Luis Abdala-Roberts

Plant diversity effects on insect herbivores and their natural enemies: current thinking, recent findings, and future directions

A rich body of theory has been developed to predict the effects of plant diversity on communities at higher trophic levels and the mechanisms underpinning such effects. However, there are currently a number of key gaps in knowledge that have hindered the development of a predictive framework of plant diversity effects on consumers. For instance, we still know very little about how the magnitude of plant trait variation (e.g. intra-specific vs. inter-specific), as well as the identity and combined effects of plant, herbivore and natural enemy traits, mediate plant diversity effects on consumers. Moreover, the fine-scale mechanisms (e.g. changes in consumer behaviour or recruitment responses) underlying such diversity effects in many cases remain elusive or have been overlooked. In addition, most studies of plant diversity effects on associated consumers have been developed under a static, unidirectional (bottom-up) framework of effects on herbivores and predators without taking into account the potential for dynamic feedbacks across trophic levels. Here we seek to address these key gaps in knowledge as well as to capitalize on recent advances and emerging frameworks in plant biodiversity research. In doing so, we provide new insights as well as recommendations which will stimulate new research and advance this field of study.

Positive Effects of Plant Genotypic and Species Diversity on Anti-Herbivore Defenses in a Tropical Tree Species

Despite increasing evidence that plant intra- and inter-specific diversity increases primary productivity, and that such effect may in turn cascade up to influence herbivores, there is little information about plant diversity effects on plant anti-herbivore defenses, the relative importance of different sources of plant diversity, and the mechanisms for such effects. For example, increased plant growth at high diversity may lead to reduced investment in defenses via growth-defense trade-offs. Alternatively, positive effects of plant diversity on plant growth may lead to increased herbivore abundance which in turn leads to a greater investment in plant defenses. The magnitude of trait variation underlying diversity effects is usually greater among species than among genotypes within a given species, so plant species diversity effects on resource use by producers as well as on higher trophic levels should be stronger than genotypic diversity effects. Here we compared the relative importance of plant genotypic and species diversity on anti-herbivore defenses and whether such effects are mediated indirectly via diversity effects on plant growth and/or herbivore damage. To this end, we performed a large-scale field experiment where we manipulated genotypic diversity of big-leaf mahogany (Swietenia macrophylla) and tree species diversity, and measured effects on mahogany growth, damage by the stem-boring specialist caterpillar Hypsipyla grandella, and defensive traits (polyphenolics and condensed tannins in stem and leaves). We found that both forms of plant diversity had positive effects on stem (but not leaf) defenses. However, neither source of diversity influenced mahogany growth, and diversity effects on defenses were not mediated by either growth-defense trade-offs or changes in stem-borer damage. Although the mechanism(s) of diversity effects on plant defenses are yet to be determined, our study is one of the few to test for and show producer diversity effects on plant chemical defenses.

Local adaptation of Ruellia nudiflora (Acanthaceae) to biotic counterparts: complex scenarios revealed when two herbivore guilds are considered.

This study evaluated whether the herb Ruellia nudiflora is locally adapted to a specialist insect seed predator (SP) and insect folivores, and if plant local adaptation (LA) to the former is more likely. A reciprocal transplant experiment was conducted using three sites in Yucatan (Mexico) (n = 864 plants). A third of the plants of each origin were placed at each site, and we recorded the following during a 9‐month period: fruit number, leaf damage, and fruits attacked by SP. Results indicated lack of plant LA for all the variables measured. Instead, seed predation was c. 100% greater for native plants at one study site, suggesting insect LA or plant maladaptation; folivory was homogeneous across sites/origins. Based on these results, we discuss differences in the potential each herbivore guild has to promote plant LA, as well as divergent evolutionary outcomes of plant–herbivore interactions across sites.

Ecological and evolutionary consequences of plant genotype diversity in a tri-trophic system

The mechanisms by which plant diversity influences consumers are largely unexplored. Plant diversity reduces among-plant competition, and as a result, may have cascading bottom-up effects through altered resource quantity and quality. Less understood are parallel effects of resource heterogeneity on consumer foraging behaviors, and the consequences of such effects for trophic interactions and feedbacks on plant performance. Here, we asked whether genotypic diversity in the herb Ruellia nudiflora influences seed predator (SP) and parasitoid functional responses, and if such effects in turn influence selection on the plant. We established plots with plants of one or five genetic families (pool = 14) and measured fruit, seed predator, and parasitoid abundance. By eliminating direct plant–plant interactions, this experiment explicitly tested for plant diversity effects occurring through altered consumer behaviors (vs. effects through changes in plant quantity or quality). We compared observed plant fitness (under three trophic levels) to projected fitness in the absence of parasitoids (two trophic levels) and in the absence of seed predation (one trophic level) by computing the number of seeds consumed by the SP and the number of seeds rescued from consumption by parasitoids. We then compared the strength and mode of selection on fruit number between levels of diversity, separately under each trophic scenario. Plant diversity did not influence fruit, seed predator, or parasitoid abundance, but did alter plant–SP interactions. SP recruitment resembled a Type II functional response but saturated weakly in polycultures, with fewer SPs at intermediate fruit abundance and more SPs at high fruit abundance relative to monoculture. Parasitoid recruitment was weakly positively density dependent and unaffected by diversity. Importantly, we found that under the bi-trophic scenario, the effect of diversity on SP recruitment altered the mode of selection on fruit number, from directional selection at low diversity to nonlinear (stabilizing) selection at high diversity. In contrast, diversity did not alter selection under mono- or tri-trophic scenarios. Therefore, diversity effects on SP functional responses fed back to alter selection on fruit number, but parasitoids eliminated this linkage by weakening herbivore selection. Collectively, these findings provide novel evidence for the mechanistic basis of eco-evolutionary feedbacks between plant diversity and consumers.

