Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T09:19:51.418Z Has data issue: false hasContentIssue false

Filling gaps in the seed dispersal effectiveness model for Prosopis flexuosa: quality of seed treatment in the digestive tract of native animals

Published online by Cambridge University Press:  28 October 2020

Claudia M. Campos*
Affiliation:
IADIZA, Instituto Argentino de Investigaciones de las Zonas Áridas, Universidad Nacional de Cuyo, Gobierno de Mendoza, CONICET, Mendoza, Argentina
Liliana Ramos
Affiliation:
IADIZA, Instituto Argentino de Investigaciones de las Zonas Áridas, Universidad Nacional de Cuyo, Gobierno de Mendoza, CONICET, Mendoza, Argentina
Noelia Manrique
Affiliation:
CIGEOBIO, Centro de Investigaciones de la Geósfera y Biósfera, Universidad Nacional de San Juan, CONICET, San Juan, Argentina
Mónica I. Cona
Affiliation:
IADIZA, Instituto Argentino de Investigaciones de las Zonas Áridas, Universidad Nacional de Cuyo, Gobierno de Mendoza, CONICET, Mendoza, Argentina
Carmen Sartor
Affiliation:
Cátedra de Ecología, Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Mendoza, Argentina
Claudia de los Ríos
Affiliation:
Departamento de Biología, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de San Juan, San Juan, Argentina
Flavio M. Cappa
Affiliation:
CIGEOBIO, Centro de Investigaciones de la Geósfera y Biósfera, Universidad Nacional de San Juan, CONICET, San Juan, Argentina
*
Author for Correspondence: Claudia M. Campos, E-mail: ccampos@mendoza-conicet.gob.ar

Abstract

For endozoochorous species, the quality component of seed dispersal effectiveness depends in part on the treatment seeds receive in the animal's gut. Covering a variety of taxa, diet, digestion system and body size of Prosopis flexuosa seed dispersers, we analysed differences among species in (1) mean retention time of ingested seeds, (2) recovery of viable seeds, (3) seed germination in comparison with seeds collected from trees and (4) germination of seeds after two different periods of retention in the gut. Feeding experiments were conducted with captive individuals of Dolichotis patagonum, Lycalopex gymnocercus, Rhea americana, Chelonoidis chilensis and Lama guanicoe. On the first day, we provided them with fruits containing controlled amounts of seed, and on the subsequent days, we collected faeces in order to recover seeds. We performed germination and viability tests on seeds coming from faeces and collected from trees. The results showed differences among species in the mean retention time of seeds. Chelonoidis chilensis had the longest mean retention time, but its effect on seed recovery and germination was similar to that of the other species, except for L. guanicoe, which showed the lowest seed recovery. When scarification and promotion of seed germination were considered, herbivorous mammals and tortoises (L. guanicoe, D. patagonum and C. chilensis) were the ones increasing germinability, whereas R. americana and L. gymnocercus did not significantly increase final seed germination percentage, which was similar to that for seeds collected from trees. P. flexuosa seeds receive a variety of treatments from endozoochorous dispersers, which might result in an overall fitness benefit for a plant living in unpredictable environments.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Álvarez, JA and Villagra, PE (2009) Prosopis flexuosa DC. (Fabaceae, Mimosoideae). Kurtziana 35, 4761.Google Scholar
