Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology

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Caterpillars escape predation in habitat and thermal refuges

1. Climate and, therefore, abiotic conditions, are changing rapidly, and many ecological interactions depend on them. In this study, how abiotic conditions mediate a predator–prey interaction were examined. 2. Caterpillars of Platyprepia virginalis (Boisduval) (Arctiidae) were found previously to be more abundant in wet habitats and thick litter cover compared with drier habitats and little or no litter. We hypothesised that wet litter provided caterpillars with refuges from an important ant predator, Formica lasioides. It was further hypothesised that caterpillars would be able to move at lower temperatures than ants, thus providing them with a thermal refuge. 3. In the lab, caterpillars were more likely to escape ant predation and survive on wet litter and at lower temperatures. At all temperatures, ant recruitment was lower in wet litter than dry litter although ants were more active on litter than bare soil. Thus, wet litter may serve as a habitat refuge for caterpillars from ants. 4. Caterpillars were able to maintain activity at temperatures 8–14 °C lower than F. lasioides. Thus colder temperatures may serve as a thermal refuge for caterpillars from ants. 5. It was hypothesised that caterpillars can escape ant predation when precipitation causes wet litter and at temperatures that they experience commonly in the field. This mismatch between caterpillars and their predators in ability to tolerate wet litter and low temperatures may affect their field distribution and abundance. Expected future warmer and drier conditions may not provide these refuges.     

Reduced Aggressive Behavior: A Benefit of Silk-Spinning in the Parsnip Webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae)

The parsnip webworm, Depressaria pastinacella, spins a silken web within the umbels of its host plant, the wild parsnip Pastinaca sativa, and aggressively defends this web against conspecifics. We first established experimentally that the number of aggressive interactions between caterpillars with their webs removed was significantly higher than for webworms with intact webs. In order to determine whether web-spinning acts to divide food resources and reduce aggressive interactions, we measured relative weight gain and total silk production of parsnip webworms isolated from one another, grouped together with webbing undisturbed, and grouped together with webbing removed daily. Parsnip webworms isolated from one another and therefore unable to engage in aggressive interactions attained the highest pupal weights and spun the smallest amount of silk; caterpillars with webs removed daily and therefore with frequent aggressive interactions until territories were reestablished had the lowest pupal weights and spun the greatest quantity of silk. Our findings indicate that, for the parsnip webworm, constructing a silken web reduces aggressive encounters among conspecifics.     

Effect of temperature and leaf age on growth versus moulting time of a generalist caterpillar fed plantain (Plantago lanceolata)

Abstract.

• 1 The simultaneous effects of daytime temperature (20°C versus 30°C) and leaf age (new versus intermediate-aged) on a generalist insect herbivore were examined. Fourth-instar Spilosoma congrua caterpillars were tested on plantain (Plantago lanceolata), one of this lepidopteran species’host plants, for which the major defensive chemicals, iridoid glycosides (aucubin and catalpol), could be quantified.
• 2 Cool temperature depressed amount of food eaten, amount of frass, and consumption and growth rates, and increased the proportion of time spent in the non-feeding period (from head-capsule slippage to ecdysis).
• 3 Average iridoid glycoside concentration was 2.8% dry weight (d.w.) in new leaves and 1.6% d.w. in intermediate-aged leaves. When fed new leaves, the caterpillars had a higher efficiency of conversion of ingested food to biomass and a higher growth rate than those fed intermediate-aged leaves. Furthermore, the proportion of time spent in the non-feeding period was prolonged by a diet of intermediate-aged leaves.
• 4 A second experiment showed that the percentage dry weight of aucubin, catalpol and total iridoid glycosides increased over 24 h in incubated, excised leaves, which meant that the caterpillars in the first experiment experienced somewhat higher iridoid glycoside concentrations than the levels in fresh leaves.
• 5 Overall, these results indicate that this generalist should prefer new plantain leaves over older leaves even though new leaves contain higher concentrations of iridoid glycosides.

     

The influence of diet on growth and secretion behaviour of myrmecophilous Polyommatus icarus caterpillars (Lepidoptera: Lycaenidae)

Abstract.

