SciELO - Scientific Electronic Library Online

 
 número129Sistemas silvopastoriles enriquecidos: una propuesta para integrar la conservación en la producción ganadera en comunidades rurales de Los Tuxtlas, MéxicoXerocomellus carmeniae (Boletales, Basidiomycota), un nuevo hongo del noreste de México índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Acta botánica mexicana

versão On-line ISSN 2448-7589versão impressa ISSN 0187-7151

Act. Bot. Mex  no.129 Pátzcuaro  2022  Epub 31-Out-2022

https://doi.org/10.21829/abm129.2022.2023 

Research articles

Scarification of yellow mombin endocarps (Spondias mombin, Anacardiaceae) due to passage through the digestive tract of mantled howler monkeys (Alouatta palliata mexicana): a microscopic look

Escarificación de endocarpos del jobo (Spondias mombin, Anacardiaceae) debido al paso por el tracto digestivo de monos aulladores de manto (Alouatta palliata mexicana): un vistazo microscópico

Daniela Alicia Torres-Anaya1 
http://orcid.org/0000-0001-5958-7705

Wesley Dáttilo2 
http://orcid.org/0000-0002-4758-4379

Greta Hanako Rosas-Saito3 
http://orcid.org/0000-0003-3203-5980

Juan Carlos Serio-Silva4  5 
http://orcid.org/0000-0002-0582-2041

1Instituto de Ecología, A.C., Posgrado en Ciencias, Carretera antigua a Coatepec km 351, 91073 Xalapa-Enríquez, Veracruz, Mexico.

2Instituto de Ecología, A.C., Red de Ecoetología, Carretera antigua a Coatepec km 351, 91073 Xalapa-Enríquez, Veracruz, Mexico.

3Instituto de Ecología, A.C., Red de Estudios Moleculares Avanzados, Carretera antigua a Coatepec km 351, 91073 Xalapa-Enríquez, Veracruz, Mexico.

4Instituto de Ecología, A.C., Red de Biología y Conservación de Vertebrados, Carretera antigua a Coatepec km 351, 91073 Xalapa-Enríquez, Veracruz, Mexico.


Abstract:

Background and Aims:

Several studies have emphasized the important role of howler monkeys (Alouatta palliata mexicana) in seed dispersal and, as a result, in the regeneration of fleshy-fruited plant populations in tropical forests. However, there is little empirical evidence regarding the possible mechanisms that would allow howler monkeys to promote seed germination of many plant species, including seed coat scarification. In this study, we evaluated whether endocarps of Spondias mombin (Anacardiaceae), an important species in howler monkey diet, could be scarified by passage through the digestive tract of these primates.

Methods:

We collected endocarps from howler monkey feces as well as ripe fruits fallen on the ground, in the region of Los Tuxtlas, Catemaco municipality, Veracruz, Mexico. By analyzing endocarp transverse sections using a scanning electron microscope, we measured the thickness of the outer layer and tested differences between both types of samples (i.e., fruit endocarps and endocarps that had passed through the digestive tract).

Key results:

We observed that the outer layer thickness of endocarps in fruits was greater (X~=47.05±9.69 µm) than that of endocarps found in feces (X~=1.51±3.60 µm) (W=0.48, p<0.001).

Conclusions:

Our results highlight that consumption of S. mombin endocarps by A. p. mexicana may have a scarification effect on the tissues that constitute the outer layer. This supports the hypothesis of the role of frugivores, such as howler monkeys, in reducing the seed coat and thus increasing germination ability; therefore, being key organisms in regeneration dynamics of tropical forests.

Key words: frugivory; primates; scanning electron microscopy; seed dispersal effectiveness

Resumen:

Antecedentes y Objetivos:

Diversos estudios han destacado el importante papel de los monos aulladores (Alouatta palliata mexicana) en la dispersión de semillas y, con ello, en la regeneración de las poblaciones de plantas con frutos carnosos de los bosques tropicales. Sin embargo, poca es la evidencia empírica sobre cuáles podrían ser los mecanismos que les permitiría a los monos aulladores favorecer la germinación de las semillas de muchas especies de plantas, incluyendo la escarificación de su cubierta externa. En este trabajo se evaluó si los endocarpos de Spondias mombin (Anacardiaceae), una especie importante en la dieta de los monos aulladores, podrían ser escarificados al pasar por el tracto digestivo de estos primates.

