9
This article was downloaded by: [The University of Manchester Library] On: 18 December 2014, At: 11:04 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Marine Biology Research Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/smar20 Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions Elena Baeza-Rojano a , José M. Guerra-García a , M. Pilar Cabezas a & Isabel Pacios a a Laboratorio de Biología Marina, Dpto. Fisiología y Zoología, Facultad de Biología , Universidad de Sevilla , Sevilla, Spain Published online: 04 Dec 2010. To cite this article: Elena Baeza-Rojano , José M. Guerra-García , M. Pilar Cabezas & Isabel Pacios (2011) Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions, Marine Biology Research, 7:1, 85-92 To link to this article: http://dx.doi.org/10.1080/17451001003713571 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions

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Page 1: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

This article was downloaded by: [The University of Manchester Library]On: 18 December 2014, At: 11:04Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK

Marine Biology ResearchPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/smar20

Life history of Caprella grandimana (Crustacea:Amphipoda) reared under laboratory conditionsElena Baeza-Rojano a , José M. Guerra-García a , M. Pilar Cabezas a & Isabel Pacios aa Laboratorio de Biología Marina, Dpto. Fisiología y Zoología, Facultad de Biología ,Universidad de Sevilla , Sevilla, SpainPublished online: 04 Dec 2010.

To cite this article: Elena Baeza-Rojano , José M. Guerra-García , M. Pilar Cabezas & Isabel Pacios (2011) Life history ofCaprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions, Marine Biology Research, 7:1, 85-92

To link to this article: http://dx.doi.org/10.1080/17451001003713571

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose ofthe Content. Any opinions and views expressed in this publication are the opinions and views of the authors,and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be reliedupon and should be independently verified with primary sources of information. Taylor and Francis shallnot be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and otherliabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to orarising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Page 2: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

ORIGINAL ARTICLE

Life history of Caprella grandimana (Crustacea: Amphipoda) rearedunder laboratory conditions

ELENA BAEZA-ROJANO*, JOSE M. GUERRA-GARCIA, M. PILAR CABEZAS &

ISABEL PACIOS

Laboratorio de Biologıa Marina, Dpto. Fisiologıa y Zoologıa, Facultad de Biologıa, Universidad de Sevilla, Sevilla, Spain

AbstractGrowth, maturity, and reproduction of 112 juveniles of Caprella grandimana obtained from 26 ovigerous females werestudied under laboratory conditions at 178C, and with a 12-h photoperiod. The newly hatched juveniles were transferred tosmall glass containers and fed with a mixture of diatoms Phaeodactylum tricornutum and Tetraselmis chuii (1:1). Afteremerging from the brood pouch, caprellids were considered as Instar I (1 mm length). Sexes were not able to be identifieduntil Instar III. In males the moulting interval gradually increased up to Instar X, producing a final instar which livedsignificantly longer than the previous one. Female intermoult period remained constant until they died. The body lengthand flagellar articles increased faster in males than females at each instar. Females reached the mature stage at Instar V andVI with a mean of 38.4 days, producing their first brood 10 days later at 49.1 days. The mean of eggs produced by eachfemale was 7.6 and the number of offspring emerged was 5. There was a significant correlation between the average lengthof the female in each instar and the number of eggs and offspring per brood. This is the first time that a Mediterraneanspecies has been successfully reared under laboratory conditions. These studies are basic for future ecotoxicological researchand management of the caprellid species.

Key words: Amphipod, Caprella grandimana, laboratory culture, life cycle, Tarifa Island

Introduction

Caprella grandimana (Mayer, 1882) is a common

amphipod species spread throughout the Mediterra-

nean Sea (Krapp-Schickel 1993) and the Atlantic

African coast from Cape Spartel to Cap Blanc

(Morocco) (Bellan-Santini & Ruffo 1998). In the

Straits of Gibraltar, this species is mainly found

associated to the algae Corallina elongata (J. Ellis

and Solander) and Jania rubens ((Linnaeus) J.V.

Lamouroux) in low intertidal zones throughout the

year.

The body is smooth except for the 5th to 7th

pereonites, which carry small humps (Figure 1). The

head lacks a rostrum, with antenna 1 about half

the body length, and the flagellum slightly shorter

than the peduncle, with short setae. The gnathopod

2 propodus on the male is elliptical, nearly twice as

long as broad, the dorsal edge with a few short setae,

and convex palm with one very acute process which

delimits a concavity filled with a membranous sac,

distally with a triangular process. Guerra-Garcıa

et al. (2001) redescribed C. grandimana based on

specimens from the Straits of Gibraltar, and pointed

out the presence of two abdominal appendages in

males instead of one.

