Inferring social structure and its drivers from refuge use in the desert tortoise, a relatively solitary species

Behavioral Ecology and Sociobiology

Volumn 70, Issue 8, 2016, Pages 1277-1289

  Sah, Pratha ^a   Nussear, Kenneth E ^b   Esque, Todd C ^c   Aiello, Christina M ^c,d   Hudson, Peter J ^d   Bansal, Shweta ^a,e  

^a GEORGETOWN UNIVERSITY   (United States)

^b UNIVERSITY OF NEVADA   (United States)

^c U S GEOLOGICAL SURVEY   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Behavioral stress response; Bipartite networks; Generalized linear mixed models; Gopherus agassizii; Modularity; Mycoplasma agassizii

Indexed keywords

ANIMALIA; GOPHERUS AGASSIZII; MYCOPLASMA AGASSIZII; TESTUDINIDAE;

EID: 84970965882     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-016-2136-9     Document Type: Article

References (75)

1. Bansal S, Khandelwal S, Meyers L A (2009) Exploring biological network structure with clustered random networks. BMC Bioinfo 10:405
2. Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. https://gephi.org
3. Behringer D C, Butler IV MJ (2010) Disease avoidance influences shelter use and predation in Caribbean spiny lobster. Behav Ecol Sociobiol 64(5):747–755
4. Berger-Tal O, Polak T, Oron A, Lubin Y, Kotler B P, Saltz D (2011) Integrating animal behavior and conservation biology: a conceptual framework. Behav Ecol 22(2):236–239
5. Brown MB, Schumacher IM, Klein PA, Harris K, Correll T, Jacobson ER (1994) Mycoplasma agassizii causes upper respiratory tract disease in the Desert Tortoise. Infect Immun 62(10):4580–4586
6. Bulova S J (1994) Patterns of burrow use by desert tortoises: gender differences and seasonal trends. Herpetol Monogr 8:133–143
7. Bulova S J (1997) Conspecific chemical cues influence burrow choice by desert tortoises (Gopherus agassizii). Copeia 1997(4):802–810
8. Carr JW (2015) MantelTest. http://jwcarr.github.io/MantelTest
9. Carter G G, Wilkinson G S (2013) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc B 280:20122573
10. Cooper W E Jr (2015) Escaping from predators: an integrative view of escape decisions. Cambridge University Press, Cambridge
11. Croft D P, Krause J, James R (2004) Social networks in the guppy (Poecilia reticulata). Proc R Soc Lond B 271:S516–S519
12. Cross P C, Lloyd-smith J O, Bowers J A, Hay C T, Hofmeyr M, Getz W M (2004) Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffalo in the Kruger National Park. Ann Zool Fenn 41:879–892
13. Davis S, Abbasi B, Shah S, Telfer S, Begon M (2015) Spatial analyses of wildlife contact networks. J R Soc Interface 20141004(102):12
14. Department of the Interior (1973) Endangered species act. Tech. rep., U.S. Fish and Wildlife Service, Washington, DC
15. Department of the Interior (2011) Revised recovery plan for the Mojave population of the desert tortoise (Gopherus agassizii). Tech. rep., U.S. Fish and Wildlife Service, Sacramento
16. Dodd K C, Seigel R A (1991) Relocation, repatriation, and translocation of amphibians and reptiles: are they conservation strategies that work? Herpetologica 47(3):336–350
17. Drake K K, Nussear K E, Esque T C, Barber A M, Vittum K M, Medica P A, Tracy C R, Hunter K W (2012) Does translocation influence physiological stress in the desert tortoise? Anim Conserv 15 (6):560–570
18. Duda J J, Krzysik A J, Freilich J E (1999) Effects of drought on desert tortoise movement and activity. J Wildlife Manage 63(4):1181–1192
19. Esque T C, Nussear K E, Drake K K, Walde A, Berry K, Averill-Murray R, Woodman A, Boarman W, Medica P, Mack J, Heaton J (2010) Effects of subsidized predators, resource variability, and human population density on desert tortoise populations in the Mojave Desert, USA. Endanger Species Res 12:167–177
20. Eubanks J O, Michener W K, Guyer C (2003) Patterns of movement and burrow use in a population of gopher tortoises (Gopherus polyphemus). Herpetologica 59(3):311–321
21. Fortuna M A, Popa-Lisseanu A G, Ibȧṅez C, Bascompte J (2009) The roosting spatial network of a bird-predator bat. Ecology 90(4):934–944
22. Fox J, Monette G (1992) Generalized collinearity diagnostics. J Am Stat Assoc 87(417):178–183
23. Franks B R, Avery H W, Spotila J R (2011) Home range and movement of desert tortoises Gopherus agassizii in the Mojave Desert of California, USA. Endanger Species Res 13(3):191–201
