Effects of maternal conditions on early life history traits of black porgy Acanthopagrus schlegeli

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Þ 0888 Blackwell Wissenschafts!Verlag\ Berlin Accepted] May 04\ 0887 ISSN 9064Ð7548

Effects of maternal conditions on early life history traits of black porgy Acanthopagrus

schlegeli

Wen!Bin Huang0

\ Tai!Sheng Chiu0

and Chang!tai Shih1

0_{Institute of Zoolo`y\ National Taiwan University\ Taipei\ Taiwan\ R[O[C[^}1_{Institute of Oceano`raphy\ National Taiwan University\} Taipei\ Taiwan 095\ R[O[C[

Summary

This work examined the e}ects of maternal conditions on early life history traits of black porgy Acanthopagrus schlegeli[ Age! II females produced signi_cantly larger eggs as compared to the same size of Age!III females[ Also\ within each of the age groups\ there was a positive relationship between egg size and female size[ The larger eggs generally had larger volumes of oil globules\ required longer incubation periods "hatching age#\ and produced larger larvae that endured longer to starvation[ Hatching age was covaried negatively with yolk volume at hatching\ indicating that embryonic development consumed primarily yolk as its energy resource[ The condition factor\ gonadosomatic index\ hepatosomatic index\ and lipid content of the females were not related to the early life history traits of their o}spring[

Introduction

Concurrence of oceanographic conditions in favour of food production and _rst feeding of _sh larvae is critical to their survival "Lasker 0870#[ Starvation may account for most of the larval mortality "Elliott 0875#\ and fasting endurance is of importance for their survival "Ojanguren et al[ 0885#[ The size of larvae has been known to relate positively to the resistance to starvation "Hunter 0870^ Marsh 0875^ Miller et al[ 0877#[ It is reasonable to assume that in unfavourable conditions\ a larva with high fasting endurance has a better chance to overcome the situation than a larva with low endurance[

In the early life history of marine _sh\ larger eggs produce larger larvae that will subsist longer without food "Blaxter 0858^ Hempel 0868^ Hunter 0870#[ Larger eggs provide more energy for development "Hempel 0868#\ and larger larvae with more yolk might have a competitive advantage at birth "Lagomarsino et al[ 0877#[ These initial size advantages of the larger larvae probably account for some increase in their early growth and survival "Henrich 0877^ Hutchings 0880#[ Accordingly\ egg size is an important factor contributing to the survival of early life stages of _sh "Hinckley 0889#[ Although egg size is primarily determined genetically\ it is also a}ected by other factors such as age and size of the mother "Springate et al[ 0874#[ In some species of _sh\ older and heavier females produce larger eggs than younger and lighter females "Beacham and Murray 0874#[ As the mother|s condition is one of the important factors that a}ect the survival of larvae\ it should be explicitly considered when e}ects of egg size on the early life history traits are gen! eralized "Chambers et al[ 0878#[

The black porgy\ Acanthopagrus schlegeli\ is widely dis! tributed and considered as one of the valuable commercial

U[S[ Copyright Clearance Center Code Statement]9064Ð7548:88:0491Ð9976,03[99:9

species in many parts of Asia "Chang and Yueh 0889#\ par! ticularly in Taiwan and Japan[ It is one of the dominant species in the _sh larval community in the coastal waters of western Taiwan "Huang and Chiu 0886#[ Embryonic and larval devel! opment of the black porgy have been described by Fukuhara "0876#[ In this study we intended to determine whether the maternal condition of black porgy a}ects egg size and early life history traits of their o}spring[

Materials and methods

Thirty ripe females] black porgy\ 05 Age!II _sh and 03 Age!III _sh\ were collected in March 0886 and 0887 from the brood! stock _sh ponds at the Tainan Branch of Taiwan Fisheries Research Institute[ They were unfed\ acclimated in 599 L tanks for 1Ð2 days\ and divided into _ve groups "blocks# for fer! tilization according to their time of ovulation[ Eggs from each female were fertilized with milt from one male[ The fertilized eggs were then transferred to two 0!L beakers to replicate the experiment[ The acclimation of the females and the experiment with eggs and larvae were conducted at a temperature of 10 2 9[4 >C\ salinity of 23 2 9[4 -\ and photoperiod of 00!h light and 02!h dark[