Masting promotes individual- and population-level reproduction by increasing pollination efficiency

Masting is a reproductive strategy defined as the intermittent and synchronized production of large seed crops by a plant population. The pollination efficiency hypothesis proposes that masting increases pollination success in plants. Despite its general appeal, no previous studies have used long-term data together with population- and individual-level analyses to assess pollination efficiency between mast and non-mast events. Here we rigorously tested the pollination efficiency hypothesis in ponderosa pine (Pinus ponderosa), a long-lived monoecious, wind-pollinated species, using a data set on 217 trees monitored annually for 20 years. Relative investment in male and female function by individual trees did not vary between mast and non-mast years. At both the population and individual level, the rate of production of mature female cones relative to male strobili production was higher in mast than non-mast years, consistent with the predicted benefit of reproductive synchrony on reproductive success. In addition, at the individual level we found a higher conversion of unfertilized female conelets into mature female cones during a mast year compared to a non-mast year. Collectively, parallel results at the population and individual tree level provide robust evidence for the ecological, and potentially also evolutionary, benefits of masting through increased pollination efficiency.

Patterns of among- and within-species variation in heterospecific pollen receipt: The importance of ecological generalization

PREMISE OF THE STUDY Coflowering plants are at risk for receiving pollen from heterospecifics as well as conspecifics, yet evidence shows wide variation in the degree that heterospecific pollen transfer occurs. Evaluation of patterns and correlates of among- and within-species variation in heterospecific pollen (HP) receipt is key to understanding its importance for floral evolution and species coexistence; however, the rarity of deeply sampled multispecies comparisons has precluded such an evaluation. METHODS We evaluated patterns of among- and within-species variation in HP load size and diversity in 19 species across three distinct plant communities. We assessed the importance of phenotypic specialization (floral phenotype), ecological specialization (contemporary visitor assemblage), and conspecific flower density as determinants of among-species variation. We present hypotheses for different accrual patterns of HP within species based on the evenness and quality of floral visitors and evaluated these by characterizing the relationship between conspecific pollen (CP) and HP receipt. KEY RESULTS We found that within-species variation in HP receipt was greater than among-species and among-communities variation. Among species, ecological generalization emerged as the strongest driver of variation in HP receipt irrespective of phenotypic specialization. Within-species variation in HP load size and diversity was predicted most often from two CP-HP relationships (linear or exponentially decreasing), suggesting that two distinct types of plant-pollinator interactions prevail. CONCLUSIONS Our results give important insights into the potential drivers of among- and within-species variation in HP receipt. They also highlight the value of explorations of patterns at the intraspecific level, which can ultimately shed light on plant-pollinator-mediated selection in diverse plant communities.

Test of biotic and abiotic correlates of latitudinal variation in defences in the perennial herb Ruellia nudiflora

Summary Geographic variation in abiotic factors and species interactions is widespread and is hypothesized to generate concomitant patterns of species trait variation. For example, higher rates of herbivory at lower latitudes are thought to select for increased plant defences, although latitudinal variation in defences may also be influenced directly by abiotic factors and indirectly by predators and parasitoids reducing herbivore pressure. We measured defences of the herb Ruellia nudiflora among 30 populations spanning a latitudinal gradient from northern Yucatan to southern Belize that vary substantially in leaf herbivory (fourfold), seed herbivory (25-fold) and seed herbivore parasitism (14-fold). These surveyed populations span one-third of the species’ latitudinal distribution (5° of latitude), the entire precipitation gradient of its distribution, and one-third of the temperature gradient of its distribution. Our prior work showed that leaf herbivory decreased with latitude and that seed herbivory increased with latitude. Here, we measured leaf trichome density and leaf and seed phenolics and tested whether latitudinal variation in climate, herbivory and parasitism explained latitudinal variation in these defensive traits. Patterns of variation in leaf trichomes fully supported predictions, with trichome density increasing with a parallel increase in herbivory towards lower latitudes. While seed phenolics were positively associated with herbivory, and seed herbivory tended to increase with latitude, the predicted (positive) association between latitude and defence was not detectable. There was no detectable association between parasitoids and seed defences. In addition, the association between leaf herbivory and phenolics was weak, and leaf phenolics were not associated with latitude. Importantly, variation in the abiotic environment was associated with plant defence, indicating that abiotic factors can play a major role in shaping plant defences, independently of herbivory. Synthesis. Latitudinal variation in abiotic factors may drive concomitant patterns of variation in plant defences, independently of herbivory. Collectively, these findings highlight the need for assessing geographic variation in plant defences from a multi-factorial perspective, testing for the simultaneous influence of biotic and abiotic factors.

