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

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Abstract

For several species, refuges (such as burrows, dens, roosts, nests) are an essential resource for protection from predators and extreme environmental conditions. Refuges also serve as focal sites for social interactions, including mating, courtship, and aggression. Knowledge of refuge use patterns can therefore provide information about social structure, mating, and foraging success, as well as the robustness and health of wildlife populations, especially for species considered to be relatively solitary. In this study, we construct networks of burrow use to infer social associations in a threatened wildlife species typically considered solitary—the desert tortoise. We show that tortoise social networks are significantly different than null networks of random associations, and have moderate spatial constraints. We next use statistical models to identify major mechanisms behind individual-level variation in tortoise burrow use, popularity of burrows in desert tortoise habitat, and test for stressor-driven changes in refuge use patterns. We show that seasonal variation has a strong impact on tortoise burrow switching behavior. On the other hand, burrow age and topographical condition influence the number of tortoises visiting a burrow in desert tortoise habitat. Of three major population stressors affecting this species (translocation, drought, disease), translocation alters tortoise burrow switching behavior, with translocated animals visiting fewer unique burrows than residents. In a species that is not social, our study highlights the importance of leveraging refuge use behavior to study the presence of and mechanisms behind non-random social structure and individual-level variation. Our analysis of the impact of stressors on refuge-based social structure further emphasizes the potential of this method to detect environmental or anthropogenic disturbances.

Significance statement

Adaptive and social behavior that affects fitness is now being increasingly incorporated in the conservation and management of wildlife species. However, direct observations of social interactions in species considered to be solitary are difficult, and therefore integration of behavior in conservation and management decisions in such species has been infrequent. For such species, we propose quantifying refuge use behavior as it can provide insights towards their (hidden) social structure, establish relevant contact patterns of infectious disease spread, and provide early warning signals of population stressors. Our study highlights this approach in a long-lived and threatened species, the desert tortoise. We provide evidence toward the presence of and identify mechanisms behind the social structure in desert tortoises formed by their burrow use preferences. We also show how individuals burrow use behavior responds to the presence of population stressors.

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References

  • Bansal S, Khandelwal S, Meyers L A (2009) Exploring biological network structure with clustered random networks. BMC Bioinfo 10:405

    Article  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. https://gephi.org

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bulova S J (1994) Patterns of burrow use by desert tortoises: gender differences and seasonal trends. Herpetol Monogr 8:133–143

    Article  Google Scholar 

  • Bulova S J (1997) Conspecific chemical cues influence burrow choice by desert tortoises (Gopherus agassizii). Copeia 1997(4):802–810

    Article  Google Scholar 

  • Carr JW (2015) MantelTest. http://jwcarr.github.io/MantelTest

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Cooper W E Jr (2015) Escaping from predators: an integrative view of escape decisions. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Croft D P, Krause J, James R (2004) Social networks in the guppy (Poecilia reticulata). Proc R Soc Lond B 271:S516–S519

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Davis S, Abbasi B, Shah S, Telfer S, Begon M (2015) Spatial analyses of wildlife contact networks. J R Soc Interface 20141004(102):12

    Google Scholar 

  • Department of the Interior (1973) Endangered species act. Tech. rep., U.S. Fish and Wildlife Service, Washington, DC

  • 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

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Fox J, Monette G (1992) Generalized collinearity diagnostics. J Am Stat Assoc 87(417):178–183

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Germano J M, Bishop P J (2009) Suitability of amphibians and reptiles for translocation. Conserv Biol 23 (1):7–15

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Girvan M, Newman M E J (2002) Community structure in social and biological networks. P Natl Acad Sci USA 99(12):7821–7826

    Article  CAS  Google Scholar 

  • Godfrey S S (2013) Networks and the ecology of parasite transmission: a framework for wildlife parasitology. Int J Parasitol Parasites Wildl 2:235–245

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Harrell F E (2002) Regression modeling strategies: with applications to linear models, logistic and ordinal regression, and survival analysis, 1st edn. Springer, London

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hinderle D (2011) Desert tortoises (Gopherus agassizii) and translocation: homing, behavior, habitat and shell temperature experiments. Tech. rep., San Diego State University, San Diego

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biomet J 50(3):346–363

    Article  Google Scholar 

  • 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

  • Jachowski D S, Slotow R, Millspaugh J J (2012) Physiological stress and refuge behavior by african elephants. PLoS ONE 7:e31818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Manno T G (2008) Social networking in the Columbian ground squirrel, Spermophilus columbianus. Anim Behav 75(4):1221–1228

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nagy K A, Medica P A (1986) Physiological ecology of desert tortoises in southern Nevada. Herpetologica 42(1):73–92

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Method Ecol Evol 1:103–113

    Article  Google Scholar 

  • Scott J, Carrington P (eds) (2011) The SAGE handbook of social network analysis. SAGE publications, London

    Google Scholar 

  • Singmann H (2013) afex: analysis of factorial experiments, https://cran.r-project.org/web/packages/afex

  • 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

    Article  PubMed  Google Scholar 

  • Wilson D S (1991) Estimates of survival for juvenile gopher tortoises, Gopherus polyphemus. J Herpetol 25 (3):376–379

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Winkelmann R (2003) Econometric analysis of count data. Springer Science & Business Media, Heidelberg

    Book  Google Scholar 

  • Witmer G W (2005) Wildlife population monitoring: some practical considerations. Wildlife Res 32:259–263

    Article  Google Scholar 

  • Zuur A, Ieno E, Elphick C S (2010) A protocol for data exploration to avoid common statistical problems. Method Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

We thank Phil Medica for feedback on a previous version of this manuscript. We thank Ian T. Carroll and anonymous reviewers for helpful comments to improve the quality of the paper. We thank Clarence Everly, Department of Defense, Ft. Irwin National Training Center for the support in acquiring the data analyzed in this paper. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S.Government.

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Authors and Affiliations

  1. Department of Biology, Georgetown University, Washington, DC, USA

    Pratha Sah & Shweta Bansal

  2. Department of Geography, University of Nevada Reno, Reno, NV, USA

    Kenneth E. Nussear

  3. U. S. Geological Survey, Western Ecological Research Center, Las Vegas Field Station, Henderson, NV, USA

    Todd C. Esque & Christina M. Aiello

  4. Department of Biology, Pennsylvania State University, University Park, PA, USA

    Christina M. Aiello & Peter J. Hudson

  5. Fogarty International Center, National Institutes of Health, Bethesda, MD, USA

    Shweta Bansal

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  1. Pratha Sah
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  2. Kenneth E. Nussear
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  4. Christina M. Aiello
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  6. Shweta Bansal
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Correspondence to Shweta Bansal.

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Funding

This work was funded by the National Science Foundation Ecology of Infections Diseases grant 1216054 Invasion and Infection: Translocation and Transmission: An Experimental Study with Mycoplasma in Desert Tortoises. This work was also partially funded by a grant from the Department of Defense, Ft. Irwin National Training Center, and by the Ecosystems Mission Area of the U.S. Geological Survey.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Communicated by: S. J. Downes

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Sah, P., Nussear, K.E., Esque, T.C. et al. Inferring social structure and its drivers from refuge use in the desert tortoise, a relatively solitary species. Behav Ecol Sociobiol 70, 1277–1289 (2016). https://doi.org/10.1007/s00265-016-2136-9

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