Cuticular bacteria appear detrimental to social spiders in mixed but not monoculture exposure

Current Zoology

Volumn 62, Issue 4, 2016, Pages 377-384

  Keiser, Carl N ^a   Shearer, Taylor A ^a   Demarco, Alexander E ^a   Brittingham, Hayley A ^a   Knutson, Karen A ^a   Kuo, Candice ^a   Zhao, Katherine ^a   Pruitt, Jonathan N ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Cuticular bacteria; Sickness behavior; Social spider; Stegodyphus dumicola

Indexed keywords

EID: 84986242740     PISSN: 16745507     EISSN: None     Source Type: Journal    
DOI: 10.1093/cz/zow015     Document Type: Article

References (90)

1. Avilés L, Varas C, Dyreson E, 1999. Does the African social spider Stegodyphus dumicola control the sex of individual offspring? Behav Ecol Sociobiol 46:237-243.
2. Barth FG, Höller A, 1999. Dynamics of arthropod filiform hairs. V. The response of spider trichobothria to natural stimuli. Phil Trans Roy Soc Lond Series B: Biol Sci 354:183-192.
3. Basset A, Khush RS, Braun A, Gardan L, Boccard F et al., 2000. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci 97:3376-3381. doi: 10.1073/pnas.97.7.3376.
4. Ben-Yosef M, Jurkevitch E, Yuval B, 2008. Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol Entom 33:145-154. doi: 10.1111/j.1365-3032.2008.00617.x.
5. Bilde T, Coates K, Birkhofer K, Bird T, Maklakov A et al., 2007. Survival benefits select for group living in a social spider despite reproductive costs. J Evol Biol 20:2412-2426.
6. Brey PT, Lee W-J, Yamakawa M, Koizumi Y, Perrot S et al., 1993. Role of the integument in insect immunity: Epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proc Natl Acad Sci 90:6275-6279.
7. Broderick NA, Raffa KF, Handelsman J, 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci 103:15196-15199. doi: 10.1073/pnas.0604865103.
8. Broderick NA, Robinson CJ, McMahon MD, Holt J, Handelsman J et al., 2009. Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol 7:11.
9. Brown CR, Brown MB, 1986. Ectoparasitism as a cost of coloniality in cliff swallows Hirundo pyrrhonota. Ecology 67:1206-1218.
10. Casadevall A, Pirofski L, 2000. Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68:6511-6518.
11. Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A, 2011. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet 7:e1002272-e1002272.
12. Chapman MH, Hoy MA, 1991. Relative toxicity of Bacillus thuringiensis var. tenebrionis to the two-spotted spider mite Tetranychus urticae Koch and its predator Metaseiulus occidentalis (Nesbitt) (Acari, Tetranychidae and Phytoseiidae). J Appl Entom 111:147-154.
13. Cogen A, Nizet V, Gallo R, 2008. Skin microbiota: a source of disease or defence? Br J Dermatol 158:442-455.
14. Crickmore N, 2005. Using worms to better understand how Bacillus thuringiensis kills insects. Trends in Microbiol 13:347-350.
15. Del Fiol Federica TS, Riccardo G, 2007. Fungal spores and pollen as potential nutritional additives for the cross spider Araneus diadematus Clerck (Araneae, Araneidae). Boletín Micológico 22:47-50.
16. Dethlefsen L, McFall-Ngai M, Relman DA, 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-818.
17. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB, 2012. Animal behavior and the microbiome. Science 338:198-199.
18. Fedhila S, Nel P, Lereclus D, 2002. The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J Bacteriol 184:3296-3304.
19. Fitt GP, O'Brien R, 1985. Bacteria associated with four species of Dacus (Diptera: Tephritidae) and their role in the nutrition of the larvae. Oecologia 67:447-454.
20. Foelix R, 2010. Biology of Spiders. Oxford: Oxford University Press.
