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Linking changes in landscape structure to population changes of an endangered primate

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Abstract

Context

Non-human primates are among the most threatened mammals on Earth. Although some species, such as howler monkeys, are thought to be resistant to initial phases of habitat disturbance, the lack of longitudinal studies prevents determining if this holds over time.

Objectives

We assessed temporal changes in landscape structure in the Lacandona rainforest, Mexico, and how these changes relate to population trends of black howler monkeys (Alouatta pigra).

Methods

We surveyed primates in 22 forest sites in 2011 and 2017, and related temporal changes in primate abundance and immature-to-female ratio with changes in the spatial structure of local landscapes (forest cover, matrix openness, number of forest patches, and forest edge density) using a multi-scale approach.

Results

Landscape changes occurring over a 6-year period were strongly associated with temporal changes in population parameters. Primate abundance increased as forest cover increased. Both primate abundance and immature-to-female ratio increased in sites located in landscapes where the number of patches increased over time, but where the proportion of open matrix decreased. Edge density showed a negative effect on immature-to-female ratio.

Conclusions

This endangered primate might not be as tolerant to landscape disturbance as generally thought. Allowing forest patches to increase in number and/or size through active or passive restoration (reverse fragmentation), and preventing forest loss and an increase in matrix openness are key management strategies to preserve howler monkeys in this biodiversity hotspot.

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References

  • Andresen E, Arroyo-Rodríguez V, Ramos-Robles M (2018) Primate seed dispersal: old and new challenges. Int J Primatol 39:443–465

    Article  Google Scholar 

  • Anzures-Dadda A, Manson RH (2007) Patch- and landscape-scale effects on howler monkey distribution and abundance in rainforest fragments. Anim Conserv 10:69–76

    Article  Google Scholar 

  • Arce-Peña NP, Arroyo-Rodríguez V, San-José M, Jiménez-González D, Franch-Pardo I, Andresen E, Ávila-Cabadilla LD (2019) Landscape predictors of rodent dynamics in fragmented rainforests. Biodivers Conserv 28:655–669

    Article  Google Scholar 

  • Arriaga L, Espinoza J, Aguilar C, Martínez E, Gómez L, Loa E (2000) Regiones terrestres prioritarias de México. CONABIO, Mexico City

    Google Scholar 

  • Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, González-Perez IM, Garmendia A, Solà M, Estrada A (2013) The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico. Landscape Ecol 8:1717–1727

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Mandujano S, Benítez-Malvido J (2008) Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los Tuxtlas, Mexico. Am J Primatol 70:69–77

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Pérez-Elissetche GK, Ordóñez-Gómez JD, González-Zamora A, Chaves OM, Sánchez-López S, Chapman CA, Morales-Hernández K, Pablo-Rodríguez M, Ramos-Fernández G (2017) Spider monkeys in human-modified landscapes: the importance of the matrix. Trop Conserv Sci 10:1–30

    Google Scholar 

  • Asensio N, Arroyo-Rodríguez V, Dunn JC, Cristobal-Azkarate J (2009) Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica 41:768–773

    Article  Google Scholar 

  • Benchimol M, Peres CA (2013a) Anthropogenic modulators of species-area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Divers Distrib 19:1339–1352

    Article  Google Scholar 

  • Benchimol M, Peres CA (2013b) Predicting primate local extinctions within “real-world” forest fragments: a pan-neotropical analysis. Am J Primatol 76:289–302

    Article  PubMed  Google Scholar 

  • Bennet AF, Saunders DA (2010) Habitat fragmentation and landscape change. In: Sodhi NS, Ehrlich PR (eds) Conservation biology for all. Oxford University Press, Oxford, pp 88–106

    Chapter  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calcagno V, de Mazancourt C (2010) Glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29

    Article  Google Scholar 

  • Camara G, Souza RCM, Freitas UM, Garrido J (1996) SPRING: integrating remote sensing and GIS by object-oriented data modelling. Comput Graph 20:395–403

    Article  Google Scholar 

  • Carabias J, de la Maza J, Cadena R (2015) Conservación y desarrollo sustentable en la Selva Lacandona. 25 años de actividades y experiencias. Natura y Ecosistemas Mexicanos, Mexico City

