Geographical variation in parasitism shapes larval immune function in a phytophagous insect

Two of the central goals of immunoecology are to understand natural variation in the immune system among populations and to identify those selection pressures that shape immune traits. Maintenance of the immune system can be costly, and both food quality and parasitism selection pressure are factors potentially driving immunocompetence. In tritrophic interactions involving phytophagous insects, host plants, and natural enemies, the immunocompetence of phytophagous insects is constrained by selective forces from both the host plants and the natural enemies. Here, we assessed the roles of host plants and natural enemies as selective pressures on immune variation among natural populations of Lobesia botrana. Our results showed marked geographical variation in immune defenses and parasitism among different natural populations. Larval immune functions were dependent of the host plant quality and were positively correlated to parasitism, suggesting that parasitoids select for greater investment into immunity in moth. Furthermore, investment in immune defense was negatively correlated with body size, suggesting that it is metabolically expensive. The findings emphasize the roles of host plants and parasitoids as selective forces shaping host immune functions in natural conditions. We argue that kinds of study are central to understanding natural variations in immune functions, and the selective forces beyond.     

Impact of variable nitrogen fertilisation on arthropods in cotton in Georgia, USA

Reducing fertiliser applications can reduce production costs for cotton (Gossypium hirsutum L.) growers, as well as nitrogen (N) leaching into the soil and contamination of surface and ground water. But altered N fertilisation may also affect pests and their natural enemies. In this study, plots with four different levels of fertiliser input (0, 45, 90 and 135 kg ha⁻¹ N) were used to investigate the influence of N on cotton pest and beneficial arthropod populations, and on cotton yield in Tifton, GA, USA. We predicted that (1) N fertilisation will correlate positively with cotton plant growth; (2) increased N fertilisation will increase pest populations because plants with more N will be more nutritious for and attractive to herbivores; (3) populations of beneficial arthropods and predation of pests will decline with increased N fertilisation because of reduced plant signaling; (4) increased N fertilisation will increase pest mortality due to parasitoids because of increased host quality. Cotton plant growth was enhanced by N fertilisation but yield was unaffected. N fertilisation significantly affected some pest arthropods but inconsistently. Mirids were most abundant in the high N treatment in 1 year of the study and cotton aphids were most abundant in the highest N treatment in the other year of the study. Arthropod predators were generally more abundant in the high N treatment but only spiders and Geocoris spp. were significantly affected by N treatment, with highest numbers present in the highest N treatment but the significant differences were each only in a single year. The greatest mortality of sentinel pest eggs (Spodoptera exigua) due to predation occurred under low N conditions. N fertilisation had no significant effects on parasitism of feral or sentinel caterpillars.     

What’s the buzz? Ultrasonic and sonic warning signals in caterpillars of the great peacock moth (Saturnia pyri)

Caterpillars have many natural enemies and, therefore, have evolved a diversity of antipredator strategies. Most research focuses on those strategies (crypsis, countershading, and warning coloration) targeting visually guided predators. In contrast, defensive sounds, although documented for more than a century, have been poorly studied. We report on a novel form of sound production—chirping—in caterpillars of the common European Great Peacock moth (Saturnia pyri). Chirps are broadband, with dominant peaks ranging between the sonic (3.7 kHz) and ultrasonic (55.1 kHz) and are generated by a rapid succession of mandibular “tooth strikes.” Chirp trains are induced by simulated predator attacks and precede or accompany the secretion of a defensive chemical from integumental bristles, supporting our hypothesis that these sounds function in acoustic aposematism. We propose that these caterpillars generate multimodal warning signals (visual, chemical, and acoustic) to target the dominant sensory modalities of different predators, including birds, bats, and invertebrates. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Field vole (Microtus agrestis) seasonal spacing behavior: the effect of predation risk by mustelids

