Fecundity and effects of bopyrid infestationon egg production in the Caribbeansponge-dwelling snapping shrimpSynalpheus yano (Decapoda: Alpheidae)

patricio herna’ ez1,2

, betel marti’nez-guerrero3

, arthur anker4

and ingo s. wehrtmann1,5

1Unidad de Investigacion Pesquera y Acuicultura (UNIP), Centro de Investigaciones en Ciencias del Mar y Limnologıa, Universidadde Costa Rica (CIMAR), 2Museo del Mar, Universidad Arturo Prat, Casilla 121, Iquique, Chile, 3Laboratorio de Sistematica deInvertebrados Marinos (LABSIM), Universidad del Mar, Campus Puerto Angel, Puerto Angel, Oaxaca CP 70902, Mexico,4Dickinson Hall, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611-7800, USA, 5Escuela de Biologıa,Universidad de Costa Rica, 2060 San Jose, Costa Rica

Several Synalpheus species have been reported as hosts of bopyrid parasites; however, the impact of infestation on egg pro-duction is still unknown. Therefore, the present work studied reproductive aspects and the effect of parasitism on fecundityof the alpheid shrimp Synalpheus yano from Bocas del Toro, Caribbean coast of Panama. Un-infested females (N ¼ 84)ranging from 3.7 to 9.6 mm carapace length, produced between 5 and 246 eggs (average: 98+64.6), and egg number increasedsignificantly with female size. The eggs were relatively large (0.6–1.3 mm in diameter), but within the range of otherSynalpheus species, and egg size did not differ significantly between un-infested and infested females. Despite these largeeggs, the morphological characteristics of hatching larvae indicate a planktotrophic development. During the incubationperiod, the egg volume increased from 0.100 to 0.218 mm3, representing an overall increase of 118%. A total of 18 females(16% of all ovigerous individuals) were infested, and the occurrence of parasitic infestation was more pronounced inlarger females. Infested females ranging from 4.6 to 9.4 mm carapace length, produced between 22 and 166 eggs (average:81+44.4). Egg-bearing females infested by parasitic bopyrids carried on average 41% fewer eggs than similar-sizedfemales without parasites. The co-occurrence of parasites and developing eggs, however, indicates that the bopyrid parasitedoes not necessarily castrate its host. Therefore, we encourage more comparative intraspecific studies on egg production ininfested and un-infested females to assess the impact of infestation on fecundity in caridean shrimp.

Keywords: Alpheidae, Synalpheus, shrimp, sponge-dwelling, egg production, parasitism, bopyrid, Hemiarthrinae, Panama

Submitted 17 June 2009; accepted 8 August 2009

I N T R O D U C T I O N

The American species of the snapping shrimp familyAlpheidae have received a great deal of attention during thelast decade. Most publications involving these interesting car-idean shrimps are taxonomic descriptions and species revi-sions (i.e. Anker & Iliffe, 2000; Anker & Felder, 2005;Anker, 2007; Rıos & Duffy, 2007; Anker et al., 2007, 2008),new records and range extensions (i.e. Hermoso-Salazar &Hendrickx, 2005; Anker, 2007), behavioural studies, i.e. onmate choice (Rahman et al., 2004) and studies on eusociality(Duffy et al., 2002; Duffy, 2003), as well as results from stillongoing research on molecular and morphological evolution(Williams et al., 2001; Morrison et al., 2004; Mathews, 2006;Hurt et al., 2009; Mathews & Anker, 2009).

Our knowledge of the reproductive ecology of tropicalAmerican alpheids is rather poor. Corey & Reid (1991)

examined reproductive aspects of 16 alpheid species fromFlorida; their results revealed that many of these species tendto produce small eggs. There is, however, evidence thatalpheid shrimps can also produce large eggs, indicating a ten-dency for an abbreviated larval development (Felder, 1982;Dardeau, 1984; Wehrtmann & Albornoz, 2002). To our bestknowledge, data on reproductive patterns of Central Americanalpheids are still deficient except for the description of first post-embryonic stages in the transisthmian sister species Alpheussaxidomus and A. simus (Wehrtmann & Albornoz, 2002).