Métodos:

Se colectaron endocarpos de las heces de monos aulladores, así como frutos maduros del suelo, en la región de Los Tuxtlas, municipio Catemaco, Veracruz, México. Mediante cortes transversales de los endocarpos y su análisis en el microscopio electrónico de barrido, se tomaron medidas del grosor de la cubierta externa y probaron las diferencias entre ambos tipos de muestras (i.e., endocarpos de frutos y endocarpos que pasaron por el tracto digestivo).

Resultados clave:

Se observó que el grosor de la cubierta de los endocarpos en frutos fue mayor (X~=47.05±9.69 µm) que el de endocarpos en heces (X~=1.51±3.60 µm) (W=0.48, p<0.001).

Conclusiones:

Los resultados evidencian que la ingesta de endocarpos de S. mombin por A. p. mexicana puede tener un efecto de escarificación de los tejidos que conforman su cubierta externa. Esto apoya la versión sobre la función de los frugívoros, como los monos aulladores, reduciendo la cubierta externa de las semillas y aumentando así su capacidad para germinar; siendo, por lo tanto, organismos clave en la dinámica de regeneración de bosques tropicales.

Palabras clave: efectividad de dispersión de semillas; frugivoría; microscopía electrónica de barrido; primates

Introduction

Frugivory is one of the principal processes in the natural regeneration of numerous plant populations, given that this is mostly sustained by animal-mediated seed dispersal (Jordano, 2000). Seed dispersers play a key role in ecology and evolution of fleshy-fruited plants, especially in tropical environments, where it is estimated that between 70% and 90% of all woody species are dispersed by vertebrates (Fleming et al., 1987; Jordano, 2000). In this animal-plant interaction, animals obtain nutrients from fruit consumption, whereas plants are able to disperse their seeds far from the parent plant. Moreover, they can obtain other benefits from the treatment the seeds undergo in the disperser’s digestive tract, such as pulp removal (seed cleaning), outer layer scarification, and/or fertilization effects by nutrients in the fecal matter in which seeds are embedded (Dennis, 2007; Traveset et al., 2007; Schupp et al. 2010).

Some vertebrate groups, owing to their anatomical, physiological and behavioral traits, can be important seed dispersers in tropical environments (Chapman and Russo, 2006). Primates, for instance, ingest a wide variety of fruits and defecate or spit out numerous seeds (Lambert, 1999). As a consequence, their great value for maintaining vegetal structure and composition of the ecosystems they inhabit has been acknowledged (Duncan and Chapman, 1999; Chapman and Russo, 2006; Link and Di Fiore, 2006; Stevenson, 2011). Howler monkeys (Alouatta spp.) are a genus of primates distributed in tropical areas from the northwest of Argentina to the south of Mexico. They are considered effective dispersers since many of the seeds they ingest remain viable after passing through their digestive tract (Arroyo-Rodríguez et al., 2015). In addition, because of their body size (≥4 kg), they are able to transport large seeds (≥10 mm) (Andresen, 2002). Dispersal services provided by these primates might be particularly relevant for some plant species with voluminous seeds (Anzures-Dadda et al., 2011), especially in heavily defaunated environments where many primary dispersers are no longer present (Gardner et al., 2019). The mantled howler monkey (Alouatta palliata mexicana Merriam, 1902), an endangered primate species, has its northern distribution limit on the American continent in the Los Tuxtlas region, Veracruz state, Mexico, where it feeds on the fruits of at least 51 plant species (22 families, 33 genera) (Estrada and Coates-Estrada, 1984; Serio-Silva et al., 2002; Asensio et al., 2007), therefore being a potential disperser of their seeds.

The yellow mombin (Spondias mombin L.) is one of the three species from the family Anacardiaceae whose fruits are ingested by mantled howler monkeys in the region of Los Tuxtlas (Dáttilo et al., 2014). During the fructification period (July-October) these fruits constitute a significant source of lipids, proteins, minerals, fiber, and mostly carbohydrates and energy (Kcal) (Serio-Silva et al., 2002; Vázquez-Torres et al., 2010; Hauck-Tiburski et al., 2011). This tree is native from the south of Mexico to the east of Brazil, though widely cultivated in moist tropics (Mitchell and Daly, 2015). Its dispersal unit is a lignified endocarp of 18-25 mm in length, by 12-18 mm in diameter, inside of which are found up to five radially arranged seeds (Fig. 1) (Lozano, 1986; Azevedo et al., 2004; Niembro-Rocas et al., 2010). The endocarp represents a physical barrier that, while it protects seeds from possible environmental aggressions (e.g., extreme temperatures, fungi, bacteria, and predation) (Soriano and Martínez-Villegas, 2019), establishes physical dormancy; since its hardness limits embryo expansion, gas exchange and/or water absorption, rendering germination a slow and irregular process (Baskin et al., 2000; Martins et al., 2019; Magalhães de Souza et al., 2020). In order to break this type of dormancy and promote germination, it is necessary to fracture this layer and, in nature, rupture can happen via abrasion by animal ingestion (Delgado-Sánchez et al., 2011; Baskin and Baskin, 2014).

