Journal of the Marine Biological Association of the United Kingdom, page 1 of 8. doi:10.

1017/S0025315409991093

# Marine Biological Association of the United Kingdom, 2009

Fecundity and effects of bopyrid infestation on egg production in the Caribbean sponge-dwelling snapping shrimp Synalpheus yano (Decapoda: Alpheidae)
ez1,2, betel marti nez-guerrero3, arthur anker4 and ingo s. wehrtmann1,5 patricio herna
n Pesquera y Acuicultura (UNIP), Centro de Investigaciones en Ciencias del Mar y Limnolog a, Universidad Unidad de Investigacio tica de de Costa Rica (CIMAR), 2Museo del Mar, Universidad Arturo Prat, Casilla 121, Iquique, Chile, 3Laboratorio de Sistema ngel, Puerto A ngel, Oaxaca CP 70902, Me xico, Invertebrados Marinos (LABSIM), Universidad del Mar, Campus Puerto A 4 a, Dickinson Hall, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611-7800, USA, 5Escuela de Biolog , Costa Rica Universidad de Costa Rica, 2060 San Jose
1

Several Synalpheus species have been reported as hosts of bopyrid parasites; however, the impact of infestation on egg production is still unknown. Therefore, the present work studied reproductive aspects and the effect of parasitism on fecundity of the alpheid shrimp Synalpheus yano from Bocas del Toro, Caribbean coast of Panama. Un-infested females (N 84) ranging from 3.7 to 9.6 mm carapace length, produced between 5 and 246 eggs (average: 98+64.6), and egg number increased signicantly with female size. The eggs were relatively large (0.6 1.3 mm in diameter), but within the range of other Synalpheus species, and egg size did not differ signicantly between un-infested and infested females. Despite these large eggs, the morphological characteristics of hatching larvae indicate a planktotrophic development. During the incubation period, 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 in larger 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-sized females without parasites. The co-occurrence of parasites and developing eggs, however, indicates that the bopyrid parasite does not necessarily castrate its host. Therefore, we encourage more comparative intraspecic studies on egg production in infested 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

INTRODUCTION

The American species of the snapping shrimp family Alpheidae have received a great deal of attention during the last decade. Most publications involving these interesting caridean shrimps are taxonomic descriptions and species revisions (i.e. Anker & Iliffe, 2000; Anker & Felder, 2005; os & Duffy, 2007; Anker et al., 2007, 2008), Anker, 2007; R new records and range extensions (i.e. Hermoso-Salazar & Hendrickx, 2005; Anker, 2007), behavioural studies, i.e. on mate choice (Rahman et al., 2004) and studies on eusociality (Duffy et al., 2002; Duffy, 2003), as well as results from still ongoing 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 tropical American alpheids is rather poor. Corey & Reid (1991)

Corresponding author: I.S. Wehrtmann Email: ingowehrtmann@gmx.de

examined reproductive aspects of 16 alpheid species from Florida; their results revealed that many of these species tend to produce small eggs. There is, however, evidence that alpheid shrimps can also produce large eggs, indicating a tendency for an abbreviated larval development (Felder, 1982; Dardeau, 1984; Wehrtmann & Albornoz, 2002). To our best knowledge, data on reproductive patterns of Central American alpheids are still decient except for the description of rst postembryonic stages in the transisthmian sister species Alpheus saxidomus and A. simus (Wehrtmann & Albornoz, 2002). Fecundity has been widely recognized as one of the ecologically most important features in the life history of many invertebrates, including decapod crustaceans (i.e. Hines, 1991; Somers, 1991). This aspect usually refers to the total number of eggs (here we use the term eggs also for developing embryos) carried by the females. As in many decapods, a positive relationship has been observed between fecundity and female size in alpheid shrimps. The correlation coefcient (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 of eggs during the embryogenesis (for review see Kuris, 1991).
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ez et al . patricio herna

