Abstract
Gregarines are ubiquitous protozoan parasites that infect arthropods worldwide. More than 1,600 gregarine species have been described, but only a small percentage of invertebrates have been surveyed for these apicomplexan parasites. Adult dragonfly populations were surveyed for gregarines at two reservoirs in Texas, USA for 2 years. Gregarine prevalence and intensity were compared intraspecifically between host genders and reservoirs, among wing loads, and through time. Of the 29 dragonfly species collected, 41% hosted gregarines. Nine of these dragonfly species were previously undocumented as hosts. Among the commonly collected hosts, prevalence ranged from 18 to 52%. Parasites were aggregated among hosts and had a median intensity of five parasites per host. Gregarines were found only in hosts exceeding a minimum wing load, indicating that gregarines are likely not transferred from the naiad to adult during emergence. Prevalence and intensity increased during both years, suggesting that gregarine oocyst viability parallels increasing host population densities and may be short-lived. Prevalence and intensity also differed between dragonfly populations at two reservoirs. Regression analyses revealed that host species, host gender, month, and year were significant explanatory variables related to gregarine prevalence and intensity. Abundant information on odonate distributions, diversity, and mating activities makes dragonfly–gregarine systems excellent avenues for ecological, evolutionary, and parasitological research. Our results emphasize the importance of considering season, hosts, and habitat when studying gregarine–dragonfly ecology.
Similar content being viewed by others
References
Abbott JC (2005) Dragonflies and damselflies of Texas and the South-Central United States. Princeton University Press, Princeton
Abramson JH (2004) WINPEPI (PEPI-for-Windows):computer programs for epidemiologists. Epidemiol Perspect Innovat 1:6
Abramson JH (2005) Manual of the module DESCRIBE (version 1.49) of WINPEPI (PEPI-for-Windows). http://www.brixtonhealth.com/pepi4windows.html. Accessed 30 October 2009
Åbro A (1974) The gregarine infection in different species of Odonata from the same habitat. Zool Scripta 3:111–120
Åbro A (1976) The mode of gregarine infection in Zygoptera (Odonata). Zool Scripta 5:265–275
Åbro A (1996) Gregarine infection of adult Calopteryx virgo L. (Odonata: Zygoptera). J Nat Hist 30:855–859
Amano H, Hayashi K, Kasuya E (2008) Avoidance of egg parasitism through submerged oviposition by tandem pairs in the water strider, Aquarius paludum insularis (Heteroptera: Gerridae). Ecol Entomol 33:560–563
Baird MS, Tibbs JE (2005) Statewide freshwater fisheries monitoring and management program: 2004 survey report. Texas Parks & Wildlife and Sport Fish Restoration. http://www.tpwd.state.tx.us/publications/pwdpubs/media/lake_survey/pwd_rp_t3200_1386_2004.pdf. Accessed 3 December 2009
Boisier P, Jambou R, Raharimalala L, Roux J (2002) Relationship between parasite density and fever risk in a community exposed to a low level of malaria transmission in Madagascar Highlands. Am J Trop Med Hyg 67:137–140
Bried JT, Ervin GN (2007) Intraspecific models and spatiotemporal context of size–mass relationships in adult dragonflies. J N Am Bentol Soc 26:681–693
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
Bush AO, Fernandez JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge
Cáceres CE, Hall SR, Duffy MA, Tessier AJ, Helmle C, MacIntyre S (2006) Physical structure of lakes constrains epidemics in Daphnia populations. Ecology 87:1438–1444
Canales-Lazcano J, Contreras-Garduno J, Cordoba-Aguilar A (2005) Fitness-related attributes and gregarine burden in a non-territorial damselfly Enallagma praevarum Hagen (Zygoptera: Coenagrionidae). Odonatologica 34:123–130
