Skip to main content
SpringerLink
Log in

Dispersal of a defensive symbiont depends on contact between hosts, host health, and host size

  • Highlighted Student Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Symbiont dispersal is necessary for the maintenance of defense mutualisms in space and time, and the distribution of symbionts among hosts should be intricately tied to symbiont dispersal behaviors. However, we know surprisingly little about how most defensive symbionts find and choose advantageous hosts or what cues trigger symbionts to disperse from their current hosts. In a series of six experiments, we explored the dispersal ecology of an oligochaete worm (Chaetogaster limnaei) that protects snail hosts from infection by larval trematode parasites. Specifically, we determined the factors that affected net symbiont dispersal from a current “donor” host to a new “receiver” host. Symbionts rarely dispersed unless hosts directly came in contact with one another. However, symbionts overcame their reluctance to disperse across the open environment if the donor host died. When hosts came in direct contact, net symbiont dispersal varied with both host size and trematode infection status, whereas symbiont density did not influence the probability of symbiont dispersal. Together, these experiments show that symbiont dispersal is not a constant, random process, as is often assumed in symbiont dispersal models, but rather the probability of dispersal varies with ecological conditions and among individual hosts. The observed heterogeneity in dispersal rates among hosts may help to explain symbiont aggregation among snail hosts in nature.

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
Fig. 4

Similar content being viewed by others

References

  • Altwegg R, Collingham YC, Erni B, Huntley B (2013) Density-dependent dispersal and the speed of range expansions. Divers Distrib 19:60–68

    Article  Google Scholar 

  • Anderson R, Gordon D (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398. doi:10.1017/S0031182000055347

    Article  PubMed  Google Scholar 

  • Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev 87:290–312. doi:10.1111/j.1469-185X.2011.00201.x

    Article  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev Camb Philos Soc 80:205–225. doi:10.1017/S1464793104006645

    Article  PubMed  Google Scholar 

  • Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. doi:10.1038/nrmicro2262

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brown BL, Creed RP, Skelton J, Rollins MA, Farrell KJ (2012) The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments. Oecologia 170:199–207. doi:10.1007/s00442-012-2280-5

    Article  PubMed  Google Scholar 

  • Buse, A (1968) A comparative study of the morphology, behavior and ecology of Chaetogaster limnaei (von Baer) from several host species. PhD dissertation, University of Wales

  • Buse A (1972) Behavioural aspects of the relationship of Chaetogaster limnaei (Oligochaeta: Naididae) with its gastropod host. Anim Behav 20:274–279

    Article  CAS  PubMed  Google Scholar 

  • Calow P (1978) The evolution of life-history strategies in fresh-water gastropods. Malacologia 17:351–364

    Google Scholar 

  • Castro P (1978) Movements between coral colonies in Trapezia ferruginea (Crustacea: Brachyura), an obligate symbiont of scleractinian corals. Mar Biol 46:237–245. doi:10.1007/BF00390685

    Article  Google Scholar 

  • Clay CA, Lehmer EM, Previtali A, St Jeor S, Dearing MD (2009) Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission. Proc R Soc B Biol Sci 276:1305–1312

    Article  Google Scholar 

  • Cooper C, Walters J (2002) Experimental evidence of disrupted dispersal causing decline of an Australian passerine in fragmented habitat. Conserv Biol 16:471–478. doi:10.1046/j.1523-1739.2002.00346.x

    Article  Google Scholar 

  • Cote J, Clobert J (2010) Risky dispersal: avoiding kin competition despite uncertainty. Ecology 91:1485–1493. doi:10.1890/09-0387.1

    Article  CAS  PubMed  Google Scholar 

  • Dalesman S, Rundle SD, Coleman RA, Cotton PA (2006) Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. Anim Behav 71:789–797. doi:10.1016/j.anbehav.2005.05.028

