Skip to main content

Advertisement

SpringerLink
Log in

Can secondary forests mitigate the negative effect of old-growth forest loss on biodiversity? A landscape-scale assessment of two endangered primates

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Old-growth forest loss drives the global biodiversity crisis. Nevertheless, this impact could be buffered by the increasing expansion of secondary (regenerating) forests, which can provide supplementary habitat for wildlife.

Objectives

We tested this hypothesis assessing the effect of old-growth and secondary forest cover on the abundance and immature-to-female ratio (proxy of reproductive success) of two endangered primates: Geoffroy’ spider monkeys and black howler monkeys.

Methods

We measured the response and predictor variables across 18 whole landscapes (landscape-scale approach) in the Lacandona rainforest, Mexico. As there could be tipping points of forest loss beyond which species extinction is accelerated (extinction thresholds), we separately tested the linear and non-linear effect of forest cover on each response, independently for three spatial scales.

Results

We found stronger and larger-scale negative responses to forest loss in spider monkeys than in howler monkeys. However, the data were better predicted by linear models, giving no support to the extinction threshold hypothesis. In both species, forest loss had stronger negative impacts on monkey abundance when considering old-growth forest, than when considering secondary forest cover, or total (old-growth + secondary) forest cover. Yet, the immature-to-female ratio was weakly related to forest cover in both species.

Conclusion

Secondary forests seem to have a weak buffering effect in both species, possibly because they are relatively young (< 30 years old) and do not have large trees. This implies that old-growth forests are irreplaceable for preventing primate extirpation, especially for species with specialized diet and large spatial requirements, such as spider monkeys.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amato KR, Garber PA (2014) Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 76:774–787

    Article  CAS  PubMed  Google Scholar 

  • Andren H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat, a review. Oikos 71(3):355–366

    Article  Google Scholar 

  • Arce-Peña NP, Arroyo-Rodríguez V, Dias PAD, Franch-Pardo I, Andrensen E (2019) Linking changes in landscape structure to population changes of an endangered primate. Landsc Ecol 34:2687–2701

    Article  Google Scholar 

  • Arriaga L, Espinoza JM, Aguilar C, Martínez E, Gómez L et al (2000) Regiones terrestres prioritarias de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (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, Fahrig L (2014) Why is a landscape perspective important in studies of primates? Am J Primatol 76:901–909

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Cuesta-del Moral E, Mandujano S, Chapman CA, Reyna-Hurtado R, Fahrig L (2013a) Assessing habitat fragmentation effects for primates: the importance of evaluating questions at the correct scale. In: Marsh LK, Chapman CA (eds) Primates in fragments: complexity and resilience. Developments in primatology: progress and prospects. Springer, New York, pp 13–28

    Google Scholar 

  • Arroyo-Rodríguez V, Gonzalez-Perez IM, Garmendia A, Sola M, Estrada A (2013b) The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico. Landsc Ecol 9:1717–1727

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Andresen E, Bravo SP, Stevenson PR (2015) Seed dispersal by howler monkeys: current knowledge, conservation implications and future directions. In: Kowalewski M, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer developments in primatology, progress and prospects book series. Springer, New York, pp 111–139

    Chapter  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. https://doi.org/10.1177/1940082917719788

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Fahrig L, Tabarelli M, Watling JI, Tischendorf L, Benchimol M, Cazetta E, Faria D, Leal IR, Melo FPL, Morante-Filho JC, Santos BA, Arasa-Gisbert R, Arce-Peña N, Cervantes-López MJ, Cudney-Valenzuela S, Galán-Acedo C, San-José M, Vieira ICG, Slik JWF, Nowakowski J, Tscharntke T (2020) Designing optimal human-modified landscapes for forest biodiversity conservation. Ecol Lett 23:1404–1420

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Fahrig L, Watling JI, Nowakowski J, Tabarelli M, Tischendorf L, Melo FPL, Santos BA, Benchimol M, Morante-Filho JC, Slik JWF, Vieira IDG, Tscharntke T (2021) Preserving 40% forest cover is a valuable and well‐supported conservation guideline: reply to Banks‐Leite et al. Ecol Lett 24:1114–1116

