Disentangling the coexistence strategies of mud-daubing wasp species through trophic analysis in oases of Baja California peninsula
Autoři:
Armando Falcón-Brindis aff001; Ricardo Rodríguez-Estrella aff001; María Luisa Jiménez aff001
Působiště autorů:
Entomology and Arachnology Laboratory (Laboratorio de Aracnología y Entomología), Conservation and Environmental Planning Program (Programa de Planeación Ambiental y Conservación), Northwest Biological Research Center (Centro de Investigaciones Biológicas
aff001; Entomology and Arachnology Laboratory (Laboratorio de Aracnología y Entomología), Conservation and Environmental Planning Program (Programa de Planeación Ambiental y Conservación), Northwest Biological Research Center (Centro de Investigaciones Biológicas
aff001
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225266
Souhrn
Species within the same trophic level show different strategies to avoid competition. Among these mechanisms, differences in body size, spatio-temporal segregation, and diet preference often leads to a niche partitioning. Nonetheless, little attention on coexisting predatory insects and their network interactions has been paid. In this study, we analyzed the strategies to avoid competition among three sympatric mud-daubing wasps of the genus Trypoxylon (Hymenoptera: Crabronidae) in oases and their surrounding xeric area from the Baja California peninsula, Mexico. We compared the prey richness, composition and proportion of spider guilds that were captured by the wasps. We tested whether the differences in wasp body size explained the niche breadth, niche overlap and the size of spider prey. We assessed the spider-wasp interactions through a network analysis. With the use of trap-nests, we collected 52 spider species captured by the wasps. Both the guild and species composition of preyed spiders was different between the three wasp species. Differential proportions in the capture of spider guilds and a little diet overlap were found among the wasp species. We found that the wasp body size was positively correlated with prey size, but it was not a proxy of niche breadth. Moreover, the largest wasp species was able to nest in both mesic and xeric habitats, while the two smaller species were restricted to the oases. This study reveals that the diversity of spiders in oases of Baja California peninsula is crucial to maintain highly specialized oasis-dependent wasp species. The niche partitioning between mud-daubing wasps can be shaped by their inherent body size limitations and hunting strategies through foraging specialization for specific spider guilds. Food selection and slight differences in body size reduce competition and allow the coexistence of sympatric wasps. Our study is the first approach exploring the interaction networks between mud-daubing wasps and their spider preys, highlighting new insights into the morphological and ecological factors that shape antagonistic interactions, and allow the coexistence of predators in deserts.
Klíčová slova:
Physiological parameters – Spiders – Species diversity – Trophic interactions – Predation – Ecological niches – Deserts – Spider webs
Zdroje
1. Cornell H. Niche overlap. In A Hastings Gross LJ, editors. Encyclopedia of Theoretical Ecology. California: University of California Press; 2012. p. 489–498.
2. Clewlow HL, Takahashi A, Watanabe S, Votier SC, Downie R, Ratcliffe N. Niche partitioning of sympatric penguins by leapfrog foraging appears to be resilient to climate change. J Anim Ecol. 2018; 00:1–13. https://doi.org/10.1111/1365-2656.12919 29235116
3. MacArthur RH, Levins R. The limiting similarity, convergence, and divergence of coexisting species. Am Nat. 1967; 101: 377–385.
4. Bolnick DI. Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature. 2001; 410: 463–466. doi: 10.1038/35068555 11260712
5. Yu DW, Wilson HB, Frederickson ME, Palominos W, De La Colina R, Edwars DP, Balareso AA. Experimental demonstration of species coexistence enabled by dispersal limitation. J Anim Ecol. 2004; 73: 1102–1114. https://doi.org/10.1111/j.0021-8790.2004.00877.x
6. Sexton JP, Montiel J, Shay JE, Stephens MR, Slatyer RA. Evolution of ecological niche breadth. Annu Rev Ecol Evol Syst. 2017; 48: 183–203. https://doi.org/10.1146/annurev-ecolsys-110316-023003
7. Churchfield S, Nesterenko VA, Shvarts EA. Food niche overlap and ecological separation amongst six species of coexisting forest shrews (Insectivora: Soricidae) in the Russian Far East. J Zool. 1999; 248: 349–359.
