Unclusterable, Underdispersed Arrangement of Insect-Pollinated Plants
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bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999169; this version posted September 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Herrera – 1 1 Unclusterable, underdispersed arrangement of insect-pollinated plants 2 in pollinator niche space 3 4 5 Carlos M. Herrera 1 6 Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avenida 7 Americo Vespucio 26, E-41092 Sevilla, Spain 8 9 Running head: Plant species in pollinator niche space 10 11 1 E-mail: [email protected] bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999169; this version posted September 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Herrera – 2 12 Abstract. Pollinators can mediate facilitative or competitive relationships between plant 13 species, but the comparative importance of these two conflicting phenomena in shaping 14 community-wide pollinator resource use remains unexplored. This paper examines the idea that 15 the arrangement in pollinator niche space of plant species samples comprising complete or 16 nearly complete regional or local plant communities can help to evaluate the relative importance 17 of facilitation and competition as drivers of community-wide pollinator resource use. Pollinator 18 composition data for insect-pollinated plants from the Sierra de Cazorla mountains (southeastern 19 Spain), comprising 85% of families and ~95% of widely distributed insect-pollinated species, 20 were used to address the following questions at regional (45 sites, 221 plant species) and local 21 (one site, 73 plant species) spatial scales: (1) Do objectively identifiable plant species clusters 22 occur in pollinator niche space ? Four different pollinator niche spaces were considered whose 23 axes were defined by insect orders, families, genera and species; and (2) If all plant species form 24 a single, indivisible cluster in pollinator niche space, Are they overdispersed or underdispersed 25 relative to a random arrangement ? “Clusterability” tests failed to reject the null hypothesis that 26 there was only one pollinator-defined plant species cluster in pollinator niche space, irrespective 27 of spatial scale, pollinator niche space or pollinator importance measurement (proportions of 28 pollinator individuals or flowers visited by each pollinator type). Observed means of pairwise 29 interspecific dissimilarity in pollinator composition were smaller than randomly simulated 30 values in the order-, family- and genus-defined pollinator niche spaces at both spatial scales, 31 thus revealing significantly non-random, underdispersed arrangement of plant species within the 32 single cluster existing in each of these pollinator niche spaces. In the undisturbed montane 33 habitats studied, arrangement of insect-pollinated plant species in pollinator niche space did not 34 support a major role for interspecific competition as a force shaping community-wide pollinator bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999169; this version posted September 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Herrera – 3 35 resource use by plants, but rather suggested a situation closer to the facilitation-dominated 36 extreme in a hypothetical competition-facilitation gradient. Results also highlight the 37 importance of investigations on complete or nearly complete insect-pollinated plant 38 communities for addressing novel hypotheses on the ecology and evolution of plant-pollinator 39 systems. 40 41 Key words:clusterability; Mediterranean mountain habitats; plant community; pollinator 42 composition; pollinator niche space; pollinator syndromes. 43 44 INTRODUCTION 45 The maturation of a full-fledged niche theory was a significant landmark in the trajectory of 46 twentieth-century ecology (Vandermeer 1972, Chase and Leibold 2003, Ricklefs 2012). 47 Originally aimed at investigating how many and how similar coexisting species could be in a 48 community, niche theory was predominantly concerned with animal communities and rested on 49 the overarching assumption that interspecific competition for limiting resources is a major 50 driving force in shaping community composition and resource use by individual species (Chase 51 and Leibold 2003). Notions derived from niche theory sometimes also made their way into plant 52 community studies. In particular, the niche theory framework is behind investigations of plant- 53 pollinator interactions that have envisaged animal pollinators as “resources” exploited by insect- 54 pollinated plants to ensure sexual reproduction, since competition for pollinators may result in 55 loss of pollinator visits (exploitation) and/or disruption of conspecific pollen flow (interference) 56 (Waser 1978, Pleasants 1980). In this context, pollinator partitioning over daily or seasonal 57 gradients (Herrera 1990, Stone et al. 1998, Aizen and Vázquez 2006, de Souza et al. 2017), bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999169; this version posted September 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Herrera – 4 58 generalization vs. specialization on pollinators as alternative strategies of resource use (Herrera 59 1996, 2005, Waser et al. 1996, Armbruster 2017), divergence in pollinator composition as a 60 mechanism alleviating interspecific competition (Moldenke 1975, Kephart 1983, Johnson 2010, 61 Bouman et al. 2016, Johnson and Bronstein 2019), or pollinator-mediated plant species 62 coexistence (Paw 2013, Benadi 2015, Benadi and Paw 2018), are all notions rooted in niche 63 theory that to a greater or lesser extent share the canonical assumption that competition is an 64 important driving force. 65 One insufficiently acknowledged limitation of the application of competition-laden niche 66 theory to plant-pollinator systems is that, under certain circumstances, pollinator sharing by 67 different plant species can result in facilitation rather than competition (Thomson 1978, Rathcke 68 1983, Callaway 1995). This possibility has been verified experimentally many times (see Braun 69 and Lortie 2019 for review). Proximate mechanisms leading to pollinator-mediated interspecific 70 facilitation include the “magnet species effect”, whereby plant species highly attractive to 71 pollinators can benefit co-flowering ones in the neighborhood that are visited less often (Laverty 72 1992, Johnson et al. 2003, Hansen et al. 2007, Molina-Montenegro et al. 2008, Pellegrino et al. 73 2016); sequential facilitation, whereby earlier-flowering plant species benefit later-flowering 74 ones at the same location by sustaining populations of site-faithful, shared pollinators (Waser 75 and Real 1979, Ogilvie and Thomson 2016); floral mimicry, in which plant species can derive 76 reproductive success when the colour, shape or scent of their flowers resemble those of a co- 77 blooming plant (Gumbert and Kunze 2001, Johnson et al. 2003, Pellegrino et al. 2008); and 78 diffuse beneficial effects of floral diversity at the plant community level on the pollination 79 success of individual species (Ghazoul 2006, Seifan et al. 2014, Norfolk et al. 2016). bioRxiv preprint doi: https://doi.org/10.1101/2020.03.19.999169; this version posted September 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Herrera – 5 80 While the reality of both facilitative and competitive phenomena in plant-pollinator systems 81 is well established, their comparative importance as drivers of pollinator resource use in natural 82 communities remain essentially unexplored to date (but see, e.g., Moeller 2004, Tur et al. 2016, 83 Eisen et al. 2019). The deleterious effect of interspecific pollen transfer due to pollinator sharing 84 has been traditionally interpreted as supporting a role of competition in organizing plant- 85 pollinator interactions by favoring pollinator partitioning (Stebbins 1970, Waser 1978, Wilson 86 and Thomson 1996, Morales and Traveset 2008, Mitchell et al. 2009), yet recent studies suggest 87 that some plant species can tolerate high levels of heterospecific pollen transfer without major 88 detrimental effects on reproduction (Arceo-Gómez et al. 2018, Fang et al. 2019, Ashman et al. 89 2020). The hitherto little-explored possibility thus remains that facilitative interactions among 90 animal-pollinated plants could also be significant drivers of plant-pollinator interactions at the 91 community level, since the net outcome of opposing facilitative and competitive forces will 92 depend on environmental context (Moeller 2004, Ghazoul 2006, Ye et al. 2014, Fitch 2017, 93 Eisen et al. 2019) and the benefits