Figure 1: Yellow mombin (Spondias mombin L.) endocarp transverse section. P=parenchyma; Sc=sclerenchyma; S=seed; L=locule. This picture shows a mature seed and four immature ones, contained in each of the five locules. 

During the passage through the digestive tract of a frugivore, the outer layer of a seed can be scarified mechanically or chemically, making it more permeable to water and gases in the environment, as well as decreasing the pressure needed to break it (Paulsen and Högstedt, 2002; Traveset et al., 2007). This treatment can determine the seeds’ germination ability and it can be key in population dynamics of many fleshy-fruited plant species (Traveset et al., 2007; Schupp et al., 2010). Particularly, howler monkeys may be able to swallow some mombin fruits and defecate whole endocarps, unlike other smaller frugivores which only consume the pulp, such as birds and bats (Janzen, 1985; Bravo, 2009; Arroyo-Rodríguez et al., 2015). Furthermore, due to chewing and long retention time in the intestines of these primates (approximately 20.4 hours) (Garber et al., 2015), it has been suggested that endocarps can be sufficiently scarified to break physical dormancy of the seeds and facilitate their germination (Baskin and Baskin, 2014). So far, no studies have measured scarification of the tissues structuring or surrounding seeds later dispersed by howler monkeys, nor by any other primate, despite this mechanism has been considered influential in their high effectiveness as dispersers. Therefore, the goal of this study was to evaluate, by scanning electron microscopy techniques, Spondias mombin endocarp scarification as a consequence of digestive tract passage in Alouatta palliata mexicana.

Materials and Methods

Study site

The Los Tuxtlas Biosphere Reserve (LTBR) is located in the southeast of Veracruz, Mexico. This region comprises a steep elevation gradient (0-1720 m a.s.l.), which influences weather and local vegetation significantly. The weather is tropical wet, with a mean annual precipitation of 4900 mm, and temperatures ranging between 27 and 36 °C, for the upper range, and 8 and 18 °C for the lower range (Soto and Gama, 1997). The study site, where howler monkey (A. p. mexicana) feces and ripe yellow mombin fruits were collected, is at the limits of the LTBR in the locality of Coyame, neighboring Catemaco Lake (18°26ʹ12.60ʹʹN, 95°1ʹ44.80ʹʹW) (Fig. 2). The original vegetation around the lake was mostly constituted by tall evergreen forest (Castillo and Laborde, 2004), but currently only a few isolated elements and heavily disturbed rainforest fragments in different succession stages remain (González-Christen et al., 2013). Particularly, the study site is mainly constituted by patches of secondary vegetation, alternating with anthropized zones, such as dwellings and disturbed areas for agricultural activities, mostly livestock.

Figure 2: Locality of collection of feces of Alouatta palliata mexicana Merriam, 1902 and ripe fruits of Spondias mombin L., within the Los Tuxtlas Biosphere Reserve, in Catemaco municipality, Veracruz, Mexico. 

Endocarp collection and separation

In August 2018, yellow mombin trees in which, according to locals, sightings of howler monkeys occurred, were identified. Individuals were located and feces containing endocarps (N=22) as well as ripe fruits fallen on the ground (N=22) were collected, some of which had been thrown by the monkeys after partially removing the pulp, but leaving the endocarps intact (Fig. 3). It is important to mention that the number of trees from which the samples were obtained is unknown. Endocarps were extracted manually from fruits and feces; they were washed with distilled water until all pulp or fecal matter was removed. Then, in order to prevent the growth of fungi and/or bacteria over the endocarps, they were introduced in a digital dehydrator (NESCO© FD-2000, Fort Atkinson, USA) at 40 °C for seven hours in the laboratory of the Red de Biología y Conservación de Vertebrados, of the Instituto de Ecología, A.C. (INECOL) in Xalapa, Veracruz, Mexico.

Figure 3: Field collection of yellow mombin endocarps in fruits and droppings. A., adult female of Alouatta palliata mexicana Merriam, 1902; B., mature fruit of Spondias mombin L.; C., endocarp defecated by a howler monkey. 

