Discussion
Our data revealed a strong link between the average and maximum seed and
fruit sizes consumed and the body mass of frugivorous mammals (see
Fig.1). These data thus indicate that larger mammals generally consume
larger fruits and ingest larger seeds. It is important to note that the
largest seeds can only be ingested by large mammals (Forget et
al. 2007), but the opposite is not true, large mammals can ingest many
small seeds. Furthermore, seed size does not necessarily correlate with
fruit size, e.g. Annona muricata , as large fruits can contain
numerous small seeds.
Skull dimensions including jaw gape, jaw length, canine overlap, and the
distance between molars also appear good predictors of the size of
ingested seeds (see Fig.2). These measurements mainly reflect the food
passage and maximal jaw opening (Hylander 2013). Consequently, cranial
dimensions, especially those linked with food passage size constrain the
size of seeds ingested. Moreover, coronoid height and jaw width appear
predictors of the size of ingested fruits. These dimensions reflect the
food passage and the bite force of the species. Nevertheless, these data
suggest that the size of consumed fruits is less predictable than the
size of seeds. Large-sized fruits can be broken into pieces or eaten
without being detached from their support by some bats (Morrison 1980;
Singaravelan & Marimuthu 2008). Carnivores sometimes drop large fruit
to the ground to break it up (Howe 1986), while the dexterity of
primates enables them to consume fruit larger than their gape (Peckreet al. 2019).
The same analysis was carried out only for Chiroptera and revealed
co-variations similar to the multi-taxon analysis (see Fig. 2 and 3).
Thus, also within Chiroptera the morphology of the cranium appears to
limit the size of the seeds that can be ingested and dispersed. This
pattern is relatively strong and reveal few different behaviours in the
treatment of seeds by Chiroptera. Bats consume the pulp of the fruits,
swallow small seeds, or drop them if they are too large to be swallowed
(Forget et al. 2007; Lobova et al 2009). However, the same
analysis was not significant for Primates. Although many of them swallow
seeds, some primates consistently spit large seeds (Lambert 1999). It
suggests that taxa with diverse handling behaviour (swallowing versus
spitting) might not be well represented by this model.
Our analysis exploring relations between transit times, seed dispersal
distances and body mass of primates did reveal covariation (see Fig. 4).
Gorillas dispersed seeds further than tamarins, for example, showing
that body mass is the principal driver of these covariations. This
reflects the strong relationship between body mass and seed retention
times suggested in previous studies (Wotton & Kelly 2012; Yoshikawaet al. 2019).
Our analysis exploring relationships between skull dimensions, seed
dispersal distances and transit times of primates was significant.
However, the covariations were quite variable and dependent on the
species involved. A possible explanation can be the difference in group
size among primate species. There is a positive correlation between
primate body mass and group size (Clutton-Brock & Harvey 1977).
Primates living in large groups travel further than species in small
groups (Wrangham et al. 1993). Nevertheless, further studies
exploring how primates and other mammals manipulate fruits and seeds are
needed to better understand these relationships. Our limited database
does not allow to test for this relationship at the moment, but this is
an obvious issue for future studies.
Oral behaviours related to food acquisition and ingestion are reflected
in the form of the skull, jaws and teeth. Consequently, based on cranial
morphology, several examples show the possibility to infer feeding or
dietary behaviour to museum specimens (Dumont 1997; Bargo 2001; Jungerset al. 2002). In addition, evidence shows that body size can be
used as a strong indicator of seed retention time of extinct animals.
This is suggested by a study using body mass of extinct Mesozoic
dinosaurs to deduce their seed retention times that determines the
spatial pattern of seed dispersal (Yoshikawa et al. 2019). The
strong covariations that we observed, indicate that seed size ingested,
retention times and seed dispersal distance could be inferred in extinct
animals based on morphological measurements.
Significant gaps in our understanding of the diet in frugivorous
carnivores were apparent. For example, data on seeds ingested by the
binturong (Arctictis binturong) are based on a single individual
(Nakabayashi et al. 2017). Consequently, we were able to gather
data on ingested seeds for only a small number of species (N=13).
Despite the few studies on carnivores, these animals have the potential
to be excellent dispersers. For example, the civet (Paradoxurus
hermaphroditus ) can swallow and disperse disproportionately large seeds
(Nakashima et al. 2010) and seeds can be retained for several
hours in the digestive tract during which the animal can travel several
hundreds of meters (Nakashima et al. 2010).
Our results demonstrate a tight link between seed traits and the skull
dimensions and body mass in frugivorous mammals. In harvested forests
for timber, the average seed size decreases because plants with large
seeds (hardwood, commercial species) are often harvested (Markl et
al. 2012) which can, in turn, impact large-bodied frugivores by
modifying the availability of their food resources. Conversely, if large
dispersers go extinct, e.g. through hunting, average seed size will also
decrease given that size and cranial morphology appear tightly
correlated to seed size dispersed. This is suggested by a study in South
American forests, where the loss of large fruit-eaters has led to a
reduction in the average seed size of Euterpe edulis palms
(Galetti et al. 2013). Furthermore, it has been shown that
defaunation also leaves its signature in the gene pool of plant
populations (Pacheco & Simonetti 2000; Carvalho et al. 2016).
Thus, the absence of seed dispersers does not only result in phenotypic
changes but also affects allelic frequencies of plants, with unknown
effects on the long-term persistence of plant species and entire
communities.
In this study, we have shown that large mammals are essential for
dispersing the seeds of large-seeded plants. Our results underline the
importance of maintaining functional diversity in seed dispersers to
maintain tropical forest structure and regeneration, because of
morphological constraints on seed sizes consumed by different species.
In addition, we have shown that morphological characteristics can be
used to predict seed dispersal patterns of recent or extinct mammals
which also provide a basis for predicting the consequences of frugivore
extinction within tropical forests.