Prevalences of Parasitized and Hyperparasitized Crabs Near South Georgia
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MARINE ECOLOGY PROGRESS SERIES hblished September 3 Mar Ecol Prog Ser Prevalences of parasitized and hyperparasitized crabs near South Georgia George Watters* U.S. AMLR Program, NOAA Fisheries, PO Box 271, San Diego, California 92038, USA ABSTRACT: This study identifies sources of variation in the prevalences of parasitized and hyperpara- sitized Paralomis spinosissima, a lithodid found around South Georgia. The parasite is Briarosaccus cal- losus, a rhizocephalan; the hyperparasite is an undescribed linopsinine. Generalized additive models were used to model data collected dunng 1992 and 1995. Parasites were less prevalent on female crabs and most prevalent in submarine canyons The former effect may be due to sex-specific differences in gill cleaning behavior, and the latter effect may result from reduced gill cleaning efficiency in areas where the seafloor is covered with fine sediment. The size-prevalence curve was dome-shaped: this probably indicates that B. callosus reduces the growth rate and increases the mortality rate of P spin- osissima. Parasite prevalence decreased with increasing crab density but increased with increasing parasitized crab density. These results suggest that parasitized crabs do not aggregate with unpara- sitized males. Habitat was a significant source of variation in hyperparasite prevalence during 1992 but not 1995. Between-year comparisons of parasite and hyperparasite prevalences were equivocal and failed to provide convincing evidence against parameter statlonanty and stability in the P. spinosis- sima-B. callosus-liriopsinine system KEY WORDS: Lithodid crabs . Rhizocephalan barnacles . Cryptoniscid isopods . Parasitism . Hyper- parasitism - Prevalence . Generalized additive models INTRODUCTION isopods generally have rhizocephalan hosts (Caullery 1908, Nielsen & Stromberg 1973). Paralomis spinosissima is a lithodid crab that has Parasitized and hyperparasitized Paralomis spinosis- recently been targeted by an exploratory fishery oper- sima are easy to identify. A parasitized crab is recog- ating off the south Atlantic island of South Georgia. P. nizable when at least one externa (this is the rhizo- spinosissima is frequently parasitized by the rhizo- cephalan's reproductive structure) has emerged cephalan Briarosaccus callosus, and many of the rhizo- through the ventral abdominal cuticle. This method of cephalans are, in turn, hosts for an hyperparasitic iso- identification may underestimate the true prevalence pod (Otto & MacIntosh 1996). The hyperparasite is rate because there is a lag between the times of initial currently undescribed, but lt is believed to be from the infection and emergence of the externa. A hyperpara- family Cryptoniscidae (Otto & MacIntosh 1996). Cryp- sitized crab is recognizable when at least one bulbous, toniscids comprise 7 subfamilies that can, in part, be sac-like structure (this is a female hyperparasite) has separated on the basis of host specificity (Nielsen & attached to the external surface of the rhizocephalan's Stromberg 1973). The hyperparasite of B. callosus is externa. probably from the subfamily Liriopsinae since these Histological sections of parasitized crabs have shown that an individual Briarosaccus callosus can sterilize its crab host (Sparks & Morado 1986), and 'Present address: Inter-Amencan Tropical Tuna Commission, histological sections of hyperparasitized rhizocepha- 8604 La Jolla Shores Drive, La Jolla, California 92037, USA. lans have shown that an individual liriopsinine can E-mail: [email protected] also sterilize its parasite host (Caullery 1908). These O Inter-Research 1998 Resale of full article not permitted 216 Mar Ecol Prog Ser 170: 215-229, 1998 facts are important because they imply that the popu- Liriopsinae have been found on at least 3 lithodids lation-level consequences of parasitism and hyperpar- that are known to be parasitized by Briarosaccus cal- asitism in the Paralomis spinosissima-B. callosus-liri- losus: Paralomis bouvieri (Pohle 1992a), Neolithodes opsinine system can be studied by considering grimaldii (Pohle 1992b), and Paralomis spinosissima prevalence rates rather than infection intensities (i.e. (Otto & Macintosh 1996). These 3 accounts contain parasite and hyperparasite burdens). There are in- few data on the prevalence of hyperparasitized crabs, stances of multiple parasitism and hyperparasitism and there is no information about which variables around South Georgia, but it is questionable whether contribute to variation in hyperparasite prevalence. these instances have a substantial impact on the sys- The literature does, however, contain information on. tem's dynamics. This view is supported by the work of vanation in the prevalences