    Article  Google Scholar 

  • Daniels S, Walters J (2000) Between-year breeding dispersal in red-cockaded woodpeckers: multiple causes and estimated cost. Ecology 81:2473–2484. doi:10.1890/0012-9658(2000)081[2473:BYBDIR]2.0.CO;2

  • De Kock LL, Robinson AE (1966) Observations on a lemming movement in Jämtland, Sweden, in autumn 1963. J Mammal 47:490–499

    Article  Google Scholar 

  • Desrochers A, Hannon S (1997) Gap crossing decisions by forest songbirds during the post-fledging period. Conserv Biol 11:1204–1210. doi:10.1046/j.1523-1739.1997.96187.x

    Article  Google Scholar 

  • Dillon R (2000) The ecology of freshwater molluscs. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Edwards D, Hassall M, Sutherland W, Yu D (2006) Assembling a mutualism: ant symbionts locate their host plants by detecting volatile chemicals. Insect Soc 53:172–176. doi:10.1007/s00040-00

    Article  Google Scholar 

  • Fernandez J, Goater TM, Esch GW (1991) Population dynamics of Chaetogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). Am Midl Nat 125:195–205

    Article  Google Scholar 

  • Fred MS, Brommer JE (2009) Resources influence dispersal and population structure in an endangered butterfly. Insect Conserv Divers 2:176–182. doi:10.1111/j.1752-4598.2009.00059.x

    Article  Google Scholar 

  • Gil-Turnes MS, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118. doi:10.1126/science.2781297

    Article  CAS  PubMed  Google Scholar 

  • Glynn P (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecol Monogr 46:431–456

    Article  Google Scholar 

  • Glynn P (1983) Increased survivorship in corals harboring crustacean symbionts. Mar Biol Lett 4:105–111

    Google Scholar 

  • Glynn P (1987) Some ecological consequences of coral-crustacean guard mutualisms in the Indian and Pacific Oceans. Symbiosis 4:301–324

    Google Scholar 

  • Gruffydd LD (1965) The population biology of Chaetogaster limnaei limnaei and Chaetogaster limnaei vaghini (Oligochaeta). Br Ecol Soc 34:667–690

    Google Scholar 

  • Hay M, Parker J, Burkepile D (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu Rev Ecol Evol Syst 35:175–197. doi:10.1146/annurev.ecolsys.34.011802.132357

    Article  Google Scholar 

  • Heil M, Fiala B, Maschwitz U, Linsenmair K (2001) On benefits of indirect defence: short- and long-term studies of antiherbivore protection via mutualistic ants. Oecologia 126:395–403. doi:10.1007/S004420000532

    Article  Google Scholar 

  • Henry LM, Peccoud J, Simon JC, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013) Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol 23:1713–1717. doi:10.1016/j.cub.2013.07.029

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holland JN, DeAngelis DL, Bronstein JL (2002) Population dynamics and mutualism: functional responses of benefits and costs. Am Nat 159:231–244. doi:10.1086/338510

    Article  PubMed  Google Scholar 

  • Hopkins SR, Wyderko JA, Sheehy RR, Belden LK, Wojdak JM (2013) Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts. Ecol Evol 3:4427–4438. doi:10.1002/ece3.634

    Article  PubMed Central  PubMed  Google Scholar 

  • Ibrahim MM (2007) Population dynamics of Chaetogaster limnaei (Oligochaeta: Naididae) in the field populations of freshwater snails and its implications as a potential regulator of trematode larvae community. Parasitol Res 101:25–33. doi:10.1007/s00436-006-0436-0

    Article  PubMed  Google Scholar 

  • Janzen D (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275

    Article  Google Scholar 

  • Janzen D (1985) The natural history of mutualism. In: Boucher DH (ed) The biology of mutualism. Oxford University Press, New York, pp 40–99

    Google Scholar 

  • Khalil L (1961) On the capture and destruction of miracidia by Chaetogaster limnaei (Oligochaeta). J Helminthol 35:269–275

