SpringerLink
Log in

Cascading impacts of anthropogenically driven habitat loss: deforestation, flooding, and possible lead poisoning in howler monkeys (Alouatta pigra)

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

To construct informed conservation plans, researchers must go beyond understanding readily apparent threats such as habitat loss and bush-meat hunting. They must predict subtle and cascading effects of anthropogenic environmental modifications. This study considered a potential cascading effect of deforestation on the howler monkeys (Alouatta pigra) of Balancán, Mexico. Deforestation intensifies flooding. Thus, we predicted that increased flooding of the Usumacinta River, which creates large bodies of water that slowly evaporate, would produce increased lead content in the soils and plants, resulting in lead exposure in the howler monkeys. The average lead levels were 18.18 ± 6.76 ppm in the soils and 5.85 ± 4.37 ppm in the plants. However, the average lead content of the hair of 13 captured howler monkeys was 24.12 ± 5.84 ppm. The lead levels in the animals were correlated with 2 of 15 blood traits (lactate dehydrogenase and total bilirubin) previously documented to be associated with exposure to lead. Our research illustrates the urgent need to set reference values indicating when adverse impacts of high environmental lead levels occur, whether anthropogenic or natural, and the need to evaluate possible cascading effects of deforestation on primates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allard P, Fairbrother A, Hope BK, Hull RN, Johnson MS, Kapustka L, Mann G, McDonald B, Shample BE (2010) Recommendations for the development and application of wildlife toxicity reference values. Integr Environ Assess Manag 6:28–37

    CAS  PubMed  Google Scholar 

  • Améndola-Pimenta M, García-Feria L, Serio-Silva JC, Rico-Gray V (2009) Noninvasive collection of fresh hairs from free-ranging howler monkeys for DNA extraction. Am J Primatol 71:359–363

    Article  PubMed  Google Scholar 

  • Balagangatharathilagar M, Swarup D, Patra RC, Dwivedi SK (2006) Blood lead level in dogs from urban and rural areas of India and its relation to animal and environmental variables. Sci Total Environ 359:130–134

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya A, Shukla R, Auyang ED, Dietrich KN, Bornschein R (2007) Effect of succimer chelation therapy on postural balance and gain outcomes in children with early exposure to environmental lead. Neurotoxicology 28:686–695

    Article  CAS  PubMed  Google Scholar 

  • Bonilla-Sanchez YM, Serio-Silva JC, Pozo-Montuy G, Chapman CA (2012) Does the expansion of eucalyptus plantations signal hope or despair for black howler monkeys? Int J Primatol 33:233–245

    Article  Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244

    Article  Google Scholar 

  • Chapman CA, Chapman LJ (2003) Deforestation in tropical Africa: impacts on aquatic ecosystems. In: Crisman TL, Chapman LJ, Chapman CA, Kaufman LS (eds) Conservation, ecology, and management of African fresh water. University Presses of Florida, Gainesville, pp 229–246

    Google Scholar 

  • Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10:16–33

    Article  Google Scholar 

  • Comision Nacional del Agua (CNA) (2010). Retrived 25 Aug 2014 at http://www.cna.gob.mx

  • D’Have H, Scheirs J, Mubiana V, Verhagen R, Blust R, de Coen W (2005) Nondestructive pollution exposure assessment in the European hedgehog (Erinaceus eropaeus): I. Relationships between concentrations of metals and arsenic in hair, spines and soil. Environ Toxicol Chem 24:2356–2364

    Article  PubMed  Google Scholar 

  • Díaz-López HM (2010) Uso del espacio horizontal y vertical por Alouatta pigra en el dosel de plantaciones agroforestales de eucalipto (Eucalyptus grandis) en Balancán. Universidad Juárez Autónoma de Tabasco, Tabasco

    Google Scholar 

  • Engel G, O’Hara TM, Cardona-Marek T, Heidrich J, Chalise MK, Kyes R, Jones-Engel L (2010) Synanthropic primates in Asia: potential sentinels for environmental toxins. Am J Phys Anthropol 142:453–460

    Article  PubMed Central  PubMed  Google Scholar 

  • Fergusson JE, Hibbard KA, Ting RLH (1981) Lead in human hair: general survey-battery factory employees and their families. Environ Pollut 2:235–248

    Article  CAS  Google Scholar 

  • Fisher LE (1954) Lead poisoning in a gorilla. J Am Vet Med Assoc 125:478–479

    CAS  PubMed  Google Scholar 

  • Gama L, Ordonez EM, Villanueva-Garcia C, Ortiz-Peres A, Lopez HD, Torres RC, M.E.M V (2010) Floods in Tabasco Mexico: history and perspectives. WIT Trans Ecol Environ 133:25–33

    Article  Google Scholar 

  • Gilbert SG, Rice DC (1987) Low-level lifetime lead exposure produced behavioral toxicity (spatial discrimination reversal) in adult monkeys. Toxiological Appl Pharmacol 91:484–490