    Article  PubMed  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 

  • Blanco V, Waltert M (2013) Does the tropical agricultural matrix bear potential for primate conservation? A baseline study from Western Uganda. J Nat Conserv 21:383–393

    Article  Google Scholar 

  • Bowman J, Jaeger JA, Fahrig L (2002) Dispersal distance of mammals is proportional to home range size. Ecology 83:2049–2055

    Article  Google Scholar 

  • Boyle SA, Smith AT (2010) Can landscape and species characteristics predict primate presence in forest fragments in the Brazilian Amazon? Biol Conserv 143:1134–1143

    Article  Google Scholar 

  • Brindis-Badillo D, Arroyo-Rodríguez V, Mendoza E, Wies G, Martínez-Ramos M (2022) Conserving dominant trees in human-modified landscapes at the Lacandon tropical rainforest. Biol Conserv 270:109548

    Article  Google Scholar 

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

    Google Scholar 

  • Carabias J, De la Maza J, Cadena R (2015) Conservación y desarrollo sustentable en la Selva Lacandona. Natura y Ecosistemas Mexicanos A.C., Mexico City

    Google Scholar 

  • Carrara E, Arroyo-Rodríguez V, Vega-Rivera JH, Schondube JE, de Freitas SM, Fahrig L (2015) Impact of landscape composition and configuration on forest specialist and generalist bird species in the fragmented Lacandona rainforest, Mexico. Biol Conserv 184:117–126

    Article  Google Scholar 

  • Carretero-Pinzon X, Defler TR, McAlpine CA, Rhodes JR (2017) The influence of landscape relative to site and patch variables on primate distributions in the Colombian Llanos. Landsc Ecol 32:883–896

    Article  Google Scholar 

  • Chapman CA, Peres CA (2021) Primate conservation: lessons learned in the last 20 years can guide future efforts. Evol Anthropol 30:345–361

    Article  PubMed  Google Scholar 

  • Chapman CA, Bonnell TR, Gogarten JF, Lambert JE, Omeja PA, Twinomugisha D, Wasserman MD, Rothman JM (2013) Are primates ecosystem engineers? Int J Primatol 34:1–14

    Article  Google Scholar 

  • Chaves OM, Stoner KE, Arroyo-Rodríguez V (2011a) Seasonal differences in activity patterns of Geoffroyi’s spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in southern Mexico. Int J Primatol 32:960–973

    Article  Google Scholar 

  • Chaves OM, Stoner KE, Arroyo-Rodríguez V, Estrada A (2011b) Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rainforests in southern Mexico. Int J Primatol 32:177–192

    Article  Google Scholar 

  • Cortés-Ortíz L, Rosales-Meda M, Marsh LK, Mittermeier RA (2020) Alouatta pigra. The IUCN Red List of Threat Species 2020: e.T914A17926000. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T914A17926000.en. Accessed Oct 2021

  • Cortés-Ortíz L, Solano-Rojas D, Rosales-Meda M, Williams-Guillen K et al (2021) Ateles geoffroyi (amended version of 2020 assessment). The IUCN Red List of Threat Species 2021: e.T2279A191688782. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T2279A191688782.en. Accessed Oct 2021

  • 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 

  • Cudney-Valenzuela S, Arroyo-Rodríguez V, Andrensen E, Toledo-Aceves T (2022) What determines the scale of landscape effect on tropical arboreal mammals? Landsc Ecol 37:1497–1507

    Article  Google Scholar 

  • Di Fiore A, Link A, Campbell CJ (2011) The Atelines: behavioural and socioecological diversity in a New World monkey radiation. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, New York, pp 155–188

    Google Scholar 

  • Dias PAD, Rangel-Negrín A (2015) Diets of howler monkeys. In: Howler monkeys. Springer, New York, pp 21–56

