Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T17:09:13.327Z Has data issue: false hasContentIssue false

Interactions between ants and non-myrmecochorous diaspores in a West African montane landscape

Published online by Cambridge University Press:  28 April 2021

Jennifer A. Agaldo*
Affiliation:
School of Biological Sciences, University of Canterbury, 20 Kirkwood Avenue, Upper Riccarton, Christchurch8041, New Zealand
Alexander V. Christianini
Affiliation:
Universidade Federal de Sao Carlos: Sorocaba, Washington Luis Highway 235km-SP-310, Brazil
Hazel M. Chapman
Affiliation:
School of Biological Sciences, University of Canterbury, 20 Kirkwood Avenue, Upper Riccarton, Christchurch8041, New Zealand
*
Author for correspondence:*Jennifer A. Agaldo, Email: arubemi@yahoo.com

Abstract

Myrmecochory, the dispersal of seeds with lipid-rich appendages by ants, is a significant ant–plant interaction. Less well understood is the potential for ant dispersal of non-myrmecochorous seeds. Here we investigate ant–diaspore interactions in a West African montane habitat. We combine observation with depot experiments to determine ant species that move diaspores and distance moved across a forest-edge-grassland gradient. We recorded seed cleaning by ants using a bird/mammal dispersed Paullinia pinnata to determine whether seed cleaning improved plant fitness. We found that two out of a total of 17 ant species (Pheidole sp. 1 and Myrmicaria opaciventris) interacted with 10 species of non-myrmecochorous diaspores across nine plant families. Diaspores were from large canopy trees, understorey trees and vines. Both ant species interacted with small (≤0.24 g) and large (≥0.24 g) diaspores. Ants individually moved small diaspores up to 1.2 m and worked together to clean larger ones. Our experiments with P. pinnata showed that ants removed the pulp of 70% of fruit over 5 days. Cleaned seeds germinated significantly faster and produced seedlings with significantly longer shoot length and higher fresh weight than seedlings from intact seeds. Together our results suggest that ant dispersal may be less significant than seed cleaning in Afromontane forests. However, given the decline in vertebrate frugivores across Africa, a small dispersal advantage may become increasingly important to plant fitness.

Type
Research Article
Copyright
© The Author(s), 2021. 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

