Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-21T14:31:12.622Z Has data issue: false hasContentIssue false
  • English
  • Français

Dung beetles and fecal helminth transmission: patterns, mechanisms and questions

Published online by Cambridge University Press:  18 December 2013

ELIZABETH NICHOLS  and
ANDRÉS GÓMEZ
ELIZABETH NICHOLS*
Affiliation:
Department of Ecology, University of São Paulo, São Paulo, SP, Brazil Lancaster Environment Centre, Lancaster University, Lancaster, UK
ANDRÉS GÓMEZ
Affiliation:
Center for Biodiversity and Conservation, American Museum of Natural History, New York, NY, USA
*
*Corresponding author: Department of Ecology, University of São Paulo, São Paulo, SP, Brazil; Lancaster Environment Centre, Lancaster University, Lancaster, UK. E-mail: lizsnichols@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Dung beetles are detrivorous insects that feed on and reproduce in the fecal material of vertebrates. This dependency on vertebrate feces implies frequent contact between dung beetles and parasitic helminths with a fecal component to their life-cycle. Interactions between dung beetles and helminths carry both positive and negative consequences for successful parasite transmission, however to date there has been no systematic review of dung beetle-helminth interactions, their epidemiological importance, or their underlying mechanisms. Here we review the observational evidence of beetle biodiversity–helminth transmission relationships, propose five mechanisms by which dung beetles influence helminth survival and transmission, and highlight areas for future research. Efforts to understand how anthropogenic impacts on biodiversity may influence parasite transmission must include the development of detailed, mechanistic understanding of the multiple interactions between free-living and parasitic species within ecological communities. The dung beetle–helminth system may be a promising future model system with which to understand these complex relationships.

Keywords

Scarabaeinaedisease ecologyenvironmental changeparasite ecologymacroparasitemicroparasite
Type
Review Article
Information
Parasitology , Volume 141 , Issue 5 , April 2014 , pp. 614 - 623
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorsen, O. (2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society B – Biological Sciences 269, 1625–1632. doi: 10.1098/rspb.2002.2064.CrossRefGoogle ScholarPubMed
Alicata, J. E. (1935). Early Development Stages of Nematodes Occurring in Swine. U.S. Department of Agriculture Technical Bulletin No. 489. Washington, DC, USA.Google Scholar
Arnold, S. J. (1983). Morphology, performance and fitness. American Zoologist 23, 347–361.CrossRefGoogle Scholar
Bailey, W. S. (1972). Spirocera lupi: a continuing inquiry. Journal of Parasitology 58, 3–22.Google Scholar
Bailey, W. S., Cabrera, D. J. and Diamond, D. L. (1963). Beetles of the family Scarabaeidae as intermediate hosts for Spirocerca lupi . Journal of Parasitology 49, 485–488.Google Scholar
Bergstrom, R. C., Maki, L. R. and Werner, B. A. (1976). Small dung beetles as biological control agents: laboratory studies of beetle action on trichostrongylid eggs in sheep and cattle feces. Proceedings of the Helminthological Society of Washington 43, 171–174.Google Scholar
Biggane, R. P. J. and Gormally, M. J. (1994). The effect of dung beetle activity on the discharge of Pilobolus (Fungi, Mucorales) sporangia in cattle, sheep and horse faeces. Entomophaga 39, 95–98.Google Scholar
Bílý, S. and Prokopic, J. (1977). Destruction of Ascaris suum eggs during their feeding to various species of beetles. Folia Parasitologica 24, 343–345.Google Scholar
Bílý, S., Stĕrba, J. and Dyková, I. (1978). Results of an artificial feeding of eggs of Taenia saginata Goeze, 1782 to various beetle species. Folia Parasitologica 25, 257–260.Google Scholar
Bornemissza, G. F. (1960). Could dung eating insects improve our pastures? Journal of the Australian Institute of Agricultural Science 26, 54–56.Google Scholar
