Parasitology Research

, Volume 117, Issue 5, pp 1621–1630 | Cite as

Nestedness in assemblages of helminth parasites of bats: a function of geography, environment, or host nestedness?

  • Elizabeth M. Warburton
  • Luther Van Der Mescht
  • Irina S. Khokhlova
  • Boris R. Krasnov
  • Maarten J. Vonhof
Original Paper


Nested subsets occur in ecological communities when species-poor communities are subsets of larger, species-rich communities. Understanding this pattern can help elucidate species colonization abilities, extinction risks, and general structuring of biological communities. Here, we evaluate nestedness in a poorly studied host–parasite system, bats and their helminths, across the Japanese archipelago and within its different bioclimatic regions. We hypothesized that (1) if helminth communities are nested across geographic sites at the level of the archipelago, then broad-scale processes, like colonization-extinction dynamics, mainly structure parasite assemblages; (2) if helminth communities are nested across geographic sites at the level of the bioclimatic region, then fine-scale environmental variation plays a significant role in species nestedness; (3) if helminth community nestedness mirrors host species nestedness, then communities are nested because the habitats they occupy are nested; and (4) if nestedness does not occur or if it is not correlated with any geographical or host data, then passive sampling could be responsible for the patterns of parasite assemblage in our sample. We found that helminth communities were nested across host species throughout the archipelago but, when considering each bioclimatic region, helminths in only one region were significantly more nested than the null model. Helminth communities were also nested across sites within all four bioclimatic regions. These results suggest that helminths form nested subsets across the archipelago due to broad-scale processes that reflect the overall lineages of their mammalian hosts; however, at the regional scale, environmental processes related to nestedness of their habitats drive parasite community nestedness.


Helminths Bats Japan Nestedness Community structure 



The authors would like to thank D.M. Courtney for her help in collecting literature for the dataset. We also thank G. Bell and S. Pilosof for statistical advice. Finally, the authors thank the two anonymous reviewers for their constructive comments on the manuscript. This work was partially supported by a National Institute of Allergy and Infectious Diseases EID Research Opportunities Award to MJV (R01 AI079231-01) and the Israel Science Foundation (grant 146/17 to BRK and ISK). EMW was supported by the Fulbright Foundation (USIEF postdoctoral fellowship), the Swiss Institute for Dryland Environmental and Energy Research and the Blaustein Center for Scientific Cooperation (Blaustein postdoctoral fellowship). LVDM was supported by the Blaustein Center for Scientific Cooperation and the French Associates for Agriculture and Biotechnology of the Drylands. This is publication 960 of the Mitrani Department of Desert Ecology.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

436_2018_5844_MOESM1_ESM.docx (39 kb)
ESM 1 (DOCX 39 kb)


