Human disturbance influences reproductive success and growth rate in California sea lions (Zalophus californianus)

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  French, Susannah S ^a   González Suárez, Manuela ^b,c,d   Young, Julie K ^b,e   Durham, Susan ^a   Gerber, Leah R ^b  

^a UTAH STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UPMC University Paris 06   (France)

^d DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^e NATIONAL WILDLIFE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; ENVIRONMENTAL IMPACT; FEMALE; GROWTH RATE; HUMAN ACTIVITIES; LIFE HISTORY; MALE; MEXICO; NEWBORN; NONHUMAN; POPULATION GROWTH; REPRODUCTION; SEAL; ZALOPHUS CALIFORNIANUS; ANIMAL; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; HUMAN; PHYSIOLOGY; POPULATION DYNAMICS; TIME; UNITED STATES;

ANIMALIA; VERTEBRATA; ZALOPHUS; ZALOPHUS CALIFORNIANUS;

ANIMALS; ANIMALS, NEWBORN; CALIFORNIA; FEMALE; GEOGRAPHY; HUMAN ACTIVITIES; HUMANS; MALE; POPULATION DYNAMICS; REPRODUCTION; SEA LIONS; TIME FACTORS;

EID: 79952754646     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017686     Document Type: Article

References (66)

1. Flather CH, Cordell HK, (1995) Outdoor recreation: historical and anticipated trends. In: Knight RL, Gutzwiller KJ, editors. Wildlife and recreationists: coexistence through management and research Washington DC Island Press pp. 3-16.
2. Williams R, Lusseau D, Hammond PS, (2006) Estimating relative energetic costs of human disturbance to killer whales (Ornicus orca). Biol Conserv 133: 301-311.
3. Rode KD, Farley SD, Fortín J, Robbins CT, (2007) Nutritional consequences of experimentally introduced tourism in brown bears. J Wildl Manage 71: 929-939.
4. Boydston EE, Kapheim KM, Watts HE, Szykman M, Holekamp KE, (2003) Altered behaviour in spotted hyenas associated with increased human activity. Anim Conserv 6: 207-219.
5. Gerodette T, Gilmartin WG, (1990) Demographic consequences of changing pupping and hauling sites of the Hawaiian monk seal. Conserv Biol 4: 423-430.
6. Constantine R, Brunton DH, Dennis T, (2004) Dolphin-watching tour boats change bottlenose dolphin (Tursiops truncatus) behaviour. Biol Conserv 117: 299-307.
7. Romero LM, Wikelski M, (2002) Exposure to tourism reduces stress-induced corticosterone levels in Galapagos marine iguanas. Biol Conserv 108: 371-374.
8. Walker BG, Boersma PD, Wingfield JC, (2005) Physiological and behavioral differences in Magellanic Penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv Biol 19: 1571-1577.
9. Walker BG, Boersma PD, Wingfield JC, (2006) Habituation of adult magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conserv Biol 20: 146-154.
10. Mullner A, Linsenmair KE, Wikelski M, (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118: 549-558.
11. Creel S, Fox JE, Hardy A, Sands J, Garrott B, et al. (2002) Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv Biol 16: 809-814.
12. Riedman M, (1990) The pinnipeds: seals, sea lions, and walruses. Berkeley University of California Press.
13. Labrada-Martagon V, Aurioles-Gamboa D, Martinez-Diaz SF, (2005) Natural and human disturbance in a rookery of the California sea lion (Zalophus californianus californianus) in the Gulf of California, Mexico. Latin Am J Aquatic Mamm 4: 175-186.
14. Velarde E, Anderson DW, (1994) Conservation and management of seabird islands in the Gulf of California: setbacks and successes. In: Nettleship DN, Burger J, Gochfeld M, editors. Seabirds and islands: treats, case studies, and action plans Cambridge ICBP Technical Publication pp. 229-243.
15. Carabias-Lillo J, Maza-Elvira JDL, Gutierrez-Carbonell D, Gomez-Cruz M, Anaya-Reyna G, et al. (2000) Programa de Manejo Area de Protection de Flora y Fauna Islas de Golfo de California, Mexico. Mexico City Comision Nacional de Areas Naturales Protegidas.
16. UNESCO Decision: 29COM 8B.9. Nominations of natural properties to the World Heritage list (islands and protected Areas of the Gulf of California).http://whc.unesco.org/en/decisions/472/.