Bessega, C, Pometti, C, Campos, C, Saidman, BO and Vilardi, JC (2017) Implications of mating system and pollen dispersal indices for management and conservation of the semi-arid species Prosopis flexuosa (Leguminosae). Forest Ecology and Management 400, 218227.CrossRefGoogle Scholar
Bjorndal, KA (1997) Fermentation in reptiles and amphibians, pp. 199230 in Mackie, RO and White, BA (Eds) Gastrointestinal microbiology. Boston, MA, Chapman and Hall Microbiology Series, Springer.CrossRefGoogle Scholar
Burkart, A (1976) A monograph of the genus Prosopis (Leguminosae subfam. Mimosoidae). Journal of the Arnold Arboretum 57, 219525.Google Scholar
Bustamante, RO, Simonetti, JA and Mella, JE (1992) Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecologica 13, 203208.Google Scholar
Cain, ML, Milligan, BG and Strand, AE (2000) Long-distance seed dispersal in plant populations. American Journal of Botany 87, 12171227.CrossRefGoogle ScholarPubMed
Campos, C and Ojeda, R (1997) Dispersal and germination of Prosopis flexuosa (Fabaceae) seeds by desert mammals in Argentina. Journal of Arid Environments 35, 707714.CrossRefGoogle Scholar
Campos, CM and Velez, S (2015) Almacenadores y frugívoros oportunistas: el papel de los mamíferos en la dispersión del algarrobo (Prosopis flexuosa DC) en el desierto del Monte, Argentina. Revista Ecosistemas 24, 2834.CrossRefGoogle Scholar
Campos, C, Giannoni, S, Taraborelli, P and Borghi, C (2007) Removal of mesquite seeds by small rodents in the Monte desert, Argentina. Journal of Arid Environments 69, 228236.CrossRefGoogle Scholar
Campos, CM, Peco, B, Campos, VE, Malo, JE, Giannoni, SM and Suárez, F (2008) Endozoochory by native and exotic herbivores in dry areas: consequences for germination and survival of Prosopis seeds. Seed Science Research 18, 91100.CrossRefGoogle Scholar
Campos, CM, Campos, V, Mongeaud, A, Borghi, C, de los Ríos, C and Giannoni, S (2011) Relationships between Prosopis flexuosa (Fabaceae) and cattle in the Monte desert: seeds, seedlings and saplings on cattle-use site classes. Revista Chilena de Historia Natural 84, 289299.CrossRefGoogle Scholar
Campos, CM, Campos, VE, Miguel, F and Cona, MI (2016) Management of protected areas and its effect on an ecosystem function: removal of Prosopis flexuosa seeds by mammals in Argentinian drylands. PLoS ONE 11, 9.Google Scholar
Campos, CM, Campos, VE, Giannoni, SM, Rodríguez, D, Albanese, S and Cona, MI (2017) Role of small rodents in the seed dispersal process: Microcavia australis consuming Prosopis flexuosa fruits. Austral Ecology 42, 113119.CrossRefGoogle Scholar
Campos, CM, Velez, S, Miguel, MF, Papú, S and Cona, MI (2018) Studying the quantity component of seed dispersal effectiveness from exclosure treatments and camera trapping. Ecology and Evolution 8, 54705479.CrossRefGoogle ScholarPubMed
Castle, EJ (1956) The rate of passage of foodstuffs through the alimentary tract of the goat. 1. Studies on adult animals fed on hay and concentrates. British Journal of Nutrition 10, 1523.CrossRefGoogle ScholarPubMed
Castro, SA, Silva, SI, Meserve, PL, Gutiérrez, JL, Contreras, LC and Jaksic, FB (1994) Frugivoría y dispersión de semillas de pimiento (Schinus molle) por el zorro culpeo (Pseudalopex culpaeus) en el Parque Nacional Fray Jorge (IV Región, Chile). Revista Chilena de Historia Natural 67, 169176.Google Scholar
Catalán, LA and Balzarini, M (1992) Improved laboratory germination conditions for several arboreal Prosopis species: P. chilensis, P. flexuosa, P. nigra, P. alba, P. caldenia and P. affinis. Seed Science and Technology 20, 293298.Google Scholar