There are numerous studies showing that predation risk may change different aspects of the behavior of prey, such as habitat use, activity pattern, and foraging. Prey should exhibit the strongest antipredatory response against their most deadly predator. Small mustelids are considered the most important mammalian predators of voles. Nevertheless, there is no general agreement as to whether strong antipredatory reactions exist in natural free-living populations of voles. Here, we studied the field vole Microtus agrestis spatial reaction to high predation risk from small mustelids in the breeding (August) and nonbreeding (October) seasons under natural conditions. Voles were exposed to a caged weasel (Mustela nivalis) and a stoat (Mustela erminea), as well as to the odors of these predators. The reactions of 30 field voles were monitored with radiotelemetry. The field voles were found to display antipredator reactions that varied with season. In the breeding period, in response to predation risk, voles reduced locomotory activity and daily-range size, whereas in the nonbreeding period they did not. Changes in home range position were similar for control and treatment voles, in both the breeding and nonbreeding periods. The results indicate that mustelid predators modify the spatial behavior of small rodents in natural conditions depending on season. This might be a reflection of differences in state-dependent responses to predation from sexually active or inactive individuals. This suggests that the basic antipredatory reaction of voles under high predation risk from small mustelids limits their locomotory activity.     

Indirect interactions between a phytopathogenic and an entomopathogenic fungus

Slow growth in herbivores may lead to higher mortality, due to prolonged exposure to natural enemies. A number of studies has tested the 'slow-growth, high-mortality' hypothesis using predators or parasitoids as natural enemies of the herbivore, but the possible role of pathogens is poorly documented. We provide evidence that phytopathogenic infection of a plant enhances the susceptibility of herbivore larvae to a generalist entomopathogen. Larvae of the mustard leaf beetle Phaedon cochleariae grow more slowly when feeding on Chinese cabbage leaves infected by the phytopathogenic fungus Alternaria brassicae than larvae feeding on healthy leaves. Treatment of such larvae feeding on diseased plants with an LD₅₀ of the entomopathogenic fungus Metarhizium anisopliae resulted in 100% mortality, compared with a mortality rate of 54% in the control larvae feeding on uninfected leaves. This is the first demonstration of an interaction between a phyto- and an entomopathogenic fungus.     

Development of a generalist predator,Podisus maculiventris,on glucosinolate sequestering and nonsequestering prey

Insect herbivores exhibit various strategies to counter the toxic effects of plant chemical defenses. These strategies include the detoxification, excretion, and sequestration of plant secondary metabolites. The latter strategy is often considered to provide an additional benefit in that it provides herbivores with protection against natural enemies such as predators. Profiles of sequestered chemicals are influenced by the food plants from which these chemicals are derived. We compared the effects of sequestration and nonsequestration of plant secondary metabolites in two specialist herbivores on the development of a generalist predator, Podisus maculiventris. Profiles of glucosinolates, secondary metabolites characteristic for the Brassicaceae, are known to differ considerably both inter- and intraspecifically. Throughout their immature (=nymphal) development, the predator was fed on larval stages of either sequestering (turnip sawfly, Athalia rosae) or nonsequestering (small cabbage white butterfly, Pieris rapae) prey that in turn had been feeding on plants originating from three wild cabbage (Brassica oleracea) populations that have previously been shown to differ in their glucosinolate profiles. We compared survival, development time, and adult body mass as parameters for bug performance. Our results show that sequestration of glucosinolates by A. rosae only marginally affected the development of P. maculiventris. The effects of plant population on predator performance were variable. We suggest that sequestration of glucosinolates by A. rosae functions not only as a defensive mechanism against some predators, but may also be an alternative way of harmlessly dealing with plant allelochemicals.     

