Biology and occurrence of Inga Busk species (Lepidoptera: Oecophoridae) on Cerrado host plants

We sampled Inga Busk species caterpillars weekly in the cerrado on 15 plants of Diospyros burchellii Hern. (Ebenaceae) from January 2002 to December 2003, on 30 plants of Caryocar brasiliense (Caryocaraceae) from July 2003 to June 2004, and since 1991 on several other plant species. In total we found 15 species of Inga on cerrado host plants. Nine species were very rare, with only one to five adults reared. The other six species occurred throughout the year, with higher abundance during the dry season, from May to July, coinciding with overall peaks of caterpillar abundance in the cerrado. Caterpillars of the genus Inga build shelters by tying and lining two mature or old leaves with silk and frass, where they rest and develop (a common habit found in Oecophorinae). The final instar builds a special envelope inside the leaf shelter, where it will complete the larval stage and pupate. The species are very difficult to distinguish in the immature stages. External features were useful in identifying only four species: I. haemataula (Meyrick), I. phaecrossa (Meyrick), I. ancorata (Walsingham), and I. corystes (Meyrick). These four species are polyphagous and have wide geographical distributions. In this paper we provide information on the natural history and host plants of six Inga species common on cerrado host plants, for which there are no reports in the literature.     

Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna

1. Predatory ants may reduce infestation by herbivorous insects, and slow‐moving Lepidopteran larvae are often vulnerable on foliage. We investigate whether caterpillars with morphological or behavioural defences have decreased risk of falling prey to ants, and if defence traits mediate host plant use in ant‐rich cerrado savanna. 2. Caterpillars were surveyed in four cerrado localities in southeast Brazil (70–460 km apart). The efficacy of caterpillar defensive traits against predation by two common ant species (Camponotus crassus, C. renggeri) was assessed through experimental trials using caterpillars of different species and captive ant colonies. 3. Although ant presence can reduce caterpillar infestation, the ants' predatory effects depend on caterpillar defence traits. Shelter construction and morphological defences can prevent ant attacks (primary defence), but once exposed or discovered by ants, caterpillars rely on their size and/or behaviour to survive (secondary defence). 4. Defence efficiency depends on ant identity: C. renggeri was more aggressive and lethal to caterpillars than C. crassus. Caterpillars without morphological defences or inside open shelters were found on plants with decreased ant numbers. No unsheltered caterpillar was found on plants with extrafloral nectaries (EFNs). Caterpillars using EFN‐bearing plants lived in closed shelters or presented morphological defences (hairs, spines), and were less frequently attacked by ants during trials. 5. The efficiency of defences against ants is thus crucial for caterpillar survival and determines host plant use by lepidopterans in cerrado. Our study highlights the effect of EFN‐mediated ant‐plant interactions on host plant use by insect herbivores, emphasizing the importance of a tritrophic viewpoint in risky environments.     

Fitness costs and benefits of shelter building and leaf trenching behaviour in a pyralid caterpillar

1. Shelter building and petiole trenching in the Lepidoptera is a behaviour that mediates ecological pressures including those exerted by both food plants and natural enemies. 2. Fitness costs and benefits of trenching and shelter‐building behaviour related to predation and larval performance were investigated in a pyralid species that inhabits and feeds on leaf shelters. 3. Assays comparing the performance of caterpillars feeding on trenched versus non‐trenched foliage and fresh versus dry leaves were conducted. Whereas pupal weight was positively affected by petiole trenching, larval development was delayed when caterpillars fed on dry leaves. 4. A field experiment comparing predation on caterpillars inside and outside shelters demonstrated that predation was significantly higher for exposed caterpillars. 5. No physiological costs associated with shelter building were found given that caterpillars performed equally regardless of the number of shelters they built. 6. The effect sizes of top‐down and bottom‐up forces on pupal weight, development time, and predation risk indicated that the major effect of shelters is through the reduction of predation risk. The integration of experiments and natural history observations showed that fitness benefits provided by shelters change across ontogeny.     

