Opinion Flowering plants under global pollinator decline 1 2 2 1 Michel Thomann , Eric Imbert , Ce´ line Devaux , and Pierre-Olivier Cheptou 1 UMR 5175 CEFE, Centre d’Ecologie Fonctionnelle et Evolutive (CNRS), 1919 Route de Mende, F-34293 Montpellier Cedex 05, France 2 Institut des Sciences de l’Evolution de Montpellier, UMR 5554 CNRS, Universite´ de Montpellier II, CC 065, 34095 Montpellier Cedex 05, France There is now compelling evidence of a reduction of polli- lead to changes at the plant community level [12] through nator richness and density at a global scale. In this opinion ‘speciessorting’ thatexcludesthemostpollinator-dependent article, we argue that such pollinator decline intensifies species. Beyond plant community changes, we hypothesise pollen limitation and reduces plant reproductive success, that short-term adaptation of plant populations can take threatening natural populations of extinction. We use place and mitigate the impact of pollinator decline on plant genetic architecture and selection experiments on floral demography, possibly rescuing them from extinction. traits and evaluate the potential for plant reproductive In this opinion article, we investigate the potential for strategies to adapt rapidly to new pollination environ- plant reproductive strategies (including mating system ments. We propose that plant reproductive strategies and floral traits) to adapt to the current decline of their could adapt to the current pollinator decline by decreas- main pollinators. We use data describing (i) the effect of ing or increasing their reliance to pollinators, for example, pollinator abundance on seed set, (ii) the genetic architec- increasing autonomous selfing or reinforcing interactions ture, (iii) phenotypic selection on floral traits in natural with pollinators. We further discuss if and how adaptation populations, and (iv) the demographic effects of pollinator of plant reproductive strategies can buffer the demo- abundance. Confronting these scattered elements with graphic consequences of pollinator decline, and possibly theory of plant mating systems helps evaluate the poten- rescue plant populations from extinction. tial for contemporary evolution of plant reproductive strat- egies and determine whether it can buffer the detrimental Plant–pollinator interactions under pollinator decline effects of pollinator decline on plant demography. Insect pollination is a prevalent ecological process: more than 80% of wild plant species [1] and almost 75% of Effect of pollinator decline on plant reproductive cultivated plant species [2] rely on insects, particularly success wild bees, for fruit and seed production. Pollinator decline potentially has a major effect on plant As a facet of global changes, the recent decline of insect reproductive success. Studies of pollination and plant seed pollinator communities is currently a major concern [3], set along fragmentation gradients provide indirect evi- because of its impact on ecological and agricultural sys- dence that pollinator decline can exacerbate existing levels tems. Changes in anthropogenic land use and agricultural of pollen limitation (see Glossary) in natural populations intensification are considered as the main causes of current [13,14]. A meta-analysis comparing fragmented with pollinator decline [1]. Bees have experienced worldwide unfragmented habitats found that seed set reduction, reduction in species richness [4,5], functional composition due to fragmentation, is higher for self-incompatible spe- [6], and population density [7,8], a pattern that has in- cies than for self-compatible species [15], a pattern that can creased since the 1950s [9]. This global trend nevertheless be explained by reduced pollinator abundance rather than hides discrepancies among functional groups of bees, be- increased mate limitation. Moreover, decreased pollinator cause species with medium or long proboscis are the most richness and density, and associated reduced number of impacted [8]. The alteration of pollinator communities is likely to have cascading effects on plant population dynamics and thus on Glossary population persistence. Reduction of population densities of Autonomous selfing: within flower spontaneous selfing, that is, not necessitat- the endemic New Zealand shrub Rhabdothamnus solandri ing pollinator vectors. was shown to be linked to the rarefaction of its most efficient Evolutionary rescue: the recovering of sustainable population growth rate via adaptive changes. pollinators (birds in this case) [10]. Other studies have Geitonogamy: among flower selfing resulting from pollinator foraging shown a parallel decline of entomophilous plants and their behaviour within individual plants. pollinators [4,11], suggesting that pollinator decline can Inbreeding depression: the reduced fitness of offspring from related indivi- duals. In hermaphroditic individuals, inbreeding depression is classically estimated as the fitness reduction of selfed progeny relative to outcrossed Corresponding author: Cheptou, P-O. ([email protected]). progeny. Keywords: plant mating system; pollen limitation; adaptation; demography. Pollen limitation: the reduction of fruit or seed set due to limited pollen receipt. Reproductive assurance: the increase of seed set by selfing when outcrossed 1360-1385/$ – see front matter success is pollen limited. ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2013.04.002 Trends in Plant Science, July 2013, Vol. 18, No. 7 353 Opinion Trends in Plant Science July 2013, Vol. 18, No. 7 (A) 12 (B) 60 (C) 60 10 50 50 8 40 40 6 30 30 4 20 20 2 10 10 Wild bees per 15 min Seeds per plant (x100) Seeds per plant Seeds per plant (x100) Seeds per plant 0 0 0 0 100 400 900 1600 0 100 400 900 1600 0 4 8121620 Distance from nearest grassland (m) Distance from nearest grassland (m) Flower-vising bees per 15 min TRENDS in Plant Science Figure 1. Reduction of seed set associated with a reduction of pollinator visits along gradients of habitat isolation. Such spatial patterns provide surrogates for the effect of pollinator decline on plant seed set [1]. Increasing distance from natural habitats (i.e., increasing isolation) decreases the number of bees visiting the mustard plant, Sinapis arvensis (A), and results in a substantial decrease in plant seed set (B, C). Reproduced from [16]. pollinator visits, quantity of pollen receipt and seed set, are [21,22]. Therefore, we expect variation in pollen receipt to frequently observed with increasing isolation in fragmen- translate into larger variance in fitness among plants when ted landscapes [16–18] (Figure 1), even for generalist self- pollen limitation is stronger, for example, induced by polli- compatible plant species [19]. Similarly, populations of nator decline. anthropogenically disturbed habitats exhibit higher self- ing rates than those in undisturbed habitats, probably Two putative directions for plant reproductive because of a reduction of outcrossed pollen receipt [20]. strategies adaptation Disentangling the effect of pollinator limitation from mate Pollen limitation is a major ecological factor promoting the limitation is however difficult without additional informa- evolution of plant reproductive strategies [23]. At a con- tion, for example, on plant and pollinator densities. temporary time scale, we hypothesise two main evolution- Pollinator decline can magnify selection on floral traits ary scenarios under pollinator decline for plants whose involved in pollen transfer (Box 1), because the relationship reproductive success is mainly ensured by pollinators: between pollen receipt and seed set is usually saturating (i) evolution towards less reliance on pollinators by Box 1. Plant reproductive traits in two scenarios of adaptation Evolution towards autonomous selfing visitation rates comprise large corolla size (Figure IB), large floral Highly selfing species often share a suit of traits that constitute a selfing display (i.e., numerous flowers open simultaneously, Figure IC), syndrome. Specifically, traits associated with high autonomous selfing strong scent, and large rewards. When pollination is low and are low herkogamy (i.e., anther-stigma distance) and low dichogamy unpredictable, a longer individual flowering period is also expected. (i.e., temporal separation between mature anthers and mature stigmas, Less predictable adaptive changes could also include all traits Figure IA). Small flowers are also often associated with autonomous involved in attraction cues for pollinators (including floral colour), selfing. Similarly, shorter flower longevity, lower pollen:ovule ratio, pollen placement on pollinators body (positioning of fertile organs and smaller rewards could be selected along with the evolution of and floral design), and the adjustment of individual flowering time higher selfing rates. (mean and variance) with the activity of pollinators. Evolution towards reinforced interactions with pollinators Numerous traits are correlated to pollinator visitation rates and efficiency of pollen transfer. Floral traits associated with high (A) 0.9 (B) 1 (C) ) 3 0.8 0.9 -1 0.7 0.8 0.6 0.7 plant level 2 0.5 0.6 0.5 0.4 0.4 0.3 Selfing rate 1 0.3 flower level 0.2 0.2 0.1 Probability of bee visit 0.1 0 0 Pollinator visit rate (per h 0 00.20.40.60.8 1 < 12 12–14 14–16 16–18 > 18 2 4 816 Dichogamy index Floral diameter (mm) Floral display (number of flowers) TRENDS in Plant Science Figure I. Examples of relationships between several floral traits and plant reproductive