Genetic Resources and Crop Evolution

, Volume 66, Issue 2, pp 401–413 | Cite as

Priority areas to collect germplasm of Annona (Annonaceae) in Mexico based on diversity and species richness indices

  • Diana Escobedo-López
  • Eduardo Campos-Rojas
  • J. Rubén Rodríguez-Núñez
  • Iran Alia-Tejacal
  • Carlos A. Núñez-ColínEmail author
Research Article


Annona genus refers to several tropical and subtropical species, which some of them have horticultural importance as fruit crops. Mexico reports 18 native and four exotic species of Annona genus in the country. Nevertheless, there are not studies about where to collect the germplasm of Annona in Mexico. This study aims to map the diversity (DI) and species richness (SR) of this genus to identify the best regions of Mexico to collect germplasm and to prioritize areas of conservation. It showed that germplasm of Annona genus is distributed in both tropical and subtropical areas in Mexico. The map of the observed SR showed that maximum SR of Annona genus were in Mexican Pacific Coast and Gulf of Mexico. Meanwhile in the map of Chao’s estimator of SR showed that the maximum SR of Annona genus were in Mexican Pacific Coast and Basin of Balsas. The map of Brillouin’s DI showed that maximum value of this index for Annona genus were in the same that showed the highest values of observed SR.


Annona Diversity index Estimators of species richness GIS Underutilized and neglected fruits 



Thanks to Mexico’s National Commission for Knowledge and Use of the Biodiversity (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, CONABIO, Mexico) for to facilitate the obtaining of passport data of the Global Network about Biodiversity Information (Red Mundial de Información sobre Biodiversidad, REMIB) for this investigation. The authors also thanks to anonymous reviewers for their thoughtful commentaries.


This work was supported by SAGARPA-CONACYT fund (project 266891) and by Universidad de Guanajuato (project CIIC 297/2018)

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10722_2018_718_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)