Catalán, LA and Macchiavelli, RE (1991) Improving germination in Prosopis flexuosa D.C. and P. alba Griseb. with hot water treatments and scarification. Seed Science and Technology 19, 253262.Google Scholar
Chambers, J and MacMahon, J (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25, 263292.CrossRefGoogle Scholar
Clemens, ET and Stevens, CE (1980) A comparison of gastrointestinal transit time in ten species of mammal. Journal of Agricultural Science, Cambridge 94, 735737.CrossRefGoogle Scholar
Cony, M (1993) Programa de Conservación y Mejoramiento de Especies del Género Prosopis en la Provincia Fitogeográfica del Monte, Argentina. Convenio CIID-IADIZA, pp. 3772 in IADIZA (Ed.) Contribuciones Mendocinas a la Quinta Reunión de Regional para América Latina y el Caribe de la Red de Forestación del CIID. Conservación y Mejoramiento de Especies del Género Prosopis. Mendoza, IADIZA-CRICYT-CIID.Google Scholar
Cony, MA and Trione, SO (1996) Germination with respect to temperature of two Argentinian Prosopis species. Journal of Arid Environments 33, 225236.CrossRefGoogle Scholar
Dellafiore, CM (2018) ¿Afecta el zorro (Lycalopex gymnocercus) la germinación de piracanta (Pyracantha atalantoides) Rosaceae? Mastozoología Neotropical 25, 5358.CrossRefGoogle Scholar
Esteban, LR and Thompson, JR (1988) The digestive system of New World camelids - common digestive diseases of llamas. Iowa State University Veterinarian 50, 117121.Google Scholar
Fedriani, JM and Delibes, M (2009) Functional diversity in fruit-frugivore interactions: a field experiment with Mediterranean mammals. Ecography 32, 983992.CrossRefGoogle Scholar
Frei, S, Ortmann, S, Reutlinger, C, Kreuzer, M, Hatt, JM and Clauss, M (2015) Comparative digesta retention patterns in ratites. The Auk 132, 119131.CrossRefGoogle Scholar
Gardener, CJ, McIvor, JG and Jansen, A (1993) Passage of legume and grass seeds through the digestive tract of cattle and their survival in faeces. Journal of Applied Ecology 30, 6374.CrossRefGoogle Scholar
Giannoni, SM, Campos, VE, Andino, N, Ramos-Castilla, M, Orofino, A, Borghi, CE, de los Ríos, C and Campos, CM (2013) Hoarding patterns of sigmodontine rodent species in the Central Monte desert (Argentina). Austral Ecology 38, 485492.CrossRefGoogle Scholar
González-Varo, JP, López-Bao, JV and Guitián, J (2013) Functional diversity among seed dispersal kernels generated by carnivorous mammals. Journal of Animal Ecology 82, 562571.CrossRefGoogle ScholarPubMed
Howe, HF and Smallwood, J (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201228.Google Scholar
Hume, ID (1989) Optimal digestive strategies in mammalian herbivores. Physiological Zoology 62, 11451163.CrossRefGoogle Scholar
Hume, ID and Warner, ACI (1980) Evolution of microbial digestion in mammals, pp. 665684 in Ruckebusch, Y and Thivend, P (Eds) Digestive physiology and metabolism in ruminants. Dordrecht, Netherlands, Springer.CrossRefGoogle Scholar
Illius, AW and Gordon, IJ (1993) Diet selection in mammalian herbivores: constraints and tactics, pp. 157181 in Highes, RN (Ed.) An interdisciplinary approach to foraging behaviour. Boston, Blackwell Scientific Publishers.Google Scholar
Janzen, DH (1970) Herbivores and the number of tree species in tropical forests. American Naturalist 104, 501528.CrossRefGoogle Scholar
Janzen, DH, Demment, MW and Robertson, JB (1985) How fast and why do germinating Guanacaste seeds (Enterolobium cyclocarpum) die inside cows and horses? Biotropica 17, 322325.CrossRefGoogle Scholar