8. Woodward G, Hildrew AG. Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol. 2002; 71: 1063–1074. https://doi.org/10.1046/j.1365-2656.2002.00669.x
9. Jeglinski JWE, Goetz KT, Werner C, Costa DP, Trillmich F. Same size–same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. J Anim Ecol. 2013; 82: 694–706. https://doi.org/10.1111/1365-2656.12019 23351022
10. Wilson DS. The adequacy of body size as a niche difference. Am Nat. 1975; 109: 769–784.
11. Cohen JE, Pimm SL, Yodzis P, Saldaña J. Body sizes of animal predators and animal prey in food webs. J Anim Ecol, 1993; 62: 67–78.
12. Saulinho HHL, Trivinho-Strixino S. Body length determines the diet and niche specialization of non-biting midge predator (Tanypodinae) larvae in shallow reservoirs. Neotrop Entomol. 2019; 48: 136–142 https://doi.org/10.1007/s13744-018-0620-9 30039478
13. Scriven JJ, Whitehorn PR, Goulson D, Tinsley MC. Niche partitioning in a sympatric cryptic species complex. Ecol Evol. 2016; 6: 1328–1339. https://doi.org/10.1002/ece3.1965 26848386
14. Begon M, Townsend CR, Harper JL. Ecology, from individuals to ecosystems. Oxford: Balckwell Publishing; 2006.
15. Cornell H. Search strategies and the adaptive significance of switching in some general predators. Am Nat. 1976; 110: 317–320.
16. Punzo F. Experience affects hunting behavior of the wasp, Pepsis Mildei Stål (Hymenoptera: Pompilidae). J N Y Entomol Soc. 2005; 113: 222–229. https://doi.org/10.1664/0028-7199(2005)113[0222:EAHBOT]2.0.CO;2
17. Evans HE, O’Neill KM. The sand wasps: natural history and behavior. Cambridge: Harvard University Press; 2007.
18. Araújo MS, Gonzaga MO. Individual specialization in the hunting wasp Trypoxylon (Trypargylum) albonigrum (Hymenoptra, Crabronidae). Behav Ecol Sociobiol. 2007; 61: 1855–1863. https://doi.org/10.1007/s00265-007-0425-z
19. Pitilin RB, Araújo MS, Buschini MLT. Individual specialization in the hunting-wasp Trypoxylon (Trypargilum) agamemnon Richards (Hymenoptera: Crabronidae). Zool Stud. 2012; 51: 655–662. Available from: http://zoolstud.sinica.edu.tw/Journals/51.5/655.pdf
20. Santoro D, Polidori C, Asís JD, Tormos J. Complex interactions between components of individual prey specialization affect mechanisms of niche variation in a grasshopper-hunting wasp. J Anim Ecol. 2011; 80: 1123–1133. doi: 10.1111/j.1365-2656.2011.01874.x 21644980
21. Polidori C, Mendiola P, Asís JD, Tormos J, Garcia MD, Selfa J. Predatory habits of the grasshopper-hunting wasp Stizus continuus (Hymenoptera: Crabronidae): diet preference, predator-prey size relationships and foraging capacity. J Nat Hist. 2009; 43: 2985–3000.
22. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulse CD, Forister ML. The ecology of individuals: incidence and implications of individual specialization. Am Nat. 2003; 161: 1–28. https://doi.org/10.1086/343878 12650459
23. Costa-Pereira R, Rudolf VHW, Souza FL, Araújo MS. Drivers of individual niche variation in coexisting species. J Anim Ecol. 2018; 87: 1452–1464. doi: 10.1111/1365-2656.12879 29938791
24. Bohart RM, Menke AS. Sphecid wasps of the world: a generic revision. Berkeley: University of California Press; 1976.
25. Krombein KV. Trap-nesting wasps and bees: Life stories, nests and associates. Washington D.C.: Smithsonian Press; 1967.
26. Coville RE. Wasps of the genus Trypoxylon subgenus Trypargilum in North America (Hymenoptera: Sphecidae). Univ Cal Publ Entomol. 1982; 97: 1–147.
