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A comparative evaluation of northern and southern Ixodes scapularis questing height and hiding behaviour in the USA

Published online by Cambridge University Press:  10 August 2020

Mackenzie Tietjen*
Affiliation:
Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX77843, USA
Maria D. Esteve-Gasent
Affiliation:
Department of Veterinary Pathobiology, Texas A&M University, 4467 TAMU, College Station, TX77843, USA
Andrew Y. Li
Affiliation:
USDA, ARS, Invasive Insect Biocontrol and Behavior Laboratory, 10300 Baltimore Avenue, Beltsville, MD20705, USA
Raul F. Medina
Affiliation:
Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX77843, USA
*
Author for correspondence: Mackenzie Tietjen, E-mail: mackenzie.tietjen@usda.gov

Abstract

Ticks display a distinct type of host-seeking behaviour called questing. It has been proposed that the questing behaviour of Ixodes scapularis explains the geographic variation in Lyme disease (LD) risk in the eastern USA because the northern population has been shown to quest more often than the southern population. The height at which questing occurs is variable and this study aimed to characterize questing height for I. scapularis. Ticks were collected from a northern and southern state (i.e. Maryland and Texas) and bioassays were conducted. We report that nymphs from Texas quested at lower heights compared to nymphs from Maryland. In addition, only Texas nymphs exhibited a behaviour we call ‘hiding behaviour’. These results may reflect the different composition of hosts between these two areas as the south has a higher abundance of lizards. In contrast, there was no significant difference in questing height between Maryland adults and Texas adults which was to be expected since adults are feeding on white-tailed deer in both locations. If all southern I. scapularis nymphs are questing at lower heights, this might make them less likely to come into contact with humans and this may be contributing to the geographical difference in LD prevalence.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

Current address: USDA–ARS Knipling–Bushland U.S. Livestock Insects Research Laboratory, 2700 Fredericksburg Rd. Kerrville, TX 78028, USA.

This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the USDA for its use. The USDA is an equal opportunity provider and employer.

References

Allan, SA, Simmons, LA and Burridge, MJ (2001) Ixodid ticks on white-tailed deer and feral swine in Florida. Journal of Vector Ecology 26, 93102.Google ScholarPubMed
Apperson, CS, Levine, JF, Evans, TL, Braswell, A and Heller, J (1993) Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina, USA. Experimental and Applied Acarology 17, 719731.Google ScholarPubMed
Arsnoe, IM, Hickling, GJ, Ginsberg, HS, McElreath, R and Tsao, JI (2015) Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human Lyme disease risk. PLoS ONE 10, 21.CrossRefGoogle ScholarPubMed
Arsnoe, I, Tsao, JI and Hickling, GJ (2019) Nymphal Ixodes scapularis questing behavior explains geographic variation in Lyme borreliosis risk in the eastern United States. Ticks and Tick-Borne Diseases 10, 553563.CrossRefGoogle ScholarPubMed
Barker, SC and Walker, AR (2014) Ticks of Australia. The species that infest domestic animals and humans. Zootaxa 3816, 1144.CrossRefGoogle Scholar