During the last decade, an effort has been under-

taken to contribute to the knowledge of the Caprel-

lidea from the Iberian Peninsula and nearby areas,

especially in the Straits of Gibraltar (e.g. Guerra-

Garcıa et al. 2000, 2001, 2002; Guerra-Garcıa 2001;

Guerra-Garcıa & Takeuchi 2002), since this is where

there is a very high proportion of endemic Caprelli-

dea species, contributing 30.8% to the endemism of

the Mediterranean population. However, nowadays,

the ecological knowledge and life history of peracarid

fauna including caprellids over this region is still very

scarce. No studies have been carried out on growth

*Correspondence: E. Baeza-Rojano, Laboratorio de Biologıa Marina, Dpto. Fisiologıa y Zoologıa, Facultad de Biologıa, Universidad de

Sevilla, Avda. Reina Mercedes 6, 41012, Sevilla, Spain. E-mail: [email protected]

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory,

University of Copenhagen, Denmark

Marine Biology Research, 2011; 7: 85�92

(Accepted 15 January 2010; Published online 2 December 2010; Printed 16 December 2010)

ISSN 1745-1000 print/ISSN 1745-1019 online # 2011 Taylor & Francis

DOI: 10.1080/17451001003713571

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Page 3: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

rate and maturity periods of the Caprellids from this

zone and all the existing information is based on

species collected from other latitudes. In colder

waters, Caprella septentrionalis (Krøyer, 1839),

Pseudoprotella phasma (Montagu, 1804), and Caprella

acanthifera (Leach, 1814) showed short reproductive

periods or a limited number of generations per year

(Heptner, 1963; Hughes, 1978; Costello & Myers,

1989). On the other hand, Caprella danilevskii

(Czerniavski, 1868), Caprella tsugarensis (Utinomi,

1947), Caprella decipiens (Mayer, 1890), Caprella

verrucosa (Boeck, 1871), and Caprella okadai

(Arimoto, 1930), collected from warmer Japanese

waters, continued their reproductive cycle for almost

the whole year (Imada & Kikuchi 1984; Aoki 1988;

Takeuchi et al. 1990). Samples of C. grandimana

collected every two months during a two-year

period (Guerra-Garcıa et al. 2009a) proved that

C. grandimana reproduces all year around.

Currently, P. phasma, C. danilevskii, C. okadai, and

the invasive Caprella mutica (Schurin, 1935) have

been the only species successfully reared under

laboratory conditions in order to follow any signs

of moulting as well as spawning to attain knowledge

of their complete life history (Harrison 1940;

Takeuchi & Hirano 1991, 1992a; Cook et al. 2007).

Corallina elongata is one of the most abundant

calcareous macroalgae in the shallow waters of the

Mediterranean, and forms the ‘Corallina elongata

community’ between 0 and 5 m depth. Many authors

have indicated the presence of communities domi-

nated by C. elongata on the coasts of the western

Mediterranean (Gili & Ros 1985; Ballesteros 1988;

Soltan et al. 2001). This species constitutes one of

the dominant algae in the intertidal ecosystems in the

Straits of Gibraltar (Guerra-Garcıa et al. 2006).

Five species of caprellids have been recorded as

being associated with the intertidal algae Corallina

elongata in this area: C. acanthifera, C. grandimana,

Caprella hirsuta (Mayer, 1890), Caprella liparotensis

(Haller, 1879), and Caprella penantis (Leach, 1814).

Caprella grandimana and C. penantis are the most

common species showing a density up to 2000�3000

ind l�1 of algae, respectively (Guerra-Garcıa et al.

2009b).

In the present study, we focused on the life history

of C. grandimana, one of the dominant peracarid

species in the intertidal ecosystems of the Straits of

Gibraltar.

Material and methods

Tarifa Island (36800?00.7??N, 5836?37.5??W) is a

marine reserve located within the ‘Parque Natural

del Estrecho’ in the Gibraltar Straits. It represents

the southernmost enclave of Europe and its inter-

tidal ecosystems are among the most diverse of the

Iberian Peninsula. Caprella grandimana was collected

from Corallina elongata and Jania rubens in the low

intertidal zone of Tarifa Island at low tide, in

December 2007 and March 2008. The individuals

studied were taken directly off the algae in the field,

and in the laboratory 26 ovigerous females were

selected and isolated in small glass containers of

120 ml with a diameter of 6.5 cm and 6 cm in height.