Fecundity has been widely recognized as one of the ecolo-gically most important features in the life history of manyinvertebrates, including decapod crustaceans (i.e. Hines,1991; Somers, 1991). This aspect usually refers to the totalnumber of eggs (here we use the term ‘eggs’ also for develop-ing embryos) carried by the females. As in many decapods, apositive relationship has been observed between fecundity andfemale size in alpheid shrimps. The correlation coefficient (r)reported for some of these species (Corey & Reid, 1991;Lardies & Wehrtmann, 1997) is highly variable (0.54–0.99),suggesting that endo-exogenous factors may provoke loss ofeggs during the embryogenesis (for review see Kuris, 1991).

Corresponding author:I.S. WehrtmannEmail: ingowehrtmann@gmx.de

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Journal of the Marine Biological Association of the United Kingdom, page 1 of 8. # Marine Biological Association of the United Kingdom, 2009doi:10.1017/S0025315409991093

Egg size offers valuable information on a species’ reproduc-tive strategy. It serves as a useful indicator for the duration ofembryogenesis and larval size at hatching (Steele & Steele,1975; Wehrtmann & Lopez, 2003). Many species ofSynalpheus show a clear correlation between egg size andtype of larval development, ranging from normal (¼extended) via abbreviated to quasi-direct (see Coutiere,1898; Dardeau, 1984; Duffy, 1996). However, more detailedinformation on this issue is presently restricted to just a fewalpheid species.

Synalpheus, being one of the most species-rich genera of theAlpheidae, with well over 60 species in the Caribbean regionalone (Rıos & Duffy, 2007; Anker & Toth, 2008), receivedmore attention compared to the other genera of this family,mainly due to the fact that some species form eusocial coloniesin sponges (Duffy et al., 2000, 2002). The eusocial Synalpheusinhabit the internal canals of larger demosponges, forming colo-nies of up to several hundred individuals, but containing onlyone reproductive female equivalent of a ‘queen’ in insectsocieties. Despite this extraordinary behaviour and a great scien-tific potential of these shrimps, their reproductive biology ispoorly known (Duffy et al., 2002). However, the vast majorityof sponge-dwelling Synalpheus are pair-living species.

Synalpheus yano (originally described as Zuzalpheus yanoRıos & Duffy, 2007; see Anker & De Grave, 2008 for syno-nymy of Zuzalpheus) is apparently a pair-living species. It isone of the most common sponge-dwelling species ofSynalpheus of Bocas del Toro, a small archipelago on theCaribbean coast of Panama. In Bocas del Toro, this speciesmost frequently associates with the bright red-orangesponge Lissodendoryx colombiensis Zea & van Soest, 1986.The same sponge is used by S. yano as main host at the typelocality in Belize, although three other sponge species havebeen reported as facultative hosts there (Rıos & Duffy, 2007).

The presence of parasitic bopyrid isopods (Epicaridea:Bopyridae; mainly Bopyrinae and Hemiarthrinae), has beendocumented in a number of decapod crustaceans, includingspecies of Alpheus and Synalpheus (Markham, 1986). These

parasites may cause castration by: (1) inhibiting the matu-ration of the female gonad; and (2) feminizing parasitizedmales (Reinhard, 1956; van Wyk, 1982; O’Brien & van Wyk,1985; Gonzalez & Acuna, 2004; Calado et al., 2005). Moststudies focus on the intensity and prevalence of infestation,population structure and energetics of the bopyrid isopodparasite and its decapod host (Beck, 1980; Gonzalez &Acuna, 2004; Smith et al., 2008). However, detailed data onthe impact of parasitic infestation on egg production in cari-deans are rather limited. The presence of adult abdominalbopyrids in egg-bearing females of Synalpheus highlights thecomplexity of parasite–host interactions and the lack ofknowledge on this topic (see Calado et al., 2005).

The aim of the present study is to provide information onthe fecundity, egg volume and energy allocation for reproduc-tion in S. yano. Also shown are the effects of parasitism bybopyrids on egg production in this species. We compare ourresults with those available for other tropical–subtropicalalpheid species.