Benoit, JB, Lopez-Martinez, G, Philips, SA, Elnitsky, MA, Yoder, JA, Lee, RE and Denlinger, DL (2008) The seabird tick, Ixodes uriae, uses uric acid in penguin guano as a kairomone and guanine in tick feces as an assembly pheromone on the Antarctic Peninsula. Polar Biology 31, 1445.CrossRefGoogle Scholar
Blanquart, F, Kaltz, O, Nuismer, SL and Gandon, S (2013) A practical guide to measuring local adaptation. Ecology Letters 16, 11951205.CrossRefGoogle ScholarPubMed
Brinton, EP, Beck, DE and Allred, DM (1965) Identification of the adults, nymphs and larvae of ticks of the genus Dermacentor Koch (Ixodidae) in the western United States. Brigham Young University Science Bulletin. Biological Series 5, 1.Google Scholar
Camin, JH and Drenner, RW (1978) Climbing behavior and host-finding of larval rabbit ticks (Haemaphysalis leporispalustris). Journal of Parasitology 64, 905909.Google Scholar
Carey, MG, Carey, AB, Main, AJ, Krinsky, WL and Sprance, HE (1981) Ixodes dammini (Acari: Ixodidae) in forests in Connecticut. Journal of Medical Entomology 18, 175176.CrossRefGoogle ScholarPubMed
Carroll, J, Klun, J and Schmidtmann, E (1995) Evidence for kairomonal influence on selection of host-ambushing sites by adult Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 32, 119125.CrossRefGoogle Scholar
Centers for Disease Control and Prevention (2017) Lyme disease. In reported cases of Lyme disease by state of locality, 2006–2016. Available at www.cdc.gov/lyme/stats/tables.html (accessed May 20 2019).Google Scholar
Charlwood, J (1996) Biological variation in Anopheles darlingi Root. Memórias do Instituto Oswaldo Cruz 91, 391398.CrossRefGoogle ScholarPubMed
Clifford, CM, Anastos, G and Elbl, A (1961) The larval Ixodid ticks of the eastern United States (Acarina: Ixodidae). Miscellaneous Publications of The Entomological Society of America 2, 213237.Google Scholar
DeFoliart, G, Grimstad, P and Watts, D (1987) Advances in mosquito-borne arbovirus/vector research. Annual Review of Entomology 32, 479505.CrossRefGoogle ScholarPubMed
Diuk-Wasser, MA, Gatewood, AG, Cortinas, MR, Yaremych-Hamer, S, Tsao, J, Kitron, U, Hickling, G, Brownstein, JS, Walker, E, Piesman, J and Fish, D (2006) Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. Journal of Medical Entomology 43, 166176.CrossRefGoogle Scholar
Drew, ML and Samuel, W (1985) Factors affecting transmission of larval winter ticks, Dermacentor albipictus (Packard), to moose, Alces alces L., in Alberta, Canada. Journal of Wildlife Diseases 21, 274282.CrossRefGoogle Scholar
Durden, LA and Keirans, JE (1996) Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medical/veterinary importance, Entomological Society of America.Google Scholar
Durden, LA, Luckhart, S, Mullen, GR and Smith, S (1991) Tick infestations of white-tailed deer in Alabama. Journal of Wildlife Diseases 27, 606614.CrossRefGoogle ScholarPubMed
Durden, LA, Oliver, JH, Banks, CW and Vogel, GN (2002) Parasitism of lizards by immature stages of the blacklegged tick, Ixodes scapularis (Acari: Ixodidae). Experimental and Applied Acarology 26, 257266.CrossRefGoogle Scholar
Eisen, RJ, Eisen, L and Beard, CB (2016) County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. Journal of Medical Entomology 53, 349386.CrossRefGoogle ScholarPubMed
Falco, RC and Fish, D (1991) Horizontal movement of adult Ixodes dammini (Acari: Ixodidae) attracted to CO2-baited traps. Journal of Medical Entomology 28, 726729.CrossRefGoogle ScholarPubMed
