Skip to main content
SpringerLink
Log in

Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms

  • Community Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Tetraphyllidean cestodes are cosmopolitan, remarkably host specific, and form the most speciose and diverse group of helminths infecting elasmobranchs (sharks, skates and rays). They show substantial interspecific variation in a variety of morphological traits, including body size. Tetraphyllideans represent therefore, an ideal group in which to examine the relationship between parasite body size and abundance. The individual and combined effects of host size, environmental temperature, host habitat, host environment, host physiology, and host type (all likely correlates of parasite body size) on parasite length were assessed using general linear model analyses using data from 515 tetraphyllidean cestode species (182 species were included in analyses). The relationships between tetraphyllidean cestode length and intensity and abundance of infection were assessed using simple linear regression analyses. Due to the contrasting morphologies between shark and batoid hosts, and contrasting physiologies between sharks of the Lamnidae family and other sharks, analyses were repeated in different subsets based on host morphology and physiologies (“sharks” vs. batoids) to determine the influence of these variables on adult tetraphyllidean tapeworm body size. Results presented herein indicate that host body size, environmental temperature and host habitat are relatively important variables in models explaining interspecific variations in tetraphyllidean tapeworm length. In addition, a negative relationship between tetraphyllidean body size and intensity of infection was apparent. These results suggest that space constraints and ambient temperature, via their effects on metabolism and growth, determine adult tetraphyllidean cestode size. Consequently, a trade-off between size and numbers is possibly imposed by external forces influencing host size, hence limiting physical space or other resources available to the parasites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agusti C, Aznar FJ, Raga JA (2005a) Tetraphyllidean plerocercoids from western Mediterranean cetaceans and other marine mammals around the world: a comprehensive morphological analysis. J Parasitol. doi:10.1645/GE-372R

  • Agusti C, Aznar FJ, Olson PD, Littlewood DTJ, Kostadinova A, Raga JA (2005b) Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dolphins (Stenella coeruleoalba) from the west Mediterranean. Parasitology. doi:10.1017/S0031182004006754

  • Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York

    Book  Google Scholar 

  • Arneberg P, Skorping A, Read AF (1998) Parasite abundance, body size, life histories, and the energetic equivalence rule. Am Nat. doi: 10.1086/286136

  • Bernal D, Donley JM, Shadwick RE, Syme DA (2005) Mamma-like muscle powered swimming in a cold-water shark. Nature. doi: 10.1038/nature04007

  • Blackburn TM, Gaston KJ (1997) A critical assessment of the form of the interspecific relationship between abundance and body size in animals. J Anim Ecol 66:233–249

    Article  Google Scholar 

  • Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib. doi:10.1046/j.1472-4642.1999.00046.x

  • Brickle P, Olson PD, Littlewood DTJ, Bishop A, Arkhipkin AI (2001) Parasites of Loligo gahi, with a phylogenetically based identification of their cestode larvae. Can J Zool. doi:10.1139/cjz-79-12-2289

  • Brown JH (2005) Macroecology. University of Chicago Press, Chicago

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Bush AO, Lotz JM (2000) The ecology of “crowding”. J Parasitol. doi:10.1645/0022-3395(2000)086[0212:TEOC]2.0.CO;2

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Caira JN, Jensen K (2001) An investigation of the co-evolutionary relationships between onchobothriid tapeworms and their elasmobranch hosts. Int J Parasitol. doi:10.1016/S0020-7519(01)00206-5

  • Caira JN, Reyda F (2005) Eucestoda (true tapeworms). In: Rohde K (ed) Marine parasitology. CSIRO, Collingwood, pp 92–104

    Google Scholar 

  • Caira JN, Healy CJ (2008) Order Tetraphyllidea Carus, 1863. In: Caira JN, Jensen K, Healy CJ (eds) The global cestode database (online). www.cestodedatabase.org. Accessed April 2008

  • Caira JN, Jensen K, Healy CJ (2001) Interrelationships among tetraphyllidean and lecanicephalidean cestodes. In: Littlewood T, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 135–158

