Variable nursery pollinator importance and its effect on plant reproductive success

Abstract

Nursery pollination, in which insects use as hosts the very plants they pollinate, ranges from obligate mutualism to parasitism. In the non-obligate interaction between Greya moths and the host Lithophragma sp., the relative density of nursery pollinators and copollinators, which do not use plant tissues for larval development, is a key determinant of the interaction's outcome. Silene (Caryophyllaceae) nursery pollination by Hadena moths (Lepidoptera: Noctuidae), studied primarily in Europe, is considered antagonistic because copollinators comprise a substantial proportion of the pollinator community. However, there are few studies that ascertain the direction of the Silene-Hadena interaction by taking into account both pollinator service and seed predation. Here, we report a novel comprehensive evaluation of the direction of the interaction between North American Hadena ectypa on Silene stellata, by comparing the relative contributions of nursery and copollinators to S. stellata pollination and relate this to variation in fruit predation and reproductive success of S. stellata across multiple sites and years. Hadena ectypa pollinator importance (pollen deposited/visit/h) varied between years, resulting from variable visitation rate. Copollinator importance was higher than H. ectypa in 1 year and equivalent in another. In two of three sites, lowered H. ectypa activity was not correlated with a significant decrease in plant reproductive success, indicating a negative interaction. Although pollinator service by H. ectypa is substantial in this system, copollinators' service is at least as great, and when the cost of fruit predation is factored in, the net effect of the interaction is parasitism of host plants.

Diversification through multitrait evolution in a coevolving interaction

“…Parasitism of flowers or seeds is common among insects, but many plant linages have flowers poorly suited to pollination by ovipositing insects (25). Interactions between some plant and insect lineages, such as Silene plants and Hadena moths, seem to remain at the interface between parasitism and mutualism; however, like Lithophragma and Greya, they may possibly vary in ecological outcome among populations (4,29). It is likely, though, that more plants are pollinated by floral parasites than is currently known.…”

“…Pollination by these floral parasites, sometimes called nursery pollination, involves reciprocally obligate interactions between a plant species and either one insect species or a small group of insect species within a lineage, potentially driven by selection imposed on the parasitic component of the interaction. Pollination by floral parasites has arisen and diversified repeatedly among plant lineages that are common components of terrestrial communities worldwide (4)(5)(6)(7)(8)(9). Examples include yuccas in North America, figs in tropical environments, globeflowers (Trollius; Ranunculaceae) in boreal ecosystems, and leafflower (Glochidion; Phyllanthaceae) trees in Asia and the Pacific islands (7,(10)(11)(12).…”

InvasiveSilene latifoliaMay Benefit from a Native Pollinating Seed Predator,Hadena ectypa, in North America

“…Hadena ectypa moths oviposit in S. stellata (N) flowers throughout the flower's lifetime, usually at the base of the ovary, on the ovary or nectary or inside surface of the calyx. In the field, larvae will eat ovules within flowers and seeds within developing fruits until they begin to harden and (due to their feeding requirements of 30-40 fruits under lab conditions) must move among flowers and fruits within plants, and possibly between plants, in order to complete development before diapause (Reynolds et al 2012). …”

“…Although H. ectypa adults avoided ovipositing on S. latifolia (I), the lack of larval feeding preference may result in negative impacts for S. latifolia (I). Since H. ectypa requires a large number of flowers/fruits (20-40 flowers/unhardened fruits under lab conditions; Reynolds et al 2012) to complete development, they must move within plants and may move between neighboring plants. As a result, when S. latifolia (I) co-occurs in close proximity to S. stellata (N), larvae might be able to reach and consume developing S. latifolia (I) fruit.…”

Do Flower Color and Floral Scent of Silene Species affect Host Preference of Hadena bicruris, a Seed-Eating Pollinator, under Field Conditions?

“…In non-obligate associations, unresolved evolutionary conflicts are expected: plants gain from attracting insects for pollination but suffer from seed predation or herbivory [5]. The plants' costs and benefits of interacting with nursery pollinators may further depend on the presence of co-pollinators and other herbivores [5]–[8].…”