    Google Scholar 

  • Chapman CA, Bortolamiol S, Matsuda I, Omeja PA, Paim FP, Reyna-Hurtado R, Sengupta R, Valenta K (2018) Primate population dynamics: variation in abundance over space and time. Biodivers Conserv 27:1221–1238

    Article  Google Scholar 

  • Cristóbal-Askarate J, Veá J, Asensio N, Rodríguez-Luna E (2005) Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico. Am J Primatol 67:209–222

    Article  Google Scholar 

  • Cristóbal-Azkarate J, Arroyo-Rodríguez V (2007) Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69:1013–1029

    Article  PubMed  Google Scholar 

  • Cristóbal-Azkarate J, Dunn JC, Domingo-Balcells C, Veá-Baró J (2017) A demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico. PeerJ 5:e3547

    Article  PubMed  PubMed Central  Google Scholar 

  • Crockett CM, Eisenberg JF (1987) Howlers: Variations in group size and demography. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 54–68

    Google Scholar 

  • Da Silva LG, Ribeiro MC, Hasui E, da Costa CA, Da Cunha RGT (2015) Patch size, functional isolation, visibility and matrix permeability influences neotropical primate occurrence within highly fragmented landscapes. PLoS ONE 10:e0114025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Castillo RF (2015) A conceptual framework to describe the ecology of fragmented landscapes and implications for conservation and management. Ecol Appl 25:1447–1455

    Article  PubMed  Google Scholar 

  • Dias PAD, Coyohua-Fuentes A, Canales-Espinosa D, Rangel-Negrín A (2015) Group structure and dynamics in black howlers (Alouatta pigra): a 7-year perspective. Int J Primatol 36:311–331

    Article  Google Scholar 

  • Dias PAD, Coyohua-Fuentes A, Canales-Espinosa D, Rangel-Negrín A (2016) Factors influencing the reproductive success of female black howlers (Alouatta pigra). Int J Primatol 37:638–655

    Article  Google Scholar 

  • Dias PAD, Rangel-Negrín A (2015) Diets of howler monkeys. In: Kowaleski MM, Garber PA, Cortés-Ortíz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer, New York, pp 21–56

    Chapter  Google Scholar 

  • Dunning JB, Danielson BJ, Pulliam R (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175

    Article  Google Scholar 

  • Eigenbrod F, Hecnar SJ, Fahrig L (2011) Sub-optimal study design has major impacts on landscape-scale inference. Biol Conserv 144:298–305

    Article  Google Scholar 

  • Estrada A (1984) Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. J Primatol 5:105–131

    Google Scholar 

  • Estrada A, Coates-Estrada R (1996) Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. Int J Primatol 17:759–783

    Article  Google Scholar 

  • Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KAI, Nijman V, Heymann EW, Lambert JE, Rovero F, Barelli C, Setchell JM, Gillespie TR, Mittermeier RA, Arregoitia LV, de Guinea M, Gouveia S, Dobrovolski R, Shanee S, Shanee N, Boyle SA, Fuentes A, MacKinnon KC, Amato KR, Meyer ALS, Wich S, Sussman RW, Pan R, Kone I, Li B (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada A, Mendoza A, Castellanos L, Pacheco R, Van Belle S, García Y, Muñoz D (2002) Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico. Am J Primatol 58:45–55

    Article  PubMed  Google Scholar 

  • Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Ewers RM, Didham RK, Pearse WD, Lefebvre V, Rosa IMD, Carreiras JMB, Lucas RM, Reuman DC (2013) Using landscape history to predict biodiversity patterns in fragmented landscapes. Ecol Lett 16:1221–1233

    Article  PubMed  PubMed Central  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Article  Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23

    Article  Google Scholar 

  • Fahrig L, Arroyo-Rodríguez V, Bennett J, Boucher-Lalonde V, Cazeta E, Currie D, Eigenbrod F, Ford A, Jaeger J, Koper N, Martin A, Metzger JP, Morrison P, Rhodes J, Saunders D, Simberloff D, Smith A, Tischendorf L, Vellend M, Watling J (2019) Is habitat fragmentation bad for biodiversity? Biol Conserv 230:179–186

    Article  Google Scholar 

  • Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112

    Article  PubMed  Google Scholar 

  • Fortes VB, Bicca-Marques JC, Urbani B, Fernández VA, da Pereira ST (2015) Ranging behavior and spatial cognition of howler monkeys. In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology, and conservation. Springer, New York, pp 219–255