  • Dias PAD, Rangel-Negrín A, Coyohua-Fuentes A, Canales-Espinosa D (2014) Variation in dietary breadth among groups of black howler monkeys is not associated with the vegetation attributes of forest fragments. Am J Primatol 76:1151–1162

    Article  PubMed  Google Scholar 

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

    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, 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 KA, 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 

  • Ewers RM, Didham RK (2005) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Fahrig L (1997) Relative effects of habitat loss and fragmentation on population extinction. J Wildl Manag 61(3):603–610

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Farneda FZ, Rocha R, López-Baucells A, Groenenberg M, Silva I et al (2015) Trait‐related responses to habitat fragmentation in Amazonian bats. J Appl Ecol 52:1381–1391

    Article  Google Scholar 

  • Ferreira AS, Peres CA, Bogoni JA, Cassano CR (2018) Use of agroecosystem matrix habitats by mammalian carnivores (Carnivora): a global-scale analysis. Mamm Rev 48:312–327

    Article  Google Scholar 

  • Ficetola FG, Denoel M (2009) Ecological thresholds: an assessment of methods to identify abrupt changes in species–habitat relationships. Ecography 32:1075–1084

    Article  Google Scholar 

  • Fortes VB, Bicca-Marques JC, Urbani B, Fernández VA, Pereira TS (2015) Ranging behavior and spatial cognition of howler monkeys. In: Kowalewski M, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer developments in primatology, progress and prospects book series. Springer, New York, pp 219–255

    Chapter  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Estrada A, Ramos-Fernandez G (2018) Drivers of the spatial scale that best predict primate responses to landscape structure. Ecography 41:2027–2037

    Article  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Estrada A, Ramos-Fernandez G (2019a) Forest cover and matrix functionality drive the abundance and reproductive success of an endangered primate in two fragmented rainforests. Landsc Ecol 34:147–158

    Article  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Cudney-Valenzuela SJ, Fahrig L (2019b) A global assessment of primate responses to landscape structure. Biol Rev 94:1605–1618

    Article  PubMed  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Andresen E, Arasa-Gisbert R (2019c) Ecological traits of the world’s primates. Sci Data 6:1–5

    Article  Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Chapman CA (2021) Beyond patch size: the impact of regional context and habitat quality on three endangered primates. Perspect Ecol Conserv 19:207–215

    Google Scholar 

  • Garber PA, Estrada A, Pavelka MSM, Luecke L (2005) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 563–584

    Google Scholar 

  • García del Valle Y, Caballero EJ, Martorell C, Ruan-Soto F, Enriquez PL (2015) Cultural significance of wild mammals in Mayan and Mestizo communities of the Lacandon Rainforest, Chiapas, Mexico. J Ethnobiol Ethnomed 11:1–14

    Article  Google Scholar 

  • Gestich CC, Arroyo-Rodríguez V, Saranholi BH, Cunha RGT, Setz LZF, Ribeiro MC (2021) Forest loss and fragmentation can promote the crowding effect in a forest-specialist primate. Landsc Ecol 37:147–157

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gilbert KA (2003) Primates and fragmentation of the Amazon forest. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic/Plenum Press, New York, pp 145–157

    Chapter  Google Scholar 

  • Global Forest Watch (2021) World Resources Institute. http://www.globalforestwatch.org.. Accessed 1 June 2022

  • González-Zamora A, Arroyo-Rodríguez V, Chavez O, Sanchez-Lopez S, Stoner KE, Riba-Hernández P (2009) Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions. Am J Primatol 71:8–20

    Article  PubMed  Google Scholar 

  • González-Zamora A, Arroyo-Rodríguez V, Escobar F, Rös M, Oyama K, Ibarra-Manríquez G, Stoner KE, Chapman CA (2014) Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS ONE 9(2):e89346

    Article  PubMed  PubMed Central  Google Scholar 

  • Holland JD, Bert DG, Fahrig L (2004) Determining the spatial scale of species’ response to habitat. Bioscience 54:227–233