• 1 Caterpillars of the facultatively myrmecophilous butterfly Polyommatus icarus were reared on inflorescences, or foliage, of four natural hostplant species and on an artificial diet to study dietary effects on larval growth and secretory capacity.
• 2 Caterpillars achieved highest weights and relative growth rates when fed flowers of Medicago sativa, Lotus corniculatus or Melilotus officinalis. Larvae reared on Coroniüa varia (flowers and leaves), foliage of M.sativa and on the artificial diet pupated at lower weights and achieved lower growth rates.
• 3 In standardized experiments with the ant species Lasius flavus, secretion rates from the dorsal nectar organ (DNO) were 2 times higher among flower-fed caterpillars than among foliage-fed siblings or caterpillars on the artificial diet. Larvae reared on C.varia flowers were superior to all other food treatments with respect to secretion rates.
• 4 High water content of larval diet, as in flowers, appears to be important for lycaenid caterpillars to achieve high secretion rates, whereas the correlation between myrmecophily and nutrient availability, as evidenced by growth rates, was less pronounced.
• 5 Using experimental data on larval growth and secretion rates, the lifetime volume of secretions from the DNO is estimated to range from 2 to 5 μl in most food treatments. Only on C.varia flowers (5.5–8.7 μl) and on M.sativa leaves (0.9–1.1 μl) did the caterpillars deviate in their absolute investment in myrmecophily.
• 6 The estimated lifetime investment accounted for 1.6–5.5% of prepupal fresh weight in all food treatments except on C.varia flowers (7.8–12.3%).

     

Invasive plant population and herbivore identity affect latex induction

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Behaviour of specialist and generalist caterpillars on plantain (Plantago lanceolata)

Abstract.

• 1 Foraging patterns of specialist (Junonia coenia Hubner: Nymphalidae) and generalist (Spilosoma congrua Wlk.: Arctiidae) caterpillars on five genotypes of plantain (Plantago lanceolata L.: Plantaginaceae) were examined in an experimental garden.
• 2 Movement by the specialists reflected declining availability of new leaves. When direct sunlight was available, these caterpillars were usually exposed to it.
• 3 Although the generalists also preferred new leaves, they spent less than 50% of their time on the plantain and changed location more frequently than the specialists. They often hid at the base of plants or under leaves.
• 4 Plant genotype influenced the apparency of the specialists and damage by the herbivores.

     

The osmaterial glands of the swallowtail butterfly Eurytides marcellus as a defence against natural enemies

ABSTRACT.

• 1 Natural enemies account for almost all mortality of zebra swallowtail caterpillars (Eurytides marcellus [Cramer]) feeding on pawpaw (Asimina spp.) in Florida.
• 2 The osmaterial glands of the third instar caterpillars reduce predation rates in the spring, but not later in the season.
• 3 The seasonal decline in effectiveness of osmateria in deterring natural enemies probably stems from a reduction in the importance of the predators that are repelled by osmateria.

     

Leaf shelter-building caterpillars harness forces generated by axial retraction of stretched and wetted silk

Leaf shelter-building caterpillars generate most of the force required to pull leaf surfaces together by stretching silk strands while spinning. Axially retractive forces produced by columns of stretched strands enabled caterpillars in our study to generate forces as great as 0.3 Newtons (i.e., a 30-g force). We found that caterpillar silk also contracts instantly when wetted, producing an additional, though smaller, axially retractive force. Contraction ratios (final length/ original length) of the wetted silk of 19 species ranged from 0.21 to 0.93 and were smallest among species that use their silk to make leaf shelters. Our study, the first to identify the specific sources of the energy harnessed by caterpillars to tie, roll, or fold leaves, indicates that silk properties and caterpillar behavior have coevolved to facilitate the leaf shelter-building process.     

The effect of sunlight on leaf litter quality reduces growth of the shredder Klapopteryx kuscheli

• 1 The direct effect of sunlight on the conditioning, breakdown and incorporation of leaf litter in stream food webs has not yet been considered. The aim here was to evaluate the effects of light intensity on the colonization of leaf litter by microorganisms and its resulting quality as food for the stonefly shredder Klapopteryx kuscheli.
• 2 Leaf litter was conditioned for 2 months in an open reach of a second‐order stream in litter bags either exposed to or shaded from direct sunlight. Subsequently, we performed laboratory experiments to test larval consumption, growth, growth efficiency and feeding preference fed on both leaf litter treatments.
• 3 Leaf litter in the unshaded treatment had three times more chlorophyll‐a (Chl‐a) than that in the shaded treatment, 50% lower fungal biomass and similar bacterial abundance. Although larvae did not prefer either food and fed at the same rate on both leaf litter treatments, they grew twice as fast on the shade‐conditioned leaves and attained a two‐fold higher growth efficiency.
• 4 Sunlight can have significant effects on detritus‐based food webs. Riparian modification induced by human activities in forested catchments increases the potential for sunlight to influence detritus dynamics.

