Going to great lengths: selection for long corolla tubes in an extremely specialized bat–flower mutualism

Abstract

In a hypothesis that has remained controversial since its inception, Darwin suggested that long-tubed flowers and long-tongued pollinators evolved together in a coevolutionary race, with each selecting for increasing length in the other. Although the selective pressures that flowers impose on tongue length are relatively straightforward, in that longer tongues allow access to more nectar, selective pressures that pollinators impose on flower length are less clear. Here, we test for such selective pressures in the highly specialized mutualism between the nectar bat Anoura fistulata, which can extend its tongue twice as far as other nectar bats, and Centropogon nigricans, which has flowers of a similar length (8-9 cm). We used flight cage experiments to examine the effects of artificially manipulated flower lengths on (i) bat behaviour and (ii) pollen transfer. Increased length produced longer visits, but did not affect the force bats applied during visits. In the second experiment, flower length increased both the male and female components of flower function: long male flowers delivered more pollen grains and long female flowers received more pollen grains. However, pollen transfer was not correlated with visit duration, so the mechanism behind differences in pollen transfer remains unclear. By demonstrating that bats select for increasing flower length, these results are consistent with the hypothesis that A. fistulata evolved its remarkable tongue in a coevolutionary race with long-tubed flowers similar to that envisioned by Darwin.

Morphological specialization influences nectar extraction efficiency of sympatric nectar-feeding bats

“…Similar to the present experiments, these bats hovered longer at flowers with deeper nectar levels, probably in an attempt to extract nectar from almost empty flowers; thus, our experiments indeed reflect the natural behaviour of glossophagine bats. In flight cage pollination experiments, Muchhala and Thomson also found an increase in visit duration when bats were forced to visit longer flowers (Muchhala and Thomson, 2009). …”

The ecological role of extremely long-proboscid Neotropical butterflies (Lepidoptera: Hesperiidae) in plant-pollinator networks

“…Many scientists have pondered over the evolutionary processes that led to the development of particularly elongate proboscides in flower-visiting insects (Darwin 1862;Johnson 1997;Johnson and Anderson 2010;Muchhala and Thomson 2009;Nilsson 1988Nilsson , 1998Pauw et al 2009;Rodríguez-Gironés and Llandres 2008;Rodríguez-Gironés and Santamaría 2007;Wasserthal 1997Wasserthal , 1998Whittall and Hodges 2007). The most widely accepted hypothesis for the evolution of extreme mouthpart lengths is that they coevolved with long nectar spurs of angiosperms.…”

Geographic Variation in Flower Size and Flower-Visitor Composition of Two Bumblebee-Pollinated, Spring-Flowering Herbs, <i>Lamium album</i> L. var. <i>barbatum</i> (Lamiaceae) and <i>Meehania urticifolia</i> (Lamiaceae)

“…Moreover, bumblebees have been reported to visit these flowers (L. album [17] [27]; M. urticifolia [28] [29]). Many studies have shown that in long-tubed flower species, flower dimensions such as corolla length and corolla tube length are correlated with pollinator size [22] [30] [31]. However, nectar robbers sometimes seriously decrease the fitness of long-tubed flower species [32], and adaptive changes in flower traits to prevent nectar robbing have been reported in some plants [9] [11].…”