  1. Anaya-Esparza JL, Ramírez-Marez MV, Montalvo-González E, Sánchez-Burgos JA (2018) Cherimoya (Annona cherimola Mill.). In: Yahia EM (ed) Fruit, and vegetable phytochemicals. Chemistry and human health, 2nd edn. Wiley, Chichester, pp 993–1002. Google Scholar
  2. Andrés Agustín J (2015) Situación actual de las investigaciones de las Anonáceas en México. In: Vidal Lezama E, Vidal Martínez NA, Vidal Hernández L (eds) Anonáceas. Plantas Antiguas. Estudios Modernos. Parte 2. Universidad Autónoma Chapingo, Chapingo, pp 27–40Google Scholar
  3. Andrés Agustín J, Segura Ledesma S (2014) Conservación y uso de los recursos genéticos de Annonaceae en México. Rev Bras Frutic 36:118–124. CrossRefGoogle Scholar
  4. Anuragi H, Dhaduk HL, Kumar S, Dhruve JJ, Parekh MJ, Sakure AA (2016) Molecular diversity of Annona species and proximate fruit composition of selected genotypes. 3 Biotechnol 6:204. Google Scholar
  5. Awachare CM, Curian RM, Upreti KK, Laxman RH (2018) Morpho-physiological diversity in Annona species. Sci Hortic 234:58–62. CrossRefGoogle Scholar
  6. Bharad SG, Kulwal PL, Bagal SA (2009) Genetic diversity study in Annona squamosa by morphological, biochemical and RAPD markers. Acta Hortic 839:615–624. CrossRefGoogle Scholar
  7. Brown J, Laurentín H, Dávila M (2003) Genetic relationships between nine Annona muricata accessions using RAPD markers. Fruits 58:255–259. CrossRefGoogle Scholar
  8. Cazares-Sánchez E, Núñez-Colín CA, Domínguez-Álvarez JL, Luna-Morales CC, Rojas-Martínez RI, Segura S (2010) Potential biogeographic distribution of guava (Psidium guajava L.) in Mexico. Acta Hortic 849:55–62. CrossRefGoogle Scholar
  9. Chao A, Colwell RK, Lin CW, Gotelli NJ (2009) Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90:1125–1133. CrossRefGoogle Scholar
  10. Cocklin C (1989) Mathematical programming and resources planning I: the limitations of traditional optimization. J Environ Manag 28:127–141Google Scholar
  11. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (2017) Base de datos SNIB-REMIB. CONABIO, Mexico CityGoogle Scholar
  12. Coria-Téllez AV, Montalvo-González E, Obledo-Vázquez EN (2018) Soursop (Annona muricata). In: Yahia EM (ed) Fruit, and vegetable phytochemicals. Chemistry and human health, 2nd edn. Wiley, Chichester, pp 1243–1252. Google Scholar
  13. Couvreur TPL, Pirie MD, Chatrou LW, Saunders RMK, Su YCF, Richardson JE, Erkens RHJ (2011) Early evolutionary history of the flowering plant family Annonaceae: steady diversification and boreotropical geodispersal. J Biogeogr 38:664–680. CrossRefGoogle Scholar
  14. Dobzhansky T (1970) Genetics of the evolutionary process. Columbia University Press, New YorkGoogle Scholar
  15. Donadio LC (1997) Situação atual e perspectivas das Anonáceas. In: São José AR, Souza IVB, Morais OM, Rebouças TNH (eds) Anonáceas. Produção e Mercado (pinha, graviola, atemóia e cherimólia). Universidade Estadual do Sudoeste da Bahia, Vitoria da Conquista, pp 1–4Google Scholar
  16. Encina CL (2005) In: Litz RE (ed) Biotechnology of fruit and nut crops. Biotechnology in agriculture, vol 29. CABI publishing, London, pp 74–87CrossRefGoogle Scholar
  17. Escobedo-López D, Núñez-Colín CA, Espitia-Rangel E (2014) Adaptation of Cultivated Amaranth (Amaranthus spp.) and their wild relatives in Mexico. J Crop Improv 28:203–213. CrossRefGoogle Scholar
  18. Escribano P, Viruel MA, Hormaza JI (2004) Characterization and cross-species amplification of microsatellite markers in cherimoya (Annona cherimola Mill., Annonaceae). Mol Ecol Resour 4:746–748. CrossRefGoogle Scholar
  19. Escribano P, Viruel MA, Hormaza JI (2007) Molecular analysis of genetic diversity and geographic origin within an ex situ germplasm collection of cherimoya by using SSRs. J Am Soc Hortic Sci 132:357–367CrossRefGoogle Scholar
  20. Escribano P, Viruel MA, Hormaza JI (2008) Development of 52 new polymorphic SSR markers from cherimoya (Annona cherimola Mill.): transferability to related taxa and selection of a reduced set for DNA fingerprinting and diversity studies. Mol Ecol Resour 8:317–321. CrossRefGoogle Scholar
