John T. Smiley

Plant chemistry and the evolution of host specificity: new evidence from heliconius and passiflora.

Larval growth rates of Heliconius butterflies do not closely parallel host plant choice, an indication that factors other than host plant chemistry are important in evolving host specificity. High growth rate in one species is correlated with reduction in number of palatable host species. This suggests a mechanism by which ecologically restricted species become progressively biochemically specialized.

Ecological Effects of Salicin at Three Trophic Levels: New Problems from Old Adaptations

Salicin, a toxic phenol glycoside, is used by larvae of the beetle Chrysomela aenicollis as a substrate for producing defensive secretions. In the east-central Sierra Nevada mountains of California, salicin concentrations ranged from 0.05 percent to over 5 percent of dry weight in leaves of different plants of Salix orestera, the Sierra willow. Beetles produced more secretion and suffered less predation on willows containing more salicin. In addition, leaf damage due to herbivory among 16 willow clones ranged from 0 to 20 percent of leaf area and was linearly related to salicin content. These results illustrate how a plant secondary chemical can become a problem for the plant when herbivores are adapted to use the chemical for their own benefit. The results also show the effect of a plant chemical on three trophic levels—the producer, a herbivore, and the predators of the herbivore.

PREDATOR DIVERSITY AND IDENTITY DRIVE INTERACTION STRENGTH AND TROPHIC CASCADES IN A FOOD WEB

Declining predator diversity may drastically affect the biomass and productivity of herbivores and plants. Understanding how changes in predator diversity can propagate through food webs to alter ecosystem function is one of the most challenging ecological research topics today. We studied the effects of predator removal in a simple natural food web in the Sierra Nevada mountains of California (USA). By excluding the predators of the third trophic level of a food web in a full-factorial design, we monitored cascading effects of varying predator diversity and composition on the herbivorous beetle Chrysomela aeneicollis and the willow Salix orestera, which compose the first and second trophic levels of the food web. Decreasing predator diversity increased herbivore biomass and survivorship, and consequently increased the amount of plant biomass consumed via a trophic cascade. Despite this simple linear mean effect of diversity on the strength of the trophic cascade, we found additivity, compensation, and interference in the effects of multiple predators on herbivores and plants. Herbivore survivorship and predator-prey interaction strengths varied with predator diversity, predator identity, and the identity of coexisting predators. Additive effects of predators on herbivores and plants may have been driven by temporal niche separation, whereas compensatory effects and interference occurred among predators with a similar phenology. Together, these results suggest that while the general trends of diversity effects may appear linear and additive, other information about species identity was required to predict the effects of removing individual predators. In a community that is not temporally well-mixed, predator traits such as phenology may help predict impacts of species loss on other species. Information about predator natural history and food web structure may help explain variation in predator diversity effects on trophic cascades and ecosystem function.

ANT CONSTANCY AT PASSIFLORA EXTRAFLORAL NECTARIES: EFFECTS ON CATERPILLAR SURVIVAL'

I examined the role of ants in controlling the magnitude and distribution of caterpillar survival at Corcovado National Park, Costa Rica. Ants of 29 species were observed visiting the extrafloral nectary glands of Passiflora vitifolia and P. quadrangularis. Plants attended by ants had ants present 60% of the time. Approximately equal numbers of plants attended by ants and plants without ants were treated with Tanglefoot to exclude walking predators from a single branch on each plant. Heliconius ismenius caterpillars were placed on the treated plants and an equivalent set of unmanipulated controls, and their growth and survivorship were measured. Forty-eight percent of caterpillars died over a 2-d period on unmanipulated plants with many ants, while only 20, 22, and 23% died on unmanipulated plants with few ants, Tanglefoot-treated branches with many ants outside the Tanglefoot barrier, and Tanglefoot-treated branches with few ants outside the Tanglefoot barrier, respectively. This suggests that ants were the only significant walking predator of Heliconius ismenius caterpillars in this habitat, and that z75% of the deaths observed on control plants were on plants with ants. After 4 d all caterpillars were replaced by a second set of caterpillars. Measurements of these latter individuals revealed that mortality was 62, 46, and 24% on control plants on which caterpillars previously survived for 0, 2, and 4 d, respectively. No trend was observed on branches with ants excluded. This indicates that the effects of ant predation are locally stable, i.e., that ant constancy causes plants to be heterogeneous in their suitability as host plants. Caterpillars thus are much more likely to survive on some plants than on others. Analysis of caterpillar growth rates did not reveal any effects on survival; i.e., slow-growing caterpillars survived as well as fast-growing ones.