Micromorphological analyses

Using single edge razors, endocarp transverse sections were obtained, which were fixed in 3% glutaraldehyde buffered with Sorenson´s phosphate and kept under environmental pressure and room temperature for 12 hours. After fixation, three washes with phosphate buffer were done, for 15 minutes each.

Sections were dehydrated through a graded series of ethanol (2-hour intervals for each 10% increment of ethanol), starting with 30% OH, to 90% ethanol. Then, sections were immersed in absolute alcohol three times for an hour. Once dehydrated, they were dried in a critical point dryer (K580, Quorum, Laughton, UK) in the laboratory of the Red de Estudios Moleculares Avanzados, from INECOL, in Xalapa, Veracruz, Mexico. Finally, they were mounted using aluminum sample holders over a conductive carbon tape and thinly coated with gold. Samples were analyzed using a scanning electron microscope (QuantaTM 250 FEG, Field Electron and Ion Company, Hillsboro, USA) of the Red de Estudios Moleculares Avanzados, from INECOL, in Xalapa, Veracruz, Mexico, producing digital images at 500× magnification. Finally, for each photograph, 10 measures of endocarp’s outer layer thickness were taken, using ImageJ v. 1.53a software (Schneider et al., 2012).

Statistical analysis

Given the non-normal distribution of measurement data, statistical differences between both sample types were determined by a Wilcoxon signed-rank test, using RStudio software v. 1.4.1717 (RStudio Team, 2021). Endocarp treatment (fruits/droppings) was considered an explanatory variable and outer layer thickness a response variable.

Results

We observed that the outer layer of endocarps extracted from S. mombin fruits was thicker (X~=48.16±9.72 µm, N=22) than that of the endocarps ingested by howler monkeys (X~=1.51±3.60 µm, N=22) (W=0.48, p<0.001) (Fig. 4). It is worth mentioning that in most cases (81.8%) this tissue was completely scarified, together with some parenchymal and vascular bundle cells (Fig. 5).

Figure 4: Data distribution of outer layer thickness of Spondias mombin L. intact endocarps (Fruits) and after gut passage in Alouatta palliata mexicana Merriam, 1902 specimens (Droppings). For the latter, outliers correspond to endocarps whose outer layer was not completely scarified. 

Figure 5: Scanning electron microscope images of yellow mombin (Spondias mombin L.) endocarp transverse sections. St=sclerenchymatous tissue; P=parenchyma; Vb=vascular bundle. A-C., endocarps extracted from mature fruits; D-F. endocarps extracted from feces of mantled howler monkey (Alouatta palliata mexicana Merriam, 1902). In D a remnant of sclerenchymatous tissue on a vascular bundle is marked with an arrow. 

Discussion

Our evidence shows that passage through the digestive tract of A. p. mexicana modified the thickness of the outer layer of the endocarps of S. mombin, which is a layer of sclerenchymatous tissue composed of fiber cells, which delimits the endocarp and it is adjacent to the mesocarp of the fruit (Mitchell and Daly, 2015; Herrera et al., 2018). While yellow mombin fruits are not highly ingested by howler monkeys in the LTBR region, as opposed to other species whose fruits are available throughout the year (e.g., Ficus spp.) (Estrada and Coates-Estrada, 1984; Cristóbal-Azkarate and Arroyo-Rodríguez, 2007), their consumption might be a determining event for the establishment of new yellow mombin individuals and the permanence of this population. This is due to the quality of the treatment in the digestive tract, which could influence the breaking of physical dormancy of seeds found within endocarps.

The effect in seed structure as a result of frugivory has been reported and measured in some species of animals and plants. Just as consumption of S. mombin fruits by A. p. mexicana decreased the thickness of the endocarp outer layer, Nogales et al. (2005) observed that seed coat of Rubia fruticosa Aiton seeds ingested by lizards (Gallotia sp.), birds (Sylvia sp., Corvus sp., Larus sp.), squirrels (Atlantoxerus sp.), and rabbits (Oryctolagus sp.), was thinner in relation to intact seeds; finding, in addition, differences among animal groups. On the contrary, Ribeiro et al. (2016) did not observe differences in seed coat thickness of Clidemia urceolata DC., Miconia rubiginosa (Bonpl.) DC. and Leandra aurea (Cham.) Cogn., ingested and defecated by two bird species (Tangara sayaca Linnaeus, 1766 and Schistoclamys ruficapillus Vieillot, 1817), and non-ingested seeds. Hence, the degree of scarification depends both on inherent traits of frugivore species and traits of the fruits they ingest and their dispersal structures; accordingly, understanding the interaction between animal and plant traits is necessary to comprehend the extent and effectiveness of endozoochory (Schupp, 1993; Schupp et al., 2010).