  21. Espitia-Rangel E, Escobedo-López D, Mapes-Sánchez C, Núñez-Colín CA (2010) Áreas prioritarias para colectar germoplasma de Amaranthus en México con base en la diversidad y riqueza de especies. Rev Mex Cienc Agr 1:609–617Google Scholar
  22. Fu XY, Peng SX, Yang S, Chen YH, Zhang JY, Mo WP, Zhu JY, Ye YX, Huang XM (2012) Effects of flooding on grafted Annona plants of different scion/rootstock combinations. Agric Sci 3:249–256. Google Scholar
  23. Green CS (1975) A comparison of diversity indices. In: Bascom WS (ed) Coastal water research project annual report number 15. Southern California Coastal Water Research Project, Segundo, pp 79–83Google Scholar
  24. Guarino L, Jarvis A, Hijmans RJ, Maxted N (2002) Geographic information systems (GIS) and the conservation and use of plant genetic resources. In: Engels JMM, Ramanatha Rao V, Brown AHD, Jackson MT (eds) Managing plant genetic diversity. International Plant Genetic Resources Institute (IPGRI), Rome, pp 387–404Google Scholar
  25. Hijmans RJ, Spooner DM (2001) Geographic distribution of wild potato species. Am J Bot 88:2101–2112. CrossRefGoogle Scholar
  26. Hijmans RJ, Spooner DM, Salas AR, Guarino L, de la Cruz J (2002) Atlas of wild potatoes. Systematic and ecogeographic studies on crop genepools 10. International Plant Genetic Resources Institute (IPGRI), RomeGoogle Scholar
  27. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. CrossRefGoogle Scholar
  28. Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS version 7.5. Manual. LizardTech and the University of California, BerkeleyGoogle Scholar
  29. Kershaw M, Williams PH, Mace GM (1994) Conservation of Afrotropical antelopes: consequences and efficiency of using different site selection methods and diversity criteria. Biodivers Conserv 3:354–372. CrossRefGoogle Scholar
  30. Larranaga N, Hormaza JI (2015) DNA barcoding of perennial fruit tree species of agronomic interest in the genus Annona (Annonaceae). Front Plant Sci 6:589. CrossRefGoogle Scholar
  31. Larranaga N, Albertazzi FJ, Fontecha G, Palmieri M, Rainer H, van Zonneveld M, Hormaza JI (2017) A Mesoamerican origin of cherimoya (Annona cherimola Mill.): implications for the conservation of plant genetic resources. Mol Ecol 26:4116–4130. CrossRefGoogle Scholar
  32. László Z, Baur H, Tóthmérész B (2013) Multivariate ratio analysis reveals Trigonoderus pedicellaris Thomson (Hymenoptera, Chalcidoidea, Pteromalidae) as a valid species. Syst Entomol 38:753–762. CrossRefGoogle Scholar
  33. León-Fernández AE, Montalvo-González E (2018) Sugar Apple (Annona squamosa). In: Yahia EM (ed) Fruit, and vegetable phytochemicals. Chemistry and human health, 2nd edn. Wiley, Chichester, pp 1253–1258. Google Scholar
  34. Morrone JJ, Escalante T, Rodríguez-Tapia G (2017) Mexican biogeographic provinces: map and shapefiles. Zootaxa 4277:277–279. CrossRefGoogle Scholar
  35. Núñez-Colín CA, Goytia-Jiménez MA (2009) Distribution and agroclimatic characterization of potential cultivation region sod physic nut in Mexico. Pesqui Agropecu Bras 44:1078–1085. CrossRefGoogle Scholar
  36. Núñez-Colín CA, Escobedo-López D, Hernández-Martínez MA, Ortega-Rodríguez C (2012a) Modelos de las zonas adecuadas de adaptación del tejocote (Crataegus mexicana DC.) por efecto del cambio climático. Agron Mesoam 23:241–246CrossRefGoogle Scholar
  37. Núñez-Colín CA, Hernández-Martínez MA, Escobedo-López D, Ortega-Rodríguez C (2012b) Priority areas to collect germplasm of Malacomeles (Rosaceae) in Mexico based on diversity and species richness indices. Plant Genet Resour 10:128–133. CrossRefGoogle Scholar
  38. Núñez-Colín CA, Alia-Tejacal I, Villarreal-Fuentes JM, Escobedo-López D, Rodríguez-Núñez JR, Peña-Caballero V (2017) Distribución, caracterización eco-climática y zonas potenciales de cultivo del zapote mamey en México. Rev Chapingo Ser Hortic 23:83–96. Google Scholar
  39. Núñez-Elisea R, Schaffer B, Fisher JB, Colls AM, Crane JH (1999) Influence of flooding on net CO2 assimilation, growth and stem anatomy of Annona species. Ann Bot 84:771–780. CrossRefGoogle Scholar
  40. Núñez-Elisea R, Caldeira ML, Crane JH, Schaffer B (2000) Clonal propagation of pond apple (Annona glabra L.) a flood tolerant rootstock for commercial Annona species. Proc Fla State Hortic Soc 113:15–16Google Scholar
