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Research Article
Preliminary survey of a nemertean crab egg predator, Carcinonemertes, on its host crab, Callinectes arcuatus (Decapoda, Portunidae) from Golfo de Nicoya, Pacific Costa Rica
expand article infoRobert Okazaki, Ingo Wehrtmann
† Weber State University, Ogden, United States of America
‡ Universidad de Costa Rica, San Pedro de Montes de Oca, Costa Rica
Open Access

Abstract

The possible presence of egg predators in brood masses of portunid crabs from Pacific Central America has not been studied yet. This survey reports the finding of a nemertean crab egg predator on the portunid crab, Callinectes arcuatus, from the Golfo de Nicoya, Pacific Costa Rica. Nemerteans were found in the egg masses of 26 out of the 74 crabs for a prevalence of 35%. The intensity (mean number of worms/ infected crab) was estimated to be 18 with a variance of 1–123 worms/infected crab. No nemerteans were observed either in the 19 C. arcuatus from Golfo Dulce (southern Pacific coast) and the 10 Portunus asper from Herradura-Jaco (central Pacific coast). This nemertean is a member of the genus Carcinonemertes, which has been reported from the Caribbean coast of Panama. However, the encountered Carcinonemertes sp. is the first published finding and report from Costa Rica and Pacific Central America.

Keywords

Callinectes arcuatus, egg mortality, crab egg predator, Central America

Introduction

The arched portunid crab, Callinectes arcuatus Ordway, 1863 has become an increasingly important growing fishery resource along the Pacific coast from Mexico to Ecuador (Paul 1982; Castro and De Alteris 1989). In the Golfo de Nicoya of the Pacific coast of Costa Rica, Dittel (1993) reported a large population of this portunid crab. More recently, Fischer and Wolff (2006) analyzed the current level of exploitation of this resource by size frequency analysis of trap and trawl catches in the Golfo de Nicoya; the results of this study revealed the potential of increasing catch yield about 20% without a detriment to the crab population. Thus, the C. arcuatus fishery is becoming recognized as a commercially important fishery for Costa Rica.

Phylum Nemertea, commonly called ribbon or proboscid worms, comprise approximately 1250 species (Kajihara et al. 2008). These ribbon worms are generally predators using their proboscis to capture prey. One monostiliferous hoplonemertean family, Carcinonemertidae, consists of nemerteans that are ecto-symbiont egg predators of decapods (Wickham and Kuris 1985, 1988, Kuris and Wickham 1987; Kuris 1993; McDermott 2006; Sadeghian and Santos 2010). These worms were implicated to cause 50% brood mortality in the Cancer magister fishery in northern California (Wickham 1979).

Carcinonemertids have been reported in Panamanian crabs, but so far only from the Caribbean coast (Collin et al. 2005). As far as we know, no published information is available about the possible infestation of egg masses of portunid crabs along the Pacific coast of Central America. Therefore, this study was conducted to determine if nemertean crab egg predators are present on Callinectes arcuatus from Golfo de Nicoya. If these nemerteans are found, then baseline numbers of infestation and incidence can be established to monitor future increases and their impact on a growing fishery.

Methods

The following numbers and species of ovigerous crabs were collected by local fishermen: 74 specimens of Callinectes arcuatus from Golfo de Nicoya, central Pacific (10°0'00"N, 85°0'00"W), 19 of C. arcuatus from Golfo Dulce, southern Pacific (8°32'16"N, 84°41'35"W), and 10 of Portunus asper (A. Milne-Edwards, 1861) from trawls off the coast of Herradura-Jaco, central Pacific (9°64'00"N, 84°65'00"W). All crabs were shipped under ice to the Universidad de Costa Rica in San José and then stored frozen.

After the crabs were allowed to thaw, eight pleopods of each crab were carefully snipped at the bases, wet weighed, and then placed in seawater. A MS5 Leitz dissecting microscope was used to examine the pleopods for nemerteans, worm sheaths, and worm egg strings. Sheaths without worms were considered in the count for infestation. During holding of the crabs in the containers by fishermen, stressed worms have been observed to leave the egg masses, which have become suboptimal for the nemerteans (J. Norenburg, pers. comm.). A total of 824 pleopods were analyzed.

To quantify the worm dispersion and infestation on host crabs, prevalence and intensity were measured. Prevalence, an indicator of infestation, was defined as numbers of infected host crabs per total host crabs × 100. Intensity, indicator of dispersion amongst infected host crabs, was defined as mean number of worms per infected host crab.

Results

Golfo de Nicoya

A total of 26 egg masses out of 74 crabs were found to be infested with worms (Fig. 1A) for a prevalence of 35%. The worm was tentatively identified as belonging to the genus Carcinonemertes with a single stylet (Fig. 1B). Worm length averaged about ~7.0 mm with widths about 0.13 mm.