Scarification of the outer layer of S. mombin endocarps by gut passage in mantled howler monkeys could eventually promote and/or facilitate mombin seed germination, although this was not evaluated in this study. However, for the black howler monkey (Alouatta pigra Lawrence, 1933) and spider monkey (Ateles geoffroyi Kuhl, 1820), the other two primate species distributed in Mexico, it has been reported that mombin fruit ingestion results in faster germination and higher germination percentage in relation to those fruits that were not ingested (Morales-Mávil et al., 2005; González-Di Pierro et al., 2021). The same applies to frugivores in other groups, such as the green iguana (Iguana iguana Linnaeus, 1758) and the toucan (Ramphastos sulfuratus R. Lesson, 1830), which also occur in the LTBR region (Morales-Mávil et al., 2005). Therefore, it is evident that frugivory has a positive effect on S. mombin seed germination, which might be due in part to the thinning of the endocarp outer layer, as a consequence of its consumption, as in the results here obtained.

The present study represents the first evaluation of the scarification effect by howler monkeys (A. p. mexicana), or any other primate, using electron scanning microscopy techniques. These results present a detailed look at the abrasion that different seed tissues can experience when being ingested by howler monkeys, which contributes to a better understanding of the many processes involved in seed dispersal dynamics carried out by primates. Finally, for future studies, we consider that it is of great importance to carry out germination tests, in order to have a more comprehensive view of this animal-plant interaction and of its importance for biodiversity maintenance and conservation.

Acknowledgements

Authors thank Alicia Alejandra Hernández Tejeda for the support in sample collection and during early stages of microscopy samples preparation, Jorge Ramos Luna for field work support and audiovisual materials (photographs and video), Adriana Sandoval Comte for her support in generating the map of the study site, and Sergio Albino Miranda for his support in treatment of biological samples in the laboratory of the Red de Biología y Conservación de Vertebrados, at INECOL. Likewise, to the personnel of the microscopy unit of the Red de Estudios Moleculares Avanzados, from the same institution.

Literature cited

Andresen, E. 2002. Primary seed dispersal by red howler monkeys and the effect of defecation pattern on the fate of dispersed seeds. Biotropica 34(2): 261-272. DOI: https://doi.org/10.1111/j.1744-7429.2002.tb00537.x [ Links ]

Anzures-Dadda, A., E. Andresen, M. L. Martínez and R. H. Manson. 2011. Absence of howlers (Alouatta palliata) influences tree seedlings densities in tropical rain forest fragments in southern Mexico. International Journal of Primatology 32: 634-651. DOI: https://doi.org/10.1007/s10764-011-9492-0 [ Links ]

Arroyo-Rodríguez, V., E. Andresen , S. P. Bravo and P. R. Stevenson. 2015. Seed Dispersal by Howler Monkeys: Current Knowledge, Conservation Implications, and Future Directions. In: Kowalewski, M. M., P. A. Garber, L. Cortés-Ortiz, B. Urbani and D. Youlatos (eds.). Howler Monkeys: Behavior, Ecology, and Conservation. Springer. Nueva York, USA. Pp. 111-139. DOI: https://doi.org/10.1007/978-1-4939-1960-4_5 [ Links ]

Asensio, N., J. Cristobal-Azkarate, P. A. D. Dias, J. J. Vea and E. Rodríguez-Luna. 2007. Foraging Habits of Alouatta palliata mexicana in Three Forest Fragments. Folia Primatologica 78(3): 141-153. DOI: https://doi.org/10.1159/000099136 [ Links ]

Azevedo, D. de M., A. M. da Silva Mendes and A. F. de Figuereido. 2004. Característica da germinação e morfologia do endocarpo e plântula de taperebá (Spondias mombin L.) - Anacardiaceae. Jaboticabal, Revista Brasileira de Fruticultura 26(3): 534-537. DOI: https://doi.org/10.1590/S0100-29452004000300038 [ Links ]

Baskin, C. C. and J. M. Baskin. 2014. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. Elsevier. San Diego, USA. 1586 pp. DOI: https://doi.org/10.1016/C2013-0-00597-X [ Links ]

Baskin, J. M., C. C. Baskin and X. Lix. 2000. Taxonomy, Anatomy and Evolution of Physical Dormancy in Seeds. Plant Species Biology 15(2): 139-152. DOI: https://doi.org/10.1046/j.1442-1984.2000.00034.x [ Links ]