Patterns of pollen exploitation by Heliconius butterflies

SummaryWe have studied pollen feeding habits of ten species of Heliconius butterflies in six major study areas in Trinidad and Costa Rica, and examined inter-species differences in pollen utilization under greenhouse conditions. We found:1.Females collected significantly more pollen than males.2.Older individuals generally collected significantly more pollen than younger individuals.3.Amount of pollen collected may vary significantly through time at a single site, apparently because of changing weather conditions.4.Amount of pollen collected may vary significantly between species at a single site at a given time, apparently because of differences in per capita resource availability to species using different habitats.5.Different species had significantly differing abilities to exploit small grained or large grained pollens, which resulted in significant differences in mean pollen collected at different sites by the same species.6.Species exploiting both large and small grained pollens showed significant differences through time in the ratio of large to small grained pollens utilized.

Heliconius Caterpillar Mortality during Establishment on Plants With and Without Attending Ants

Rates of disappearance (mortality) in Heliconius caterpillars of various sizes were investigated by experimental placement on Passiflora host plants growing in their native rain forest habitat. Survivorship of experimental larvae was similar to that of Heliconius larvae in natural populations: 60% mortality during the initial 2 d, followed by 30% mortality during each 2—d period thereafter. Survivorship was not dependent on larval size or instar, nor was it related to larval growth rate or host plant isolation from surrounding foliage. However, survivorship was appreciably lower on host plants on which ants were attending extrafloral nectaries (70% vs. 45% mortality in first 2 d), indicating that ants may be a primary source of high mortality. I conclude that for these Heliconius, high first—instar mortality is not due to the small size of the caterpillars but rather is a consequence of ant attendance to some host plants; most caterpillars on plants with ants are killed in the first instar, while caterpillars on ant—free plants have much lower mortality and make up the majority of the cohort in later instars.

Effects of Temperature on Physiology and Reproductive Success of a Montane Leaf Beetle: Implications for Persistence of Native Populations Enduring Climate Change

Understanding how climate change impacts natural systems requires investigations of the effects of environmental variation on vulnerable species and documentation of how populations respond to change. The willow beetle Chrysomela aeneicollis is ideal for such studies. It lives in California’s Sierra Nevada on the southern edge of its worldwide range. Beetles experience elevated air temperatures during summertime egg laying and larval development. Exposure to these temperatures causes physiological stress, which may reduce reproductive success and endanger populations. The glycolytic enzyme phosphoglucose isomerase (PGI) is a marker of temperature adaptation in C. aeneicollis. PGI allele frequency varies across a latitudinal gradient: allele 1 is common in Rock Creek (RC), which is cooler and to the north, and allele 4 is common in Big Pine Creek (BPC), which is warmer and to the south. In populations that are intermediate in geography and climate (e.g., Bishop Creek [BC]), PGI‐4 frequency increases from north to south such that alleles 1 and 4 are in relatively equal frequency in southern BC. Over the past decade, Sierra Nevada beetle populations have colonized high elevations and have become extinct at lower elevations where they were once common. In BC, the magnitude of PGI allele frequency fluctuations among life‐history stages is related to maximal air temperature, with the frequency of PGI‐4 increasing after the hottest part of summer. To identify mechanisms that may cause shifts in PGI allele frequency, we measured metabolic rate and fecundity for beetles collected at BC. Metabolic rate of males and females was measured at 20° and 36°C using flow‐through respirometry. To measure laboratory fecundity, mating pairs were acclimated for 4 h each afternoon at a control temperature (20°C) or at mildly elevated temperatures (26° or 32°C) and number of eggs laid was counted daily for 24 d, after which tissue levels of 70‐kD heat shock proteins (Hsp70) were determined. Previous studies had demonstrated differences in Hsp70 expression among PGI genotypes at these temperatures. To measure field fecundity, mating pairs from BC were transplanted to similar elevations in BPC, BC, and RC and were monitored in situ for 24 d. Metabolic rate was higher for PGI 4‐4 genotypes than for PGI 1‐4 or PGI 1‐1 individuals at 36°C but not at 20°C. In contrast, laboratory fecundity was greatest for females possessing PGI‐1, independent of acclimation temperature. At the end of the laboratory fecundity experiment, Hsp70 expression was positively related to fecundity, suggesting minimal reproductive cost of upregulation of heat shock proteins in response to mild heat stress. In the field, fecundity was highest for PGI 1‐1 and PGI 1‐4 individuals in RC and PGI 4‐4 individuals in BPC and was similar for all genotypes in BC. Thus, fecundity in nature was greatest for the genotypes that were most common in each area. Taken together, data reported here suggest that hot, dry summers in the Sierra Nevada may result in an increase in frequency of the PGI‐4 allele and shifts to higher elevations for C. aeneicollis populations.

