Tall herb herbivory resistance reflects historic exposure to leaf beetles in a boreal archipelago age-gradient

In this paper, we introduce the coevolution-by-coexistence hypothesis which predicts that the strength of a coevolutionary adaptation will become increasingly apparent as long as the corresponding selection from an interacting counterpart continues. Hence, evolutionary interactions between plants and their herbivores can be studied by comparing discrete plant populations with known history of herbivore colonization. We studied populations of the host plant, Filipendula ulmaria (meadow sweet), on six islands, in a Bothnian archipelago subject to isostatic rebound, that represent a spatio-temporal gradient of coexistence with its two major herbivores, the specialist leaf beetles Galerucella tenella and Altica engstroemi. Regression analyses showed that a number of traits important for insect-plant interactions (leaf concentrations of individual phenolics and condensed tannins, plant height, G. tenella adult feeding and oviposition) were significantly correlated with island age. First, leaf concentrations of condensed tannins and individual phenolics were positively correlated with island age, suggesting that plant resistance increased after herbivore colonization and continued to increase in parallel to increasing time of past coexistence, while plant height showed a reverse negative correlation. Second, a multi-choice experiment with G. tenella showed that both oviposition and leaf consumption of the host plants were negatively correlated with island age. Third, larvae performed poorly on well-defended, older host populations and well on less-defended, younger populations. Thus, no parameter assessed in this study falsifies the coevolution-by-coexistence hypothesis. We conclude that spatio-temporal gradients present in rising archipelagos offer unique opportunities to address evolutionary interactions, but care has to be taken as abiotic (and other biotic) factors may interact in a complicated way.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Behavioural resistance against a protozoan parasite in the monarch butterfly

1. As parasites can dramatically reduce the fitness of their hosts, there should be strong selection for hosts to evolve and maintain defence mechanisms against their parasites. One way in which hosts may protect themselves against parasitism is through altered behaviours, but such defences have been much less studied than other forms of parasite resistance. 2. We studied whether monarch butterflies (Danaus plexippus L.) use altered behaviours to protect themselves and their offspring against the protozoan parasite Ophryocystis elektroscirrha (McLaughlin & Myers (1970), Journal of Protozoology, 17, p. 300). In particular, we studied whether (i) monarch larvae can avoid contact with infectious parasite spores; (ii) infected larvae preferentially consume therapeutic food plants when given a choice or increase the intake of such plants in the absence of choice; and (iii) infected female butterflies preferentially lay their eggs on medicinal plants that make their offspring less sick. 3. We found that monarch larvae were unable to avoid infectious parasite spores. Larvae were also not able to preferentially feed on therapeutic food plants or increase the ingestion of such plants. However, infected female butterflies preferentially laid their eggs on food plants that reduce parasite growth in their offspring. 4. Our results suggest that animals may use altered behaviours as a protection against parasites and that such behaviours may be limited to a single stage in the host-parasite life cycle. Our results also suggest that animals may use altered behaviours to protect their offspring instead of themselves. Thus, our study indicates that an inclusive fitness approach should be adopted to study behavioural defences against parasites.     

Defense syndromes against herbivory in a cerrado plant community

Plants have traits against herbivory that may occur together and increase defense efficiency. We tested whether there are defense syndromes in a cerrado community and, if so, whether there is a phylogenetic signal in them. We measured nine defense traits from a woodland cerrado community in southeastern Brazil. We tested the correlation between all pairs of traits and grouped the species into defense syndromes according to their traits. Most pairwise correlations of traits were complementary. Plants with lower specific leaf area also presented tougher leaves, with low nitrogen, more trichomes, and tannins. We found five syndromes: two with low defenses and high nutritional quality, two with high defenses and low nutritional quality, and one with traits compensating each other. There were two predominant strategies against herbivory in cerrado: “tolerance” and “low nutritional quality” syndromes. Phylogeny did not determine the suite of traits species presented. We argue that herbivory exerts significant selection pressure on these plant defense traits.     

Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata

Allocation theory suggests that the optimal level of resistance against herbivores should vary with the risk of herbivory if allocation to resistance is costly. The perennial herb Arabidopsis lyrata has a genetically based polymorphism for trichome production and occurs in a glabrous and a trichome-producing form. Leaf trichomes (hairs) can protect plants against insect herbivores, and may increase tolerance to drought and UV-radiation. To examine the functional significance of trichome production, we documented the frequency of glabrous plants and damage by insect herbivores in 30 A. lyrata populations in Sweden and Norway. The proportion of glabrous plants ranged from 0.10 to 0.71 (median=0.44) in polymorphic populations; 7 of 12 populations in Norway and 14 of 18 populations in Sweden were monomorphic glabrous, i.e. with fewer than 5% trichome-producing plants. The mean proportion of the leaf area removed by herbivores varied substantially among populations and years. With few exceptions, glabrous plants were more damaged than trichome-producing plants in polymorphic populations. The intensity of herbivory quantified as the mean damage to glabrous plants tended to be higher in polymorphic populations than in populations monomorphic for the glabrous morph and was higher in Sweden than in Norway. In Norway, both the magnitude of herbivore damage and the frequency of trichome-producing plants tended to decrease with increasing altitude. The results indicate that leaf trichomes contribute to resistance against herbivorous insects in A. lyrata , and suggest that herbivore-mediated selection contributes to the maintenance of the polymorphism in trichome production.     

Algal resistance to herbivory on a Caribbean barrier reef

Field and laboratory research at Carrie Bow Cay, Belize showed that macroalgae, grouped in functional-form units resisted fish and urchin herbivory in the following order (from high to low resistance): Crustose-Group, Jointed Calcareous-Group, Thick Leathery-Group, Coarsely Branched-Group, Filamentous-Group and Sheet-Group; thereby supporting the hypothesis that crustose, calcareous and thick algae have evolved antipredator defenses and should show the greatest resistance to herbivory with a gradation of increasing palatability towards filaments and sheets. Of the 21 species examined, several (e.g.,Dictyota cervicornis on grids,Laurencia obtusa andStypopodium zonale) had exceptionally low losses to fish grazing, probably due to chemical defences. The sea urchin,Diadema antillarum, was more inclined to feed on algae with known toxic secondary metabolites than were herbivorous fishes; hypothetically related to the differences in mobility and concomitant modes of feeding. Tough leathery forms such asSargassum polyceratium andTurbinaria turbinata resisted grazing by bottom feeding parrotfishes (Scaridae) and surgeonfishes (Acanthuridae) but were susceptible when suspended midway in the water column, possibly due to the presence of rudderfishes (Kyphosidae) which readily consume drift Sargassaceae. The overall tendencies support our predicted relationship between grazer-resistance and algal morphology. In conjunction with our previously reported findings concerning primary productivity, toughness and calorimetry for many of the same species, these results lend credence to generalizations relating form with function in marine macroalgae.     

Sexual dimorphism in response to herbivory and competition in the dioecious herb Spinacia oleracea

Plant Ecology - Sexual dimorphism is common in dioecious plant species and is usually attributed to different cost of reproduction associated with male and female functions. Differences in growth...     

Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels

We experimentally investigated how pollinator- and herbivore-induced changes influence the performance of the long-lived herb Primula veris. Eight treatments that corresponded to natural factors normally affecting this species were designed to enhance or reduce reproductive success and resource availability (flower removal, supplementary pollination, defoliation). During the experimental season and in the following year we quantified responses in terms of survival, growth, and seed production of reproductive plants. Matrix population models were used to calculate population growth rate using the demographic parameters recorded in permanent plots and respective treatment groups. Seed production was not limited by pollen availability, and we found no evidence of a cost of reproduction. Leaf removal had either no effect or a negative effect on future performance, depending on the timing of removal. Defoliation early in the season reduced current seed production and future growth, whereas removal during fruit development affected performance in the following year. Demographic models suggest that leaf damage has a smaller negative impact than flower removal on overall performance in this population. Our results suggest that the source-sink paths vary over the season and that the timing of herbivory may influence the extent to which effects are carried over to subsequent reproductive seasons.     