Egg size offers valuable information on a species reproductive strategy. It serves as a useful indicator for the duration of embryogenesis and larval size at hatching (Steele & Steele, pez, 2003). Many species of 1975; Wehrtmann & Lo Synalpheus show a clear correlation between egg size and type of larval development, ranging from normal ( `re, extended) via abbreviated to quasi-direct (see Coutie 1898; Dardeau, 1984; Duffy, 1996). However, more detailed information on this issue is presently restricted to just a few alpheid species. Synalpheus, being one of the most species-rich genera of the Alpheidae, with well over 60 species in the Caribbean region os & Duffy, 2007; Anker & To th, 2008), received alone (R more attention compared to the other genera of this family, mainly due to the fact that some species form eusocial colonies in sponges (Duffy et al., 2000, 2002). The eusocial Synalpheus inhabit the internal canals of larger demosponges, forming colonies of up to several hundred individuals, but containing only one reproductive female equivalent of a queen in insect societies. Despite this extraordinary behaviour and a great scientic potential of these shrimps, their reproductive biology is poorly known (Duffy et al., 2002). However, the vast majority of sponge-dwelling Synalpheus are pair-living species. Synalpheus yano (originally described as Zuzalpheus yano os & Duffy, 2007; see Anker & De Grave, 2008 for synoR nymy of Zuzalpheus) is apparently a pair-living species. It is one of the most common sponge-dwelling species of Synalpheus of Bocas del Toro, a small archipelago on the Caribbean coast of Panama. In Bocas del Toro, this species most frequently associates with the bright red-orange sponge Lissodendoryx colombiensis Zea & van Soest, 1986. The same sponge is used by S. yano as main host at the type locality in Belize, although three other sponge species have os & Duffy, 2007). been reported as facultative hosts there (R The presence of parasitic bopyrid isopods (Epicaridea: Bopyridae; mainly Bopyrinae and Hemiarthrinae), has been documented in a number of decapod crustaceans, including species of Alpheus and Synalpheus (Markham, 1986). These

parasites may cause castration by: (1) inhibiting the maturation of the female gonad; and (2) feminizing parasitized males (Reinhard, 1956; van Wyk, 1982; OBrien & van Wyk, lez & Acun a, 2004; Calado et al., 2005). Most 1985; Gonza studies focus on the intensity and prevalence of infestation, population structure and energetics of the bopyrid isopod lez & parasite and its decapod host (Beck, 1980; Gonza a, 2004; Smith et al., 2008). However, detailed data on Acun the impact of parasitic infestation on egg production in carideans are rather limited. The presence of adult abdominal bopyrids in egg-bearing females of Synalpheus highlights the complexity of parasite host interactions and the lack of knowledge on this topic (see Calado et al., 2005). The aim of the present study is to provide information on the fecundity, egg volume and energy allocation for reproduction in S. yano. Also shown are the effects of parasitism by bopyrids on egg production in this species. We compare our results with those available for other tropical subtropical alpheid species.

MATERIALS AND METHODS

Study area
Ovigerous females of S. yano were collected in August 2008 during a shrimp taxonomy course in Bocas del Toro, Caribbean coast of Panama (Figure 1). The Bocas del Toro archipelago comprises several larger and many smaller islands and patchy reefs and sponge gardens supporting a very diverse fauna. Initially, a small number of ovigerous females of S. yano were extracted from internal canals of a red-orange sponge, Lissodendoryx colombiensis that is fairly common in these sponge gardens and also grows on jetty pilings or large pieces of coral rubble, at shallow depths (1 5 m). Consequently, a fairly large number (.20) of these sponges was collected and revised to obtain a sufcient number of ovigerous females. In the laboratory,

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

reproduction and bopyrid infestation in s. yano

specimens were extracted from sponge canals and preserved in ethanol (75%). We also collected ovigerous females of other alpheid species (Alpheus spp., other Synalpheus spp. and Automate sp.), e.g. in coral rubble and other sponges. The total number of collected individuals per species was relatively low, mostly due to time constraints. However, because of insufcient knowledge of reproductive traits in Central American Alpheidae, we decided to include these data in the present study.