of hosts parasitized by Kuris (1974). Kuris noted that multiple infections by isopods from another subfamily in the Cryptonisci- parasitic castrators and hypercastrators like rhizo- dae, the Cabiropsinae. Cabiropsinae parasitize iso- cephalans and Liriopsinae do not usually have addi- pods (Nielsen & Strijmberg 1973); some Cabiropsinae tive pathogenic effects on individual hosts. The out- are parasites, others are hyperparasites. Nielsen & come from a single act of parasitic castration (or Stromberg (1965) studied a parasitic cabiropsinine. hypercastration) has the same population-level conse- They found that cabiropsinine prevalence varied with quence (i.e. the 'reproductive death' of one host) as host sex, host maturity state, host size, and month. the outcome from an instance of multiple parasitic Nielsen & Stromberg also noted that there may be castration (or hypercastration). geographical differences in cabiropsinine prevalence. In the case of Briarosaccus callosus, a second argu- Sassaman (1985) and Owens (1993) studied hyperpar- ment can be made for considering parasite prevalence asitic Cabiropsinae. The hyperparasitic Cabiropsinae rather than intensity of infection. The size of an externa are typically hosted by bopyrid isopods (bopyrids par- is positively correlated with the host crab's carapace asitize many marine crustaceans, and the family length, but the average size of externae involved in Bopyridae is closely related to the Cryptoniscidae). multiple infections is smaller than the average size of Sassaman observed that cabiropsinine prevalence externae from single infections (Bower & Sloan 1985). varied with changes in bopyrid abundance. Owens Under the reasonable assumption that the fecundity of observed that cabiropsinine prevalence varied with B, callosus is positively correlated with externa size, season, geographical area, bopyrid size, the bopyrid the findings of Bower & Sloan (1985) suggest that the host's size (in this case the bopyrids parasitized total fecundity of a population of B. callosus is limited various species of prawns), and the bopyrid's host more by numbers and sizes of parasitized crabs than species. by numbers of parasite externae. The objective of this study is to develop an appropri- Briarosaccus callosus parasitizes at least 12 species ate context for the construction of a mathematical host- of lithodid crabs (Boschma 1962, Hoggarth 1990, Pohle parasite-hyperparasite model that describes the Par- 1992a, Hseg 1995), and the prevalence of this rhizo- alomis spinosissima-Briarosaccus callosus-liriopsinine cephalan varies both between and w~thinits host spe- system (this mathematical model is presented in G. cies. Between hosts, prevalence rates can vary from Watters & R. Deriso unpubl.). This context develop- less than 1 % (e.g. Paralomis granulosa from the Falk- ment includes consideration of whether the P. spinosis- land Islands in Hoggarth 1990) to more than 75 % (e.g. sima-B. callosus-liriopsinine system is governed by Paralithodes platypus from Glacier Bay, Alaska in stationary (temporally invariant) population dynamics Hawkes et al. 198613).A number of variables contribute parameters and whether the system is stable. These 2 to within-species variation in B. callosus prevalence. topics are addressed by a sequence of comparisons in These variables include the sex and size of an individ- which statistical models of parasite and hyperparasite ual host (e.g. Sloan 1984, Hawkes et al. 1985c, 198613, prevalence rates are initially constructed from one set Hoggarth 1990, Abello & Macpherson 1992) as well as of data and then compared to data that were collected the habitat from which an individual crab was cap- 3 yr later. Checks for stationarity and stability have not tured (e.g. Sloan 1984, Hawkes et al. 1986a, b). Differ- been made in previous studies of lithodid-B. callosus ences in local densities of unparasitized and para- relationships. sitized crabs may also contribute to within-host variation in paraslte prevalence. For example, Sloan (1984) observed prevalence rates between about 3 and MATERIALS AND METHODS 44'26 on Lithodes aequispina at locations where catches per unit of effort (catch rates are proxy esti- Data sources. Two data sets were used to study vari- mates of local crab density) varied between about 3 ation in the prevalence of parasitized and hyperpara- and 24 crabs caught per trap fished. sitized Paralomis spinosissima; one data set was col- Watters: Prevalences of parasitized and hyperparasitized crabs lected in 1992, and the other was collected in 1995. Otto & Macintosh (1996) made biologi- cal observations on a large sample of P. spin- osissima; a subset of their observations com- prised the '1992 data'. The 1992 data included records of the sex, size (carapace length in mm), and parasitism and hyperparasitism