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Integrating expert knowledge and ecological niche models to estimate Mexican primates’ distribution

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Abstract

Ecological niche modeling is used to estimate species distributions based on occurrence records and environmental variables, but it seldom includes explicit biotic or historical factors that are important in determining the distribution of species. Expert knowledge can provide additional valuable information regarding ecological or historical attributes of species, but the influence of integrating this information in the modeling process has been poorly explored. Here, we integrated expert knowledge in different stages of the niche modeling process to improve the representation of the actual geographic distributions of Mexican primates (Ateles geoffroyi, Alouatta pigra, and A. palliata mexicana). We designed an elicitation process to acquire information from experts and such information was integrated by an iterative process that consisted of reviews of input data by experts, production of ecological niche models (ENMs), and evaluation of model outputs to provide feedback. We built ENMs using the maximum entropy algorithm along with a dataset of occurrence records gathered from a public source and records provided by the experts. Models without expert knowledge were also built for comparison, and both models, with and without expert knowledge, were evaluated using four validation metrics that provide a measure of accuracy for presence-absence predictions (specificity, sensitivity, kappa, true skill statistic). Integrating expert knowledge to build ENMs produced better results for potential distributions than models without expert knowledge, but a much greater improvement in the transition from potential to realized geographic distributions by reducing overprediction, resulting in better representations of the actual geographic distributions of species. Furthermore, with the combination of niche models and expert knowledge we were able to identify an area of sympatry between A. palliata mexicana and A. pigra. We argue that the inclusion of expert knowledge at different stages in the construction of niche models in an explicit and systematic fashion is a recommended practice as it produces overall positive results for representing realized species distributions.

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Acknowledgements

We are grateful to the 46 primatologists who participated in the elicitation process and shared their knowledge with us (Appendix 1). The elicitation workshop was funded by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad and the Comisión Nacional de Áreas Naturales Protegidas, México. Sergio Díaz-Martínez provided support for the edition of images and helpful comments on earlier versions of this paper. GRF thanks the Instituto Politécnico Nacional and CONACYT (grant 157656). GPM thanks the colleagues of COBIUS A.C., the regional citizens who participated in the monitoring sessions and the directors of the natural protected areas: Selva El Ocote, Sepultura, Encrucijada, Sian Kaan, Yum Balam, Balam Kaax, UayMil, Cañón de Sumidero, Laguna de Términos, and Pantanos de Centla, from CONANP, for their sponsorship by the PROMOBI y PROCER 2013-2016 programs. ECP thanks the Posgrado en Ciencias Biológicas (PCB) at the Universidad Nacional Autónoma de México for logistic and academic support. This paper is part of the requirements for the PhD in Sciences at the PCB-UNAM. ECP was supported by a graduate scholarship from the Consejo Nacional de Ciencia y Tecnología, Mexico.

Author information

Author notes

  1. Enrique Martínez-Meyer

    Present address: Centro del Cambio Global y la Sustentabilidad, AC, Centenario Instituto Juárez s/n, 86080, Villahermosa, Mexico

Authors and Affiliations

  1. Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico

    Edith Calixto-Pérez & Enrique Martínez-Meyer

  2. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico

    Edith Calixto-Pérez

  3. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico City, 14010, Mexico

    Jesús Alarcón-Guerrero, Tania Urquiza-Haas & Patricia Koleff

  4. Unidad Interdisciplinaria en Ingeniería y Tecnologías Avanzadas, Instituto Politécnico Nacional, Mexico City, Mexico

    Gabriel Ramos-Fernández

  5. Instituto de Investigaciones en Matemáticas Aplicadas y en Sistemas, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Gabriel Ramos-Fernández

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

    Pedro Américo D. Dias & Ariadna Rangel-Negrín

  7. Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Yucatán, 97310, Mexico

    Monica Améndola-Pimenta

  8. Institut Obert de Catalunya, Avinguda del Parallel, Barcelona, 08004, Spain

    Cristina Domingo

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

    Víctor Arroyo-Rodríguez

  10. Conservación de la Biodiversidad del Usumacinta, AC, Emiliano Zapata, 86990, Tabasco, Mexico

    Gilberto Pozo-Montuy & Braulio Pinacho-Guendulain

  11. Grupo de Biología para la Conservación, S. de R.L. de C.V., 72810, Puebla de Zaragoza, Mexico

    Gilberto Pozo-Montuy

Authors
  1. Edith Calixto-Pérez
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  2. Jesús Alarcón-Guerrero
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  3. Gabriel Ramos-Fernández
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  4. Pedro Américo D. Dias
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  5. Ariadna Rangel-Negrín
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  6. Monica Améndola-Pimenta
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  7. Cristina Domingo
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  8. Víctor Arroyo-Rodríguez
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  9. Gilberto Pozo-Montuy
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  10. Braulio Pinacho-Guendulain
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  11. Tania Urquiza-Haas
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  12. Patricia Koleff
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  13. Enrique Martínez-Meyer
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Corresponding author

Correspondence to Enrique Martínez-Meyer.