17. Tershy BR, Breese D, Croll DA, (1997) Human perturbations and conservation for San Pedro Mártir Island, Islas del Golfo de California Reserve, Mexico. Environ Conserv 24: 261-270.
18. Szteren D, Aurioles D, Gerber LR, (2006) Population status and trends of the California sea lion (Zalophus californianus californianus) in the Gulf of California, México. In: Trites AW, Atkinson SP, DeMaster DP, Fritz LW, Gelatt TS, editors. Sea lions of the world Fairbanks Alaska Sea Grant College Program, University of Alaska Fairbanks pp. 369-384.
19. Crone EE, (2001) Is survivorship a better fitness surrogate than fecundity? Evolution 55: 2611-2614.
20. Heppell SS, Caswell H, Crowder LB, (2000) Life histories and elasticity patterns: Perturbation analysis for species with minimal demographic data. Ecology 81: 654-665.
21. Saether BE, Bakke O, (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81: 642-653.
22. Barlow SM, Knight AF, Sullivan FM, (1978) Delay in postnatal growth and development of offspring produced by maternal restraint stress during pregnancy in the rat. Teratology 18: 211-218.
23. Hayward LS, Wingfield JC, (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135: 365-371.
24. Tilbrook AJ, Turner AI, Clarke IJ, (2000) Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Reprod 5: 105-113.
25. Garcia-Aguilar MC, Aurioles-Gamboa D, (2003) Breeding season of the California sea lion (Zalophus californianus) in the Gulf of California, Mexico. Aq Mamm 29: 67-76.
26. Dhabhar FS, McEwen BS, (1997) Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11: 286-306.
27. Moore IT, Jessop TS, (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43: 39-47.
28. Romero LM, (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128: 1-24.
29. Dendrinos P, Karamanlidis AA, Kotomatas S, Legakis A, Tounta E, et al. (2007) Pupping habitat use in the Mediterranean monk seal: a long-term study. Mar Mamm Sci 23: 615-628.
30. Harrington FH, Veitch AM, (1992) Calving success of woodland caribou exposed to low-level jet fighter overflights. Arctic 45: 213-218.
31. Kenyon KW, (1972) Man versus monk seal. J Mammal 53: 687-696.
32. Phillips GE, Alldredge AW, (2000) Reproductive success of elk following disturbance by humans during calving season. J Wildl Manage 64: 521-530.
33. White CM, Thurow TL, (1985) Reproduction of ferruginous hawks exposed to controlled disturbance. Condor 87: 14-22.
34. Yarmoloy PA, Bayer M, Geist V, (1988) Behavior responses and reproduction of mule deer, Odocoileus hemionus, does following experimental harassment with an all-terrain vehicle. Can Field Nat 102: 425-429.
35. Ono KA, Boness DJ, (1996) Sexual dimorphism in sea lion pups: Differential maternal investment, or sex-specific differences in energy allocation? Behav Ecol Sociobiol 38: 31-41.
36. Boness DJ, Oftedal OT, Ono KA, (1991) The effects of El Niño on pup development in the California sea lion (Zalophus californianus). I. Early postnatal growth. In: Trillmich F, Ono KA, editors. Pinnipeds and El Niño New York Springer-Verlag pp. 173-179.
37. Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ, (2007) Elevated hormonal stress response and reduced reproductive output in Yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol 152: 54-63.
38. Kight CR, Swaddle JP, (2007) Associations of anthropogenic activity and disturbance with fitness metrics of eastern bluebirds (Sialia sialis). Biol Conserv 138: 189-197.
39. Luque SP, Aurioles-Gamboa D, (2001) Sex differences in body size and body condition of California sea lion (Zalophus californianus) pups from the Gulf of California. Mar Mamm Sci 17: 147-160.
40. Pickering AD, Pottinger TG, Sumpter JP, Carragher JF, Le Bail PY, (1991) Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 83: 86-93.
41. Seggie JA, Brown GM, (1975) Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can J Physiol Pharm 53: 629-637.
42. Salvante KG, Williams TD, (2003) Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. Gen Comp Endocrinol 130: 205-214.
