The co-existence of multiple oak leaf flushes contributes to the large within-tree variation in chemistry, insect attack and pathogen infection.

Many plant species produce multiple leaf flushes during the growing season, which might have major consequences for within-plant variation in chemistry and species interactions. Yet, we lack a theoretical or empirical framework for how differences among leaf flushes might shape variation in damage by insects and diseases. We assessed the impact of leaf flush identity on leaf chemistry, insect attack and pathogen infection on the pedunculate oak Quercus robur by sampling leaves from each leaf flush in 20 populations across seven European countries during an entire growing season. The first leaf flush had higher levels of primary compounds, and lower levels of secondary compounds, than the second flush, whereas plant chemistry was highly variable in the third flush. Insect attack decreased from the first to the third flush, whereas infection by oak powdery mildew was lowest on leaves from the first flush. The relationship between plant chemistry, insect attack and pathogen infection varied strongly among leaf flushes and seasons. Our findings demonstrate the importance of considering differences among leaf flushes for our understanding of within-tree variation in chemistry, insect attack and disease levels, something particularly relevant given the expected increase in the number of leaf flushes with climate change.

Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species.

BACKGROUND AND AIMS: Classic theory on geographical gradients in plant-herbivore interactions assumes that herbivore pressure and plant defences increase towards warmer and more stable climates found at lower latitudes. However, the generality of these expectations has been recently called into question by conflicting empirical evidence. One possible explanation for this ambiguity is that most studies have reported on patterns of either herbivory or plant defences whereas few have measured both, thus preventing a full understanding of the implications of observed patterns for plant-herbivore interactions. In addition, studies have typically not measured climatic factors affecting plant-herbivore interactions, despite their expected influence on plant and herbivore traits. METHODS: Here we tested for latitudinal variation in insect seed predation and seed traits putatively associated with insect attack across 36 Quercus robur populations distributed along a 20° latitudinal gradient. We then further investigated the associations between climatic factors, seed traits and seed predation to test for climate-based mechanisms of latitudinal variation in seed predation. KEY RESULTS: We found strong but contrasting latitudinal clines in seed predation and seed traits, whereby seed predation increased whereas seed phenolics and phosphorus decreased towards lower latitudes. We also found a strong direct association between temperature and seed predation, with the latter increasing towards warmer climates. In addition, temperature was negatively associated with seed traits, with populations at warmer sites having lower levels of total phenolics and phosphorus. In turn, these negative associations between temperature and seed traits led to a positive indirect association between temperature and seed predation. CONCLUSIONS: These results help unravel how plant-herbivore interactions play out along latitudinal gradients and expose the role of climate in driving these outcomes through its dual effects on plant defences and herbivores. Accordingly, this emphasizes the need to account for abiotic variation while testing concurrently for latitudinal variation in plant traits and herbivore pressure.

Parallel increases in insect herbivory and defenses with increasing elevation for both saplings and adult trees of oak (Quercus) species.

PREMISE: Herbivory is predicted to increase toward warmer and more stable climates found at lower elevations, and this increase should select for higher plant defenses. Still, a number of recent studies have reported either no evidence of such gradients or reverse patterns. One source of inconsistency may be that plant ontogenetic variation is usually not accounted for and may influence levels of plant defenses and herbivory. METHODS: We tested for elevational gradients in insect leaf herbivory and leaf traits putatively associated with herbivore resistance across eight oak (Quercus, Fagaceae) species and compared these patterns for saplings and adult trees. To this end, we surveyed insect leaf herbivory and leaf traits (phenolic compounds, toughness and nutrients) in naturally occurring populations of each oak species at low-, mid- or high-elevation sites throughout the Iberian Peninsula. RESULTS: Leaf herbivory and chemical defenses (lignins) were unexpectedly higher at mid- and high-elevation sites than at low-elevation sites. In addition, leaf chemical defenses (lignins and condensed tannins) were higher for saplings than adult trees, whereas herbivory did not significantly differ between ontogenetic stages. Overall, elevational variation in herbivory and plant chemical defenses were consistent across ontogenetic stages (i.e., elevational gradients were not contingent upon tree ontogeny), and herbivory and leaf traits were not associated across elevations. CONCLUSIONS: These findings suggest disassociated patterns of elevational variation in herbivory and leaf traits, which, in turn, are independent of plant ontogenetic stage.

Greater phylogenetic distance from native oaks predicts escape from insect leaf herbivores by non-native oak saplings.

