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Long-term changes in mole cricket body size associated with enemy-free space and a novel range

  • Pablo E. AllenEmail author
  • Larissa Laforest
  • Sonia I. Diyaljee
  • Hailee M. Smith
  • Dieu X. Tran
  • Alex M. Winsor
  • Adam G. Dale
Original Paper

Abstract

Exotic species can cause ecosystem and landscape-level changes in their novel ranges, but factors associated with novel ranges can also change the invaders. By tracking trait changes over space and time, we can learn about the future ecological and economic implications of invasive species’ dispersal. Here, we investigated body size changes of two invasive mole cricket species, Neoscapteriscus borellii and N. vicinus, introduced to the U.S. from South America (≈ 1904) without natural enemies, and later exposed to them (≈ 1980) through classical biological control. We compared body sizes of N. vicinus and N. borellii in the novel range from before biological control and 30 years after, as well as N. borellii in its native range at the same time period. Contrary to expectations, our data suggest that N. borellii and N. vicinus body sizes have increased since re-establishment of interactions with their natural enemies. Our results also suggest that N. borellii body size decreased in enemy-free space after U.S. invasion and prior to biological control. Selection or reduced intraspecific competition, both likely associated with biological control, may explain the changes in body size over time. Although these results warrant further research, they provide valuable insights into the long-term effects of invasion and classical biological control.

Keywords

Enemy release hypothesis Density-dependence Entomopathogenic nematodes Invasive species Parasitism 

Notes

Acknowledgements

We sincerely thank the Florida farm managers for their cooperation during this study. Christine W. Miller and Anne Donnelly provided critical assistance in the initiation of this project and the mechanisms by which the data were collected. We thank J. Howard Frank and Thomas J. Walker, who both provided valuable insight and input, which were highly valuable for the design and methodology used in this study. We also thank Tim Forrest, who provided his raw data collected in the 1980s from a previous publication, which played a key role in this study. Nicole Benda, Rebecca Perry, and Alex LoCastro each provided essential help with field work and data collection. We thank Barukh Rohde, Avraham Brun-Kestler, and Custom Engineered Solutions for acoustic trap development and maintenance. Funding for this work was provided by United States Department of Agriculture-National Institute of Food and Agriculture Grant 2016-38,503-25899 to AGD, and the University of Florida Agricultural Experiment Station.

Supplementary material

10530_2019_2127_MOESM1_ESM.docx (3.4 mb)
Supplementary material 1 (DOCX 3449 kb)

