Batesian mimicry in plants: The significance of shared leaf shape between Alseuosmia pusilla and Pseudowintera colorata

<p>There is an immense amount of variation in leaf shape, size, and colouration, both across and within plant species. Leaf shape and colour, in some instances, can be attributed as a physiological response to particular abiotic stressors. However, leaf shape, size, and colour are used by herbivores to identify sources of palatable foliage for food. It is possible, therefore, that an undefended plant might gain protection from herbivores by matching leaf characteristics of a chemically defended species. The matching of defensive signals by an undefended species in order to dupe a predator is known as Batesian mimicry, and whilst believed to be a relatively common phenomenon amongst animals, it has yet to be proven in plants. The foliage of Alseuosmia pusilla (Colenso) A. Cunningham, is strikingly similar to the human eye to that of Pseudowintera colorata (Raoul) Dandy, an unrelated sympatric species found in New Zealand. Unlike the foliage of A. pusilla, that of P. colorata contains a number of secondary metabolites associated with herbivore defence, including a sesquiterpene dialdehyde known as polygodial, a known potent insect antifeedant that imparts a pungent peppery taste when eaten. It has been hypothesised that this similarity evolved under browsing pressure from nine species of large extinct herbivorous birds, collectively known as moa. Whilst moa became extinct soon after the arrival of humans, the large herbivore guild has been effectively replaced by a range of introduced mammalian herbivores including several species of deer, though to what degree remains controversial. In chapter two, I established a robust spatially explicit morphometric analysis method to test how similar the leaves of A. pusilla and P. colorata leaves were, and whether leaf shape was a distinctive trait within their shared habitat. Using the Cartesian coordinates of leaf margins as descriptors of leaf shape, I found that P. colorata leaves were morphologically distinct from all of the neighbouring species except for those of A. pusilla. A. pusilla individuals were more similar to neighbouring than to distant P. colorata, and 90% of leaf shape variation in the two species varied similarly across an elevational gradient. The data are consistent with Batesian mimicry, wherein the conspicuous characteristic of a defended model is replicated by an undefended mimic across its entire growing range. In chapter three, I tested how leaf shape variation within, and between, A. pusilla and P. colorata responded when exposed to high levels of mammalian herbivory. I demonstrated that in a forest population of P. colorata and A. pusilla exposed to high mammalian herbivory pressure, leaf shape variation is reduced in both focal species, but not in other sympatric species. This is consistent with Batesian mimicry, wherein increased herbivory pressure selects for a stronger signal in the distinctive characteristic of the defended plant, and through the selection for mimicry, variation in the mimic’s phenotype converges on the model’s phenotype. Additionally, when alternative palatable food is preferentially targeted, P. colorata increased in abundance along with a proportionate increase in A. pusilla’s abundance. Invertebrate herbivory was estimated to be similar on both species at both sites. In chapter four, I tested the hypothesis that A. pusilla is a Batesian mimic of P. colorata using farmed red deer (Cervus elaphus scoticus) in feeding trials. The deer found A. pusilla more palatable than P. colorata, and after eating a P. colorata individual, they became reluctant to eat another plant. Although the two plants differ significantly in volatile organic compound emissions, deer were equally likely to first eat an A. pusilla as they were a P. colorata, therefore were unable to use olfactory cues, or visually differentiate between the two species. As the relative abundance of P. colorata increased, herbivory damage was lower, both in the defended P. colorata and in the undefended A. pusilla. This study provides the first unequivocal proof of defensive Batesian mimicry in plants. In chapter five, using humans as surrogate herbivores, I tested how leaf shape and colour can be used as cues or signals by herbivores when foraging for food under different conditions. Subjects found leaf size a distracting characteristic, foraging more effectively when A. pusilla and P. colorata individuals were most similar in 94% of their shared shape variation. The trait of leaf colour, whilst unreliable by itself, acted to potentiate the trait of leaf shape, as a signal or cue. Fast feedback on species palatability improved accuracy in identifying A. pusilla, but neither fast nor slow feedback improved discriminability of P. colorata. A. pusilla leaves were harder to discriminate when presented on a “disruptive” backdrop. My results demonstrate that leaf shape can act as a signal or cue. These results indicate why further research into plant-herbivore communication is important and that it could provide powerful insights into the functional significance of leaf morphology. This thesis provides a significant contribution to our understanding of how leaves function as signals or cues to herbivores in three ways: (i) it provides the first detailed and powerful quantitative evidence of leaf shape matching between two species, and demonstrates the importance of using a spatially explicit morphometric method when investigating leaf shape; (ii) it is the first to unequivocally prove defensive Batesian mimicry in plants; and (iii) it demonstrates that leaf traits can act as signals or cues.</p>