24. Germano J M, Bishop P J (2009) Suitability of amphibians and reptiles for translocation. Conserv Biol 23 (1):7–15
25. van Gils J A, Kraan C, Dekinga A, Koolhaas A, Drent J, de Goeij P, Piersma T (2009) Reversed optimality and predictive ecology: burrowing depth forecasts population change in a bivalve. Biol Lett 5(1):5–8
26. Girvan M, Newman M E J (2002) Community structure in social and biological networks. P Natl Acad Sci USA 99(12):7821–7826
27. Godfrey S S (2013) Networks and the ecology of parasite transmission: a framework for wildlife parasitology. Int J Parasitol Parasites Wildl 2:235–245
28. Godfrey S S, Bull C M, James R, Murray K (2009) Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav Ecol Sociobiol 63(7):1045–1056
29. Gough H M, Gascho Landis A M, Stoeckel J A (2012) Behaviour and physiology are linked in the responses of freshwater mussels to drought. Freshwater Biol 57(11):2356–2366
30. Griffin R H, Nunn C L (2011) Community structure and the spread of infectious disease in primate social networks. Evol Ecol 26(4):779–800
31. Hagberg A A, Schult D A, Swart P J (2008) Exploring network structure, dynamics, and function using NetworkX. Proc Python Sci Conf (SciPy2008) 836:11–15
32. Halstead B J, McCoy E D, Stilson T A, Mushinsky H R (2007) Alternative foraging tactics of juvenile gopher tortoises (Gopherus Polyphemus) examined using correlated random walk models. Herpetologica 63(4):472–481
33. Harless M L, Walde A D, Delaney D K, Pater L L, Hayes W K (2009) Home range, spatial overlap, and burrow use of the desert tortoise in the West Mojave Desert. Copeia 2009 (2):378–389
34. Harrell F E (2002) Regression modeling strategies: with applications to linear models, logistic and ordinal regression, and survival analysis, 1st edn. Springer, London
35. Henen B T, Peterson C C, Wallis I R, Berry K H, Nagy K A (1998) Effects of climatic variation on field metabolism and water relations of desert tortoises. Oecologia 117(3):365–373
36. Hinderle D (2011) Desert tortoises (Gopherus agassizii) and translocation: homing, behavior, habitat and shell temperature experiments. Tech. rep., San Diego State University, San Diego
37. Hinderle D, Lewison R L, Walde A D, Deutschman D, Boarman W I (2015) The effects of homing and movement behaviors on translocation: desert tortoises in the western Mojave Desert. J Wildlife Manage 79(1):137–147
38. Hirsch B T, Prange S, Hauver S A, Gehrt S D (2013) Raccoon social networks and the potential for disease transmission. PLoS ONE 8:e75830
39. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biomet J 50(3):346–363
40. Inman R D, Nussear K E, Esque T C, Vandergast A G, Hathaway S A, Wood D A, Barr K R, Fisher R N (2014) Mapping habitat for multiple species in the Desert Southwest. US Geological Survey, Reston
41. Jachowski D S, Slotow R, Millspaugh J J (2012) Physiological stress and refuge behavior by african elephants. PLoS ONE 7:e31818
42. Jacobson E R, Brown M B, Wendland L D, Brown D R, Klein P A, Christopher M M, Berry K H (2014) Mycoplasmosis and upper respiratory tract disease of tortoises: a review and update. Vet J 201(3):257–64
43. Kerr G D, Bull C M (2006) Movement patterns in the monogamous sleepy lizard (Tiliqua rugosa): effects of gender, drought, time of year and time of day. J Zool 269(2):137–147
44. Kurvers R H J M, Krause J, Croft D P, Wilson A D M, Wolf M (2014) The evolutionary and ecological consequences of animal social networks: emerging issues. Trends Ecol Evol 29(6):326–35
45. Leu S T, Kappeler P M, Bull C M (2010) Refuge sharing network predicts ectoparasite load in a lizard. Behav Ecol Sociobiol 64(9):1495–1503
46. Leu S T, Kappeler P M, Bull C M (2011) The influence of refuge sharing on social behaviour in the lizard Tiliqua rugosa. Behav Ecol Sociobiol 65(4):837–847
47. Longshore K M, Jaeger J R, Sappington J M (2003) Desert tortoise (Gopherus agassizii) survival at two eastern Mojave Desert sites: death by short-term drought? J Herpetol 37(1):169–177
48. Lovich J E, Yackulic C B, Freilich J, Agha M, Austin M, Meyer K P, Arundel T R, Hansen J, Vamstad M S, Root S A (2014) Climatic variation and tortoise survival: has a desert species met its match? Biol Conserv 169:214–224
49. Lusseau D, Wilson B, Hammond P S, Grellier K, Durban J W, Parsons K M, Barton T R, Thompson P M (2006) Quantifying the influence of sociality on population structure in bottlenose dolphins. J Anim Ecol 75(1):14–24
