Interhabitat variation in diplochory: Seed dispersal effectiveness by birds and ants differs between tropical forest and savanna

Camargo, Paulo H. S. A.; Rodrigues, Suelen Barbosa Moraes; Piratelli, Augusto João; Oliveira, Paulo S.

doi:10.1016/j.ppees.2019.04.002

Cited by 20 publications

(19 citation statements)

References 52 publications

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“…Diaspore-animal interactions in tropical ecosystems often involve different agents of dispersal in subsequent steps (Camargo, Rodrigues, Piratelli, Oliveira, & Christianini, 2019;Vander Wall & Longland, 2004). Secondary seed dispersal has been commonly attributed to vertebrates, such as rodents (Feer & Forget, 2002;Genrich, Mello, Silveira, Bronstein, & Paglia, 2017;Lessa, Geise, & Costa, 2013).…”

Section: Introductionmentioning

confidence: 99%

Topsoil disturbance reshapes diaspore interactions with ground‐foraging animals in a megadiverse grassland

Arruda

Costa

Guerra

et al. 2020

J Vegetation Science

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Questions Anthropogenic disturbances are known to be followed by extremely poor recovery in edaphic grasslands. However, the role of interactions with diaspore predators and secondary dispersers, which compose the dispersal filter and modulate plant community recovery, has been overlooked. We performed field experiments to investigate how soil disturbances affect diaspore interactions with the ground‐foraging fauna to better understand how disturbance influences regeneration potential. Location Campo rupestre vegetation, megadiverse edaphic grasslands, southeastern Brazil. Methods We used diaspores from five native species to compare removal rates between disturbed (top soil removal) and preserved sites; we also controlled invertebrate and vertebrate access to determine their role. In addition, we assessed differences in the diaspore removal effectiveness (DRE) and the structure of animal–diaspore interactions through network based‐approach. Results For three species, the average diaspore removal rates was relatively high (between 30% and 70%). Invertebrates were the most common removal agents in both disturbed and preserved sites. Interactions with foraging fauna and removal rates were 20% smaller in disturbed sites. Considering all diaspore removal events in disturbed sites, 24% resulted in the displacement from disturbed to preserved sites, but no diaspore was transported from preserved to disturbed ones. The animal–diaspore network was exclusively composed by ant–diaspore interactions and was more diverse and robust in preserved sites compared with disturbed ones. Seed predator ants (Pheidole and Dorymyrmex) were more common in disturbed sites. Furthermore, significant differences were found in the DRE between ant species and site types, suggesting specificity in the provision of dispersal services. Conclusions Topsoil removal affected removal proportions, DRE and ant–diaspore interaction network structure. The lack of diaspore dispersal towards disturbed sites indicates that soil removal affects secondary seed removal dynamics, impeding recovery potential. Disturbance negatively affected diaspore fate by reshaping interactions with ground‐foraging secondary seed dispersers and predators, constraining the development of seed bank and thus impacting upon vegetation dynamics and resilience.

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Section: Introductionmentioning

confidence: 99%

Topsoil disturbance reshapes diaspore interactions with ground‐foraging animals in a megadiverse grassland

Arruda

Costa

Guerra

et al. 2020

J Vegetation Science

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“…In other systems, nevertheless, ants are known to be important secondary seed dispersers (e.g. Bieber, Silva, & Oliveira, 2013; Camargo, Rodrigues, Piratelli, Oliveira, & Christianini, 2019; Christianini & Oliveira, 2010; Levey & Byrne, 1993).…”

Section: Methodsmentioning

confidence: 99%

Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed‐dispersing ants

Palacio

Siepielski

Lacoretz

et al. 2020

J of Evolutionary Biology

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Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy-fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.

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“…Approximately 11,000 species of plants world‐wide possess lipid‐rich appendages (elaiosomes) that are attractive to foraging ants (Beattie & Culver, 1981; Gorb & Gorb, 2003; Lengyel et al., 2010). While myrmecochory is technically a generalized mutualism, we now know that in many systems, interactions are asymmetrical in that only a few ant species act as high‐quality seed dispersers for several species of plants (Camargo, Rodrigues, Piratelli, Oliveira, & Christianini, 2019; Gove, Majer, & Dunn, 2007; Manzaneda & Rey, 2009; Ness, Morin, & Giladi, 2009; Warren & Giladi, 2014; Zhu, Wang, & Codella, 2017). High‐quality seed‐dispersers are often large scavenging or omnivorous ants that forage individually and discover food quickly.…”

Section: Introductionmentioning

confidence: 99%

“…Poor seed‐dispersers are ant species that interact with myrmecochorous seeds, but fail to move seeds, move them short distances or to inhospitable locations or consume parts of or damage seeds (Giladi, 2006; Warren & Giladi, 2014). In ecosystems where myrmecochory is common, particular ant species or genera that are high‐quality seed‐dispersers serve the role of ‘keystone’ or major dispersers of myrmecochorous plants (Camargo et al, 2019; Gove et al., 2007; Manzaneda & Rey, 2009; Ness et al., 2009; Zhu et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

Interactions between seed‐dispersing ant species affect plant community composition in field mesocosms

Prior

Meadley‐Dunphy

Frederickson

2020

Journal of Animal Ecology

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1. In generalized mutualisms, species vary in the quality of services they provide to their partners directly via traits that affect partner fitness and indirectly via traits that influence interactions among mutualist species that play similar functional roles. Myrmecochory, or seed dispersal by ants, is a generalized mutualism with ant species varying in the quality of dispersal services they provide to their plant partners. Variation in ant species identity can directly impact seed dispersal patterns and plant community composition; however, we know less about how interactions among seed-dispersing ant species indirectly influence plant partners. 2. The invasive ant Myrmica rubra, is a high-quality seed-disperser in its native range that interacts with myrmecochores (ant-dispersed plants) and the high-quality seed disperser Aphaenogaster sp. in its invaded range. We use this system to examine how interactions between two functionally similar mutualist ant species influence the recruitment and community composition of ant-dispersed plants. 3. We performed a field mesocosm experiment and a laboratory behavioural experiment to compare discovery and dominance behaviours between ant species, and seed dispersal and seedling recruitment of four myrmecochore species among intraspecific interaction treatments of each ant species and an interspecific interaction treatment. 4. We found that M. rubra was better at discovering and dispersing seeds, but Aphaenogaster sp. was dominantly aggressive over M. rubra. Interspecific interactions dampened seed dispersal relative to dispersal by the better disperser. Despite this dampening, we found no effect of interspecific interactions on seedling recruitment. However, community composition of seedlings in the interspecific interaction treatment was more similar to composition in the aggressively dominant ant (Aphaenogaster sp.) treatment than in the better discoverer ant M. rubra treatment. 5. We show that interspecific interactions between mutualist species in the same functional guild affect the outcome of mutualistic interactions with partner species. Despite the native ant dispersing fewer seeds, its dominance over the subordinate (invasive) ant has the potential to allow for some level of biotic resistance against the effects of M. rubra on plant communities when these species coexist.

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Interhabitat variation in diplochory: Seed dispersal effectiveness by birds and ants differs between tropical forest and savanna

Cited by 20 publications

References 52 publications

Topsoil disturbance reshapes diaspore interactions with ground‐foraging animals in a megadiverse grassland

Topsoil disturbance reshapes diaspore interactions with ground‐foraging animals in a megadiverse grassland

Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed‐dispersing ants

Interactions between seed‐dispersing ant species affect plant community composition in field mesocosms

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