     

Performance as a fish predator of largemouth bass [<Emphasis Type="Italic">Micropterus salmoides</Emphasis> (Lacepède)] invading Japanese freshwaters: a review

This review focuses on how predator performance of the invasive largemouth bass [Micropterus salmoides (Lacepède)] has been, or will be, formed in Japanese freshwaters. Predation impacts of largemouth bass on fish communities appear pervasive in both Japanese as well as North American freshwaters. Factors affecting performance as a piscivorous predator are (1) light intensity and water clarity, (2) oxygen depletion, (3) prey size and gape size, (4) behavioral refuge of prey, (5) weed beds as refuge for prey fish, (6) interaction with bluegill. Size and behavioral refuges requirements are so rigorous that they may have evolved only in some North American prey fish species like bluegill; therefore, most Japanese native fish species are unlikely to be equipped with such refuges. However, refuge habitats like aquatic weed beds could develop in Japanese freshwaters, allowing prey fish species to survive under predation pressure. The density, architecture, and species composition of aquatic plants may affect their suitability as refuges. Studies in Japanese waters have suggested that the presence of rich aquatic vegetation or invasive bluegill in bass-introduced waters have suppressed the predation impact of largemouth bass on fish communities. In addition to these environmental factors, original genotypic and phenotypic traits of the introduced largemouth bass, and hybridization between different lineages of largemouth bass or with Florida bass [Micropterus floridanus (Lesueur)] may be involved in further adaptation of invasive largemouth bass to Japanese freshwaters.     

Responses of leaf C:N:P stoichiometry to water supply in the desert shrub Zygophyllum xanthoxylum

• Based on the elemental composition of major biochemical molecules associated with different biological functions, the ‘growth rate hypothesis’ proposed that organisms with a higher growth rate would be coupled to lower C:N, especially lower C:P and N:P ratios. However, the applicability of the growth rate hypothesis for plants is unclear, especially for shrubs growing under different water supply.
• We performed an experiment with eight soil moisture levels (soil water content: 4%, 6%, 8%, 13%, 18%, 23%, 26% and 28%) to evaluate the effects of water availability on leaf C:N:P stoichiometry in the shrub Zygophyllum xanthoxylum.
• We found that leaves grew slowly and favored accumulation of P over C and N under both high and low water supply. Thus, leaf C:P and N:P ratios were unimodally related to soil water content, in parallel with individual leaf area and mass. As a result, there were significant positive correlations between leaf C:P and N:P with leaf growth (u).
• Our result that slower‐growing leaves had lower C:P and N:P ratios does not support the growth rate hypothesis, which predicted a negative association of N:P ratio with growth rate, but it is consistent with recent theoretical derivations of growth–stoichiometry relations in plants, where N:P ratio is predicted to increase with increasing growth for very low growth rates, suggesting leaf growth limitation by C and N rather than P for drought and water saturation.

     

Interactions between Chromolaena odorata (Asteraceae) and Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae)

Feeding of Pareuchaetes pseudoinsulata caterpillars caused the leaves of Chromolaena odorata to turn yellow. Leaf yellowing could not be induced either by artificial removal of leaves or by drenching the plant with a solution of excreta from P. pseudoinsulata caterpillars. Yellow leaves appeared tougher but had the same energy level as that of green leaves. The amount of nitrate-nitrogen was significantly higher in yellow leaves than green leaves. P. pseudoinsulata caterpillars prefer to feed on green leaves. When forced to feed on yellow leaves, they exhibit slow growth and high mortality. Defensive factors in plants attacked by insects seemed to prevent further infestation of plants. In the field, caterpillars on the yellow plants were found during both day and night whereas on green plants they appeared to feed at night and hide in the ground at daytime.     

Can protective attributes of artificial refuges offset predation risk in lizards?