Abiem, I, Arellano, G, Kenfack, D and Chapman, H (2020) Afromontane forest diversity and the role of grassland-forest transition in tree species distribution. Diversity 12, 30.CrossRefGoogle Scholar
Agaldo, JA (2017) The role of ants in seed dispersal and regeneration in a degraded West African montane forest-grassland landscape, Ngel Nyaki Forest Reserve, Nigeria Thesis. University of Canterbury.Google Scholar
Agosti, D, Majer, JD, Alonso, LE and Schultz, TR (2000) Standard methods for measuring and monitoring biodiversity. Smithsonian Institution, Washington DC, (9), 280.Google Scholar
Andersen, AN (1988) Dispersal distance as a benefit of myrmecochory. Oecologia 75, 507511.CrossRefGoogle ScholarPubMed
Andersen, AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. Journal of Biogeography 22, 1529.CrossRefGoogle Scholar
Barnes, AD and Chapman, HM (2014) Dispersal traits determine passive restoration trajectory of a Nigerian montane forest. Acta Oecologica 56, 3240.CrossRefGoogle Scholar
Beck, J and Chapman, H (2008) A population estimate of the endangered chimpanzee Pan troglodytes vellerosus in a Nigerian montane forest: implications for conservation. Oryx 42, 448451.CrossRefGoogle Scholar
Bernstein, RA (1975) Foraging strategies of ants in response to variable food density. Ecology 56, 213219.CrossRefGoogle Scholar
Bolton, B (1994) Identification Guide to the Ant Genera of the World. Cambridge, MA: Harvard University Press.Google Scholar
Bowers, MA and Dooley, JL (1993) Predation hazard and seed removal by small mammals: microhabitat versus patch scale effects. Oecologia 94, 247254.CrossRefGoogle ScholarPubMed
Bruhl, CA, Mohamed, M and Linsenmair, KE (1999) Altitudinal distribution of leaf litter ants along a transect in primary forests on Mount Kinabalu, Sabah, Malaysia. Journal of Tropical Ecology 15, 265277.CrossRefGoogle Scholar
Cain, ML, Milligan, BG and Strand, AE (2000) Long-distance seed dispersal in plant populations. American Journal of Botany 87, 12171227.CrossRefGoogle ScholarPubMed
Camargo, PH, Martins, MM, Feitosa, RM and Christianini, AV (2016) Bird and ant synergy increases the seed dispersal effectiveness of an ornithochoric shrub. Oecologia 181, 507518.CrossRefGoogle ScholarPubMed
Camargo, PH, Rodrigues, SB, Piratelli, AJ, Oliveira, PS and Christianini, AV (2019) Interhabitat variation in diplochory: seed dispersal effectiveness by birds and ants differs between tropical forest and savanna. Perspectives in Plant Ecology, Evolution and Systematics 38, 4857.CrossRefGoogle Scholar
Chapman, H (2008) The Nigerian Montane Forest Project. Tropinet 19, 79.Google Scholar
Chapman, H, Cordeiro, NJ, Dutton, P, Wenny, D, Kitamura, S, Kaplin, B and Lawes, MJ (2016) Seed-dispersal ecology of tropical montane forests. Journal of Tropical Ecology 32, 437454.CrossRefGoogle Scholar
Chapman, JD, Chapman, JD and Chapman, H (2001) The forest flora of Taraba and Adamawa States, Nigeria: an ecological account and plant species checklist. Department of Plant and Microbial Sciences, University of Canterbury.Google Scholar
Christian, CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413, 635639.CrossRefGoogle ScholarPubMed
Christianini, AV and Oliveira, PS (2010) Birds and ants provide complementary seed dispersal in a neotropical savanna. Journal of Ecology 98, 573582.CrossRefGoogle Scholar
Christianini, AV and Oliveira, PS (2013) Edge effects decrease ant-derived benefits to seedlings in a neotropical savanna. Arthropod–Plant Interactions 7, 191199.CrossRefGoogle Scholar
Christianini, AV, Mayhé-Nunes, AJ and Oliveira, PS (2007) The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna. Journal of Tropical Ecology 23, 343351.CrossRefGoogle Scholar
Christianini, AV, Mayhé-Nunes, AJ and Oliveira, PS (2012) Exploitation of fallen diaspores by ants: are there ant–plant partner choices? Biotropica 44, 360367.CrossRefGoogle Scholar
Connell, JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Dynamics of Populations 298, 312.Google Scholar
Cordeiro, NJ and Howe, HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proceedings of the National Academy of Sciences USA 100, 1405214056.CrossRefGoogle Scholar
Crawley, MJ (2002) Statistical Computing: An Introduction to Data Analysis using S-Plus (No. 001.6424 C73).Google Scholar
Dunn, RR, Agosti, D, Andersen, AN, Arnan, X, Bruhl, CA, Cerdá, X ... Sanders, NJ (2009) Climatic drivers of hemispheric asymmetry in global patterns of ant species richness. Ecology letters 12, 324333.CrossRefGoogle ScholarPubMed
Farji‐Brener, AG and Werenkraut, V (2017) The effects of ant nests on soil fertility and plant performance: a meta‐analysis. Journal of Animal Ecology 86, 866877.CrossRefGoogle ScholarPubMed
Gallegos, SC, Hensen, I and Schleuning, M (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. Journal of Ecology 102, 659666.CrossRefGoogle Scholar