21. Forster LM, 1977. A qualitative analysis of hunting behaviour in jumping spiders (Araneae: Salticidae). New Zeal J Zool 4:51-62.
22. Freitak D, Heckel DG, Vogel H, 2009. Bacterial feeding induces changes in immune-related gene expression and has trans-generational impacts in the cabbage looper Trichoplusia ni. Front Zool 6:7.
23. Freitak D, Wheat CW, Heckel DG, Vogel H, 2007. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol 5:56.
24. Gaver-Wainwright MM, Zack RS, Foradori MJ, Lavine LC, 2011. Misdiagnosis of spider bites: bacterial associates, mechanical pathogen transfer, and hemolytic potential of venom from the hobo spider Tegenaria agrestis (Araneae: Agelenidae). J Med Entom 48:382-388.
25. Gill SS, Cowles EA, Pietrantonio PV, 1992. The mode of action of Bacillus thuringiensis endotoxins. Ann Rev Entom 37:615-634.
26. Gneiding K, Frodl R, Funke G, 2008. Identities of Microbacterium spp. encountered in human clinical specimens. J Clin Microbiol 46:3646-3652.
27. González-Tokman D, Ruch J, Pulpitel T, Ponton F, 2014. Cuticular antifungals in spiders: density-and condition dependence. PLoS ONE 9:e91785.
28. Goodacre SL, Martin OY, Bonte D, Hutchings L, Woolley C et al., 2009. Microbial modification of host long-distance dispersal capacity. BMC Biol 7:32.
29. Grice EA, Segre JA, 2011. The skin microbiome. Nat Rev Microbiol 9:244-253.
30. Gunnarsson B, Goodacre SL, Hewitt GM, 2009. Sex ratio, mating behaviour and Wolbachia infections in a sheetweb spider. Biol J Linn Soc 98:181-186.
31. Hall IM, Arakawa K, Dulmage HT, Correa J, 1977. The pathogenicity of strains of Bacillus thuringiensis to larvae of Aedes and to Culex mosquitoes. Mosq News 37:246-251.
32. Henschel J, Lubin Y, Schneider J, 1995. Sexual competition in an inbreeding social spider Stegodyphus dumicola (Araneae: Eresidae). Insectes Sociaux 42:419-426.
33. Henschel JR, 1998. Predation on social and solitary individuals of the spider Stegodyphus dumicola (Araneae, Eresidae). J Arachnol 67:61-69.
34. Hodgson DJ, Rainey PB, Buckling A, 2002. Mechanisms linking diversity, productivity and invasibility in experimental bacterial communities. Proc Roy Soc Lond B: Biol Sci 269:2277-2283.
35. Höfte H, Whiteley H, 1989. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev 53:242-255.
36. Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T, 2008. Symbiont acquisition alters behaviour of stinkbug nymphs. Biol Lett 4:45-48. doi: 10.1098/rsbl.2007.0510.
37. Hugenholtz P, Tyson GW, 2008. Microbiology: metagenomics. Nature 455:481-483.
38. Johannesen J, Hennig A, Dommermuth B, Schneider JM, 2002. Mitochondrial DNA distributions indicate colony propagation by single matri-lineages in the social spider Stegodyphus dumicola (Eresidae). Biol J Linn Soc 76:591-600.
39. Jones D, Keddie R. 2006. The genus Arthrobacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, editors. The Prokaryotes. New York: Springer. 945-960.
40. Jones TC, Riechert SE, Dalrymple SE, Parker PG, 2007. Fostering model explains variation in levels of sociality in a spider system. Animal Behav 73:195-204.
41. Keiser CN, Jones DK, Modlmeier AP, Pruitt JN, 2014a. Exploring the effects of individual traits and within-colony variation on task differentiation and collective behavior in a desert social spider. Behav Ecol Sociobiol 68:839-850.
42. Keiser CN, Modlmeier AP, Singh N, Jones DK, Pruitt JN, 2014b. Exploring how a shift in the physical environment shapes individual and group behavior across two social contexts. Ethology 120:825-833.
43. Keiser CN, Pruitt JN, 2014. Personality composition is more important than group size in determining collective foraging behaviour in the wild. Proc Roy Soc B: Biol Sci 281:20141424.