Figure 1.

A Unidentified Carcinonemertes sp. from an ovigerous female of Callinectes arcuatus collected in Golfo de Nicoya, Pacific coast of Costa Rica. B Single basis and stylet observed in a nemertean from the egg mass of Callinectes arcuatus collected in Golfo de Nicoya, Pacific coast of Costa Rica.

Most worms were found to be inside sheaths (Fig. 2a). The mucous sheaths were linear, of small height (15–25 µm), and dome-shaped with uniformly distributed lapillae (Fig. 2b). Cursory investigation of the gills of the C. arcuatus found no ensheathed nemerteans. Worm egg strings were also observed intertwined around the crab eggs (Fig. 3).

Figure 2.

A Nemertean worm emerging from the mucous sheath, observed in the egg mass of Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica. B Mucous sheath of a nemertean worm showing pronounced domed lapillae, observed in the egg mass of Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica.

Figure 3.

Nemertean worm egg strings (encircled) amongst eggs of Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica.

Worms were found throughout the egg mass, but more often encountered at the base of pleopods. The pleopodal base of one crab showed pronounced egg mortalities (Fig. 4A) and an accumulation of worms in the mid pleopodal regions (Fig. 4B).

Figure 4.

A Severe crab egg mortalities (encircled) at lateral base of a pleopod from an ovigerous female Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica. B Nemertean worms (encircled) between the lateral middle and lateral base of a pleopod from an ovigerous female of Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica.

Mean intensity (# worms/infested crab) was 18 (range 1–123 worms). Linear regression analysis showed no significance (r2 = 0.12; correlation coefficient 0.35; P = 0.09) between crab size (carapace width) and worm intensity (Fig. 5).

Figure 5.

Linear regression analysis between size (carapace width) of ovigerous females of Callinectes arcuatus, Golfo de Nicoya, Pacific Costa Rica, and nemertean worm intensity.

Golfo Dulce and Herradura/Jaco

No worm infestations were found on crabs collected from Golfo Dulce and from off the coast of Herradura/Jaco.

Discussion

This survey is the first report of a carcinonemertid crab egg predator on the portunid Callinectes arcuatus from Golfo de Nicoya in the Pacific coast of Costa Rica, and as far as we know, also the first published report from the Pacific coast of Central America. The observation of a single stylet near the brain is a characteristic of the genus Carcinonemertes. Further histological analysis will be needed to confirm the presence of the Takakura’s duct system (Humes 1942). In male Carcinonemertes, this duct system includes the vas efferens, vas deferens, seminal vesicle and gonoduct (Shields and Kuris 1990).

Nemerteans have been previously reported on the rafting crab, Plagusia immaculata Lamarck, 1818, from Pacific Panamanian coast (M. Torchin, unpubl.) and on unidentified crabs from Bocas del Toro, Caribbean coast of Panama (Collin et al. 2005). From unpublished 2004 survey of Panamanian crabs from the Caribbean coast (C. Santos, pers. comm.) carcinonemertids have been reported on Leptodius floridanus (Gibbes, 1850), Macrocoeloma trispinosum (Latreille, 1825), Mithraculus cinctimanus (Stimpson, 1860), Mithraculus forceps (A. Milne-Edwards, 1875), Mithrax caribbaeus (M. J. Rathbun, 1900, Mithrax spinosissimus (Lamarck, 1818), Panopeus lacustris Desbonne, 1867 and Pilumnus pannosus M. J. Rathbun, 1896.

This study found a 35% prevalence of this carcinonemertid on Callinectes arcuatus from the population from Golfo de Nicoya and none from Golfo Dulce. Wickham (1979) reported 100% prevalence for Carcinonemertes errans on Dungeness crab, Cancer magister (Dana, 1852) while Shields et al. (1990) found >97% prevalence on the yellow rock crab, Cancer anthonyi (M. J. Rathbun, 1897). Golfo de Nicoya is considered one of the most productive estuaries in the world (Cordoba-Muñoz 1998; Gocke et al. 2001), and is also the most important fishery area in Costa Rica (Cortés and Wehrtmann 2009). The Golfo de Nicoya is highly impacted by human activities and one of the most polluted regions along the Pacific coast of Costa Rica (Vargas 1995). These conditions may enhance the prevalence and transmission of these nemertean crab egg predators. In contrast, Golfo Dulce is a deep tropical, highly stratified and low-productivity fjord (Quesada-Alpízar and Cortés 2006). Especially the limited water circulation in this tropical fjord may restrict dispersion and transmission of nemerteans. Kuris et al. (1991) reported that infestation of nemerteans on the red king crab was highly variable; high egg mortalities were observed in geographically clustered crab populations.

The carcinonemertid encountered in our study may be host-specific to C. arcuatus and have not exploited other crab hosts, such as Portunus asper from offshore of Herradura and Jaco. Further investigations are needed to determine the extent of nemertean prevalence on other potential host crabs.

