Life-cycle mediated effects of urbanization on parasite communities in the estuarine fish, Fundulus heteroclitus

English version

Autoři: James M. Alfieri ^aff001; Tavis K. Anderson ^aff002
Působiště autorů: Ecology and Evolutionary Biology Interdisciplinary PhD Program, Texas A&M University, College Station, TX, United States of America ^aff001; Virus and Prion Research Unit, National Animal Disease Center, USDA—ARS, Ames, IA, United States of America ^aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225896

Souhrn

This study examined the relationship between urbanization and parasite community structure in the estuarine fish, Fundulus heteroclitus. We measured landscape and physicochemical factors associated with urbanization at 6 sites from 4 collection periods. Concurrently, we quantified the metazoan parasite community in F. heteroclitus collected at those sites, with 105 fish studied per site during the 4 collection periods. Parasite community composition differed among sites. Host size was the most important variable for direct life-cycle parasite assemblages and indirect life-cycle parasites at the individual fish level, while landscape and physicochemical factors determined the structure of indirect life-cycle parasite assemblages at the population scale. Variation in the prevalence and intensity of infection of two indirect life-cycle parasites, Lasiocotus minutus and Glossocercus caribaensis, were the primary parasites that drove differences across sites. Variation in the presence/absence of these indirect life-cycle parasite species was associated with sediment Ni concentrations, patch density, and marsh size. Our data support the hypothesis that urbanization, acting at both landscape and physicochemical scales, can have a significant impact on parasite community structure. This, however, varied by parasite life history: there was little effect of urbanization on the prevalence and intensity of direct life-cycle parasites, but significant variation was detected for indirect life-cycle parasites. This study demonstrates how anthropogenically driven landscape change influences fine-scale population dynamics of parasites.

Klíčová slova:

Parasitic diseases – Screening guidelines – Community structure – Islands – Sediment – Estuaries – Parasitic life cycles – Marshes

Zdroje

1. Lowe MR, Peterson MS. Effects of Coastal Urbanization on Salt-Marsh Faunal Assemblages in the Northern Gulf of Mexico. Marine and Coastal Fisheries. 2014;6: 89–107. doi: 10.1080/19425120.2014.893467

2. Lerberg SB, Holland AF, Sanger DM. Responses of tidal creek macrobenthic communities to the effects of watershed development. Estuaries. 2000;23: 838. doi: 10.2307/1353001

3. Anderson TK, Sukhdeo MVK. Abiotic versus biotic hierarchies in the assembly of parasite populations. Parasitology. 2010;137: 743–754. doi: 10.1017/S0031182009991430 20025818

4. Blanar CA, Marcogliese DJ, Couillard CM. Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitol (Praha). 2011;58: 240–248.

5. Anderson TK, Sukhdeo MVK. The relationship between community species richness and the richness of the parasite community in Fundulus heteroclitus. J Parasitol. 2013;99: 391–396. doi: 10.1645/GE-2940.1 23198795

6. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 1997;83: 575–583. 9267395

7. Dugarov ZN, Baldanova DR, Khamnueva TR. Impact of the degree of urbanization on composition and structure of helminth communities in the Mongolian racerunner (Eremias argus) Peters, 1869. J Helminthol. 2018;92: 178–186. doi: 10.1017/S0022149X17000268 28349852

8. Calegaro-Marques C, Amato SB. Urbanization breaks up host-parasite interactions: a case study on parasite community ecology of rufous-bellied thrushes (Turdus rufiventris) along a rural-urban gradient. PLoS One. 2014;9: e103144. doi: 10.1371/journal.pone.0103144 25068271

9. Blanar CA, Hewitt M, McMaster M, Kirk J, Wang Z, Norwood W, et al. Parasite community similarity in Athabasca River trout-perch (Percopsis omiscomaycus) varies with local-scale land use and sediment hydrocarbons, but not distance or linear gradients. Parasitol Res. 2016;115: 3853–3866. doi: 10.1007/s00436-016-5151-x 27314231

10. Anderson TK, Sukhdeo MVK. Qualitative community stability determines parasite establishment and richness in estuarine marshes. PeerJ. 2013;1: e92. doi: 10.7717/peerj.92 23802092

11. Hechinger RF, Lafferty KD, Huspeni TC, Brooks AJ, Kuris AM. Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia. 2007;151: 82–92. doi: 10.1007/s00442-006-0568-z 17024376

12. Hudson PJ, Dobson AP, Lafferty KD. Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol (Amst). 2006;21: 381–385. doi: 10.1016/j.tree.2006.04.007 16713014

13. Arneberg P, Skorping A, Grenfell B, Read AF. Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B. 1998;265: 1283–1289. doi: 10.1098/rspb.1998.0431

14. Nunn CL, Altizer S, Jones KE, Sechrest W. Comparative tests of parasite species richness in primates. Am Nat. 2003;162: 597–614. doi: 10.1086/378721 14618538