Jordano, P (2000) Fruits and frugivory, pp. 125166 in Fenner, M (Ed.) Seeds: the ecology of regeneration in plant communities. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Jordano, P, Forget, PM, Lambert, JE, Böhning-Gaese, K, Traveset, A and Wright, SJ (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7, 321323.CrossRefGoogle ScholarPubMed
Kufner, MB and Durañona, G (1991) Consumo y eficiencia digestiva del mara, Dolichotis patagonum (Rodentia: Caviidae). Ecologla Austral 1, 5055.Google Scholar
León-Lobos, PM and Kalin-Arroyo, MT (1994) Germinación de semillaje Lifhrea caustica (Mol.) H. et A. (Anacardiacea) dispersadas por Pseudalopex sp. (Canidae) en el bosque esclerófilo de Chile central. Revista Chilena de Historia Natural 67, 5964.Google Scholar
Maldonado, DE, Loayza, AP, Garcia, E and Pacheco, LF (2018) Qualitative aspects of the effectiveness of Culpeo foxes (Lycalopex culpaeus) as dispersers of Prosopis alba (Fabaceae) in a Bolivian dry valley. Acta Oecologica 87, 2933.CrossRefGoogle Scholar
Miguel, F, Cona, MI and Campos, CM (2017) Seed removal by terrestrial mammals in Argentinian drylands under different land management practices. Seed Science Research 27, 174182.CrossRefGoogle Scholar
Miguel, MF, Tabeni, S, Cona, MI and Campos, CM (2018a) Secondary seed dispersal by mammals between protected and grazed semiarid woodland. Forest Ecology and Management 422, 4148.CrossRefGoogle Scholar
Miguel, MF, Jordano, P, Tabeni, S and Campos, CM (2018b) Context-dependency and anthropogenic effects on individual plant-frugivore networks. Oikos 127, 10451059.CrossRefGoogle Scholar
Nathan, R and Muller-Landau, HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15, 278285.CrossRefGoogle ScholarPubMed
Ortega-Baes, P, de Viana, M and Saravia, M (2001) The fate of Prosopis ferox seeds from unremoved pods at National Park Los Cardones. Journal of Arid Environments 48, 185190.CrossRefGoogle Scholar
Ortega-Baes, P, de Viana, M and Suhring, S (2002) Germination in Prosopis ferox: effects of mechanical, chemical and biological scarificators. Journal of Arid Environments 50, 185189.CrossRefGoogle Scholar
Peinetti, R, Pereyra, M, Kin, A and Sosa, A (1993) Effects of cattle ingestion on viability and germination rate of caldén (Prosopis caldenia) seeds. Journal of Range Management 46, 483486.CrossRefGoogle Scholar
Peláez, DV, Bóo, RM and Elia, OR (1992) Emergence and seedling survival of caldén in the semiarid region of Argentina. Journal of Range Management 45, 564566.CrossRefGoogle Scholar
Picard, M, Papaix, J, Gosselin, F, Picot, D, Bideau, E and Baltzinger, C (2015) Temporal dynamics of seed excretion by wild ungulates: implications for plant dispersal. Ecology and Evolution 5, 23212632.CrossRefGoogle ScholarPubMed
Pili-Sevilla, E (1987) Germination and tetrazolium testing. Seed Science and Technology 15, 691698.Google Scholar
Pratolongo, P, Quintana, R, Malvárez, I and Cagnoni, M (2003) Comparative analysis of variables associated with germination and seedling establishment for Prosopis nigra (Griseb.) Hieron and Acacia caven (Mol.) Mol. Forest Ecology and Management 179, 1525.CrossRefGoogle Scholar
Razanamandranto, S, Tigabu, M, Neya, S and Odén, PC (2004) Effects of gut treatment on recovery and germinability of bovine and ovine ingested seeds of four woody species from the Sudanian savanna in West Africa. Flora 199, 389397.CrossRefGoogle Scholar
Renison, D, Valladares, G and Martella, MB (2010) The effect of passage through the gut of the Greater Rhea (Rhea americana) on germination of tree seeds: implications for forest restoration. Emu 110, 125131.CrossRefGoogle Scholar
