Host specificity of adult versus larval cestodes of the elasmobranch tapeworm order Trypanorhyncha

https://doi.org/10.1016/j.ijpara.2007.08.011Get rights and content

Abstract

Host specificity between the adult and final larval stages (plerocercus, plerocercoid, or merocercoid) of a diversity of trypanorhynch species was compared using the host specificity index (HSs). Index values were generated for a total of 63 species representing all five trypanorhynch superfamilies and 11 families. Host specificity of both adults and final larvae was found to be widely variable among species, ranging from very high (oioxenous) to very low (euryxenous) for both stages. However, in general, host specificity was highest for the adult stage in the definitive host (mean HSs = 3.86) and lowest for the final larval stage in the second intermediate host (mean HSs = 6.29). This difference was found to be significant using the Wilcoxon signed-rank test. Limited data available for procercoids in the first intermediate host suggest that this stage exhibits a degree of specificity intermediate between that of the former two stages (mean HSs = 4.23). No taxonomic trend was seen. Species with a plerocercoid final larval stage (mean HSs = 8.62) were significantly less host-specific than those with plerocerci or merocercoids (mean HSs = 5.56). This result may reflect the use of paratenic hosts by species possessing the relatively more resilient plerocercoid as their final larval stage. These results provide an example of how HSs can be used to compare levels of host specificity, in this instance, among stages of polyxenous life cycles. They also emphasise the importance of articulating the life cycle stage under consideration when general statements are made about host specificity.

Introduction

Many groups of parasites are polyxenous, utilising two or more hosts over the course of their development. A question of interest in such organisms is the relative degree of host specificity exhibited by the different life cycle stages of a species. The issue of whether general trends exist in the relative degrees of host specificity of different life cycle stages is one of the more intriguing aspects of the biology of polyxenous organisms. For example, Poulin (2007) noted that it has been predicted that parasites with complex life cycles should display a higher specificity for their intermediate host than for their definitive host. Specific examples of this trend are known. For example, the sporocysts and redia of Schistosoma japonicum exhibit a greater degree of host specificity for their molluscan first intermediate host, than the adult does for its definitive host (e.g. Kennedy, 1975). In contrast, in other taxa it is the adult stage that has been shown to be more host-specific. For example, whereas the adult of the bothriocephalidean cestode Triaenophorus nodulosus parasitises only fish of the genus Esox, the procercoid of this species has the ability to parasitise a wide variety of copepods (Kuperman, 1981). Similarly, Esch and Fernández (1993) found that metacercariae of the digenean Clinostomum campanulatum exhibit much less specificity for the intermediate and/or paratenic fish host than the adult does for the bird definitive host. It could also be argued that transmission mode may play a role in determining the degree of host specificity of a particular life cycle stage.

However, the issue of relative specificity among the life cycle stages of polyxenous species remains largely untested (see Poulin, 2007). This is due, in part, to a lack of data. In many instances comprehensive host data are not available for one or more of the life cycle stages under consideration either as a result of lack of sampling effort, inaccessibility of existing data or, more commonly, because larval stages cannot be reliably identified to species. Another contributing factor has been the lack of an objective method for the rigorous quantitative assessment of the degree of host specificity from a phylogenetic perspective. The latter circumstance has recently substantially improved with the development of several indices (Caira et al., 2003, Poulin and Mouillot, 2003, Poulin and Mouillot, 2005) of host specificity designed to allow host taxonomy to be incorporated into specificity assessments. As a consequence, it is now possible to quantitatively address questions of relative host specificity.

Trypanorhynch cestodes are a group of polyxenous parasites that are particularly appropriate for such investigation. Their life cycle stages typically consist of a procercoid, followed by a plerocercus (or in some species a plerocercoid or merocercoid) and ultimately the adult. An individual trypanorhynch passes through at least three different hosts over the course of its life (Dollfus, 1942; Mattis, 1986. Development of two tetrarhynchidean cestodes from the northern Gulf of Mexico. Ph.D. Thesis, University Southern Mississippi). The taxonomy of trypanorhynchs relies heavily on tentacle armature (Campbell and Beveridge, 1994), a feature present in both the adult and the final larval stage of these tapeworms, and thus the final larval stage can be identified reliably to species. Perhaps most importantly, however, comprehensive host data for trypanorhynchs have recently been made available by Palm (2004) who compiled approximately 4000 host/parasite records for larval and adult trypanorhynchs. Although trypanorhynchs are generally considered to exhibit relatively low host specificity at any particular life stage (e.g., Palm et al., 1997, Palm et al., 2007, Beveridge et al., 2000, Palm, 2004, Palm and Klimpel, 2007), detailed studies on particular species have suggested otherwise (e.g., Beveridge and Jones, 2000, Beveridge and Duffy, 2005). However, apart from a statement by Dollfus (1942) that it is rare for a trypanorhynch to parasitise only a single host species in each of its three life cycle stages (most have multiple hosts in all three life cycle stages), little attention has been paid to the relative host specificities of the adult versus larval stages in this order of parasites.

