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 animal consumers will influence ecosystem dynamics via effects on plant population dynamics and differences in long-distance seed dispersal, and may subsequently affect ecosystem functions such as carbon storage. The quantification of intra- and inter-specific variation in outcomes of plant-frugivore interactions - and their positive and negative effects on the seed-to-seedling transition of animal-dispersed plants - should be a key research focus to understand better the mutualism-antagonism continuum and its importance for ecosystem dynamics.

Keywords: Arecaceae; ecosystem functioning; ectozoochory; endozoochory; granivory; palm endocarp; seed caching; seed dispersal distance; seed predation; vertebrate.

Fig. 1

Methodological framework for synthesizing interaction outcomes in Neotropical palm–frugivore interactions along a mutualism–antagonism continuum. From a comprehensive literature review, pairwise interaction data between palms and vertebrate fruit, pulp and seed consumers were identified. Qualitative and quantitative information on feeding types, animal traits and interaction outcomes was extracted. Interaction outcomes were summarized along a mutualism–antagonism continuum at the level of species, families, feeding types and traits.

Fig. 2

Flow diagram depicting the identification of articles, their manual screening, and reasons for eligibility of interaction records and their inclusion or exclusion. The structure of the flow diagram follows the PRISMA statement for transparent reporting of systematic reviews (Moher et al., 2009).

Fig. 3

Frequency of types of feeding interactions for four taxonomic classes of frugivores (birds, mammals, reptiles and fish). Proportions of interactions are calculated based on the number of interaction records for which feeding interaction types could be identified (birds: N = 310; mammals: N = 708; reptiles: N = 10; fish: N = 15). Feeding interaction types: fruit‐eating = ingesting entire fruits; pulp‐eating = feeding on fruit mesocarps only; seed‐eating = feeding only on seeds (discarding fruit mesocarp).

Fig. 4

Examples of how the consumption behaviour involved in different feeding interaction types (fruit‐, pulp‐ and seed‐eating) can affect interaction outcomes during the seed‐to‐seedling transition of plants (e.g. seed viability, seed deposition, and seedling establishment). The examples are not exhaustive and refer to consumption behaviours associated with the digestive processing of fruits by fruit‐eaters, the handling ability of pulp‐ and seed‐eaters, and the seed‐caching behaviour of seed‐eaters, as reported in studies of palms (Arecaceae). Silhouettes representing animal taxa exemplify core groups of animal consumers of palm fruits, pulp and seeds. Palm–frugivore interactions are not restricted to these taxa.

Fig. 5

Proportion of interaction records that describe positive, negative or dual interaction outcomes for different taxonomic classes of animals (birds, mammals, reptiles, fish), per feeding interaction type. (A) Fruit‐eating (N = 398 interaction records), (B) pulp‐eating (N = 87 interaction records), and (C) seed‐eating (N = 370 interaction records).

Fig. 6

Variation in interaction outcomes within and across different feeding guilds (fruit‐, pulp‐ and seed‐eating). The proportion of positive interaction outcomes (x‐axis) is shown for different behavioural traits and separated by taxonomic class of frugivores. Behavioural traits are related to the digestive‐processing type (defecation, regurgitation, both) of fruit‐eaters, the fruit‐handling ability (high, intermediate, low) of pulp‐eaters and seed‐eaters, and the seed‐caching behaviour (caching, no caching) of seed‐eaters. The right side of the continuum (>50%) shows mostly mutualistic outcomes and the left side (<50%) mainly antagonistic outcomes.

Fig. 7

Dispersal distances of fruit‐eaters, pulp‐eaters and seed‐eaters involved in in Neotropical palm–frugivore interactions. (A) Distribution of mean dispersal distances (logarithmic axis) for fruit‐ (N = 3 records), pulp‐ (N = 25 records) and seed‐eating (N = 34 records), involving a total of 26 frugivore species and 22 palm species. (B) Distribution of maximum dispersal distances (logarithmic axis) recorded for fruit‐ (N = 4 records), pulp‐ (N = 2 records) and seed‐eating (N = 25 records), involving a total of 13 frugivore species and 18 palm species. Data on dispersal distances compiled from published articles (see Appendix S6).