A 1 mm plastic mesh, replaced weekly, was used as a

substratum for attachment. One hundred and twelve

newly hatched individuals were monitored through-

out their complete life cycle. The hatchlings were

introduced into new glass containers in groups of a

maximum of five individuals without the female,

since no evidence of maternal care was found for this

species; young did not cling to their mother, nor

did they remain together. During the first days, the

plastic mesh was substituted for small pieces of

J. rubens and C. elongata for the juveniles. Once

they reached maturity, a pair of females and males

were selected and placed in separate glass vessels.

The male was separated from the female when eggs

were present in the brood pouch. They were main-

tained at 178C with a photoperiod of 12 h light:

12 h dark. We selected this temperature because it

represents the average temperature throughout the

year in the sampling site at Tarifa Island (personal

observation, Guerra-Garcıa et al. 2004). The sea-

water used for culture was artificial water (ReefSalt

of SeachemTM) prepared with a salinity of 35.5. The

water in the glass containers was changed daily.

Individuals were fed with a mixture of algae,

made from lyophilized colonies of the diatom

Phaeodactylum tricornutum ((Bohlin) Lewin) and

Tetraselmis chuii (Butcher) (1:1). Previous studies

Figure 1. Schematic drawing of the lateral body shape of Caprella

grandimana from Tarifa Island. Refigured from Guerra-Garcıa

et al. (2001). Scale bar: 1 mm.

86 E. Baeza-Rojano et al.

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Page 4: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

on total fatty acid composition of individuals col-

lected from the Strait of Gibraltar suggested a

greater contribution of diatoms and macroalgae in

the diet of C. grandimana (Guerra-Garcıa et al.

2004). These colonies were prepared daily, resus-

pended in the artificial seawater and introduced

once a day by pipette into each vessel. The caprellids

held the diatom colonies with their first gnathopods

and consumed them using their maxillipeds.

All the specimens were observed daily under a

binocular microscope for any signs of spawning,

moulting, or release of the young. Caprellids moulted

successively after their emergence from the brood

pouch, at Instar I (according to the system adopted by

Takeuchi & Hirano 1991), until their death. At each

instar stage after each moulting, body length was

measured while the caprellids remained with their

pereonites straightened over the mesh. The number

of flagellar articles on the first antenna was also

counted. The maturation stage of the female was

classified at immature, premature and mature stage

by the study of the morphology of the paired

oostegites located on pereonites III and IV (Takeuchi

1989).

The number of eggs could be counted through the

transparent oostegites of the brood pouch, as well as

the number of offspring that emerged from each

female in each reproduction event.

Mating behaviour was observed daily in each

container for 5 min.

Statistical analyses

Possible differences of life span, body length and

moulting intervals between males and females were

tested with a Kruskal�Wallis test. Univariate ana-

lyses were carried out using SPSS 17.

Results

Life span and survival

Forty-nine females and 53 males from 26 ovigerous

females of Caprella grandimana collected from Tarifa

Island were studied under laboratory conditions for

their whole life span, reaching on average, a survival

cycle of 104.5940.3 days, at 178C. Females lived

120.2944.7 days (mean9S.D.) and males 89.99

29.3 days (mean9S.D.), attaining a maximum of

209 days and 127 days, respectively (Table I);

females had a life span significantly longer than

males (Kruskal�Wallis�15.6, pB0.001).

Both females and males had a very high survival

rate during their first period of the life cycle, but it

began to decrease at Instar VI during the reproduc-

tive phase (Figure 2a). Males suffered a very marked

decrease of their survival rate during the last three

instars, with only 13% surviving at the last instar

(Figure 2b).

Moulting cycle

The moulting rate was found to be higher in

females than males, as females always moulted after

the release of their young from the brood pouch.

Figure 3 indicates the number and duration of each

instar in males and females. Males only reached

Instar X after nine moults while females continued

to Instar XVIII, moulting 18 times (Table I).

Caprellids have been observed eating their own

exuviae.

Newly hatched juveniles moulted every 6.4�10.8 days until reaching Instar IV, when their gender

could be identified under a binocular microscope.

The development in the young females of an

immature brood pouch in their pereonites was clear.

Later, the moulting intervals of males gradually

increased from 6.992.9 to 32.4911.4 days until

the last Instar X.