    Chapter  Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE publications Inc, Thousand Oaks

    Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Andresen E, Arregoitia LV, Vega E, Peres CA, Ewers RM (2019a) The conservation value of human-modified landscapes for the world’s primates. Nat Commun 10:152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Arasa-Gisbert R, Andresen E (2019b) Ecological traits of the world’s primates. Sci Data 6:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Cudney-Valenzuela S, Fahrig L (2019c) A global assessment of primate responses to landscape structure. Biol Rev. https://doi.org/10.1111/brv.12517

    Article  PubMed  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Estrada A, Ramos-Fernández G (2018) Drivers of the spatial scale that best predict primate responses to landscape structure. Ecography 41:1–11

    Article  Google Scholar 

  • Gestich CC, Arroyo-Rodríguez V, Ribeiro MC, da Cunha RGT, Setz EZF (2019) Unraveling the scales of effect of landscape structure on primate species richness and density of titi monkeys (Callicebus nigrifrons). Ecol Res 34:150–159

    Article  Google Scholar 

  • Gibson L, Ming-Lee T, Pin-Koh L, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE, Sodhi NS (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478:378–383

    Article  CAS  PubMed  Google Scholar 

  • Grez A, Zaviezo T, Tischendorf L, Fahrig L (2004) A transient, positive effect of habitat fragmentation on insect population densities. Oecologia 141:444–451

    Article  PubMed  Google Scholar 

  • Hagolle O, Sylvander S, Huc M, Claverie M, Clesse D, Dechoz C, Lonjou V, Poulain V (2015) SPOT-4 (Take 5): simulation of Sentinel-2 time series on 45 large sites. Remote Sens 7:12242–12264

    Article  Google Scholar 

  • Hanski I (1999) Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes. Oikos 87:209–219

    Article  Google Scholar 

  • Hanski I (2013) Extinction debt at different spatial scales. Anim Conserv 16:12–13

    Article  Google Scholar 

  • Holzmann I, Agostini I, Areta JI, Ferreyra H, Beldomenico P, Di Biteti MS (2010) Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina. Am J Primatol 72:475–480

    PubMed  Google Scholar 

  • Horwich RH, Johnson ED (1986) Geographical distribution of the black howler (Alouatta pigra) in Central America. Primates 27:53–62

    Article  Google Scholar 

  • Instituto Nacional de Ecología (2000) Programa de Manejo Reserva de la Biósfera Montes Azules. Secretaría de Medio Ambiente y Recursos Naturales, Mexico City

    Google Scholar 

  • Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Glob Ecol Biogeogr 24:52–63

    Article  Google Scholar 

  • Kowalewski MM, Zunino GE (1999) Impact of deforestation on a population of Alouatta caraya in Northern Argentina. Folia Primatol 70:163–166

    Article  CAS  Google Scholar 

  • Laurance WF (1991) Ecological correlates of extinction proneness in Australian tropical rain forest mammals. Conserv Biol 5:79–89

    Article  Google Scholar 

  • Marsh LK, Cuarón AD, Cortés-Ortíz L, Shedden A, Rodríguez-Luna E, de Grammont PC (2008) Alouatta pigra. IUCN Red List Threat Species 2008:41

    Google Scholar 

  • Medellín R (1994) Mammal diversity and conservation in the Selva Lacandona, Chiapas, Mexico. Conserv Biol 8:780–799

    Article  Google Scholar 

  • McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Computer software program produced by the authors at the University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html. Accessed 17 Jan 2019

  • Melo F, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468

    Article  PubMed  Google Scholar 

  • Metzger JP, Camargo AM, Dixo M, Bernacci LC, Ribeiro MC, Godoy AMT, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142:1166–1177

    Article  Google Scholar 

  • Michalski F, Peres C (2005) Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biol Conserv 124:383–396

    Article  Google Scholar 

  • Morante-Filho JC, Arroyo-Rodríguez V, Pessoa MS, Cazetta E, Faria D (2018) Direct and cascading effects of landscape structure on tropical forest and non-forest frugivorous birds. Ecol Appl 28:2024–2032

    Article  PubMed  Google Scholar 

  • Neter J, Kutner MH, Nachtshein CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill/Irwin, New York