Batesian mimicry in plants: The significance of shared leaf shape between Alseuosmia pusilla and Pseudowintera colorata

<p>There is an immense amount of variation in leaf shape, size, and colouration, both across and within plant species. Leaf shape and colour, in some instances, can be attributed as a physiological response to particular abiotic stressors. However, leaf shape, size, and colour are used by herbivores to identify sources of palatable foliage for food. It is possible, therefore, that an undefended plant might gain protection from herbivores by matching leaf characteristics of a chemically defended species. The matching of defensive signals by an undefended species in order to dupe a predator is known as Batesian mimicry, and whilst believed to be a relatively common phenomenon amongst animals, it has yet to be proven in plants. The foliage of Alseuosmia pusilla (Colenso) A. Cunningham, is strikingly similar to the human eye to that of Pseudowintera colorata (Raoul) Dandy, an unrelated sympatric species found in New Zealand. Unlike the foliage of A. pusilla, that of P. colorata contains a number of secondary metabolites associated with herbivore defence, including a sesquiterpene dialdehyde known as polygodial, a known potent insect antifeedant that imparts a pungent peppery taste when eaten. It has been hypothesised that this similarity evolved under browsing pressure from nine species of large extinct herbivorous birds, collectively known as moa. Whilst moa became extinct soon after the arrival of humans, the large herbivore guild has been effectively replaced by a range of introduced mammalian herbivores including several species of deer, though to what degree remains controversial. In chapter two, I established a robust spatially explicit morphometric analysis method to test how similar the leaves of A. pusilla and P. colorata leaves were, and whether leaf shape was a distinctive trait within their shared habitat. Using the Cartesian coordinates of leaf margins as descriptors of leaf shape, I found that P. colorata leaves were morphologically distinct from all of the neighbouring species except for those of A. pusilla. A. pusilla individuals were more similar to neighbouring than to distant P. colorata, and 90% of leaf shape variation in the two species varied similarly across an elevational gradient. The data are consistent with Batesian mimicry, wherein the conspicuous characteristic of a defended model is replicated by an undefended mimic across its entire growing range. In chapter three, I tested how leaf shape variation within, and between, A. pusilla and P. colorata responded when exposed to high levels of mammalian herbivory. I demonstrated that in a forest population of P. colorata and A. pusilla exposed to high mammalian herbivory pressure, leaf shape variation is reduced in both focal species, but not in other sympatric species. This is consistent with Batesian mimicry, wherein increased herbivory pressure selects for a stronger signal in the distinctive characteristic of the defended plant, and through the selection for mimicry, variation in the mimic’s phenotype converges on the model’s phenotype. Additionally, when alternative palatable food is preferentially targeted, P. colorata increased in abundance along with a proportionate increase in A. pusilla’s abundance. Invertebrate herbivory was estimated to be similar on both species at both sites. In chapter four, I tested the hypothesis that A. pusilla is a Batesian mimic of P. colorata using farmed red deer (Cervus elaphus scoticus) in feeding trials. The deer found A. pusilla more palatable than P. colorata, and after eating a P. colorata individual, they became reluctant to eat another plant. Although the two plants differ significantly in volatile organic compound emissions, deer were equally likely to first eat an A. pusilla as they were a P. colorata, therefore were unable to use olfactory cues, or visually differentiate between the two species. As the relative abundance of P. colorata increased, herbivory damage was lower, both in the defended P. colorata and in the undefended A. pusilla. This study provides the first unequivocal proof of defensive Batesian mimicry in plants. In chapter five, using humans as surrogate herbivores, I tested how leaf shape and colour can be used as cues or signals by herbivores when foraging for food under different conditions. Subjects found leaf size a distracting characteristic, foraging more effectively when A. pusilla and P. colorata individuals were most similar in 94% of their shared shape variation. The trait of leaf colour, whilst unreliable by itself, acted to potentiate the trait of leaf shape, as a signal or cue. Fast feedback on species palatability improved accuracy in identifying A. pusilla, but neither fast nor slow feedback improved discriminability of P. colorata. A. pusilla leaves were harder to discriminate when presented on a “disruptive” backdrop. My results demonstrate that leaf shape can act as a signal or cue. These results indicate why further research into plant-herbivore communication is important and that it could provide powerful insights into the functional significance of leaf morphology. This thesis provides a significant contribution to our understanding of how leaves function as signals or cues to herbivores in three ways: (i) it provides the first detailed and powerful quantitative evidence of leaf shape matching between two species, and demonstrates the importance of using a spatially explicit morphometric method when investigating leaf shape; (ii) it is the first to unequivocally prove defensive Batesian mimicry in plants; and (iii) it demonstrates that leaf traits can act as signals or cues.</p>