    Article  CAS  Google Scholar 

  • Glander KE, Fedigan LM, Fedigan L, Chapman CA (1991) Field methods for capture and measurement of three monkey species in Costa Rica. Folia Primatol 57:70–82

    Article  CAS  PubMed  Google Scholar 

  • Goyer RA (1990) Lead toxicity: from overt to subclinical to subtle health effects. Environ Health Perspect 86:177–181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853

    Article  CAS  PubMed  Google Scholar 

  • Hindle E, Stevenson AC (1930) Hitherto undescribed intranuclear bodies in wild rats and monkeys, compared with known virus bodies in other animals. Trans R Soc Trop Med Hyg 23:327

    Google Scholar 

  • Infantas VMM (2005) Intoxicación por plomo. Rev Soc Per Med Inter 18:22–27

    Google Scholar 

  • Iyengar V, Wolttlez J (1988) Trace elements in human clinical specimens: evaluation of literature data to identify reference values. Clin Chem 34:474–481

    CAS  PubMed  Google Scholar 

  • Jacob AL, Vaccaro I, Sengupta R, Hartter J, Chapman CA (2008) How can conservation biology best prepare for declining rural population and ecological homogenization? Trop Conserv Sci 1:307–320

    Google Scholar 

  • Jusko TA, Henderson CR, Lanphear BP, Cory-Slechta DA, Parsons PJ, Canfield RL (2008) Blood concentrations <10 ug/dL and child intelligence at 6 years of age. Environ Health Perspect 116:243–248

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lanphear BP, Hornung R, Khoury J, Yolton K, Baghurst P, Bellinger DC, Canfield RL, Dietrich KN, Bornschein R, Greene T, Rothenberg SJ, Needleman HL, Schnaas L, Wasserman G, Graziano J, Roberts R (2005) Low-level environmental lead exposure and children’s intellectual function: an international pooled analysis. Environ Health Perspect 114:894–899

    Article  Google Scholar 

  • Lee J-I, Jung W-Y, Lee G, Kim M-S, Kim Y-S, Park C-G, Kim S-J (2012) Heavy metal concentrations in hair of newly imported China-origin rhesus macaques (Macaca mulatta). Lab Anim Res 28:151–154

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu J, Li J, Zhang B, Cao J, Cao Z, Domagalski J (2009) Ecological risk of heavy metals in sediments of the Luan River source water. Ecotoxicology 18:748–758

    Article  CAS  PubMed  Google Scholar 

  • Mendoza E, Dirzo R (1999) Deforetation in Lacandonia (southeast Mexico): evidence for the declaration of the northernmost tropical hot-spot. Biodivers Conserv 8:1621–1641

    Article  Google Scholar 

  • Mitra AK, Haque A, Islam M, Bashar SA (2009) Lead poisoning: an alarming public health problem in Bangladesh. Int J Environ Res Pub Health 6:84–95

    Article  CAS  Google Scholar 

  • Moguel E, Molina-Enríquez F (2000) La precipitación fluvial en Tabasco y Chiapas. Kuxulkab Revista de Divulgación Científica 10:1–19

    Google Scholar 

  • Monsu JMT, Cevalier DP, de Gopegui RR (2001) Intoxicación por plomo en el perro: caso clinic. Avepa 21:37–42

    Google Scholar 

  • Olguin EJ, Sánchez-Galvan G, Perez-Perez T, Perez-Orozco A (2005) Surface adsorption, untracellular accumulation and compartmentalization of Pb (II) in batch-operated lagoons with Salvinia minima as affected by environmental conditions, EDTA and nutrients. J Ind Microbiol Biotechnol 32:577–586

    Article  CAS  PubMed  Google Scholar 

  • Poot A, Gillissen F, Koelmans AA (2007) Effects of flow regime and flooding on heavy metal availability in sediment and soil of a dynamic river system. Environ Pollut 148:779–787

    Article  CAS  PubMed  Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC (2006) Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en hábitat fragmentado en Balancán, Tabasco, México. Acta Zool Mex 22:53–66

    Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC, Bonilla-Sánchez YM, Bynum N, Landgrave R (2008) Current status of the habitat and population of the black howler monkey (Alouatta pigra) in Balancán, Tabasco, Mexico. Am J Primatol 70:1–8

  • Pozo-Montuy G, Bonilla-Sánchez YM, Díaz-López HM, Serio-Silva JC (2009) Estudio poblacional de monos aulladores negros Alouatta pigra habitando dentro de plantaciones de Eucalipto en Balancán, Tabasco. In: IV Congreso Mexicano de Primatología, Villahermosa

  • Pozo-Montuy G, Serio-Silva JC, Bonilla-Sanchez YM (2011) The influence of the matrix on the survival of arboreal primates in fragmented landscapes. Primates 52:139–147