Temporal and spatial variation of Stenoma cathosiota Meyrick (Lepidoptera: Elachistidae) caterpillar abundance in the cerrado of Brasilia, Brazil

The caterpillars of Stenoma cathosiota Meyrick feed on Roupala montana Aubl. (Proteaceae) in the cerrado of the Distrito Federal, Brazil. They construct shelters by joining leaves of the plant where they feed and pupate. The caterpillars are parasitized by a wasp (Hymenoptera: Brachonidae), which emerges from the pupae. Caterpillar abundance and parasitism frequency were associated in an area of frequently burned cerrado (biennial fire) and in another area that burns sporadically (1987 and 1994). For S. cathosiota, the variation among years in a single area, with sporadic fires, was greater than the variation among areas with different fire regimes. Caterpillar abundance among years was significantly different in the area that burns sporadically (chi2 = 24.06; df. = 1; P = 0.000). However, there were no significant differences on caterpillar abundance between areas for the same period (chi2 = 3.45; df. = 1; P = 0.063). Parasitism frequency was high, reaching 29% of the collected caterpillars, and did not differ among areas. The great temporal variation in abundance of lepidopteran caterpillars in the cerrado makes it difficult to determine the effects that fire exerts over this fauna.     

Host ontogeny determines parasitoid use of a forest caterpillar

For most organisms, patterns of natural enemy‐mediated mortality change over the course of development. Shifts in enemy pressure are particularly relevant for organisms that exhibit exponential growth during development, such as juvenile insects that increase their mass by several orders of magnitude. As one of the dominant groups of insect herbivores in most terrestrial plant communities, larval lepidopterans (caterpillars) are host to a diverse array of parasitoids. Previous research has described how the frequency of herbivore parasitism varies among host plants or habitats, but much less is known about how parasitism pressure changes during host development. To test whether the two major parasitoid taxa, wasps and flies, differentially attack shared hosts based on host developmental stage, we simultaneously exposed early‐ and late‐instar Euclea delphinii Boisduval (Lepidoptera: Limacodidae) caterpillars to parasitism in the field. We found strong evidence that parasitoids partition hosts by size; adult female wasps preferentially parasitized small caterpillars, whereas adult female flies preferred to attack large caterpillars. Our results demonstrate that host ontogeny is a major determinant of parasitoid host selection. Documenting how shifts in enemy pressure vary with development is important to understanding both the population biology and evolutionary ecology of prey species and their enemies.     

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.     

Seasonal variation in diet breadth of folivorous Lepidoptera in the Brazilian cerrado

Documented patterns of specialization and species interactions often omit plasticity in resource use across space and time, yet such variation is an important part of species interactions. To examine temporal variation in resource use, we compared species‐ and community‐level patterns of host plant use by folivorous caterpillars between the dry and rainy seasons in four preserved areas of cerrado vegetation in the Distrito Federal, Brazil. We sampled plants and caterpillars in 10 m circular plots monthly from March 2010 to March 2011. At the community level, we found a significant increase in the mean diet breadth of dry season caterpillars relative to those collected in the rainy season. Families and species of moths varied in diet breadth, but most exhibited a seasonal expansion. In particular, intraspecific comparisons showed a 30% increase in the number of host plants used in the dry season compared to the rainy season. These results provide a clear example of how temporal variation in resource use is heterogeneous, and more generalized patterns of resource use can emerge from studies at large temporal scales. Thus, seasonal or annual heterogeneity may obscure ecologically relevant specialized interactions that occur at smaller scales.     

Long-term seasonal fluctuations of lepidopteran cereal stemborers and their natural enemies on maize and wild host plants in southern Benin

