Parental resource and offspring liability: the influence of extrafloral nectar on oviposition by a leaf-mining moth.

For many insect herbivores, maternal host selection is a critical determinant of offspring survival; however, maternal fitness is also affected by adult resources such as food availability. Consequently, adult resources may promote oviposition in sub-optimal locations when measured in terms of offspring performance. We tested whether oviposition site preference is primarily shaped by proximity to adult food resources or offspring performance in the aspen leaf miner (Phyllocnistis populiella). Quaking aspen (Populus tremuloides) produce extrafloral nectaries (EFNs) on a subset of their leaves. EFN expression on leaves is associated with decreased P. populiella damage and larval performance; however, P. populiella adults feed from EFNs. We reduced extrafloral nectar availability on entire aspen ramets and excluded crawling predators in a full factorial experiment at two sites in interior Alaska, USA. Patterns of egg deposition by P. populiella appeared to be primarily affected by offspring survival rather than adult resource availability. While oviposition was unaffected by nectar availability, adult moths laid fewer eggs on leaves with than without EFNs. By avoiding leaves with EFNs, moths increased offspring survival. Both moths and predators distinguished between leaves with and without EFNs even when nectar and visual cues were obscured, and therefore may respond to chemical cues associated with EFN expression.

Overwintering physiology and microhabitat use of Phyllocnistis populiella (Lepidoptera: Gracilliariidae) in interior Alaska.

We investigated the overwintering physiology and behavior of Phyllocnistis populiella Chambers, the aspen leaf miner, which has caused severe and widespread damage to aspen in Alaska over the past 10 yr. Active P. populiella moths caught in spring and summer supercooled to an average temperature of -16°C, whereas dormant moths excavated from hibernacula in the leaf litter during fall and winter supercooled to an average of -32°C. None of the moths survived freezing in the laboratory. Counts of overwintering moths in leaf litter across microhabitats in interior Alaska demonstrated that moths occurred at significantly higher density beneath white spruce trees than beneath the aspen host, several other hardwood species, or in open areas among trees. During winter, the temperature 1-2 cm below the surface of the leaf litter beneath white spruce trees was on average 7-9°C colder than beneath aspen trees, and we estimate that during at least one period of the winter the temperature under some white spruce trees may have been cold enough to cause mortality. However, the leaf litter under white spruce trees was significantly drier than the litter from other microhabitats, which may assist P. populiella moths to avoid inoculative freezing because of physical contact with ice. We conclude that in interior Alaska, P. populiella overwinter in a supercooled state within leaf litter mainly under nonhost trees, and may prefer relatively dry microhabitats over moister ones at the expense of lower environmental temperature.

Defensive effects of extrafloral nectaries in quaking aspen differ with scale.

The effects of plant defenses on herbivory can differ among spatial scales. This may be particularly common with indirect defenses, such as extrafloral nectaries (EFNs), that attract predatory arthropods and are dependent on predator distribution, abundance, and behavior. We tested the defensive effects of EFNs in quaking aspen (Populus tremuloides Michx.) against damage by a specialist herbivore, the aspen leaf miner (Phyllocnistis populiella Cham.), at the scale of individual leaves and entire ramets (i.e., stems). Experiments excluding crawling arthropods revealed that the effects of aspen EFNs differed at the leaf and ramet scales. Crawling predators caused similar reductions in the percent leaf area mined on individual leaves with and without EFNs. However, the extent to which crawling predators increased leaf miner mortality and, consequently, reduced mining damage increased with EFN expression at the ramet scale. Thus, aspen EFNs provided a diffuse defense, reducing damage to leaves across a ramet regardless of leaf-scale EFN expression. We detected lower leaf miner damage and survival unassociated with crawling predators on EFN-bearing leaves, suggesting that direct defenses (e.g., chemical defenses) were stronger on leaves with than without EFNs. Greater direct defenses on EFN-bearing leaves may reduce the probability of losing these leaves and thus weakening ramet-scale EFN defense. Aspen growth was not related to EFN expression or the presence of crawling predators over the course of a single season. Different effects of aspen EFNs at the leaf and ramet scales suggest that future studies may benefit from examining indirect defenses simultaneously at multiple scales.

Induction of phenolic glycosides by quaking aspen (Populus tremuloides) leaves in relation to extrafloral nectaries and epidermal leaf mining.