Falco, RC and Fish, D (1992) A comparison of methods for sampling the deer tick, Ixodes dammini, in a Lyme disease endemic area. Experimental and Applied Acarology 14, 165173.Google Scholar
Feria-Arroyo, TP, Castro-Arellano, I, Gordillo-Perez, G, Cavazos, AL, Vargas-Sandoval, M, Grover, A, Torres, J, Medina, RF, de León, AAP and Esteve-Gassent, MD (2014) Implications of climate change on the distribution of the tick vector Ixodes scapularis and risk for Lyme disease in the Texas-Mexico transboundary region. Parasites & Vectors 7, 199.CrossRefGoogle ScholarPubMed
Fish, D and Dowler, RC (1989) Host associations of ticks (Acari: Ixodidae) parasitizing medium-sized mammals in a Lyme disease endemic area of southern New York. Journal of Medical Entomology 26, 200209.CrossRefGoogle Scholar
Friard, O and Gamba, M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution 7, 13251330.CrossRefGoogle Scholar
Garvin, SD, Noden, BH, Dillwith, JW, Fox, SF, Payton, ME and Barker, RW (2015) Sylvatic infestation of Oklahoma reptiles with immature Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 52, 873878.CrossRefGoogle Scholar
Giery, ST and Ostfeld, RS (2007) The role of lizards in the ecology of Lyme disease in two endemic zones of the northeastern United States. Journal of Parasitology 93, 511517.CrossRefGoogle ScholarPubMed
Ginsberg, HS, Albert, M, Acevedo, L, Dyer, MC, Arsnoe, IM, Tsao, JI, Mather, TN and LeBrun, RA (2017) Environmental factors affecting survival of immature Ixodes scapularis and implications for geographical distribution of Lyme disease: the climate/behavior hypothesis. PLoS ONE 12, e0168723.Google ScholarPubMed
Goddard, J and Piesman, J (2006) New records of immature Ixodes scapularis from Mississippi. Journal of Vector Ecology 31, 421422.CrossRefGoogle ScholarPubMed
Godfrey, SS, Nelson, NJ and Bull, CM (2011) Microhabitat choice and host-seeking behaviour of the tuatara tick, Amblyomma sphenodonti (Acari: Ixodidae). New Zealand Journal of Ecology 35, 5260.Google Scholar
Goltz, L and Goddard, J (2013) Observations on the seasonality of Ixodes scapularis Say in Mississippi, USA. Systematic and Applied Acarology 18, 212217.CrossRefGoogle Scholar
Gulia-Nuss, M, Nuss, AB, Meyer, JM, Sonenshine, DE, Roe, RM, Waterhouse, RM, Sattelle, DB, de la Fuente, J, Ribeiro, JM, Megy, K, Thimmapuram, J, Miller, JR, Walenz, BP, Koren, S, Hostetler, JB, Thiagarajan, M, Joardar, VS, Hannick, LI, Bidwell, S, Hammond, MP, Young, S, Zeng, Q, Abrudan, JL, Almeida, FC, Ayllon, N, Bhide, K, Bissinger, BW, Bonzon-Kulichenko, E, Buckingham, SD, Caffrey, DR, Caimano, MJ, Croset, V, Driscoll, T, Gilbert, D, Gillespie, JJ, Giraldo-Calderon, GI, Grabowski, JM, Jiang, D, Khalil, SMS, Kim, D, Kocan, KM, Koci, J, Kuhn, RJ, Kurtti, TJ, Lees, K, Lang, EG, Kennedy, RC, Kwon, H, Perera, R, Qi, Y, Radolf, JD, Sakamoto, JM, Sanchez-Gracia, A, Severo, MS, Silverman, N, Simo, L, Tojo, M, Tornador, C, Van Zee, JP, Vazquez, J, Vieira, FG, Villar, M, Wespiser, AR, Yang, Y, Zhu, J, Arensburger, P, Pietrantonio, PV, Barker, SC, Shao, R, Zdobnov, EM, Hauser, F, Grimmelikhuijzen, CJP, Park, Y, Rozas, J, Benton, R, Pedra, JHF, Nelson, DR, Unger, MF, Tubio, JMC, Tu, Z, Robertson, HM, Shumway, M, Sutton, G, Wortman, JR, Lawson, D, Wikel, SK, Nene, VM, Fraser, CM, Collins, FH, Birren, B, Nelson, KE, Caler, E and Hill, CA (2016) Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nature Communications 7, 113. doi: 10.1038/ncomms10507Google ScholarPubMed
