Anthropogenic impacts on plant-animal mutualisms: A global synthesis for pollination and seed dispersal

Teixido, Alberto L.; Fuzessy, Lisieux Franco; Souza, Camila Silveira; Gomes, Ingrid N.; Kaminski, Lucas A.; Oliveira, Patrícia Carla de; Maruyama, Pietro Kiyoshi

doi:10.1016/j.biocon.2022.109461

Cited by 24 publications

(14 citation statements)

References 115 publications

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“…Animal‐mediated plant dispersal thereby enables critical supporting services, including primary production and nutrient cycling (Herrera et al ., 1994; Lundberg & Moberg, 2003; Hougner, Colding & Söderqvist, 2005; Garcia, Zamora & Amico, 2010; Wenny et al ., 2011). However, interrelated drivers of global change, such as extinctions, introductions, and habitat conversion, alter the composition of plant–animal mutualisms and the interactions among participating organisms (Brook, Sodhi & Bradshaw, 2008; De Vos et al ., 2014; McConkey, 2018; Teixido et al ., 2022). By perturbing plant–animal mutualisms, global change may thus impact the quality of ecosystem services.…”

Section: Ecological Significance Of Passive Directed Dispersalmentioning

confidence: 99%

Passive directed dispersal of plants by animals

2022

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Conceptual gaps and imprecise terms and definitions may obscure the breadth of plant-animal dispersal relationships involved in directed dispersal. The term 'directed' indicates predictable delivery to favourable microsites. However, directed dispersal was initially considered uncommon in diffuse mutualisms (i.e. those involving many species), partly because plants rarely influence post-removal propagule fate without specialized adaptations. This rationale implies that donor plants play an active role in directed dispersal by manipulating vector behaviour after propagule removal. However, even in most classic examples of directed dispersal, participating plants do not influence animal behaviour after propagule removal. Instead, such plants may take advantage of vector attraction to favourable plant microsites, indicating a need to expand upon current interpretations of directed dispersal. We contend that directed dispersal can emerge whenever propagules are disproportionately delivered to favourable microsites as a result of predictably skewed vector behaviour. Thus, we propose distinguishing active and passive forms of directed dispersal. In active directed dispersal, the donor plant achieves disproportionate arrival to favourable microsites by influencing vector behaviour after propagule removal. By contrast, passive directed dispersal occurs when the donor plant takes advantage of vector behaviour to arrive at favourable microsites. Whereas predictable post-removal vector behaviour is dictated by characteristics of the donor plant in active directed dispersal, characteristics of the destination dictate predictable post-removal vector behaviour in passive directed dispersal. Importantly, this passive form of directed dispersal may emerge in more plant-animal dispersal relationships because specialized adaptations in donor plants that influence post-removal vector behaviour are not required. We explore the occurrence and consequences of passive directed dispersal using the unifying generalized gravity model of dispersal. This model successfully describes vectored dispersal by incorporating the influence of the environment (i.e. attractiveness of microsites) on vector movement. When applying gravity models to dispersal, the three components of Newton's gravity equation (i.e. gravitational force, object mass, and distance between centres of mass) become analogous to propagules moving towards a location based on characteristics of the donor plant, the destination, and relocation processes. The generalized gravity model predicts passive directed dispersal in plant-animal dispersal relationships when (i) animal vectors are predictably attracted to specific destinations, (ii) animal vectors disproportionately disperse propagules to those destinations, and (iii) those destinations are also favourable microsites for the dispersed plants. Our literature search produced evidence for these three conditions broadly, and we identified 13 distinct scenarios where passive directed dispersal likely occurs because vector behavio...

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Section: Ecological Significance Of Passive Directed Dispersalmentioning

confidence: 99%

Passive directed dispersal of plants by animals

2022

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“…The growing number of vertebrate species at risk of extinction threatens biodiversity and ecosystem health by compromising key interactions between species-such as seed dispersal by fruit-eating animals-that are critical for the functioning of natural ecosystems [1][2][3][4][5]. Tropical forest ecosystems are among the most vulnerable to negative effects following vertebrate species losses, particularly because the majority of tropical plant species rely on frugivores for animal-mediated seed dispersal [6,7].…”

Section: Introductionmentioning

confidence: 99%

Loss of endangered frugivores from seed dispersal networks generates severe mutualism disruption

Lamperty

Brosi

2022

Proc. R. Soc. B.

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Many tropical seed-dispersing frugivores are facing extinction, but the consequences of the loss of endangered frugivores for seed dispersal is not well understood. We investigated the role of frugivore endangerment status via robustness-to-coextinction simulations (in this context, more accurately described as robustness-to-partner-loss simulations) using data from the Brazilian Atlantic Forest biodiversity hotspot. By simulating the extinction of endangered frugivores, we found a rapid and disproportionate loss of tree species with dispersal partners in the network, and this surprisingly surpassed any other frugivore extinction scenario, including the loss of the most generalist frugivores first. A key driver of this pattern is that many specialist plants rely on at-risk frugivores as seed-dispersal partners. Moreover, interaction compensation in the absence of endangered frugivores may be unlikely because frugivores with growing populations forage on fewer plant species than frugivores with declining populations. Therefore, protecting endangered frugivores could be critical for maintaining tropical forest seed dispersal, and their loss may have higher-than-expected functional consequences for tropical forests, their regeneration processes, and the maintenance of tropical plant diversity

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“…Although extreme events can eliminate new colonists, a more common effect is to disturb the arrival site, reducing competition [22]. Severe disruption can influence colonization whether it is natural (e.g., volcanic eruptions [23]) or anthropogenic (e.g., farming, hunting, and urbanization [24,25]). However, relative to natural extreme events, anthropogenic disturbances are more likely to cause long-lasting or permanent changes.…”

Section: Determinants Of Post-ldd Establishment Success (1) Propagule...mentioning

confidence: 99%

“…The world's biota is being profoundly affected by biological invasions and climate change [24]. Research placing anthropogenic distribution changes in the context of natural ones over geological time is critically needed.…”

Section: Bridging Disciplines and Connecting The Past To The Presentmentioning

confidence: 99%