43. Taylor EN, Malawy MA, Browning DM, Lemar SV, DeNardo DF, (2005) Effects of food supplementation on the physiological ecology of female Western diamond-backed rattlesnakes (Crotalus atrox). Oecologia 144: 206-213.
44. Wikelski M, Carrillo V, Trillmich F, (1997) Energy limits to body size in a grazing reptile, the Galapagos marine iguana. Ecology 78: 2204-2217.
45. Le Boeuf BJ, Aurioles D, Condit R, Fox C, Gisiner R, et al. (1983) Size and distribution of the California sea lion population in Mexico. Proc Calif Acad Sci 43: 77-85.
46. Gerber LR, (2006) Including behavioral data in demographic models improves estimates of population viability. Front Ecol Environ 4: 419-427.
47. Jacobs DF, Hernandez-Camacho CJ, Young JK, Gerber LR, (2009) Determinants of outcomes of agonistic interactions among male California sea lions (Zalophus californianus). J Mammal 89: 1212-1217.
48. Robertson KL, Runcorn CW, Young JK, Gerber LR, (2008) Spatial and temporal patterns of territory use of male California sea lions (Zalophus californianus) in the Gulf of California, Mexico. Can J Zool 86: 237-244.
49. Young JK, González-Suárez M, Gerber LR, (2008) Determinants of agonistic interactions in California sea lions. Behaviour 145: 1797-1810.
50. González-Suárez M, Gerber LR, (2008) Habitat preferences of California sea lions: implications for conservation. J Mammal 89: 1521-1528.
51. Labrada-Martagon V, (2003) Influencia del turismo sobre la conducta del lobo marino de California, Zalophus californianus, en la lobera Los Islotes, Baja California Sur, Mexico. Centro Interdisciplinario de Ciencias Marinas. La Paz Instituto Politecnico Nacional.
52. Demas, GE, (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45: 173-180.
53. Demas, GE, Drazen, DL, Nelson, RJ, (2003) Reductions in total body fat decrease humoral immunity. Proc Roy Soc B-Biol Sci 270: 905-911.
54. French, SS, DeNardo, DF, Moore, MC, (2007) Trade-offs between the reproductive and immune systems: Facultative responses to resources or obligate responses to reproduction? Am Nat 170: 79-89.
55. Lourdais O, Bonnet X, Shine R, Taylor EN, (2003) When does a reproducing female viper (Vipera aspis) 'decide' on her litter size? J Zool 259: 123-129.
56. Pauli JN, Buskirk SW, (2007) Risk-disturbance overrides density dependence in a hunted colonial rodent, the black-tailed prairie dog Cynomys ludovicianus. J Appl Ecol 44: 1219-1230.
57. Castellini MA, Calkins DG, (1993) Mass estimates using body morphology in Steller sea lions. Mar Mamm Sci 9: 48-54.
58. Castellini MA, Kooyman GL, (1990) Length, Girth and Mass Relationships in Weddell Seals (Leptonychotes weddellii). Mar Mamm Sci 6: 75-77.
59. Bliese PD, Ployhart RE, (2002) Growth modeling using random coefficient models: Model building, testing, and illustrations. Organ Res Meth 5: 362-387.
60. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O, (2006) SAS® for Mixed Models, Second Edition. Cary, NC SAS Institute Inc.
61. Day RW, Quinn GP, (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monog 59: 433-463.
62. Hurlbert SH, Lombardi CM, (2009) Final collapse of the Neyman-Pearson decision theoretic framework and rise of the neoFisherian. Ann Zool Fenn 46: 311-349.
63. Caswell H, (2001) Matrix population models. Construction,analysis,and interpretation Sunderland Sinauer.
64. Wielgus J, Gonzalez-Suarez M, Aurioles-Gamboa D, Gerber LR, (2008) A noninvasive demographic assessment of sea lions based on stage-specific abundances. Ecol Applic 18: 1287-1296.
65. Gonzalez-Suarez M, Flatz R, Aurioles-Gamboa D, Hedrick PW, Gerber LR, (2009) Isolation by distance among California sea lion populations in Mexico: redefining management stocks. Mol Ecol 18: 1088-1099.
66. Gonzalez-Suarez M, McCluney KE, Aurioles D, Gerber L, (2006) Incorporating uncertainty in spatial structure for viability predictions: a case study of California sea lions (Zalophus californianus californianus). Anim Conserv 9: 356-356.