Bowman, D. D. (2008). Georgis’ Parasitology for Veterinarians, 9 Edn. Saunders, Amsterdam, the Netherlands.Google Scholar
Bryan, R. P. (1973). The effects of dung beetle activity on the numbers of parasitic gastrointestinal helmintic larvae recovered from pasture samples. Australian Journal of Agricultural Research 24, 161–168.Google Scholar
Bryan, R. P. (1976). The effects of the dung beetle, Onthophagus gazella, on the ecology of the infective larvae of gastrointestinal nematodes of cattle. Australian Journal of Agricultural Research 27, 567–574.Google Scholar
Bryan, R. P. and Kerr, J. D. (1989). Factors affecting the survival and migration of the free living stages of gastrointestinal nematode parasites of cattle in central Queensland. Veterinary Parasitology 30, 315–326.CrossRefGoogle ScholarPubMed
Chirico, J., Wiktelius, S. and Waller, P. J. (2003). Dung beetle activity and the development of trichostrongylid eggs into infective larvae in cattle faeces. Veterinary Parasitology 118, 157–163.Google Scholar
Coldham, J. (2011). Dung Beetles and Internal Parasites of Sheep. Meat & Livestock Australia Limited, North Sydney, Australia.Google Scholar
Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T. and Mitchell, C. E. (2010). Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13, 1221–1232.CrossRefGoogle ScholarPubMed
Davis, A. (2009). Outlines of composition, spatial pattern and hypothetical origins of regional dung beetle faunas. In Evolutionary Biology and Conservation of Dung Beetles (ed. Scholtz, C., Davis, A. L. V. and Kryger, U.), pp. 365–383. Pensoft, Sofia, Bulgaria.Google Scholar
Davis, A. L. V., Scholtz, C. H. and Swemmer, A. M. (2012). Effects of land usage on dung beetle assemblage structure: Kruger National Park versus adjacent farmland in South Africa. Journal of Insect Conservation 16, 399–411.CrossRefGoogle Scholar
Dobson, A. P. and Hudson, P. J. (1992). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. II. Population models. Journal of Animal Ecology 61, 487–498.CrossRefGoogle Scholar
Durie, P. H. (1961). Parasitic gastroenteritis of cattle: the distribution and survival of infective strongyle larvae on pasture. Australian Journal of Agricultural Research 12, 1200–1211.Google Scholar
du Toit, C. A., Holter, P., Lutermann, H. and Scholtz, C. H. (2012). Role of dung beetle feeding mechanisms in limiting the suitability of species as hosts for the nematode Spirocerca lupi . Medical and Veterinary Entomology 26, 455–457.Google Scholar
Edwards, P. B. and Aschenborn, H. H. (1987). Patterns of nesting and dung burial in Onitis dung beetles: implications for pasture productivity and fly control. Journal of Applied Ecology 24, 837–851.Google Scholar
Estrada, A. and Coates-Estrada, R. (1991). Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 7, 459–474.Google Scholar
Estrada, A. and Coates-Estrada, R. (2002). Dung beetles in continuous forest, forest fragments and in an agricultural mosaic habitat island at Los Tuxtlas, Mexico. Biodiversity and Conservation 11, 1903–1918.Google Scholar
Fincher, G. T. (1973). Nidification and reproduction of Phanaeus spp. in three textural classes of soil (Coleoptera: Scarabaeidae). Coleopterists Bulletin 27, 33–37.Google Scholar
Fincher, G. T. and Marti, O. G. (1982). Onthophagus gazella as an intermediate host for spiruroids in Georgia and Texas. Southwestern Entomologist 7, 125–129.Google Scholar
García-Robledo, C., Erickson, D. L., Staines, C. L., Erwin, T. L. and Kress, W. J. (2013). Tropical plant-herbivore networks: reconstructing species interactions using DNA barcodes. PLoS ONE 8, e52967.Google Scholar
Gardner, T. A., Hernandez, M. I. M., Barlow, J. and Peres, C. A. (2008). Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology 45, 883–893.Google Scholar
Gazzinelli, A., Correa-Oliveira, R., Yang, G. J., Boatin, B. A. and Kloos, H. (2012). A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLoS Neglected Tropical Diseases 6, e1603.CrossRefGoogle ScholarPubMed
