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Life history of the sandy beach amphipodDeshayesorchestia deshayesii (Crustacea: Talitridae)from Bizerta beach (North of Tunisia)Amel Ayari-Akkaria, Raja Jelassia, Hajer Khemaissiaa & Karima Nasri-Ammara

a Faculté des Sciences de Tunis, Université de Tunis El Manar, Unité de recherche Bio-Ecologie et Systématique Évolutive, Tunis 2092, TunisiaPublished online: 29 May 2014.

To cite this article: Amel Ayari-Akkari, Raja Jelassi, Hajer Khemaissia & Karima Nasri-Ammar (2014) Life history of the sandybeach amphipod Deshayesorchestia deshayesii (Crustacea: Talitridae) from Bizerta beach (North of Tunisia), InvertebrateReproduction & Development, 58:4, 269-277, DOI: 10.1080/07924259.2014.920422

To link to this article: http://dx.doi.org/10.1080/07924259.2014.920422

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Life history of the sandy beach amphipod Deshayesorchestia deshayesii (Crustacea: Talitridae)from Bizerta beach (North of Tunisia)

Amel Ayari-Akkari*1, Raja Jelassi1, Hajer Khemaissia and Karima Nasri-Ammar

Faculté des Sciences de Tunis, Université de Tunis El Manar, Unité de recherche Bio-Ecologie et Systématique Évolutive, Tunis 2092,Tunisia

(Received 20 February 2013; accepted 1 April 2014)

Population dynamics and reproductive activity of the amphipod Deshayesorchestia deshayesii were studied monthly fromJune 2007 to December 2008 in Bizerta beach. During this period, 6577 specimens of D. deshayesii were identified; thesex ratio was female biased, with a mean of the monthly sex ratios equal to 0.21 ± 0.12. Due to the absence of embryosor eggs in the female brood pouches and juveniles in the samples, results suggested that the reproductive seasonextended from April to November, with a sexual resting period during winter from December to March. Brood size var-ied between 4 and 17 eggs and fecundity appeared to be correlated with female size. Six cohorts were identified on thefirst sampling date. Additionally, 12 new cohorts were detected during the study period. Life span was estimated at 5–7months depending on the time of birth. Cohorts that appeared at the beginning of the reproductive period tended to haveshorter lives than those born later in the season. These results suggest that D. deshayesii can be considered as a semi-annual species, with iteroparous females.

Keywords: population dynamics; reproductive activity; life history; Talitridae

Introduction

Deshayesorchestia deshayesii is a nocturnal, detritivorousamphipod, which occupies the supra-littoral zone onsome Tunisian beaches (Ayari & Nasri-Ammar 2008).During daytime, it lives in non permanent burrows or ishidden amongst decaying seaweed, debris and otherstorm-deposited materials (Bulnheim & Scholl 1986). Itburies itself in the Posidonia oceanica strand line associ-ated with some other macrophytes, where it avoids desic-cation (Scapini 1997, 1999) by burrowing amongst thefronds. D. deshayesii prefers fine sand on shelteredshores (Bulnheim & Scholl 1986). In fact, these ecologi-cal requirements allow the species to have a wide butpatchy distribution. This fragmentation of an originallycontinuous distribution probably reflects the impact ofthe human activities (Ketmaier et al. 2003). Furthermore,sandy beaches are often heavily used by humans inurban areas. Consequently, the destruction of sand dunesand intense recreational activities are often the mostcommon anthropogenic disturbances.

D. deshayesii is the most abundant amphipod livingin Bizerta beach, where it cohabits with four othertalitrid species (Ayari, Bohli, & Nasri-Ammar, 2011):Talitrus saltator, Orchestia gammarellus Orchestia medi-terranea and Orchestia montagui. Moreover, the speciesplays an important ecological role as a decomposer andcan constitute an important prey species for birds

(Scapini 1999; Ketmaier et al. 2003). Also, it can beconsidered as a potential bioindicator for the quality ofsandy beaches (Grifiths et al. 1983; Ketmaier et al.2003).

Reproductive strategies and population dynamics werestudied in several populations of amphipods as in thespecies O. mediterranea (Louis 1977; Wildish 1979),Talorchestia quoyana (Marsden 1991), T. saltator(Williams 1978; Marques et al. 2003) and O. gammarellus(Persson 1999).

