Species’ range limits, when not caused by dispersal limitation, should generally reflect the limits of the ecological niche. In many species, niches and ranges seem to be limited by climatic factors such as temperature and precipitation (Sexton et al., 2009). Species’ distribution modelling (SDM) indicates that a handful of climate variables can often explain distribution limits rather well (e.g., Normand et al., 2009; Lee-Yaw et al., 2016). However, biotic interactions – possibly interacting with climate – have been considered less often in distribution modelling, and in the study of species’ distribution limits more generally (Sexton et al., 2009). Neglect of biotic interactions is not justified because empirical studies show that they affect species persistence. Examples include interspecific competitors (Jankowski et al., 2010; Stanton-Geddes et al., 2012), parasites and pathogens (Briers, 2003; Coates et al., 2017), and herbivores (Galen, 1990; Benning et al., 2019). Mutualistic interactions are also known to affect species persistence, especially in plant-pollinator systems (Stone and Jenkins, 2008; Chalcoff et al., 2012; Moeller et al., 2012). Here we explored the mechanisms by which pollinators may help determine range limits of a plant.
Pollinator service is especially important for plant persistence as 80% of all temperate-zone flowering plant species rely on animals for pollination (Ollerton et al., 2011). At range edges, reduced pollinator service might constrain the abundance of plants that rely on animals as pollen vectors for reproduction (Gaston, 2009). Indeed, population persistence is commonly reduced at range edges. A meta-analysis of transplant experiments, mostly on plants, across and beyond range limits revealed that lifetime performance declined beyond the range in 83% of studies (Hargreaves et al., 2014). The decline could be caused by a change in climatic conditions beyond the edge (Lee-Yaw et al., 2016), but biotic interactions such as a lack of suitable pollinators could also contribute to range limits. Variation in pollinator service across the distribution of plant species can be related to climatic conditions that favour the activity of pollinators (Chalcoff et al., 2012; Moeller et al., 2012), but pollinator services could also vary due to attractiveness and pollinator preferences. For example, as climatic conditions deteriorate toward range limits – possibly together with habitat availability or habitat quality – population census size, local flower density, flower attractiveness or the richness of flowering plant species may decrease. Below we discuss in detail the mechanisms potentially reducing pollinator service and their relation with plant species’ range limits.
One mechanism that may reduce pollinator service at a plant’s range edge is based on the observation that across the distribution of a species, abundance tends to decline toward the edges, presumably because habitat suitability decreases toward range edges (Brown, 1984). The so-called ‘abundant-center hypothesis’ is broadly supported by a recent study documenting a decline of both the density of populations and the density of individuals within populations from the centre to the edges of species’ distribution (Pironon et al., 2017). Lower regional and local densities of plants at range edges may also lower attractiveness to pollinators because pollinators commonly exhibit a preference for patches with a high density of flowering plants (reviewed by Ohashi and Yahara, 1999; Stone and Jenkins, 2008; Elliott and Irwin, 2009). This hypothesis describes an Allee effect (Courchamp et al., 1999), namely that pollinator service is lower in plant populations of small size and low density.
A second mechanism is reduced floral attractiveness at range edges. Animal-pollinated plants can sometimes enhance attractiveness to pollinators by producing more flowers per plant or larger flowers ( e.g., Klinkhamer and De Jong, 1990; Grindeland et al., 2005). However, investments in the floral display may be costly and hard to achieve if the environment is marginal and provides limited resources. Furthermore, plants of range edge populations often experience reduced individual performance from mutation accumulation due to genetic drift caused by past range expansion or long-term isolation (Willi et al., 2018; Willi and Van Buskirk, 2019; Perrier et al., 2020). Perrier et al. showed that a decline in performance of Arabidopsis lyrata at the range edge was caused by reduced flower production. Moreover, floral attractiveness may be lower at range edges because of a transition in the mating system from outcrossing to selfing (Morgan and Wilson, 2005; Moeller, 2006). Higher rates of self-compatibility and selfing have been noted in range-edge populations (e.g., Griffin and Willi, 2014), and this may be accompanied by changes in floral morphology such as a reduction in flower size (Darling et al., 2008; Dart et al., 2012). Hence, reduced attractiveness of flowers due to ecological or genetic causes may be another reason why pollinator service is low at range edges.
A third possible mechanism is related to the richness of flowering plant species and the diversity of resources offered to pollinators. Previous studies have reported a positive relationship between the diversity and abundance of pollinators and the diversity of flower types among co-occurring plants (e.g. Biesmeijer et al., 2006; Lázaro and Totland, 2010). The richness and abundance of other flowering plants increase the diversity of resources available to pollinators and therefore attract a broader diversity of insect visitors. If conditions at the edge of a species’ range become marginal for several plant species and the community is therefore less diverse, pollinator service may generally decline.
Finally, a fourth mechanism for reduced pollinator service at a plant’s range edge is that climatic conditions may be unsuitable for pollinator activity. As conditions are expected to become harsher toward the edges, guilds of pollinators that are to some extent specialized on a community of plants may also decline in abundance. It is well known that pollinator abundance and metabolic activity are highly affected by temperature (Herrera, 1990; Hillyer and Silman, 2010; Rader et al., 2012; Knop et al., 2018). It is reasonable to propose that an environmental gradient that limits plant populations may have similar consequences for the pollinator assembly (e.g., Battisti et al., 2006).
In this study, we tested whether pollinator service decreased toward the range edges of a plant species (research question I) and explored the mechanisms at play (research question II). Our study organism was the short-lived perennial Arabidopsis lyrata subsp. lyrata in North America, which has been the subject of ongoing research focusing on the ecological and evolutionary causes of distribution limits (Lee-Yaw et al., 2018; Willi et al., 2018, 2020; Perrier et al., 2020; Sánchez-Castro et al., 2021 unpublished data). We assessed daily visitation of flowers by pollinators in 13 populations across a latitudinal gradient of 1100km in the eastern United States, including replicate populations at the southern limit, centre of the range, and northern range limit. We quantified and identified pollinators using time-lapse cameras in each population, and tested the four mechanisms by relating pollinator data to population and site characteristics.