M A T E R I A L S A N D M E T H O D S

Study areaOvigerous females of S. yano were collected in August 2008during a shrimp taxonomy course in Bocas del Toro,Caribbean coast of Panama (Figure 1). The Bocas del Toroarchipelago comprises several larger and many smallerislands and patchy reefs and sponge gardens supporting avery diverse fauna. Initially, a small number of ovigerousfemales of S. yano were extracted from internal canals of ared-orange sponge, Lissodendoryx colombiensis that is fairlycommon in these sponge gardens and also grows on jettypilings or large pieces of coral rubble, at shallowdepths (1–5 m). Consequently, a fairly large number (.20)of these sponges was collected and revised to obtain a suffi-cient number of ovigerous females. In the laboratory,

Fig. 1. Sampling locations in Bocas del Toro, Caribbean coast of Panama.

2 patricio herna’ ez et al.

specimens were extracted from sponge canals and preservedin ethanol (75%).

We also collected ovigerous females of other alpheidspecies (Alpheus spp., other Synalpheus spp. and Automatesp.), e.g. in coral rubble and other sponges. The totalnumber of collected individuals per species was relativelylow, mostly due to time constraints. However, because ofinsufficient knowledge of reproductive traits in CentralAmerican Alpheidae, we decided to include these data in thepresent study.

Analyses of materialAll specimens of Synalpheus were identified using an identifi-cation key based on Rıos & Duffy (2007). We measured thecarapace length (CL, in mm) of each female from the tip ofthe rostrum to the posterior margin of the carapace; thismeasurement was recorded with the aid of a stereomicroscopeprovided with an ocular micrometer (nearest 0.1 mm). Thesize at first maturity was established as 50% of the overallsize–frequency distribution for ovigerous females, as deter-mined after fitting a sigmoid curve to the relationshipbetween the percentage of ovigerous females and size, using0.1 mm size-classes (Wenner et al., 1974).

After removing the complete egg mass from each female, thetotal number of eggs (EN) was determined by counting themunder a Leitz stereomicroscope. All collected ovigerousfemales of S. yano were examined for the presence of parasiticisopods (Epicaridea, Bopyridae and Hemiarthrinae) (seeDardeau, 1984; Markham, 1985). Developing eggs of eachspecies were classified into three stages (Stages I–III) basedon the shape and development of both abdomen and eyes, asdescribed by Wehrtmann (1990). We separated arbitrarily 20embryos from the egg mass and measured the width andlength of each egg under a microscope equipped with a cali-brated ocular micrometer. These data were used to calculateegg volume (EV) according to the formula proposed byTurner & Lawrence (1979) for oblate spheroids: EV ¼ 1/6(a � b2

� p), where a represents length, and b width. Thevolume increment during the incubation period was calculatedusing the equation proposed by Kobayashi & Matsuura (1995).

The energy allocation for egg production was estimated bydetermining the reproductive output (RO) of the females, con-sidering only recently extruded eggs (Stage I). Females andtheir corresponding egg masses were dried at 60ºC for 24hours, and the resulting data were used in the formula pro-posed by Clarke et al. (1991): RO ¼ dry weight of the entireegg mass/dry weight of the female without eggs.

Data analysisThe relation between fecundity and female size was describedby an allometric model (Y ¼ a . Xb), which has been usedwidely for this purpose in similar studies with other decapods(i.e. Corey & Reid, 1991; Hines, 1991; Hernaez & Palma,2003). According to Somers (1991), an isometric relation isindicated by values for b that are near 3. Thus, b values of,2.90 and .3.10 were taken as indication of a negative andpositive allometric relation, respectively (Somerton, 1980).An analysis of covariance (ANCOVA; Zar, 1999) wasapplied to analyse the relation between egg number andfemale CL for each embryonic stage to estimate possible eggloss during the incubation period. In the case of a significant

difference between egg numbers per stage (P , 0.05), aTukey a posteriori test was applied to establish the similaritybetween each pair of developmental stages (Zar, 1999).

The area of egg attachment was frequently infested withparasitic isopods, Hemiarthrinae (Dardeau, 1984; P. Hernaez,personal observation; Figure 2). In order to evaluate the poss-ible impact of parasitic infestation on egg production, we ana-lysed the fecundity of infested and non-infested females, andcompared the slopes of each scenario applying the analysis ofcovariance (ANCOVA; Zar, 1999).