The primary goal of this paper is to evaluate the relative host specificities of the adult and final larval stage (i.e., plerocercus, plerocercoid or merocercoid) of a diversity of trypanorhynchs to determine if a general specificity trend exists within the polyxenous life cycle pattern exhibited by this group. As a secondary goal we hope to illustrate how host specificity indices, such as HSs, can be used to add rigor to assessments of a wide spectrum of questions about relative host specificity, even beyond life cycle stages, as such qualitative indices allow statistical tests to be employed to address specific questions. For example, while this index has been applied to a diversity of species in some groups of cestodes that parasitise elasmobranchs (see Caira et al., 2003), it has never been applied to trypanorhychs. Similarly, although Palm (2004) predicted that certain trypanorhynch taxa, such as tentaculariids, are generally less host-specific than the eutetrarhynchids, this hypothesis remains untested. The final goal of this paper is to focus attention on the fact that in polyxenous species, different life cycle stages may exhibit widely divergent degrees of host specificity and thus general statements about the host specificity of groups should include articulation of the life cycle stage under consideration (e.g. Polyanskii, 1955, Holmes, 1990, Marcogliese, 1995). Our hope is that this will help to elucidate the potential of different life cycle stages to contribute to the exploration and exploitation of new hosts and habitats, and thus, ultimately, their contribution to the evolutionary trajectories of species.

Section snippets

Materials and methods

In general, host association data for the 63 trypanorhynch species included here were taken from Palm (2004). However, in the cases of three species, additional data beyond Palm (2004) were available and were included. These species are Callitetrarhynchus speciosus (Palm, personal observations), Pintneriella musculicola (Palm, personal observations), and Mixonybelinia beveridgei (see Knoff et al., 2004). Only those species for which comprehensive host data were available for both the adult and

Results

Adult and final larval stage host data were obtained for 63 species exemplifying all five superfamilies of trypanorhynchs (sensu Palm, 2004). These consisted of eight species of Eutetrarhynchoidea representing two of the four known families, six species of Gymnorhynchoidea representing all four families, 29 species of Lacistorhynchoidea representing both families in the superfamily and both subfamilies of Lacistorhynchidae (Grillotiinae and Lacistorhynchinae), five species of Otobothrioidea

Discussion

Our results suggest that, in general, the final larval stage (plerocercoid, plerocercus or merocercoid) of trypanorhynchs is significantly less host-specific than the adult stage. In only a very few cases were adults found to be less host-specific than their final larval counterparts, and in only a single case (Gymnorhynchus gigas) was the adult stage found to be conspicuously less host-specific than its corresponding larval stage. In most cases, the degree of host specificity exhibited by the

Acknowledgements

We thank Kent Holsinger for his assistance with the Wilcoxon signed-rank tests and Claire Healy and Tom Mattis for helpful comments on an earlier version of this manuscript. Financial support was provided by the German Research Council (DFG PA 664/4-1) (HWP) and the National Science Foundation (DEB 011882) (JNC).

References (31)

  • H.W. Palm et al.

    Evolution of the parasitic life in the ocean

    Trends Parasitol.

    (2007)
  • J.G. Baer

    Ecology of Animal Parasites

    (1951)
  • I. Beveridge et al.

    Prochristianella spinulfera n. sp. (Cestoda: Trypanorhyncha) from Australian dasyatid and rhinobatid rays

    Syst. Parasitol.

    (2000)
  • I. Beveridge et al.

    Redescription of Cetorhinicola acanthocapax Beveridge & Campbell, 1988 (Cestoda: Trypanorhyncha) from the basking shark Cetorhinus maximus (Gunnerus)

    Syst. Parasitol.

    (2005)
  • I. Beveridge et al.

    New records of the cestode genus Pseudotobothrium (Trypanorhyncha: Otobothriidae) from Australian fishes

    Trans. Roy. Soc. S. Aust.

    (2000)
  • J.N. Caira et al.

    Grillotia similis (Linton, 1908) comb. n. (Cestoda: Trypanorhyncha) from nurse sharks in the Florida keys

    J. Helminthol. Soc. Wash.

    (1990)
  • J.N. Caira et al.

    On a new index of host specificity

  • R.A. Campbell et al.

    Order Trypanorhyncha Diesing, 1863

  • P.R. Cislo et al.

    The parasite assemblage in the spiral intestine of the shark Mustelus canis

    J. Parasitol.

    (1993)
  • R.P. Dollfus

    Études critiques sur les Tétrarhynques du Museum de Paris

    Arch. Mus. Nat. Hist. Nat.

    (1942)
  • GW. Esch et al.

    A Functional Biology of Parasitism

    (1993)
  • M.M. Friggens et al.

    Niche partitioning in the cestode communities of two elasmobranchs

    Oikos

    (2005)
  • J.C. Holmes

    Helminth communities in marine fishes

  • E. Jakob et al.

    Parasites of commercially important fish species from the southern Java coast, Indonesia, including the distribution pattern of trypanorhynch cestodes

    Verhandl. Ges. Ichthyol.

    (2006)
  • C.R. Kennedy

    Ecological Animal Parasitology

    (1975)
  • Cited by (0)

    View full text