In this study, the estimated infestation of 18 is low compared to 46,000 reported for Carcinonemertes errans Wickham, 1978 on Cancer magister by Wickham (1979) and 692 (86.5 worms/pleopod × 8) for Cancer anthonyi (Shields et al. 1990). This low intensity may be a reflection of several factors. Firstly, this symbiotic relationship between the worm and Callinectes arcuatus may have evolved most recently. Secondly, the artisan fishery inclusion of small-sized crabs, as well as both males and females, might contribute to the low reproduction of worms, which need ovigerous crabs to complete their reproductive cycle. Therefore, the lower intensities observed in C. arcuatus and C. anthonyi compared to C. magister could be due to the fact that both female and male crabs are taken out in the C. arcuatus and C. anthonyi fisheries.

Although in this preliminary study, worm incidence was low for Callinectes arcuatus from the Golfo de Nicoya, future monitoring of the carcinonemertid is strongly recommended. Collapse of this growing artisan fishery could potentially occur if worm population were somehow to explode, especially in these times of unstable climatic change. In 1981, the red king crab fishery recorded the third highest historical yield; however three years later, the fishery suffered the lowest catch in its 30 year history (Kuris et al. 1991). High red king crab egg mortality was correlated with high-intensity infestations of nemerteans in the egg mass (Kuris et al. 1991).

In the present study, the worms and their sheaths were observed in the medial middle and base areas of the pleopod. Pleopods of one crab sample showed very high egg moralities in these regions (refer to Fig. 4A, B). These findings are in agreement with similar observations from other crabs. Higher worm presence and abundance as well as egg mortalities in these pleopodal areas were also reported for Cancer anthonyi (Shields et al. 1990) and for Cancer magister (Okazaki and Kuris 2004).

Most spawning of C. arcuatus occurs during the dry season from December to April, when ovigerous females migrate from the low salinity areas of the inner gulf to the high salinity waters in the outer gulf where the larvae hatch (DeVries et al. 1983). Larval development is completed within 70 days (Paul 1982; Dittel and Epifano 1984). Further studies are suggested to determine whether nemerteans complete their life cycle on one brood of host eggs or remain on the crab for a subsequent brood to complete another reproductive cycle. After host eclosion, carcinonemertids on portunid crabs encyst between the branchial lamellae and then lie dormant until the female crab oviposits (Humes 1942; Shields and Kuris 1990). In this study examination of branchial chambers of female crabs did not reveal encysted worms but barnacles from the genus Octolasmis (unpubl observations).

In this study, frozen crab samples were analyzed due to the logistics and limitations of receiving ovigerous crabs from fishermen. Worms have been observed to leave the crab egg mass when the crabs are out of the water (J. Norenburg, pers. comm.). Future studies using freshly trapped ovigerous crabs are suggested to improve infestation and incidence numbers. Also live nemerteans would allow for further histological and DNA analyses for phylogenetic relationships with other Carcinonemertes species.

Acknowledgements

Research funding was provided by Research, Scholarship & Professional Growth Committee, Department of Zoology & College of Science of Weber State University (WSU). Logistical support came from the Unidad de Investigación Pesquera y Acuicultura (UNIP) of the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) of Universidad de Costa Rica (UCR). We would like to thank Edgar Villegas, Raquel Romero, Fresia Villalobos, Vanessa Nielsen, Professors Gustavo Gutiérrez and Adarli Romero (UCR) as well as Bailey Eames (WSU) for their technical assistance. We thank Patricia Sadeghian from the Santa Barbara Museum of Natural History for her helpful interpretation of the lapillae found on the worm sheaths. We appreciate the technical comments from two anonymous reviewers who added constructive criticisms to greatly improve the manuscript.

