Passive directed dispersal of plants by animals. (30th June 2022)

• Record Type: Journal Article
• Authors: Mason, David S.; Baruzzi, Carolina; Lashley, Marcus A.
• Is Part Of: Biological reviews. Volume 97:Number 5(2022)
• Page Start: 1908
• Page End: 1929
• Publication Date: 2022-06-30
• Subjects: coevolution -- directed dispersal -- dispersal patterns and processes -- endozoochory -- epizoochory -- global change -- gravity framework of dispersal -- plant dispersal -- resource tracking -- zoochory; Biology -- Periodicals; 570
• DOI: 10.1111/brv.12875
• Languages: English
• ISSNs: 1464-7931

Abstract

ABSTRACT: 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 behaviour is predictably skewed towards favourable microsites. We discuss the wide applicability of passive directed dispersal to plant–animal mutualisms and provide new insights into the vulnerability of those mutualisms to global change.