Abstract  The seasonal fluctuation of lepidopteran cereal stemborers on maize and wild host plants (i.e., grasses and a few sedges) was investigated in southern Benin from 1988 to 1998 by time series analysis and repeated-measures analysis of variance (ANOVA). In addition, a walk-in light trap was used to study the flight behavior of adult moths. On both cereals and grasses, the noctuid Sesamia calamistis was the predominant species, followed by the pyralid Eldana saccharina . The noctuid Busseola fusca was rare on both maize and wild host plants. In general, pest populations increased during the course of the year to reach peak densities during the second short rainy season, and then crashed to close to zero during the dry season. On wild host plants, egg masses and other immature stages were collected throughout the year but they were higher on wild grasses than maize during the off-season. Thus wild host plants can be considered as refuge for both borers and natural enemies during the off-season, when maize is not available. However, only four out of the eleven wild host species played a discernable role. S. calamistis egg densities appeared to be influenced by density-dependent factors, suggesting an effect of natural enemies. Temperature and rainfall had a negative effect on egg abundance. Larval parasitism by a Kenyan strain of the braconid Cotesia sesamiae , which was released in southern Benin in the early 1990s, and by the tachinid Sturmiopsis parasitica varied between seasons and years but there were no discernable patterns. For both parasitoids and borer host species, parasitism was positively correlated with trap catches of adult moths. The recovery of C. sesamiae during a 2-year period suggests that the parasitoid has established its population in southern Benin.     

Predicting the effects of climate change on natural enemies of agricultural pests

Climate change can have diverse effects on natural enemies of pest species. Here we review these effects and their likely impacts on pest control. The fitness of natural enemies can be altered in response to changes in herbivore quality and size induced by temperature and CO₂ effects on plants. The susceptibility of herbivores to predation and parasitism could be decreased through the production of additional plant foliage or altered timing of herbivore life cycles in response to plant phenological changes. The effectiveness of natural enemies in controlling pests will decrease if pest distributions shift into regions outside the distribution of their natural enemies, although a new community of enemies might then provide some level of control. As well as being affected by climate through host plants and associated herbivores, the abundance and activity of natural enemies will be altered through adaptive management strategies adopted by farmers to cope with climate change. These strategies may lead to a mismatch between pests and enemies in space and time, decreasing their effectiveness for biocontrol. Because of the diverse and often indirect effects of climate change on natural enemies, predictions will be difficult unless there is a good understanding of the way environmental effects impact on tritrophic interactions. In addition, evolutionary changes in both hosts and natural enemies might have unexpected consequences on levels of biocontrol exerted by enemies. We consider interactions between the pest light brown apple moth and its natural enemies to illustrate the type of data that needs to be collected to make useful predictions.     

Elevational contrast in predation and parasitism risk to caterpillars in a tropical rainforest

Invertebrate predators and parasitoids are among the most important natural enemies of insect herbivores. Yet, the strength of natural enemy pressure along an altitudinal gradient and interactions between the groups of natural enemies (such as predation on parasitized prey) are not well known. Various methods are used to reveal the mortality factors of herbivores. Predation pressure is usually assessed through exposure of artificial prey. However, this method cannot provide information about the attacks of parasitoids, or their eventual interactions with predators. Furthermore, artificial or dead prey might not attract predators because they do not show expected host behavior, and this method mostly cannot distinguish between predation and scavenging. For the first time in a tropical rainforest, we quantified elevational contrast in mortality factors using exposure of live caterpillars. We exposed a total of 800 live caterpillars of Talanga excelsalis moresbyensis Strand (Lepidoptera: Crambidae) on saplings of Ficus copiosa Steud. (Moraceae) at two elevations in primary tropical rain forest in Papua New Guinea (200 and 1 200 m a.s.l.). We exposed the caterpillars in two treatments: exposed to and protected from invertebrate predators and parasitoids. Disappearance of caterpillars was significantly higher in the exposed treatment. Furthermore, caterpillar disappearance was significantly higher in lowlands than in highlands (43 vs. 12%). We consider the vast majority of the disappearance to be due to predation, as migration of the caterpillars from the focal trees was not observed (except one caterpillar). This estimate of invertebrate predation rate corresponds with studies which used artificial caterpillar models. No significant difference in parasitism rate between the two elevations was observed (12 vs. 13%). The combination of the disappearance and parasitism rate patterns means that larval parasitoids face stronger pressure from invertebrate predators through higher predation of their hosts in the lowlands than in the highlands.     