Fig. 8

The mutualism–antagonism continuum in Neotropical palm–frugivore interactions. The proportion of positive interaction outcomes from qualitative and quantitative evidence reported in the literature is summarized for frugivore families and species along the mutualism–antagonism continuum (x‐axis). The left side of the continuum mostly shows antagonistic families or species (total or mean values in red; proportion of positive outcomes <0.5) and the right side mostly mutualistic species or families (total or mean values in blue; proportion of positive outcomes ≥0.5). Grey dots represent the proportion of positive outcomes for species within families (A) or individual studies within species (C), with grey horizontal lines indicating the range. (A) Qualitative family‐level data summarizing the proportion of positive outcomes across species within 17 frugivore families from 124 papers, with a total of 495 interaction records. The number of species (2–12) and the number of interaction records (mean ± SD: 29.1 ± 23.3, range: 7–83 outcome records) varies per family. (B) Qualitative species‐level data showing the average proportion of positive outcomes for 34 frugivore species with ≥5 outcome observations (mean ± SD: 11.9 ± 11.8, range: 5–53 outcome records) from 111 papers, with a total of 406 interaction records. (C) Quantitative species‐level data for three species of frugivores (the lowland tapir Tapirus terrestris, the red‐rumped agouti Dasyprocta leporina, and the hyacinth macaw Anodorhynchus hyacinthinus) summarizing evidence on the proportion of positive outcomes (five records per species) from six scientific studies. Outcome data are provided in a supplementary file containing interaction records and outcomes extracted from the sources (Continuum data; Dracxler & Kissling, 2021).

Fig. 9

Examples of methods for assessing the effects of frugivores on seed‐to‐seedling transitions, separated by feeding interaction types. The suggested methods allow for assessing interaction aspects such as interaction frequency (e.g. number of visits), fruit removal and consumption behaviour of frugivores, and their effects on plant population dynamics (seed survival and seed fate) and demography (seed germination and seedling establishment). Blue, yellow and orange circles show methods applicable to fruit‐eating (‘fruit’), pulp‐eating (‘pulp’) and seed‐eating (‘seed’), respectively.

Fig. 10

Variation of palm fruit traits and types of feeding interactions, and their influence on interaction outcomes. (A) Fruit‐eating: the fleshy‐fibrous fruits of the palm Euterpe edulis (show in the inset) are eaten whole mainly by birds, such as the red‐breasted toucan Ramphastos dicolorus, involving interactions that tend to result in positive outcomes (mainly via regurgitation of viable endocarps). Their thin endocarps, however, are destroyed when consumed by rodents or ungulates, resulting in negative outcomes. (B) Pulp‐eating interactions usually involve consumption of fleshy or fleshy‐fibrous fruits such as those of the palm genus Mauritiella (top left) and Syagrus (bottom), by animals such as the ochre‐marked parakeet Pyrrhura cruentata (shown feeding on the pulp of the African oil palm Elaeis guineensis, an exotic palm species in the Americas). (C) Seed‐eating is very frequent among scatter‐hoarding rodents such as the Central American agouti Dasyprocta punctata, which consumes the endosperm (white) enclosed in stony endocarps such as those found in Astrocaryum and Attalea palms (bottom right). These interactions often result in positive outcomes due to caching behaviour, but variation of endocarp traits (top right and bottom middle; endocarps of different palm genera) influences the decision‐making process by animals and thus interaction outcomes. Photograph credits: A, Toucan – Mathias Pires, fruit and endocarp – Caroline Dracxler; B, Parakeet – Mathias Pires, fruits – Caroline Dracxler; C, Agouti – Christian Ziegler, fruits and endocarps – Caroline Dracxler.

Fig. 11

Frequency distribution of palm fruit sizes recorded in different types of feeding interactions with frugivores (fruit‐, pulp‐ and seed‐eating). Fruit size measurements (average fruit width in cm; log‐transformed data) were extracted from PalmTraits 1.0 (Kissling et al., 2019) for all palm species (N = 106 species) that are captured in the data set of palm–frugivore interaction records (Dracxler & Kissling, 2021). Fruit sizes of 80, 27 and 63 palm species are included for fruit‐, pulp‐ and seed‐eating, respectively (Appendix S9).