Abstract
Fruit ingestion by frugivores and the subsequent passage of seeds through their digestive tract can influence seed germination patterns. The removal of germination inhibitors contained in the fruit pulp (deinhibition effect), and/or the abrasion of the seed coat (scarification effect), can modify the probability and speed of seed germination. We followed seven groups of black-and-gold howler monkeys (Alouatta caraya) in northeastern Argentina between November 2012 and January 2013 to study the effect of seed passage through the howler monkeys’ gut on seed germination. For three native and one exotic species, we compared the proportion of germination and germination times among seeds in three different treatments: gut-passed seeds (GP), manually extracted seeds from fruits (ME), and seeds in intact fruits (IF). Paired comparisons between treatments allowed us to assess the overall effect of seed passage (total effect without distinguishing individual effects, GP vs. IF), deinhibition effect (ME vs. IF), and scarification effect (GP vs. ME). Our results suggest that passage through the howler monkeys’ gut enhances seed germination by an increase in the proportion of germinated seeds and/or by a reduction in germination times. We found that deinhibition enhanced germination in three out of the four studied species, while scarification enhanced germination in one and decreased germination in another species. Our work highlights that gut passage may affect seed germination by different mechanisms, and all of these mechanisms should be considered in germination studies. It also emphasizes the importance of A. caraya as a seed disperser in northeastern Argentina, showing the high quality of the treatment provided to seeds.
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References
Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Information theory: proceedings of the second international symposium. Akademiai Kiado, Budapest, pp 267–281
Andresen E (2002) Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34:261–272. https://doi.org/10.1111/j.1744-7429.2002.tb00537.x
Arroyo-Rodríguez V, Andresen E, Bravo SP, Stevenson PR (2015) Seed dispersal by howler monkeys: current knowledge, conservation implications, and future directions. In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer, New York, pp 111–139
Barnea A, Yom-Tov Y, Friedman J (1990) Differential germination of two closely related species of Solanum in response to bird ingestion. Oikos 57:222–228. https://doi.org/10.2307/3565943
Bates D, Maechler M, Bolker B, Walker S (2015) fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bosu PP, Apetorgbor MM, Refera A (2009) Ecology and management of tropical Africa’s forest invaders. In: Kohli RK, Shibu J, Singh HP, Batish DR (eds) Invasive plants and forest ecosystems. Taylor & Francis, Florida, pp 355–376
Bravo SP, Zunino GE (2000) Germination of seeds from three species dispersed by black howler monkeys (Alouatta caraya). Folia Primatol 71:342–345. https://doi.org/10.1159/000021757
Bravo SP, Kowalewski MM, Zunino GE (1995) Dispersión y germinación de semillas de Ficus monckii por el mono aullador negro (Alouatta caraya). Boletín Primatológico Latinoamericano 5:25–27
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9(2):378–400
Delgado A (2005) Estudio de patrones de uso de sitios de defecación y su posible relación con infecciones endoparasitarias en dos grupos de monos aulladores negros y dorados (Alouatta caraya) en el nordeste Argentino. Bachelors dissertation, Universidad Nacional del Nordeste
Estrada A, Coates-Estrada R (1984) Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Mexico. Am J Primatol 6:77–91. https://doi.org/10.1002/ajp.1350060202
Evenari M (1949) Germination inhibitors. Bot Rev 15:153–194. https://doi.org/10.1007/BF02861721
Fernández VA (2014) Ecología nutricional del mono aullador negro y dorado (Alouatta caraya) en el límite sur de su distribución. Doctoral dissertation, Universidad de Buenos Aires
Fuzessy LF, Cornelissen TG, Janson C, Silveira FAO (2016) How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos 125:1069–1080. https://doi.org/10.1111/oik.02986
