Reciprocal Trophic Interactions and Transmission of Blood Parasites between Mosquitoes and Frogs
Abstract
:1. Introduction
2. Habitat Synchrony and Trophic Consequences
2.1. Co-Occurrence of Mosquitoes with Different Species of Frogs
2.2. Trophic Competition in Synchronous Habitats
3. Mosquito-Vectored Parasites of Frogs
3.1. Trophic Transmission of Hepatozoon Species
3.2. Potential Transmission of Amphibian Trypanosomes by Mosquitoes
3.3. Salivary Transmission of Filarial Worms
3.4. Mechanical and Salivary Transmission of Viruses
4. Host Selection and Preference by Mosquitoes with Consequences for Parasite Transmission
5. Conclusions
References
- Hurd, H.; Hogg, J.C.; Renshaw, M. Interactions between bloodfeeding, fecundity and infection in mosquitoes. Parasitol. Today 1995, 11, 411–416. [Google Scholar] [CrossRef]
- Hudson, P.J.; Dobson, A.P.; Lafferty, K.D. Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 2006, 21, 381–385. [Google Scholar] [CrossRef]
- Bardsely, J.E.; Harmsen, R. The trypanosomes of anura. Adv. Parasitol. 1973, 11, 1–73. [Google Scholar] [CrossRef]
- Klaphake, E. Bacterial and parasitic diseases of amphibians. Vet. Clin. North Am. Exot. Anim. Pract. 2009, 12, 597–608. [Google Scholar] [CrossRef]
- Crans, W.J. The blood feeding habits of Culex territans Walker. Mosq. News 1970, 30, 445–447. [Google Scholar]
- Chamberlain, R.W.; Sudia, W.D. Mechanism of transmission of viruses by mosquitoes. Annu. Rev. Entomol. 1961, 6, 371–390. [Google Scholar] [CrossRef]
- Burkett-Cadena, N.D.; Graham, S.P.; Hassan, H.K.; Guyer, C.; Eubanks, M.D.; Katholi, C.R.; Unnasch, T.R. Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. Am. J. Trop. Med. 2008, 79, 809–815. [Google Scholar]
- Barta, J.R.; Desser, S.S. Blood parasites of amphibians from algonquin park, ontario. J. Wildl. Dis. 1984, 20, 180–185. [Google Scholar]
- Gruia-Gray, J.; Desser, S.S. Cytopathological observations and epizootiology of frog erythrocytic virus in bullfrogs (Rana catesbeiana). J. Wildl. Dis. 1992, 28, 34–41. [Google Scholar]
- Bartlett-Healy, K.; Crans, W.; Gaugler, R. Vertebrate hosts and phylogenetic relationships of amphibian trypanosomes from a potential invertebrate vector, Culex territans Walker (Diptera: Culicidae). J. Parasitol. 2009, 95, 381–387. [Google Scholar] [CrossRef]
- Smyth, J.D.; Smyth, M.M. Frogs as Host-Parasite Systems I; Macmillan Press Ltd.: London and Basingstoke, UK, 1980. [Google Scholar]
- Smith, T.G. The genus Hepatozoon (Apicomplexa: Adeleina). J. Parasitol. 1996, 82, 565–585. [Google Scholar] [CrossRef]
- Desser, S.S.; McIver, S.B.; Jez, D. Observations on the role of simulids and culicids in the transmission of avian and anuran trypanosomes. Int. J. Parasitol. 1975, 5, 507–509. [Google Scholar] [CrossRef]
- Cupp, E.W.; Zhang, D.; Yue, X.; Cupp, M.S.; Guyer, C.; Sprenger, T.R.; Unnasch, T.R. Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephaomyelitis virus focus in central Alabama. Am. Soc. Trop. Med. Hyg. 2004, 71, 272–276. [Google Scholar]
