Fruit-eating vertebrates play an important role in plant reproduction through seed dispersal (Levin et al., 2003). At local scales, seed dispersal increases plant fitness by potentially reducing competition between parent plants and their progeny and lowering the risk of density-dependent disease and predation (Janzen, 1970). Not only does seed dispersal promote community diversity (Harrison et al., 2013), it also reduces species aggregation (Wandrag et al., 2017). At landscape scales, long-distance dispersal (LDD) links local populations within a metapopulation, facilitates gene flow, and promotes migration and colonization of new habitats (Cain et al., 2000; Nathan, 2006). LDD by large vertebrates is of particular interest for biodiversity conservation because large-bodied vertebrates, past and present, are most at risk of human-related extinctions (Davidson et al., 2009). Under global climate change, the loss of large vertebrate seed dispersal services could compromise the survival of plant species that depend on range shifts driven by migration and colonization.

Vertebrate species affect plant community composition and population expansion by shaping the seed shadow – the spatial distribution of seeds relative to the parent plant. After fruit consumption, two key processes determine the seed shadow: gut passage time (GPT), the time between seed ingestion and defecation, and animal movement. Large, wide-ranging species with slow GPTs, therefore, disperse seeds farther on average than small-bodied species with fast GPTs (Vidal et al., 2013; Bunney et al., 2017). GPS technology can precisely measure animal movement (Kays et al., 2015), but measurements of GPT are less precisely known. GPT estimates have primarily depended on trials with captive animals owing to difficulties of relocating ingested seeds in the wild (Kinahan et al., 2007; Campos-Arceiz and Blake, 2011; Harich et al., 2016; Bunney et al., 2017). Captive animals, however, often have different diets and behaviors than wild animals, potentially introducing considerable error into the modeling of realistic seed shadows (Campos-Arceiz et al., 2008).

Most studies of vertebrate seed dispersal have focused on estimating species-level seed dispersal services (Holbrook et al., 2002; Russo et al., 2006; Blake et al., 2009), ignoring individual physiological traits (sex and size) and behavioral differences (boldness, aggressiveness, and sociability) (Zwolak and Sih, 2020). But individuals can vary consistently in behavior, with behaviors often covarying in behavioral syndromes, such as being more or less active (Sih et al., 2004). Behavioral syndromes could have direct ecological effects for seed dispersal (Sih et al., 2012). More exploratory, active foragers, for example, will likely have larger home ranges, higher encounter rates with high quality fruits, and consume more fruit because of higher energy needs (Zwolak and Sih, 2020). Thus, behavioral syndromes that control movement patterns of frugivores might affect seed dispersal distances and even the probability that seeds are deposited in suitable sites for recruitment.

To advance knowledge of seed dispersal for both theory and management, we need to understand the extrinsic, environmental and intrinsic, individual drivers of seed dispersal. Forest elephants (Loxodonta cyclotis) are an ideal model for studying variation in seed dispersal because they are intelligent, highly mobile, keystone seed dispersers in African tropical forests. Forest elephants consume seeds of more species than any other large vertebrate (Beirne et al., 2020) and are the sole disperser of many large or robustly encapsulated seed species (Guimarães et al., 2008; Beaune et al., 2013). With daily travel distances of 7.4 km per day (Mills et al., 2018) and annual home ranges of 195 km² (Beirne et al., 2021), they contribute to LDD. Using coarse GPT categories for small and large seeds, Blake et al. (2009) estimated that 88% of elephant-dispersed seeds were moved >1 km and 14% of seeds were moved >10 km from parent plants. Forest elephants, however, likely vary in the quality of their seed dispersal services with habitat use, sex and individual behavior. Male elephants, for example, move farther and have larger home range size and weaker site fidelity than females (Beirne et al., 2021). And, forest elephants exhibit distinct behavioral syndromes along an axis that varies from individuals with smaller home ranges, shorter movement distances and less exploratory behavior to those with larger ranges, longer movement distances and more exploratory behavior (Beirne et al., 2021). Finally, poaching and habitat loss have drastically reduced forest elephant populations in the last two decades (Maisels et al., 2013; Poulsen et al., 2017, 2018), thus we need to understand how the reduction or loss of seed dispersal services provided by elephants could affect forest species composition.