    Google Scholar 

  • Carbone C, Rowcliffe JM, Cowlishaw G, Isaac NJB (2007) The scaling of abundance in consumers and their resources: implications for the energy equivalence rule. Am Nat. doi:10.1086/519858

  • Carey FG, Teal JM (1969) Mako and porbeagle: warm-bodied sharks. Comp Biochem Physiol 28:199–204

    Article  CAS  PubMed  Google Scholar 

  • Compagno LJV (1999) Systematics and body forms. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. John Hopkins University Press, Baltimore, pp 1–42

    Google Scholar 

  • Compagno LJV, Dando M, Fowler S (2005) Sharks of the world. Princeton University Press, Princeton

    Google Scholar 

  • Damuth J (1981) Population density and body size in mammals. Nature. doi:10.1038/290699a0

  • Damuth J (1987) Interspecific allometry of population density in mammals and other animals: the independence of body mass and population energy-use. Biol J Linn Soc. doi:10.1111/j.1095-8312.1987.tb01990.x

  • Enquist BJ, Brown JH, West GB (1998) Allometric scaling of plant energetics and population density. Nature. doi:10.1038/25977

  • Friggens MM, Brown JH (2005) Niche partitioning in the cestode communities of two elasmobranchs. Oikos. doi:10.1111/j.0030-1299.2005.13275.x

  • Froese R, Pauly D (eds) (2008) Fishbase. World Wide Web electronic publication. www.fishbase.org. version (04/2008)

  • George-Nascimento M, Munoz G, Marquet PA, Poulin R (2004) Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecol Lett. doi:10.1111/j.1461-0248.2004.00609.x

  • Hausdorf B (2007) The interspecific relationship between abundance and body size in central European land snail assemblages. Basic Appl Ecol. doi:10.1016/j.baae.2006.03.005

  • Heins DC, Baker JA, Martin HC (2002) The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. J Parasitol. doi:10.1645/0022-3395(2002)088[0302:TCEITC]2.0.CO;2

  • Holmgren S, Nilsson S (1999) Digestive system. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. John Hopkins University Press, Baltimore, pp 144–173

    Google Scholar 

  • Kohler NE, Casey JG, Turner PA (1998) NMFS cooperative shark tagging program, 1962–93: an atlas of shark tag and recapture data. Mar Fish Rev 60(2):1–87

    Google Scholar 

  • Luque JL, Poulin R (2004) Use of fish as intermediate hosts by metazoan parasites: a comparative analysis. Acta Parasitol 49:353–361

    Google Scholar 

  • Luque JL, Poulin R (2008) Linking ecology with parasite diversity in Neotropical fishes. J Fish Biol. doi:10.1111/j.1095-8649.2007.01695.x

  • May RM (1992) How many species inhabit the Earth? Sci Am 267:42–48

    Article  Google Scholar 

  • Morand S, Legendre P, Gardner SL, Hugot J-P (1996) Body size evolution of oxyurid (Nematoda) parasites: the role of hosts. Oecologia 107:274–282

    Article  Google Scholar 

  • Musick JA, Harbin MM, Compagno LJV (2004) Historical zoogeography of the Selachii. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC, Boca Raton, pp 33–78

    Google Scholar 

  • Pascual S, Resero M, Adrias C, Guerra A (1995) Helminth fauna of the short finned squid Ilex coindetti (Cephalopoda: Ommastrephidae) off NW Spain. Dis Aquat Organ. doi:10.3354/dao023071

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Google Scholar 

  • Poulin R (1995a) Clutch size and egg size in free-living and parasitic copepods: a comparative analysis. Evolution 49:325–336

    Article  Google Scholar 

  • Poulin R (1995b) Evolutionary influences on body size in free-living and parasitic isopods. Biol J Linn Soc. doi:10.1111/j.1095-8312.1995.tb01035.x

  • Poulin R (1996a) The evolution of life history strategies in parasitic animals. Adv Parasitol 37:107–134

