Volume 107, Issue 6 p. 845-847
News & Views
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Is heterospecific pollen receipt the missing link in understanding pollen limitation of plant reproduction?

Tia-Lynn Ashman

Corresponding Author

Tia-Lynn Ashman

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA

Author for correspondence (e-mail: [email protected])Search for more papers by this author
Gerardo Arceo-Gómez

Gerardo Arceo-Gómez

Department of Biological Sciences, East Tennessee State University, Johnson City, TN, USA

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Joanne M. Bennett

Joanne M. Bennett

Institute of Biology, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, 06108 Halle (Saale), Germany

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

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Tiffany M. Knight

Tiffany M. Knight

Institute of Biology, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, 06108 Halle (Saale), Germany

Department of Community Ecology, Helmholtz Centre for Environmental Research – UFZ, Theodor-Lieser-Straße 4, 06120 Halle(Saale), Germany

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

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First published: 23 May 2020
Citations: 19

How will anthropogenic changes (species invasions/extinctions, land-use conversion, and climate change) influence the pollination and reproductive success of the world's angiosperms, 85% of which require animal pollination (Ollerton et al., 2011)? Answering this question requires understanding the mechanisms that cause pollen limitation of seed production. Pollen limitation (PL) is widespread (Bennett et al., 2018) and occurs when pollinators fail to deliver adequate quantity or quality of pollen to stigmas (Ashman et al., 2004). It is thought to primarily occur when there are few pollinators visiting the plants or when the pollinators that visit do not bring enough conspecific pollen (CP) or bring CP that is of low quality (e.g., self pollen that comes from a different flowers on the same plant) (Ashman et al., 2004; Aizen and Harder, 2007). Often left out of the conversation on PL, however, is that pollinators can also transfer heterospecific pollen (HP) among species (but see Jakobsson et al., 2009; McKinney and Goodell, 2010).

Studies of HP receipt on stigmas collected late in anthesis demonstrate that almost all plants (88%) receive at least some HP, and when they do, it can make up to 75% of the total stigmatic pollen load (Ashman and Arceo-Gómez, 2013; Arceo-Gómez et al., 2019). The HP deposited on stigmas can interfere with CP tube growth and reduce CP germination and fertilization (Morales and Traveset, 2008), though the effects can vary widely (Ashman and Arceo-Gómez, 2013). Thus, HP can be viewed as the lowest quality pollen that a flower might receive as it cannot result in legitimate seed production and can even reduce seed set. Moreover, if there is a trade off between HP and CP transport on pollinators’ bodies, greater HP transfer can lead to deposition of fewer CP on a conspecific stigma (e.g., Moreira-Hernández and Muchhala, 2018). Anthropogenic environmental changes may influence PL through changes in the quantity and quality of CP, as well as the quantity (and identity) of HP delivered by pollinators. Predicting which plant species will be most vulnerable to PL in the future requires an understanding of both these mechanisms.

Traditional means to measure PL involve randomly assigning flowers to open, naturally pollinated (control) and hand-pollinated (supplemental) treatments, and subsequently measuring the degree to which reproductive success is increased in the supplement treatment (Bennett et al., 2018). Because the pollen supplementation treatment is applied to stigmas that are also open to natural pollination (Ashman et al., 2004; Bennett et al., 2018), these stigmas may have previously received or may subsequently receive both CP and HP. There are several ways that HP could affect estimates of PL. First, higher reproductive success in the supplement treatment, which indicates PL, could be due not to insufficient CP but rather due to strong HP interference in the open flowers (not supplemented); the CP supplement treatment increases the ratio of CP to HP and thus decreases the importance of HP interference (Fig. 1A). Another possibility is that the higher reproductive success in the supplement treatment could be due to the supplemental CP (in recently opened flowers) preventing subsequent HP deposition/adherence, which may be common in open flowers that are not supplemented with CP (Fig. 1B). Last, some researchers measure PL by comparing flowers of open-pollinated plants to those that are hand-outcrossed and then bagged to prevent pollinator visitation (Bennett et al., 2018; Fig. 1C). In the extreme case in these experiments, the open treatment might have both HP and low-quality CP compared to the supplement treatment, which only receives the high-quality CP given in the treatment (the bagging prevents anything else from arriving on the stigma). It is worth noting that even these scenarios oversimplify the dynamics of natural pollen transfer. Nevertheless, they still reveal the potential complexity of interspecific pollen interactions on the stigma (between CP and HP) that result from pollen transport on pollinator bodies (Arceo-Gómez and Ashman, 2011; Minnaar et al., 2018) and that can impact PL.

Details are in the caption following the image
Flow diagram showing how both conspecific (CP; blue symbols) and heterospecific (HP; orange symbols) pollen receipt could affect pollen limitation when comparing seed production after natural pollination to that from supplementation pollination where (A) supplemental pollen is added late, (B) supplemental pollen is added early, or (C) only high-quality (large symbols) outcrossed pollen is added to a flower that is then bagged to exclude pollinators.