Indirect interactions mediated by leaf shelters in animal–plant communities

Leaf shelters indirectly mediate interactions in animal–plant communities by providing the occupants with several kinds of benefits, as physical ecosystem engineering. The occupants benefit from favorable microhabitat, reduction in antiherbivore defense, and protection from natural enemies. The primary shelter maker has to spend energy and time and producing silk, but shelter users have great advantages without incurring costs. Shelter users consist of a wide range of arthropod taxa and can be divided into two groups: coexisting organisms that live with a primary shelter maker in the same shelter, and secondary users, which inhabit a leaf shelter after it is utilized by a shelter maker. Leaf shelters mediate interactions between (1) primary shelter makers and coexisting organisms or (2) primary shelter makers and secondary users, (3) secondary users, (4) shelter users and their natural enemies, and (5) primary shelter makers, secondary users, and their host plants. Most interactions between primary shelter makers and coexisting organisms constitute a direct trophic linkage rather than indirect ones. There are actually unidirectional beneficial effects from a primary shelter maker to secondary shelter users, whereas leaf shelters mediate competition and predation among shelter users. By providing a leaf shelter, a shelter maker leads to increased diversity of interactions. Leaf shelters modify the distribution of organisms on the host plant and influence herbivory on the host plant. In tritrophic interactions, leaf shelters act as cues for natural enemies that search for a shelter user as prey. Furthermore, by enhancing habitat heterogeneity, leaf shelters affect the abundance and species richness of arthropods on host plants. Received: July 24, 2000 / Accepted: February 15, 2001     

The relative importance of resources and natural enemies in determining herbivore abundance: thistles, tephritids and parasitoids

1. The relative importance of host-plant resources and natural enemies in influencing the abundance of insect herbivores was investigated in potted plant and natural population experiments, using tephritid (Diptera: Tephritidae) flies, their host plant, creeping thistle Cirsium arvense, and their Hymenoptera parasitoids. 2. Experimental manipulation of host-plant quality (i.e. levels of host-plant nutrients) and resource availability (i.e. the number of buds) increased tephritid abundance. There was no evidence that the seed-feeding tephritid fly Xyphosia miliaria preferentially oviposited on fertilized C. arvense. 3. At low thistle densities, X. miliaria showed a constant rate of resource exploitation. At higher thistle densities, a threshold was detected, above which additional buds were not attacked. 4. Parasitism attack was variable across host (tephritid) densities but levels of parasitism were consistently higher on the fertilized thistles. 5. Experimental manipulation of host-plant quality and resource availability (quantity) not only directly affects the tephritid population but also, indirectly, leads to high rates of parasitism. Both chemical and physical characteristics of host plants affect the performance of natural enemies. 6. Both top-down and bottom-up forces act to influence tephritid abundance, with bottom-up influences appearing to be the most important.     

Costly leaf shelters protect moth pupae from parasitoids

Many caterpillars construct shelters by folding leaves and feeding from within. Many shelter-constructing species suffer high rates of parasitism as larvae or pupae. In spite of the likely significance, the effects of these shelters on the survival of pupae and the trade-off between feeding and constructing shelters have attracted little experimental attention. In both field and laboratory experiments, fern-feeding caterpillars [Herpetogramma theseusalis (Walker) (Lepidoptera: Crambidae)] invested heavily in shelters, losing weight and significantly delaying pupation rather than feeding or pupating in exposed locations. Experimentally thinning the walls of shelters in the field doubled the parasitism rate. Parasitism of pupae exceeded predation by an order of magnitude or more in both seasons of this study. Caterpillars constructed similarly sized shelters regardless of availability of fern fronds, resulting in incomplete shelters on especially small fronds, putting pupae at increased risk of parasitism. We suggest that similar interactions are common and merit more attention.     

Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities

Ant dominance in tropical ecosystems can be explained by a capacity to exploit liquid foods such as extrafloral nectaries (EFNs) and secretions from honeydew-producing hemipterans (HPHs). Such nutritious exudates may determine ant distribution in space and shape specialization in ant–plant interactions. We provide a first assessment of how EFNs and HPHs mediate the structure of ant assemblages, ant visitation intensity, and characteristics of ant–plant interaction networks across space in Brazilian “cerrado” savanna. We used arboreal pitfall traps to sample visiting ants in four cerrado localities and recorded the presence of lepidopteran larvae to determine their possible response to ant visitation. Ant species composition and richness did not differ regardless of the presence of liquid rewards on plants, and most network patterns did not show consistent differences. However, in two of the four sites, ant densities were higher on plants with HPHs or EFNs due to increased activity by Camponotus and Pseudomyrmex ants. At these two sites, plants with liquid food sources had a more specific ant assemblage (higher specialization d′) than did plants without resources, and caterpillars were more frequently found on plants with fewer workers of Camponotus and Pseudomyrmex. Plants with HPHs had increased ant visitation and accumulated more ant species than did plants with EFNs or without liquid foods. Ant response to such food sources may thus depend on local conditions and identity of ant species, and may determine how ant assemblages are structured. Results highlight how different patterns of ant visitation to liquid resources can produce distinctive effects on herbivore infestation.     

Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Diversity and specificity of host‐natural enemy interactions in an urban‐rural interface

1. Urbanisation and agricultural intensification cause the replacement of natural ecosystems but might also create novel habitats in urban and rural ecosystems promoting some insect communities by providing food and nesting resources. 2. This study investigated how host–natural enemy communities change in urban and rural landscapes and their transitional zone, the urban–rural interface, by using trap nests for cavity‐nesting Hymenoptera in gardens and rapeseed fields that were either isolated or paired in the urban–rural interface. 3. Host dynamics were important for natural enemy occurrence, species richness and parasitism rates, and landscape effects were evident for natural enemy variables except for the richness of bee natural enemies. The number of parasitised brood cells was at its highest in the urban–rural interface, but the highest parasitism rates of bees were observed in isolated gardens. Parasitism rates of bees were negatively affected by host abundance, while parasitism rates of wasps were positively affected. 4. Higher specialisation and lower connectivity of host–natural enemy interactions were found in paired habitats than in isolated habitats. This indicates that paired habitats comprise more specific natural enemies and vulnerable interactions, while isolated habitats comprise more generalist natural enemies, and thus interactions appear more stable. 5. These results confirm that host dynamics play an essential role in the abundance and richness of natural enemies and drive parasitism. However, high habitat heterogeneity found in the urban–rural interface can also have an effect on host–natural enemy communities. This highlights that the provisioning of resources in the urban–rural interface can benefit insect communities in these areas.     

Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar

Although many organisms show daily rhythms in their activity patterns, the mechanistic causes of these patterns are poorly understood. Here we show that host plant volatiles affect the nocturnal behavior of the caterpillar Mythimna separata. Irrespective of light status, the caterpillars behaved as if they were in the dark when exposed to volatiles emitted from host plants (either uninfested or infested by conspecific larvae) in the dark. Likewise, irrespective of light status, the caterpillars behaved as if they were in the light when exposed to volatiles emitted from plants in the light. Caterpillars apparently utilize plant volatile information to sense their environment and modulate their daily activity patterns, thereby potentially avoiding the threat of parasitism.     

Effects of variation among plant species on the interaction between a herbivore and its parasitoid

Abstract.  1. Previous studies have demonstrated that phenotypic traits of plants have the potential to affect interactions between herbivores and their natural enemies. Consequently, the impact of natural enemies on herbivore vital rates and population dynamics may vary among plant species. This study was designed to investigate the potential for density-dependent parasitism of an aphid herbivore feeding on six different host plant species.
2. Population densities of the aphid Aphis nerii B de F (Homoptera: Aphididae) and its parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) were recorded within a single growing season on six different species of milkweed in the genus Asclepias L. (Asclepiadaceae). Asclepias species are known to vary in their quality as food for herbivores. Although data on plant quality were not available in this study, population data were analysed to determine the effects of different Asclepias species on rates of parasitism and aphid population growth.
3. Parasitism rates of A. nerii varied among Asclepias species but were temporally density dependent over at least some range of aphid density on all plant species. Aphid population growth rates also varied among Asclepias species, and declined with an increase in the maximum parasitism rates among plant species; however, in no case was density-dependent parasitism sufficient to prevent exponential population growth of aphids within the growing season. The results serve to emphasise that, if natural enemies are to regulate herbivore populations, density-dependent mortality is a necessary, but not sufficient, condition for regulation.