Gormally, M. J. (1993). The effect of dung beetle activity on the discharge of Pilobus sporangia in cattle faeces. Medical and Veterinary Entomology 7, 197–198.CrossRefGoogle Scholar
Gottlieb, Y., Markovics, A., lKlementa, E., Naora, S., Samish, M., Arocha, I. and Lavya, E. (2011). Characterization of Onthophagus sellatus as the major intermediate host of the dog esophageal worm Spirocerca lupi in Israel. Veterinary Parasitology 180, 378–382.Google Scholar
Grønvold, J., Sommer, C., Holter, P. and Nansen, P. (1992). Reduced splash dispersal of bovine parasitic nematodes from cow pats by the dung beetle Diastellopalpus quinquedens . Journal of Parasitology 78, 845–848.CrossRefGoogle Scholar
Grønvold, J., Henriksen, S. A., Larsen, M., Nansen, P. and Wolstrup, J. (1996). Biological control. Aspects of biological control – with special reference to arthropods, protozoans and helminths of domesticated animals. Veterinary Parasitology 64, 47–64.CrossRefGoogle ScholarPubMed
Halffter, G. and Edmonds, W. D. (1982). The Nesting Behavior of Dung Beetles (Scarabaeinae). An Ecological and Evolutive Approach. Instituto de Ecología, México, DF.Google Scholar
Hawley, D. M. and Altizer, S. M. (2010). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 48–60.Google Scholar
Holter, P. (2000). Particle feeding in Aphodius dung beetles (Scarabaeidae): old hypotheses and new experimental evidence. Functional Ecology 14, 631–637.Google Scholar
Holter, P. (2004). Dung feeding in hydrophilid, geotrupid and scarabaeid beetles: examples of parallel evolution. European Journal of Entomology 101, 365–372.Google Scholar
Holter, P. and Scholtz, C. H. (2005). Are ball-rolling (Scarabaeini, Gymnopleurini, Sisyphini) and tunnelling scarabaeine dung beetles equally choosy about the size of ingested dung particles? Ecological Entomology 30, 700–705.Google Scholar
Holter, P. and Scholtz, C. H. (2007). What do dung beetles eat? Ecological Entomology 32, 690–697.Google Scholar
Holter, P., Scholtz, C. H. and Wardhaugh, K. W. (2002). Dung feeding in adult scarabaeines (tunnellers and endocoprids): even large dung beetles eat small particles. Ecological Entmology 27, 169–176.Google Scholar
Hotez, P. J. (2009). Mass drug administration and integrated control for the world's high-prevalence neglected tropical diseases. Clinical Pharmacology and Therapeutics 85, 659–664.Google Scholar
Houston, R. S., Craig, T. M. and Fincher, G. T. (1984). Effects of Onthophagus gazella F (Coleoptera: Scarabaeidae) on free-living strongyloids of equids. American Journal of Veterinary Research 45, 572–574.Google ScholarPubMed
Hutchinson, G. W., Abba, S. A. and Mfitilodze, M. W. (1989). Seasonal translation of equine strongyle infective larvae to herbage in tropical Australia. Veterinary Parasitology 33, 251–263.Google Scholar
Johnson, P. T. J. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961–970.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Preston, D. L., Hoverman, J. T., Henderson, J. S., Paull, S. H., Richgels, K. L. D. and Redmond, M. D. (2012 a). Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93, 56–64.Google Scholar
Johnson, P. T. J., Rohr, J. R., Hoverman, J. T., Kellermanns, E., Bowerman, J. and Lunde, K. B. (2012 b). Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235–242.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230–233.CrossRefGoogle ScholarPubMed
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.CrossRefGoogle ScholarPubMed
Larsen, T., Williams, N. and Kremen, C. (2005). Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters 8, 538–547.Google Scholar
Lindquist, A. W. (1933). Amounts of dung buried and soil excavated by certain Coprini (Scarabaeideae). Kansas Entomological Society 6, 109–125.Google Scholar
Lopez, A. D. and Mathers, C. D. (2006). Measuring the global burden of disease and epidemiological transitions: 2002–2030. Annals of Tropical Medicine and Parasitology 100, 481–499.Google Scholar
Lucker, J. T. (1936). Extent of vertical migration of horse strongyle larvae in soils of different types. Journal of Agricultural Research 52, 353–361.Google Scholar