We studied the effect of epidermal leaf mining on the leaf chemistry of quaking aspen, Populus tremuloides, during an outbreak of the aspen leaf miner, Phyllocnistis populiella, in the boreal forest of interior Alaska. Phyllocnistis populiella feeds on the epidermal cells of P. tremuloides leaves. Eleven days after the onset of leaf mining, concentrations of the phenolic glycosides tremulacin and salicortin were significantly higher in aspen leaves that had received natural levels of leaf mining than in leaves sprayed with insecticide to reduce mining damage. In a second experiment, we examined the time course of induction in more detail. The levels of foliar phenolic glycosides in naturally mined ramets increased relative to the levels in insecticide-treated ramets on the ninth day following the onset of leaf mining. Induction occurred while some leaf miner larvae were still feeding and when leaves had sustained mining over 5% of the leaf surface. Leaves with extrafloral nectaries (EFNs) had significantly higher constitutive and induced levels of phenolic glycosides than leaves lacking EFNs, but there was no difference in the ability of leaves with and without EFNs to induce phenolic glycosides in response to mining. Previous work showed that the extent of leaf mining damage was negatively related to the total foliar phenolic glycoside concentration, suggesting that phenolic glycosides deter or reduce mining damage. The results presented here demonstrate that induction of phenolic glycosides can be triggered by relatively small amounts of mining damage confined to the epidermal tissue, and that these changes in leaf chemistry occur while a subset of leaf miners are still feeding within the leaf.

Within-plant distribution of phenolic glycosides and extrafloral nectaries in trembling aspen (Populus tremuloides; Salicaceae).

Expression of foliar secondary compounds and extrafloral nectaries (EFNs) within the same leaves may be incompatible if secondary compounds repel beneficial insects that might otherwise be attracted to EFNs. This study examined the within-plant distributions of phenolic glycosides and EFNs in trembling aspen, Populus tremuloides, and their relationships to herbivore damage. Populus tremuloides expresses extrafloral nectaries (EFNs) on a subset of its leaves. We studied short and tall naturally occurring aspen ramets across multiple sites in interior Alaska. Contrary to our expectations, foliar phenolic glycoside concentrations were approximately 30% greater on leaves bearing EFNs than on leaves without EFNs. The mean concentration of foliar phenolic glycosides in short ramets was nine times that in tall ramets. Phenolic glycoside concentration was negatively related to leaf mining damage by Phyllocnistis populiella (Lepidoptera; Gracilliadae) at concentrations greater than 27 mg/g, whereas the presence of EFNs was unrelated to mining damage. The positive association of chemical defensive compounds and EFNs in leaves suggests that, for species with variation in EFN expression, negative correlations between herbivory and EFN expression may arise indirectly from associated effects of other, correlated types of defense.

Impact of epidermal leaf mining by the aspen leaf miner (Phyllocnistis populiella) on the growth, physiology, and leaf longevity of quaking aspen.

The aspen leaf miner, Phyllocnistis populiella, feeds on the contents of epidermal cells on both top (adaxial) and bottom (abaxial) surfaces of quaking aspen leaves, leaving the photosynthetic tissue of the mesophyll intact. This type of feeding is taxonomically restricted to a small subset of leaf mining insects but can cause widespread plant damage during outbreaks. We studied the effect of epidermal mining on aspen growth and physiology during an outbreak of P. populiella in the boreal forest of interior Alaska. Experimental reduction of leaf miner density across two sites and 3 years significantly increased annual aspen growth rates relative to naturally mined controls. Leaf mining damage was negatively related to leaf longevity. Leaves with heavy mining damage abscised 4 weeks earlier, on average, than leaves with minimal mining damage. Mining damage to the top and bottom surfaces of leaves had different effects on physiology. Mining on the top surface of the leaf had no significant effect on photosynthesis or conductance and was unrelated to leaf stable C isotope ratio (delta(13)C). Mining damage to the bottom leaf surface, where stomata are located, had significant negative effects on net photosynthesis and water vapor conductance. Percent bottom mining was positively related to leaf delta(13)C. Taken together, the data suggest that the primary mechanism for the reduction of photosynthesis by epidermal leaf mining by P. populiella is the failure of stomata to open normally on bottom-mined leaves.

Fitness consequences of choosy oviposition for a time-limited butterfly.

For the majority of insects, a female's choice of oviposition site(s) greatly influences both the success of individual offspring and her own total fitness. Theory predicts that females most strongly limited by egg number will employ greater oviposition site discrimination than those predominately subject to time limitation. The reproductive success of the butterfly Pieris virginiensis at our Connecticut, USA, field site is strongly time constrained on two fronts. First, during their three-week flight season, only 60% of days and 28% of daytime hours were suitable for flight. Second, larval survival is impacted by the rapid senescence of their spring ephemeral host plant Dentaria diphylla, with eggs laid during the first half of the flight season having approximately three times the survival chance of those laid later. Yet, on average, females choose to oviposit on only half the plants they closely inspect and fly over most ramets without any inspection. Our experiments demonstrate that the preferred host ramets confer an approximate two-fold survival advantage. Females are not choosing plants that senesce later, despite the advantage that such plants would confer. We use empirical data on female behavior and larval performance to parameterize a simulation model. Model results suggest that, despite the notable time limitation in this system, the observed level of female oviposition site preference not only increases individual larval survival, but also total female fitness. Low egg loads in this species may contribute to selection for strong host plant discrimination.