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The Ecological Significance of Secondary Seed Dispersal By SYNTHESIS & INTEGRATION The ecological significance of secondary seed dispersal by carnivores € € € 1, 1 1 1 ANNI HAMALAINEN , KATE BROADLEY, AMANDA DROGHINI, JESSICA A. HAINES, 1 1 1,2 CLAYTON T. LAMB, STAN BOUTIN, AND SOPHIE GILBERT 1Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2M9 Canada 2Department of Fish and Wildlife Sciences, University of Idaho, Moscow, Idaho 83843 USA Citation: Ham€ al€ ainen,€ A., K. Broadley, A. Droghini, J. A. Haines, C. T. Lamb, S. Boutin, and S. Gilbert. 2017. The ecological significance of secondary seed dispersal by carnivores. Ecosphere 8(2):e01685. 10.1002/ecs2.1685 Abstract. Animals play an important role in the seed dispersal of many plants. It is increasingly recog- nized, however, that the actions of a single disperser rarely determine a seed’s fate and final location; rather, multiple abiotic or animal dispersal vectors are involved. Some carnivores act as secondary dis- persers by preying on primary seed dispersers or seed predators, inadvertently consuming seeds contained in their prey’s digestive tracts and later depositing viable seeds, a process known as diploendozoochory. Carnivores occupy an array of ecological niches and thus range broadly on the landscape. Consequently, secondary seed dispersal by carnivores could have important consequences for plant dispersal outcomes, with implications for ecosystem functioning under a changing climate and across disturbed landscapes where dispersal may be otherwise limited. For example, trophic downgrading through the loss of carni- vores may reduce or eliminate diploendozoochory and thus compromise population connectivity for lower trophic levels. We review the literature on diploendozoochory and conclude that the ecological impact of a secondary vs. primary seed disperser depends on the relative dispersal distances, germination success, and the proportion of seeds exposed to secondary dispersal by carnivores. None of the studies up to present day have been able to rigorously assess the ecological significance of this process. We provide a framework of the components that determine the significance of diploendozoochory across systems and identify the components that must be addressed in future studies attempting to assess the ecological importance of diploendozoochory. Key words: climate change; diplochory; diploendozoochory; fragmentation; indirect dispersal; invasive species; polychory; predator; secondary dispersal; seed dispersal; seed dispersal effectiveness; seed predation. Received 19 December 2016; accepted 22 December 2016. Corresponding Editor: Debra P. C. Peters. Copyright: © 2017 Ham€ al€ ainen€ et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected] INTRODUCTION resources, reduce density-dependent seedling mortality, and may have better chances of encoun- Owing to their sessile adult lives, plants have tering suitable microhabitats for recruitment evolved numerous ways to ensure offspring dis- (Howe and Smallwood 1982). In addition to dis- perse away from the immediate vicinity of the persal by abiotic means such as wind and water, parent plant, typically via the movement of seeds. seed dispersal by animals (zoochory) is a common This movement is beneficial because seedlings dispersal mechanism that allows seeds to be that take root further away from their parent plant deposited some distance away from the parent avoid competing with related individuals for plant through animal vectors. While plants with ❖ www.esajournals.org 1 February 2017 ❖ Volume 8(2) ❖ Article e01685 € € € SYNTHESIS & INTEGRATION HAMALAINEN ET AL. high rates of seed predation have evolved adapta- been made to sufficiently establish the importance tions that minimize seed losses by animals (Hulme of the mechanism. A synthesis of the topic is there- and Benkman 2002), plants that rely on zoochory fore needed to enable broader predictions on the often produce seeds encased in fleshy fruits to prevalence and ecological role of diploendozoo- promote consumption by dispersers (endozoo- chory to help direct future research into the chory; Schaefer and Ruxton 2011). Estimates of phenomenon. the number of plants dispersed by animals vary Presumably, the effects of secondary dispersal widely, but endozoochory is estimated to be the depend strongly on the characteristics of the ani- primary dispersal mechanism in up to 94% of mal vectors and plants involved, as well as the woody plants, depending on the region (Jordano habitats they occupy. Therefore, we identified 2000, Buitron-Jurado and Ramırez 2014). Further- characteristics of the dispersal process that are more, many plants that do not seem to have adap- likely