The time between the last moult and death among

all males was 32.5914.1 days, which was signifi-

cantly longer than all their previous moulting inter-

vals (Kruskal�Wallis�34.4, pB0.001). (In the final

period before they die, males of Caprella grandimana

have an accumulation of particles which completely

covers their body surface.)

Table I. Life history traits of Caprella grandimana reared in the laboratory (temperature 178C, salinity 35.5. M�male, F�female).

Life-cycle criteria M/F Range Mean 9SD n

Life span (days) M 36�127 89.9 29.3 53

F 38�209 120.2 44.7 49

Number of moults M 3�9 7 1.4 51

F 3�18 10 3.5 49

Mature body length (mm) M 4.5�6.7 5.4 0.8 51

F 2.9�4.8 4 0.4 42

No. of juveniles per brood (average) F 1�15 5 3.5 57

No. of eggs per brood (average) F 1�18 7.6 3.8 231

Incubation time (days) F 7�13 10.5 1.3 49

Sexual maturity of females (days) F 21�67 38.4 8.5 45

Life history of Caprella grandimana 87

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Page 5: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

In females, the moulting frequency gradually

increased from 8.293.1 to 13.994.1 until Instar

V, and stabilized at 10.8�16.9 days from Instar V to

Instar XVIII. In contrast to males, the moulting

interval from last moult to death was not signifi-

cantly different to the rest of intervals.

Growth rate: body length and number of flagellar articles

of antenna 1

The growth rate was the same for males and females

before their gender was determined. After Instar IV,

the males had a higher size increment per moulting

within a shorter period compared to females.

Growth increment per instar is given in Figure 4.

Males increased the body length at each instar,

following a straight-line growth rate, reaching a

maximum value of 6.7 mm at Instar XI. The average

male body length was 5.4 mm for all mature stages.

However, in females, the rate of increase of body

length followed a polynomial curve, generally higher

in early developmental stages and decreasing after

Instar XVI. The maximum length was 6.7 mm in

males and 4.8 mm in females (Table I). Significant

differences could be found in body length between

males and females after Instar VI (Kruskal�Wallis,

pB0.001).

The number of flagellar articles in the antenna 1

was always two in newly born juveniles, plus three

basal articles at the peduncle. Males increased one

article in the flagellum before each moulting up to

Instar IX and females up to Instar VII. Afterwards,

males and females increased less than 1 article

per moulting (Figure 5). The number of flagellar

articles was always higher in males than females in all

instars from their gender differentiation stage. The

0

25

50

75

100(a)

(b)Instar

Sur

viva

l rat

e (%

)

0

25

50

75

100

I II III IV V VI VII VIII IX X XI XIII XIV XV XVI XVII XVIII XIX

IV V VI VII VIII IX X XI XII XIII XIV XVI XVII XVIII XIX

Instar

Sur

viva

l rat

e (%

) Females

Males

Figure 2. (a) General survival rate in Caprella grandimana at each

instar in laboratory conditions. (b) Survival rates of males and

females of Caprella grandimana reared in laboratory conditions.

Juvenile Instars I�III were not separated into males and females,

since their gender could not be identified under a binocular

microscope.

0

10

20

30

40

50

I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIII XIX

Instar

Dur

atio

n (d

ays)

MalesFemalesJuveniles

Figure 3. Duration of each instar (Mean9S.D.) in males, females and juveniles of Caprella grandimana. Instars I�III juveniles were not

separated into males and females, since the gender could not be identified under a binocular microscope.

Females;y = -0,019x2 + 0,6018x + 0,4397

R2 = 0,9976

Males;y = 0,6203x + 0,2015

R2 = 0,9899

0

2

4

6

8

I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIIIXIX

Instar

Bod

y le

ngth

(m

m)

Females

Males

Juveniles

Figure 4. Total body length and growth increment per instar

(Mean9S.D.) in males, females and juveniles of Caprella

grandimana. Juvenile Instars I�III were not separated into males

and females, since gender could not be differentiated.

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Page 6: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

maximum number of articles was 11 in males and 10

in females.

Maturation and sex ratio throughout the lifespan

Eighty-six per cent of the females reached the

mature stage at Instar V and VI and only 11% at

Instar VII. So a mature stage was achieved on

average of 38.498.5 days after emergence from the

brood pouch (Table I). Clutches of ovigerous

females collected from Tarifa resulted in a similar

number of females and males (49 females/53 males),

but the number of males decreased due to mortality

at an earlier age, consequently the number of males

was relatively lower than females towards the end of

the life cycle.