27. Blackledge TA, Coddington JA, Gillespie RG. Are three-dimensional spider webs defensive adaptations? Ecol Lett, 2003; 6: 13–18. https://doi.org/10.1046/j.1461-0248.2003.00384.x
28. Cardoso P, Pékar S, Jocqué R, Coddington JA. Global patterns of guild composition and functional diversity of spiders. PLoS ONE. 2011; 6: e21710. https://doi.org/10.1371/journal.pone.0021710 21738772
29. Sanders D, Vogel E, Knop E. Individual and species-specific traits explain niche size and functional role in spiders as generalist predators. J Anim Ecol. 2015; 84: 134–142. https://doi.org/10.1111/1365-2656.12271 25041766
30. Traveset A, Tur C, Trøjelsgaard K, Heleno R, Castro-Urgal R, Olesen JM. Global patterns of mainland and insular pollination networks. Glob Ecol Biogeogr. 2016; 25: 880–890. https://doi.org/10.1111/geb.12362
31. Grant PR. Evolution on islands. Oxford: Oxford University Press; 1998.
32. Drake DR, Mulder CPH, Towns DR, Daugherty CH. The biology of insularity: an introduction. J Biogeogr. 2002; 29: 563–569. https://doi.org/10.1046/j.1365-2699.2002.00706.x
33. Rodríguez-Estrella R. Los oasis de Baja California Sur: su importancia y conservación. In: Rodríguez-Estrella R, Cariño Olvera M, Aceves García F, editors. Reunión de análisis de los oasis de Baja California Sur: importancia y conservación. La Paz, BCS: CIBNOR, UABCS, SEMARNAT; 2004. p. 1–8.
34. Rodríguez-Estrella R, Arriaga L. Implicaciones ecológicas de las actividades humanas en la biota asociada a los oasis. In: Arriaga L, Rodríguez-Estrella R, editors. Los oasis de la península de Baja California. La Paz, BCS: CIBNOR; 1997. p. 285–292.
35. Jiménez ML, Nieto-Castañeda IG, Correa-Ramírez MM, Palacios-Cardiel C. Las arañas de los oasis de la región meridional de la península de Baja California, México. Revista Mexicana de Biodiversidad, 2015; 86: 319–331. https://doi.org/10.1016/j.rmb.2015.04.028
36. MacArthur RH. The theory of the niche. In: Lewontin RC, editor. Population biology and evolution. New York, NY: Syracuse University Press; 1968. p. 159–176.
37. Wiggins IL. Flora of Baja California. Stanford, CA: Stanford University Press; 1980.
38. Servicio Meteorológico Nacional (SMN); 2017. [cited 2018 April 10]. Available from: http://smn.cna.gob.mx/es/.
39. INEGI. Climate maps and datasets; 2017. [cited 2017 June 16] Available from: www.inegi.org.mx
40. Uetz GW, Halaj J, Cady AB. Guild structure of spiders in major crops. J Arachnol. 1999; 27: 270–280.
41. Chao A, Chiu CH, Jost L. Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annu. Rev. Ecol. Evol. Syst. 2014; 45: 297–324. https://doi.org/10.1146/annurev-ecolsys-120213-091540
42. Colwell RK, Coddington JA. Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci. 1994; 345: 101–118. doi: 10.1098/rstb.1994.0091 7972351
43. Hsieh TC, Ma KH, Chao A. (2018) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.17. ed2018
44. R Core Team. R: A language and environment for statistical computing. 3.6.1 2019-07-05 ed. Vienna, Austria. 2019.
45. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001; 26: 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
46. Anderson MJ, Ellingsen KE, McArdle BH. Multivariate dispersion as a measure of beta diversity. Ecol Lett. 2006; 9: 683–693. https://doi.org/10.1111/j.1461-0248.2006.00926.x 16706913
47. Kruskal JB, Wish M. Multidimensional scaling. California: Sage Publications; 1978.
48. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.5–3. ed2018.
49. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015; 67: 1–48.
50. Colwell RK, Futuyma DJ. On the measurement of niche breadth and overlap. Ecology. 1971; 52: 567–576. doi: 10.2307/1934144 28973805
51. Hulbert SH. The measurement of niche overlap and some relatives. Ecology. 1978; 59: 67–77.
52. Levins R. Evolution in changing environments: Some theoretical explorations. Princeton: Princeton University Press; 1968.
53. Zhang J. spaa: SPecies Association Analysis. R package version 0.2.2. ed2018.
54. Blüthgen N, Menzel F, Blüthgen N. Measuring specialization in species interaction networks. BMC Ecol. 2006; 6: id9. https://doi.org/10.1186/1472-6785-6-9
55. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N. Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol. 2007; 17: 341–346. https://doi.org/10.1016/j.cub.2006.12.039 17275300
56. Blüthgen N, Fründ J, Vázquez DP, Menzel F. What do interaction network metrics tell us about specialization and biological traits? Ecology. 2008; 89: 3387–3399. https://doi.org/10.1890/07-2121.1 19137945
57. Dormann CF, Gruber B, Fruend J. Introducing the bipartite Package: Analysing Ecological Networks. R news. 2008; Vol 8/2, 8–11.