Hamer, SA, Tsao, JI, Walker, ED and Hickling, GJ (2010) Invasion of the Lyme disease vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity. Ecohealth 7, 4763.CrossRefGoogle ScholarPubMed
Hinckley, AF, Connally, NP, Meek, JI, Johnson, BJ, Kemperman, MM, Feldman, KA, White, JL and Mead, PS (2014) Lyme disease testing by large commercial laboratories in the United States. Clinical Infectious Diseases 59, 676681.CrossRefGoogle ScholarPubMed
James, AM and Oliver, JH Jr (1990) Feeding and host preference of immature Ixodes dammini, I. scapularis, and I. pacificus (Acari: Ixodidae). Journal of Medical Entomology 27, 324330.CrossRefGoogle Scholar
Keirans, JE and Clifford, CM (1978) The genus Ixodes in the United States: a scanning electron microscope study and key to the adults. Journal of Medical Entomology 15, 138.Google Scholar
Keirans, JE and Durden, LA (1998) Illustrated key to nymphs of the tick genus Amblyomma (Acari: Ixodidae) found in the United States. Journal of Medical Entomology 35, 489495.CrossRefGoogle ScholarPubMed
Keirans, JE and Litwak, TR (1989) Pictorial key to the adults of hard ticks, family Ixodidae (Ixodida: Ixodoidea), east of the Mississippi River. Journal of Medical Entomology 26, 435448.Google Scholar
Keirans, JE, Hutcheson, HJ, Durden, LA and Klompen, JSH (1996) Ixodes (Ixodes) scapularis (Acari: Ixodidae): redescription of all active stages, distribution, hosts, geographical variation, and medical and veterinary importance. Journal of Medical Entomology 33, 297318.CrossRefGoogle ScholarPubMed
Khatchikian, CE, Prusinski, MA, Stone, M, Backenson, PB, Wang, IN, Foley, E, Seifert, SN, Levy, MZ and Brisson, D (2015) Recent and rapid population growth and range expansion of the Lyme disease tick vector, Ixodes scapularis, in North America. Evolution 69, 16781689.Google ScholarPubMed
Kocan, AA, Mukolwe, SW, Murphy, GL, Barker, RW and Kocan, KM (1992) Isolation of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) from Ixodes scapularis and Dermacentor albipictus ticks (Acari: Ixodide) in Oklahoma. Journal of Medical Entomology 29, 630633.CrossRefGoogle Scholar
Kollars, TM, Oliver, JH, Kollars, PG and Durden, LA (1999) Seasonal activity and host associations of Ixodes scapularis (Acari: Ixodidae) in southeastern Missouri. Journal of Medical Entomology 36, 720726.CrossRefGoogle Scholar
Larson, RT, Lee, X, Zembsch, T, Bron, GM and Paskewitz, SM (2019) Immature Ixodes scapularis (Acari: Ixodidae) collected from Peromyscus leucopus (Rodentia: Cricetidae) and Peromyscus maniculatus (Rodentia: Cricetidae) nests in northern Wisconsin. Journal of Medical Entomology 57, 304307.CrossRefGoogle Scholar
Lees, AD (1948) The sensory physiology of the sheep tick, Ixodes ricinus. Journal of Experimental Biology 25, 145207.Google Scholar
Levine, JF, Apperson, CS, Howard, P, Washburn, M and Braswell, AL (1997) Lizards as hosts for immature Ixodes scapularis (Acari: Ixodidae) in North Carolina. Journal of Medical Entomology 34, 594598.CrossRefGoogle Scholar
Lounibos, LP and Conn, JE (2000) Malaria vector heterogeneity in South America. American Entomologist 46, 238249.CrossRefGoogle Scholar
Loye, JE and Lane, RS (1988) Questing behavior of Ixodes pacificus (Acari: Ixodidae) in relation to meteorological and seasonal factors. Journal of Medical Entomology 25, 391398.CrossRefGoogle ScholarPubMed
Macarthur, R and Macarthur, JW (1961) On bird species diversity. Ecology 42, 594, –&.CrossRefGoogle Scholar