    Article  CAS  PubMed  Google Scholar 

  • Léna J, Clobert J, Fraipont MD, Lecomte J, Guyot G (1998) The relative influence of density and kinship on dispersal in the common lizard. Behav Ecol 9:500–507. doi:10.1093/beheco/9.5.500

    Article  Google Scholar 

  • Lindberg W, Stanton G (1989) Resource quality, dispersion and mating prospects for crabs occupying bryozoan colonies. J Exp Mar Bio Ecol 128:257–282. doi:10.1016/0022-0981(89)90031-2

    Article  Google Scholar 

  • Lloyd-Smith J, Schreiber S, Kopp P, Getz W (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359

    Article  CAS  PubMed  Google Scholar 

  • Lubin Y, Ellner S, Kotzman M (1993) Web relocation and habitat selection in desert widow spider. Ecology 74:1915–1928. doi:10.2307/1940835

    Article  Google Scholar 

  • McKoy SA, Hyslop EJ, Robinson RD (2011) Associations between two trematode parasites, an ectosymbiotic annelid, and Thiara (Tarebia) granifera (Gastropoda) in Jamaica. J Parasitol 97:828–832. doi:10.1645/GE-2494.1

    Article  PubMed  Google Scholar 

  • Mehrparvar M, Zytynska SE, Weisser WW (2013) Multiple cues for winged morph production in an aphid metacommunity. PLoS One 8:e58323. doi:10.1371/journal.pone.0058323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Negovetich N, Esch G (2008) Quantitative estimation of the cost of parasitic castration in a Helisoma anceps population using a matrix population model. J Parasitol 94:1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Okabe K, Makino S (2008) Parasitic mites as part-time bodyguards of a host wasp. Proc R Soc B Biol Sci 275:2293–2297. doi:10.1098/rspb.2008.0586

    Article  Google Scholar 

  • Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world—advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355. doi:10.1111/1365-2435.12133

    Article  Google Scholar 

  • Osman R, Haugsness J (1981) Mutualism among sessile invertebrates: a mediator of competition and predation. Science 211:846–848. doi:10.1126/science.211.4484.846

    Article  CAS  PubMed  Google Scholar 

  • Pap PL, Tökölyi J, Szép T (2005) Host–symbiont relationship and abundance of feather mites in relation to age and body condition of the barn swallow (Hirundo rustica): an experimental study. Can J Zool 83:1059–1066. doi:10.1139/z05-100

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org/

  • Rodgers JK, Sandland GJ, Joyce SR, Minchella DJ (2005) Multi-species interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata). J Parasitol 91:709–712

    Article  PubMed  Google Scholar 

  • Sankurathri C, Holmes JC (1976) Effects of thermal effluents on parasites and commensals of Physa gyrina Say (Mollusca: Gastropoda) and their interactions at Lake Wabamun, Alberta. Can J Zool 54:1742–1753

    Article  Google Scholar 

  • Schell SC (1985) Handbook of trematodes of North America: North of Mexico. University Press of Idaho, Moscow

    Google Scholar 

  • Shaw R (1992) Host tracking and photosensitivity in Chaetogaster limnaei limnaei (Oligochaeta). Can J Zool 70:578–581

    Article  Google Scholar 

  • Shigina N (1970) A contribution to the feeding of Chaetogaster limnaei and its role in the extermination of trematode larvae. Zool Zhurnal 49:673–679

    Google Scholar 

  • Smythe A, Forgrave K, Patti A, Hochberg R, Litvaitis MK (in press) Untangling the ecology, taxonomy, and evolution of the Chaetogaster limnaei (Oligochaeta: Naididae) species complex. J Parasitol

  • Stella JS, Munday PL, Jones GP (2011) Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce. Coral Reefs 30:719–727. doi:10.1007/s00338-011-0748-0