R E S U L T S

Egg production of un-infested females S. yanoA total of 249 individuals of S. yano were analysed; 112 ofthem were ovigerous females (45%). Regarding theun-infested females (N ¼ 84), 23 were at Stage I, 37 at StageII, and 24 females carried eggs close to hatching (Stage III).These females measured from 3.7 to 9.6 CL mm (average5.6+1.16 mm), and 73% of them were in the range between4.1 and 6.0 mm CL. The total number of eggs in un-infestedS. yano varied between 6 and 246 (average: 98+64.6). Thefecundity increased significantly with female size (simpleregression; r ¼ 0.70; P , 0.05); however, the correlation wasrelatively low explaining approximately 50% of the observedvariability (Figure 3). During the incubation period,

Fig. 2. Specimen of Synalpheus yano with a parasitic isopod (PI), collected inBocas del Toro, Caribbean coast of Panama.

Fig. 3. Relation between carapace length (CL) and number of eggs (EN) inun-infested ovigerous females of Synalpheus yano in Bocas del Toro,Caribbean coast of Panama.

reproduction and bopyrid infestation in s. yano 3

un-infested females of S. yano lost approximately 16% of theirinitially produced eggs (ANCOVA, f ¼ 23.5; P , 0.05).However, no statistically significant differences were detectedbetween numbers of eggs at different developmental stages(Tukey test, P . 0.05).

During the incubation period, the egg volume in un-infestedfemales increased from 0.100 to 0.218 mm3, representingan overall increase of 118% (Figure 4). The average RO ofS. yano was 25.7+11.48% of their dry weight, and variedbetween 10.5 and 44.9%. RO did not increase with the femalesize (Spearman test, P . 0.05). The egg mass comprised onaverage 35% of the dry body weight of females.

Comparison of egg production betweeninfested and un-infested females of S. yanoOut of 112 analysed egg-bearing females, 18 (16%) wereinfested by bopyrids; seven females carried eggs in Stage I,four in Stage II and seven in Stage III. Infested femalesmeasured from 4.6 to 9.4 mm CL (average 6.7+1.30 mm)and produced between 22 and 166 eggs (average: 81+44.4).During the incubation period, infested females lost approxi-mately 39% of their initially produced eggs (ANCOVA, f ¼23.5; P , 0.05), and no statistically significant differenceswere detected between the numbers of eggs at different devel-opmental stages (Tukey test, P , 0.05).

Since we did not detect any statistically significant differ-ence of egg number between the three embryonic stages, wepooled the data of un-infested ovigerous females independentof their developmental stage to assess the impact of parasiteson egg production: ANCOVAs revealed statistically signifi-cant differences between the two slopes (Figure 5); femalesinfested by bopyrids carried 41% fewer eggs than similar-sizedfemales without parasites.

Egg length and egg volume in Stages I and III of infestedfemales varied between 0.74 and 0.97 mm (average:0.86+0.179 mm) and from 0.118 to 0.246 mm3 (average:0.17+0.116 mm3), respectively. The volume increase duringdevelopment was slightly higher in the un-infested than ininfested females (117% versus 108%, respectively). Wedetected, however, no statistically significant differencesbetween the egg length and egg volume carried by bothinfected and un-infected females (Student’s t-test, P . 0.05).

The morphological sexual maturity of un-infested femaleswas reached at a size of 5.7 mm CL (Figure 6). The relativelylow number of ovigerous females with parasites did not allowa similar analysis for this group. The same figure shows thenumber of parasitized females per size-class. The smallestindividuals (3.1–4.0 mm CL) were not infested, and parasiteswere detected exclusively in ovigerous females ranging in sizebetween 4.6 and 9.4 mm CL. Highest occurrence was recordedin egg-bearing females between 5.1 and 8.0 mm CL, represent-ing 72% of all infested specimens.