Giladi, I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112, 481492.CrossRefGoogle Scholar
Gómez, C and Espadaler, X (2013) An update of the world survey of myrmecochorous dispersal distances. Ecography 36, 11931201.CrossRefGoogle Scholar
Gómez, JM, Schupp, EW and Jordano, P (2019) Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biological Reviews 94, 874902.CrossRefGoogle ScholarPubMed
Gorb, E And Gorb, S (2003) Seed Dispersal by Ants in a Deciduous Forest Ecosystem: Mechanisms, Strategies, Adaptations. Dordrecht: Springer.CrossRefGoogle Scholar
Gove, AD, Majer, JD and Dunn, RR (2007) A keystone ant species promotes seed dispersal in a “diffuse” mutualism. Oecologia 153, 687697.CrossRefGoogle Scholar
Guénard, B, Weiser, MD and Dunn, RR (2012) Global models of ant diversity suggest regions where new discoveries are most likely are under disproportionate deforestation threat. Proceedings of the National Academy of Sciences USA 109, 73687373.CrossRefGoogle ScholarPubMed
Harrison, XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2, e616.CrossRefGoogle ScholarPubMed
Hölldobler, B and Wilson, EO (1990) The Ants. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Howe, HF and Miriti, MN (2000) No question: seed dispersal matters. Trends in Ecology & Evolution 15, 434436.CrossRefGoogle ScholarPubMed
Hubbell, SP, Foster, RB, O’Brien, ST, Harms, KE, Condit, R, Wechsler, B De Lao, SL (1999) Light-Gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283, 554557.CrossRefGoogle Scholar
Janzen, DH (1970) Herbivores and the number of tree species in tropical forests. American Naturalist 104, 501528.CrossRefGoogle Scholar
Kaspari, M (1993) Body size and microclimate use in Neotropical granivorous ants. Oecologia 96, 500507.CrossRefGoogle ScholarPubMed
Kenne, M and Dejean, A (1997) Caste polyethism and honeydew collection activity in foraging workers of Myrmicaria opaciventris. Sociobiology 30, 247255.Google Scholar
Kenne, M and Dejean, A (1999) Spatial distribution, size and density of nests of Myrmicaria opaciventris Emery (Formicidae, Myrmicinae). Insectes Sociaux 46, 179185.CrossRefGoogle Scholar
Leal, IR, Wirth, R and Tabarelli, M (2007) Seed dispersal by ants in the semi-arid Caatinga of north-east Brazil. Annals of Botany 99, 885894.CrossRefGoogle ScholarPubMed
Leal, LC, Andersen, AN and Leal, IR (2014) Anthropogenic disturbance reduces seed-dispersal services for myrmecochorous plants in the Brazilian Caatinga. Oecologia 174, 173181.CrossRefGoogle ScholarPubMed
Levey, DJ and Byrne, MM (1993) Complex ant–plant interactions: rain-forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74, 18021812.CrossRefGoogle Scholar
Magalhães, VB, Espírito Santo, NB, Salles, LF, Soares, H Jr and Oliveira, PS (2018) Secondary seed dispersal by ants in Neotropical cerrado savanna: species-specific effects on seeds and seedlings of Siparuna guianensis (Siparunaceae). Ecological Entomology 43, 665674.CrossRefGoogle Scholar
Mascaro, J, Schnitzer, SA and Carson, WP (2004) Liana diversity, abundance, and mortality in a tropical wet forest in Costa Rica. Forest Ecology and Management 190, 314.CrossRefGoogle Scholar
Matthesius, A (2006) Testing the Janzen–Connell model for species diversity in a West African montane forest. MSc thesis, University of Canterbury, New Zealand.Google Scholar
Matthesius, A, Chapman, H and Kelly, D (2011) Testing for Janzen–Connell effects in a west African montane forest. Biotropica 43, 7783.CrossRefGoogle Scholar
Moles, AT and Westoby, M (2004) What do seedlings die from and what are the implications for evolution of seed size? Oikos 106, 193199.CrossRefGoogle Scholar
Nathan, R and Muller-Landau, HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution 15, 278285.CrossRefGoogle ScholarPubMed
Ness, JH, Bronstein, JL, Andersen, AN and Holland, JN (2004). Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions. Ecology 85, 12441250.CrossRefGoogle Scholar
O’Dowd, DJ and Gill, AM (1984) Predator satiation and site alteration following fire: mass reproduction of alpine ash (Eucalyptus delegatensis) in southeastern Australia. Ecology 65, 10521066.CrossRefGoogle Scholar
Oliveira, PS, Galetti, M, Pedroni, F and Morellato, LPC (1995) Seed cleaning by Mycocepurus goeldii ants (Attini) facilitates germination in Hymenaea courbaril (Caesalpiniaceae). Biotropica 27, 518522.CrossRefGoogle Scholar
Orrock, JL and Christopher, CC (2010) Density of intraspecific competitors determines the occurrence and benefits of accelerated germination. American Journal of Botany 97, 694699.CrossRefGoogle ScholarPubMed
Palfi, Z, Spooner, PG and Robinson, W (2017) Seed dispersal distances by ants increase in response to anthropogenic disturbances in Australian roadside environments. Frontiers in Ecology and Evolution 5, 132.CrossRefGoogle Scholar