Artificial refuges are often used to supplement habitat in areas where natural shelters have been degraded or removed. Although artificial refuges are intended to support particular species, they may be equally attractive and accessible to others, including predators. We explored the influence of snake predation risk and shelter attributes on the overnight use of different artificial refuges (timber, tiles, and iron) using the predator‐prey relationship between Boulenger's skink, Morethia boulengeri and the curl snake, Suta suta. We collected adult M. boulengeri from two bioregions in south‐eastern Australia: the Riverina, where the two species co‐occur, and the South Western Slopes, where S. suta does not occur. Two adult S. suta were collected for use as chemical donors. We conducted four experiments on overnight refuge choice to determine: (i) predator‐scent avoidance, (ii) artificial refuge preferences, (iii) a trade‐off between a preferred refuge and predator‐avoidance, and (iv) the effect of gap height on refuge preference. We found that skinks avoided predator‐scented refuges in favour of identical, but unscented refuges. Skinks preferred timber refuges, and most skinks maintained this preference when predator‐scent was added. However, when gap height was manipulated, skinks shifted to the refuge with the smallest gap. Skinks displayed complex regional variation in behaviour; skinks from both bioregions avoided predator‐scent, but in the trade‐off experiment, skinks from the South Western Slopes were less likely to avoid predator‐scented timber refuges than those from the Riverina. Our findings suggest that protective refuge attributes, such as small gap height, can offset the risk implied by predator‐scent within a refuge. This study highlights the need to consider predator‐prey interactions when designing and using artificial refuges for habitat restoration or biological monitoring.     

Effects of herbivory and genotype on growth and survivorship of sand-dune willow (Salix cordata)

Abstract.

• 1 The response of different clones of sand-dune willow, Salix cordata, to herbivory by a specialist herbivore, Altica subplicata, was studied in three glasshouse experiments. Plants were caged and exposed to three herbivory treatments: no beetles, low number of beetles, and high number of beetles.
• 2 Plants consistently had significantly higher growth rates in the absence of herbivory than under conditions of low or high herbivory (1.5–6 times higher).
• 3 Herbivore treatment influenced mortality from drought stress; more plants from the low and high herbivory treatments (40% and 80%) died from drought stress than did control plants (0%).
• 4 Clone genotype significantly influenced growth rates and the susceptibility of plants to drought stress. However, clones showed similar growth responses to herbivory, suggesting a lack of genetic variation in tolerance or resistance to herbivory.

     

Predation and avoidance of tough leaves by aquatic larvae of the moth Parapoynx rugosalis (Lepidoptera: Pyralidae)

Abstract.

• 1 Aquatic larvae of the pyralid moth Parapoynx rugosalis Möschler repeatedly construct protective cases by cutting portions (discs) from leaves of the waterlily Nymphaea ampla and sandwich themselves between the disc and the underside of the host leaf. Construction of a new case requires leaving the old case, thus increasing exposure to predators and parasites.
• 2 In an experiment, larvae with protective cases experienced no mortality due to predation by fish, whereas larvae without cases experienced substantial predation.
• 3 In a series of choice tests, larvae preferentially selected young, tender leaves over old, tough leaves for construction of cases, and larvae spent significantly less time completing their shelters when cutting discs from young, tender leaves.
• 4 A partial explanation of why larvae select young, tender leaves for construction of their protective shelters may be that exposure time to predators during construction is minimized.
• 5 The same mechanism linking preferences for tender leaves to reduced exposure to predators during construction may also apply to other insect herbivores exhibiting leaf-rolling or case-building behaviour.

     

Presence of predatory wasps and stinkbugs alters foraging behavior of cryptic and non-cryptic caterpillars on plantain (Plantago lanceolata)