Moreover, in different tunisian sandy beaches, distri-bution, orientation, locomotor rhythm and biology ofmany Talitridae have been studied: T. saltator andD. deshayesii (Bizerta beach, 37°19ʹN, 09°51ʹE, Ayari &Nasri-Ammar 2011a), T. saltator (Barkoukech beach,36°58ʹN, 8°50ʹE, Nasri-Ammar & Morgan 2005, 2006),T. saltator and Talorchestia brito (Zouaraa beach37°0ʹN, 08°53ʹE, Charfi-Cheikhrouha et al. 2000; Scapiniet al. 2002; Marques et al. 2003; Bouslama et al. 2009),T. saltator (Korba beach, 36°37ʹN, 10°54ʹE, Nasri-Ammar & Morgan 2005; Bouslama et al. 2007) and alsoT. saltator (Gabes beach, 33° 52ʹN, 10° 07ʹE, Ayari &Nasri-Ammar 2011b, 2011c).

This present study was carried out to characterize thelife cycle and the dynamics of the population ofD. deshayesii at Bizerta beach, and to compare theseresults with other populations over the complete range of

*Corresponding author. Email: ayari_amel13@yahoo.fr1Amel Ayari-Akkari and Raja Jelassi contributed equally to conducting the research and writing the manuscript.

© 2014 Taylor & Francis

Invertebrate Reproduction & Development, 2014Vol. 58, No. 4, 269–277, http://dx.doi.org/10.1080/07924259.2014.920422

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distribution on this species. According to the literature,D. deshayesii was noted at several beaches of the Tuni-sian coast, at the level of the Black Sea, the North-Eastbeaches of the Atlantic Ocean and the Mediterraneancoast. Moreover, we had chosen this Bizerta beachbecause a significant density of the concerned specieswas recorded.

Materials and methods

Study area and field sampling

The study site, Bizerta beach located in North of Tunisiain the littoral area (37°19ʹ17.1ʹʹN; 09°51ʹ57.3ʹʹE),(Figure 1) is characterized by the presence of a band ofP. oceanica and some algae (Ulva sp.; Padina sp.;Cymodocea nodosa) that runs parallel to the coast. Thismicro-tidal beach measures 9.5–19.5 m in width depend-ing on the season (Table 1).

Field work was conducted each month, from June2007 to December 2008, in the supra-littoral zone. Spec-imens were collected by hand, during the morning andsampling effort varied from 1 to 2 h. Other talitrid spe-cies were collected: O. gammarellus, O. mediterraneaand O. montagui within the band of the vegetation nearthe shoreline, while T. saltator specimens were collectedfrom their burrows in the sand in the same supra-littoralzone. During the sampling, sand moisture and tempera-ture were recorded (Table 1).

Laboratory procedures

In the laboratory, the specimens collected were observedunder binocular microscopes and identified species

measured (cephalic and body lengths), counted andsexed for different categories: non-sexually differentiatedjuveniles, adult males, young females, reproductivefemales with empty oostegites, reproductive females(with setae or with eggs/embrios), etc. Furthermore, theeggs present in the marsupium, were counted and catego-rized into five classes depending on the status of devel-opment of the eggs according to Marques et al. (2003).Both the animals and eggs were preserved in tubescontaining 70° ethanol.

Statistical analyses

The modal distributions were tracked in successive sam-ple dates by means of size-class (0.04 mm) frequencyanalysis, which was carried out using the probabilitypaper method (Harding 1949), as performed by Cassie(1954, 1963). Distributions are assumed to result frompulses in recruitment (cohorts). Computations used theANAMOD software (Nogueira 1992), and the reliabilityof the distribution separation method was tested withboth the χ2 and G tests (p ≤ 0.05).

Results

Sex ratio

The structure of the population during the sampling per-iod showed a total number of 3806 females (includingall reproductive stages), and only 829 individuals corre-sponding to males (Figure 2). Consequently, the male:female ratio was strongly female biased throughout the

Figure 1. Sampling site: Bizerta beach (37°19ʹ17.1ʹʹN; 09°51ʹ57.3ʹʹE) (Mediterranean Sea, Tunisia).

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period of study. In fact, the overall sex ratio was equalto 0.22. Furthermore, females are smaller than males.

The monthly variation of the sex ratio of D. deshayesiiduring the 18 months of study, showed that thelowest values were observed at the end of fall (inNovember)/early winter (in December), while three peakscorresponding to the highest values were recorded duringearly fall (September), summer (June) and spring (April)(Figure 3).

Fecundity

Fecundity, varied between 4 and 17 eggs and the bodylength of ovigerous females varied between 4.6 and 10.7

mm. The majority of highest fecundities was recorded inthe end of the reproductive activity but this fecundityvaried over time.

Only ovigerous females during the earlier stages ofdevelopment of embryos were considered, to be sure thatthey did not have a loss of eggs. A correlation betweenfecundity and female size was evident with a correlationcoefficient (r² = 0.6019) (Figure 4).