  1. Abu Baker M, Patterson BD (2011) Patterns in the local assembly of Egyptian rodent faunas: co-occurrence and nestedness. J Arid Environ 75:14–19. CrossRefGoogle Scholar
  2. Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. CrossRefGoogle Scholar
  3. Andrén H (1994) Can one use nested subset pattern to reject the random sample hypothesis—examples from boreal bird communities. Oikos 70:489–491. CrossRefGoogle Scholar
  4. Barclay RMR, Harder LD (2003) Life histories of bats: life in the slow lane. In: Kunz TH, Fenton MB (eds) Bat ecology. University of Chicago Press, Chicago, pp 209–253Google Scholar
  5. Beckett SJ, Boulton CA, Williams HT (2014) FALCON: a software package for analysis of nestedness in bipartite networks. F1000 Res 3:185. Google Scholar
  6. de Bellocq JG, Sara M, Casanova JC, Feliu C, Morand S (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitol Res 90:64–70. PubMedGoogle Scholar
  7. Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449CrossRefGoogle Scholar
  8. Brown JH, Fox BJ, Kelt DA (2000) Assembly rules: desert rodent communities are structured at scales from local to continental. Am Nat 156:314–321. CrossRefPubMedGoogle Scholar
  9. Calmé S, Desrochers A (1999) Nested bird and micro-habitat assemblages in a peatland archipelago. Oecologia 118:361–370. CrossRefPubMedGoogle Scholar
  10. Coggins JR, Tedesco JL, Rupprecht CE (1982) Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte), in a Wisconsin hibernaculum. Am Midl Nat 107:305–315. CrossRefGoogle Scholar
  11. Cook RR, Quinn JF (1995) The influence of colonization in nested species subsets. Oecologia 102:413–424. CrossRefPubMedGoogle Scholar
  12. Cutler AH (1994) Nested biotas and biological conservation—metrics, mechanisms, and meaning of nestedness. Landsc Urban Plan 28:73–82. CrossRefGoogle Scholar
  13. Darlington P Jr (1957) Zoogeography: the geographical distribution of animals. Wiley, HobokenGoogle Scholar
  14. Drakare S, Lennon JJ, Hillebrand H (2006) The imprint of the geographical, evolutionary and ecological context on species–area relationships. Ecol Lett 9:215–227CrossRefPubMedGoogle Scholar
  15. Esslinger JH (1973) Genus Litomosoides Chandler, 1931 (Filarioidea-Onchocercidae) in Colombian bats and rats. J Parasitol 59:225–246. CrossRefPubMedGoogle Scholar
  16. Fahrig L (2002) Effect of habitat fragmentation on the extinction threshold: a synthesis. Ecol Appl 12:346–353Google Scholar
  17. Fellis K, Esch G (2005) Variation in life cycle affects the distance decay of similarity among bluegill sunfish parasite communities. J Parasitol 91:1484–1486. CrossRefPubMedGoogle Scholar
  18. Ficetola GF, De Bernardi F (2004) Amphibians in a human-dominated landscape: the community structure is related to habitat features and isolation. Biol Conserv 119:219–230. CrossRefGoogle Scholar
  19. Fox BJ, Kirkland GL (1992) An assembly rule for functional-groups applied to North American soricid communities. J Mammal 73:491–503. CrossRefGoogle Scholar
  20. González M, Oliva M (2009) Is the nestedness of metazoan parasite assemblages of marine fishes from the southeastern Pacific coast a pattern associated with the geographical distributional range of the host? Parasitology 136:401–409CrossRefPubMedGoogle Scholar
  21. González MT, Poulin R (2005) Nested patterns in parasite component communities of a marine fish along its latitudinal range on the Pacific coast of South America. Parasitology 131:569–577. CrossRefPubMedGoogle Scholar
  22. Gotelli NJ, Ellison AM (2002) Assembly rules for New England ant assemblages. Oikos 99(3):591–599CrossRefGoogle Scholar
  23. Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc R Soc Lond B 272:1059–1066. CrossRefGoogle Scholar
  24. Higgins CL, Willig MR, Strauss RE (2006) The role of stochastic processes in producing nested patterns of species distributions. Oikos 114:159–167CrossRefGoogle Scholar
  25. Honnay O, Hermy M, Coppin P (1999) Nested plant communities in deciduous forest fragments: species relaxation or nested habitats? Oikos 84:119–129. CrossRefGoogle Scholar
  26. Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SAJ, de Meester L, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM, Mazzeo N, Iglesias C, Reizenstein M, Malmquist HJ, Liu Z, Balayla D, Lazzaro X (2010) Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90. CrossRefGoogle Scholar
  27. Jones KE, MacLarnon A (2001) Bat life histories: testing models of mammalian life-history evolution. Evol Ecol Res 3:465–476Google Scholar
  28. Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781. CrossRefPubMedGoogle Scholar
  29. Kelt DA, Rogovin K, Shenbrot G, Brown JH (1999) Patterns in the structure of Asian and North American desert small mammal communities. J Biogeogr 26:825–841. CrossRefGoogle Scholar
  30. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Koppen-Geiger climate classification updated. Meteorol Z 15:259–263. CrossRefGoogle Scholar
  31. Kruess A (2003) Effects of landscape structure and habitat type on a plant-herbivore-parasitoid community. Ecography 26(3):283–290CrossRefGoogle Scholar
  32. Kunz TH, Fenton MB (2005) Bat ecology. University of Chicago Press, ChicagoGoogle Scholar
  33. Laurance WF, Yensen E (1991) Predicting the impacts of edge effects in fragmented habitats. Biol Conserv 55:77–92CrossRefGoogle Scholar
  34. Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91(1):3–17CrossRefGoogle Scholar
  35. Lotz J, Bush A, Font W (1995) Recruitment-driven, spatially discontinuous communities - a null model for transferred patterns in target communities of intestinal helminths. J Parasitol 81:12–24. CrossRefPubMedGoogle Scholar
  36. McCay TS, Lovallo MJ, Ford WM, Menzel MA (2004) Assembly rules for functional groups of North American shrews: effects of geographic range and habitat partitioning. Oikos 107:141–147. CrossRefGoogle Scholar