For each of the females\ body weight and standard length were measured before fertilization^ immediately thereafter the gonad\ liver and other visceral organs were removed and weighed[ The _sh and visceral organs were then frozen[ Later "within six weeks# samples were collected from the dorsal muscle\ ventral muscle\ and liver and their lipid contents deter! mined by the method described by Folch et al[ "0846#[ Maternal conditions studied were] "0# age "1# body size "2# condition factor "body weight:standard length2

# "3# gonadosomatic index "gonad weight:body weight# "4# hepatosomatic index "liver weight:body weight# "5# ratio of visceral organ "excluding gonad and liver# weight to body weight\ and "6# percentage contents of lipid in dorsal muscle\ ventral muscle\ and liver[

For eggs and larvae\ seven early life history traits were exam! ined] "0# egg volume "egg size# "1# oil globule volume in egg at the morula stage three hours after fertilization "2# hatching age "incubation period of egg# "3# body length of hatchling "larva immediately after hatching# "4# yolk volume of hatchling "5# oil globule volume of hatchling\ and "6# life span of larva[ Egg volume\ oil globule volume of egg and oil globule volume of hatchling were estimated by measuring their diameters[ Hatch! lings were anaesthetized in the 299 mg L−0

1!phenoxyethanol solution and their body length\ length and height of yolk\ and diameter of oil globule were measured[ Because the yolk of a hatchling is oval in shape\ its volume was estimated by its length and height\ and subtracted from the volume of oil globules it

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contained[ The larvae were unfed during the experiment\ and the duration "days# between the time of hatching and the time of death of a larva was recorded as its larval life span\ the endurance level to starvation[

The relationship between pairs of traits was assessed by the coe.cient of partial correlation[ A two!stage nested design\ with 29 females nested under 4 groups of fertilization\ was used to determine the female|s e}ect on each of the early life history traits "Montgomery 0886#[ The percentages of the total variance due to the female source were compared among the early life history traits[ The e}ects of maternal condition on early life history traits were assessed by the coe.cient of simple corre! lation[ In addition\ the relationship of a female|s condition to her egg size was determined by multiple linear regression analysis[

Prior to analysis we logged transformed egg volume\ oil glob! ule volume in egg\ and yolk and oil globule volumes of each hatchling[ Two!stage nested design\ variance components in

ANOVA\ and partial and simple correlations were performed and estimated using SAS "SAS Institute\ Inc[ 0876#[

Results

The egg volumes from 29 females ranged between 9[143 and 9[392 mm2

with a mean 2 standard deviation of 9[214 2 9[920 mm2

"n 899#[ The variations in egg volume and its oil globule volume were fairly similar with the coe.cient of vari! ation "CV\ standard deviation:mean# of 9[98 and 9[00\ respec! tively[ The variations were high for yolk volume and oil globule volume of each hatchling "CV 9[04 and 9[05#\ and low for hatching age\ body length of hatchling\ and life span of larva "CV 9[93\ 9[93\ and 9[95#[

There were eight signi_cant coe.cients of partial correlation between early life history traits "Fig[ 0#[ Oil globule volume in egg\ incubation period\ body length of hatchling\ and yolk volume of the hatchling were covaried with egg volume[ Yolk volume of the hatchling increased with increasing oil globule volume of the hatchling but decreased with increasing hatching age[ Oil globule volumes of hatchling and egg were correlated[ Body length of the hatchling was the only trait that covaried with the larval life span[ Compared to smaller eggs\ larger eggs had larger oil globule volumes\ longer incubation periods for hatching\ and produced larger larvae\ which had larger energy reserves "i[e[ yolk and oil globule# to endure longer to starvation[ The above _ndings indicated that egg volume was the most important early history trait which determined most of the other traits for black porgy[ The negative correlation between yolk volume of hatchling and hatching age suggest that yolk\ not oil globule in the yolk\ is the main energy source for the embryonic development[

