Deciphering seed dispersal decisions: Size, not tannin content, drives seed fate and survival in a tropical forest

Abstract

Scatter-hoarding animals can dramatically affect plant survival by depositing seeds in favorable microhabitats away from parent plants (seed dispersal) and by consuming seeds (seed predation). By understanding how scatter hoarders make seed dispersal decisions, we can infer how different plant chemical defenses or seed set strategies may influence seed survival and, ultimately, plant recruitment. We used a wild population of Central American agoutis, Dasyprocta punctata, to experimentally test how seed chemistry and size influence seed fates in a tropical premontane wet forest in Costa Rica. We hypothesized that seeds perceived by agoutis to be very valuable (large, non-toxic seeds) would be taken far from sources and preferentially cached over less valuable (small, toxic) seeds. Using artificial seeds created from baked polymer clay and peanuts, we manipulated seed chemistry (0%, 2%, 15% tannic acid) and size (4, 14, 24 g) in fully factorial paired-choice field experiments. We tracked the fates of individually numbered threadmarked seeds in space and time. There was no difference in the handling, regardless of size, of non-toxic and toxic seeds by agoutis. Large (24 g) seeds were moved farthest and preferentially hoarded by agoutis, whereas small (4 g) seeds were mostly eaten in situ. By experimentally manipulating seed chemistry and size with a high degree of replication using artificial seeds in the field, we have determined how these plant functional traits affect agouti seed dispersal decisions, with implications for plant propagation and the evolution of seed size.

Post-Dispersal Seed Removal in a Large-Seeded Palm by Frugivore Mammals in Western Ecuador

“…On the other side, removal by larger rodents such as agoutis, spiny rats, pacas ( Cuniculus paca ), and red-tailed squirrels ( Sciurus granatensis ) could enhance effective seed dispersal because rodents cache seeds in microsites where they have higher chances of being recruited to become reproductive adults (Choo et al., 2012; Dunham, 2011). In addition, agoutis, spiny rats, and squirrels scatter-hoard seeds, which increases seed dispersal distances through time (Brodin, 2010; Carvajal & Adler, 2008; Dittel et al., 2015; Jansen et al., 2012; Kuprewicz & García‐Robledo, 2019; Wright & Duber, 2001).…”

“…For this reason, seed dispersal over long-distances must be rare in the agroforestry system. On the other side, agoutis and pacas are among the main seed removers in the two forests, which is a habitat where their populations are abundant (Aliaga-Rossel et al., 2008; Beck-King et al., 1999; Kuprewicz & García‐Robledo, 2019). Agoutis could be responsible for long-distance dispersal events for more than 100 m which were previously estimated in the less-disturbed forest through a genetic parentage analysis in established seedlings (Escobar et al.…”

“…The limited seed removal by larger rodents such as agoutis and pacas in the agroforestry system suggests that dispersal occurs mostly over short distances in this habitat. Agoutis are the only rodents that are capable of dispersing large seeds over long-distances through scatter-hoarding (Jansen et al., 2012; Kuprewicz & García‐Robledo, 2019). For instance, a single large seed of the Neotropical palm Astrocaryum standleyanum can be buried and re-cached up to 36 times by agoutis, and in this way, become dispersed more than 100 m away from the parental palm (Jansen et al., 2012).…”

“…Many generalist animals may only feed on the fleshy fruit and do not provide effective dispersal for large seeds (Howe, 2016). Some rodent species are considered effective secondary dispersers of large seeds because they promote directed dispersal to specific microsites, and may scatter-hoard seeds in shallow caches for further consumption (Aliaga-Rossel et al., 2008; Brodin, 2010; Campos et al., 2017; Carvajal & Adler, 2008; Choo et al., 2012; Dittel et al., 2015; Haugaasen et al., 2010; Jansen et al., 2012; Kuprewicz & García‐Robledo, 2019; Sunyer et al., 2013; Vander Wall et al., 2005). Seeds that are not recovered from such caches can germinate and establish because seed burial reduces seed predation (Crawley & Long, 1995; Forget et al., 1994), increasing plant recruitment and regeneration (Dunham, 2011).…”

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive

“…Seed size, tannins and nutrient content of artificial seeds all affected various stages of the seed dispersal process by rodents, with size and nutrients tending to favour dispersal, and tannins disfavouring dispersal (Wang et al 2013). In contrast, artificial seed experiments with Dasyprocta punctata in Costa Rica suggest size but not tannin concentration affect seed dispersal decisions (Kuprewicz and García-Robledo 2019). Furthermore, artificial seeds with different characteristics were cached in different microhabitats, which can affect quality of dispersal; larger and more nutritious seeds were most likely to be cached under shrubs (Wang and Corlett 2017).…”