50. MacIntosh A J J, Jacobs A, Garcia C, Shimizu K, Mouri K, Huffman M A, Hernandez A D (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PloS ONE 7:e51144
51. Mann J, Stanton M A, Patterson E M, Bienenstock E J, Singh L O (2012) Social networks reveal cultural behaviour in tool-using using dolphins. Nat Commun 3:980
52. Manno T G (2008) Social networking in the Columbian ground squirrel, Spermophilus columbianus. Anim Behav 75(4):1221–1228
53. McGuire J L, Smith L L, Guyer C, Yabsley M J (2014) Effects of mycoplasmal upper-respiratory-tract disease on movement and thermoregulatory behavior of gopher tortoises (Gopherus Polyphemus) in Georgia, USA. J Wildlife Dis 50 (4):745–756
54. Mcrae W A, Landers J L, Garner J A (1981) Movement patterns and home Range of the gopher tortoise. Am Midl Nat 106(1):165–179
55. Morris D W, Kotler B P, Brown J S, Sundararaj V, Ale S B (2009) Behavioral indicators for conserving mammal diversity. Ann NY Acad Sci 1162:334–56
56. Moule H, Michelangeli M, Thompson M B, Chapple D G (2015) The influence of urbanization on the behaviour of an Australian lizard and the presence of an activity-exploratory behavioural syndrome. J Zool 298:103–111
57. Mushinsky H R, Stilson T A, McCoy E D (2003) Diet and dietary preference of the juvenile gopher tortoise (Gopherus Polyphemus). Herpetologica 59(4):475–483
58. Nagy K A, Medica P A (1986) Physiological ecology of desert tortoises in southern Nevada. Herpetologica 42(1):73–92
59. Niblick H A, Rostal DC, Classen T (1994) Role of male-male interactions and female choice in the mating system of the desert tortoise, Gopherus agassizii. Herpetol Monogr 8:124–132
60. Nussear K E, Tracy C R, Medica P A, Wilson D S, Marlow R W, Corn P S (2012) Translocation as a conservation tool for Agassiz’s desert tortoises: survivorship, reproduction, and movements. J Wildlife Manage 76(7):1341–1353
61. Pasquaretta C, Levé M, Claidière N, van de Waal E, Whiten A, MacIntosh AJJ, Pelé M, Bergstrom ML, Borgeaud C, Brosnan SF, Crofoot MC, Fedigan LM, Fichtel C, Hopper LM, Mareno MC, Petit O, Schnoell AV, di Sorrentino EP, Thierry B, Tiddi B, Sueur C (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600
62. Peterson C C (1994) Different rates and causes of high mortality in two populations of the threatened desert tortoise Gopherus agassizii. Biol Conserv 70(2):101–108
63. Peterson C C (1996) Anhomeostasis: seasonal water and solute in two relations of the desert populations tortoise (Gopherus agassizil) during Chronic Drought. Physiol Zool 69(6):1324–1358
64. Pinter-Wollman N, Hobson E A, Smith J E, Edelman A J, Shizuka D, de Silva S, Waters JS, Prager SD, Sasaki T, Wittemyer G, Fewell J, McDonald DB (2013) The dynamics of animal social networks: analytical, conceptual, and theoretical advances. Behav Ecol 25(2):242–255
65. Porphyre T, McKenzie J, Stevenson M A (2011) Contact patterns as a risk factor for bovine tuberculosis infection in a free-living adult brushtail possum Trichosurus vulpecula population. Prev Vet Med 100(3–4):221–230
66. Sandmeier F C, Tracy C R, DuPré S, Hunter K (2009) Upper respiratory tract disease (URTD) as a threat to desert tortoise populations: a reevaluation. Biol Conserv 142(7):1255–1268
67. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Method Ecol Evol 1:103–113
68. Scott J, Carrington P (eds) (2011) The SAGE handbook of social network analysis. SAGE publications, London
69. Singmann H (2013) afex: analysis of factorial experiments, https://cran.r-project.org/web/packages/afex
70. Vander Wal E, Paquet PC, Andrés JA (2012) Influence of landscape and social interactions on transmission of disease in a social cervid. Mol Ecol 21(5):1271–82
71. Wilson D S (1991) Estimates of survival for juvenile gopher tortoises, Gopherus polyphemus. J Herpetol 25 (3):376–379
72. Wilson D S, Morafka D J, Tracy C R, Nagy K A (1999) Winter activity of juvenile desert tortoises (Gopherus agassizii) in the Mojave Desert. J Herpetol 33(3):496–501
73. Winkelmann R (2003) Econometric analysis of count data. Springer Science & Business Media, Heidelberg
74. Witmer G W (2005) Wildlife population monitoring: some practical considerations. Wildlife Res 32:259–263
75. Zuur A, Ieno E, Elphick C S (2010) A protocol for data exploration to avoid common statistical problems. Method Ecol Evol 1:3–14