difference between egg numbers per stage (P , 0.05), a Tukey a posteriori test was applied to establish the similarity between each pair of developmental stages (Zar, 1999). The area of egg attachment was frequently infested with ez, parasitic isopods, Hemiarthrinae (Dardeau, 1984; P. Herna personal observation; Figure 2). In order to evaluate the possible impact of parasitic infestation on egg production, we analysed the fecundity of infested and non-infested females, and compared the slopes of each scenario applying the analysis of covariance (ANCOVA; Zar, 1999).

Analyses of material
All specimens of Synalpheus were identied using an identios & Duffy (2007). We measured the cation key based on R carapace length (CL, in mm) of each female from the tip of the rostrum to the posterior margin of the carapace; this measurement was recorded with the aid of a stereomicroscope provided with an ocular micrometer (nearest 0.1 mm). The size at rst maturity was established as 50% of the overall size frequency distribution for ovigerous females, as determined after tting a sigmoid curve to the relationship between the percentage of ovigerous females and size, using 0.1 mm size-classes (Wenner et al., 1974). After removing the complete egg mass from each female, the total number of eggs (EN) was determined by counting them under a Leitz stereomicroscope. All collected ovigerous females of S. yano were examined for the presence of parasitic isopods (Epicaridea, Bopyridae and Hemiarthrinae) (see Dardeau, 1984; Markham, 1985). Developing eggs of each species were classied into three stages (Stages I III) based on the shape and development of both abdomen and eyes, as described by Wehrtmann (1990). We separated arbitrarily 20 embryos from the egg mass and measured the width and length of each egg under a microscope equipped with a calibrated ocular micrometer. These data were used to calculate egg volume (EV) according to the formula proposed by Turner & Lawrence (1979) for oblate spheroids: EV 1/6 (a b2 p), where a represents length, and b width. The volume increment during the incubation period was calculated using the equation proposed by Kobayashi & Matsuura (1995). The energy allocation for egg production was estimated by determining the reproductive output (RO) of the females, considering only recently extruded eggs (Stage I). Females and their corresponding egg masses were dried at 60C for 24 hours, and the resulting data were used in the formula proposed by Clarke et al. (1991): RO dry weight of the entire egg mass/dry weight of the female without eggs.

RESULTS

Egg production of un-infested females S. yano

A total of 249 individuals of S. yano were analysed; 112 of them were ovigerous females (45%). Regarding the un-infested females (N 84), 23 were at Stage I, 37 at Stage II, and 24 females carried eggs close to hatching (Stage III). These females measured from 3.7 to 9.6 CL mm (average 5.6+1.16 mm), and 73% of them were in the range between 4.1 and 6.0 mm CL. The total number of eggs in un-infested S. yano varied between 6 and 246 (average: 98+64.6). The fecundity increased signicantly with female size (simple regression; r 0.70; P , 0.05); however, the correlation was relatively low explaining approximately 50% of the observed variability (Figure 3). During the incubation period,

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

Data analysis
The relation between fecundity and female size was described by an allometric model (Y a . Xb), which has been used widely for this purpose in similar studies with other decapods ez & Palma, (i.e. Corey & Reid, 1991; Hines, 1991; Herna 2003). According to Somers (1991), an isometric relation is indicated by values for b that are near 3. Thus, b values of ,2.90 and . 3.10 were taken as indication of a negative and positive allometric relation, respectively (Somerton, 1980). An analysis of covariance (ANCOVA; Zar, 1999) was applied to analyse the relation between egg number and female CL for each embryonic stage to estimate possible egg loss during the incubation period. In the case of a signicant

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

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un-infested females of S. yano lost approximately 16% of their initially produced eggs (ANCOVA, f 23.5; P , 0.05). However, no statistically signicant differences were detected between numbers of eggs at different developmental stages (Tukey test, P . 0.05). During the incubation period, the egg volume in un-infested females increased from 0.100 to 0.218 mm3, representing an overall increase of 118% (Figure 4). The average RO of S. yano was 25.7+11.48% of their dry weight, and varied between 10.5 and 44.9%. RO did not increase with the female size (Spearman test, P . 0.05). The egg mass comprised on average 35% of the dry body weight of females.
Fig. 5. Egg production in Synalpheus yano from Bocas del Toro, Caribbean coast of Panama, with a comparison of slopes between un-infested and infested females.

