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.