The mutualism–antagonism continuum in Neotropical palm–frugivore interactions: from interaction outcomes to ecosystem dynamics

Abstract

Frugivory, that is feeding on fruits, pulp or seeds by animals, is usually considered a mutualism when interactions involve seed dispersal, and an antagonism when it results in the predation and destruction of seeds. Nevertheless, most frugivory interactions involve both benefits and disadvantages for plants, and the net interaction outcomes thus tend to vary along a continuum from mutualism to antagonism. Quantifying outcome variation is challenging and the ecological contribution of frugivorous animals to plant demography thus remains little explored. This is particularly true for interactions in which animals do not ingest entire fruits, that is in seed‐eating and pulp‐eating. Here, we provide a comprehensive review of Neotropical palm–frugivore interactions, with a focus on how frugivore consumption behaviour (i.e. digestive processing, fruit‐handling ability and caching behaviour) and feeding types (fruit‐eating, pulp‐eating and seed‐eating) influence interaction outcomes at different demographic stages of palms. We compiled a total of 1043 species‐level palm–frugivore interaction records that explicitly captured information on which parts of palm fruits are eaten by animals. These records showed consumption of fruits of 106 Neotropical palm species by 273 vertebrate species, especially birds (50%) and mammals (45%), but also fish (3%) and reptiles (2%). Fruit‐eating involved all four taxonomic vertebrate classes whereas seed‐eating and pulp‐eating were only recorded among birds and mammals. Most fruit‐eating interactions (77%) resulted in positive interaction outcomes for plants (e.g. gut‐passed seeds are viable or seeds are successfully dispersed), regardless of the digestive processing type of vertebrate consumers (seed defecation versus regurgitation). The majority of pulp‐eating interactions (91%) also resulted in positive interaction outcomes, for instance via pulp removal that promoted seed germination or via dispersal of intact palm seeds by external transport, especially if animals have a good fruit‐handling ability (e.g. primates, and some parrots). By contrast, seed‐eating interactions mostly resulted in dual outcomes (60%), where interactions had both negative effects on seed survival and positive outcomes through seed caching and external (non‐digestive) seed dispersal. A detailed synthesis of available field studies with qualitative and quantitative information provided evidence that 12 families and 27 species of mammals and birds are predominantly on the mutualistic side of the continuum whereas five mammalian families, six mammal and one reptile species are on the antagonistic side. The synthesis also revealed that most species can act as partial mutualists, even if they are typically considered antagonists. Our review demonstrates how different consumption behaviours and feeding types of vertebrate fruit consumers can influence seed dispersal and regeneration of palms, and thus ultimately affect the structure and functioning of tropical ecosystems. Variation in feeding types of anim...

Conflicting selection pressures on seed size and germination caused by carnivorous seed dispersers

“…These findings advance our understanding of the broad paradigm of seed dispersal mechanisms, particularly regarding plant-mammal mutualistic interactions (Draper et al 2022). Unfortunately, many large and medium-sized mammal populations in Asia are declining due to intensifying global climate change, and anthropogenic pressures have deteriorated their survival habitats (Corlett 2017), which could have broad consequences for forest recruitment and ecosystem functionality (Marques Dracxler & Kissling 2022).…”

“…Effective seed dispersal requires the placement of viable seeds at sites that contribute to germination, establishment, and seedling growth (Marques Dracxler & Kissling 2022). Although birds, bats, primates, and herbivorous mammals have long been recognized as effective seed dispersers (Schupp 1993; Hernández et al.…”

“…Plants produce nutritious fleshy fruits to attract animals that usually consume the pulp and regurgitate or defecate the seeds, which may lead to successful seed dispersal if done by legitimate dispersers (Marques Dracxler & Kissling 2022). Effective dispersers should ingest and defecate undamaged seeds (Nakashima & Do Linh San 2022) and transport these seeds away from the parent plant to particular microsites and/or recently opened patches following disturbance for further germination and seedling growth (Dimitri & Longland 2022), and their gut transit should also have positive impact on germination success (Torres et al 2020).…”

The megaherbivore gap after the non-avian dinosaur extinctions modified trait evolution and diversification of tropical palms

“…parrots) or scatter-hoarders (e.g. rodents) [ 12 ]. Furthermore, the high rate of palm fruit size evolution during the PMHG is consistent with the large palm fossil fruits from a Palaeocene Colombian rainforest [ 49 ] and coincided with the radiation of small to medium-sized arboreal frugivorous birds and mammals [ 7 , 57 ] that were likely good dispersers of palm fruits [ 30 ].…”

“…Angiosperms are therefore expected to show numerous adaptations to the presence of, and potential interaction with, megaherbivores. Nevertheless, megafaunal fruits and spiny defences do not exclude interactions with smaller-bodied dispersers and grazers [ 11 , 12 ].…”