Stochastic LTRE analysis of the effects of herbivory on the population dynamics of a perennial grassland herb

Herbivores can have strong deleterious effects on vital rates (growth, reproduction, and survival) and thus negatively impact the population dynamics of plant species. In practice, however, these effects might be strongly correlated, for example as a result of tradeoffs between vital rates. To get better insights into the effects of herbivory on the population dynamics of the long‐lived grassland plant Primula veris population projection matrices were constructed from demographic data collected between 1999 and 2008 (nine annual transitions). Data were collected in two large grassland populations, each of which was subjected to two treatments (grazing by cattle versus a mowing treatment), yielding a total of 36 matrices. We applied a lower‐level vital rate life table response experiment (LTRE) using the small noise approximation (SNA) of the stochastic population growth rate to disentangle the contributions of changes in mean vital rates, variability in vital rates, correlations between vital rates and vital rate elasticities to the difference in the stochastic growth rate. Stochastic growth rates (a= log λ_S) were significantly lower in grazed than in mown plots (a= 0.0185 and 0.1019, respectively). SNA LTRE analysis showed that contributions of mean vital rates by far made the largest contribution to the observed difference in a between grazed and control plots. In particular, changes in sexual reproduction rates made the largest contributions to lower the stochastic growth rate in grazed plots: both adult flowering probabilities and flower and seed production were importantly lower in grazed populations, but these negative effects were largely buffered by increased establishment and seedling survival rates. Among the stochastic terms of the SNA decomposition, contributions of covariance and correlations between vital rates had the largest impact, whereas contributions of elasticities were smaller. The strongest correlation driver was the association between adult survival and seedling establishment, suggesting that environmental conditions favouring adult survival also are beneficial for seedling establishment. Overall, our results show that herbivory had a strong negative effect on the long‐term population growth rate of P. veris that was primarily mediated by differences in fecundity (flower and seed production) and germination.     

Sex allocation under simulated herbivory in the generalist perennial herb Paeonia broteroi (Paeoniaceae)

Theories of optimal resource allocation in flowering plants postulate that allocation to sexual functions are balanced. While many studies have found such evidence in hermaphroditic species among flowers, plants or populations, or at different phenological stages, it has not been supported by other studies. This has been explained by differences among genotypes in ability to acquire resources, resource partitioning among traits unrelated to reproduction or strong selection to maintain positive genetic correlation among traits. I studied how herbivory affected resource allocation to sexual functions in the perennial herb Paeonia broteroi (Paeoniaceae) by measuring a number of floral traits in control plants and in experimental plants under simulated herbivory. The species shows very little plasticity in resource allocation between sexual structures and functions, and appears to be highly sensitive to alterations in the balance of resource acquisition and allocation, with an immediate outcome in terms of seed production and a mid-term response in terms of sprouting and flowering. Plants' ability to collect resources for growth and reproduction before their senescence at the end of the reproductive season, are compromised. This may limit their reproductive potential, the maintenance and growth of their populations, and may influence their demographic state and the plants' ability to respond to selective pressures by external biotic agents.     

Members only: induced systemic resistance to herbivory in a clonal plant network

The stoloniferous herb Trifolium repens was used to study the expression of induced systemic resistance (ISR) to the generalist caterpillar Spodoptera exigua in interconnected ramets of clonal fragments. The ISR was assessed as caterpillar preference in dual choice tests between control and systemically induced plants. The ISR was detected in young ramets, after inducing older sibling ramets on the same stolon by a controlled herbivore attack. However, older ramets did not receive a defense induction signal from younger ramets unless the predominant phloem flow was reversed by means of basal shading. This provides evidence for the notion that in T. repens the clone-internal expression of ISR is coupled to phloem transport and follows source–sink gradients. The inducibility of the genotypes was not linked to their constitutive ability to produce cyanide, implying the absence of a trade-off between these two defense traits. To our knowledge, this is the first study that explores ISR to herbivory in the context of physiological integration in potentially extensive clonal plant networks.     