Bravo, S. P. 2009. Implications of Behavior and Gut Passage for Seed Dispersal Quality: The Case of Black and Gold Howler Monkeys. Biotropica 41(6): 751-758. DOI: https://doi.org/10.1111/j.1744-7429.2009.00538.x [ Links ]

Carvalho, J. E. U. and W. M. Nascimento. 2020. Water absorption and physiological responses of hog plum tree diaspores to storage. Revista Brasileira de Fruticultura 42(3): 1-10. DOI: https://doi.org/10.1590/0100-29452020573 [ Links ]

Castillo, G. and J. Laborde. 2004. La vegetación. In: Guevara, S., J. Laborde and G. Sánchez-Ríos (eds.). Los Tuxtlas, el paisaje de la sierra. Instituto de Ecología, A.C.-Unión Europea. Xalapa, México. Pp. 231-265. [ Links ]

Chapman, C. A. and S. E. Russo. 2006. Primate Seed Dispersal: Linking Behavioral Ecology with Forest Community Structure. In: Campbell, J., A. F. Fuentes, K. C. MacKinnon, M. Panger and S. Bearder (eds.). Primates in Perspective. Oxford University Press. Oxford, USA. Pp. 510-525. [ Links ]

Cristóbal-Azkarate, J. and V. Arroyo-Rodríguez. 2007. Diet and Activity Pattern of Howler Monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of Habitat Fragmentation and Implications for Conservation. American Journal of Primatology 69(9): 1013-1029. DOI: https://doi.org/10.1002/ajp.20420 [ Links ]

Dáttilo, W., J. C. Serio-Silva, C. A. Chapman and V. Rico-Gray. 2014. Highly Nested Diets in Intrapopulation Monkey-Resource Food Webs. American Journal of Primatology 76(7): 670-678. DOI: https://doi.org/10.1002/ajp.22261 [ Links ]

Delgado-Sánchez, P., M. A. Ortega-Amaro, J. F. Jiménez-Bremont and J. Flores. 2011. Are fungi important for breaking seed dormancy in desert species? Experimental evidence in Opuntia streptacantha (Cactaceae). Plant Biology 13(1): 154-159. DOI: https://doi.org/10.1111/j.1438-8677.2010.00333.x [ Links ]

Dennis, A. J. 2007. Frugivores and Frugivory. In: Dennis, A. J., E. W. Schupp, R. J. Green and D. A. Westcott. Seed Dispersal: Theory and its Application in a Changing World. CABI. Wallingford, UK. Pp. 1-3. [ Links ]

Duncan, R. S. and C. A. Chapman . 1999. Seed Dispersal and Potential Forest Succession in Abandoned Agriculture in Tropical Africa. Ecological Applications 9(3): 998-1008. DOI: https://doi.org/10.2307/2641345 [ Links ]

Estrada, A. and R. Coates-Estrada. 1984. Fruit eating and seed dispersal by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. American Journal of Primatology 6(2): 77-91. DOI: https://doi.org/10.1002/ajp.1350060202 [ Links ]

Fadimu, O. Y., O. T. H. Idowu and S. J. Ipinlaye. 2014. Studies on the Dormancy and Germination of Stony Fruits of Hog plum (Spondias mombin) in Response to Different Pre-Soaking Seed Treatments. International Research Journal of Biological Sciences 3(6): 57-62. [ Links ]

Fleming, T. H., R. Breitwisch and G. H. Whitesides. 1987. Patterns of Tropical Vertebrate Frugivore Diversity. Annual Review of Ecology and Systematics 18(1): 91-109. DOI: https://doi.org/10.1146/annurev.es.18.110187.000515 [ Links ]

Garber, P. A., N. Righini and M. M. Kowalewski. 2015. Evidence of Alternative Dietary Syndromes and Nutritional Goals in the Genus Alouatta. In: Kowalewski, M. M., P. A. Garber, L. Cortés-Ortiz, B. Urbani and D. Youlatos (eds.). Howler Monkeys: Behavior, Ecology, and Conservation. Springer. Nueva York, USA. Pp. 85-109. DOI: https://doi.org/10.1007/978-1-4939-1960-4_4 [ Links ]

Gardner, C. J., J. E. Bicknell, W. Baldwin-Cantello, M. J. Struebig and Z. G. Davies. 2019. Quantifying the impacts of defaunation on natural forest regeneration in a global meta-analysis. Nature Communications 10(1): 1-7. DOI: https://doi.org/10.1038/s41467-019-12539-1 [ Links ]