- Borkent, A.; Belton, P. Attraction of female Uranotanenia lowii (Diptera: Culicidae) to frog calls in Costa Rica. Can. Entomol. 2006, 138, 91–94. [Google Scholar] [CrossRef]
- Belkin, J.N.; Hogue, C.L. A review of the crabhole mosquitoes of the genus Deinocerites (Diptera, Culicidae). Univ. Calif. Publ. Entomol. 1959, 14, 411–458. [Google Scholar]
- Bailey, J.K. Aedes aegypti as a possible new invertebrate host for frog trypanosomes. Exp. Parasitol. 1962, 12, 155–163. [Google Scholar] [CrossRef]
- Causey, O.R. Aedes and Culex mosquitoes as intermediate hosts of frog filarial, Foleyella sp. Am. J. Epidemiol. 1939, 29, 79–81. [Google Scholar]
- Wood, D.M.; Dang, P.T.; Ellis, R.A. Genus Culex Linnaeus. In The Insects and Arachnids of Canada; Canadian Government Publishing Centre: Hull, QC, Canada, 1979; pp. 272–286. [Google Scholar]
- Bentley, M.D.; Day, J.F. Chemical ecology and behavioural aspects of mosquito oviposition. Annu. Rev. Entomol. 1989, 34, 401–421. [Google Scholar] [CrossRef]
- Rubbo, M.J.; Lanterman, J.L.; Falco, R.C.; Daniels, T.J. The influence of amphibians on mosquitoes in seasonal pools: Can wetlands protection help to minimize disease risk? Wetlands 2011, 31, 799–804. [Google Scholar] [CrossRef]
- Bartlett-Healy, K.; Crans, W.; Gaugler, R. Temporal and spatial synchrony of Culex territans (Diptera: Culicidae) with their amphibian hosts. J. Med. Entomol. 2008, 45, 1032–1038. [Google Scholar]
- Petranka, J.W.; Thomas, D.A.G. Explosive breeding reduces egg and tadpole cannibalism in the wood frog, Rana sylvatica. Anim. Behav. 1995, 50, 731–739. [Google Scholar] [CrossRef]
- Bellis, E.D. Home range and movements of the wood frog in a northern bog. Ecology 1965, 46, 90–98. [Google Scholar] [CrossRef]
- McCauley, S.J.; Bouchard, S.S.; Farina, B.J.; Isvaran, K.; Quader, S.; Wood, D.W.; St. Mary, C.M. Energetic dynamics and anuran breeding phenology: Insights from a dynamic game. Behav. Ecol. 2000, 11, 429–436. [Google Scholar] [CrossRef]
- Paton, P.W.C.; Crouch, W.B. Using the phenology of pond-breeding amphibians to develop conservation strategies. Conserv. Biol. 2000, 16, 194–204. [Google Scholar]
- Skelly, D.K. Tadpole communities: Pond performance and predation are powerful forces shaping the structure of tadpole communities. Am. Sci. 1997, 85, 36–45. [Google Scholar]
- Wells, K.D. Territoriality and male mating success in the green frog (Rana clamitans). Ecology 1977, 58, 750–762. [Google Scholar] [CrossRef]
- Willis, Y.L.; Moyle, D.L.; Baskett, T.S. Emergence, breeding, hibernation, movements and transformation in the bullfrog, Rana catesbeiana in Missouri. Copeia 1956, 1, 30–41. [Google Scholar]
- Mokany, A.; Shine, R. Oviposition site selection by mosquitoes is affected by cues from conspecific larvae and anuran tadpoles. Austr. Ecol. 2003, 28, 33–37. [Google Scholar] [CrossRef]
- Angelon, K.A.; Petranka, J.W. Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J. Chem. Ecol. 2002, 28, 797–806. [Google Scholar] [CrossRef]
- Mokany, A.; Shine, R. Competition between tadpoles and mosquito larvae. Oecologia 2003, 135, 615–620. [Google Scholar]