Each of the early life history traits varied signi_cantly among the 29 females\ however\ not the blocks of fertilization "Table 0#[ The percentage of variance due to maternal parents was greater for egg volume and hatching age "Table 1#[ None of the early life history traits was signi_cantly related to the size of the mother "P × 9[94# when the two age groups were combined[ When the age factor was statistically removed by linear regression\ egg volume\ hatching age\ and body length and yolk volume of hatchling were signi_cantly positively correlated to standard length and body weight of females "Table 1#[ Also\ the larval life span was signi_cantly positively correlated to the ratio of visceral organ weight to body weight of the females\ which was mainly due to high content of fat tissue around the intestine[ No signi_cant correlation was found between other

maternal conditions "condition factor\ gonadosomatic index\ hepatosomatic index\ and the lipid contents of muscles and liver# and the early life history traits of the o}spring "Table 1#[ The multiple regression equation between egg volume "Y\ dependent variable# and age "X0# and body weight "X1# of females "independent variables# was expressed by Y 136[0Ð 65[9 X0¦ 9[159 X1Ð9[905 X0X1\ where if Age!II then X0 9 and if Age!III then X0 0 "d[f[ 2\ 785\ R1 9[348\ F!value 142[4\ P 9[999#[ This equation showed that when the 29 females were divided into Age!II and Age!III groups\ within each of the age groups there was a signi_cantly regressive relationship between egg volume and female body weight "Fig[ 1#[ Analysis of covariance suggested that the slopes of the regression lines of the two age groups were not signi_cantly di}erent "d[f[ 0\ 785\ F!value 9[573\ P 9[397#\ but that the elevations of the two lines were signi_cantly di}erent "d[f[ 0\ 785\ F!value 46[79\ P 9[999#[ In other words\ Age!II females produced larger eggs per unit of body weight than Age!III females[

Discussion

Egg size

The results of this study demonstrated that the black porgy larvae from large eggs with large oil globules had longer incu! bation periods and had larger size and yolk reserves at hatching than those from small eggs "Fig[ 0#[ The positive relationship of body length and yolk volume of hatchlings to egg size has been documented in several species of _sh "Miller et al[ 0884^ Chambers and Leggett 0885#\ particularly in salmonids "Springate and Bromage 0874^ Lagomarsino et al[ 0877#\ but a few studies reported no such correlation "Reagan and Conley 0866^ Bengston et al[ 0876\ Lagomarsino et al[ 0877#[ In con! trast to the absence of association between size of egg and in! cubation period and between initial yolk volume in eggs and hatching size "Blaxter 0877#\ these associations were distinct in the black porgy "Fig[ 0#\ similar to the _ndings in the capelin by Chambers et al[ "0878#[

Temporal matching of resources and consumers is critical to the survival of _sh larvae "Lasker 0870#[ High fasting endurance should increase the chance of encountering suitable food before the onset of irreversible starvation\ and increase the chance of survival "Chambers et al[ 0878#[ O}spring performance traits are positively size!dependent "Marsh 0875^ Sinervo and McEd! ward 0877^ Sinervo 0889#[ Larvae hatched from relatively large eggs with more yolk might have a competitive advantage at birth over larvae from smaller eggs with less yolk "Blaxter and Hempel 0852^ Bagenal 0858^ Lagomarsino et al[ 0877#[ Also\ larger larvae are less restricted to the timing of _rst feeding and the size of prey "Miller et al[ 0884#[ In this study\ the longer life span of starved larvae of the black porgy with the trait of large hatchling sizes "Fig[ 0# agreed with most of the previous reports that body size is positively related with the resistance to star! vation "Hunter 0870^ Marsh 0875^ Miller et al[ 0877#[ In addition\ the successful initiation of feeding of _sh larvae is considerably a}ected by their size and condition\ such as the amount of their energy reserves "Heming 0871#[ Also\ their predation pressure is negatively correlated with their size "Miller et al[ 0877#[ Reduction in larval size at hatching was considered to be analogous to a sublethal response "Rosenthal and Alderdice 0865#[ The initial size advantage of _sh larvae prob! ably accounts for some of the increase in their early survival and growth "Henrich 0877^ Hutchings 0880#[

