Creeping ‘Fruitless Falls’: Reproductive Failure in Heterostylous Plants in Fragmented Landscapes

Abstract

In recent years, increasing instances of ‘fruitless falls’, i.e., seed set failure of flowering plants, have been appreciated for both cultivated and wild plants. Species having a sophisticated entomophilous breeding system such as heterostyly are likely to be most vulnerable to the detrimental effects of pollinator loss, resulting in fruitless falls through compatible pollen limitation. Our studies on pollination and seed set in wild populations of heterostylous species, Primula sieboldii, P. kisoana and Persicaria japonica, and a few remaining populations of a highly endangered monomorphic species Crepidiastrum ameristophyllum suggested that fruitless falls have been already rather common among wild plants in present-day fragmented landscapes. Serious effects of pollinator loss have been recognized for a Primula sieboldii population in a small nature reserve in the floodplain of the Arakawa River, which is an ‘insular habitat’ surrounded by the urbanized area of Greater Tokyo. Fertility of the rare short-homostyle far surpasses those of normal heterostylous morphs, of which fertility is severely limited by pollinator availability. Model simulation predicts the possibility of a large loss of genetic variation within a few generations under the present strong fertility selection for the homostyle. For small populations or isolated individuals in fragmented habitats, reduced opportunity for mating, i.e., one typical form of the Allee effects, is another major cause of seed set failure. Among 20 populations of P. sieboldii investigated in southern Hokkaido, only a negligible number of seeds were set in smaller populations consisting of less than four genets, while in larger populations, population mean seed set depended strongly on pollinator availability which can be assessed by craw marks left on the flower petals by effective pollinator queen bumblebees. Seed set failure due to reduced opportunity for mating because of solitude was also demonstrated for isolated genets or smaller populations of other heterostylous species, Primula kisoana and Persicaria japonica in highly fragmented deciduous forests and moist tall grasslands, respectively. We also demonstrated the detrimental effects of isolation, i.e., absence of mating partners, in a highly endangered homomorphic species, Crepidiastrum ameristophyllum endemic to the Bonin Islands. Fruitless falls ascribed to the Allee effects are likely to be already ubiquitous among wild plants subjected to habitat fragmentation or other threats to biodiversity. Habitat and/or population restoration and ‘pollinator therapy’ management based on sound population and reproductive ecology are urgently required to strive against fruitless falls.