58. Dormann CF, Fruend J, Bluethgen N, Gruber B. Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J. 2009; 2: 7–24. doi: 10.2174/1874213000902010007
59. Evans HE. A revision of the Mexican and Central American spider wasps of the subfamily Pompilinae (Hymenoptera: Pompilidae). Mem Am Entomol Soc. 1966; 20: 1–442.
60. Izenman AJ. Modern multivariate statistical techniques. Philadelphia: Springer; 2013.
61. Revelle W. psych: Procedures for Personality and Psychological Research. R package version 1.8.10. ed2018.
62. Novosolov M, Rodda GH, Gainsbury AM, Meiri S. Dietary niche variation and its relationship to lizard population density. J Anim Ecol. 2018; 87: 285–292. https://doi.org/10.1111/1365-2656.12762 28944457
63. Jiménez ML, Tejas A. Las arañas presa de la avispa lodera Trypoxylon (Trypargilum) tridentatum tridentatum en Baja California Sur, México. Southwestern Entomologist, 1994; 19: 173–180.
64. Domínguez K, Jiménez ML. Composition of spider prey captured by the wasp Trypoxylon (Trypargilum) tridentatum tridentatum in two habitats in an oasis in Baja California Sur, México. Can Entomol. 2008; 140: 388–392. https://doi.org/10.4039/n07-048
65. Llinas-Gutiérrez J, Jiménez ML. Arañas de humedales del sur de Baja California, México. An Inst Biol. 2004; 75: 283–302. Available from: http://www.redalyc.org/articulo.oa?id=45875205
66. Piel WH. The systematics of Neotropical orb-weaving spiders in the genus Metepeira (Araneae: Araneidae). Bull Mus Comp Zool. 2001; 157: 1–92.
67. Blackledge TA, Wenzel JW. Silk mediated defense by an orb web spider against predatory mud-dauber wasps. Behaviour. 2001; 138: 155–171.
68. Uma DB, Weiss MR. Chemical mediation of prey recognition by spider-hunting wasps. Ethology. 2010; 116: 85–95. https://doi.org/10.1111/j.1439-0310.2009.01715.x
69. Eberhard WG. The predatory behaviour of two wasps, Agenoideus humils (Pompilidae) and Sceliphron caementarium (Sphecidae), on the orb weaving spider Araneus cornatus (Araneidae). Psyche. 1970; 77: 243–251.
70. Rayor LS. Attack strategies of predatory wasps (Hymenoptera: Pompilidae; Sphecidae) on colonial orb web-building spiders (Araneidae: Metepeira incrassata). J. Kans. Entomol. Soc. 1996; 69: 67–75.
71. Punzo F, Ludwig L. Behavioral responses to Pepsis thisbe (Hymenoptera: Pompilidae) to chemosensory cues associated with host spiders. J Insect Behav. 2005; 18: 757–766. doi: 10.1007/s10905-005-8738-0
72. Punzo F. Female spider wasps, Anoplius splendens Driesbach (Hymenoptera: Pompilidae), learn to associate the odor of host feces with the presence of the host. J Entomol Sci. 2006; 41: 202–210. doi: 10.18474/0749-8004-41.3.202
73. Foelix RF. Biology of spiders. New York: Oxford University Press; 2011.
74. Blackledge TA, Pickett KM. Predatory interactions between mud-dauber wasps (Hymenoptera, Sphecidae) and Argiope (Araneae, Araneidae) in captivity. J Arachnol. 2000; 28: 211–216. https://doi.org/10.1636/0161-8202(2000)028[0211:PIBMDW]2.0.CO;2
75. Machovsky-Capuska GE, Miller MGR, Silva FRO, Amiot C, Stockin KA, Senior AM, Schuckard R, Melville D, Raubenheimer D. The nutritional nexus: Linking niche, habitat variability and prey composition in a generalist marine predator. J Anim Ecol. 2018; 87: 1286–1298. https://doi.org/10.1111/1365-2656.12856 29873067
76. Judd TM, Magnus RM, Fasnacht MP. A nutritional profile of the social wasp Polistes metricus: Differences in nutrient levels between castes and changes within castes during the annual life cycle. J Insect Physiol. 2010; 56: 42–56. https://doi.org/10.1016/j.jinsphys.2009.09.002 19781547
77. Daugherty TH, Toth AL, Robinson GE. Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol Ecol. 2011; 20: 5337–5347. https://doi.org/10.1111/j.1365-294X.2011.05344.x 22066722
78. Cross EA, Stith MG, Bauman TR. Bionomics of the organ-pipe mud-dauber, Trypoxylon politum (Hymenoptera: Sphecoidea). Ann Entom Soc Am. 1975; 68: 901–916.