Growth and life span

Size frequency distributions were estimated for the rec-ognition of cohorts in the D. deshayesii population. Sixcohorts were recognized during the first sampling in June

Table 1. Monthly variation of environmental conditions recorded during sample collection (T: temperature; RH: relative humidity).

Sand T (°C) Sand RH (%) Air T (°C) Air RH (%) Beach width (m)

June 2007 25.8 65 29 43 12.8July 2007 31.05 63.5 31 59 10.5August 2007 31.1 66 32.75 62 10.5September 2007 30.5 69.5 31.8 45.5 10.9October 2007 25.45 73.5 25.6 71.5 9.5November 2007 21.1 71 22.15 65 13.5December 2007 17.85 73 19.35 57 14.4January 2008 17.35 66.5 19 62.5 16.1February 2008 16.1 81.5 18.8 62 19.5March 2008 15.85 82 20.15 76.5 11.4April 2008 20.8 75.5 21.4 61 12.7May 2008 21.5 80 22.5 66.5 13.2June 2008 25.4 71.5 30.6 46 17.6July 2008 29.95 73.5 31.6 66 15.7August 2008 31.2 71.5 31.85 69.5 13.1September 2008 28.35 75.5 32.1 67 14.3October 2008 23.15 82 27.55 72.5 13November 2008 21.25 73 23.65 66 16.2December 2008 14.7 84.5 20.35 67.5 12

Figure 2. Structure of the population of D. deshayesii during the study period. (Young F: young females, NRF: non reproductivefemales and RF: reproductive females).

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2007 and 12 new cohorts were detected along the studyperiod (Figure 5). These 12 new cohorts appeared,respectively, on July 2007 (cohort 7); August 2007(cohort 8); September 2007 (cohort 9); November 2007(cohort 10); January 2008 (cohort 11); February 2008(cohort 12); March 2008 (cohort 13); May 2008 (cohort14); June 2008 (cohort 15); September 2008 (cohort 16);October 2008 (cohort 17) and November 2008 (cohort18).

The minimum average cephalic length (CL) of newcohorts ranged from 0.3407 to 0.5293 mm correspondingto a total body length (TL) varying, respectively,between 2.25 mm and 5 mm. Whereas the maximum val-ues of CL ranged from 0. 9336 to 1.2373 mm corre-spondingly to a TL between 8.8 and 12 mm (Figure 6).

Furthermore, growth appeared to be continuous overthe life span of D. deshayesii (Figure 6). Seasonality wasalso observed in the growth pattern and individuals hada life expectancy of 5–7 months.

Life cycle

To determine the male and ovigerous female contributionto recruitment frequency size analysis was performed.Cohorts born during the beginning of the reproductive sea-son reproduced during the same period, and had shorterlife spans (5 months). Whereas those born in late summer /early fall survived the winter, had longer lifetimes (7months) and became sexually active for breeding duringthe next reproductive season. Moreover, females of D. des-hayesii bred at least twice during their life (Figure 7).

Figure 3. Monthly variation of the sex ratio (number of males/number of females) of D. deshayesii during the study period.

Figure 4. Relationship between the number of eggs in the brood pouch and female size in D. deshayesii on Bizerta beach.

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Discussion

During the study period, we have noted the absence ofovigerous females during the winter. Consequently, thispopulation is characterized by a seasonal reproductiveactivity. We suggested that the reproductive activity andrecruitment extended from April to November with asexual rest period of four months from December toMarch. Due to paucity of information on the dynamicsof D. deshayesii populations, we compared our resultswith other species of Talitridae. Seasonal reproductionwas also observed in several populations of amphipodssuch as the population of O. mediterranea from the

Medway estuary in Great Britain, characterized by a per-iod of sexual rest spanning from October to mid-April(Wildish 1979) and populations from Languedoc pondsin southern France with a resting period from Novemberto mid-March (Louis 1977). In addition, Marsden(1991), Williams (1978) and Persson (1999) showed thatthis type of reproduction was also present in T. quoyana(New Zealand), T. saltator (Atlantic coasts) andO. gammarellus (Baltic coasts). Other populations ofamphipods were characterized by a continuous reproduc-tive activity such as seen in Talorchestia capensis(Van Senus 1988), Platorchestia platensis with a

Figure 5. (Parts 1 + 2). Size frequency distribution of the population of D. deshayesii on Bizerta beach from June 2007 to December2008. Sampling dates are indicated; arrows indicate average cephalic length of the numbered cohorts or groups of cohorts; black areasindicate ovigerous females.