Mortality of pollen beetle (Meligethes spp.) larvae due to predators and parasitoids in rape fields and the effect of conservation strips

In 1996–1999, different mortality factors of pollen beetle larvae were investigated in twenty six rape fields in the northern part of Switzerland which had either a wild flower strip or an extensively managed meadow adjacent to the long side of the field. At 3 and 30 m into the crop from the conservation strip, total mortality, mortality from predators, parasitoids and unspecified factors were measured. Total pollen beetle larval mortality was 66–96%. Mortality caused by predators was 16–27% and there was no significant difference between mortality at 3 m and that 30 m from the extensively managed meadows. However, in fields with wild flower strips adjacent to them, the percentage mortality from predators was significantly greater at 30 m than at 3 m. The range of parasitism of pollen beetle larvae was 0–54% and was on average greater at 3 m than at 30 m. In fields with wild flower strips, the percentage parasitism with Tersilochus heterocerus was significantly higher than in fields with extensively managed meadows. However, mortality from all parasitoids was only 1–2% and there was no significant difference between 3 and 30 m. The effect of parasitoids on pollen beetle mortality was masked by the high unspecified mortality and the mortality from predators. The unspecified mortality was 46–72% and was significantly greater in 1998 and 1999 than in 1996 and 1997. These differences are probably because of meteorological factors (wet in 1999 and dry in 1998). The possible influences of the two types of conservation strips on pollen beetle larval density were investigated. The results show that in fields with adjacent wild flower strips, the pollen beetle larvae were more evenly distributed (but not significantly so) than in fields with extensively managed meadows where larval density decreases faster from the edge into the rape field.     

Feeding repellence in Antarctic bryozoans

The Antarctic sea star Odontaster validus and the amphipod Cheirimedon femoratus are important predators in benthic communities. Some bryozoans are part of the diet of the asteroid and represent both potential host biosubstrata and prey for this omnivorous lysianassid amphipod. In response to such ecological pressure, bryozoans are expected to develop strategies to deter potential predators, ranging from physical to chemical mechanisms. However, the chemical ecology of Antarctic bryozoans has been scarcely studied. In this study we evaluated the presence of defenses against predation in selected species of Antarctic bryozoans. The sympatric omnivorous consumers O. validus and C. femoratus were selected to perform feeding assays with 16 ether extracts (EE) and 16 butanol extracts (BE) obtained from 16 samples that belonged to 13 different bryozoan species. Most species (9) were active (12 EE and 1 BE) in sea star bioassays. Only 1 BE displayed repellence, indicating that repellents against the sea star are mainly lipophilic. Repellence toward C. femoratus was found in all species in different extracts (10 EE and 12 BE), suggesting that defenses against the amphipod might be both lipophilic and hydrophilic. Interspecific and intraspecific variability of bioactivity was occasionally detected, suggesting possible environmental inductive responses, symbiotic associations, and/or genetic variability. Multivariate analysis revealed similarities among species in relation to bioactivities of EE and/or BE. These findings support the hypothesis that, while in some cases alternative chemical or physical mechanisms may also provide protection, repellent compounds play an important role in Antarctic bryozoans as defenses against predators.     

Tracking parasitoids with the stable isotope 44Ca in agroecosystems

Habitat management influences spatial and temporal distribution of parasitoids in farmland. The current work evaluates, for the first time, the potential of a novel marking technique using a calcium stable isotope (⁴⁴Ca) under field conditions. In two subsequent trials, ⁴⁴Ca-enriched Cotesia glomerata parasitoids were released into an organically managed cabbage field in a region known to harbor natural populations of this species. The trap plants infested with Pieris brassicae host larvae were distributed in the trial areas and collected 3 days after parasitoid release. Parasitism by released wasps was determined through calcium isotope analysis of the recovered caterpillars using inductively coupled plasma mass spectrometry (ICPMS). The spatial habitat use by female parasitoids was determined based on marked caterpillars on the trap plants. Both trials yielded relatively consistent results, showing that C. glomerata females dispersed over at least 50 m within 3 days. The total proportion of caterpillars parasitized by the marked wasps amounted to 32.4 and 24.4%, respectively, with no statistically significant difference. The potential of this approach for field investigations on habitat management and biological control is discussed.     