    Article  Google Scholar 

  • Stier AC, Gil MA, McKeon CS, Lemer S, Leray M, Mills SC, Osenberg CW (2012) Housekeeping mutualisms: do more symbionts facilitate host performance? PLoS One 7:e32079. doi:10.1371/journal.pone.0032079

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stoll S, Früh D, Westerwald B, Hormel N, Haase P (2013) Density-dependent relationship between Chaetogaster limnaei limnaei (Oligochaeta) and the freshwater snail Physa acuta (Pulmonata). Freshwater Sci 32:642–649. doi:10.1899/12-072.1

    Article  Google Scholar 

  • Sutherland WJ, Gill JA, Norris K (2002) Density-dependent dispersal in animals: concepts, evidence, mechanisms and consequences. In: Bullock JM, Kenwared KE, Hails RS (eds) Dispersal. Blackwell, Oxford, pp 134–151

    Google Scholar 

  • Vaghin V (1946) On the biological species of Chaetogaster limnaei K. Baer. Dokl Akad Nauk SSSR 51:481–484

    Google Scholar 

  • Walke JB, Harris RN, Reinert LK, Rollins-Smith LA, Woodhams DC (2011) Social immunity in amphibians: evidence for vertical transmission of innate defenses. Biotropica 43:396–400. doi:10.1111/j.1744-7429.2011.00787.x

    Article  Google Scholar 

  • Waser PM, Nichols KM, Hadfield JD (2013) Fitness consequences of dispersal: is leaving home the best of a bad lot? Ecology 94:1287–1295

    Article  CAS  PubMed  Google Scholar 

  • White JF, Torres MF (2009) Defensive mutualism in microbial symbiosis. CRC, Boca Raton

    Book  Google Scholar 

  • Woodhams DC, Vredenburg VT, Simon MA, Billheimer D, Shakhtour B, Shyr Y, Briggs CJ, Rollins-Smith LA, Harris RN (2007) Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol Conserv 138:390–398. doi:10.1016/j.biocon.2007.05.004

    Article  Google Scholar 

  • Zimmermann MR, Luth KE, Esch GW (2013) Shedding Patterns of Daubaylia potomaca (Nematoda: Rhabditida). J Parasitol 99:966–969. doi:10.1645/13-260.1

    Article  PubMed  Google Scholar 

  • Zohdy S, Kemp AD, Durden LA, Wright PC, Jernvall J (2012) Mapping the social network: tracking lice in a wild primate (Microcebus rufus) population to infer social contacts and vector potential. BMC Ecol 12:4. doi:10.1186/1472-6785-12-4

    Article  PubMed Central  PubMed  Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

Many thanks to J. Walters for helpful comments and discussions of the manuscript. This work was supported by National Science Foundation grants DEB-0918656 (J. M. W.) and DEB-0918960 (L. K. B.). L. J. B. was supported by a Research Experience for Undergraduates supplement to NSF DEB-0918656.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    Skylar R. Hopkins & Lisa K. Belden

  2. Biology Department, The College of William and Mary, Williamsburg, VA, USA

    Lindsey J. Boyle

  3. Department of Biology, Radford University, Radford, VA, USA

    Jeremy M. Wojdak

Authors
  1. Skylar R. Hopkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lindsey J. Boyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa K. Belden
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeremy M. Wojdak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Skylar R. Hopkins.

Additional information

Communicated by Pieter Johnson.

Symbiont dispersal among hosts is usually assumed to occur randomly, with an equal probability of dispersal among all hosts. Here, we show that symbiont dispersal rates vary with ecological conditions and among individual hosts. This non-random symbiont dispersal can help explain why symbionts are aggregated among hosts, which in turn has important consequences for symbiont–host interactions.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hopkins, S.R., Boyle, L.J., Belden, L.K. et al. Dispersal of a defensive symbiont depends on contact between hosts, host health, and host size. Oecologia 179, 307–318 (2015). https://doi.org/10.1007/s00442-015-3333-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3333-3

Keywords

Search

Navigation