Mating behaviour and reproduction

Precopulatory mate-guarding was not observed in

Caprella grandimana during the study; males did not

carry the female until she could be fertilized to

guard her against other males. Instead, males only

came into contact with females to check if they were

receptive. After moulting took place, females were

ready to be fertilized, and the male would grasp

the female with the first gnathopods and pereiopods

5 and formed the precopulatory pair in the same way

described for the reproductive behaviour of Caprella

laeviuscula by Caine (1991), and Caprella scaura by

Lim & Alexander (1986). After oviposition, a mass of

eggs appeared into the brood pouch. No females were

found with eggs in the brood pouch in the absence of

males. The incubation period of the embryos was

recorded as the period from copulation to release of

juveniles from the brood pouch. The average incuba-

tion period for this species was 10.591.3 days. Thus,

the average generation length of this species was

estimated to be 48.9 days at 178C (Table I).

Fertility

The average number of embryos produced from

a single female in a single brood was 7.693.8,

increasing from 4 at Instar V to 18 at Instar XVIII.

The number of offspring that finally emerged from

the brood pouch was 5.093.5, half of the total

number of eggs released into the brood pouch, and a

maximum of 15 juveniles emerged at Instar XVIII

(Table I). Therefore, the number of eggs/juveniles

produced from a single brood increased with the age

of the female, and a positive correlation was also

0

2

4

6

8

10

12

I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIII XIX

Instar

Art

icle

num

bers

Males

Females

Juveniles

Figure 5. Number of flagellar articles (Mean9S.D.) of antennae I per instar in Caprella grandimana. Up to Instar IV females and males

could not be differentiated, so article numbers were the same in juveniles.

Nº of offspring;y = 2,4036x - 4,794

R2 = 0,1552

Nº of eggs;y = 4,0106x - 7,9391

R2 = 0,4829

0

2

4

6

8

10

12

14

16

18

20

2,5 3 3,5 4 4,5 5 5,5 6

Body length (mm)

Num

ber

of e

ggs

0

2

4

6

8

10

12

14

16

18

20

Num

ber

of o

ffspr

ing

Number of eggs

Number of offspring

Figure 6. Correlation of number of eggs and number of offspring with female total body length in Caprella grandimana. Number of eggs

(n�231 broods). Number of offspring (n�57 broods with offspring). Both correlations were significant at pB0.001.

Life history of Caprella grandimana 89

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Page 7: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

found between body length and the number of eggs/

juveniles produced (Figure 6).

Decaying or disappearing of eggs during the

incubation period was observed in 31% of cases.

Discussion

Despite the importance of caprellids in Mediterra-

nean ecosystems, this is the first time in which a

Mediterranean species has been successfully reared

under laboratory conditions throughout all instars of

their cycle until completion of their life history.

These studies are elemental for future ecotoxicolo-

gical research and management of caprellid species.

Caprella grandimana was characterized by a lack

of maternal care behaviour in early stages of growth;

small first instar juveniles used Corallina elongata

thalli as habitat substrata, and no young were seen

clinging to the mother or staying near to her.

According to Aoki (1999), caprellids which produce

small first instar young (B1.3 mm) and live on

seaweed with thick thalli and branches such as

Sargassum patens (Agardh, 1820) need to use an

epiphytic secondary habitat or depend on maternal

care to hold on to the substratum and be able of

survive. However, C. elongata has thin branches

which allow the small first instar to hold them tight,

and this allows for C. grandimana juveniles not to

need the help of epiphytic or maternal care at their

first stage of life.

With regard to the moulting cycle, males and

females had different numbers of moults throughout

their life, following a similar process as described in

Pseudoprotella phasma by Harrison (1940). Males

only lived up to Instar X, while females continued

moulting up to Instar XVIII. Takeuchi & Hirano

(1991, 1992a) found the same pattern in Caprella

okadai, and Caprella danilevskii, where females had

more moults rate than males, and had a survival time

significantly longer than males.

The duration of each instar in females from VI

onward remained stable until they died, but in males

it gradually increased from Instar IV up to their last

instar, which was significantly longer than their

previous moulting interval. This case has not been

reported in any other species of Caprellidea or

Gammaridea in laboratory experiments. During

this last instar, larger males began to be covered by

detritus and other particles until all the gnathopods

and pereonites were completely covered with detri-

tus. During sampling in the field, well-developed

males also showed their bodies completely covered

with detritus, so it seems that males at their last

instar cannot moult and retain the same cuticule

without growing until their death. The pattern of

flagellar articles added to antenna 1 also differed

between males and females as reported for

C. danilevskii and C. okadai (Takeuchi & Hirano

1991, 1992a), so in this species it is necessary to

know the flagellar pattern to be able to determine the

instar only by the number of flagellar articles. Males

had a higher number than females. Upon reaching

sexual maturity, males continued to increase the

number articles, and females remained more or less

constant with 10 articles, so with this flagellar

pattern it is easy to determine the instar stage in

the field, and to know if females and males are able

or not to reproduce according to the number of

articles in their antenna 1.