Evolutionary ecology of Datura stramonium: equal plant fitness benefits of growth and resistance against herbivory

This study evaluated how natural selection act upon two proposed alternatives of defence (growth and resistance) against natural enemies in a common garden experiment using genetic material (full-sibs) from three populations of the annual plant Datura stramonium. Genetic and phenotypic correlations were used to search for a negative association between both alternatives of defence. Finally, the presence/absence of natural enemies was manipulated to evaluate the selective value of growth as a response against herbivory. Results indicated the presence of genetic variation for growth and resistance (1--relative damage), whereas only population differentiation for resistance was detected. No correlation between growth and resistance was detected either at the phenotypic or the genetic level. Selection analysis revealed the presence of equal fitness benefits of growth and resistance among populations. The presence/absence of natural herbivores revealed that herbivory did not alter the pattern of selection on growth. The results indicate that both strategies of defence can evolve simultaneously within populations of D. stramonium.     

Increased life span in a polyphenic butterfly artificially selected for starvation resistance

Starvation resistance is closely associated with fitness in natural populations of many organisms. It often co-varies with longevity and is a relevant target for understanding the evolution of aging. We selected for increased starvation resistance in the seasonally polyphenic butterfly Bicyclus anynana in a warm, wet-seasonal environment over 17 generations. We measured the response to selection for two selected lines compared to that of an unselected stock. Results show an increase in survival under adult starvation of 50%-100%. In addition, selection lines showed an increase in life span under normal adult feeding of 30%-50%. Female reproduction was changed toward laying fewer but larger eggs. The results indicate a sex-specific response to selection: females reallocated resources toward a more durable body, whereas males appeared to increase starvation resistance through changed metabolic rate. The phenotype produced by artificial selection resembles the form that occurs in the cool, dry-season environment, which suggests that selection has targeted the regulatory mechanisms for survival that are also involved in the suite of traits (including starvation resistance) central to the adaptive plastic response of this butterfly to seasonal conditions. In general, these results imply that the regulation of life span involves mechanisms of phenotypic plasticity.     

Higher resistance to herbivory in introduced compared to native populations of a seaweed

Non-indigenous species (NIS) are important components of global change, and in order to manage such species it is important to understand which factors affect their success. Interactions with enemies in the new range have been shown to be important for the outcome of introductions, but thus far most studies on NIS–enemy interactions have considered only specialist herbivores in terrestrial systems. Here we present the results from the first biogeographic study that compares herbivore resistance between populations in the native and new region of a non-indigenous seaweed. We show that low consumption of the non-indigenous seaweed by a generalist herbivore is caused by higher chemical defence levels and herbivore resistance in the new range—and not by the failure of the herbivore to recognise the non-indigenous seaweed as a suitable host. Since most seaweed–herbivore interactions are dominated by generalist herbivores, this pattern could be common in marine communities. Our results also reveal that traits used to predict the invasive potential of species, such as their resistance to enemies, can change during the invasion process, but not always in the way predicted by dominant theories.     

Seedling resistance to herbivory as a predictor of relative abundance in a synthesised prairie community

In a laboratory experiment seedlings of 24 perennial herbaceous prairie species were offered to the omnivorous cricket Acheta domestica in an extended feeding trial. Leaf damage was monitored daily allowing an index of palatability to be calculated for each plant species. The index of palatability successfully predicted relative abundance within the same set of species in an independently-conducted study involving community assembly from seed in low-fertility plots. These results support the hypothesis that resistance to herbivory may be an important component of plant fitness in unproductive vegetation. However, the correlation between palatability and community composition may be interpreted as a positive association between traits that lead to high competitive ability and herbivory resistance. There is a need to establish whether the success of the dominant grasses at Cedar Creek arises from their superior ability to capture nitrogen from low external concentrations or is, rather, due to their superior ability to minimise nitrogen loss to herbivores.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.