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significant slowdown of reproductive activity in Januaryand February (Ciavatti 1989) and O. montagui and

O. mediterranea from the lagoon of Bizerta in Tunisia(Djelassi 2008). Marques et al. (2003) showed in

Figure 5. (Continued)

Figure 6. Estimated growth and life span (field growth data) of the population of D. deshayesii cohorts or groups of cohorts atBizerta beach (average cephalic length ± standard deviation) during the period of study. Broken lines indicate probable cohort mergingor cohort development over time.

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populations of Italian and Portuguese T. saltator thatrecruitment periods were shorter in the north and muchlonger in the south.

The sex ratio in D. deshayesii from Bizerta beach,showed a clear dominance of females throughout the 18months of study. A female-biased sex ratio is very commonin amphipods as has been described for O. gammarellus(Jones & Wigham 1993; Persson 1999; Dias & Sprung2004; Djelassi 2008), Peudorchestoidea brasiliensis(Cardoso & Veloso 1996), T. capensis (Van Senus 1988),O. mediterranea (Djelassi 2008) and also in T. saltator andT. brito from Zouaraa beach (Charfi-Cheikhrouha et al.2000). This substantial difference between males andfemales can be explained by a significant mortality of oldermales contributing to the coupling or by the presence of afeminizing bacteria Wolbachia type revealed in several spe-cies of isopods (Rigaud et al. 1997) and in some species ofamphipods as Talorchestia deshayesii and O. gammarellus(Cordaux et al. 2001). Moreover, a sex-ratio biased infavour of males, was revealed in the populations ofT. saltator from Collelungo beach (Italy) and Lavos beach(Portugal) (Marques et al. 2003).

Furthermore, an evident correlation between fecun-dity and the body length of ovigerous females was estab-lished. This result confirmed those observed inT. saltator at the Atlantic coast (Williams 1978), inNeohaustorius schmitzi at the North of Carolina (Dexter1971) and in T. saltator from Korba beach in Tunisia(Bouslama et al. 2009).

The modal distributions analysis revealed theappearance of 12 new cohorts, during the 18 months ofstudy. In other localities, during a sampling period of 12months, and among different populations of T. saltator

from Korba (Tunisia) (Bouslama et al. 2007), Zouaraa(Tunisie) (Bouslama et al. 2009), Collelungo (Italy)(Marques et al. 2003) and Lavos (Portugal) (Marqueset al. 2003) the number of new cohorts detected were,respectively, equal to nine, six, eight and five cohorts.Compared with these last species, we suggest that thenumber of cohorts was a characteristic depending on thestrategy of the species to increase their existence to faceenvironmental conditions in their localities. We suggestthat an increase of the frequency of recruitment may helpspecies to assure their survival and continuity.

In the present study, specimens of D. deshayesii werecharacterized by a maximum life expectancy of 5–7months. Our results were similar to those estimated forother species of Talitridae: 5–8 and 6–11 months inT. saltator, respectively, at Zouaraa beach (Tunisia) andLavos beach (Portugal) (Marques et al. 2003); 6–8 and6–9 months, respectively, at two Tunisian beaches: Zou-araa and Korba in T. saltator (Bouslama et al. 2009) andalso 5–9 months in O. mediterranea from Moroccan beach(El Kaim et al. 1985). Furthermore, Marques et al. (2003)suggested that the variability of the life span correlatedwith the geographic cline, decreased from northern Euro-pean Talitridae populations towards the Mediterranean.

D. deshayesii, from Bizerta beach, can produce newcohorts two or three times per year. This patterncorresponds to a semi-annual life cycle with iteroparousfemales. Similarly, females of O. gammarellus in a saltmarsh in Portugal, can breed three or even more timesper year (Dias & Sprung 2004). Generally, this plasticityobserved in the life cycle pattern has been characterizedin several other populations of amphipods (Wildish1982).

Figure 7. Analysis of the recruitment pattern of the population of D. deshayesii at Bizerta beach. The horizontal arrows representthe period during which the cohort was followed in the study period, starting in the solid circles. The assumed contributions of eachcohort or group of cohorts are indicated (triangles). Contributions of the various cohorts to recruitment are indicated.

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A similar study on the population dynamics of T. sal-tator, living in the same supra-littoral zone, is beingundertaken and should allow us to compare the adaptivestrategies of these two sympatric species regarding thesharing of the ecological niche. Furthermore, along theTunisian coast, our research represents a first study onthe population dynamics of the talitrid D. deshayesii.

Funding

The study was supported by the Research Unit of Animal Biol-ogy and Evolutionary Systematics [grant number UR11ES11],Faculty of Science of Tunis, University of Tunis El Manar.

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