It has been proposed by numerous authors that egg size in~uences larval survival through its e}ect on larval size\ growth

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Fig[ 0[ Partial correlations between early life history traits of the black porgy\ Acanthopagrus schlegeli[ Only signi_cant correlations are shown "P ³ 9[94\ d[f[ 42#

Table 0

Analysis of variance table for the e}ects of fertilized blocks and females on egg volume "EV#\ oil globule volume in egg "OVE#\ hatching age "AGE#\ body length at hatching "BL#\ yolk volume at hatching "YV#\ oil globule volume at hatching "OVH#\ and life span "LS# of black porgy\ Acanthopagrus schlegeli

Source of Sum of

variation squares df Mean square F!ratio P!value

EV

blocks 9[565 3 9[058 9[64 9[455

females "within blocks# 4[505 14 9[114 019[83 9[999

Error 0[505 769 9[991

OVE

blocks 0[964 3 9[158 0[37 9[128

Error 5[329 769 9[996

AGE

blocks 153[4 3 55[01 0[07 9[231

Error 281[1 769 9[34

BL

blocks 9[298 3 9[966 9[42 9[607

Error 2[119 769 9[993

YV

blocks 9[819 3 9[129 9[45 9[586

Error 7[706 769 9[909

OVH

blocks 2[329 3 9[747 1[28 9[966

Error 09[741 769 9[901

LS

blocks 1[056 3 9[431 9[05 9[845

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Percentage of total variance in each early life history trait due to maternal e}ect\ and coe.cients "r!value# of correlation of the traits to maternal conditions of the black porgy "SL\ standard length^ BW\ body weight\ CF\ condition factor^ GSI\ gonadosomatic index^ HSI\ hepatosomatic index^ RVB\ ratio of visceral organ "excluding gonad and liver# weight to "BW#

Egg Oil globule Age at Length at Yolk vol[ Oil globule vol[ Posthatching vol[ vol[ in egg hatching hatching at hatching at hatching lifespan

0# ) variance 60[91 26[62 57[92 40[99 40[46 27[43 35[69 1# Maternal size SL 9[63 9[15 9[36 9[32 9[34 9[96 9[21 BW 9[64 9[24 9[37 9[30 9[31 9[19 9[07 2# CF −9[05 9[96 9[92 −9[21 −9[12 9[97 −9[22 3# GSI 9[01 9[00 9[22 −9[29 −9[11 9[05 −9[02 4# HSI −9[00 −9[23 −9[94 9[97 −9[92 9[95 −9[96 5# RVB −9[94 9[01 −9[24 9[22 9[00 9[08 9[49 6# Crude Lipid ")# Dorsal muscle −9[19 −9[22 −9[92 −9[18 9[19 9[11 −9[00 Ventral muscle −9[02 −9[29 9[92 9[93 9[08 9[06 −9[93 Liver −9[07 9[95 −9[92 −9[14 9[90 9[24 −9[98 Signi_cant at 4) level "P ³ 9[94#[ Signi_cant at 0) level "P ³ 9[90#[

Fig[ 1[ A plot of egg volume "mean 2 0 standard deviation# on body weight of its mother in two year classes of the black porgy

rate\ mouth size\ and length of time from hatching to starvation "Blaxter and Hempel 0852^ Bagenal 0858^ Ware 0864^ Knutsen and Tilseth 0874#[ Larger eggs provide more energy for growth and development and generally produce larger larvae which are able to avoid predators more e}ectively\ survive longer without feeding\ search through a larger volume of water for prey\ and eat prey of a greater variety of sizes "Hinckley 0889#[ If growth rates are positively related to initial body size "Ojanguren et al[ 0885#\ larger larvae will spend less time at the most vulnerable sizes "Miller et al[ 0877#[ Large size also provides a potential advantage in competition for territory "Huntingford et al[ 0889#[ On the other hand\ larger eggs take more time to incubate "Chambers et al[ 0878^ Wootton 0883^ this study#[ If egg pre! dation is size dependent or daily mortality rate is higher in the embryonic than in the larval period\ producing large eggs and an extended embryonic period are seen as the cost for being large at hatching "Chambers et al[ 0878^ Miller et al[ 0884#[