Prenatal cannibalism in an insect

Host selection and infection strategies of parasitoids often correlate with high parental investment and low numbers of progeny. In this study, we investigate how additional internal mechanisms might shape brood size and fitness of the offspring. Emblemasoma auditrix is a parasitoid fly in which about 38 larvae hatch simultaneously in utero. After host location, a single larva is deposited into the host, where it rapidly develops and pupates after about 5 days. The search for hosts can take several weeks, and during that time, the larvae arrest their development and remain in the first larval instar. Nevertheless, the larvae increase in weight within the uterus, and this growth correlates to a decrease in the number of larvae, although no larvae are deposited. Thus, our data indicate a first case of prenatal cannibalism in an invertebrate with larvae feeding on each other within the uterus of the adult.     

Pre-pupation behaviour of the aphid parasitoid <Emphasis Type="Italic">Aphidius ervi</Emphasis> (Haliday) and its consequences for pre-imaginal learning

Olfactory learning may occur at different stages of insect ontogeny. In parasitoid wasps, it has been mostly shown at adult emergence, whilst it remains controversial at pre-imaginal stages. We followed larval growth of the parasitoid wasp, Aphidius ervi Haliday, inside the host aphid, Acyrthosiphom pisum Harris, and characterised in detail the behaviour of third instar larvae. We found that just before cocoon spinning begins, the third instar larva bites a hole through the ventral side of the mummified aphid exoskeleton. We then evaluated whether this period of exposure to the external environment represented a sensitive stage for olfactory learning. In our first experiment, the third instar larvae were allowed to spin their cocoon on the host plant (Vicia faba L.) surface or on a plastic plate covering the portion of the host plant exposed to the ventral opening. Recently emerged adults of the first group showed a preference for plant volatiles in a glass Y-olfactometer, whereas no preference was found in adults of the second group. In a second experiment, during the period in which the aphid carcass remains open or is being sealed by cocoon spinning, third instar larvae were exposed for 24 h to either vanilla odours or water vapours as control. In this experiment, half of the parasitoid larvae were later excised from the mummy to avoid further exposure to vanilla. Adult parasitoids exposed to vanilla during the larval ventral opening of the mummy showed a significant preference for vanilla odours in the olfactometer, regardless of excision from the mummy. The larval behaviour described and the results of the manipulations performed are discussed as evidences for the acquisition of olfactory memory during the larval stage and its persistence through metamorphosis.     

Interactions of host-plant resistance in cotton with predators and parasites

Results from no-choice field and greenhouse studies established an inverse relationship between plant trichome density in cotton and the level of successful attacks on Heliothis zea (Boddie) eggs by the parasite, Trichogramma pretiosum (Riley) and the predator, Chrysopa rufilabris (Burmeister). Thus, plant damage from H. zea can be reduced on glabrous cotton phenotypes due to antixenosis and increased entomophage effectiveness compared to hirsute and pilose phenotypes. Studies by other scientists which demonstrate interactions of natural enemies with host-plant resistance in cotton are also discussed. Symbiotic relationships between the host-plant and its associated predator/parasitoid complex may significantly influence the expression of host-plant resistance in cotton. Scientists involved in programs for development of host-plant resistant cultivars are encouraged to utilize sources of resistance which increase effectiveness of key natural enemies of the major pest species.     