Mather, TN, Wilson, ML, Moore, SI, Ribeiro, JMC and Spielman, A (1989) Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). American Journal of Epidemiology 130, 143150.Google Scholar
Mejlon, HA and Jaenson, TGT (1997) Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae). Experimental and Applied Acarology 21, 747754.Google Scholar
Mitchell, L and Rockett, L (1979) Vertical stratification preferences of adult female mosquitoes in a sylvan habitat (Diptera: Culicidae). The Great Lakes Entomologist 12, 219223.Google Scholar
Needham, GR and Teel, PD (1991) Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36, 659681.Google ScholarPubMed
Nelson, CA, Saha, S, Kugeler, KJ, Delorey, MJ, Shankar, MB, Hinckley, AF and Mead, PS (2015) Incidence of clinician-diagnosed Lyme disease, United States, 2005–2010. Emerging Infectious Diseases 21, 16251631.CrossRefGoogle ScholarPubMed
Norris, DE, Klompen, JSH, Keirans, JE and Black, WC (1996) Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. Journal of Medical Entomology 33, 7889.CrossRefGoogle ScholarPubMed
Olive, CW (1980) Foraging specialization in orb-weaving spiders. Ecology 61, 11331144.CrossRefGoogle Scholar
Oliver, JH (1996) Lyme borreliosis in the southern United States: a review. Journal of Parasitology 82, 926935.CrossRefGoogle ScholarPubMed
Oliver, JH, Chandler, FW, Luttrell, MP, James, AM, Stallknecht, DE, McGuire, BS, Hutcheson, HJ, Cummins, GA and Lane, RS (1993 a) Isolation and transmission of the Lyme disease spirochete from the Southeastern United States. Proceedings of the National Academy of Sciences USA 90, 73717375.CrossRefGoogle ScholarPubMed
Oliver, JH, Cummins, GA and Joiner, MS (1993 b) Immature Ixodes scapularis (Acari: Ixodidae) parasitizing lizards from the southeastern USA. Journal of Parasitology 79, 684689.CrossRefGoogle Scholar
Oliver, JH, Owsley, MR, Hutcheson, HJ, James, AM, Chen, CS, Irby, WS, Dotson, EM and McLain, DK (1993 c) Conspecificity of the ticks Ixodes scapularis and Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 30, 5463.CrossRefGoogle Scholar
Oliver, JH, Chandler, FW, James, AM, Sanders, FH, Hutcheson, HJ, Huey, LO, McGuire, BS and Lane, RS (1995) Natural occurrence and characterization of the Lyme disease Spirochete, Borrelia burgdorferi, in cotton rats (Sigmodon hispidus) from Georgia and Florida. Journal of Parasitology 81, 3036.CrossRefGoogle ScholarPubMed
Oorebeek, M, Sharrad, R and Kleindorfer, S (2009) What attracts larval Ixodes hirsti (Acari: Ixodidae) to their host? Parasitology Research 104, 623.CrossRefGoogle ScholarPubMed
Pianka, ER (1977) Reptilian species diversity. In Biology of the Reptilia. New York, NY, USA: Academic Press, Vol. 7, pp. 134.Google Scholar
Piesman, J and Spielman, A (1979) Host-associations and seasonal abundance of immature Ixodes dammini in southeastern Massachusetts. Annals of the Entomological Society of America 72, 829832.CrossRefGoogle Scholar
Powell, R, Conant, R and Collins, JT (2016) A Field Guide to Reptiles & Amphibians: Eastern and Central North America, 4th Edn. Boston: Houghton Mifflin.Google Scholar
Reid, FA (2006) A Field Guide to Mammals of North America. New York, NY: Houghton Mifflin.Google Scholar
Rich, SM, Caporale, DA, Telford, SR, Kocher, TD, Hartl, DL and Spielman, A (1995) Distribution of the Ixodes ricinus-like ticks of eastern North America. Proceedings of the National Academy of Sciences USA 92, 62846288.CrossRefGoogle ScholarPubMed