79. Poisot T, Stouffer DB, Gravel D. Beyond species: why ecological interaction networks vary through space and time. Oikos. 2015; 124: 243–251. https://doi.org/10.1111/oik.01719
80. Memmott J, Martinez ND, Cohen JE. Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. J Anim Ecol. 2001; 69: 1–15. https://doi.org/10.1046/j.1365-2656.2000.00367.x
81. Polidori C, Santoro D, Asís JD, Tormos J. Individual prey specialization in wasps: Predator size is a weak predictor of taxonomic niche width and niche overlap. In: Polidori C. Predation in the Hymenoptera: an evolutionary perspective. Kerala: Transworld Research Network; 2011. pp. 101–121.
82. Coello C. Effects of prey size and load carriage on the evolution of foraging strategies in wasps. In: Polidori C. Predation in the Hymenoptera: an evolutionary perspective. Kerala: Transworld Research Network; 2011. pp. 23–37.
83. Araújo MS, Gonzaga MO. Individual specialization in the hunting wasp Trypoxylon (Trypargilum) albonigrum (Hymenoptera, Crabronidae). Behav Ecol Sociobiol. 2007; 61: 1855–1863. https://doi.org/10.1007/s00265-007-0425-z
84. Buschini MLT, Borba NA, Brescovit AD. Prey selection in the trap-nesting wasp Trypoxylon (Trypargilum) opacum Brèthes (Hymenprtera; Crabronidae). Braz J Biol. 2010; 70: 529–536. https://doi.org/10.1590/S1519-69842010000300009 20730339
85. Buschini MLT, Borba NA, Brescovit AD. Patterns of prey selection of Trypoxylon (Trypargilum) lactitarse Saussure (Hymenoptera: Crabronidae) in southern Brazil. Braz J Biol. 2008. 68: 519–528. https://doi.org/10.1590/S1519-69842008000300008 18833472
86. Brändle M, Öhlschläger S, Brandl R. Range sizes in butterflies: correlation across scales. Evol Ecol Res. 2002; 4: 993–1004. Available from: http://www.evolutionary-ecology.com/issues/v04n07/ffar1430.pdf
87. Schowalter TD. Insect ecology, an ecosystem approach. London: Academic Press; 2011.
88. Heinrich B. Thermoregulation in endothermic insects. Science. 1974; 185: 747–756. doi: 10.1126/science.185.4153.747 4602075
89. Kühsel S, Brückner A, Schmelzle S, Heethoff M, Blüthgen N. Surface area–volume ratios in insects. Insect Sci. 2016; 00, 1–13. https://doi.org/10.1111/1744-7917.12362
90. O'Neill KM, O'Neill RP. Thermal stress and microhabitat selection in territorial males of the digger wasp Philanthus psyche (Hymenoptera: Sphecidae). J Therm Biol. 1988; 13:15–20.
91. Herrera CM. Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb, Ecology. 1995; 76: 218–228.
92. Heinrich B. (1993). The hot-blooded insects, strategies and mechanisms of thermoregulation. London: Springer Berlin Heidelberg. 1993.
93. Santos GMM, Presley SJ. Niche overlap and temporal activity patterns of social wasps (Hymenoptera: Vespidae) in a Brazilian cashew orchard. Sociobiology. 2010; 121–131.
94. Kasper ML, Reeson AF, Cooper SJB, Perry KM, Austin AD. Assessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA. Mol Ecol. 2004; 13: 2037–2048. doi: 10.1111/j.1365-294X.2004.02193.x 15189224
95. Morato EF, Martins RP. An overview of proximate factors affecting the nesting behavior of solitary wasps and bees (Hymenoptera: Aculeata) in preexisting cavities in wood. Neotrop Entomol. 2006; 35: 285–298. https://doi.org/10.1590/S1519-715566X2006000300001 18575687
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