Other alpheid speciesTable 1 presents some preliminary data on egg production intwo other sponge-associated Synalpheus species (S. chacei andS. idios), and two free-living alpheids, Alpheus angulosus andAutomate evermanni (all from Bocas del Toro). The largestof them, A. angulosus, carried the highest number of eggs;S. idios, one of the smallest species studied herein, producedthe lowest number of eggs, which, however, were by far thelargest (1.04 mm3). Egg volume among these four speciesvaried between 0.09 mm3 and 0.16 mm3 (Table 1).

Fig. 4. Egg volume (mean+SD) of developing embryos (Stages I–III) ofun-infested and infested females of Synalpheus yano in Bocas del Toro,Caribbean coast of Panama. The numbers for un-infested and infestedfemales indicate the increase of egg volume during embryonic development.

Fig. 5. Egg production in Synalpheus yano from Bocas del Toro, Caribbeancoast of Panama, with a comparison of slopes between un-infested andinfested females.

Fig. 6. Number of individuals of un-infested and infested females persize-range (carapace length (CL)), and morphological maturity curve inun-infested ovigerous females of Synalpheus yano in Bocas del Toro,Caribbean coast of Panama. The number indicates the size at first maturityestablished as the 50% of the overall.

4 patricio herna’ ez et al.

D I S C U S S I O N

Social organization of S. yanoSo far, eusociality has been documented or is strongly sus-pected in nine western Atlantic species of Synalpheus, includ-ing S. regalis, S. chacei, S. filidigitus, S. duffyi and S. riosi(Duffy, 1996, 1998; Duffy & Macdonald, 1999; Anker &Toth, 2008). This life style implies a complex social organiz-ation where reproduction is restricted to a single female, the‘queen’ (Duffy, 1996, 2007). Although at first glance, S. yanomay appear as a ‘colonial species’, based on large numbersof individuals obtained from the same host sponge, it actuallyis a pair-living species, with each male–female pair beingrestricted to a small portion of the host sponge (A. Anker, per-sonal observation). Sponge portioning among different indi-viduals of S. yano, or between S. yano and other species ofSynalpheus such as S. dardeaui, remains to be investigatedin detail.

Egg production in S. yanoIn comparison to other caridean shrimps (see Corey & Reid,1991) S. yano produces relatively large eggs (0.7–1.3 mm indiameter). However, when compared to the available datafor other representatives of Synalpheus, the egg size ofS. yano is within the range reported for other species of thisgenus (Table 2). Although the range of egg size in allsponge-dwelling species of Synalpheus listed in Table 2 fluctu-ates around 1 mm, reproductive strategies are different amongspecies: S. brooksi and S. longicarpus are known to have aquasi-direct development, whereas all other species seem tohave at least one zoeal stage. In the case of S. yano, a recently-hatched larva is a typical Zoea I (see Albornoz & Wehrtmann,1997), with sessile eyes, a telson bearing 7þ7 distal spines, and

without developing uropods. Thus, egg size alone, even inspecies of the same genus, inhabiting the same type of habitats,and having roughly the same adult size (e.g. S. longicarpus), isnot a reliable indicator for the type of postembryonic develop-ment. Future studies need to clarify the underlying evolution-ary and ecological factors responsible for shaping thereproductive strategy in these sponge-dwelling species.

In un-infested S. yano, the egg volume increased approxi-mately 118% during embryogenesis, whilst egg loss duringembryonic development was low (�15%) and statisticallynot significant. Egg loss in S. yano is within the range reportedfor some other alpheid shrimps, e.g. Betaeus emarginatus:11.6%; B. truncatus: 19.1% (Lardies & Wehrtmann, 2001);Alpheus armillatus: 12.2% (Pavanelli et al., 2008). Egg swellingduring egg development is well documented in decapods, andmay fluctuate in alpheid shrimps between 19% and 274%(Corey & Reid, 1991; Lardies & Wehrtmann, 2001). The factthat despite a substantial egg swelling during embryogenesisthe observed egg loss was insignificant suggests that thespace available for the egg attachment in S. yano is sufficientto accommodate and to maintain the total number of eggsuntil hatching occurs. This scenario contradicts the generalassumption that substantial egg volume increase is associatedwith a considerable egg loss during embryonic development(Kuris, 1991). The low egg mortality observed in S. yanomight be related to: (1) an efficient parental care duringembryogenesis promoted by the pair living in a smallportion of the host; and (2) to the fact that this species livesin sponges, which provide a relatively protected microhabitat,reducing the possible abrasion of developing egg during rapidmovements and probably containing fewer pathogenescompared to the exterior.