References

  • Castro KM, De Alteris JT (1989) Development of a swimming crab fishery in Ecuador. In: Pollnack RB, Morrisey MT (Eds) Aspects of a small-scale fishery development. International Center for Marine Resource Development (ICMRD) Kingston.
  • Collin R, Diaz MC, Norenburg J, Rocha RM, Sanchez JA, Schulz A, Schwartz ML, Valdes A (2005) Photographic identification guide to some common marine invertebrates of Bocas Del Toro, Panama. Caribbean Journal of Science 41: 638–707.
  • Córdoba-Muñoz R (1998) Primary productivity in the water column of Estero Morales, a mangrove system in the Gulf of Nicoya, Costa Rica. Revista de Biología Tropical 46 (Suppl 6): 257–262.
  • Cortes J, Wehrtmann IS (2009) Chapter I. Diversity of Marine Habitats of the Caribbean and Pacific of Costa Rica. In: Wehrtmann IS, Cortés J (Eds) Marine Biodiversity of Costa Rica, Central America. Springer + Business Media B. V., 1–45.
  • DeVries MC, Epifanio CE, Dittel AI (1983) Reproductive periodicity of the tropical crab Callinectes arcuatus Ordway in Central America. Estuarine, Coastal and Shelf Science 17: 709–716. doi: 10.1016/0272-7714(83)90036-7
  • Dittel AI (1993) Cambios en los hábitos de Callinectes arcuatus (Crustacea: Decapoda) en el Golfo de Nicoya. Revista de Biología Tropical 41: 639–646.
  • Dittel AI, Epifanio CE (1984) Growth and development of the portunid crab Callinectes arcuatus Ordway: Zoeae, megalopae and juveniles. Journal of Crustacean Biology 4: 491–494. doi: 10.2307/1548044
  • Fischer S, Wolff, M (2006) Fisheries assessment of Callinectes arcuatus (Brachyura, Portunidae) in the Gulf of Nicoya, Costa Rica. Fisheries Research 77: 301–311. doi: 10.1016/j.fishres.2005.11.009
  • Gocke K, Cortés J, Murillo M (2001) The annual cycle of primary production in a tropical estuary: the inner regions of the Golfo de Nicoya, Costa Rica. Revista de Biología Tropical 49 (Suppl 2): 289–306.
  • Humes AG (1942) The morphology, taxonomy, bionomics of the nemertean genus Carcinonemertes. Illinois Biological Monograph 18: 1–105.
  • Kajihara H, Chernyshev AV, Sun S, Sundberg P, Crandall FB (2008) Checklist of nemertean genera and species published between 1995 and 2007. Species Diversity 13: 245–274.
  • Kuris AM (1993) Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories. Hydrobiologia 266: 1–14. doi: 10.1007/BF00013355
  • Kuris AM, Wickham DE (1987) Effect of nemertean egg predators on crustaceans. Bulletin of Marine Science 41: 151–164.
  • Kuris AM, Blau SF, Paul AJ, Shields JD, Wickham DE (1991) Infestation by brood symbionts and their impact on egg mortality in the red king crab, Paralithodes camtschatica in Alaska: Geographic and temporal variation. Canadian Journal of Fisheries and Aquatic Sciences 48: 559–568. doi: 10.1139/f91-071
  • McDermott JJ (2006) Nemerteans as hosts for symbionts: a review. Journal of Natural History 40: 1007–1020. doi: 10.1080/00222930600834121
  • Okazaki RK, Kuris AM (2004) Effect of nemertean on crab egg mortality in the Dungeness crab, Cancer magister. 3rd Brazilian Crustacean Congress and The Crustacean Society Meeting. Florianópolis, SC Brazil (Abstract).
  • Paul RKG (1982) Abundance, breeding and growth of Callinectes arcuatus Ordway and Callinectes toxotes Ordway (Decapoda, Brachyura, Portunidae) in a lagoon system on the Mexican Pacific coast. Estuarine Coastal and Shelf Science 14: 13–26. doi: 10.1016/S0302-3524(82)80064-9
  • Quesada-Alpízar MA, Cortés J (2006) Los ecosistemas marinos del Pacífico sur de Costa Rica: estado del conocimiento y perspectivas del manejo. Revista de Biología Tropical 54 (Suppl 1): 101–145.
  • Sadeghian PS, Santos C (2010) Two new species of Carcinonemertes (Hoplonemertea: Carcinonemertidae) living in association with leucosiid crabs from California and Tasmania. Journal of Natural History 44: 2395–2409. doi: 10.1080/00222933.2010.505014
  • Shields JD, Okazaki RK, Kuris, AM (1990) Brood mortality and egg predation by the nemertean Carcinonemertes epialti, on the yellow rock crab, Cancer anthonyi in southern California. Canadian Journal of Fisheries and Aquatic Sciences 47: 1275–1281. doi: 10.1139/f90-146
  • Shields JD, Kuris AM (1990) Carcinonemertes wickhami n. sp. (Nemertea), a symbiotic egg predator from the spiny lobster Panulirus interruptus in southern California, with remarks on symbiont-host adaptations. Fishery Bulletin 88: 279–287.
  • Vargas JA (1995) The Gulf of Nicoya estuary: past, present and future cooperative research. Helgoländer Meeresuntersuchungen 49: 821–828. doi: 10.1007/BF02368405
  • Wickham DE (1979) Carcinonemertes errans and fouling in the eggs of the Dungeness crab. Journal of Fishery Research Board Canada 36: 1319–1324. doi: 10.1139/f79-190
  • Wickham DE, Kuris AM (1985) The comparative ecology of nemertean egg predators. American Zoologist 25: 127–134.
  • Wickham DE, Kuris AM (1988) Diversity among nemertean egg predators of decapod crustaceans. Hydrobiologia 156: 23–30. doi: 10.1007/BF00027974