- Hagman, M.; Shine, R. Effects of invasive cane toads on Australian mosquitoes: Does the dark cloud have a silver lining? Biol. Invasions 2007, 9, 445–452. [Google Scholar] [CrossRef]
- Blaustein, L.; Margalit, J. Priority effects in temporary pools: nature and outcome of mosquito larva-toad tadpole interactions depend on order of entrance. J. Anim. Ecol. 1996, 65, 77–84. [Google Scholar] [CrossRef]
- Spielman, A.; Sullivan, J.J. Predation on peridomestic mosquitoes by hylid tadpoles on Grand Bahama Island. Am. J. Trop. Med. Hyg. 1974, 23, 704–709. [Google Scholar]
- Blaustein, L.; Margalit, J. Mosquito larvae (Culiseta longiareolata) prey upon and compete with toad tadpoles (Bufo viridis). J. Anim. Ecol. 1994, 43, 841–850. [Google Scholar] [CrossRef]
- DuRant, S.E.; Hopkins, W.A. Amphibian predation of larval mosquitoes. Can. J. Zool. 2008, 86, 1159–1164. [Google Scholar] [CrossRef]
- Rhagavendra, K.; Sharma, P.; Dash, A.P. Biological control for mosquito populations through frogs: Opportunities and constrains. Indian J. Med. Res. 2008, 128, 22–25. [Google Scholar]
- Lawler, S.P.; Dritz, D.; Strange, T.; Holyoak, M. Effects of introduced mosquitofish and bullfrogs on the threatened California Red-Legged Frog. Conserv. Biol. 1999, 13, 613–622. [Google Scholar] [CrossRef]
- Boulianne, B.A.B.; Evans, R.C.; Smith, T.G. Phylogenetic analysis of Hepatozoon species (Apicomplexa: Adeleorina) infecting frogs of Nova Scotia, Canada, determined by ITS-1 sequences. J. Parasitol. 2007, 93, 1435–1441. [Google Scholar] [CrossRef]
- Kim, B.; Smith, T.G.; Desser, S.S. The life history and host specificity of Hepatozoon clamatae (Apicomplexa: Adeleorina) and ITS-1 nucleotide sequence variation of Hepatozoon species of frogs and mosquitoes from Ontario. J. Parasitol. 1998, 84, 789–797. [Google Scholar] [CrossRef]
- Desser, S.S.; Hong, H.; Martin, D.S. The life history, ultrastructure and experimental transmission of Hepatozoon catesbianae n. comb., an Apicomplexan parasite of the bullfrog, Rana catesbeiana and the mosquito, Culex territans in Algonquin Park, Ontario. J. Parasitol. 1995, 81, 212–222. [Google Scholar] [CrossRef]
- Brown, G.P.; Shilton, C.M.; Shine, R. Do parasites matter? Assessing the fitness consequences of haemogregarine infection in snakes. Can. J. Zool. 2006, 84, 668–676. [Google Scholar] [CrossRef]
- Madsen, T.; Ujvari, B.; Olsson, M. Old pythons stay fit; effects of haematozoan infections on life history traits of a large tropical predator. Popul. Ecol. 2005, 142, 407–412. [Google Scholar]
- Ewing, S.A.; Panciera, R.J. American canine hepatozoonosis. Clin. Microbiol. Rev. 2003, 16, 688–697. [Google Scholar] [CrossRef]
- Wozniak, E.J.; Kazacos, K.R.; Telford, S., Jr.; Mclaughlin, G.L. Characterization of the clinical and anatomical pathological changes associated with Hepatozoon mocassini infections in unnatural reptilian hosts. Int. J. Parasitol. 1996, 26, 141–146. [Google Scholar] [CrossRef]
- Harkness, L.M.; Drohan, A.E.; Dickson, C.M.; Smith, T.G. Experimental transmission of Hepatozoon clamatae (Apicomplexa: Adeleida) to the wood frog, Rana sylvatica, and to the mosquito Culex pipiens. J. Parasitol. 2010, 96, 434–436. [Google Scholar] [CrossRef]