The efficiency of a size-specific fecundity regression modelin decapods generally is evaluated by the coefficient of deter-mination (Somers, 1991). In S. yano, the determination

Table 1. Range and average of carapace length (CL), number of produced eggs (EN) and egg volume (EV) in six species of the family Alpheidae fromBocas del Toro, Caribbean coast of Panama. N, number of individuals; SD, standard deviation.

Species N Carapace length (mm) Number of eggs (mm) Egg volume (mm3)

Range Mean+++++SD Range Mean+++++SD Range Mean+++++SD

Alpheus angulosus 01 — 9.0 — 146 — 0.09Automate evermanni 01 — 7.1 — 67 — 0.16Synalpheus chacei 02 — 3.7/3.7 — 14/18 — 0.14/0.16S. idios 04 3.7–4.2 3.9+0.21 9–18 12+4.3 0.70–1.20 1.04+0.233S. scaphoceris 01 — 4.3 — 33 — 0.16S. yano 84 3.7–9.6 5.6+1.16 6–246 98+64.6 0.06–0.51 0.15+0.084

Table 2. Range of carapace length, number of produced eggs, egg size and number of larval stages in some sponge-dwelling Synalpheus from the westernAtlantic. Carapace length and egg number were obtained from Corey & Reid (1991), size of eggs and number of larval stages are from Brooks & Herrick,

(1892), Coutiere, (1909) and Dobkin, (1965, 1969).

Species Carapace lengthrange (mm)

Egg numberrange

Size eggrange (mm)

Number oflarval stages

References

S. brooksi 3.4–4.5 1–15 0.9–1.6 0 (directdevelopment)

Dobkin, 1965, 1969

S. herricki 3.5–5.1 11–81 .1 1 Coutiere, 1909; Corey & Reid, 1991S. longicarpus 5.5–8.0 27–349 1–1.1 0 (direct

development)Brooks & Herrick, 1892; Corey &

Reid, 1991S. pectiniger 3.5–4.6 4–17 .1 1 Coutiere, 1909; Corey & Reid, 1991S. yano 3.7–9.6 6–246 0.6–1.3 1 or more Present study

reproduction and bopyrid infestation in s. yano 5

coefficient (lineal regression: r2 ¼ 0.43) was within the rangereported for other alpheid shrimps from temperate and tropi-cal–subtropical waters (0.23 to 0.97; Corey & Reid, 1991;Lardies & Wehrtmann, 1997, 2001; Pavanelli et al., 2008).Present evidence suggests that sponge-dwelling Synalpheushave a low relationship between egg number and femalebody size (S. brooksi ¼ 0.54, S. longicarpus ¼ 0.65 andS. pectiniger ¼ 0.23; Corey & Reid, 1991), and thus S. yanois not an exception. All these species are known to beoccasionally infested by abdominal bopyrid parasites(Dardeau, 1984), which in brooding females interact withtheir egg masses. Therefore, we assume that the low determi-nation coefficient may be linked to the bopyrid parasitism.However, this aspect needs further attention in future studies.

Reproductive output of S. yanoBrood weight of marine decapods is highly variable and gener-ally constrained to approximately 4 to 30% of the female bodyweight, for instance in Alpheoidea: 7–12% (Pavanelli et al.,2008, in press); in Anomura: 3–33% (Hernaez & Palma,2003); in Brachyura: 10% (Hines, 1982), and in Thalassinidea:15% (Hernaez et al., 2008). Ovigerous females of S. yano inverted35% of their weight in egg production, and this value is substan-tially higher than those observed in some temperate-cold wateralpheids, such as Betaeus emarginatus: 8.5%, and B. truncatus:9.7–14% (Lardies & Wehrtmann, 2001), and other subtropicalspecies such as A. armillatus: 12.1% (Pavanelli et al., 2008)and A. nuttingi: 7.3% (Pavanelli et al., in press). The largereproductive output in S. yano may be an adaptation to asponge-dwelling life style. This conclusion is supportedby the fact that pinnotherid crabs living in different hostspecies show even higher reproductive outputs, e.g.Pinnotheres ostreum (Pinnotheridae): 66%, and Fabia subqua-drata (Pinnotheridae): 97% (Hines, 1992).