44. Lambert B, Peferoen M, 1992. Insecticidal promise of Bacillus thuringiensis. BioScience 42:112-122.
45. Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M, 2009. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 96:557-567.
46. Luo X, Zhang J, Li D, Xin Y, Xin D et al., 2014. Planomicrobium soli sp. nov. isolated from soil. Int J Syst Evol Microbiol 64:2700-2705.
47. Mandell GL, Bennett JE, Dolin R, 2009. Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases. Churchhill Livingston: Elsevier.
48. Mans JJ, von Lackum K, Dorsey C, Willis S, Wallet SM et al., 2009. The degree of microbiome complexity influences the epithelial response to infection. BMC Genom 10:380.
49. Mascarelli PE, Maggi RG, Hopkins S, Mozayeni BR, Trull CL et al., 2013. Bartonella henselae infection in a family experiencing neurological and neurocognitive abnormalities after woodlouse hunter spider bites. Parasit Vect 6:98.
50. Mathew A, Pandey M, Murthy N, 1999. Survival analysis: caveats and pitfalls. Eur J Surg Oncol (EJSO) 25:321-329.
51. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T et al., 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229-3236.
52. Navon A, Ascher K, 2000. Bioassays of Entomopathogenic Microbes and Nematodes. New York: Cabi.
53. Nentwig W, 1985. Social spiders catch larger prey: a study of Anelosimus eximius (Araneae: Theridiidae). Behav Ecol Sociobiol 17:79-85.
54. Newton AC, Fitt BD, Atkins SD, Walters DR, Daniell TJ, 2010. Pathogenesis, parasitism and mutualism in the trophic space of microbe-plant interactions. Trends Microbiol 18:365-373.
55. Paul R, Bihlmayer S, Colmorgen M, Zahler S, 1994. The open circulatory system of spiders (Eurypelma californicum, Pholcus phalangioides): a survey of functional morphology and physiology. Physiol Zool 1360-1382.
56. PieM, Rosengaus R, Calleri D, Traniello J, 2005. Density and disease resistance in group-living insects: do eusocial species exhibit density-dependent prophylaxis? Ethol, Ecol Evol 17:41-50.
57. Pruitt JN, Grinsted L, Settepani V, 2013. Linking levels of personality: personalities of the 'average' and 'most extreme' group members predict colony-level personality. Animal Behav 86:391-399.
58. RamseyMM, Rumbaugh KP, Whiteley M, 2011. Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7:e1002012.
59. Ramsey MM, Whiteley M, 2009. Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci 106:1578-1583.
60. Randolph S, Gern L, Nuttall P, 1996. Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol Today 12:472-479.
61. Raymond B, Johnston PR, Wright DJ, Ellis RJ, Crickmore N et al., 2009. A mid-gut microbiota is not required for the pathogenicity of Bacillus thuringiensis to diamondback moth larvae. Environ Microbiol 11:2556-2563.
62. Riechert SE, Hedrick AV, 1993. A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae, Agelenidae). Animal Behav 46:669-675.
63. Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S et al., 1996. A canine distemper virus epidemic in Serengeti lions Panthera leo. Nature 379:441-445.
64. Rosengaus R, Jordan C, Lefebvre M, Traniello J, 1999. Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86:544-548.
65. Rosengaus RB, Maxmen AB, Coates LE, Traniello JF, 1998. Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav Ecol Sociobiol 44:125-134.
66. Roth O, Sadd BM, Schmid-Hempel P, Kurtz J, 2009. Strain-specific priming of resistance in the red flour beetle Tribolium castaneum. Proc Roy Soc B: Biol Sci 276:145-151.