Effects of climate on reproductive investment in a masting species: Assessment of climatic predictors and underlying mechanisms

Summary 1. Mechanisms by which climatic factors drive reproductive investment and phenology in masting species are not completely understood. Climatic conditions may act as a proximate cue, stimulating the onset of reproduction and indirectly increasing fitness through benefits associated with synchronous reproduction among individuals. Alternatively, climatic conditions may directly influence individual-level allocation to reproduction and reproductive success through effects occurring independently of synchronous reproduction. We previously showed that masting in a ponderosa pine (Pinus ponderosa) population was strongly influenced by spring mean temperature 2 years before seed cone maturation (Ti-2). However, recent work shows that the difference in temperature between previous growing seasons (DT) is more predictive of reproductive investment in long-lived tree species. 2. Here, we compared four candidate models that predict seed cone production in P. ponderosa based upon different climatic factors (including Ti-2 and DT models). After determining the best climatic predictor, we tested for a potential mechanism by which climate might directly influence seed cone production independent of benefits via synchrony, namely effects of temperature on trade-offs between current and past reproduction (determined by underlying resource availability). 3. We found that Ti-2 (rather than DT) was the best predictor of seed cone production. We further show that this same climatic factor exerts a direct fitness benefit to individuals by reducing the strength of trade-offs between current and past reproductive efforts. 4. Synthesis. We demonstrate that a single climatic factor provides fitness benefits to individuals directly, by weakening reproductive trade-offs, and indirectly through the benefits associated with synchrony and masting. This suggests a mechanism for the origin and maintenance of masting: individuals initially respond to climatic cues that directly enhance reproduction (e.g. lower reproductive costs through weakened trade-offs) and this dynamic, expressed across multiple individuals, reinforces these benefits through the economies of scale associated with synchrony and masting.

Biotic and abiotic factors associated with altitudinal variation in plant traits and herbivory in a dominant oak species

PREMISE OF THE STUDY It is generally thought that herbivore pressure is higher at lower elevations where climate is warmer and less seasonal, and that this has led to higher levels of plant defense investment at low elevations. However, the generality of this expectation has been called into question by recent studies. METHODS We tested for altitudinal gradients in insect leaf damage, plant defenses (phenolic compounds), and nutritional traits (phosphorus and nitrogen) in leaves of the long-lived tree Quercus robur, and further investigated the abiotic factors associated with such gradients. We sampled 20 populations of Q. robur distributed along an altitudinal gradient spanning 35-869 m above sea level, which covered most of the altitudinal range of this species and varied substantially in abiotic conditions, plant traits, and herbivory. KEY RESULTS Univariate regressions showed that leaf herbivory, phenolics, and phosphorus increased toward higher elevations, whereas leaf nitrogen did not vary with altitude. Multiple regression analyses indicated that temperature was the single most important factor associated with herbivory and appears to be strongly associated with altitudinal variation in damage. Leaf phenolics were also correlated with herbivory, but in a manner that suggests these chemical defenses do not underlie altitudinal variation in damage. In addition, we found that variation in leaf traits (phenolics and nutrients) was in turn associated with both climatic and soil variables. CONCLUSIONS Overall, these findings suggest that altitudinal gradients in herbivory and defenses in Q. robur are uncoupled and that elevational variation in herbivory and plant traits responds mainly to abiotic factors.

Specificity of induced defenses, growth, and reproduction in lima bean (Phaseolus lunatus) in response to multispecies herbivory

UNLABELLED • PREMISE OF THE STUDY Following herbivore attack, plants can either reduce damage by inducing defenses or mitigate herbivory effects through compensatory growth and reproduction. It is increasingly recognized that such induced defenses in plants are herbivore-specific, but less is known about the specificity of compensatory responses. Damage by multiple herbivores may also lead to synergistic effects on induction and plant fitness that differ from those caused by a single herbivore species. Although largely unstudied, the order of arrival and damage by different herbivore species might also play an important role in the impacts of herbivory on plants.• METHODS We investigated the specificity of defense induction (phenolics) and effects on growth (number of stems and leaves) and reproduction (number of seeds, seed mass, and germination rate) from feeding by two generalist leaf-chewing herbivores (Spodoptera eridania and Diabrotica balteata) on Phaseolus lunatus plants and evaluated whether simultaneous attack by both herbivores and their order of arrival influenced such dynamics.• KEY RESULTS Herbivory increased levels of leaf phenolics, but such effects were not herbivore-specific. In contrast, herbivory enhanced seed germination in an herbivore-specific manner. For all variables measured, the combined effects of both herbivore species did not differ from their individual effects. Finally, the order of herbivore arrival did not influence defense induction, plant growth, or seed number but did influence seed mass and germination.• CONCLUSIONS Overall, this study highlights novel aspects of the specificity of plant responses induced by damage from multiple species of herbivores and uniquely associates such effects with plant lifetime fitness.