Here we quantify seed dispersal by forest elephants to improve understanding of their role in LDD. To do so, we use a novel experimental approach to: (1) estimate the GPT distribution of wild forest elephants and compare them to existing estimates; (2) model elephant-mediated seed dispersal patterns, using GPS tracking data from 96 elephants; and (3) evaluate the effects of human disturbance, habitat openness, elephant sex, and behavioral syndrome on seed dispersal distances. Filling gaps in the knowledge of a keystone seed disperser contributes to forecasting future forest composition in light of climate change, deforestation, and defaunation.

By integrating gut passage data from wild forest elephants with movement patterns from 96 GPS-collared individuals, we support previous findings that forest elephants are important long-distance seed dispersers (Blake et al., 2009). Median seed dispersal distance was 5.3 km, with 89% of seeds dispersed farther than 1-km and 10% of seeds dispersed farther than 14-km. At average GPT, maximum simulated seed dispersal was 101 km and average maximum dispersal of all elephants was 40.1 km. These dispersal distances are well beyond the local neighborhood of parent trees, and likely contribute to gene flow between populations and colonization of new habitats. Seed dispersal distances, however, depend on both extrinsic and intrinsic variables. Median seed dispersal distances varied significantly across sites and with both the sex and exploratory behavior of elephants. Our study highlights the importance of intraspecific variation among seed dispersers; through the portfolio effect intraspecific variation in dispersal can increase the range of habitats and conditions where seeds are dispersed, improving the likelihood of population persistence under unfavorable events (Bolnick et al., 2011).

Among tropical animals, forest elephants play a keystone role as seed dispersers because of the high number of fruit species they consume, their slow GPTs, and relatively long dispersal distances (Blake et al., 2009; Beirne et al., 2020). Large, frugivorous birds like hornbills can fly nearly 300 miles (Holbrook et al., 2002), but their faster GPTs limit maximum seed dispersal distance to 7-km (Holbrook and Smith, 2000). Compared to other elephant species, forest elephants demonstrate longer median and maximum dispersal distances. Savanna elephants (Loxodonta africana) move 50% of ingested seeds over 2.5 km from the parent plant, with a maximum dispersal distance of 65 km (Bunney et al., 2017). Asian elephants (Elephas maximus) disperse 50% of seeds >1.2 km, with a maximum distance of 5.8 km (Campos-Arceiz et al., 2008).

The distances elephants disperse seeds vary across sites. Elephants in Wonga Wongué dispersed seeds 1-km farther on average than elephants in Ivindo. Surprisingly, even though forest elephants move faster through grasslands than other habitats (Mills et al., 2018) and two (Wonga Wongué and Moukoulaba Doudou) of the three sites with significantly longer seed dispersal than Ivindo contain extensive grasslands, seed dispersal distances were not associated with the greater presence and proportional use of open habitat by elephants. But site-level variation in dispersal distances could be caused by a multitude of factors influencing movement, including differences in landscape heterogeneity (Levey et al., 2008) and configuration (Uriarte et al., 2011), presence of clearings (baïs), topography, weather, and spatial patterns in food resources. For example, rainfall, and to a lesser extent fruit availability, predict the proportion of time forest elephants spend in long, directionally persistent movements (Beirne et al., 2020). Thus, site-specific environmental characteristics can significantly influence frugivore movement patterns, and consequently, dispersal patterns, potentially driving among population differences in plant distribution and abundance (Nuñez et al., 2019).

Despite strong effects of poaching and human activities on elephant populations and movement (Beirne et al., 2021), seed dispersal distances did not vary significantly with human disturbance. Like Markl et al. (2012), we found that dispersal distances were slightly, but not significantly, lower in disturbed areas. Failure to detect an effect might be due to our use of HFI – a relatively coarse metric of human disturbance – and because most of the focal elephants inhabited protected areas where human pressure should be weak. Our study also focused only on dispersal distance, whereas hunting and logging could affect seed dispersal by altering rates of tree visitation and fruit removal (Markl et al., 2012). Alternatively, rather than reducing movement, forest elephants might respond to human activities in other ways, such as moving nocturnally, that could have weaker effects on seed dispersal.

