v. ReÂun. Cons. Int. 

Explor. Mer. 191, 7±14. 

Alheit, J., 1993. Use of the daily egg production method for 

estimating biomass of clupeoid fishes: a review and evaluation. 

Bull. Marine. Sci. 53(2), 750±767. 

Adrianov, D.P., Lisovenko, L.A., Bulgakova, Yu.V., Oven, L.S., 

1996. Reproductive ecology of the Black Sea anchovy 

(Engraulis encrasicholus ponticus): 1. Circadian rhythms of 

oogenesis and spawning. J. Ichthyology 36(7), 515±526. 

Bagenal, T.B., 1978. T. Methods for assessment of fish production 

in fresh waters. IBP Handbook No 3, 365 pp. 

Blaxter, J.H.S., Hunter, J.R., 1982. The biology of the clupeoid 

fishes. Adv. Marine. Biol. 20, 1±223. 

Beverton, R.J.H., 1963. Maturation, growth, growth and mortality 

of clupeid and engraulid stocks in relation to fishing. Rapp. P.v. 

ReÂun. Cons. Int. Explor. Mer. 154, 44±67. 

Clarke, T.A., 1987. Fecundity and spawning frequency of the 

Hawaiian anchovy or nehu, Encrasicholina purpurea. Fish. 

Bull. 85(1), 127±138. 

Dalzell, P., 1987. Some aspects of the reproductive biology of 

stolophorid anchovies from Northern Papua New Guinea. Asian 

Fish. Sci. 1, 91±106. 

Delsman, H.C., 1931. Fish eggs and larvae from the Java Sea. De 

Treubia 13, 217±242. 

George, M.R., 1996. Contributions to the use of condition factor: 

Studies of Spanish sardine, Sardinops sagax, and southern 

Pacific jack mackerel, Trachurus picturatus murphyi, off coast 

of Chile. ICES C.M. 1996/ H:4, p. 15. 

George, M.R., 1998. Die Fortpflanzungsbiologie zweier pelagischer 

Fischarten Sardinops sagax (Jenyns, 1842) (Clupeidae) 

und Trachurus picturatus murphyi Nichols 1920 (Carangidae) 

im Auftriebsgebiet Nordchiles. Biblothek Natur & Wissenschaft, 

Bd. 14, Verlag Natur & Wissenschaft, Solingen, 

133 pp.


Gerrits, P.O., 1985. Verfahren zur FaÈrbung von Gewebe, das in 

2-Hydroxyethyl-Methacrylat eingebettet wird., 2nd ed., 

Sonderdruck fuÈr Kulzer & Co GmbH, 31 pp. 

Grimes, C.B., 1976. Certain aspects of the life history of the 

vermillion snapper, Rhomboplites aurorubens, from North and 

South Carolina waters. Ph.D. Thesis, University of North 

Carolina, 240 pp. 

Hunter, J.R., Goldberg, S.R., 1980. Spawning indicence and batch 

fecundity in northern anchovy Encrasicholina purpurea. Fish. 

Bull. 77(3), 641±652. 

Hunter, J.R., Leong, R., 1981. The spawning energetics of female 

anchovy Engraulis mordax. Fish. Bull. 79(2), 215±230. 

Hunter, J.R., Macewicz, B.J., Lo, N.C.H., Kimbrell, C.A., 1992. 

Fecundity, spawning, spawning and maturity of female Dover 

sole, Microstomus pacificus, with an evaluation of assumption 

and precision. Fish. Bull. 90(1), 101±128. 

Lasker, R., 1985. An egg production Method for estimating 

spawning biomass of pelagic: application to the northern 

anchovy, Engraulis mordax. NOAA Technical Report NMFS 

36, 99 pp. 

Lozan, J.L., 1985. Wachstum, Rekrutierung. Netzselektion, Fortpflanzung 

und Fruchtbarkeit. Fischereibiologische Methoden, 

Vol. III. Hamburg: Institut fuÈr Hydrobiologie und Fischerei. 

Luther, G., 1989. Biology of whitebait anchovies of Indian waters. 

Tuna Baitfish in the Indo-Pacific Region. Proceedings of a 

Workshop, Honiara, Solomon Islands, pp.75±82. 

Parrish, R.H., Mallicoate, D.L., Klingbeil, R.A., 1986. Age 

dependent fecundity, number of spawnings per year, sex ratio, 

sex ratio and maturation stages in northern anchovy Engraulis 

mordax. Fish. Bull. 84(3), 503±517. 

Paula e Silva, R., 1992. Growth of the Bucaneer anchovy, 

Encrasicholina punctifer off Mozambique based in samples 

collected in research surveys. Rev. Invest. Pesq. Maputo 

(Mozambique) 21, 69±78. 

Rohdenburg, H., 1995. BeitraÈge zur Baganfischerei und zur 

BestandsabschaÈtzung von Encrasicholina punctifer (Engraulidae, 

Pisces) vor der KuÈste Padangs (West Sumatra, 

Indonesien). M.Sc. Thesis University of Bremen, Germany, 

47 pp. 

Soesanto, V., 1985. Indonesian small-scale fisheries development. 

South China seafisheries development and coordinating 

programme, Manila, Philippines, 41 pp. 

Tiews, K., Ronquillo, I.A., Santos, L.M., 1970. On the biology of 

the anchovies (StolephorusLaceÂpeÁde) in Philippines waters. 

Proc. Indo-Pacific. Fish. Counc. 13(II), 20±48. 

Tzeng, W.N., Wang, Y.T., 1992. Structure, composition, composition 

and seasonal dynamics of the larval and juvenile fish 

community in the mangrove estuary of Tanshui River, Taiwan. 

Mar. Biol. 113, 481±490. 

Wright, P.J., 1989. The reproductive strategy of Stolephorus 

heterolobus in the South Java Sea. Tuna Baitfish in the Indo- 

Pacific Region. Proceedings of a workshop, Honiara, Solomon 

Islands, pp. 83±88. 

Wright, P.J., 1992. Ovarian development, spawning frequency, 

spawning frequency and batch fecundity in Encrasicholina 

heteroloba (Rupell, 1858). J. Fish. Biol. 40, 833±844.

Contributions to the reproductive biology of encrasicholina punctifer ...

You also want an ePaper? Increase the reach of your titles

Delete template?

Save as template?