Ghersa CM, De la Fuente E, Suarez S, Leon RJC (2002) Woody species invasion in the rolling pampa grasslands, Argentina. Agric Ecosyst Environ 88:271–278. https://doi.org/10.1016/S0167-8809(01)00209-2
Giannoni S, Mera Sierra R, Brengio S, Jimenez Baigorria L (2003) Guía para el uso de animales en investigaciones de campo y en cautiverio. Comisión de Ética de la SAREM. https://www.sarem.org.ar/wp-content/uploads/2014/04/Etica-SAREM.pdf. Accessed Jan 2017
Harper JL (1977) Population biology of plants. Academic Press, New York
Harrison XA (2015) A comparison of observation-level randomeffect and beta-binomial models for modelling overdispersion in Binomial data in ecology & evolution. PeerJ 3:e1114. https://doi.org/10.7717/peerj.1114
Haurez B, Tagg N, Petre C, Brostaux Y, Boubady A, Doucet J (2017) Seed dispersal effectiveness of the western lowland gorilla (Gorilla gorilla gorilla) in Gabon. Afr J Ecol 56:185–193. https://doi.org/10.1111/aje.12449
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228. https://doi.org/10.1146/annurev.es.13.110182.001221
Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. Commonwealth Agricultural Bureaux International, Wallingford, pp 125–166
Julliot C (1996) Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. Int J Primatol 17:239–258. https://doi.org/10.1007/BF02735451
Kowalewski MM, Zunino GE (2004) Birth seasonality in Alouatta caraya in Northern Argentina. Int J Primatol 25:383–400. https://doi.org/10.1023/B:IJOP.0000019158.45628.4a
Kyereh B, Agyeman VK, Abebrese IK (2014) Ecological characteristics that enhance Broussonetia papyrifera’s invasion in a semideciduous forest in Ghana. Journal of Ecosystems 6:1–6. https://doi.org/10.1155/2014/270196
Lambert JE (2001) Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. Int J Primatol 22:189–201. https://doi.org/10.1023/A:1005667313906
Malik RN, Husain SZ (2007) Broussonetia papyrifera (L.) L'her ex. Vent.: an environmental constraint on the Himalayan Foothills vegetation. Pakistan J Bot 39(4):1045–1053
Malo J, Suárez F (1995) Establishment of pasture species on cattle dung: the role of endozoochorous seeds. J Veg Sci 6:169–174. https://doi.org/10.2307/3236211
McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Texas, pp 159–191
Otani T (2004) Effects of macaque ingestion on seed destruction and germination of a fleshy-fruited tree, Eurya emarginata. Ecol Res 15:495–501. https://doi.org/10.1111/j.1440-1703.2004.00663.x
Petre C, Tagg N, Beudels-Jamar RC, Haurez B, Doucet J (2015) Western lowland gorilla seed dispersal: are seeds adapted to long gut retention times? Acta Oecol 67:59–65. https://doi.org/10.1016/j.actao.2015.06.003
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131, https://CRAN.R-project.org/package=nlme. Accessed 28 May 2019
Poulsen JR, Clark CJ, Smith TB (2001) Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. J Trop Ecol 17:787–808. https://doi.org/10.1017/S0266467401001602
Ranal MA, Santana DG (2006) How and why to measure the germination process? Rev Bras Bot 29:1–11. https://doi.org/10.1590/S0100-84042006000100002
Raño M, Kowalewski MM, Cerezo AM, Garber PA (2016) Determinants of daily path length in black and gold howler monkeys (Alouatta caraya) in northeastern Argentina. Am J Primatol 78(8):825–837. https://doi.org/10.1002/ajp.22548
Robertson AW, Trass A, Ladley JJ, Kelly D (2006) Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Funct Ecol 20:58–66. https://doi.org/10.1111/j.1365-2435.2005.01057.x
Rumiz DI (1990) Alouatta caraya: population density and demography in northern Argentina. Am J Primatol 21:279–294. https://doi.org/10.1002/ajp.1350210404
Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368. https://doi.org/10.1111/j.1365-2435.2005.00973.x
Sato H (2012) Frugivory and seed dispersal by brown lemurs in a Malagasy tropical dry forest. Biotropica 44:479–488. https://doi.org/10.1111/j.1744-7429.2011.00838.x
Schaumann F, Heinken T (2002) Endozoochorous seed dispersal by martens (Martes foina, M. martes) in two woodland habitats. Flora 197:370–378. https://doi.org/10.1078/0367-2530-00053