Lucker, J. T. (1938). Vertical migration, distribution, and survival of infective horse strongyle larvae developing in feces buried in different soils. Journal of Agricultural Research 57, 335–348.Google Scholar
Lustigman, S., Prichard, R. K., Gazzinelli, A., Grant, W. N., Boatin, B. A., McCarthy, J. S. and Basáñez, M.-G. (2012). A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Neglected Tropical Diseases 6, e1582.Google Scholar
Madle, H. (1934). Zur Kenntnis der Morphologie, Ökologie und Physiologie von Aphodius rufipes Lin. und einigen verwandten Arten. Zoologische Jahrbücher (Anatomie und Ontogenie der Tiere) 58, 303–396.Google Scholar
Martínez, A. (1959). Catálogo de los Scarabaeidae Argentinos (Coleoptera). Revista del Museo de Ciencias Naturales Bernadino Rivadavia 5, 1–126.Google Scholar
Mathison, B. and Ditrich, O. (1999). The fate of Cryptosporidium parvum oocysts ingested by dung beetles and their possible role in the dissemination of cryptosporidiosis. Journal of Parasitology 85, 678–681.CrossRefGoogle ScholarPubMed
Mazaki-Tovi, M., Baneth, G., Aroch, I., Harrus, S., Kass, P.H., Ben-Ari, T., Zur, G., Aizenberg, I., Bark, H. and Lavy, E. (2002). Canine spirocercosis: clinical, diagnostic, pathologic, and epidemiologic characteristics. Veterinary Parasitology 107, 235–250.Google Scholar
Mfitilodze, M. W. and Hutchinson, G. W. (1988). Development of free-living stages of equine strongyles in faeces on pasture in a tropical environment. Veterinary Parasitology 26, 285–296.Google Scholar
Miller, A. (1954). Dung beetles (Coleoptera, Scarabaeidae) and other insects in relation to human feces in a hookworm area of southern Georgia. American Journal of Tropical Medicine and Hygiene 3, 372–389.Google Scholar
Miller, A., Chi-Rodriquez, E. and Nichols, R. L. (1961). The fate of helminth eggs and protozoan cysts in human feces ingested by dung beetles (Coleoptera: Scarabeidae). American Journal of Tropical Medicine and Hygiene 10, 748–754.Google Scholar
Mukaratirwa, S., Pillay, E. and Munsammy, K. (2010). Experimental infection of selected arthropods with spirurid nematodes Spirocerca lupi Railliet & Henry, 1911 and Gongylonema ingluvicola Molin, 1857. Journal of Helminthology 84, 369–374. doi: 10.1017/s0022149x10000039.Google Scholar
Mutinga, M. J. and Madel, G. (1981). The role of coprophagous beetles in the dissemination of taeniasis in Kenya. Insect Science and its Application 1, 379–382.Google Scholar
Nichols, E. and Gardner, T. A. (2011). Dung beetles as a candidate study taxon in applied biodiversity conservation research. In Dung Beetle Ecology and Evolution (ed. Simmons, L. W. and Ridsdill-Smith, J.), pp. 267–291. Wiley-Blackwell, Chichester, UK.Google Scholar
Nichols, E., Gardner, T. A., Peres, C. A., Spector, S. and the Scarabaeinae Research Network (2009). Co-declining mammals and dung beetles: an impending ecological cascade. Oikos 118, 481–487.Google Scholar
Nichols, E., Uriarte, M., Bunker, D. E., Favila, M., Slade, E. M., Vulinec, K., Larsen, T., Mello, F. V. d., Louzada, J. N. C., Naeem, S. and Spector, S. H. (2013). Trait-dependent response of dung beetle populations to tropical forest conversion at local to global scales. Ecology 94, 180–189.Google Scholar
Orlofske, S. A., Jadin, R. C., Preston, D. L. and Johnson, P. T. J. (2012). Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 1247–1253.Google Scholar
Over, H. J., Jansen, J. and van Olm, P. W. (1992). Distribution and Impact of Helminth Diseases of Livestock in Developing Countries. Food and Agriculture Organization, Rome, Italy.Google Scholar
Pompanon, F., Deagle, B. E., Symondson, W. O. C., Brown, D. S., Jarman, S. N. and Taberlet, P. (2012). Who is eating what: diet assessment using next generation sequencing. Molecular Ecology 21, 1931–1950.Google Scholar
Prichard, R. K., Basáñez, M.-G., Boatin, B. A., McCarthy, J. S., García, H. H., Yang, G.-J., Sripa, B. and Lustigman, S. (2012). A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Neglected Tropical Diseases 6, e1549.Google Scholar