to influence plant fitness via germination tations for endozoochory can, nevertheless, be or recruitment success and access to suitable dispersed by animals in addition to dispersal by habitat. Using this information, we devised a other means such as wind, water, or gravity (Pake- framework to assess the importance of diploen- man et al. 2002, Orłowski et al. 2016). dozoochory in plant dispersal success under Despite such adaptations, there is increasing different conditions. Using this framework, we evidence that the final fate of seeds is not necessar- identified potential ecological consequences of ily determined by the animals that remove them secondary dispersal for ecosystem functioning. from the parent plant. Instead, multiple dispersal We then reviewed the existing literature on the vectors may be involved in taking seeds to their role of carnivores in multi-stage seed dispersal final destination or destruction (Ozinga et al. to assess the evidence in support of the identi- 2004, Vander Wall and Longland 2004); at the fied mechanisms and their implications for plant community level, plants were estimated to have dispersal. on average 2.15 dispersal vectors per species among Dutch ecosystems (Ozinga et al. 2004). WHAT MAKES DIPLOENDOZOOCHORY AN There has been increasing interest in diplochory ECOLOGICALLY SIGNIFICANT SEED DISPERSAL (two-phase dispersal, also known as “secondary MECHANISM? dispersal” or “indirect dispersal”) involving a sec- ond dispersal phase by ants, dung beetles, or scat- The overall impact of the dispersal mechanism ter-hoarding rodents that physically carry the on plant fitness is composed of the quantity of seeds to a new location (Vander Wall and Long- seeds processed by each dispersal vector, the via- land 2004), but relatively little attention has been bility of the seeds after handling and consump- paid to “diploendozoochory,” that is, seed disper- tion by each disperser, and the likelihood that sal that involves the ingestion of the seed by two the dispersed seeds will germinate and mature or more separate species of animals in sequence. into reproductive adult plants where they are Typically, this occurs when a carnivorous predator deposited (seed dispersal effectiveness frame- (hereafter referred to as carnivores) consumes a work; Schupp and Jordano 2010). In general, a primary disperser or a seed predator, along with prerequisite for successful endozoochory is that seeds in its prey’s digestive tract, and subsequently the digestive process of the animal vector does deposits the seeds in feces or in regurgitated pel- not damage the seed; thus, seeds should be swal- lets (Dean and Milton 1988, Nogales et al. 2007, lowed whole. Furthermore, the viable seed must 2012). Diploendozoochory was first documented be deposited by the final disperser at a site that by Darwin (1859), and opportunistic observations meets the minimum requirements for successful have since then been infrequently reported. germination: Deposition in a cave or a building Although diploendozoochory has recently been (Dean and Milton 1988), a highway or the ocean, approached more rigorously using experiments will usually impede seed germination. (Nogales 1999, Nogales et al. 2007, Padilla and For a carnivore to improve seed dispersal out- Nogales 2009, Padilla et al. 2012), the broader eco- comes, the seed dispersal effectiveness of diploen- logical significance of this phenomenon remains dozoochory must naturally be higher than that of largely unknown as few attempts have thus far dispersal by a single vector (Schupp and Jordano ❖ www.esajournals.org 2 February 2017 ❖ Volume 8(2) ❖ Article e01685 € € € SYNTHESIS & INTEGRATION HAMALAINEN ET AL. 2010). The types of plants and the primary and dispersers may thus deposit seeds in maladaptive secondary dispersers involved all influence dis- locations or out of their climate zone, but the persal effectiveness and the ecological significance plant could, nevertheless, benefit from the long- of the secondary dispersal phase, as detailed in distance dispersal if novel, suitable patches are the framework in Table 1. The involvement of a even occasionally reached and colonized via this carnivore in the second phase of the seed disper- process (Nathan et al. 2008, Caughlin and Fergu- sal process can influence plant fitness in three son 2013). ways: by transporting seeds, by altering the via- bility of transported seeds, and by changing the Effects on germination success quantity of seeds that are dispersed. Germination success may be altered via the treatment of a seed in a carnivore’s digestive tract Long-distance dispersal and can be differentially affected by various sec- Long-distance dispersal in plants,
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