  37. Millien-Parra V, Jaeger JJ (1999) Island biogeography of the Japanese terrestrial mammal assemblages: an example of a relict fauna. J Biogeogr 26:959–972. CrossRefGoogle Scholar
  38. Moreno T, Wallis SR, Kojima T, Gibbons W (2016) The geology of Japan. Geological Society of London, LondonCrossRefGoogle Scholar
  39. Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T (2009) The wild mammals of Japan. Shoukadoh Book Sellers, KyotoGoogle Scholar
  40. Patterson BD (1999) Contingency and determinism in mammalian biogeography: the role of history. J Mammal 80:345–360. CrossRefGoogle Scholar
  41. Patterson BD, Atmar W (1986) Nested subsets and the structure of insular mammalian faunas and archipelagoes. Biol J Linn Soc 28:65–82. CrossRefGoogle Scholar
  42. Patterson BD, Brown JH (1991) Regionally nested patterns of species composition in granivorous rodent assemblages. J Biogeogr 18:395–402. CrossRefGoogle Scholar
  43. Patterson BD, Dick CW, Dittmar K (2009) Nested distributions of bat flies (Diptera: Streblidae) on Neotropical bats: artifact and specificity in host-parasite studies. Ecography 32:481–487. CrossRefGoogle Scholar
  44. Pavoine S, Dolédec S (2005) The apportionment of quadratic entropy: a useful alternative for partitioning diversity in ecological data. Environ Ecol Stat 12(2):125–138CrossRefGoogle Scholar
  45. Pavoine S, Marcon E, Ricotta C (2016) Equivalent numbers for species, phylogenetic or functional diversity in a nested hierarchy of multiple scales. Meth Ecol Evol 7:1152–1163.
  46. Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299. CrossRefPubMedGoogle Scholar
  47. Porter WP, Budaraju S, Stewart WE, Ramankutty N (2000) Calculating climate effects on birds and mammals: impacts on biodiversity, conservation, population parameters, and global community structure. Am Zool 40:597–630.[0597:cceoba];2Google Scholar
  48. Presley SJ (2007) Streblid bat fly assemblage structure on Paraguayan Noctilio leporinus (Chiroptera : Noctilionidae): nestedness and species co-occurrence. J Trop Ecol 23:409–417. CrossRefGoogle Scholar
  49. Presley SJ (2011) Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos 120:832–841. CrossRefGoogle Scholar
  50. R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  51. Rautenbach A, Dickerson T, Schoeman MC (2014) Diversity of rodent and shrew assemblages in different vegetation types of the savannah biome in South Africa: no evidence for nested subsets or competition. Afr J Ecol 52:30–40. CrossRefGoogle Scholar
  52. Sanders NJ, Gotelli NJ, Wittman SE, Ratchford JS, Ellison AM, Jules ES (2007) Assembly rules of ground-foraging ant assemblages are contingent on disturbance, habitat and spatial scale. J Biogeography 34(9):1632–1641CrossRefGoogle Scholar
  53. Schell SC (1985) Handbook of trematodes of North America north of Mexico. Idaho Research Foundation, MoscowGoogle Scholar
  54. Shahan JL, Goodwin BJ, Rundquist BC (2017) Grassland songbird occurrence on remnant prairie patches is primarily determined by landscape characteristics. Landsc Ecol 32:971–988. CrossRefGoogle Scholar
  55. Šimková A, Sitko J, Okulewicz J, Morand S (2003) Occurrence of intermediate hosts and structure of digenean communities of the black-headed gull, Larus ridibundus (L.) Parasitology 126:69–78. CrossRefPubMedGoogle Scholar
  56. Spickett A, Junker K, Krasnov BR, Haukisalmi V, Matthee S (2017) Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa. Parasitology 144:1211–1220. CrossRefPubMedGoogle Scholar
  57. Stier AC, Hanson KM, Holbrook SJ, Schmitt RJ, Brooks AJ (2014) Predation and landscape characteristics independently affect reef fish community organization. Ecology 95:1294–1307. CrossRefPubMedGoogle Scholar
  58. Timi JT, Poulin R (2008) Different methods, different results: temporal trends in the study of nested subset patterns in parasite communities. Parasitology 135:131–138. CrossRefPubMedGoogle Scholar
  59. Van Der Mescht L, Krasnov BR, Matthee CA, Matthee S (2016) Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity. Parasitology 143:1268–1278CrossRefGoogle Scholar
  60. Vickery W, Poulin R (2002) Can helminth community patterns be amplified when transferred by predation from intermediate to definitive hosts? J Parasitol 88:650–656CrossRefPubMedGoogle Scholar
  61. Wang JP (2011) SPECIES: an R package for species richness estimation. J Stat Softw 40:1–15CrossRefGoogle Scholar
  62. Warburton EM, Kohler SL, Vonhof MJ (2016) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance-decay in a bat-helminth system. Oikos 125:374–385. CrossRefGoogle Scholar
  63. Wright DH, Reeves JH (1992) On the meaning and measurement of nestedness of species assemblages. Oecologia 92:416–428. CrossRefPubMedGoogle Scholar
  64. Wright DH, Patterson BD, Mikkelson GM, Cutler A, Atmar W (1998) A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20CrossRefGoogle Scholar
  65. Zelmer DA, Arai HP (2004) Development of nestedness: host biology as a community process in parasite infracommunities of yellow perch (Perca flavescens (Mitchill)) from Garner Lake, Alberta. J Parasitol 90:435–436. CrossRefPubMedGoogle Scholar
  66. Zelmer DA, Paredes-Calderón L, León-Règagnon V, García-Prieto L (2004) Nestedness in colonization-dominated systems: helminth infracommunities of Rana vaillanti brocchi (Anura : Ranidae) in Los Tuxtlas, Veracruz, Mexico. J Parasitol 90:705–710. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Elizabeth M. Warburton
    • 1
  • Luther Van Der Mescht
    • 1
    • 2
  • Irina S. Khokhlova
    • 2
  • Boris R. Krasnov
    • 1
  • Maarten J. Vonhof
    • 3
    • 4
  1. 1.Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben GurionIsrael
  2. 2.Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben-GurionIsrael
  3. 3.Department of Biological SciencesWestern Michigan UniversityKalamazooUSA
  4. 4.Institute of the Environment and SustainabilityWestern Michigan UniversityKalamazooUSA

Personalised recommendations