Age and size of mother

Variation in the sizes of marine _sh eggs has been associated with numerous factors including latitude\ temperature\ salinity\ egg batch sequence\ availability of food for larvae\ seasons of spawning\ years\ population origin\ and status of maternal parent "Bagenal 0860^ Springate and Bromage 0874^ Crisp 0883#[ Di}erences in egg size are thought to re~ect adaptations

by the spawning stock to varying conditions met by early larvae "Hinckley 0889#[ Maternal e}ects on egg size have been reported for a number of marine and freshwater species of _sh "Cham! bers and Waiwood 0885#[ In this study\ within the same age of black porgy\ larger size _sh produced larger size eggs "Table 0\ Fig[ 1#[ In numerous studies the egg size!female parental size relationships have been documented "Hinckley 0889#[ By contrast\ Wootton "0881# stated that in teleosts generally\ there is only a weak relationship between maternal body size and egg size\ except in some _shes such as Salmonidae[ However\ the larvae from larger parents could have inherited higher growth rates "Ojanguren et al[ 0885#[ The o}spring from larger parents with initial size advantage at hatching and with inherited higher growth rates are in favour of survival[

Nutritional status of mother

The di}erence in nutritional status of rainbow trout caused the di}erences in egg number\ diameter and chemical composition of the eggs\ and their hatchability "Springate et al[ 0874#[ Nutritional status of _sh is related to the food levels experienced before[ Evidence of the positive e}ects of female ration and condition factor "Fulton|s k# on egg size was reported by Hislop et al[ "0867# and Chambers and Waiwood "0885#\ respectively[ Chambers and Leggett "0885# concluded that maternal e}ects on o}spring are signi_cantly modulated by the environment experienced\ including water temperature and food levels\ by the female before reproduction[

In this study\ most of the conditions of mothers were unre! lated to egg size and other early life history traits\ but the ratio of visceral organ weight and body weight was related to the life span of the starved larvae "Table 1#[ This indicated that the lipid stored around the organs was an important contribution to the fasting endurance because the high weight ratio was due mainly to the increasing lipid tissue content around the intestine[ Chambers et al[ "0878# also found that an increase in oil globule volume of hatchlings extended the time of survival under star! vation in larvae[ However\ Chambers and Waiwood "0885# suggested that detecting a condition e}ect on egg size may require more direct and sensitive measures of condition[ Hinck! ley "0889# argued that gonad and liver are not particularly sensitive indicators of condition in _sh and use of the measures of these organs may have obscured a correlation between egg

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size and female parental size or conditions[ Therefore\ a possible explanation for most conditions of the maternal parent when\ unrelated to egg size and other early life history traits\ was that the conditions of the maternal parents used in this study were not sensitive enough to re~ect the condition of oogenesis of the _sh[

In conclusion\ larger females "within the same age\ i[e[ with higher growth rates# produce larger eggs which produce larger larvae with more energy available for initial growth "larger yolk reserves# and have higher resistance to starvation[ Choice of the adult _sh with high growth rate within a year!class to produce large o}spring for size advantage and with con! siderably higher fecundity to produce more eggs\ may be con! sidered for the broodstock of the black porgy in aquaculture[

Acknowledgements

We are grateful to Dr Y[ Y[ Ting\ Mr S[ L[ Yeh\ Mr Y[ T[ Chu and Mr J[ R[ Hseu of the Tainan Branch\ TFRI for donating the _sh used and o}ering assistance in this study\ and Dr W[ L[ Liao and Dr C[ M[ Kuo of the Institute of Fisheries Science\ National Taiwan University for their suggestions and assistance in lipid extraction[ The authors also wish to thank Dr C[ F[ Tsai and two anonymous referees for reading and commenting on the manuscript[

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University\ Taipei\ Taiwan 095\ R[O[C[ E!mail] d1194909Ýccms[ntu[edu[tw