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1996b) The evolution of body size in the Monogenea: the role of host size and latitude. Can J Zool 74:726–732

    Article  Google Scholar 

  • Poulin R (1997) Egg production in adult rematodes: adaptation or constraint? Parasitology. doi:10.1017/S0031182096008372

  • Poulin R (1999) Body size vs abundance among parasite species: positive relationships? Ecography. doi:10.1111/j.1600-0587.1999.tb00499.x

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

    Google Scholar 

  • Poulin R, Justine J-L (2008) Linking species abundance distribution and body size in monogenean communities. Parasitol Res. doi:10.1007/s00436-008-0953-0

  • Poulin R, Rohde K (1997) Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny. Oecologia. doi:10.1007/s004420050160

  • Read CP (1951) The “crowding effect” in tapeworm infections. J Parasitol. doi:10.1645/0022-3395(2000)086[0206:TCEITI]2.0.CO;2

  • Roberts LS (2000) The crowding effect revisited. J Parasitol. doi:10.1645/0022-3395(2000)086[0209:TCER]2.0.CO;2

  • Rohde K (2002) Ecology and biogeography of marine parasites. Adv Mar Biol. doi:10.1016/S0065-2881(02)43002-7

  • Rohde K (2005) Latitudinal, longitudinal and depth gradients. In: Rohde K (ed) Marine parasitology. CSIRO, Collingwood, pp 348–351

    Google Scholar 

  • Rohde K, Heap M (1998) Latitudinal differences in species and community richness and in community structure of metazoan ecto- and endoparasites of marine teleost fish. Int J Parasitol. doi:10.1016/S0020-7519(97)00209-9

  • Skorping A, Read AF, Keymer AE (1991) Life history covariation in intestinal nematodes in mammals. Oikos 60:365–372

    Article  Google Scholar 

  • Wilga CD, Motta PJ, Sanford CP (2007) Evolution and ecology of feeding in elasmobranchs. Integr Comp Biol. doi:10.1093/icb/icm029

  • Williams HH, Jones A (1994) Parasitic worms of fish. Taylor and Francis, London

    Google Scholar 

  • Windsor DA (1998) Most of the species on Earth are parasites. Int J Parasitol. doi:10.1016/S0020-7519(98)00153-2

  • Wojciechowska A (1990) Onchobothrium antarcticum sp. n. (Tetraphyllidea) from Bathyraja eatonii (Günther, 1876) and a plerocercoid from Notothenioidea (South Shetlands, Antarctic). Acta Parasitol 35:113–117

    Google Scholar 

  • Wojciechowska A (1993a) The tetraphyllidean and tetrabothiid cercoids from Antarctic bony fishes. I. Morphology. Identification with adult forms. Acta Parasitol 38:15–22

    Google Scholar 

  • Wojciechowska A (1993b) The tetraphyllidean and tetrabothiid cercoids from Antarctic bony fishes. II. Occurrence of cercoids in various fish species. Acta Parasitol 38:113–118

    Google Scholar 

Download references

Acknowledgments

The diligence of two anonymous reviewers is gratefully acknowledged and contributed to improving this manuscript. We thank David R. Anderson for advice regarding our analyses, Tommy Leung for translation of papers from Chinese to English and members of the Evolutionary and Ecological Parasitology Research Group at the University of Otago for useful comments on a previous version of this manuscript. Financial support from the New Brunswick Museum, through the Florence M. Christie Research Fellowship in Zoology to H. S. R., is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand

    Haseeb Sajjad Randhawa & Robert Poulin

Authors
  1. Haseeb Sajjad Randhawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Poulin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haseeb Sajjad Randhawa.

Additional information

Communicated by Carla Caceres.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 207 kb)

Supplementary material 2 (DOC 135 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Randhawa, H.S., Poulin, R. Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms. Oecologia 161, 759–769 (2009). https://doi.org/10.1007/s00442-009-1410-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1410-1

Keywords

Search

Navigation