Comparison of egg production between infested and un-infested females of S. yano

Out of 112 analysed egg-bearing females, 18 (16%) were infested by bopyrids; seven females carried eggs in Stage I, four in Stage II and seven in Stage III. Infested females measured 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 approximately 39% of their initially produced eggs (ANCOVA, f 23.5; P , 0.05), and no statistically signicant differences were detected between the numbers of eggs at different developmental stages (Tukey test, P , 0.05). Since we did not detect any statistically signicant difference of egg number between the three embryonic stages, we pooled the data of un-infested ovigerous females independent of their developmental stage to assess the impact of parasites on egg production: ANCOVAs revealed statistically signicant differences between the two slopes (Figure 5); females infested by bopyrids carried 41% fewer eggs than similar-sized females without parasites. Egg length and egg volume in Stages I and III of infested females 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 during development was slightly higher in the un-infested than in infested females (117% versus 108%, respectively). We detected, however, no statistically signicant differences between the egg length and egg volume carried by both infected and un-infected females (Students t-test, P . 0.05).

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

The morphological sexual maturity of un-infested females was reached at a size of 5.7 mm CL (Figure 6). The relatively low number of ovigerous females with parasites did not allow a similar analysis for this group. The same gure shows the number of parasitized females per size-class. The smallest individuals (3.1 4.0 mm CL) were not infested, and parasites were detected exclusively in ovigerous females ranging in size between 4.6 and 9.4 mm CL. Highest occurrence was recorded in egg-bearing females between 5.1 and 8.0 mm CL, representing 72% of all infested specimens.

Other alpheid species

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

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

reproduction and bopyrid infestation in s. yano

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 from Bocas del Toro, Caribbean coast of Panama. N, number of individuals; SD, standard deviation. Species N Carapace length (mm) Range Alpheus angulosus Automate evermanni Synalpheus chacei S. idios S. scaphoceris S. yano 01 01 02 04 01 84 3.74.2 3.79.6 Mean+SD 9.0 7.1 3.7/3.7 3.9+0.21 4.3 5.6+1.16 Number of eggs (mm) Range 918 6246 Mean+SD 146 67 14/18 12+4.3 33 98+64.6 Egg volume (mm3) Range 0.701.20 0.060.51 Mean+SD 0.09 0.16 0.14/0.16 1.04+0.233 0.16 0.15+0.084

DISCUSSION

Social organization of S. yano

So far, eusociality has been documented or is strongly suspected in nine western Atlantic species of Synalpheus, including S. regalis, S. chacei, S. lidigitus, S. duffyi and S. riosi (Duffy, 1996, 1998; Duffy & Macdonald, 1999; Anker & th, 2008). This life style implies a complex social organizTo ation where reproduction is restricted to a single female, the queen (Duffy, 1996, 2007). Although at rst glance, S. yano may appear as a colonial species, based on large numbers of individuals obtained from the same host sponge, it actually is a pair-living species, with each male female pair being restricted to a small portion of the host sponge (A. Anker, personal observation). Sponge portioning among different individuals of S. yano, or between S. yano and other species of Synalpheus such as S. dardeaui, remains to be investigated in detail.