- Smith, T.G.; Desser, S.S. Ultrastructural features of the gametogenic and sporogonic development of Hepatozoon sipedon (Apicomplex: Adeleorina). Parasites 1997, 2, 141–151. [Google Scholar]
- Bardsley, J.E.; Harmsen, R. The trypanosomes of Ranidae. I. The effects of temperature and diurnal periodicity on the peripheral parasitaemia in the bullfrog (Rana catesbeiana Shaw). Can. J. Zool. 1968, 47, 283–288. [Google Scholar] [CrossRef]
- Desser, S.S.; McIver, S.B.; Ryckman, A. Culex territans as a potential vector of Trypanosoma rotatorium. I. Development of the flagellate in the mosquito. J. Parasitol. 1973, 59, 353–358. [Google Scholar] [CrossRef]
- Benach, J.L.; Crans, W.J. Larval development and transmission of Foleyella flexicauda Schacher and Crans, 1973 (Nematoda: Filarioidea) in Culex territans. J. Parasitol. 1973, 59, 797–800. [Google Scholar] [CrossRef]
- Schacher, J.F.; Crans, W.J. Foleyella flexicauda sp. n. (Nematoda: Filarioidea) from Rana catesbeiana in New Jersey, with a review of the genus and erection of two new subgenera. J. Parasitol. 1973, 59, 685–691. [Google Scholar]
- Crans, W.J. Preliminary observations of frog filariasis in New Jersey. Bull. Wildl. Dis. Assoc. 1969, 5, 342–347. [Google Scholar]
- Causey, O.R. Development of the larval stages of Foleyella brachyoptera in mosquitoes. Am. J. Epidemiol. 1939, 30, 69–71. [Google Scholar]
- Lefèvre, T.; Lebarbenchon, C.; Gautheir-Clerc, M.; Missé, D.; Poulin, R.; Thomas, F. The ecological significance of manipulative parasites. Trends Ecol. Evol. 2009, 24, 41–48, and reference therein. [Google Scholar] [CrossRef]
- White, G.; Ottendorfer, C.; Graham, S.; Unnasch, T.R. Competency of reptiles and amphibians for Eastern Equine Encephalitis Virus. Am. J. Trop. Med. Hygi. 2011, 85, 421–425. [Google Scholar] [CrossRef]
- Belzer, W.R.; Seibert, S. A natural history of Ranavirus in an Eastern Box Turtle Population. Turt. Tortoise Newsl. 2011, 15, 18–25. [Google Scholar]
- Takken, W.; Knols, B.G.J. Odor-mediated behaviour of afrotropical malaria mosquitoes. Annu. Rev. Entomol. 1999, 44, 131–157. [Google Scholar] [CrossRef]
- Williams, C.R.; Smith, B.P.C.; Best, S.M.; Tyler, M.J. Mosquito repellents in frog skin. Biol. Lett. 2006, 2, 242–245. [Google Scholar] [CrossRef]
- Bartlett-Healy, K.; Crans, W.; Gaugler, R. Phonotaxis to amphibian vocalizations in Culex territans (Diptera: Culicidae). Ann. Entomol. Soc. Am. 2008, 101, 94–103. [Google Scholar]
- McIver, S.B. Comparative study of antennal sense organs of female culicine mosquitoes. Can. Entomol. 1970, 102, 1258–1267. [Google Scholar] [CrossRef]
- McIver, S.; Charlton, C. Studies on the sense organs on the palps of selected culicine mosquitoes. Can. J. Zool. 1970, 48, 293–295. [Google Scholar] [CrossRef]
- Bartlett, K. Factors Contributing to the Host Specificity of the Frog-Feeding Mosquito Culex Territans Walker (Diptera: Culicidae). Ph.D. Thesis, Graduate School, The State University of New Jersey, Rutgers, NJ, USA, 2009. [Google Scholar]