Field evidence for non-host predator avoidance in a manipulated amphipod

Manipulative parasites are known to alter the spatial distribution of their intermediate hosts in a way that enables trophic transmission to definitive hosts. However, field data on the ecological implications of such changes are lacking. In particular, little is known about the spatial coexistence between infected prey and dead-end predators after a parasite-induced habitat shift. Here, we used an Amphipoda (Gammarus roeseli)–Acanthocephala (Polymorphus minutus) association to investigate how infection with a manipulative parasite affects the predation risk by non-hosts within the invertebrate community. First, we collected invertebrates by sampling various natural habitats and calculated the distribution amplitude of amphipods according to their infection status. Infection with P. minutus significantly reduced the habitat breadth in G. roeseli, parasitised individuals being mainly found in floating materials whereas uninfected ones were widespread throughout the sampled habitats. Second, to test if these changes also affect the risk for P. minutus to be ingested by non-hosts, we estimated the predation risk experienced by G. roeseli within the macro-invertebrate community. The habitat overlap between potential invertebrate predators and G. roeseli showed that the spatial probability of encounter was lower for P. minutus-infected amphipods than for uninfected conspecifics. For the first time, to our knowledge, a study used ecological tools to bring field evidence for the spatial avoidance of dead-end predators in a manipulated amphipod.     

Potential for biological control of field bindweed in California's coastal vineyards

The possibility of using biological control against field bindweed, Convolvulus arvensis L., was studied in four vineyards along the California coast. Field bindweed is a dominant member of the weed community and the principal plant pest in these vineyards. There is considerable insect and mite damage to its foliage during late summer and autumn, but the stress this places on the weed is unknown. The most significant natural enemies of field bindweed are defoliating caterpillars, Bedellia somnulentella Zeller, Chaetocnema confinis Crotch, and spider mites. Non of the natural enemies present appeared to be suitable as biological control agents. However, some arthropods, such as Noctuelia floralis (Huebner), associated with field bindweed in Mediterranean Europe and Pakistan, could be useful in the California grape agroecosystem, once cleared for importation and release in North America. Others, unsuitable to release in California because of feeding on closely related native plants, may be of value in other parts of the world where no such conflicts of interest exist. It would be feasible to use biological control against field bindweed in California's coastal vineyards and, perhaps, also in orchards under present systems of cultivation. Its effectiveness could be enhanced by certain changes in growing practices, particularly the acceptance of some weed growth, and by changes in existing pest controls. Biological control of field bindweed should be considered in the development of pest management programs for such crops in California and wherever this plant is a serious pest.     

Comparative morphology and secretion chemistry of the scoli in caterpillars of<Emphasis Type="Italic"> Hyalophora cecropia</Emphasis>

The morphology of the variously coloured scoli (bristle-bearing structures on the integument, producing an exocrine secretion) on caterpillars of Hyalophora cecropia and the secondary chemistry of the discharged secretions have been investigated for the first time and compared. According to our scanning electron microscopic study, the red/orange, yellow and blue coloured groups of these glands differ morphologically. Gas chromatographic-mass spectrometric analyses showed that the patterns of secondary compounds in the respective glandular secretions are also different. Furthermore, the secretion of the penultimate larval instar is chemically distinct from that of the last instar, as are both secretions from the respective haemolymph. The results favour the idea that the differences in scoli colour, morphology and chemistry could affect various predator species differently.Electronic Supplementary Material  Supplementary material is available for this article if you access the article at . A link in the frame on the left on that page takes you directly to the supplementary material.     

Frequency of tail loss does not reflect innate predisposition in temperate New Zealand lizards

Caudal autotomy (tail shedding) is a defence mechanism against predation which is used by lizards when other tactics, such as crypsis and escape, prove ineffective. The speed at which autotomy occurs has important implications for survival, and the accuracy of tail loss is of consequence for an individual’s future fitness. Autotomy is shaped by both taxon-specific tail morphology as well as environmental factors such as predator history, and it can be difficult to distinguish between these processes. In this study, the frequency of tail-regeneration observed (field rate of autotomy), latency (speed of autotomy in the laboratory) and accuracy of tail loss were measured in six lizard species from two families (Scincidae and Diplodactylidae). The field rate and latency of autotomy was similar among all species except for the large nocturnal skink Oligosoma macgregori, which was less likely to autotomise. Latency and field rates of autotomy were not correlated, implying that the field rates of autotomy are related to predation attacks, social interactions, or some other environmental factor, rather than an innate disposition to autotomy. Further study, for example comparing populations with low and high predation pressure, will help to explain which of these factors are influencing autotomy rates.     