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.Google Scholar
Roepstorff, A., Grønvold, J., Larsen, M. N., Kraglund, H. O. and Fagerholm, H. P. (2002). The earthworm Lumbricus terrestris as a possible paratenic or intermediate host of the pig parasite Ascaris suum . Comparative Parasitology 69, 206–210.Google Scholar
Ryan, U., Yang, R., Gordon, C. and Doube, B. (2011). Effect of dung burial by the dung beetle Bubas bison on numbers and viability of Cryptosporidium oocysts in cattle dung. Experimental Parasitology 129, 1–4.Google Scholar
Saitoh, Y. and Itagaki, H. (1990). Dung beetles, Onthophagus spp., as potential transport hosts of feline coccidia. Japanese Journal of Veterinary Science 52, 293–297.Google Scholar
Schmidt, G. D., Roberts, L. S. and Janovy, J. J. (2000). Foundations of Parasitology, 6th Edn. McGraw-Hill Education, New York, NY, USA.Google Scholar
Shepherd, V. E. and Chapman, C. A. (1998). Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal Of Tropical Ecology 14, 199–215.Google Scholar
Stewart, T. B. and Kent, K. M. (1963). Beetles serving as intermediate hosts of swine nematodes in southern Georgia. Journal of Parasitology 49, 158–159.Google Scholar
Stromberg, B. (1997). Environmental factors influencing transmission. Veterinary Parasitology 72, 247–264.Google Scholar
Stumpf, I. V. K. (1986). Hospedeiros intermediários de Macracanthorynchus hirudinaceus (Pallas, 1781) (Acanthocephala) em Mandirituba, Paraná, Brasil. Acta Biologica Paranaense 15, 87–124.Google Scholar
Suzán, G., Marcé, E., Giermakowski, J. T., Mills, J. N., Ceballos, G., Ostfeld, R. S., Armién, B., Pascale, J. M. and Yates, T. L. (2009). Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4, e5461.Google Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426.Google Scholar
Vercruysse, J., Albonico, M., Behnke, J. M., Kotze, A. C., Prichard, R. K., McCarthy, J. S., Montresor, A. and Levecke, B. (2011). Is anthelmintic resistance a concern for the control of human soil-transmitted helminths? International Journal for Parasitology: Drugs and Drug Resistance 1, 14–27.Google Scholar
Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I. and Garnier, E. (2007). Let the concept of trait be functional! Oikos 116, 882–892.Google Scholar
Vulinec, K. (2000). Dung beetles (Coleoptera: Scarabaeidae), monkeys, and conservation in Amazonia. Florida Entomologist 83, 229–241.Google Scholar
Vulinec, K. (2002). Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica 34, 297–309.Google Scholar
Waghorn, T. S., Leathwick, D.M., Chen, L. Y., Gray, R. A. and Skipp, R. A. (2002). Influence of nematophagous fungi, earthworms and dung burial on development of the free-living stages of Ostertagia (Teladorsagia) circumcincta in New Zealand. Veterinary Parasitology 104, 119–129.Google Scholar
Whipple, S. D. and Hoback, W. W. (2012). A comparison of dung beetle (Coleoptera: Scarabaeidae) attraction to native and exotic mammal dung. Environmental Entomology 41, 238–244.Google Scholar
WHO (2004). The World Health Report 2004: Changing History. World Health Organization, Geneva, Switzerland.Google Scholar
WHO/UNICEF (2012). Progress on Drinking Water and Sanitation: 2012 Update. WHO/UNICEF, New York, NY, USA.Google Scholar
Williams, J. C. and Bilkovich, F. R. (1971). Development and survival of infective larvae of the cattle nematode, Ostertagia ostertagi . Journal of Parasitology 57, 327–338.Google Scholar
Wood, C. L. and Lafferty, K. D. (2012). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28, 239–247.Google Scholar
Xu, J., Liu, Q., Jing, H., Pang, B., Yang, J., Zhao, G. and Li, H. (2003). Isolation of Escherichia coli O157:H7 from dung beetles Catharsius molossus . Microbiology and Immunology 47, 45–49.Google Scholar
Supplementary material: File

NICHOLS and ANDRÉS GÓMEZ supplementary material

Supplementary table

Download NICHOLS and ANDRÉS GÓMEZ supplementary material(File)
File 24.5 KB