Predator protection versus rapid growth in a montane leaf beetle

SummaryAdults and larvae of Chrysomela aenicollis (Coleoptera: Chrysomelidae) feed on foliage of Salix species (Salicaceae) between 2,400–3,400 m above sea level in the eastcentral Sierra Nevada mountains of California. We predicted that (1) cold climatic conditions would be a more frequent source of mortality at higher elevations, (2) mildweather agents of mortality such as predation should be more severe at lower elevations, and (3) populations of C. aenicollis would be adapted to the local selective regime at each elevation. We tested these predictions in 1984 and 1985 by transferring over 6,000 eggs and larvae within and between two sites at 2,810 and 3,240 m elevation above sea level. During mild summer weather at both sites, survivorship on Salix branches isolated by a barrier of sticky resin was similar to that on control branches, and we concluded that aerial predators were the primary cause of mortality. At least one major predator, a solitary wasp (Symmorphus sp., Hymenoptera: Eumenidae), was specifically associated with C. aenicollis at the lower site, where beetle mortality was highest. At both sites in 1984 and 1985, larvae originating from the lower site remained in aggregations and survived more frequently than larvae from the upper site, suggesting that they are better defended against predators. During a storm with cold weather late in the 1984 season, larvae and pupae died more frequently at the upper site, and there was a marginally significant trend (P<0.1) for the lower site individuals to die more frequently than upper site larvae during the cold storm. Upper site larvae grew approximately 10% faster than lower site larvae at the lower site and under controlled conditions in the laboratory. These findings indicate that upper and lower site populations were adapted to the local selective regime, which suggest how populations of montane phytopagous insects may adapt to changing elevations.

Local distribution of the lycaenid butterfly, Jalmenus evagoras, in response to host ants and plants

SummaryThe caterpillars of Jalmenus evagoras are tended by ants as they feed upon Acacia trees. In the area of Brisbane, Australia, J. evagoras require ants of the Iridomyrmex anceps species group; predation and parasitism are so intense that larvae and pupae deprived of attendant ants cannot survive (Pierce 1983). We investigated the efficiency with which J. evagoras locate and exploit the “host ant” resource by sampling 737 quadrats in 30 sampling grids and six study sites containing appropriate host plants; ants were collected at baits located in the center of each quadrat. J. evagoras was found in all habitats where I. anceps cooccurred with host Acacia. Nine of the ten sampling grids which had three or more I. anceps/Acacia “host” quadrats also had colonies of J. evagoras present (or immediately adjacent), including sites as far as 35 km apart. Of 19 sampling grids on which “host” quadrats were rare (i.e., less than three quadrats), none had J. evagoras (P<0.001). Within sample grids, I. anceps was distributed indepedently from Acacia trees, suggesting that they are not dependent for their survival on either Acacia or on J. evagoras. Within montane pasture habitats, I. anceps and at least one other ground-dwelling Iridomyrmex species were distributed in mutually exclusive “ant mosaic” territories which were stable during a one month period. I. anceps did not colonize or tend pupae of J. evagoras experimentally placed in adjacent territories of a different, nontending species of Iridomyrmex, demonstrating the integrity of territory boundaries. Sampling of ants in Acacia trees revealed that, in the absence of J. evagoras, Iridomyrmex workers are not common above ground level, and that their numbers decline in larger trees (P=0.02). In I. anceps territories, eight of nine J. evagoras pupae placed in trees over 3.0 m tall were not found after 24 h whereas all ten controls placed in low trees were found and tended (P=0.00012). This may explain why J. evagoras tends to oviposit in trees less than 2.0 m tall. An alternative hypothesis, that smaller trees have higher content of total nitrogen, and are threfore more nutritious, was not supported. We conclude that the local distribution and host tree selection by J. evagoras is dependent upon the distribution, patchiness, and foraging behavior of the host ant, I. anceps, and its spatial overlap with a number of species of host Acacia.

Nesting Behavior and Prey Use in Two Geographically Separated Populations of the Specialist Wasp Symmorphus cristatus (Vespidae: Eumeninae)

Abstract The food web of Symmorphus cristatus wasps, leaf beetle larvae (Coleoptera: Chrysomelidae) and willow (Salix spp.) trees is a model system for studying the chemical ecology of plant, herbivore and predator interactions. However, little is known about the natural history and prey use of the predatory wasps. We conducted detailed observations of nesting behavior and quantified time allocation to nest building activities in Big Pine Creek in the eastern Sierra of California. Symmorphus cristatus exhibits aggressive territorial behavior over nesting and mating sites, but does not respond aggressively to kleptoparasitism by cuckoo wasps Chrysis nitidula. We also compared prey use, nest provisioning and nest architecture of wasps at Big Pine Creek and at Sebastopol, near the central California coast. Using trap-nests we identified two new prey species for S. cristatus at Sebastopol: Plagiodera californica and Chrysomela schaefferi (Coleoptera: Chrysomelidae). There were significant differences in nest architecture for the two allopatric wasp populations and, although they do not use the same prey species, populations did not differ in the mean mass of prey provided for each offspring. Five other cavity-dwelling insect species pre-empted nest sites in Sebastopol. Prey species in Sebastopol differ in the chemistry of their larval secretion. The main component of C. schaefferi secretion is salicylaldehyde, which is derived from the willow host plants. Plagiodera californica secretion contains (epi)plagiolactone, an autogenously produced monoterpene-based defensive secretion. This is the first evidence that S. cristatus uses prey larvae that possess a monoterpene-based secretion.