PREMISE: Non-native plant species have been hypothesized to experience lower herbivory in novel environments as a function of their phylogenetic distance from native plant species. Although recent work has found support for this prediction, the plant traits responsible for such patterns have been largely overlooked. METHODS: In a common garden experiment in northwestern Spain, we tested whether oak species (Quercus spp.) not native to this region that are phylogenetically more distantly related to native species exhibit less insect leaf herbivory. In addition, we also investigated plant traits potentially correlated with any such effect of phylogenetic distance. RESULTS: As expected, phylogenetic distance from native species negatively predicted insect leaf herbivory on non-native oaks. In addition, we found that the leaf traits, namely phosphorus and condensed tannins, were significantly associated with herbivory, suggesting that they are associated with the effect of phylogenetic distance on leaf herbivory on non-native oak species. CONCLUSIONS: This study contributes to a better understanding of how evolutionary relationships (relatedness) between native and non-native plant species determine the latter's success in novel environments via locally shared enemies, and encourages more work investigating the plant traits that mediate the effects of phylogenetic distance on enemy escape.

Interspecific variation in leaf functional and defensive traits in oak species and its underlying climatic drivers.

Plants exhibit a diverse set of functional traits and ecological strategies which reflect an adaptation process to the biotic and abiotic components of the environment. The Plant Economic Spectrum organizes these traits along a continuum from conservative to acquisitive resource use strategies and shows how the abiotic environment governs a species' position along the continuum. However, this framework does not typically account for leaf traits associated with herbivore resistance, despite fundamental metabolic links (and therefore co-variance) between resource use traits and defensive traits. Here we analyzed a suite of leaf traits associated with either resource use (specific leaf area [SLA], nutrients and water content) or defenses (phenolic compounds) for saplings of 11 species of oaks (Quercus spp.), and further investigated whether climatic variables underlie patterns of trait interspecific variation. An ordination of leaf traits revealed the primary axis of trait variation to be leaf economic spectrum traits associated with resource use (SLA, nitrogen, water content) in conjunction with a defensive trait (condensed tannins). Secondary and tertiary axes of trait variation were mainly associated with other defensive traits (lignins, flavonoids, and hydrolysable tannins). Within the primary axis we found a trade-off between resource use traits and both water content and condensed tannins; species with high SLA and leaf N values invested less in condensed tannins and viceversa. Moreover, temperature and precipitation mediated the trait space occupied by species, such that species distributed in warmer and drier climates had less leaf N, lower SLA, and more defenses (condensed tannins, lignins and flavonoids), whereas opposite values were observed for species distributed in colder and wetter climates. These results emphasize the role of abiotic controls over all-inclusive axes of trait variation and contribute to a more complete understanding of interspecific variation in plant functional strategies.

Intra-Specific Latitudinal Clines in Leaf Carbon, Nitrogen, and Phosphorus and their Underlying Abiotic Correlates in Ruellia Nudiflora.

While plant intra-specific variation in the stoichiometry of nutrients and carbon is well documented, clines for such traits have been less studied, despite their potential to reveal the mechanisms underlying such variation. Here we analyze latitudinal variation in the concentration of leaf nitrogen (N), phosphorus (P), carbon (C) and their ratios across 30 populations of the perennial herb Ruellia nudiflora. In addition, we further determined whether climatic and soil variables underlie any such latitudinal clines in leaf traits. The sampled transect spanned 5° latitude (ca. 900 km) and exhibited a four-fold precipitation gradient and 2 °C variation in mean annual temperature. We found that leaf P concentration increased with precipitation towards lower latitudes, whereas N and C did not exhibit latitudinal clines. In addition, N:P and C:P decreased towards lower latitudes and latitudinal variation in the former was weakly associated with soil conditions (clay content and cation exchange capacity); C:N did not exhibit a latitudinal gradient. Overall, these results emphasize the importance of addressing and disentangling the simultaneous effects of abiotic factors associated with intra-specific clines in plant stoichiometric traits, and highlight the previously underappreciated influence of abiotic factors on plant nutrients operating under sharp abiotic gradients over smaller spatial scales.

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.

Phenological and water-use patterns underlying maximum growing season length at the highest elevations: implications under climate change.

Consequences of climate change on tree phenology are readily observable, but little is known about the variations in phenological sensitivity to drought between populations within a species. In this study, we compare the phenological sensitivity to temperature and water availability in Abies pinsapo Boiss., a drought-sensitive Mediterranean fir, across its altitudinal distribution gradient. Twig growth and needle fall were related to temperature, precipitation and plant water status on a daily scale. Stands located at the top edge of the distributional range showed the most favourable water balance, maximum growth rates and little summer defoliation. Towards higher elevations, the observed delay in budburst date due to lower spring temperatures was overcome by a stronger delay in growth cessation date due to the later onset of strong water-deficit conditions in the summer. This explains an extended growing season and the greatest mean growth at the highest elevation. Conversely, lower predawn xylem water potentials and early partial stomatal closure and growth cessation were found in low-elevation A. pinsapo trees. An earlier and higher summer peak of A. pinsapo litterfall was also observed at these water-limited sites. Our results illustrate the ecophysiological background of the ongoing altitudinal shifts reported for this relict tree species under current climatic conditions.