Appendices

Appendix 1. List of 19 bioclimatic variables used into the modeling

BIO1 = annual mean temperature

BIO2 = mean diurnal range (mean of monthly (max temp–min temp))

BIO3 = isothermality (BIO2/BIO7) (*100)

BIO4 = temperature seasonality (standard deviation *100)

BIO5 = max temperature of warmest month

BIO6 = min temperature of coldest month

BIO7 = temperature annual range (BIO5–BIO6)

BIO8 = mean temperature of wettest quarter

BIO9 = mean temperature of driest quarter

BIO10 = mean temperature of warmest quarter

BIO11 = mean temperature of coldest quarter

BIO12 = annual precipitation

BIO13 = precipitation of wettest month

BIO14 = precipitation of driest month

BIO15 = precipitation seasonality (coefficient of variation)

BIO16 = precipitation of wettest quarter

BIO17 = precipitation of driest quarter

BIO18 = precipitation of warmest quarter

BIO19 = precipitation of coldest quarter

Appendix 2. Maxent default parameters

Max number of background points

10,000

Maximum iterations

500

Convergence threshold

0.00001

Convergence threshold

0.00001

Default prevalence

0.5

Appendix 3. List of experts who participated in the elicitation process

Name

Institution

Group of participation

Assistance to workshop

Participation in the electronic survey

Gabriel Ramos Fernández

President of the Mexican Association of Primatology

Core group

X

X

Pedro Américo Duarte Dias

Instituto de Neuroetología, Universidad Veracruzana

Core group

X

X

Mónica Améndola Pimenta

Mexican Association of Primatology

Core group

X

X

Ariadna Rangel Negrín

Barcelona University

Core group

X

X

Víctor Arroyo Rodríguez

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Core group

X

 

Celene Espadas Manrique

Centro de Investigación Científica de Yucatán, A.C.

Consulting group

 

X

Francisca Vidal

Instituto de Ecología A.C

Consulting group

 

X

Juan Carlos Serio Silva

Instituto de Ecología A.C.

Consulting group

 

X

Jurgi Cristóbal

Centro de Investigaciones Tropicales, Universidad Veracruzana

Consulting group

 

X

Teresita de Jesús Ortiz Martínez

Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Oaxaca.

Consulting group

X

X

Magali Bonilla

Instituto de Neuroetología, Universidad Veracruzana

Consulting group

X

X

Miguel Angel Gómez Gómez

Reserva de la Biosfera “Pantanos de Centla.” Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Patricia Oropeza Hernández

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Griselda Pérez Sarabia

Procuraduría Federal de Protección al Ambiente

Consulting group

X

 

Carlos Mario Burelos Jiménez

Chief of the Wildlife Department, Secretaría del Medio Ambiente y Recursos Naturales.

Consulting group

X

 

Gilberto Pozo Montuy

Instituto de Neuroetología, Universidad Veracruzana

Consulting group

X

X

Fernando Winzig León

Secretaría del Medio Ambiente y Recursos Naturales.

Consulting group

X

 

Rosalía Pastor Nieto

Dirección General de Zoológicos de la Ciudad de México.

Consulting group

X

 

Víctor Manuel O. Torres

Wildlife Department, Secretaría del Medio Ambiente y Recursos Naturales.

Consulting group

X

 

Jose O. Molina

Centro de Estudios de Políticas Públicas y Desarrollo Sustentable, A.C.

Consulting group

X

 

Rogelio Manríquez Martínez

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Irma de J. Serrano Sánchez

Parque Nacional Cañón del Sumidero, Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Luis Arturo Álvarez Márquez

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Patricia G. Robles Zenteno

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Eduardo Rendón Hernández

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Guillermo Islas Dondé

Facultad de Ciencias, Universidad Nacional Autónoma de México

Consulting group

X

 

Juan Carlos Sánchez Olmos

Conservación Sin Fronteras

Consulting group

X

 

Fernando Miranda Martínez

Conservación Sin Fronteras

Consulting group

X

 

Cristina Domingo Balcells

Instituto de Biología, Universidad Nacional Autónoma de México

Consulting group

X

 

Arturo Ramírez Ortiz

Conservación Sin Fronteras

Consulting group

X

 

Sandra Flores Hernández

Área de Protección de Flora y Fauna “Otoch Ma’ax Yetel Kooh”

Consulting group

X

 

Juan Manuel Cornelio Pérez

Secretaría del Medio Ambiente y Recursos Naturales.

Consulting group

X

 

Rosa Olivia Rodríguez Reyes

Reserva de la Biosfera “Pantanos de Centla,” Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Katya Andrade Escobar

Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Carlos A. Guichard Romero

Reserva de la Biosfera “El Triunfo,” Comisión Nacional de Áreas Naturales Protegidas

Consulting group

X

 

Francisco García Orduña

Instituto de Neuroetología, Universidad Veracruzana

Consulting group

X

 

Alfredo Cuarón Orozco

Multicriteria S.C.

Consulting group

X

 

Eduardo García Frapolli

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Consulting group

X

 

Ernesto Rodríguez Luna

Universidad Veracruzana

Consulting group

X

 

Armando Figueroa

Procuraduría Federal de Protección al Ambiente

Consulting group

X

 

Francisco García Contreras

Procuraduría Federal de Protección al Ambiente

Consulting group

X

 

Tamara Ortiz Ávila

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Consulting group

X

 

Mateo Pérez Ortiz

Conservación Sin Fronteras

Consulting group

X

 

Diana Platas Neri

Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de México

Consulting group

X

 

Jorge Luis Cruz Rueda de León

Unidad de Manejo de Fauna Silvestre “Nueva Era de la Chontalpa”

Consulting group

X

 

Bárbara Ayala Orozco

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Consulting group

X

 

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Calixto-Pérez, E., Alarcón-Guerrero, J., Ramos-Fernández, G. et al. Integrating expert knowledge and ecological niche models to estimate Mexican primates’ distribution. Primates 59, 451–467 (2018). https://doi.org/10.1007/s10329-018-0673-8

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