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, migration credit and species turnover. Trends Ecol Evol 25:153–160

    Article  PubMed  Google Scholar 

  • Kelaita M, Dias PAD, Aguilar-Cucurachi MS, Canales-Espinosa D, Cortes-Ortiz L (2011) Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. Am J Phys Anthropol 146:179–187

    Article  PubMed  Google Scholar 

  • Lande R (1987) Extinction thresholds in demographic models of territorial populations. Am Nat 130:624–635

    Article  Google Scholar 

  • Laurindo RS, Novaes RLM, Vizentin-Bugoni J, Gregorin R (2019) The effects of habitat loss on bat–fruit networks. Biodivers Conserv 28:589–601

    Article  Google Scholar 

  • Link A, de Luna AG, Alfonso F, Giraldo-Beltran P, Ramirez F (2010) Initial effects of fragmentation on the density of three neotropical primate species in two lowland forests of Colombia. Endanger Species Res 13:41–50

    Article  Google Scholar 

  • Lohbeck M, DeVries B, Bongers F, Martinez-Ramos M, Navarrete-Segueda A, Nicasio-Arzeta S, Siebe C, Pingarroni A, Wies G, Decuyper M (2022) Mexican agricultural frontier communities differ in forest dynamics with consequences for conservation and restoration. Remote Sens Ecol Conserv. https://doi.org/10.1002/rse2.262

    Article  Google Scholar 

  • Martin TE, Blackburn GA (2014) Conservation value of secondary forest habitats for endemic birds, a perspective from two widely separated tropical ecosystems. Ecography 37:250–260

    Article  Google Scholar 

  • McGarigal K, Cushman S, Ene E(2012) FRAGSTAT v4 (WWW Document) spatial pattern analysis program for categorical continuous maps, computer software program. Authors University of Massachusetts, Amherst. Available follow web site. www.umass.edu/landeco/research/fragstats/frags. Accessed Nov 2020

  • Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:461–468

    Article  Google Scholar 

  • Miguet P, Jackson HB, Jackson ND, Martin AE, Fahrig L (2016) What determines the spatial extent of landscape effects on species? Landsc Ecol 31:1177–1194

    Article  Google Scholar 

  • Mittermeier RA, Wilson DE, Rylands AB (2013) Handbook of the mammals of the world: primates, vol 3. Lynx Edicions, Barcelona

    Google Scholar 

  • Morante-Filho JC, Faria D, Mariano-Neto E, Rhodes J (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10:e0128923

    Article  PubMed  PubMed Central  Google Scholar 

  • Morante-Filho JC, Arroyo-Rodríguez V, Lohbeck M, Tscharntke T, Faria D (2016) Tropical forest loss and its multitrophic effects on insect herbivory. Ecology 97:3315–3325

    Article  PubMed  Google Scholar 

  • Navarrete-Segueda A, Martínez-Ramos M, Ibarra-Manríquez G, Cortés-Flores J, Vázquez-Selem L, Siebe C (2017) Availability and species diversity of forest products in a Neotropical rainforest landscape. For Ecol Manag 406:242–250

    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 

  • Palmeirim AF, Benchimol M, Morante-Filho JC, Vieira MV, Peres CA (2018) Ecological correlates of mammal β‐diversity in Amazonian land‐bridge islands: from small‐to large‐bodied species. Divers Distrib 24:1109–1120

    Article  Google Scholar 

  • Piel AK, Cohen N, Kamenya S, Ndimuligo SA, Pintea L (2015) Population status of chimpanzees in the Masito-Ugalla Ecosystem, Tanzania. Am J Primatol 77:1027–1035

    Article  PubMed  Google Scholar 

  • Poorter L, Bongers F, Aide TM, Almeyda AM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Broadbent EN, Chazdon RL, Craven D, de Almeida-Cortez JS, Cabral GAL, de Jong BHJ, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, César RG, Hall JS, Hernandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Licona JC, Lohbeck M, Marín-Spiotta E, Martínez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Muñoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, de Oliveira AA, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velázquez J, Romero-Pérez IE, Ruíz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Toledo M, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, F M Vester H, Vicentini A, Vieira ICG, Vizcarra Bentos T, Williamson GB, Rozendaal DMA (2016) Biomass resilience of Neotropical secondary forests. Nature 530:211–214