References

  1. Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352PubMedCrossRefPubMedCentralGoogle Scholar
  2. Beugnon G (1981) Orientation of Southern mole cricket, Scapteriscus acletus, landing at a sound source. Fla Entomol 64:463–468CrossRefGoogle Scholar
  3. Blankenhorn W, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol 44:413–424CrossRefGoogle Scholar
  4. Boff MIC, Wiegers GL, Smits PH (2000) Influences of host size and host species on the infectivity and development of Heterorhabditis megidis (strain NLH-E87.3). Biocontrol 45:469–482CrossRefGoogle Scholar
  5. Calsbeek R, Smith TB (2007) Probing the adaptive landscape using experimental islands: density-dependent natural selection on lizard body size. Evolution 61:1052–1061PubMedCrossRefPubMedCentralGoogle Scholar
  6. Campbell TS, Echternacht AC (2003) Introduced species as moving targets: changes in body sizes of introduced lizards following experimental introductions and historical invasions. Biol Invasions 5:193–212CrossRefGoogle Scholar
  7. De Graaf J, Schoeman AS, Brandenburg RL (2004) Seasonal development of Gryllotalpa africana (Orthoptera: Gryllotalpidae) on turfgrass in South Africa. Fla Entomol 87:130–136CrossRefGoogle Scholar
  8. Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470–474PubMedCrossRefPubMedCentralGoogle Scholar
  9. Dillman AR, Sternberg PW (2012) Entomopathogenic nematodes. Curr Biol 22:R430–R431PubMedPubMedCentralCrossRefGoogle Scholar
  10. Dillman AR, Cronin CJ, Tang J, Gray DA, Sternberg PW (2014) A modified mole cricket lure and description of Scapteriscus borellii (Orthoptera: Gryllotalpidae) range expansion and calling song in California. Environ Entomol 43:146–156PubMedPubMedCentralCrossRefGoogle Scholar
  11. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefPubMedCentralGoogle Scholar
  12. Dong N, Beck HW (1982) Mark-release of sound-attracted mole crickets: flight behavior and implications for control. Fla Entomol 65:531–538CrossRefGoogle Scholar
  13. Dunn AM, Torchin ME, Hatcher MJ, Kotanen PM, Blumenthal DM, Byers JE, Coon CAC, Frankel VM, Holt RD, Hufbauer RA, Kanarek AR, Schierenbeck KA, Wolfe LM, Perkins SE (2012) Indirect effects of parasites in invasions. Funct Ecol 26:1262–1274CrossRefGoogle Scholar
  14. Forrest TG (1980) Phonotaxis in mole crickets: its reproductive significance. Fla Entomol 63:45–53CrossRefGoogle Scholar
  15. Forrest TG (1986) Oviposition and maternal investment in mole crickets (Orthoptera: Gryllotalpidae): effects of season, size, and senescence. Ann Entomol Soc Am 79:918–924CrossRefGoogle Scholar
  16. Forrest TG (1987) Insect size tactics and developmental strategies. Oecologia 73:178–184PubMedCrossRefPubMedCentralGoogle Scholar
  17. Fowler CW (1981) Density dependence as related to life history strategy. Ecology 62:602–610CrossRefGoogle Scholar
  18. Fowler HG (1987) Geographic variation in the flight periodicity of New World mole crickets. Biol Rhythm Res 18:283–286Google Scholar
  19. Frank JH, Walker TJ (2006) Permanent control of pest mole crickets (Orthoptera: Gryllotalpidae: Scapteriscus) in Florida. Am Entomol 52:38–144CrossRefGoogle Scholar
  20. Frank JH, Parkman JP, Bennett FD (1995) Larra bicolor (Hymenoptera: Sphecidae), a biological control agent of Scapteriscus mole crickets (Orthoptera: Gryllotalpidae), established in northern Florida. Fla Entomol 78:619–623CrossRefGoogle Scholar
  21. Frank JH, Walker TJ, Parkman JP (1996) The introduction, establishment, and spread of Ormia depleta in Florida. Biol Control 6:368–377CrossRefGoogle Scholar
  22. Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152CrossRefGoogle Scholar
  23. Hayslip NC (1943) Notes on biological studies of mole crickets at Plant City, Florida. Fla Entomol 26:33–46CrossRefGoogle Scholar
  24. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309PubMedCrossRefPubMedCentralGoogle Scholar
  25. iNaturalist.org (2018) iNaturalist research-grade observations. Occurrence dataset  https://doi.org/10.15468/ab3s5x. Accessed via www.GBIF.org on 2018-07-11
  26. Johnson PT, De Roode JC, Fenton A (2015) Why infectious disease research needs community ecology. Science 349:1259504PubMedPubMedCentralCrossRefGoogle Scholar
  27. Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48PubMedCrossRefPubMedCentralGoogle Scholar
  28. Lutz FE (1908) The variation and correlations of certain taxonomic characters of Gryllus. Carnegie Inst. Wash. Publ. No. 101Google Scholar
  29. Masson L, Masson G, Beisel JN, Gutowsky LFG, Fox MG (2018) Consistent life history shifts along invasion routes? An examination of round goby populations invading on two continents. Divers Distrib 24:841–852CrossRefGoogle Scholar
  30. Mhina GJ, Leppla NC, Thomas MH, Solís D (2016) Cost effectiveness of biological control of invasive mole crickets in Florida pastures. Biol Control 100:108–115CrossRefGoogle Scholar
