Variation in the effectiveness of biotic defence: the case of an opportunistic ant-plant protection mutualism

Benefits to plants in facultative ant protection mutualisms are highly variable. This allows examination of the sources of this variation and the mechanisms by which ants protect plants. We studied opportunistic interactions between ants and an extrafloral nectary-bearing vine, Dioscorea praehensilis, during 3 different years. Variation in plant protection among years was striking. Several factors affected the effectiveness of the biotic defence. Stems recently emerged from the underground tuber were self-supporting, contacting no other plants and encountering few foraging ants. Stems then became lianescent, and contact with supporting plants greatly increased ant recruitment. Both species and number of ant workers influenced the effect of ants on the major herbivore, the chrysomelid beetle Lilioceris latipennis. Protective actions included limitation of oviposition (reduction in the number of eggs laid on the plant) and predation, leading to increased larval mortality. The probability of successful predation was strongly dependent on larval size. If temporarily low ant-patrolling activity allows larvae to grow beyond a critical size, their mechanical (thick integument) or chemical (plant-derived compounds in a fecal shield) defences become more effective against ants. Secondary metabolites derived from the host plant thus appear to be important for the anti-predator mechanisms of this beetle, being necessary for its survival and reproduction on a host plant that actively recruits ants as a biotic defence against herbivores.     

Effect of forest stand type on host plant quality and direct and indirect effects on pine sawfly performance

1. Observed lower levels of herbivory in mixed compared with monoculture stands have been hypothesized to depend on top-down forces, through higher predation pressure by natural enemies or through bottom-up mechanisms through plant quality effects on herbivore performance.
2. In this study, we compared the performance measured as host plant induced mortality, cocoon weight, and predation mortality of the European pine sawfly Neodiprion sertifer (Geoffroy) (Hymenoptera, Diprionidae) in mixed and monoculture forest stands.
3. We did not observe a difference in host plant induced mortality, cocoon weight, or predation mortality between mixed and monoculture forest stands. We did find an effect of local conditions around each experimental tree on pine sawfly performance. For example, the nitrogen content of pine needles is negatively affected by the proportion of pine around the experimental tree, which in turn increases the survival of sawfly larvae.
4. The results suggest that local conditions around individual trees are more important for the performance of the European pine sawfly than stand type, i.e. mixed or monoculture plant stands.
5. We conclude that the ongoing trend for diversification within commercial forestry calls for more research where the effects of both bottom-up and top-down effects are studied at several spatial scales.

     

Pine sawfly defence and variation in host plant resin acids: a trade-off with growth

Abstract.

• 1 The defence capability of pine sawfly larvae reared on Scots pines with low or high concentrations of resin acids was determined in a field experiment, where larvae were exposed to predatory ants, and in a laboratory experiment in which the rate of defence droplet replenishment was measured.
• 2 Larvae on low resin-acid shoots disappeared faster than larvae on high resin-acid shoots when exposed to predatory ants.
• 3 Larvae fed high resin-acid needles produced 50% larger defence droplets than larvae fed low resin-acid needles.
• 4 In an additional experiment high predation pressure was simulated by repeatedly removing defence droplets. Larvae responded by feeding more on tissue rich in resin acids, but at the cost of a reduction in growth rate.
• 5 Based on these data and earlier findings that survival and development of sawfly larvae are negatively affected by high resin-acid concentrations, we conclude that pine sawflies face a dilemma of conflicting demands, i.e. although high needle resin-acid concentrations enhance defence capability, they also reduce growth and survival. Our data also suggest that it is not necessarily the ovipositing female that has to balance this trade-off: plasticity in larval feeding behaviour provides larvae with a means to at least partly solve the dilemma.

     

Does ant predation favour leaf beetle specialization on toxic host plants?

Generalist predators are frequently seen as evolutionary forces that narrow the host range in herbivorous insects. Predators may favour specialization of herbivores on host plants containing toxic chemicals (which can be used by herbivores for their own defence) if host plant‐derived defences provide better protection from enemies than do autogenously produced defences. We compared the effectiveness of these two defensive strategies in the larvae of six species of leaf beetle (Chrysomelidae) against wood ants (Formica rufa group) in field experiments. Ants were more strongly repelled by larvae with host plant‐derived, salicylaldehyde‐containing secretions than by larvae with various autogenous secretions, but collectively foraging ants ultimately overcame any type of chemical defence by social interactions, chemical signalling, and olfactory learning. As a result, ants killed all larvae of Chrysomela lapponica defended by salicylaldehyde‐containing secretions within 2 days of their introduction to willows within 15 m of ant nests. We conclude that in the field neither type of chemical defence provides complete protection against wood ants in the vicinity of their nests, and that evolutionary shifts from autogenous production of secretion to sequestration of plant allelochemicals in leaf beetles may be favoured mostly at low ant densities on the periphery of ant foraging areas.     

Preference and performance of the sawfly Diprion pini on host and non-host plants of the genus Pinus

The sawfly, Diprion pini L., is a pest of Pinus in Europe and is mainly found on P. sylvestris L. and P. nigra laricio Poiret. The relative importance of female oviposition capacity and behaviour, egg development, and larval survival on a new host plant was measured on 11 pine species. Five were natural host plants and six non-host plants, five of which are not indigenous to Europe. Oviposition choice tests showed that females discriminated between the pine species. Egg and larval development also differed between pine species. However, the female choice was not linked with hatching rate and larval development. Results of biological tests clearly indicated that there were different response patterns of D. pini life stages in relation to pine species, and these patterns were the same with insects of four different origins. We discuss the importance of each potential barrier to colonisation of a new host.     