    Article  CAS  PubMed  Google Scholar 

  • Prasetyo RB, Kuswanto H, Iriawan N, Ulama BSS (2019) A comparison of some link functions for binomial regression models with application to school drop-out rates in East Java. AIP Conf Proc 2194:020083

    Article  Google Scholar 

  • QGIS Development Team (2021) QGIS geographic information system. Open Source Geospatial Foundation. http://qgis.org

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/.uage. Accessed June 2022

  • Ramos-Fernández G, Ayala-Orozco B (2003) Population size and habitat use of spider monkeys at Punta Laguna, Mexico. In: Marsh LK (ed) Primates in fragments. Springer, Boston, pp 191–209

    Chapter  Google Scholar 

  • Rangel-Negrín A, Coyohua-Fuentes A, Canales-Espinosa D, Dias PAD (2018a) The influence of leaf consumption on time allocation in black howler monkeys (Alouatta pigra). Folia Primatol 89:111–122

    Article  Google Scholar 

  • Rangel-Negrín A, Coyohua-Fuentes A, Chavira-Ramírez DR, Canales-Espinosa D, Dias PAD (2018b) Energetic constraints on the reproduction of female mantled howlers. Am J Primatol 81:e22925

    Article  Google Scholar 

  • Rios E, Benchimol M, De Vleeschouwer K, Cazetta E (2022) Spatial predictors and species’ traits: evaluating what really matters for medium-sized and large mammals in the Atlantic Forest, Brazil. Mamm Rev 52:236–251

    Article  Google Scholar 

  • Rocha R, Ovaskainen O, López-Baucells A, Farneda FZ, Sampaio EM, Bobrowiec PED, Cabeza M, Palmeirim JM, Meyer CFJ (2018) Secondary forest regeneration benefits old-growth specialist bats in a fragmented tropical landscape. Sci Rep 8:1–9

    Article  Google Scholar 

  • Russildi G, Arroyo-Rodríguez V, Hernández-Ordóñez O, Pineda E, Reynoso VH (2016) Species- and community-level responses to habitat spatial changes in fragmented rainforests: assessing compensatory dynamics in amphibians and reptiles. Biodivers Conserv 25:375–392

    Article  Google Scholar 

  • Rybicki J, Hanski I (2013) Species–area relationships and extinction caused by habitat loss and fragmentation. Ecol Lett 16:27–38

    Article  PubMed  Google Scholar 

  • San-José M, Arroyo-Rodríguez V, Meave JA (2020) Regional context and dispersal mode drive the impact of landscape structure on seed dispersal. Ecol Appl 30:e02033

    Article  PubMed  Google Scholar 

  • Shimooka Y, Campbell CJ, Di Fiore A, Felton AM, Izawa K et al (2008) Demography and group composition of Ateles. In: Campbell CJ et al (eds) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 329–348

    Chapter  Google Scholar 

  • Smith CC, Healey JR, Berenguer E, Young PJ, Taylor B et al (2021) Old-growth forest loss and secondary forest recovery across Amazonian countries. Environ Res Lett 16:085009

    Article  Google Scholar 

  • Supriatna J, Shekelle M, Fuad HAH, Winarni NL, Dwiyahreni AA, Farid M, Mariati S, Margules S, Prakoso B, Zakaria Z (2020) Deforestation on the Indonesian Island of Sulawesi and the loss of primate habitat. Glob Ecol Conserv 24:e01205

    Article  Google Scholar 

  • Swift TL, Hannon SJ (2010) Critical thresholds associated with habitat loss: a review of the concepts, evidence and applications. Biol Rev 85:35–53