    Article  PubMed  Google Scholar 

  • Rattner BA (2009) History of wildlife toxicology. Ecotoxicology 18:773–783

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Castillo P (1978) La fauna silvestre en el Plan Balancán Tenosique. INIREB Biblioteca del Instituto de Ecologia Xalapa, Mexico

    Google Scholar 

  • Rice DC (1997) Effects of lifetime lead exposure in monkeys on detection of pure tone. Fundam Appl Toxicol 36:112–118

    Article  CAS  PubMed  Google Scholar 

  • Rice DC, Karpinski KF (1988) Lifetime low-level lead exposure produced deficits in delayed alternation in adult monkeys. Neurotoxicol Teratol 10:207–214

    Article  CAS  PubMed  Google Scholar 

  • Rivera-Trejo F, Soto-Cortés G, Barajas-Fernández J (2009) The 2007 flooding in Tabasco, Mexico: evolution of water levels. Ingenieria Hidraulica en Mexico 24:159–166

    Google Scholar 

  • Rothwell JJ, Evans MG, Daniels SM, Allott TEH (2007) Baseflow and storm flow metal concentrations in steams draining contaminated peat moorlands in the Peak District National Park (UK). J Hydrol 341:90–104

    Article  Google Scholar 

  • Sannal E, Vargiu L, Rossetti I, Vallascas E, Floris G (2007) Correlation between blood and hair lead levels in boys and girls of Sardina (Italy). J Anthropol Res 85:173–181

    Google Scholar 

  • Schillaci MA, Lee BPY-H, Castellini JM, Reid MJC, O’Hara TM (2011) Lead levels in long-tailed macaque (Macaca fascicularis) hair from Singapore. Primates 52:163–170

    Article  PubMed  Google Scholar 

  • Serio-Silva JC, Pozo-Montuy G, Bonilla-Sánchez YM (2006) Black howler monkeys (Alouatta pigra) inhabiting eucalyptus (Eucalyptus grandis) plantations in Tabasco, Mexico: habitat use and questions to answer. Am J Primatol 68:35

    Article  Google Scholar 

  • Swarup D, Patra R, Dwivedi S, Dey S (2000) Blood lead and cadmium in dogs from urban India. Vet Hum Toxicol 42:232–233

    CAS  PubMed  Google Scholar 

  • Tong S, von Schirnding YE, Prapamontol T (2000) Environmental lead exposure: a health problem of global dimensions. Bull World Health Organ 78:1068–1077

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wright SJ, Muller-Landau HC (2006) The future of tropical forest species. Biotropica 38:287–301

    Article  Google Scholar 

  • Wright SJ, Stoner KE, Beckman N, Corlet RT, Dirzo R, Muller-Landau HC, Nunes-Iturri G, Peres CA, Wang BC (2007) The plight of large animals in tropical forest and the consequences for plant regeneration. Biotropica 39:289–291

    Article  Google Scholar 

  • Zook BC, Sauer RM, Garner FM (1974) Lead poisoning in captive wild animals. J Wildl Dis 8:264–272

    Article  Google Scholar 

Download references

Acknowledgments

The field work in this study was supported by Instituto de Ecologia AC (INECOL) and Wildlife Conservation Society (WCS)—Field Veterinary Program (FVP)—Wildlife Health Fund. Materials, equipment, and personnel from the Environmental Biotechnology Group at the Instituto de Ecologia AC (INECOL) were an important part of these analyses. Funding for the research was provided by the Canada Research Chairs Program, the Natural Science and Engineering Research Council of Canada, and Fonds Québécois de la Recherché sur la Nature et les Technologies. We thank Randy Kyes. Lisa Engel-Jones, Todd O’Hara, and Eduardo Fernandez-Duque for helpful comments on this research and all the field guides, including Mr. Dolores Tejero Geronimo and the local people from Balancán, Tabasco, México.

Author information

Authors and Affiliations

  1. Red de Biología y Conservación de Vertebrados, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico

    Juan Carlos Serio-Silva & Luis Garcia-Feria

  2. Red de Manejo Biotecnológico de Recursos, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico

    Eugenia J. Olguín & Karla Tapia-Fierro

  3. McGill School of Environment and Department of Anthropology, McGill University, Montreal, QC, H3A 2T7, Canada

    Colin A. Chapman

  4. Wildlife Conservation Society, Bronx, New York, USA

    Colin A. Chapman

Authors
  1. Juan Carlos Serio-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eugenia J. Olguín
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Garcia-Feria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karla Tapia-Fierro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Colin A. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Carlos Serio-Silva.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Serio-Silva, J.C., Olguín, E.J., Garcia-Feria, L. et al. Cascading impacts of anthropogenically driven habitat loss: deforestation, flooding, and possible lead poisoning in howler monkeys (Alouatta pigra). Primates 56, 29–35 (2015). https://doi.org/10.1007/s10329-014-0445-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-014-0445-z

Keywords

Search

Navigation