Passos, L and Oliveira, PS (2002) Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rain forest tree. Journal of Ecology 90, 517528.CrossRefGoogle Scholar
Passos, L and Oliveira, PS (2003) Interactions between ants, fruits and seeds in a restinga forest in south-eastern Brazil. Journal of Tropical Ecology 19, 261270.CrossRefGoogle Scholar
Passos, L and Oliveira, PS (2004) Interaction between ants and fruits of Guapira opposita (Nyctaginaceae) in a Brazilian sandy plain rainforest: ant effects on seeds and seedlings. Oecologia 139, 376382.CrossRefGoogle Scholar
Pirk, GI, Di Pasquo, F and de Casenave, JL (2009) Diet of two sympatric Pheidole spp. ants in the central Monte desert: implications for seed–granivore interactions. Insectes Sociaux 56, 277.CrossRefGoogle Scholar
Pizo, MA and Oliveira, PS (1998) Interaction between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil. American Journal of Botany 85, 669674.CrossRefGoogle Scholar
Pizo, MA and Oliveira, PS (2001) Size and lipid content of nonmyrmecochorous diaspores: effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil. Plant Ecology 157, 3752.CrossRefGoogle Scholar
Raimundo, RLG, Guimaraes, PR, Almeida-Neto, M and Pizo, MA (2004) The influence of fruit morphology and habitat structure on ant-seed interactions: a study with artificial fruits. Sociobiology 44, 261270.Google Scholar
Roberts, JT and Heithaus, ER (1986) Ants rearrange the vertebrate-generated seed shadow of a neotropical fig tree. Ecology 67, 10461051.CrossRefGoogle Scholar
Sabu, TK, Shiju, RT, Vinod, KV and Nithya, S (2011) A comparison of the pitfall trap, Winkler extractor and Berlese funnel for sampling ground-dwelling arthropods in tropical montane cloud forests. Journal of Insect Science 11. doi: 10.1673/031.011.0128.CrossRefGoogle ScholarPubMed
Seidler, TG and Plotkin, JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biology 4, e344.CrossRefGoogle ScholarPubMed
Smith, DS, Lau, MK, Jacobs, R, Monroy, JA, Shuster, SM and Whitham, TG (2015) Rapid plant evolution in the presence of an introduced species alters community composition. Oecologia 179, 563572.CrossRefGoogle ScholarPubMed
Svenning, JC, Normand, S and Skov, F (2006) Range filling in European trees. Journal of Biogeography 33, 20182021.CrossRefGoogle Scholar
Symonds, MR and Moussalli, A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioral Ecology and Sociobiology 65, 1321.CrossRefGoogle Scholar
Tamme, R, Götzenberger, L, Zobel, M, Bullock, JM, Hooftman, DA, Kaasik, A and Pärtel, M (2014) Predicting species’ maximum dispersal distances from simple plant traits. Ecology 95, 505513.CrossRefGoogle ScholarPubMed
Thomson, FJ, Auld, TD, Ramp, D and Kingsford, RT (2016) A switch in keystone seed-dispersing ant genera between two elevations for a myrmecochorous plant, Acacia terminalis . PLoS ONE 11, e0157632.CrossRefGoogle ScholarPubMed
Van Schaik, CP, Terborgh, JW and Wright, SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24, 353377.CrossRefGoogle Scholar
Verdú, M and Traveset, A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86, 13851394.CrossRefGoogle Scholar
Vittoz, P and Engler, R (2007) Seed dispersal distances: a typology based on dispersal modes and plant traits. Botanica Helvetica 117, 109124.CrossRefGoogle Scholar
Wang, BC and Smith, TB (2002) Closing the seed dispersal loop. Trends in Ecology & Evolution 17, 379386.CrossRefGoogle Scholar
Warren, RJ and Giladi, I (2014) Ant-mediated seed dispersal: a few ant species (Hymenoptera: Formicidae) benefit many plants. Myrmecological News 20, 129140.Google Scholar
Weckerle, CS and Rutishauser, R (2005) Gynoecium, fruit and seed structure of Paullinieae (Sapindaceae). Botanical Journal of the Linnean Society 147, 159189.CrossRefGoogle Scholar
Wenny, DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evolutionary Ecology Research 3, 3750.Google Scholar
Zamble, A, Carpentier, M, Kandoussi, A, Sahpaz, S, Petrault, O, Ouk, T and Martin-Nizard, F (2006) Paullinia pinnata extracts rich in polyphenols promote vascular relaxation via endothelium-dependent mechanisms. Journal of Cardiovascular Pharmacology 47, 599608.CrossRefGoogle Scholar
Zelikova, TJ (2008) Variation in the effects of ants on seed dispersal and ecosystem processes. Thesis. University of Colorado at Boulder.Google Scholar
Zelikova, TJ and Breed, MD (2008) Effects of habitat disturbance on ant community composition and seed dispersal by ants in a tropical dry forest in Costa Rica. Journal of Tropical Ecology 24, 309316.CrossRefGoogle Scholar
Zwiener, VP, Bihn, JH and Marques, M (2012) Ant–diaspore interactions during secondary succession in the Atlantic forest of Brazil. Revista de Biologia Tropical 60, 933942.Google ScholarPubMed