Clopton RE (1995) Domadracunculus janovyi n. gen., n. sp. (Apicomplexa: Actinocephalidae) from adults of Ischnura verticalis (Odonata: Zygoptera) in Texas. J Parasitol 81:256–260
Clopton RE (2002) Phylum Apicomplexa Levine, 1970: order Eugregarinorida Léger, 1900. In: Lee JJ, Leedale G, Patterson D, Bradbury PC (eds) Illustrated guide to the protozoa, 2nd edn. Society of protozoologists, Lawrence, pp 205–288
Clopton RE (2004) Calyxocephalus karyopera g. nov., sp. nov. (Eugregarinorida: Actinocephalidae: Actinocephalinae) from the ebony jewelwing damselfly Calopteryx maculata (Zygoptera: Calopterygidae) in southeast Nebraska: implications for mechanical prey-vector stabilization of exogenous gregarine development. Comp Parasitol 71:141–153
Clopton RE (2006) Hotel Intestine: laboratory for parasitology, gregarine information server. http://science.peru.edu/gregarina/index.html. Accessed 16 October 2009
Clopton RE, Janovy J Jr, Percival TJ (1992) Host stadium specificity in the gregarine assemblage parasitizing Tenebrio militor. J Parasitol 78:334–337
Clopton RE, Percival TJ, Janovy J Jr (1993) Nubenocephalus nebraskensis N. Gen., N. Sp. (Apilcomplexa: Actinocephalidae) from adults of Argia bipunctulata (odonata: Zygoptera). J Parasitol 79:533–537
Clopton RE, Cook TJ, Cook JL (2007) Revision of Geneiorhynchus Schneider, 1875 (Apicomplexa: Eugregarinida: Actinocephalidae: Acanthosporinae) with recognition of four new species of Geneiorhynchus and description of Geneiorhynchus manifestus n. sp. parasitizing naiads of the Green Darner, Anax junius (Odonata: Aeshnidae) in the Texas Big Thicket. Comp Parasitol 74:273–285
Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Cornell University Press, Ithaca
Elliot JM (1977) Statistical analysis of samples of Benthic Macroinvertebrates. Freshwater Biological Association, Ambleside
Forbes MR, Robb T (2008) Testing hypotheses about parasite-mediated selection using odonate hosts. In: Cordoba-Aquilar A (ed) Dragonflies & damselflies: models organisms for ecological and evolutionary research. Oxford University Press, New York, pp 175–188
Grabow K, Rüppell G (1995) Wing loading in relation to size and flight characteristics of European Odonata. Odonatologica 24:175–186
Halmetoja A, Valtonen ET, Koskenniemi E (2000) Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: a comparison of a natural lake and two acidic reservoirs in Finland. Int J Parasitol 30:1437–1444
Hays JJ, Clopton RE, Cook TJ, Cook JL (2007) Revision of the genus Nubenocephalus and description of Nubenocephalus secundus n. sp. (Apicomplexa: Actinocephalidae) parasitizing adults of Argia sedula (Odonata: Zygoptera: Coenagrionidae) in the primitive Texas Big Thicket, U.S.A. Comp Parasitol 74:286–293
Hecker KR, Forbes MR, Leonard NJ (2002) Parasitism of damselflies (Enallagma boreale) by gregarines: sex biases and relations to adult survivorship. Can J Zool 80:162–168
Jovani R, Tella JL (2006) Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol 22:214–218
Lafferty KD, Kuris AM (2005) Parasitism and environmental disturbances. In: Thomas F, Guegen F, Renaud F (eds) Parasitism and ecosystems. Oxford University Press, Oxford, pp 113–123
Lajeunesse MJ (2007) Ectoparasitism of damselflies by water mites in central Florida. Fla Entomol 15:765–778
Lajeunesse MJ, Forbes MR, Smith BP (2004) Species and sex biases in ectoparasitism of dragonflies by mites. Oikos 106:501–508
Lindsey E, Mehta M, Dhulipala V, Oberhauser K, Altizer S (2009) Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction. Ecol Entomol 34:551–561
Locklin JL, Vodopich DS (2009) Bidirectional gender biases of gregarine parasitism in two coexisting dragonflies (Anisoptera: Libellulidae). Odonatologica 38:133–140
Manwell RD (1961) Introduction to protozoology. St. Martin’s Press, New York
Morley NJ (2007) Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. Ecohealth 4:374–383
