Do benefits of seed dispersal and caching by scatterhoarders outweigh the costs of predation? An example with oaks and yellow‐necked mice

Abstract

Numerous interactions between plants and animals vary in their outcome between antagonism and mutualism. Interactions between plants and scatter‐hoarding animals provide a prime example of this phenomenon. Scatterhoarders consume large quantities of seeds (potentially reducing plant establishment), yet also disperse seeds and bury them in shallow caches (potentially improving recruitment). Despite intense work on mechanisms that cause these interactions to shift along an antagonism–mutualism continuum, it remains difficult to quantify their final outcomes. We demonstrate how readily available field data can be used to reach this goal, with interactions between rodents and two oaks species (sessile oak Quercus petraea, and red oak Q. rubra) as an empirical example. Our approach consists of quantifying the net outcome of the interaction through collecting data on different vital rates (e.g. probability that cached seeds survive to germination, probability of seedling recruitment with and without rodents; near and far from conspecific trees; with and without seed pilferage) and assembling them in a simple mathematical model. We found that during the period of the study, interactions between scatter‐hoarding rodents and both focal oaks were antagonistic. Even though caching increased the likelihood of seedling establishment, this effect was not strong enough to compensate for the costs of seed predation. Furthermore, there was no evidence that the short‐distance transportation that is usually provided by small mammals benefited early oak recruitment. Synthesis. Our empirical results demonstrated that certain common assumptions – that caching by rodents invariably benefits plant recruitment; that improved seedling establishment after seed burial is sufficient to make plant–scatterhoarder interactions mutualistic; that transportation away from maternal plants is highly beneficial—do not always hold and should be tested rather than taken for granted.

Past and present disturbances generate spatial variation in seed predation

“…Our findings that seed predation by S. hispidus is modified by past agricultural land use illustrate the potentially significant role of disturbance histories in determining the outcomes of these restoration efforts. Finally, while oak species in some ecosystems are able to overcome seed limitation by satiating predators through masting (Kelly 1994, Vander Wall 2001), vertebrate seed predation has been shown to limit oak recruitment in a variety of ecosystems (Santos and Telleria 1997, Gómez 2004, Sun et al 2004, Pé Rez‐Ramos and Marañon 2008, Cilles et al 2016, Bogdziewicz et al In press). Our results indicate that past and present disturbances that affect granivore behavior could subsequently determine when oaks may overcome seed limitation through masting.…”

On the need to evaluate costs and benefits of synzoochory for plant populations

“…The primary cost is seed predation, and its many possible benefits have been outlined by Moore and Dittel (2020); see also (Gómez, Schupp, & Jordano, 2019; Pesendorfer, Sillett, Koenig, & Morrison, 2016). We are pleased that Moore and Dittel found our recent article (Bogdziewicz, Crone, & Zwolak, 2020) thought‐provoking enough to motivate further development (Moore & Dittel, 2020). Here, we focus on the points in their commentary that were most thought‐provoking to us.…”

“…This idea is intuitively appealing, and we have in the past expressed it ourselves (e.g. Bogdziewicz, Crone, et al, 2020, 1st paragraph of introduction). However, upon reflection, we realize that this argument cannot be used to infer that a given interaction is mutualistic.…”

“…The original model included only effects of seed burial and consumption. Its modified version (Bogdziewicz, Crone, et al, 2020) incorporated the effects of seed pilferage. Moore and Dittel (2020) further extended our model by adding a negative density‐dependent effect that occurs when seeds are not dispersed by granivores.…”

“…First, benefits of seed transportation are often, but not always seen in synzoochorous and endozoochorous interactions (Fricke et al., 2013; Hirsch, Kays, Pereira, & Jansen, 2012). In the study that prompted this discussion (Bogdziewicz, Crone, et al, 2020), we directly tested for benefits of seed transportation by planting seeds at distances from 0 to 25 m from their parent plants. In one oak tree species ( Quercus petraea ), we found no effect of planting distance on seedling establishment.…”