A common thought is that plants evolve to reduce PL and that PL is evidence of a contemporary disruption from their evolutionarily stable optima allocation strategy, perhaps owing to loss of pollinators and reduced delivery of high-quality CP (reviewed by Ashman et al., 2004). Indeed, anthropogenic changes can cause severe PL, especially for pollinator-dependent species (Burns et al., 2019; J. M. Bennett et al., unpublished manuscript). However, we do not know the degree to which the evidence of PL due to anthropogenic change reflects reduced CP quantity, reduced CP quality, and/or increased HP receipt. An indication that increased HP receipt might play an important role in PL comes from the fact that conditions where PL is high are also the regions where HP transfer is observed to be high (e.g., biodiversity hotspots; Alonso et al., 2010; Arceo-Gómez et al., 2019) or expected to be high (urban or heavily invaded habitats; Johnson et al., 2019; J. M. Bennett et al., unpublished manuscript). If anthropogenic factors that reduce CP also lead to increased HP, e.g., loss of specialist pollinators and replacement by generalists (Johnson et al., 2019), then both processes may be acting in concert to reduce plant reproductive success, but without studying both aspects of pollen transfer we cannot know for certain.

Unfortunately, we find that despite the abundance of studies on plant reproductive ecology (Knight et al., 2018), there is a scarcity of cross talk between research on these two aspects of pollination. We recently reviewed, at a global scale, studies quantifying PL (1249 plant species from 927 studies; Bennett et al., 2018) and quantifying HP receipt (245 species from 26 studies; Arceo-Gómez et al., 2019) and found when combining these data sets, measures of both entities are available for less than 1% of the plant species (Fig. 2). For these species, a few studies have measured both PL and HP receipt (Jakobsson et al., 2009; Montgomery, 2009; McKinney and Goodell, 2010), but only one study directly correlated HP receipt on PL (Waites and Agren, 2004). In comparing multiple populations of Lythrum salicaria, Waites and Agren (2004) found PL decreased with number of CP grains received but found no relation with number of HP grains.

Details are in the caption following the image
Venn diagram showing the number of published studies and species in which pollen limitation (PL) or heterospecific pollen (HP) has been measured and the overlap where both were measured. Based on two recent meta-analyses, PL was measured in 1249 species from 927 published studies (orange) between 1981 and 2015 (Bennett et al., 2018), HP was measured in 245 species from 26 studies (blue) between 1986 and 2017 (Arceo-Gómez et al., 2019), while only six species from four published studies measured both PL and HP.

The shortage of studies precludes a general test of the effect of HP receipt on PL or whether the HP effect depends on CP receipt or functional plant traits (e.g., anther or stigma placement) that modify HP receipt (i.e., reduce it), yet both warrant study because together they inform more fully on the biological mechanisms of PL. For instance, specialists (those pollinated by a single species or with restrictive morphologies) are the most pollen limited (J. M. Bennett et al., unpublished manuscript), but they are also expected to have the lowest HP (Arceo-Gómez et al., 2016, 2019), so in these species PL is predicted to be related to low CP rather than high HP. In contrast, generalists (pollinated by multiple species, or with permissive morphologies) are less pollen limited (J. M. Bennett et al., unpublished manuscript), but have the greatest HP (Arceo-Gómez et al., 2016, 2019), suggesting that they may have high CP and HP (unless CP delivery trades off with HP delivery). Thus, in these species, PL is predicted to be related to high HP rather than low CP. We acknowledge, however, that mechanisms to tolerate HP receipt (see Ashman and Arceo-Gómez, 2013) may also exist and modify its effect on seed set.

In conclusion, determining whether conspecific and/or heterospecific pollen receipt lead to PL under anthropogenic change or contribute to variation in PL among plant species or phenotypes will require a pluralistic approach. To this end, we advocate for research that combines characterization of HP receipt when conducting supplemental pollinations to assess PL. It should include a characterization of both HP and CP on the stigmas of open-pollinated and pollen-supplemented plants to determine the potential contribution of HP receipt to PL. In addition, varying the timing of supplementation can be used to directly assess the impact of HP in the supplemented treatment (Fig. 1A, B). Furthermore, combining data on pollen transfer networks (i.e., amounts and identities of HP received) along with pollen supplementation studies of coflowering community members will provide insight into how pollinator-mediated interspecific relationships contribute to PL variation within natural communities. Finally, hand pollinations can include different size loads of CP and HP and varying HP identity (see Arceo-Gómez and Ashman, 2011) to identify specific effectors and their interactions. These data combinations will reveal the relative contribution of lower CP quantity and greater HP receipt to PL, and how each varies with plant traits and ecological factors. This mechanistic detail is increasingly important as different anthropogenic changes (species invasions/extinctions, land-use conversion and climate change) may disrupt different underlying mechanisms of PL and do so differently across species. For instance, loss of specialist pollinators and rise of super generalists may lead to greater amounts of HP transfer (or from different HP donors than in the past; Johnson et al., 2019), and both HP donor identity and amount can affect reproductive success (Arceo-Gómez and Ashman, 2011). Understanding these mechanisms will ultimately allow for more informed understanding of the drivers of PL as a result of anthropogenic change and lead to more effective plant conservation strategies. Further, because both HP and PL can determine species population growth and coexistence (Ashman et al., 2004; Ashman and Arceo-Gómez, 2013; Schreiber et al., 2019), they may jointly be key to larger-scale patterns of plant abundance and distribution.

Acknowledgments

Logistical support was provided by NSF DEB1452386, University of Pittsburgh Dietrich School of Arts and Sciences and a Helmholtz Association International Fellowship to T.-L.A, ETSU RDC grant to G.A.G., the Alexander von Humboldt Foundation as part of the Alexander von Humboldt Professorship of T.M.K., by the Helmholtz Association as part of the Helmholtz Recruitment Initiative to T.M.K. and a working group grant sPLAT from the Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118). The authors thank two anonymous reviewers and P. Diggle for comments that improved the manuscript.