Rodgers, SE, Zolnik, CP and Mather, TN (2007) Duration of exposure to suboptimal atmospheric moisture affects nymphal blacklegged tick survival. Journal of Medical Entomology 44, 372375.CrossRefGoogle ScholarPubMed
Rogers, JS (1976) Species density and taxonomic diversity of Texas amphibians and reptiles. Systematic Zoology 25, 2640.CrossRefGoogle Scholar
Sakamoto, JM, Goddard, J and Rasgon, JL (2014) Population and demographic structure of Ixodes scapularis Say in the eastern United States. PLoS ONE 9, 18.CrossRefGoogle ScholarPubMed
Schwartz, AM, Hinckley, AF, Mead, PS, Hook, SA and Kugeler, KJ (2017) Surveillance for Lyme disease – United States, 2008–2015. MMWR Surveillance Summaries 66, 112.Google ScholarPubMed
Stafford, KCI (1994) Survival of immature Ixodes scapularis (Acari: Ixodidae) at different relative humidities. Journal of Medical Entomology 31, 310314.CrossRefGoogle ScholarPubMed
Teltow, GJ, Fournier, PV and Rawlings, JA (1991) Isolation of Borrelia burgdorferi from arthropods collected in Texas. American Journal of Tropical Medicine and Hygiene 44, 469474.CrossRefGoogle ScholarPubMed
Tietjen, M, Esteve-Gassent, MD and Medina, RF (2019) Searching for the immature stages of Ixodes scapularis (Acari: Ixodidae) in leaf litter and soil in Texas. Journal of Medical Entomology 56, 3539.CrossRefGoogle ScholarPubMed
Tsunoda, T and Tatsuzawa, S (2004) Questing height of nymphs of the bush tick, Haemaphysalis longicornis, and its closely related species, H. mageshimaensis: correlation with body size of the host. Parasitology 128, 503509.CrossRefGoogle ScholarPubMed
Vail, SG and Smith, G (2002) Vertical movement and posture of blacklegged tick (Acari: Ixodidae) nymphs as a function of temperature and relative humidity in laboratory experiments. Journal of Medical Entomology 39, 842846.CrossRefGoogle ScholarPubMed
Van Zee, J, Black, WC, Levin, M, Goddard, J, Smith, J and Piesman, J (2013) High SNP density in the blacklegged tick, Ixodes scapularis, the principal vector of Lyme disease spirochetes. Ticks and Tick-Borne Diseases 4, 6371.CrossRefGoogle ScholarPubMed
Van Zee, J, Piesman, JF, Hojgaard, A and Black, WC (2015) Nuclear markers reveal predominantly north to south gene flow in Ixodes scapularis, the tick vector of the Lyme disease spirochete. PLoS ONE 10, 22.CrossRefGoogle ScholarPubMed
Watson, TG and Anderson, RC (1976) Ixodes scapularis say on white-tailed deer (Odocoileus virginianus) from Long Point, Ontario. Journal of Wildlife Diseases 12, 6671.CrossRefGoogle ScholarPubMed
Wilkinson, P (1953) Observations on the sensory physiology and behaviour of larvae of the cattle tick, Boophilus microplus (Can.)(Ixodidae). Australian Journal of Zoology 1, 345356.CrossRefGoogle Scholar
Williamson, PC, Billingsley, PM, Teltow, GJ, Seals, JP, Turnbough, MA and Atkinson, SF (2010) Borrelia, Ehrlichia, and Rickettsia Spp. in ticks removed from persons, Texas, USA. Emerging Infectious Diseases 16, 441446.Google ScholarPubMed
Wilson, DE and Reeder, DM (2005) Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd Edn. Baltimore, MD: Johns Hopkins University Press.Google Scholar
Wilson, ML, Litwin, TS, Gavin, TA, Capkanis, MC, Maclean, DC and Spielman, A (1990) Host-dependent differences in feeding and reproduction of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 945954.Google Scholar
Wilson, DE, Cole, RF, Nichols, JD and Foster, MS (1996) Measuring and Monitoring Biological Diversity, Standard Methods for Mammals. Washington, D.C: Smithosonian Institution Press.Google Scholar