  41. Ocampo JA, Coppens d’Eeckenbrugge G, Jarvis A (2010) Distribution of the genus Passiflora L. diversity in Colombia and its potential as an indicator for biodiversity management in the coffee growing zone. Diversity 2:1158–1180. CrossRefGoogle Scholar
  42. Pinto ACQ, Cordeiro MCR, de Andrade SEM, Ferreira FR, Filgueiras HAC, Alves RE, Kinpara DI (2005) Annona species. International Centre for Underutilised Crops, SouthamptonGoogle Scholar
  43. Rebelo AG (1994) Iterative selection procedures—centres of endemism and optimal placement of reserves. Strelitzia 1:231–257Google Scholar
  44. Rebelo AG, Siegfred WR (1992) Where should nature reserves be located in the Cape floristic region, South Africa? Models for the spatial configuration of a reserve network aimed at maximizing the protection of floral diversity. Conserv Biol 6:243–252. CrossRefGoogle Scholar
  45. Rzedowski J (1991) Diversidad y orígenes de la flora fanerogámica de México. Acta Bot Mex 14:3–21. CrossRefGoogle Scholar
  46. Rzedowski J (1993) Diversity and origins of the phanerogamic flora of Mexico. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico. Origins and distribution. Oxford University Press, New York, pp 129–144Google Scholar
  47. Sætersdal M, Line JM, Birks HJB (1993) How to maximize biological diversity in nature reserve selection: vascular plants and breeding birds in deciduous woodlands, western Norway. Biol Conserv 66:131–138. CrossRefGoogle Scholar
  48. Scheldeman X, Willemen L, Coppens d’Eeckenbrugge G, Romeijn-Peeters E, Restrepo MT, Romero Motoche J, Jiménez D, Lobo M, Medina CI, Reyes C, Rodríguez D, Ocampo JA, Van Damme P, Goetgebeur P (2007) Distribution, diversity and environmental adaptation of highland papayas (Vasconcellea spp.) in tropical and subtropical America. Biodivers Conserv 16:1867–1884. CrossRefGoogle Scholar
  49. Servicio de Información Agroalimentaria y Pesquera, SIAP (2018) Anuario Estadístico de la Producción Agrícola 2017. Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (Mexico) Accessed 12 Oct 2018
  50. Shen TJ, Chao A, Lin CF (2003) Predicting the number of new species in further taxonomic sampling. Ecology 84:798–804.;2 CrossRefGoogle Scholar
  51. Vavilov NI (1994) México y Centroamérica como centro básico de origen de las plantas cultivadas del nuevo mundo. Rev Geogr Agric 20:15–34Google Scholar
  52. Vidal Hernández L, Vidal Martínez NA, Colorado Elox JJ, Vidal Martínez EC, Ruiz Bello R, Ruiz Ramírez J, Chiquito Contreras RG, Rivera Fernández A, Alemán Chávez I (2015) Recursos fitogenéticos de las anonáceas en el estado de Veracruz. In: Vidal Lezama E, Vidal Martínez NA, Vidal Hernández L (eds) Anonáceas. Plantas Antiguas. Estudios Modernos. Parte 2. Universidad Autónoma Chapingo, Chapingo, pp 1–26Google Scholar
  53. Vidal Lezama E, Sáenz Pérez CA, Curiel Rodríguez A, Segura Ledesma SD, Cuevas Sánchez JA, Campos Rojas E (2015) Propagación sexual de cinco especies de Anonáceas. Una breve revisión. In: Vidal Lezama E, Vidal Martínez NA, Vidal Hernández L (eds) Anonáceas. Plantas Antiguas. Estudios Modernos. Parte 2. Universidad Autónoma Chapingo, Chapingo, pp 73–122Google Scholar
  54. Villaseñor JL (2003) Diversidad y distribución de las Magnoliophyta de México. Interciencia 28:160–168Google Scholar
  55. Villaseñor JL (2016) Checklist of the native vascular plants of Mexico. Rev Mex Biodivers 87(559–902):73–122. Google Scholar
  56. Zagaja SW (1988) Exploración de recursos genéticos. In: Moore JN, Janick J (eds) Métodos genotécnicos en frutales. AGT Editor, Mexico City, pp 3–12Google Scholar
  57. Zill GE, Mahdeen H (1998) Variation in graft compatibility of Annona glabra as a rootstock. Proc Fla State Hortic Soc 111:316Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Campo Experimental Bajío, Instituto Nacional de Investigaciones ForestalesAgrícolas y PecuariasCelayaMexico
  2. 2.Departamento de FitotecniaUniversidad Autónoma ChapingoTexcocoMexico
  3. 3.Programa de BiotecnologíaUniversidad de GuanajuatoCelayaMexico
  4. 4.Facultad de Ciencias AgropecuariasUniversidad Autónoma del Estado de MorelosCuernavacaMexico

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