An estimated 400–800 million tons of prey are annually killed by the global spider community

Spiders have been suspected to be one of the most important groups of natural enemies of insects worldwide. To document the impact of the global spider community as insect predators, we present estimates of the biomass of annually killed insect prey. Our estimates assessed with two different methods suggest that the annual prey kill of the global spider community is in the range of 400–800 million metric tons (fresh weight), with insects and collembolans composing >90% of the captured prey. This equals approximately 1‰ of the global terrestrial net primary production. Spiders associated with forests and grasslands account for >95% of the annual prey kill of the global spider community, whereas spiders in other habitats are rather insignificant contributors over a full year. The spider communities associated with annual crops contribute less than 2% to the global annual prey kill. This, however, can be partly explained by the fact that annual crop fields are “disturbed habitats” with a low buildup of spider biomass and that agrobiont spiders often only kill prey over short time periods in a year. Our estimates are supported by the published results of exclusion experiments, showing that the number of herbivorous/detritivorous insects and collembolans increased significantly after spider removal from experimental plots. The presented estimates of the global annual prey kill and the relative contribution of spider predation in different biomes improve the general understanding of spider ecology and provide a first assessment of the global impact of this very important predator group.     

Survey of current crop management practices in a mixed-ricefield landscape,Mekong Delta,Vietnam — potential of habitat manipulation for improved control of citrus leafminer and citrus red mite

In the Mekong Delta, Vietnam, the citrus leafminer Phyllocnistis citrella (CLM) and the citrus red mite Panonychus citri are major pests in both sweet orange (Citrus sinensis) and Tieu mandarin (C. reticulata). Survey data indicate that these pest problems might be aggravated after farmers have completely destroyed the weed flora in their orchard. As citrus farmers only perceive the larger predators such as the weaver ant Oecophylla smaragdina and spiders, and have no idea about the existence of predatory mites or parasitoids, they do not know about potential positive attributes of weeds in pest management which sustain populations of natural enemies and their alternative food. IPM training programmes could use the weaver ant as an introduction to educating farmers about predatory mites and parasitoids, and should likewise emphasise the importance of beneficial asteraceous weeds such as Ageratum conyzoides. Non-crop trees such as Spondias dulcis, Mangifera indica, Eucalyptus tereticornis and Ceiba pentandra are commonly known to offer good refuge for the weaver ant. These trees should be further studied for their temporal contribution as food resource for other natural enemies of CLM and mites. Small adjustments of current weed management techniques are suggested to improve availability of pollen and nectar for beneficials at crucial moments in the cropping season, with due respect to implications at the landscape level.     

Safe caves and dangerous forests? Predation risk may contribute to salamander colonization of subterranean habitats

Recent studies suggest that many organisms actively colonize the subterranean environment to avoid climatic stress, exploit new ecological opportunities and reduce competition and predation. Terrestrial salamanders are known to colonize the more stable subterranean habitats mainly to escape external climatic extremes, while the role of predation avoidance remains untested. To better understand the importance of predation, we used clay models of the cave salamander Speleomantes strinatii to compare the predation occurring in woodland and subterranean habitats. Models were positioned in three forests and in three caves in NW Italy. One-hundred eighty-four models were retrieved from the field and 59 (32%) were attacked by predators. Models were attacked on their head more often than expected by chance and, therefore, were perceived by predators as real prey items. In the woodlands, clay models showed a four-time higher probability of being attacked in comparison to caves, suggesting a different level of potential predation risk in these surface habitats. These findings are one of the first experimental evidences that, in terrestrial ecosystems, predation avoidance may contribute to the salamander underground colonization process.