González-Christen, A., C. A. Delfín-Alonso and A. Sosa-Martínez. 2013. Distribución y abundancia de la nutria neotropical (Lontra longicaudis annectens Major, 1897), en el Lago de Catemaco, Veracruz, México. Therya 4(2): 201-2017. DOI: https://doi.org/10.12933/therya-13-125 [ Links ]

González-Di Pierro, A, M., J. Benítez-Malvido and R. Lombera. 2021. Germination success of large-seeded plant species ingested by howler monkeys in tropical rain forest fragments. American Journal of Botany 108(9): 1625-1634. DOI: https://doi.org/10.1002/ajb2.1730 [ Links ]

Hauck-Tiburski, J., A. Rosenthal, R. Deliza, R. L. de Oliveira Godoy and S. Pacheco. 2011. Nutritional properties of yellow mombin (Spondias mombin L.) pulp. Food Research International 44(7): 2326-2331. DOI: https://doi.org/10.1016/j.foodres.2011.03.037 [ Links ]

Herrera, F., J. D. Mitchell, S. K. Pell, M. E. Collinson, D. C. Daly and S. R. Manchester. 2018. Fruit Morphology and Anatomy of the Spondioid Anacardiaceae. The Botanical Review 84(15): 315-393. DOI: https://doi.org/10.1007/s12229-018-9201-1 [ Links ]

Janzen, D. H. 1985. Spondias mombin is Culturally Deprived in Megafauna-Free Forest. Journal of Tropical Ecology 1(2): 135-155. DOI: https://doi.org/10.1017/S0266467400000195 [ Links ]

Jordano, P. 2000. Fruits and Frugivory. In: Fenner, M. (ed.). Seeds: The Ecology of Regeneration in Plant Communities. CABI Publishing. Oxford, UK. Pp. 125-165. DOI: https://doi.org/10.1079/9780851994321.0125 [ Links ]

Lambert, J. E. 1999. Seed handling in Chimpanzees (Pan troglodytes) and Redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. American Journal of Physical Anthropology 109(3): 365-386. DOI: https://doi.org/10.1002/(SICI)1096-8644(199907)109:3<365::AID-AJPA6>3.0.CO;2-Q [ Links ]

Link, A. and A. Di Fiore. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of Tropical Ecology 22(3): 235-246. DOI: https://doi.org/10.1017/S0266467405003081 [ Links ]

Lozano, N. B. 1986. Desarrollo y anatomía del fruto del jobo (Spondias mombin L.). Caldasia 14(68-70): 465-490. [ Links ]

Magalhães de Souza, P. H., A. L. Soares Lima Ragagnin, R. Carvalho Ribeiro, G. Zildo da Silva, D. I. Rocha and D. F. Pereira da Silva. 2020. Dormancy overcoming in seeds of cajá-manga (Spondias dulcis). Comunicata Scientiae 11: 1-6. DOI: https://doi.org/10.14295/cs.v11i0.3341 [ Links ]

Martins, C. C., G. Z. da Silva, L. D. Durigan and R. D. Vieira. 2019. Pregerminative treatments of yellow mombin (Spondias mombin L.) seeds. Ciência Florestal 29(1): 363-370. DOI: https://doi.org/10.5902/1980509821217 [ Links ]

Mitchell, J. D. and D. C. Daly . 2015. A revision of Spondias L. (Anacardiaceae) in the Neotropics. PhytoKeys 55: 1-92. DOI: https://doi.org/10.3897/phytokeys.55.8489 [ Links ]

Morales-Mávil, J. E., M. L. Sánchez-Marín and L. E. Domínguez-Domínguez. 2005. Comparación de la germinación de semillas de Spondias mombin ingeridas por la Iguana verde (Iguana iguana), el Tucán (Ramphastos sulfuratus) y el Mono araña (Ateles geoffroyii). In: Reynoso, V. H. and W. Medina-Mantecón (eds.). VIII Reunión Nacional sobre Iguanas en México. Held from May 19 to 25, 2005, in Lázaro Cárdenas, Michoacán, México. Instituto de Biología de la Universidad Nacional Autónoma de México. Lázaro Cárdenas, México. Pp. 93-99. [ Links ]

Niembro-Rocas, A., M. Vázquez-Torres and O. Sánchez-Sánchez. 2010. Árboles de Veracruz: 100 especies para la reforestación estratégica. Secretaría de Gobierno del Estado de Veracruz. Veracruz, México. 130 pp. [ Links ]

