The best of two worlds: ecology and evolution of ambophilous plants

Abstract

Ambophily, the mixed mode of wind and insect pollination is still poorly understood, even though it has been known to science for over 130 years. While its presence has been repeatedly inferred, experimental data remain regrettably rare. No specific suite of morphological or ecological characteristics has yet been identified for ambophilous plants and their ecology and evolution remain uncertain. In this review we summarise and evaluate our current understanding of ambophily, primarily based on experimental studies. A total of 128 ambophilous speciesincluding several agriculturally important cropshave been reported from most major habitat types worldwide, but this probably represents only a small subset of ambophilous species. Ambophilous species have evolved both from wind-and insect-pollinated ancestors, with insectpollinated ancestors mostly representing pollination by small, generalist flower visitors. We compiled floral and reproductive traits for known ambophilous species and compared our results to traits of species pollinated either by wind or by small generalist insects only. Floral traits were found to be heterogeneous and strongly overlap especially with those of species pollinated by small generalist insects, which are also the prominent pollinator group for ambophilous plants. A few ambophilous species are only pollinated by specialised bees or beetles in addition to pollination by wind. The heterogeneity of floral traits and high similarity to generalist small insect-pollinated species lead us to conclude that ambophily is not a separate pollination syndrome but includes species belonging to different insect-as well as wind-pollination syndromes. Ambophily therefore should be regarded as a pollination mode. We found that a number of ecological factors promoted the evolution of ambophily, including avoidance of pollen limitation and self-pollination, spatial flower interference and population density. However, the individual ecological factors favouring the transition to ambophily vary among species depending on species distribution, habitat, population structure and reproductive system. Finally, a number of experimental studies in combination with observations of floral traits of living and fossil species and dated phylogenies may indicate evolutionary stability. In some clades ambophily has likely prevailed for millions of years, for example in the castanoid clade of the Fagaceae.

Insects pollinated flowering plants for most of angiosperm evolutionary history

“…Thorough pollination studies that explicitly test for cryptic pollination mechanisms including selfing and ambophily are still needed in many angiosperm families (Ollerton, 2017;Abrahamczyk et al, 2022a). Further pollination studies will enable us to more fully understand the diversity and macroevolutionary dynamics of pollination systems globally.…”

“…Though none of these traits are irreversible, the tightly correlated constellation of traits may be difficult to reverse all together to return to successful cross-pollination by animals. Ambophily may play a transitional role in such instances, though ambophily has evolved more frequently from insect than wind pollinated ancestors (Abrahamczyk et al ., 2022a). Where reversals from wind to animal pollination do occur, they typically involve a transition to generalist insect pollination (Barrett, 2013).…”

“…Moreover, our understanding of angiosperm pollination depends on the fundamental work of pollination ecologists to document complex and sometimes cryptic pollination systems. Thorough pollination studies that explicitly test for cryptic pollination mechanisms including selfing and ambophily are still needed in many angiosperm families (Ollerton, 2017; Abrahamczyk et al ., 2022a). Further pollination studies will enable us to more fully understand the diversity and macroevolutionary dynamics of pollination systems globally.…”

“…However, abiotic pollination by wind or water also occurs in many diverse plant lineages, and wind pollination is estimated to have evolved at least 65 times across the angiosperms (Linder, 1998; Ackerman, 2000). Combined pollination by animals and wind (ambophily) is also found in many unrelated lineages, and may be more common than currently reported as it is rarely tested for in pollination studies (Culley et al ., 2002; Abrahamczyk et al ., 2022a).…”

Pollination mode and reproductive system of Sanguisorba minor and Sanguisorba officinalis

“…Ambophily—regular pollination by insects and wind—is much more common among plant species with generalized pollination systems than previously expected (Abrahamczyk et al, 2022). Even though ambophily is not a homogeneous pollination syndrome, the flower traits of all ambophilous species permit pollen transfer by both wind and insects (summarized in Abrahamczyk et al, 2022).…”