67. Salomon M, Lubin Y, 2007. Cooperative breeding increases reproductive success in the social spider Stegodyphus dumicola (Araneae, Eresidae). Behav Ecol Sociobiol 61:1743-1750.
68. Savini V, Catavitello C, Masciarelli G, Astolfi D, Balbinot A et al., 2010. Drug sensitivity and clinical impact of members of the genus Kocuria. J Med Microbiol 59:1395-1402.
69. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J et al., 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775-806.
70. Schumann P, Rainey FA, Burghardt J, Stackebrandt E, Weiss N, 1999. Reclassification of Brevibacterium oxydans (Chatelain and Second 1966) as Microbacterium oxydans comb. nov. Int J Syst Bacteriol 49:175-177.
71. Seibt U, Wickler W, 1987. Gerontophagy versus cannibalism in the social spiders Stegodyphus mimosarum Pavesi and Stegodyphus dumicola Pocock. Animal Behav 35:1903-1905.
72. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I et al., 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci 107:20051-20056.
73. Sibley CD, Duan K, Fischer C, Parkins MD, Storey DG et al., 2008. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4:e1000184.
74. Sloan Wilson D, Clark AB, Coleman K, Dearstyne T, 1994. Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442-446.
75. Smith D, Van Rijn S, Henschel J, Bilde T, Lubin Y, 2009. Amplified fragment length polymorphism fingerprints support limited gene flow among social spider populations. Biol J Linn Soc 97:235-246.
76. Storey JD, 2002. A direct approach to false discovery rates. J Roy Stat Soc: Series B (Statistical Methodology) 64:479-498.
77. Stratton G, Suter R, 2009. Water repellent properties of spiders: Topographical variations and functional correlates. In: Gorb S, editor. Functional Surfaces in Biology. Dordrecht, Heidelberg, London, New York: Springer, 77-95.
78. Suter RB, Stratton GE, Miller PR, 2004. Taxonomic variation among spiders in the ability to repel water: surface adhesion and hair density. J Arachnol 32:11-21.
79. Sutter GR, Raun ES, 1967. Histopathology of European-corn-borer larvae treated with Bacillus thuringiensis. J Invert Pathol 9:90-103.
80. Tanaka K, Watanabe M, 2003. Transmission of ice-nucleating active bacteria from a prey reduces cold hardiness of a predator (Araneae: Theridiidae). Naturwissenschaften 90:449-451.
81. Thompson CR, Brogan RS, Scheifele LZ, Rivers DB, 2013. Bacterial interactions with necrophagous flies. Ann Entomol Soc Am 106:799-809.
82. Traniello JF, Rosengaus RB, Savoie K, 2002. The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proc Natl Acad Sci 99:6838-6842.
83. Treherne J, Foster W, 1981. Group transmission of predator avoidance behaviour in a marine insect: the trafalgar effect. Animal Behav 29:911-917.
84. Uetz GW, Boyle J, Hieber CS, Wilcox RS, 2002. Antipredator benefits of group living in colonial web-building spiders: The 'early warning' effect. Animal Behav 63:445-452.
85. Vallet-Gely I, Lemaitre B, Boccard F, 2008. Bacterial strategies to overcome insect defences. Nat Rev Microbiol 6:302-313.
86. Vanthournout B, Hendrickx F, 2015. Endosymbiont dominated bacterial communities in a dwarf spider. PLoS ONE 10:e0117297.
87. Vanthournout B, Swaegers J, Hendrickx F, 2011. Spiders do not escape reproductive manipulations by Wolbachia. BMC Evol Biol 11:15.
88. Wallace JR, Gordon MC, Hartsell L, Mosi L, Benbow ME et al., 2010. Interaction of Mycobacterium ulcerans with mosquito species: implications for transmission and trophic relationships. Appl Environ Microbiol 76:6215-6222.
89. Wise DH, 1995. Spiders in Ecological Webs. Cambridge, UK: Cambridge University Press.
90. Zilber-Rosenberg I, Rosenberg E, 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723-735.