We examined the foraging patterns of two species of caterpillar (Junonia coenia: Nymphalidae and Spilosoma congrua: Arctiidae) that contrast in feeding specialization and crypticity on plantain (Plantago lanceolata) in the absence and presence of two different insect predators [stinkbugs, Podisus maculiventris (Pentatomidae) and wasps, Polistes fuscatus (Vespidae)]. Junonia larvae were quite apparent to human observers, feeding on upper leaf surfaces during daylight, whereas Spilosoma larvae were relatively cryptic, often hiding under leaves and in soil crevices during daylight. In the presence of either predator species, the non-cryptic Junonia caterpillars more quickly left the plant on which they were initially placed and were less apparent than Junonia larvae not exposed to predators. The presence of predators had no detectable influence on where the caterpillars occurred on the plants (new, intermediate-aged or mature leaves, or reproductive stalks). Surprisingly, the predators influenced the behavior of the inherently cryptic Spilosoma: the apparency of these larvae at night increased when wasps had access to the plots during the day. Survivorship of the non-cryptic Junonia was less than 12% when stinkbugs were present compared to 60% in their absence. Although the presence of wasps resulted in a lower relative growth rate for the non-cryptic Junonia larvae, the indirect effect of predators on reduction in survivorship due to alterations in prey growth rate through behavioral changes was less than 3%. After taking into account the decline in caterpillars per plot through predation, we found that both the amount of leaves eaten and the proportion of plants eaten were altered on plots with predators present, which suggests that the caterpillars' increased consumption countered increased maintenance costs due to the presence of predators. Overall, our results indicate that hostplant size, level of predation and type of predator can influence the degree to which these caterpillars react to the presence of insect predators. In contrast, degree of inherent feeding specialization and cryptic behavior seemed to have little effect on the expression of reactive behaviors of these caterpillars to predators.     

Silk drives aggregation and following in the neotropical caterpillar Mechanitis menapis (Nymphalidae: Ithomiini)

Gregarious larvae that use chemical communication to feed and move together are widespread among folivorous insects, although social behaviour has been studied almost exclusively in a few temperate zone genera. The Menapis (or variable) tigerwing butterfly Mechanitis menapis mantineus Hewitson (Lepidoptera, Nymphalidae, Danainae, Ithomiini) is a neotropical species whose larvae feed gregariously on Solanaceae host plants. In laboratory experiments conducted in the Ecuador cloud forest, M. menapis caterpillars are attracted to silk produced by conspecifics and show no evidence of pheromone production. Indeed, caterpillars consistently choose arenas with silk over bare arenas but do not show a preference for arenas marked with abdominal cuticular surface residues. Mechanitis menapis caterpillars on silk‐coated plants are both more mobile and more cohesive than those on control plants. Nonetheless, caterpillars move independently over unmarked surfaces and groups do not make rapid collective choices between two food sources. Collective behaviour in M. menapis thus appears to be based on aggregation on collectively produced silk to facilitate feeding, as well as using this silk to maintain cohesion. Silk production is common in caterpillars, although M. menapis appears to be unique among species studied so far in using silk to maintain group cohesion.     

Foliar damage, parasitoids and indirect competition: a test using herbivores of birch

ABSTRACT.

• 1 The hypothesis that leaf-chewing caterpillars and leaf miners indirectly compete via the influence of foliar damage on parasitoids was experimentally tested using the leaf miner Coleophora serratella (L.) and a complex of folivorous caterpillars on birch.
• 2 Separate experiments tested the effects of manipulating artificial or caterpillar-induced leaf damage on parasitism of leaf miners at several spatial scales.
• 3 Parasitism of C. serratella by specialist and generalist parasitoids was independent of the extent of either collateral or leaf-miner damage, whether experimentally or naturally induced.
• 4 Support in the literature for the hypothesis is restricted to a single case, and only on a limited spatial scale; thus, the idea that collateral damage directs parasitoid-mediated competition among herbivores remains highly speculative.

     

Developmental changes in barrier web structure under different levels of predation risk inNephila clavipes (Araneae: Tetragnathidae)

Individuals of the orb-weaving spider Nephila clavipesbuild complex webs with a region used for prey capture, the orb, and tangle webs opposite either face, the barrier webs. Barrier webs have been hypothesized to serve a variety of functions, including predator defense, and the primary function of the barrier web should be reflected in the relative size of the barrier to the orb under varying conditions of foraging success and predation risk. To investigate the effects of predation pressure and foraging success on barrier web structure, I conducted a comparative study in three disjunct populations that differed in predation risk and foraging success. Although both the orb web and the barrier webs are silk, there was no indication of a foraging-defense trade-off. Barrier web structure did not change during seasonal shifts in orb web size related to changes in preycapture rate, and barrier web silk density and orb radius were positively correlated. The hypothesis that the construction of barrier webs is in part a response to predation pressure was supported. Barrier webs do deflect attacks by some predators, and barrier webs built by small spiders, suffering frequent predation attempts, had a higher silk density than barrier webs built by larger individuals. Additionally, barrier web complexity decreased at a later age in areas with higher predation risk.