  31. Mousseau T (1997) Ectotherms follow the converse to Bergmann’s rule. Evolution 51:630–632PubMedCrossRefPubMedCentralGoogle Scholar
  32. Nguyen KB, Smart GC Jr (1990) Steinernema scapterisci n. sp. (Steinernematidae: Nematoda). J Nematol 22:187–199PubMedPubMedCentralGoogle Scholar
  33. Nguyen KB, Smart GC Jr (1991) Mode of entry and sites of development of Steinernema scapterisci in mole crickets. J Nematol 23:267PubMedPubMedCentralGoogle Scholar
  34. Nickle DA (2003) A revision of the mole cricket genus Scapteriscus with the description of a morphologically similar new genus (Orthoptera: Gryllotalpidae: Scapteriscinae). Trans Am Entomol Soc 129:411–485Google Scholar
  35. Parkman JP, Hudson WG, Frank JH, Nguyen KB, Smart GC Jr (1993) Establishment and persistence of Steinernema scapterisci (Rhabditida: Steinernematidae) in field populations of Scapteriscus spp. mole crickets (Orthoptera: Gryllotalpidae). J Entomol Sci 28:182–190CrossRefGoogle Scholar
  36. Parkman JP, Frank JH, Nguyen KB, Smart GC Jr (1994) Inoculative release of Steinernema scapterisci (Rhabditida: Steinernematidae) to suppress pest mole crickets (Orthoptera: Gryllotalpidae) on golf courses. Environ Entomol 23:1331–1337CrossRefGoogle Scholar
  37. Parkman JP, Frank JH, Walker TJ, Schuster DJ (1996) Classical biological control of Scapteriscus spp. (Orthoptera: GrylIotalpidae) in Florida. Environ Entomol 25:1415–1420CrossRefGoogle Scholar
  38. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803PubMedCrossRefPubMedCentralGoogle Scholar
  39. Poulin R, Thomas F (1999) Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitol Today 15:28–32PubMedCrossRefPubMedCentralGoogle Scholar
  40. PRISM Climate Group (2018) PRISM gridded climate data. Oregon State University. http://prism.oregonstate.edu
  41. Riemer K, Anderson-Teixeira KJ, Smith FA, Harris DJ, Ernest SM (2018) Body size shifts influence effects of increasing temperatures on ectotherm metabolism. Glob Ecol Biogeogr 27:958–967CrossRefGoogle Scholar
  42. Rohde BB, Allen PE, Benda N, Brun A, Mankin RW, Dale AG (2019) An acoustic trap to survey and capture two Neoscapteriscus species. Fla Entomol 102:654–657CrossRefGoogle Scholar
  43. Saes NB, Fowler H G (1985) Life cycles of mole crickets in South America. In: Annual report: mole cricket research 84–85, issue 7, pp 58–59Google Scholar
  44. Schäfer MA, Berger D, Rohner PT, Kjaersgaard A, Bauerfeind SS, Guillaume F, Fox C, Blanckenhorn WU (2018) Geographic clines in wing morphology relate to colonization history in New World but not Old World populations of yellow dung flies. Evolution 72:1629–1644CrossRefGoogle Scholar
  45. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675PubMedPubMedCentralCrossRefGoogle Scholar
  46. Scott ME (1987) Regulation of mouse colony abundance by Heligmosomoides polygyrus. Parasitology 95:111–124PubMedCrossRefPubMedCentralGoogle Scholar
  47. Sorensen RE, Minchella DJ (2001) Snail-trematode life history interactions: past trends and future directions. Parasitology 123:3–18CrossRefGoogle Scholar
  48. Sousa WP (1983) Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. J Exp Mar Biol Ecol 73:273–296CrossRefGoogle Scholar
  49. Torchin ME, Lafftery KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345CrossRefGoogle Scholar
  50. Ulagaraj SM, Walker TJ (1973) Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182:1278–1279PubMedCrossRefPubMedCentralGoogle Scholar
  51. Volk MI, Hoctor TS, Nettles BB, Hilsenbeck R, Putz FE, Oetting J (2017) Florida land use and land cover change in the past 100 years. In: Chassingnet EP, Jones JW, Misra V, Obeysekera J (eds) Florida’s climate: changes, variations, and impacts. Florida Climate Institute, Gainesville, pp 51–82.  https://doi.org/10.17125/fci2017.ch02 CrossRefGoogle Scholar
  52. Walker TJ (1982) Sound traps for sampling mole cricket flights (Orthoptera: Gryllotalpidae: Scapteriscus). Fla Entomol 65:105–110CrossRefGoogle Scholar
  53. Walker TJ, Nickle DA (1981) Introduction and spread of pest mole crickets: Scapteriscus vicinus and S. acletus reexamined. Ann Entomol Soc Am 74:158–163CrossRefGoogle Scholar
  54. White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:303CrossRefGoogle Scholar
  55. Wilbur HM (1977) Density-dependent aspects of growth and metamorphosis in Bufo americanus. Ecology 58:196–200CrossRefGoogle Scholar
  56. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AM (2007) Parasites alter community structure. Proc Natl Acad Sci USA 104:9335–9339PubMedCrossRefPubMedCentralGoogle Scholar
  57. Xu Y, Held DW, Hu XP (2013) Dietary choices and their implication for survival and development of omnivorous mole crickets (Orthoptera: Gryllotalpidae). AppL Soil Ecol 71:65–71CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Entomology and Nematology DepartmentUniversity of FloridaGainesvilleUSA

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