Egg production in S. yano

In comparison to other caridean shrimps (see Corey & Reid, 1991) S. yano produces relatively large eggs (0.7 1.3 mm in diameter). However, when compared to the available data for other representatives of Synalpheus, the egg size of S. yano is within the range reported for other species of this genus (Table 2). Although the range of egg size in all sponge-dwelling species of Synalpheus listed in Table 2 uctuates around 1 mm, reproductive strategies are different among species: S. brooksi and S. longicarpus are known to have a quasi-direct development, whereas all other species seem to have at least one zoeal stage. In the case of S. yano, a recentlyhatched larva is a typical Zoea I (see Albornoz & Wehrtmann, 1997), with sessile eyes, a telson bearing 77 distal spines, and

without developing uropods. Thus, egg size alone, even in species of the same genus, inhabiting the same type of habitats, and having roughly the same adult size (e.g. S. longicarpus), is not a reliable indicator for the type of postembryonic development. Future studies need to clarify the underlying evolutionary and ecological factors responsible for shaping the reproductive strategy in these sponge-dwelling species. In un-infested S. yano, the egg volume increased approximately 118% during embryogenesis, whilst egg loss during embryonic development was low (15%) and statistically not signicant. Egg loss in S. yano is within the range reported for 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 swelling during egg development is well documented in decapods, and may uctuate in alpheid shrimps between 19% and 274% (Corey & Reid, 1991; Lardies & Wehrtmann, 2001). The fact that despite a substantial egg swelling during embryogenesis the observed egg loss was insignicant suggests that the space available for the egg attachment in S. yano is sufcient to accommodate and to maintain the total number of eggs until hatching occurs. This scenario contradicts the general assumption that substantial egg volume increase is associated with a considerable egg loss during embryonic development (Kuris, 1991). The low egg mortality observed in S. yano might be related to: (1) an efcient parental care during embryogenesis promoted by the pair living in a small portion of the host; and (2) to the fact that this species lives in sponges, which provide a relatively protected microhabitat, reducing the possible abrasion of developing egg during rapid movements and probably containing fewer pathogenes compared to the exterior. The efciency of a size-specic fecundity regression model in decapods generally is evaluated by the coefcient of determination (Somers, 1991). In S. yano, the determination

Table 2. Range of carapace length, number of produced eggs, egg size and number of larval stages in some sponge-dwelling Synalpheus from the western Atlantic. Carapace length and egg number were obtained from Corey & Reid (1991), size of eggs and number of larval stages are from Brooks & Herrick, `re, (1909) and Dobkin, (1965, 1969). (1892), Coutie Species S. brooksi S. herricki S. longicarpus S. pectiniger S. yano Carapace length range (mm) 3.44.5 3.55.1 5.58.0 3.54.6 3.79.6 Egg number range 115 1181 27349 417 6246 Size egg range (mm) 0.91.6 .1 1 1.1 .1 0.61.3 Number of larval stages 0 (direct development) 1 0 (direct development) 1 1 or more References Dobkin, 1965, 1969 `re, 1909; Corey & Reid, 1991 Coutie Brooks & Herrick, 1892; Corey & Reid, 1991 `re, 1909; Corey & Reid, 1991 Coutie Present study

ez et al . patricio herna

coefcient (lineal regression: r2 0.43) was within the range reported for other alpheid shrimps from temperate and tropical subtropical waters (0.23 to 0.97; Corey & Reid, 1991; Lardies & Wehrtmann, 1997, 2001; Pavanelli et al., 2008). Present evidence suggests that sponge-dwelling Synalpheus have a low relationship between egg number and female body size (S. brooksi 0.54, S. longicarpus 0.65 and S. pectiniger 0.23; Corey & Reid, 1991), and thus S. yano is not an exception. All these species are known to be occasionally infested by abdominal bopyrid parasites (Dardeau, 1984), which in brooding females interact with their egg masses. Therefore, we assume that the low determination coefcient may be linked to the bopyrid parasitism. However, this aspect needs further attention in future studies.