Caprella grandimana had a generation period of

49.1 days at 178C, nearly double that of the caprellid

species reared by Takeuchi at 208C. It can be

understood because growth and reproduction are

strongly affected by temperature in marine crusta-

ceans, causing a rapid growth at high temperatures

and a slower growth at low temperatures. However,

if generation length of C. grandimana at 178C is

compared with that of gammarids at 178C (Wildish

1972), such as Orchestia mediterranea (Costa, 1853),

Orchestia gammarellus (Pallas, 1766), or Orchestia

remyi roffensis (Wildish, 1969), C. grandimana has a

faster generation period than gammarids at the same

temperature. Takeuchi & Hirano (1991) reported

that generation length for gammarids was longer

than the average of four Caprella species examined

by them at 208C (C. danilevskii, C. okadai, Caprella

generosa (Arimoto, 1977), Caprella brevirostris

(Mayer, 1903)). They suggested that in the Caprel-

lidea the reason may be attributable to the lack

of abdominal appendages, which in the Gammar-

idea are used for producing respiration and for

swimming.

The number of offspring that finally emerged from

the brood pouch of C. grandimana in a single brood

was only five, increasing in successive instars with

the increase in body length of the female, reaching a

maximum of 15 juveniles. In other species, this

increase in number of eggs and offspring is also

associated with an increase in female size. However,

the number of offspring emerging from C. grand-

imana was very low compared with a maximum of

82 hatchlings produced by a single female of Caprella

mutica in a single brood (Cook et al. 2007), or

50 and 32, in C. danilevskii and C. okadai, respec-

tively (Takeuchi and Hirano 1992b). The differences

in body length of each instar of different species with

different body length probably plays an important

role in fecundity, where females with small bodies in

earlier instars of their cycle have fewer offspring than

longer females in late instar, and small species like

C. grandimana (4.2 mm) also have fewer offspring

than longer species like C. mutica (7 mm).

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Page 8: Life history of Caprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions

During the reproduction of mature females, it was

found that many ovigerous females lost or dropped

their eggs from the brood pouch. This also occurred

in other two species: C. mutica females showed a

decay or loss of eggs during the incubation period

when reared at very low temperatures (5�108C)

(Hosono 2009), and the number of juveniles that

finally emerged from the brood pouch of Caprella

laeviuscula was about half of the number of

eggs carried within the brood pouch. Caine (1991)

suggested that juveniles may have eaten some of the

unhatched eggs prior to emergence from the brood

pouch.

Even so, the survival rate of juveniles of

C. grandimana that finally emerged from the

brood pouch was very high at 94%, proving that

C. grandimana seems to be a resistant species that can

be reared in laboratory conditions, supporting un-

favourable conditions such as water quality produced

by ammonia build-up from excess food (Chen et al.

1990), low oxygen concentration in small containers,

or stress caused by the manipulation of individuals

during the study.

The results of this study have implications for

future development in ecotoxicological testing with

C. grandimana. This species is capable of growing and

reproducing in captivity, and this can represent the

first step in evaluating the effects of different con-

taminants upon the growth and reproduction of this

species. Furthermore, our study provides a baseline

for knowledge of the life span of the species and its

length of survival, growth rate, maturation time and

fecundity. As pointed out by Woods (2009), caprellid

amphipods are an overlooked marine finfish aqua-

culture resource and this kind of study dealing with

life history is essential to properly address applied

studies in the future.

Acknowledgements

Financial support of this work was provided by

the Ministerio de Educacion y Ciencia (Project

CGL2007-60044/BOS) co-financed by FEDER

funds, and by the Consejerıa de Innovacion, Ciencia

y Empresa, Junta de Andalucıa (Project P07-RNM-

02524). The first author was awarded a grant-in-aid

(BES-2008-004520) from the Ministerio de Ciencia

e Innovacion in support of the present study. Special

thanks to Angela Ruiz-Cortina for English revision

of the manuscript.

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