    Google Scholar 

  • Olofsson P, Foody GM, Herold M, Stehman SV, Woodcock CE, Wulder MA (2014) Good practices for estimating area and assessing accuracy of land change. Remote Sens Environ 148:42–57

    Article  Google Scholar 

  • Ordóñez-Gómez JD, Arroyo-Rodríguez V, Nicasio-Arzeta S, Cristóbal-Azkarate J (2015) Which is the appropriate scale to assess the impact of landscape spatial configuration on the diet and behavior of spider monkeys? Am J Primatol 77:56–65

    Article  PubMed  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in s and S-plus. Springer, New York

    Book  Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC, Chapman CA, Bonilla-Sánchez YM (2013) Resource use in a landscape matrix by an arboreal primate: evidence of supplementation in black howlers (Alouatta pigra). Int J Primatol 34:714–731

    Article  Google Scholar 

  • Puig-Lagunes AA, Canales-Espinosa D, Rangel-Negrín A, Das PA (2016) The influence of spatial attributes on fragment occupancy and population structure in the Mexican mantled howler (Alouatta palliata mexicana). Int J Primatol 6:656–670

    Article  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 13 April 2019

  • Rangel-Negrín A, Coyohua-Fuentes A, Canales-Espinosa D, Dias PAD (2014) Mammal assemblages in forest fragments and landscapes occupied by black howler monkeys. Primates 55:345–352

    Article  PubMed  Google Scholar 

  • Rosales-Meda M, Estrada A, López AE (2008) Demographic survey of black howler monkey (Alouatta pigra) in the Lachuá eco-region in Alta Verapaz, Guatemala. Am J Primatol 70:231–237

    Article  PubMed  Google Scholar 

  • SEMARNAT (2010) NOM-059-SEMARNAT-2010. Protección ambiental- Especies nativas de México de flora y fauna silvestres- Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio- Lista de especies en riesgo. Diario Oficial de la Federación, Dec 30 2010

  • Silver SC, Ostro LET, Yeager CP, Horwich R (1998) Feeding ecology of the black howler monkey (Alouatta pigra) in Northern Belize. Am J Primatol 45:262–279

    Article  Google Scholar 

  • Van Belle S, Estrada A (2005) Demographic features of Alouatta pigra populations in extensive and fragmented forests. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 121–142

    Google Scholar 

  • Van Belle S, Estrada A (2008) Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra). Am J Primatol 70:613–619

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the financial support provided by Rufford Small Grants (No. 22049-1), and SEP-CONACyT (Project 2015-253946). N.P.A.P. obtained a graduate scholarship from CONACyT. This paper constitutes a partial fulfillment of the PhD program of the Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México (UNAM). We thank Luis Daniel Ávila Cabadilla for all his insightful comments to this project, and Carlos Palomares Magaña for his technical support in GIS. J. M. Lobato, H. Ferreira, A. Valencia and A. López also provided technical support. We thank landowners in the Marqués de Comillas region for allowing us to collect data on their properties, as well as the Montes Azules Biosphere Reserve and the National Commission of Natural Protected Areas (CONANP). Finally, we thank Natura y Ecosistemas Mexicanos A.C. and the Chajul Biological Station for providing logistical support. A special acknowledgement to Adolfo Jamangapé, as this study would not have been possible without his field assistance.

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Authors and Affiliations

  1. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro no. 8701. Ex-Hacienda de San José de la Huerta, 58190, Morelia, Michoacán, Mexico

    Norma P. Arce-Peña, Víctor Arroyo-Rodríguez & Ellen Andresen

  2. Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, 91190, Xalapa, Mexico

    Pedro A. D. Dias

  3. Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de México, 58190, Morelia, Michoacán, Mexico

    Iván Franch-Pardo

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  1. Norma P. Arce-Peña
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  2. Víctor Arroyo-Rodríguez
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  3. Pedro A. D. Dias
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  4. Iván Franch-Pardo
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Correspondence to Víctor Arroyo-Rodríguez.

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Arce-Peña, N.P., Arroyo-Rodríguez, V., Dias, P.A.D. et al. Linking changes in landscape structure to population changes of an endangered primate. Landscape Ecol 34, 2687–2701 (2019). https://doi.org/10.1007/s10980-019-00914-8

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