- Burkett-Cadena, N.D.; McClure, C.J.W.; Ligon, R.A.; Graham, S.P.; Guyer, C.; Hill, G.E.; Ditchkoff, S.S.; Eubanks, M.D.; Hassan, H.K.; Unnasch, T.R. Host reproductive phenology drives seasonal patterns of host use in mosquitoes. PLoS One 2011, 6, 1–7. [Google Scholar]
- McKenzie, V.J.; Starks, H.A. Blood parasites of two Costa Rican amphibians with comments on detection and microfilaria density associated with adult filarial worm intensity. J. Parasitol. 2008, 94, 824–829. [Google Scholar] [CrossRef]
- Johnson, R.N.; Young, D.G.; Butler, J.F. Trypanosome transmission by Corethrella wirthi (Diptera: Chaoboridae) to the Green Treefrog, Hyla cinerea (Anura: Hylidae). J. Med. Entomol. 1993, 30, 918–921. [Google Scholar]
- Bernal, X.E.; Rand, A.S.; Ryan, M.J. Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls. Behav. Ecol. 2006, 17, 709–715. [Google Scholar]
- Bernal, X.E.; Page, R.A.; Rand, A.S.; Ryan, M.J. Cues for eavesdroppers: Do frog calls indicate prey density and quality? Am. Nat. 2007, 169, 409–415. [Google Scholar] [CrossRef]
- Thomas, F.; Poulin, R.; de Meeüs, T.; Guégan, J.-F.; Renaud, F. Parasites and ecosystem engineering: What roles could they play? Oikos 1999, 84, 167–171. [Google Scholar] [CrossRef]
- Blaustein, A.R.; Han, B.A.; Relyea, R.A.; Johnson, P.T.J.; Buck, J.C.; Gervasi, S.S.; Kats, L.B. The complexity of amphibian population declines: Understanding the role of cofactors in driving amphibian losses. Ann. New York Acad. Sci. 1223, 108–119. [Google Scholar]
- Brooks, D.R.; Hoberg, E.P. How will global climate change affect parasite-host assemblages. Trends Parasitol. 2007, 23, 571–574. [Google Scholar] [CrossRef]
- Dunn, R.R.; Harris, N.C.; Colwell, R.K.; Koh, L.P.; Sodhi, N.S. The sixth mass coextinction: Are the most endangered species parasites and mutualists? Proc. R. Soc. Biol. Sci. 2009, 276, 3037–3045. [Google Scholar] [CrossRef]
- Gray, M.J.; Miller, D.L.; Hoverman, J.T. Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Org. 2009, 87, 243–266. [Google Scholar] [CrossRef]
- Whittington, R.J.; Becker, J.A.; Dennis, M.M. Iridovirus infections in finfish—Critical review with emphasis on ranaviruses. J. Fish Dis. 2010, 33, 95–102. [Google Scholar] [CrossRef]
© 2012 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Ferguson, L.V.; Smith, T.G. Reciprocal Trophic Interactions and Transmission of Blood Parasites between Mosquitoes and Frogs. Insects 2012, 3, 410-423. https://doi.org/10.3390/insects3020410
Ferguson LV, Smith TG. Reciprocal Trophic Interactions and Transmission of Blood Parasites between Mosquitoes and Frogs. Insects. 2012; 3(2):410-423. https://doi.org/10.3390/insects3020410
Chicago/Turabian StyleFerguson, Laura V., and Todd G. Smith. 2012. "Reciprocal Trophic Interactions and Transmission of Blood Parasites between Mosquitoes and Frogs" Insects 3, no. 2: 410-423. https://doi.org/10.3390/insects3020410
APA StyleFerguson, L. V., & Smith, T. G. (2012). Reciprocal Trophic Interactions and Transmission of Blood Parasites between Mosquitoes and Frogs. Insects, 3(2), 410-423. https://doi.org/10.3390/insects3020410