Effects of parasitism on egg production inS. yano compared to data availablefor other decapodsTo our best knowledge, the present report is the first to highlightthe impact of the infestation by abdominal bopyrids on egg pro-duction in an alpheid shrimp. Our results demonstrate that thefecundity of S. yano diminishes considerably in females infestedby bopyrids (Figure 5). It is speculated that the presence of theenormous bopyrid isopod in the abdomen (Figure 2) limitsthe available space for egg attachment, which results in consider-ably lower egg numbers in infested versus similar-sizedun-infested females (Figure 5). There is ample evidence of para-sitic castration in different decapods (Caridea: Beck, 1980;Calado et al., 2005; Anomura: Gonzalez & Acuna, 2004;Brachyura: Shields & Wood, 1993; Brockerhoff, 2004).Concerning caridean shrimps, Calado et al. (2005) studied theeffects of parasitic isopods on the reproduction of the protandricsimultaneous hermaphrodite caridean shrimp Lysmata seticau-data (Hippolytidae), and Beck (1980) examined the effects of abopyrid ectoparasite on sexual characteristics of Palaemonetespaludosus (Palaemonidae). In marked contrast to parasitizedfemales of S. yano, parasitized females of L. seticaudata andP. paludosus were not able to produce embryos. The simul-taneous presence of the bopyrids and developing eggs wasobserved also in Upogebia pugettensis (Upogebiidae), but this

phenomenon was extremely rare (Smith et al., 2008): the onlytwo ovigerous females with parasites carried substantiallyfewer eggs than un-infested females. Dardeau (1984) mentionedthe presence of hemiarthrine bopyrids in several Synalpheus(S. brooksi, S. longicarpus and S. pandionis), however, withoutindicating effects of these parasites on egg number in infestedovigerous females. Both Dardeau’s and our findings clearlyshow that infestation by bopyrid parasites does not necessarilyresult in the ‘castration’ (or in case of females: sexual inability)of the Synalpheus host.

According to our results, the infestation rate is higher inmedium-sized individuals of S. yano than in smaller ones(Figure 6). This size preference of the parasites might berelated to the moult cycle of the host: since the time intervalbetween successive moulting increases gradually with age(Bliss, 1982), it might be advantageous for the parasite toselect larger individuals of S. yano which moult less frequentlythan the smaller (younger) shrimp.

We recommend that in all future studies on fecundity indecapod crustaceans, females infested by abdominal bopyridsor other parasites, such as rhizocephalans, should be treatedseparately from un-infested females to allow a direct assess-ment of parasitism on egg production.

A C K N O W L E D G E M E N T S

We are grateful to the Smithsonian Tropical Research Institute(STRI) and the STRI station in Bocas del Toro, Panama, forproviding facilities for this study, and to Sammy De Grave(Oxford University Museum of Natural History, Oxford,UK) and Rachel Collin for co-instructing and organizing,respectively, the shrimp taxonomy course in Bocas del Toroin August 2008. We thank Catalina Benavides (UNIP,Universidad de Costa Rica), who helped us with the prep-aration of Figure 1, and two anonymous referees for theirconstructive comments.

R E F E R E N C E S

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Anker A. and Felder D.L. (2005) Description of Coutieralpheus setirostris,new genus, new species, an infaunal alpheid shrimp (Crustacea,Decapoda) from Florida, U.S.A. Crustacean Research 34, 40–52.

Anker A. and Iliffe T.M. (2000) Description of Bermudacaris harti, a newgenus and species (Crustacea: Decapoda: Alpheidae) from anchialinecaves of Bermuda. Proceedings of the Biological Society ofWashington 113, 761–775.

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Correspondence should be addressed to:Ingo S. WehrtmannEscuela de BiologıaUniversidad de Costa Rica2060 San Jose, Costa Ricaemail: ingowehrtmann@gmx.de

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