Seed dispersal distances of individual forest elephants vary with sex and behavior. Males tended to disperse seeds farther, consistent with their larger home ranges and lower site fidelity (Beirne et al., 2021). Sex-based effects are likely even stronger than our findings because males are large, have higher energy needs, and therefore likely consume more fruit and disperse more seeds than females. In addition, mammalian GPT tends to scale with mass (Abraham et al., 2021); thus, male GPTs should be slower than female GPTs.

Behavioral syndromes, specifically the degree to which elephants are idlers or explorers, significantly affect seed dispersal distances. The most exploratory elephants dispersed seeds 1.1 km farther than the least exploratory elephants and 0.6 km farther than elephants with balanced movement behavior. This is consistent with findings that colonization, invasion, and range expansion are often associated with bolder, more aggressive, or more exploratory animals (Duckworth and Badyaev, 2007; Chapple et al., 2012). Within-population variation in behavioral types of elephants can result in seeds being deposited in a more diverse array of places, including a greater range of distances away from parent plants. This will result in dispersal kernels with fatter tails. The same behavioral traits, like boldness and exploration, that positively correlate with dispersal distances might differentially affect other stages of seed dispersal. For example, fast explorers might be more likely to first find fruits that are larger, brighter or more abundant (Zwolak and Sih, 2020); alternatively, explorers can be poor dispersers if they collect fewer seeds before moving on (weaker area-concentrated search: Spiegel et al., 2017).

Our estimates of LDD for forest elephants are likely conservative for several reasons. First, our GPT estimates are largely derived from small pellets and large seeds likely have longer GPTs. In fact, the three large tin seeds recovered from our baiting trials had an average GPT of 65.6 h. Second, we based our estimates of maximum seed dispersal on median GPT, meaning that half of seeds would be passed more slowly and dispersed farther. Third, our GPT estimates were based on data from a single female elephant and two juveniles, which may not be fully reflective of larger, male elephants. Reassuringly, however, mean GPT from other studies and elephant species correspond closely to our estimate of mean GPT (Figure 2). This suggests that estimating GPT from captive elephants is an effective (and less laborious) alternative to following wild elephants in the field. Using captive elephants has the advantage of being able to control for elephant characteristics (e.g., sex, age, size, and species) and to manipulate diet items (e.g., seed size, fruit type), enabling the identification of potentially important factors that drive GPT and dispersal distances. For example, if large seeds are retained in the gut longer than small seeds (Kleyheeg et al., 2018), then elephants might provide two types of dispersal services.

Our study demonstrates the importance of forest elephants in LDD and the strong effects of extrinsic (site) and intrinsic (sex and behavioral type) variables on seed dispersal distances. It also reveals gaps in our knowledge of seed dispersal by large, frugivorous animals. The specific environmental characteristics of sites that influence disperser movements need to be investigated, particularly in the face of global climate change, habitat fragmentation, and diminishing intact wilderness. In addition, life history strategies and stages of individuals, such as phenotypic, size-, and age-related variation influence animal GPTs and movements (Byrne et al., 2019; Abraham et al., 2021). While we identified individual variation in elephant movement, individual variation in fruit consumption rates and seed deposition patterns could also strongly influence the patterns and outcomes of seed dispersal (Markl et al., 2012).

In a rapidly changing world, failure of plant species to reproduce could alter the species composition of tropical forests and reduce fruit resources to the detriment of fruit-dependent animals like forest elephants (Bush et al., 2020). Conservation of seed dispersal processes depends on protection of keystone disperser species. Thus, we need to know which habitats to conserve and possibly which individuals to protect. Male elephants, for example, are often targeted by poachers for their large tusks (Mondol et al., 2014); but bolder, more exploratory males may be more likely to disperse plant species into new or regenerating habitats. Understanding extrinsic and intrinsic drivers of seed dispersal can improve management of species critical to broader ecosystem and biosphere functioning.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.

The animal study was reviewed and approved by Duke Institutional Animal Care and Use Committee, Duke University.

JP conceived the ideas and led the writing of the manuscript. CB, MB, SK, JK, WM, GO, JM, and TN collected the data. CR, JP, CB, TM, CN, LJ, and SX analyzed the data. All authors contributed critically to the drafts and gave final approval for publication and designed the methodology.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.