Seed traits matter—Endozoochoric dispersal through a pervasive mobile linker

Abstract

Although many plants are dispersed by wind and seeds can travel long distances across unsuitable matrix areas, a large proportion relies on co‐evolved zoochorous seed dispersal to connect populations in isolated habitat islands. Particularly in agricultural landscapes, where remaining habitat patches are often very small and highly isolated, mobile linkers as zoochorous seed dispersers are critical for the population dynamics of numerous plant species. However, knowledge about the quali‐ or quantification of such mobile link processes, especially in agricultural landscapes, is still limited. In a controlled feeding experiment, we recorded the seed intake and germination success after complete digestion by the European brown hare (Lepus europaeus) and explored its mobile link potential as an endozoochoric seed disperser. Utilizing a suite of common, rare, and potentially invasive plant species, we disentangled the effects of seed morphological traits on germination success while controlling for phylogenetic relatedness. Further, we measured the landscape connectivity via hares in two contrasting agricultural landscapes (simple: few natural and semi‐natural structures, large fields; complex: high amount of natural and semi‐natural structures, small fields) using GPS‐based movement data. With 34,710 seeds of 44 plant species fed, one of 200 seeds (0.51%) with seedlings of 33 species germinated from feces. Germination after complete digestion was positively related to denser seeds with comparatively small surface area and a relatively slender and elongated shape, suggesting that, for hares, the most critical seed characteristics for successful endozoochorous seed dispersal minimize exposure of the seed to the stomach and the associated digestive system. Furthermore, we could show that a hare's retention time is long enough to interconnect different habitats, especially grasslands and fields. Thus, besides other seed dispersal mechanisms, this most likely allows hares to act as effective mobile linkers contributing to ecosystem stability in times of agricultural intensification, not only in complex but also in simple landscapes.

Flexible movement kernel estimation in habitat selection analyses with generalized additive models

“…The effects of these features could be better explained by a non-linear smooth function. For instance, it is not plausible that temperature has a linear effect on acceleration of hares since it is natural to expect less movement at extreme temperatures (Stiegler et al 2023).…”

A predominantly diurnal tropical mammal increases nocturnality in response to high temperatures

“…A meta‐analysis of empirical data found that species that are strictly diurnal are much likelier than temporally flexible species to have already displayed range shifts or contractions in response to climate change (McCain & King, 2014), and metabolic niche modeling has indicated that small diurnal mammals are disproportionately likely to lose habitat due to future warming (Bonebrake et al., 2020). Species' behavioral responses to temperatures above their optimal range will be highly important in predicting future range shifts (Levy et al., 2019; Thurman et al., 2020), as well as changes to reproductive behaviors (Sharpe et al., 2019; Stiegler et al., 2023) and interspecific interactions (Traill et al., 2010). However, for many species, the impact of environmental temperatures on behavior remains unknown (Fuller et al., 2016; Levy et al., 2019).…”

Effects of endozoochory and diploendozoochory by captive wild mammals on Juniperus deppeana seeds

“…The passage of seeds through the digestive tract of the animal is a critical phase in endozoochory because the survival of seeds in the digestive system is one of the main determinants of the success of endozoochorous dispersal. Complex interactions are, therefore, established between the characteristics of the animals and plants for their survival in the digestive tract (Cosyns et al, 2005 ; Stiegler et al, 2021 ). To understand how mammalian handling and gut passage affect seeds; for example, viability and scarification, it is essential to conduct seed‐feeding experiments under controlled experimental conditions.…”

“…However, it is important to take into consideration that the variability that exists between plants and animals means that seed‐feeding experiments can present contrasting results, with greater germination success found in some cases (Grande et al, 2013 ; Mancilla‐Leytón et al, 2011 ) and lower success in others (D'hondt & Hoffmann, 2011 ; Grande et al, 2013 ). The potential for endozoochorous dispersal in many plant species has been evaluated using seed‐feeding experiments, particularly with herbivores (Poulsen et al, 2021 ; Sadeghayobi et al, 2011 ; Wang et al, 2017 ) such as domestic rabbits, sheep, and cows (Cosyns et al, 2005 ) or by the germination testing of collected scat samples (Milotić & Hoffmann, 2016 ; Salinas & Reynoso, 2023 ; Stiegler et al, 2021 ).…”