Introduction
Most trees and woody lianas in tropical forests depend on animals for
seed dispersal (zoochory), with many trees producing fruits that are
attractive to animals (Howe & Smallwood 1982; Jordano 2000;
Buitrón-Jurado & Ramírez 2014; Howe 2014). Frugivores disperse seeds by
consuming the fruit pulp and spitting out the seeds after cleaning them
from their pulp (synzoochory) (Howe & Kerckhove 1981; Corlett & Lucas
1990; Lobova et al. 2009), or they ingest fruits whole and the
seeds are found intact in their feces (endozoochory) (Shilton et
al. 1999; Tobler et al. 2010; Beaune et al. 2013).
According to the Janzen-Connell hypothesis, the deposition of seeds away
from the parent tree could be advantageous for the plant because the
establishment and the survivorship of seedlings is affected by negative
density dependent processes such as intraspecific competition,
herbivores or pathogens (Janzen 1970; Connell 1971; Bell et al.2006; Mangan et al. 2010; Swamy et al. 2011). When
endozoochory occurs, seed dispersal distances mostly depend on the
transit time of the seed in the digestive tract and the movement of the
animal (Traveset et al. 2007). Large‐sized dispersers, like
elephants for example, show long-distance movements and long gut
retention times, thus generating a more diverse, long‐distance dispersal
pattern than smaller dispersers (Jordano et al. 2007 ;
Nathan et al. 2008; Campos-Arceiz & Blake 2011; Bueno et
al. 2013;
O′Farrill et al. 2013;
González & Stevenson 2014; Fuzessy et al. 2017). Thus, body mass
can be expected to be an important driver of seed dispersal distance.
The outcomes of interactions between plants and frugivores are
influenced by both plant and animal traits (Dehling et al. 2016).
Many traits of animals influence the quantity and quality of seed
dispersal and consequently impact the seed‐dispersal effectiveness
(Schupp et al. 2010; Beckman & Rogers 2013). Avian body mass
determines energy requirements, affecting foraging behaviour and
consequently may constrain the size of fruit that can be ingested
(Jordano 2000; Kitamura et al. 2002). Moreover, bill size or wing
morphology in birds influence fruit handling and manoeuvrability for
fruit access (Dehling et al. 2016). Nevertheless, no studies have
explored the link between body mass or skull dimensions with the size of
ingested seeds in mammals. Yet, body size and gape limitations can be
expected to be important drivers of these relationships as they are for
birds (Lord 2004; Godínez‐Alvarez et al. 2020).
Here, we focus on mammals with a predominantly frugivorous diet across
three orders: Chiroptera, Primates, and Carnivora. Frugivorous bats are
represented by the Pteropodidae family of the Old World (Africa, Asia,
Oceania) and Phyllostomidae of the New World (America). They are able to
carry up to 1.5x their body mass in fruit (Mahandran et al. 2018)
and some can ingest and defecate a large amount of small seeds (Lobovaet al. 2009). Frugivorous primates are represented by
strepsirrhines, platyrrhines (New World monkeys) and catarrhines (Old
World monkeys and apes). They constitute up to 25-40% of the biomass of
frugivorous animals in tropical forests (Chapman 1995). These taxa show
high interspecific variability in terms of seed treatment and therefore
in seed dispersal efficiency (Lambert 1999; Gross-Camp & Kaplin 2011).
Frugivorous carnivores are mainly represented by the Viverridae in the
Old World and the Procyonidae in the New World. Viverrids represent the
third largest group of frugivorous mammals in the Indo-Himalayan region
(Kitamura et al. 2002). Even if they are much less studied than
primates and bats, frugivorous carnivores are recognized as important
dispersers (Alves Costa & Eterovick 2007; Zhou et al. 2008;
Nakabayashi et al. 2016). They consume a wide variety of fruits
of which they disperse a significant number of intact seeds (Alves Costa
& Eterovick 2007; Chakravarthy & Ratnam 2015).
Using global data including Neotropics, Asia, Africa and Madagascar, we
tested the following questions:
1. Do body mass and skull dimensions predict the size of ingested seeds
and fruits? We expected a positive relationship between body mass and
cranial dimensions with the size of consumed fruits and ingested seeds.
2. Do body mass and skull dimensions influence seed dispersal distance?
We expect a positive relationship between body mass and seed dispersal
distance in relation to digestion times, with longer transit times
resulting in greater seed dispersal distances.