Nogales, M., C. Nieves, J. C. Illera, D. P. Padilla and A. Traveset. 2005. Effect of native and alien vertebrate frugivores on seed viability and germination patterns of Rubia fruticosa (Rubiaceae) in the eastern Canary Islands. Functional Ecology 19(3): 429-436. DOI: https://doi.org/10.1111/j.0269-8463.2005.00975.x [ Links ]

Paulsen, T. R. and G. Högstedt. 2002. Passage through bird guts increases germination rate and seedling growth in Sorbus aucuparia. Functional Ecology 16(5): 608-616. DOI: https://doi.org/10.1046/j.1365-2435.2002.00668.x [ Links ]

Ribeiro, R. C., M. L. N. Figueiredo, A. Picorelli, D. M. T. Oliveira and F. A. O. Silveira. 2016. Does seed coat structure modulate gut-passage effects on seed germination? Examples from Miconieae DC. (Melastomataceae). Seed Science Research 26(2): 139-147. DOI: https://doi.org/10.1017/S0960258516000064 [ Links ]

RStudio Team. 2021. RStudio: Integrated Development Environment for R. RStudio. Public Benefit Corporation. Boston, USA. URL: http://www.rstudio.com/ (consulted May, 2021). [ Links ]

Schneider, C. A., W. S. Rasband and K. W. Eliceiri. 2012. NIH Image to Image: 25 years of image analysis. Nature Methods 9(7): 671-675. DOI: https://doi.org/doi:10.1038/nmeth.2089 [ Links ]

Schupp, E. W. 1993. Quantity, quality and the Effectiveness of Seed Dispersal by Animals. Vegetatio 107: 15-29. [ Links ]

Schupp, E. W., P. Jordano and J. M. Gómez. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188(2): 333-353. DOI: https://doi.org/10.1111/j.1469-8137.2010.03402.x. [ Links ]

Serio-Silva, J. C., V. Rico-Gray, L. T. Hernández-Salazar and R. Espinosa-Gómez. 2002. The role of Ficus (Moraceae) in the diet and nutrition of a troop of Mexican howler monkeys, Alouatta palliata mexicana, released on an island in southern Veracruz, Mexico. Journal of Tropical Ecology 18(6): 913-928. DOI: https://doi.org/10.10soria17/S0266467402002596 [ Links ]

Soriano, A. and J. A. Martínez-Villegas. 2019. Latencia. In: Guevara Fefer, P. (ed.). Un viaje alrededor de la semilla. Universidad Nacional Autónoma de México. Cd. Mx., México. Pp. 103-122. [ Links ]

Soto, M. and L. Gama. 1997. Climas. In: González-Soriano, E., R. Dirzo and R. C. Vogt (eds.). Historia natural de Los Tuxtlas. Universidad Nacional Autónoma de México y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Cd. Mx., México. Pp. 7-23. [ Links ]

Stevenson, P. R. 2011. The Abundance of Large Ateline Monkeys is Positively Associated with the Diversity of Plants Regenerating in the Neotropical Forests. Biotropica 43(4): 512-519. DOI: https://doi.org/10.1111/j.1744-7429.2010.00708.x [ Links ]

Traveset, A., A. W. Robertson and J. Rodríguez-Pérez. 2007. A Review on the Role of Endozoochory in Seed Germination. In: Dennis, A. J., E. W. Schupp, R. A. Green and D. A. Westcott (eds.). Seed dispersal: Theory and its application in a changing world. CAB International. Wallingford, UK. Pp. 78-102. [ Links ]

Vázquez-Torres, M., J. Campos-Jiménez, S. Armenta-Montero and C. I. Carvajal-Hernández. 2010. Árboles de la región de Los Tuxtlas. Secretaría de Educación-Gobierno del Estado de Veracruz. Xalapa, México. 400 pp. [ Links ]

Author contributions

JCSS proposed the study and participated in sample collection; DATA, WFDC, and JCSS designed the investigation, GHRS generated the scanning electron microscope images, DATA and WFDC made the analyses. All authors participated in the generation, revision, discussion and approval of the final manuscript.

Funding

This study was funded to DATA (Grant Number: 753641) by the Consejo Nacional de Ciencia y Tecnología (CONACyT), through the Grupo de Estudios Transdisciplinarios en Primatología (GETP), in Red de Biología y Conservación de Vertebrados of the Instituto de Ecología, A.C. (INECOL).

Received: February 10, 2022; Revised: April 05, 2022; Accepted: June 09, 2022; Published: June 17, 2022

5Autor para la correspondencia: juan.serio@inecol.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License