Reproductive output of S. yano

Brood weight of marine decapods is highly variable and generally constrained to approximately 4 to 30% of the female body weight, for instance in Alpheoidea: 712% (Pavanelli et al., ez & Palma, 2008, in press); in Anomura: 333% (Herna 2003); in Brachyura: 10% (Hines, 1982), and in Thalassinidea: ez et al., 2008). Ovigerous females of S. yano inverted 15% (Herna 35% of their weight in egg production, and this value is substantially higher than those observed in some temperate-cold water alpheids, such as Betaeus emarginatus: 8.5%, and B. truncatus: 9.714% (Lardies & Wehrtmann, 2001), and other subtropical species such as A. armillatus: 12.1% (Pavanelli et al., 2008) and A. nuttingi: 7.3% (Pavanelli et al., in press). The large reproductive output in S. yano may be an adaptation to a sponge-dwelling life style. This conclusion is supported by the fact that pinnotherid crabs living in different host species show even higher reproductive outputs, e.g. Pinnotheres ostreum (Pinnotheridae): 66%, and Fabia subquadrata (Pinnotheridae): 97% (Hines, 1992).

phenomenon was extremely rare (Smith et al., 2008): the only two ovigerous females with parasites carried substantially fewer eggs than un-infested females. Dardeau (1984) mentioned the presence of hemiarthrine bopyrids in several Synalpheus (S. brooksi, S. longicarpus and S. pandionis), however, without indicating effects of these parasites on egg number in infested ovigerous females. Both Dardeaus and our ndings clearly show that infestation by bopyrid parasites does not necessarily result in the castration (or in case of females: sexual inability) of the Synalpheus host. According to our results, the infestation rate is higher in medium-sized individuals of S. yano than in smaller ones (Figure 6). This size preference of the parasites might be related to the moult cycle of the host: since the time interval between successive moulting increases gradually with age (Bliss, 1982), it might be advantageous for the parasite to select larger individuals of S. yano which moult less frequently than the smaller (younger) shrimp. We recommend that in all future studies on fecundity in decapod crustaceans, females infested by abdominal bopyrids or other parasites, such as rhizocephalans, should be treated separately from un-infested females to allow a direct assessment of parasitism on egg production.

ACKNOWLEDGEMENTS

Effects of parasitism on egg production in S. yano compared to data available for other decapods
To our best knowledge, the present report is the rst to highlight the impact of the infestation by abdominal bopyrids on egg production in an alpheid shrimp. Our results demonstrate that the fecundity of S. yano diminishes considerably in females infested by bopyrids (Figure 5). It is speculated that the presence of the enormous bopyrid isopod in the abdomen (Figure 2) limits the available space for egg attachment, which results in considerably lower egg numbers in infested versus similar-sized un-infested females (Figure 5). There is ample evidence of parasitic castration in different decapods (Caridea: Beck, 1980; lez & Acun a, 2004; Calado et al., 2005; Anomura: Gonza Brachyura: Shields & Wood, 1993; Brockerhoff, 2004). Concerning caridean shrimps, Calado et al. (2005) studied the effects of parasitic isopods on the reproduction of the protandric simultaneous hermaphrodite caridean shrimp Lysmata seticaudata (Hippolytidae), and Beck (1980) examined the effects of a bopyrid ectoparasite on sexual characteristics of Palaemonetes paludosus (Palaemonidae). In marked contrast to parasitized females of S. yano, parasitized females of L. seticaudata and P. paludosus were not able to produce embryos. The simultaneous presence of the bopyrids and developing eggs was observed also in Upogebia pugettensis (Upogebiidae), but this

We are grateful to the Smithsonian Tropical Research Institute (STRI) and the STRI station in Bocas del Toro, Panama, for providing 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 Toro in August 2008. We thank Catalina Benavides (UNIP, Universidad de Costa Rica), who helped us with the preparation of Figure 1, and two anonymous referees for their constructive comments.

REFERENCES
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reproduction and bopyrid infestation in s. yano

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Correspondence should be addressed to: Ingo S. Wehrtmann a Escuela de Biolog Universidad de Costa Rica , Costa Rica 2060 San Jose email: ingowehrtmann@gmx.de