    Article  PubMed  Google Scholar 

  • Thompson ME, Donnelly MA (2018) Effects of secondary forest succession on amphibians and reptiles: a review and meta-analysis. Copeia 106:10–19

    Article  Google Scholar 

  • Vallejos MAV, Padial AA, Simoes JR, Moteiro-Filho ELA (2019) Effects of crowding due to habitat loss on species assemblage patterns. Conserv Biol 34:405–415

    Article  PubMed  Google Scholar 

  • Van Belle S, Kulp AE, Thiessen-Bock R, Garcia M, Estrada A (2010) Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Primates 51:279–284

    Article  PubMed  Google Scholar 

  • Wallace RB (2008) Factors influencing spider monkey habitat use and ranging patterns. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 138–154

    Chapter  Google Scholar 

  • Watling JI, Arroyo-Rodríguez V, Pfeifer M, Baeten L, Banks-Leite C, Cisneros LM, Fang R, Hamel-Leigue AC, Lanchat T, Leal IR, Lens L, Possingham HP, Raheem DC, Ribeiro DB, Slade EM, Urbina-Cardona JN, Wood E, Fahrig L (2020) Support for the habitat amount hypothesis from a global synthesis of species density studies. Ecol Lett 23:674–681

    Article  PubMed  Google Scholar 

  • Wies G, Arzeta N, Martínez-Ramos M (2021) Critical ecological thresholds for conservation of tropical rainforest in human-modified landscapes. Biol Conserv 255:109023

    Article  Google Scholar 

  • Wright SJ, Muller-Landau HC (2006) The uncertain future of tropical forest species. Biotropica 38:443–445

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. In: Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W (eds) Statistics for biology and health, vol 574. Springer, New York, pp 209–236

    Google Scholar 

Download references

Acknowledgements

We especially thank Rafael Lombera for his invaluable field assistance and accommodation in the Marqués de Comillas Region. We also thank the landowners for allowing us to collect data on their properties and for their help in the field. We thank German Wies for his help digitizing the map and obtaining landscape variables, and Aline Pingarroni for sharing spatial information required to create Fig. 1.

Funding

This research was supported by SEP-CONACyT (Project 2016-285940). LLSB obtained a Graduate Scholarship from CONACyT, Mexico.

Author information

Authors and Affiliations

  1. Instituto de Ecología, A.C., 91073, Xalapa, Veracruz, Mexico

    Laura L. Saldívar-Burrola, Fabricio Villalobos & Fabiola López-Barrera

  2. Escuela Nacional de Estudios Superiores Unidad Mérida, Universidad Nacional Autónoma de México, 97357, Mérida, Yucatán, Mexico

    Marisela Martínez-Ruíz & Víctor Arroyo-Rodríguez

  3. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, 58190, Morelia, Michoacán, Mexico

    Víctor Arroyo-Rodríguez

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

    Pedro A. D. Dias

  5. Departamento de Ecología y Recursos Naturales, Universidad Nacional Autónoma de México, Coyoacán, 04510, Mexico, Mexico

    Ricard Arasa-Gisbert

Authors
  1. Laura L. Saldívar-Burrola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marisela Martínez-Ruíz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Víctor Arroyo-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabricio Villalobos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pedro A. D. Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabiola López-Barrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ricard Arasa-Gisbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

VAR and LLSB developed the idea of the study, with support from FV, PADD and FLB. LLSB collected and analyzed the data with guidance from MMR, RAG, PADD and VAR. All authors made substantial contributions to the intellectual content, interpretation and editing of the manuscript.

Corresponding author

Correspondence to Víctor Arroyo-Rodríguez.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1 DOCX 16 kb

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saldívar-Burrola, L.L., Martínez-Ruíz, M., Arroyo-Rodríguez, V. et al. Can secondary forests mitigate the negative effect of old-growth forest loss on biodiversity? A landscape-scale assessment of two endangered primates. Landsc Ecol 37, 3223–3238 (2022). https://doi.org/10.1007/s10980-022-01532-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-022-01532-7

Keywords

Search

Navigation