Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator

Abstract

Background and aims: A deeper understanding of mutualism can be reached by studying systems with measurable costs and benefits. Most studies of this type focus on an unusual class of obligate, species-specific pollination mutualisms. The interaction between Datura wrightii (Solanaceae) and the hawkmoth Manduca sexta offers similar advantages but greater generality. Adult moths both nectar at and deposit eggs on the same plant; larvae are herbivorous. The antagonistic component of this interaction has been well studied. Here the role of M. sexta as a pollinator of D. wrightii, particularly in the context of this moth's frequent nectaring visits to the bat-pollinated plant Agave palmeri, is documented.

Methods: Hand-pollinations were used to determine breeding system and the reproductive consequences of mixed loads of A. palmeri and D. wrightii pollen. Plants and moths were caged overnight to assess whether nectaring visits led to fruit and seed set. Finally, pollen deposited on field-collected stigmas was identified, with a particular focus on documenting the presence of D. wrightii and A. palmeri grains.

Key results: Datura wrightii is highly self-compatible, and a visit that deposits either outcross or self pollen almost doubles fruit and seed set compared with unvisited flowers. Manduca sexta transferred enough pollen to produce fruit and seed sets comparable to hand-pollination treatments. Agave palmeri did not interfere with D. wrightii success: in the field, stigmas received almost pure D. wrightii pollen, and hand-addition of large quantities of A. palmeri pollen had no measurable effect on fruit and seed set.

Conclusions: The floral visitation component of the D. wrightii-M. sexta interaction is indeed mutualistic. This finding is essential background to future development of this interaction as a model system for studying mutualism's costs and benefits. It is already proving valuable for dissecting third-species effects on the outcome of mutualism. Results indicate that M. sexta's heavy visitation to A. palmeri has no negative effect on the benefits conferred to D. wrightii. However, it can be predicted to augment M. sexta populations to the point where the costs of the interaction begin to exceed its benefits.

Fig. 1.

Reproductive success from hand-pollination and caged moth pollination experiments. (A) Fruit set, i.e. the percentage of flowers in that pollination treatment that set fruit. Fruit set from autonomous self-pollination was significantly lower than other treatments, which did not differ significantly from each other (see text). (B) Mean (± s.e.m.) seed set per maturing fruit. Seed set from autonomous self-pollination was significantly lower than other treatments; moth hand-pollination resulted in lower seed set than did hand self-pollination, but other treatments did not differ significantly from each other (see text). Abbreviations: aut SP, autonomous self-pollination, from unmanipulated flowers; hand OP, hand outcross-pollination, i.e. from emasculated flowers on which pollen from other plants had been actively deposited; hand SP, hand self-pollination, i.e. from flowers on which pollen from other flowers the same plant had been actively deposited; moth OP, moth outcross-pollination, i.e. from emasculated flowers exposed overnight to Manduca sexta in a cage with flowers on other plants; moth SP, moth hand-pollination, i.e. from flowers exposed overnight to M. sexta in a cage with only that plant present.

Fig. 2.

Reproductive success of hand-pollinated flowers that were and were not augmented with Agave palmeri pollen. Addition of A. palmeri pollen had no effect on fruit set (A) or mean (± s.e.m.) seed set per fruit (B). In contrast, as in the earlier experiment whose results are shown in Fig. 1, flowers receiving outcross pollen set significantly more fruits and seeds per fruit than those that were autonomously pollinated. Abbreviations: aut SP, autonomous self-pollination, from unmanipulated flowers; hand OP, hand outcross-pollination, i.e. from flowers on which pollen from other plants had been actively deposited; aut SP + Agave, flowers on which A. palmeri pollen alone was actively deposited; hand OP + Agave, emasculated flowers to which both outcross D. wrightii and A. palmeri pollen were actively deposited.