Sakaguchi, E, Nippashi, K and Endoh, G (1992) Digesta retention and fibre digestion in maras (Dolichotis patagonum) and guinea-pigs. Comparative Biochemistry and Physiology 101, 867870.Google ScholarPubMed
Samuels, IA and Levey, DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19, 365368.CrossRefGoogle Scholar
Sauer, DB and Burroughs, R (1986) Disinfection of seed surfaces with sodium hypochlorite. Phytopathology 76, 745749.CrossRefGoogle Scholar
Schupp, EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108, 1529.Google Scholar
Schupp, EW, Jordano, P and Gómez, JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333353.CrossRefGoogle ScholarPubMed
Schupp, EW, Jordano, P and Gómez, JM (2017) A general framework for effectiveness concepts in mutualisms. Ecological Letters 20, 577590.CrossRefGoogle ScholarPubMed
Sikes, R, Gannon, W and The Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235253.CrossRefGoogle Scholar
Silva, SI, Jacksic, FM and Bozinovic, F (2005) Nutritional ecology and digestive response to dietary shift in the large South American fox, Pseudalopex culpaeus. Revista Chilena de Historia Natural 78, 239246.CrossRefGoogle Scholar
Stevens, CE and Hume, ID (1995) Comparative physiology of the vertebrate digestive system. New York, Cambridge University Press.Google Scholar
Stevens, CE and Hume, ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews 78, 393427.CrossRefGoogle ScholarPubMed
Tabeni, S, Miguel, MF, Campos, CM and Cona, M (2017) Small mammal abundance and seed predation across boundaries in a restored-grazed woodland interface. Restoration Ecology 26, 787795.CrossRefGoogle Scholar
Team, RC (2016) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Torres, D, Castaño, JH and Carranza-Quiceno, JA (2020) Global patterns in seed germination after ingestion by mammals. Mammal Reviews. doi: 10.1111/mam.12195.CrossRefGoogle Scholar
Traveset, A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1, 151190.CrossRefGoogle Scholar
Traveset, A and Verdú, M (2002) A meta-analysis of the effect of gut treatment on seed germination, pp. 339350 in Levey, DJ; Silva, WR and Galetti, M (Eds) Seed dispersal and frugivory: ecology, evolution and conservation. Wallingford, CABI Publishing.Google Scholar
Traveset, A, Robertson, AW and Rodríguez-Pérez, J (2007) A review on the role of endozoochory in seed germination, pp. 78103 in Dennis, A; Green, R; Schupp, E and Westcott, D (Eds) Seed dispersal: theory and its application in a changing world. Norfolk, UK, CABI Publishing.CrossRefGoogle Scholar
van der Pijl, L (1982) Principles of dispersal in higher plants (3rd edn). Berlin, Springer-Verlag.CrossRefGoogle Scholar
Varela, RO and Bucher, EH (2002) Seed dispersal by Chelonoidis chilensis in the Chaco Dry woodland of Argentina. Journal of Herpetology 36, 137140.CrossRefGoogle Scholar
Varela, O and Bucher, EH (2006) Passage time, viability, and germination of seeds ingested by foxes. Journal of Arid Environments 67, 566578.CrossRefGoogle Scholar
Velez, S, Chacoff, NP and Campos, CM (2018) Pre-dispersal seed loss in two Proposis species (Fabacea: Mimosoidea) from the Monte Desert, Argentina. Ecología Austral 28, 361373.CrossRefGoogle Scholar
Warner, ACI (1981) The mean retention times of digesta markers in the gut of the tammar, Macropus eugenii. Australian Journal of Zoology 29, 759771.CrossRefGoogle Scholar
Supplementary material: File

Campos et al. supplementary material

Campos et al. supplementary material

Download Campos et al. supplementary material(File)
File 14.9 KB