15. Hussain S, Ram MS, Kumar A, Shivaji S, Umapathy G. Human presence increases parasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in Southern India. PLoS One. 2013;8: e63685. doi: 10.1371/journal.pone.0063685 23717465

16. Bradley CA, Altizer S. Urbanization and the ecology of wildlife diseases. Trends Ecol Evol (Amst). 2007;22: 95–102. doi: 10.1016/j.tree.2006.11.001 17113678

17. Johnson DS, Fleeger JW, Deegan LA. Large-scale manipulations reveal that top-down and bottom-up controls interact to alter habitat utilization by saltmarsh fauna. Mar Ecol Prog Ser. 2009;377: 33–41. doi: 10.3354/meps07849

18. Schotthoefer AM, Rohr JR, Cole RA, Koehler AV, Johnson CM, Johnson LB, et al. Effects of wetland vs. landscape variables on parasite communities of Rana pipiens: links to anthropogenic factors. Ecol Appl. 2011;21: 1257–1271. doi: 10.1890/10-0374.1 21774428

19. Chapman JM, Marcogliese DJ, Suski CD, Cooke SJ. Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat quality. Ecol Indic. 2015;57: 564–572. doi: 10.1016/j.ecolind.2015.05.013

20. Johnson PTJ, Wood CL, Joseph MB, Preston DL, Haas SE, Springer YP. Habitat heterogeneity drives the host-diversity-begets-parasite-diversity relationship: evidence from experimental and field studies. Ecol Lett. 2016;19: 752–761. doi: 10.1111/ele.12609 27147106

21. Paul MJ, Meyer JL. Streams in the Urban Landscape. Annu Rev Ecol Syst. 2001;32: 333–365. doi: 10.1146/annurev.ecolsys.32.081501.114040

22. Lotrich VA. Summer home range and movements of Fundulus heteroclitus (Pisces: Cyprinodontidae) in a tidal creek. Ecology. 1975;56: 191–198. doi: 10.2307/1935311

23. Teo SLH, Able KW. Habitat use and movement of the mummichog (Fundulus heteroclitus) in a restored salt marsh. Estuaries. 2003;26: 720–730. doi: 10.1007/BF02711983

24. Federal standards and procedures for the National Watershed Boundary Dataset (WBD). 4th ed. Reston, VA: U.S. Geological Survey; 2013. Report No.: 11-A3.

25. Yang L, Jin S, Danielson P, Homer C, Gass L, Bender SM, et al. A new generation of the United States National Land Cover Database: Requirements, research priorities, design, and implementation strategies. ISPRS Journal of Photogrammetry and Remote Sensing. 2018;146: 108–123. doi: 10.1016/j.isprsjprs.2018.09.006

26. NOAA Office for Coastal Management. Coastal Change Analysis Program (C-CAP) Regional Land Cover. National Oceanic and Atmospheric Administration, Office for Coastal Management;

27. McGarigal K, Marks BJ. FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station; 1995. doi: 10.2737/PNW-GTR-351

28. Valiela I, Wright JE, Teal JM, Volkmann SB. Growth, production and energy transformations in the salt-marsh killifish Fundulus heteroclitus. Mar Biol. 1977;40: 135–144. doi: 10.1007/BF00396259

29. Abraham BJ. Species Profiles. Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates (Mid-Atlantic). Mummichog and Striped Killifish. 1985.

30. Kneib RT. The Role of Fundulus heteroclitus in Salt Marsh Trophic Dynamics. Am Zool. 1986;26: 259–269. doi: 10.1093/icb/26.1.259

31. Anderson TK, Sukhdeo MVK. Host centrality in food web networks determines parasite diversity. PLoS One. 2011;6: e26798. doi: 10.1371/journal.pone.0026798 22046360

32. Harris CE, Vogelbein WK. Parasites of Mummichogs, Fundulus heteroclitus, from the York River, Virginia, U.S.A., with a Checklist of Parasites of Atlantic Coast Fundulus Spp. Comp Parasitol. 2006;73: 72–110. doi: 10.1654/41716.1

33. Stunkard HW. The morphology, life history, and systematic relations of Lasiotocus elongatus (Manter, 1931)(Trematoda: Digenea). Biol Bull. 1981;160: 155–160. doi: 10.2307/1540909

34. Ortega-Olivares MP, García-Prieto L, García-Varela M. Gryporhynchidae (Cestoda: Cyclophyllidea) in Mexico: species list, hosts, distribution and new records. Zootaxa. 2014;3795: 101–125. doi: 10.11646/zootaxa.3795.2.1 24870465

35. Dove ADM, Cribb TH. Species accumulation curves and their applications in parasite ecology. Trends Parasitol. 2006;22: 568–574. doi: 10.1016/j.pt.2006.09.008 17035087

36. Khalil LF. Order Cyclophyllidea (diagnosis and key to families). Key to the cestode parasites of vertebrates. Wallingford, UK: CAB International; 1994.

37. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.5–6 [Internet]. 2019. Available: https://CRAN.R-project.org/package=vegan

38. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2019. Available: https://www.R-project.org

39. Ishwaran H, Kogalur U. Fast Unified Random Forests for Survival, Regression, andClassification (RF-SRC). 2019.

40. Breiman L. Random Forests. Springer Science and Business Media LLC. 2001; doi: 10.1023/a:1010933404324

41. Eldridge A, Guyot P, Moscoso P, Johnston A, Eyre-Walker Y, Peck M. Sounding out ecoacoustic metrics: Avian species richness is predicted by acoustic indices in temperate but not tropical habitats. Ecol Indic. 2018;95: 939–952. doi: 10.1016/j.ecolind.2018.06.012

42. Miller K, Huettmann F, Norcross B, Lorenz M. Multivariate random forest models of estuarine-associated fish and invertebrate communities. Mar Ecol Prog Ser. 2014;500: 159–174. doi: 10.3354/meps10659

43. Buchman MF. Screening Quick Reference Tables (SQuiRTs). 2008;

44. Cempel M. Nickel: A Review of Its Sources and Environmental Toxicology. Polish Journal of Environmental Studies. 2006;

45. Field LJ, MacDonald DD, Norton SB, Ingersoll CG, Severn CG, Smorong D, et al. Predicting amphipod toxicity from sediment chemistry using logistic regression models. Environ Toxicol Chem. 2002;21: 1993–2005. doi: 10.1002/etc.5620210929 12206441

46. Guest MA, Connolly RM. Movement of carbon among estuarine habitats: the influence of saltmarsh patch size. Mar Ecol Prog Ser. 2006;310: 15–24. doi: 10.3354/meps310015

47. Peterson MS, Lowe MR. Implications of cumulative impacts to estuarine and marine habitat quality for fish and invertebrate resources. Reviews in Fisheries Science. 2009;17: 505–523. doi: 10.1080/10641260903171803

48. Partyka ML, Peterson MS. Habitat Quality and Salt-Marsh Species Assemblages along an Anthropogenic Estuarine Landscape. Journal of Coastal Research. 2008;246: 1570–1581. doi: 10.2112/07-0937.1

49. Layman CA, Quattrochi JP, Peyer CM, Allgeier JE. Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett. 2007;10: 937–944. doi: 10.1111/j.1461-0248.2007.01087.x 17845294

50. Rudershausen PJ, Merrell JH, Buckel JA. Fragmentation of habitat affects communities and movement of nekton in salt marsh tidal creeks. Mar Ecol Prog Ser. 2018;586: 57–72. doi: 10.3354/meps12385

51. Anderson TK, Sukhdeo MVK. The worm’s eye view of community ecology. A Century of Parasitology: Discoveries, ideas and lessons learned by scientists who published in the Journal of Parastiology, 1914–2014. Chichester, UK: John Wiley & Sons, Ltd; 2016. pp. 110–130. doi: 10.1002/9781118884799.ch8

52. Mooring MS. Animal Grouping for Protection from Parasites: Selfish Herd and Encounter-Dilution Effects. Behaviour. 1992;123: 173–193.

53. Sousa WP. Spatial scale and the processes structuring a guild of larval trematode parasites. In: Esch GW, Bush AO, Aho JM, editors. Parasite communities: patterns and processes. Dordrecht: Springer Netherlands; 1989. pp. 41–67. doi: 10.1007/978-94-009-0837-6_3

54. Byers JE, Malek AJ, Quevillon LE, Altman I, Keogh CL. Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos. 2015;124: 1511–1519. doi: 10.1111/oik.02088

55. Kuris AM, Blaustein AR, Alio JJ. Hosts as Islands. Am Nat. 1980;116: 570–586. doi: 10.1086/283647

56. MacArthur RH, Wilson EO. An equilibrium theory of insular zoogeography. Evolution. 1963;17: 373–387. doi: 10.1111/j.1558-5646.1963.tb03295.x

57. Guégan J-F, Lambert A, Lévêque C, Combes C, Euzet L. Can host body size explain the parasite species richness in tropical freshwater fishes? Oecologia. 1992;90: 197–204. doi: 10.1007/BF00317176 28313714

58. Morand S, Poulin R. Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology. 1998;12: 717–727. doi: 10.1023/A:1006537600093

59. Blanar CA, Munkittrick KR, Houlahan J, Maclatchy DL, Marcogliese DJ. Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquat Toxicol. 2009;93: 18–28. doi: 10.1016/j.aquatox.2009.03.002 19349083

Life-cycle mediated effects of urbanization on parasite communities in the estuarine fish, Fundulus heteroclitus

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