Staying in touch: how highly specialised moth pollinators track host plant phenology in unpredictable climates

Abstract

For pollinating insects that visit just a single flowering species, the co-occurrence of flowers and insects in time is likely to have critical implications for both plant and pollinator. Insects often utilise diapause to persist through periods in which resources are unavailable, timing their re-emergence by responding to the same environmental cues as their host plants. The obligate pollination mutualisms (OPMs) between Epicephala moths (Gracillariidae) and their leaf flower host plants are some of the most specialised interactions between plants and insects. However, to date there have been very few studies of Epicephala moth lifecycles and none of how they synchronise their activity with the flowering of their host plants. Breynia oblongifolia (Phyllanthaceae) is known to be exclusively pollinated by two highly specific species of Epicephala moth (Gracillariidae). We surveyed populations of both the host plant and its pollinators over multiple years to determine their annual phenology and then modelled the climatic factors that drive their activity. Using our newly gained knowledge of moth and host plant phenology, we then looked for evidence of diapause at both the egg and pre-pupal stages. Our phenology surveys showed that although female flowers were present throughout the entire year, the abundance of flowers and fruits was highly variable between sites and strongly associated with local rainfall and photoperiod. Fruit abundance, but not flower abundance, was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant flowers and emerge as fruits mature. Searches of overwintering flowers confirmed this, with many containing evidence of pollen and diapausing pollinators. We also observed the behaviour of adult Epicephala prior to pupation and found that ~10% of the Autumn emerging Epicephala enter diapause, eclosing to adulthood after 38-56 weeks. The remaining 90% of autumn emerging adults pupate directly with no diapause, suggesting a bet hedging strategy for adult emergence. As such, Epicephala moths appear to utilise diapause at multiple stages in their lifecycle, and possibly bet hedging, in order to deal with variable flowering phenology and climatic unpredictability.

Testing for apomixis in an obligate pollination mutualism

“…Although we found no evidence to support the existence of apomixis, we believe we may have identified other traits that act to reduce the likelihood of reproductive failure. Flowering and fruiting in B. oblongifolia is highly dependent on local rainfall (Finch et al 2021), which is highly variable in Australia (Nicholls et al 1997;Risbey et al 2009). Retaining pollinated flowers is likely to make B. oblongifolia much less vulnerable to fluctuations in rainfall by allowing Breynia to reproduce when environmental conditions are most suitable, regardless of the co-occurrence of its highly specific pollinators (Finch et al 2021).…”

“…1). Female flowers are present throughout the year, but male flowers are only present during the austral spring and summer (Finch et al 2021). Epicephala moth pollinators are active during the austral spring and summer but absent during the winter (June to September).…”

“…Many of the female flowers present during the winter contain deposited pollen that was likely deposited during the previous flowering season. However, it is unclear if these pollen grains are in fact viable, and hence further experimentation was required to confirm this (Finch et al 2021). Female flowers are pollinated by at least two species of Epicephala moth (Finch et al 2018(Finch et al , 2019.…”

“…However, up to a third of fruits contain no evidence of pollinators. Fruiting is variable between populations, occurring during the austral spring, summer and autumn in response to local rainfall and long duration photoperiods (Finch et al 2021).…”

“…The field site contains a remnant patch of Cumberland Plain Woodland, where a natural population of 200-300 B. oblongifolia forms a large component of the woodland understory. In August 2016, before the emergence of male flowers or pollinators (Finch et al 2021), we covered eight branches on each of 32 adult plants with fine nylon mesh exclusion bags. Plants > 1 m in height and > 3 m apart were chosen randomly by walking two pre-determined transects (N = 32).…”