Schupp EW, Jordano P, Gómez J (2010) Seed dispersal effectiveness revisited: a conceptual review. N Phytol 188:333–353. https://doi.org/10.1111/j.1469-8137.2010.03402.x
Stansbury CD, Vivian-Smith G (2003) Interactions between frugivorous birds and weeds in Queensland as determined from a survey of birders. Plant Prot Q 18:157–165
Stevenson PR, Castellanos MC, Pizarro JC, Garavito M (2002) Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. Int J Primatol 23:1187–1204. https://doi.org/10.1023/A:1021118618936
Tang Z, Mukherjee A, Sheng L, Cao M, Liang B, Corlett RT, Zhang S (2007) Effect of ingestion by two frugivorous bat species on the seed germination of Ficus racemosa and F. hispida (Moraceae). J Trop Ecol 23:125–127. https://doi.org/10.1017/S0266467406003737
Torresín JA, Zamboni LP, Sione WF, Rodríguez E, Aceñolaza PG (2013) Modelado de la distribución espacial de árboles exóticos invasores (AEI) en el Parque Nacional Pre-Delta (Entre Ríos, Argentina). Multequina 22:3–13. https://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S1852-73292013000100001. Accessed 18 Dec 2019
Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect Plant Ecol 1:151–190. https://doi.org/10.1078/1433-8319-00057
Traveset A, Verdu M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. Commonwealth Agricultural Bureaux International, Wallingford, pp 339–350
Traveset A, Bermejo T, Willson M (2001) Effect of manure composition on seedling emergence and growth of two common shrub species of Southeast Alaska. Plant Ecol 155:29–34. https://doi.org/10.1023/A:1013282313035
Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory in seed germination. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. Commonwealth Agricultural Bureaux International, Wallingford, pp 78–103
Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394. https://doi.org/10.1890/04-1647
Whistler WA, Elevitch CR (2006) Broussonetia papyrifera (paper mulberry). In: Elevitch CR (ed) Species profiles for Pacific Island Agroforestry. Permanent Agriculture Resourses, Hawaii. https://agroforestry.org/images/pdfs/Broussonetia-papermulb.pdf. Accessed 28 May 2019
Yagihashi T, Hayashida M, Miyamoto T (1998) Effects of bird ingestion on seed germination of Sorbus commixta. Oecologia 114:209–212. https://doi.org/10.1007/s004420050438
Yumoto T, Noma N, Maruhashi T (1998) Cheek-pouch dispersal of seeds by japanese monkeys (Macaca fuscata yakui) on Yakushima island, Japan. Primates 39:325–338. https://doi.org/10.1007/BF02573081
Zunino GE (1989) Habitat, dieta y actividad del mono aullador negro (Alouatta caraya) en el noreste de Argentina. Boletín Primatológico Latinoamericano 1:74–97
Zunino GE (1996) Análisis de nacimientos en Alouatta caraya (Primates, Cebidae), en el noreste de la Argentina. Revista del Museo Argentino de Ciencias Naturales nueva serie 133:1–10
Zunino GE, Kowalewski MM, Oklander LI, Gonzáles V (2007) Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina. Am J Primatol 69:966–975. https://doi.org/10.1002/ajp.20389
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
Our research was supported by the National Council of Scientific and Technical Research (CONICET), Argentina (PIP IU 0355). We gratefully acknowledge the help of our field assistants Fernando Mingrone and Ruby Valls. We thank Corrientes Biological Station for allowing us to use their facilities for this study. We thank Sahana Kuthyar and Alberto Fameli for proofreading the article. MK thanks Bruno K for helping him to disperse seeds. The study complies with the current laws of Argentina and followed the Argentine Society for Mammalian Studies guidelines.
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This study was funded by the National Council of Scientific and Technical Research (CONICET) (PIP IU 0355).
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Fergnani, D.M., Kowalewski, M.M. & Fernández, V.A. Germination of native and exotic seeds dispersed by wild black-and-gold howler monkeys (Alouatta caraya): assessing deinhibition and scarification effects. Primates 61, 519–527 (2020). https://doi.org/10.1007/s10329-020-00791-9
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DOI: https://doi.org/10.1007/s10329-020-00791-9