Mammalian herbivory in post-fire chaparral impacts herbaceous composition but not N and C cycling

Aims Classical theory predicts that herbivores impact herb assemblages and soil nitrogen (N) cycling through selective plant consumption and the deposition of N-rich waste, with effects dependent upon ecosystem N availability. Herbivores are predicted to accelerate N cycling when N availability is high and decelerate cycling when availability is low. However, experimental tests of these theories in natural systems are limited and have yielded contradictory results. California’s widespread chaparral shrublands provide a tractable system in which to test these theories. They are prone to periodic crown-fire, which temporarily removes living shrub cover, deposits mineral N on soils, and allows diverse herbaceous assemblages to dominate the landscape for 3-5 years. Chaparral is also increasingly vulnerable to herbaceous invasion; mammalian herbivory may limit the establishment of non-native herbs in the shrub understory. Methods We implemented a two-year herbivore-exclosure experiment (Hopland, California) to assess the impact of mammalian herbivory during early post-fire chaparral succession, both on herbaceous plant assemblages and soil N and C cycling. We predicted that, in high-N post-fire conditions, mammalian herbivory would not demonstrate a strong preference for N-fixing herbs, would accelerate N cycling, and would reduce the abundance of non-native herbs. Important Findings Excluding mammalian herbivores increased herb standing biomass by 54%, but changed neither the relative abundance of N-fixing vs. non-N-fixing herbs nor any measure of N or C cycling. Herbivore impacts on nutrient cycling may not be significant over the two-year time scale of the experiment and physical effects of herbivore activity could have counteracted the influence of plant litter and animal dung/urine inputs. Mammalian herbivores concentrated their feeding on typical non-native herbs, slightly decreasing their relative abundance; however, mammalian herbivory was not sufficient to stem the invasion of chaparral by invasive herbs or alter C and N cycling over the first two years after fire.

Competing consumers: contrasting the patterns and impacts of fire and mammalian herbivory in Africa

Fire and herbivory are the two consumers of above-ground biomass globally. They have contrasting impacts as they differ in terms of selectivity and temporal occurrence. Here, we integrate continental-scale data on fire and herbivory in Africa to explore (i) how environmental drivers constrain these two consumers and (ii) the degree to which each consumer affects the other. Environments conducive to mammalian herbivory are not necessarily the same as those conducive to fire, although their spheres of influence do overlap—especially in grassy ecosystems which are known for their frequent fires and abundance of large mammalian herbivores. Interactions between fire and herbivory can be competitive, facultative or antagonistic, and we explore this with reference to the potential for alternative ecosystem states. Although fire removes orders of magnitude more biomass than herbivory their methane emissions are very similar, and in the past, herbivores probably emitted more methane than fire. We contrast the type of herbivory and fire in different ecosystems to define ‘consumer-realms’. This article is part of the themed issue ‘Tropical grassy biomes: linking ecology, human use and conservation’.