Muchiri JM, Ascolillo L, Mugambi M, Mutwiri T, Ward HD, Naumova EN, Egorov AI, Cohen S, Else JG, Griffiths JK (2009) Seasonality of Cryptosporodium oocysts detection in surface waters of Meru, Kenya as determined by two isolation methods followed by PCR. J Water Health 7:67–75
Omoto CK, Toso M, Tang K, Sibley LD (2004) Expressed sequence tag (EST) analysis of gregarine gametocyst development. Int J Parasitol 34:1265–1271
Percival TJ, Clopton RE, Janovy J Jr (1995) Hoplorhynchus acanthatholius N. Sp. and Steganorhynchus dunwoodii N. Gen. N. Sp. (Apicomplexa: Eugregarinorida) described from coenagrionid damselflies. J Eukar Microbiol 42:406–410
Poulin R (2006) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton
Richardson S, Janovy J Jr (1990) Actinocephalus carrilynnae N. Sp. (Apicomplexa: Eugregarinorida) from the Blue Damselfly, Enallagma civile (Hagen). J Eukar Microbiol 37:567–570
Roberts LS, Janovy J Jr (2005) Foundations of parasitology, 7th edn. McGraw-Hill Publishers, New York
Rodriguez Y, Omoto CK, Gomulkiewicz R (2007) Individual and population effects of eugregarine, Gregarina niphandrodes (Eugregarinida: Gregarinidae), on Tenebrio militor (Coleoptera: Tenebrionidae). Environ Entomol 36:689–393
Sarkar NK (1997) Observations of three new and one known species of cephaline gregarines (Apicomplexa: Sporozoea: Eugregarinida: Septatina) from the odonates of Mahananda Forest, West Bengal, India. Archiv fuer Protistenkunde 148:209–213
Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton
Schreurs J, Janovy J Jr (2008) Gregarines on a diet: the effects of host starvation on Gregarina confusa Janovy et al., 2007 (Apicomplexa: Eugregarinida) in Tribolium destructor Uyttenboogaart, 1933 (Coleoptera: Tenebrionidae) larvae. J Parasitol 94:567–570
Siva-Jothy MT, Plaistow SJ (1999) A fitness cost of eugregarine parasitism in a damselfly. Ecol Entomol 24:465–470
Smith AJ, Clopton RE (2003) Efficacy of oral metronidazole and potassium sorbate against two gregarine parasites, Protomagalhaensia granulosae and Gregarina cubensis (Apicomplexa: Eugregarinida), infecting the death’s head cockroach, Blaberus discoidalis. Comp Physiol 70:196–199
Steinhaus EA (1958) Crowding as a possible stress factor in insect disease. Ecology 39:503–514
Triplehorn CA, Johnson NF (2005) Borror and DeLong’s introduction to the study of insects. Brooks Cole, Belmont
Vezzani D, Wisnivesky C (2006) Prevalence and seasonality of Ascogregarina culicis (Apicomplexa: Lecudinidae) in natural populations of Aedes aegypti (Diptera: Culicidae) from temperate Argentina. J Invertebr Pathol 96:183–187
Wilson K, Reeson AF (1998) Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol Entomol 23:100–101
Wilson K, Bjornstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, New York, pp 6–44
Zuk M (1987) The effects of gregarine parasites, body size, and time of day on spermatophore production and sexual selection in field crickets. Behav Ecol Sociobiol 21:65–72
Zuk M, McKean KA (1996) Sex differences in parasitic infection: patterns and processes. Int J Parasitol 26:1009–1024
Acknowledgments
We thank Dave Cummings, Josh Huckabee, Sal LaMastra, Justin Clanton, Victoria Prescott, Isis Domingues, Edgar Alvarez, and Tamara Strohm for their assistance in the lab and field. Terry Austin and Christie Finch assisted with graphs and Tamara Cook identified the gregarines. This research was funded by a Texas Academy of Science research grant and a Temple College Faculty Leave Development grant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Locklin, J.L., Vodopich, D.S. Patterns of gregarine parasitism in dragonflies: host, habitat, and seasonality. Parasitol Res 107, 75–87 (2010). https://doi.org/10.1007/s00436-010-1836-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-010-1836-8