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.     

Host plant derived feeding deterrence towards ants in the turnip sawfly Athalia rosae

Larvae of the sawfly Athalia rosae ruficornis Jakovlev (Hymenoptera: Tenthredinidae) feed on several glucosinolate-containing plants and have been shown to sequester the main glucosinolates of different hosts, namely sinalbin (p-hydroxybenzylglucosinolate) from Sinapis alba L., sinigrin (allylglucosinolate) from Brassica nigra (L.) Koch, and glucobarbarin ((S)-2-hydroxy-2-phenylethylglucosinolate) from Barbarea stricta Andrz. (Brassicaceae). These plant metabolites are stored in the haemolymph, which is readily released when larvae are attacked by predators. In a dual-choice bioassay the bio-activity of sawfly haemolymph collected from larvae reared on different host plants (S. alba, B. nigra, and B. stricta) was tested against the ant Myrmica rubra L. (Hymenoptera: Formicidae). The haemolymph had a stronger deterrence effect when the corresponding sawfly larvae were reared on S. alba than when reared on B. nigra and B. stricta. Haemolymph of caterpillars of Pieris rapae L. (Lepidoptera: Pieridae) that had fed on S. alba was not deterrent to the ants. No sinalbin could be detected in their haemolymph. The glucosinolates sinalbin and sinigrin, offered in a concentration comparable to that in the sawfly haemolymph, were deterrent to the ants, but not as strongly as the corresponding haemolymph samples. This suggests, that glucosinolates are not the only compounds involved in the chemical defence of A. rosae. However, the presence of sequestered glucosinolates is already a sufficient defence towards predators such as ants, and their effectiveness is modulated by the host plant chemistry.     

Cocoon predation on diprionid sawflies: the effect of forest fertility

Predation by small mammals is thought to be one of the main regulators of outbreaking sawfly species. It has been suggested that predation may be lower in poor and dryish forests, and this is the reason why outbreaks often begin from this type of environment. We studied experimentally how fertility of the forest site affects cocoon predation experienced by two sawfly species, the common pine sawfly Diprion pini (Linnaeus) and the European pine sawfly Neodiprion sertifer (Geoffroy). We applied a fertilization treatment to selected pine-dominated barren forest sites in Finland, and 2–4 years later monitored predation on the sawfly cocoons in fertilized and control areas. The results did not support the idea that forest fertility was related to cocoon predation. We also could not verify that small mammal abundance was related to fertility of the forest. The most obvious pattern we observed was that the two sawfly species differed dramatically in predation experienced. N. sertifer has its cocoon phase in mid-summer and experienced only moderate predation (37%) whereas D. pini, with its cocoon phase in autumn, suffered from very heavy predation (96%). Our observations suggest that if predation is important in controlling the population dynamics of the species, its impact depends more on the sawfly species and season than on the fertility of the forest site. Received: 1 March 1998 / Accepted: 25 May 1998     

Testing the enemies hypothesis in forest stands: the important role of tree species composition

Numerous studies conducted in agro-ecosystems support the enemies hypothesis, which states that predators and parasites are more efficient in controlling pest densities in polycultures than in monocultures. Few similar studies, however, have been conducted in forest ecosystems, and we do not yet have evidence as to whether the enemies hypothesis holds true in forests. In a 2-year study, we investigated whether the survival of autumnal moth (Epirrita autumnata) larvae and pupae differs between silver birch monocultures and two-species mixtures of birch with black alder, Norway spruce and Scots pine. We placed young larvae on birch saplings and monitored their survival until the end of the larval period, when we checked whether they had been parasitized. After the larvae had pupated, pupal survival was tested in a field trial. In 2002, the larvae disappeared earlier and their overall survival was lower in birch–pine mixtures than in other stand types. In 2003, survival probability was lowest in birch–pine stands only during the first week and there were no differences between stands in overall survival. Larval parasitism was not affected by tree species composition. Pupal weight and pupal survival were likewise not affected by stand type. Among the predators, wood ants were more abundant on birches growing in birch–pine mixtures than in other stand types probably because colonies of myrmecophilic aphids were common on pines. In contrast, spider numbers did not differ between stand types. Ant exclusion by means of a glue ring around the birch trunk increased larval survival, indicating that ants are important predators of the autumnal moth larvae; differences in larval survival between stands are probably due to differential ant predation. Our results provide only partial support for the enemies hypothesis, and suggest that it is both tree species composition and species diversity which affect herbivore survival and predation.     

Thorn‐dwelling ants provide antiherbivore defence for camelthorn trees,Vachellia erioloba,in Namibia

Ants are widely employed by plants as an antiherbivore defence. A single host plant can associate with multiple, symbiotic ant species, although usually only a single ant species at a time. Different plant‐ant species may vary in the degree to which they defend their host plant. In Kenya, ant–acacia interactions are well studied, but less is known about systems elsewhere in Africa. A southern African species, Vachellia erioloba, is occupied by thorn‐dwelling ants from three different genera. Unusually, multiple colonies of all these ants simultaneously and stably inhabit trees. We investigated if the ants on V. erioloba (i) deter insect herbivores; (ii) differ in their effectiveness depending on the identity of the herbivore; and (iii) protect the tree against an important herbivore, the larvae of the lepidopteran Gonometa postica. We show that experimental exclusion of ants leads to greater levels of herbivory on trees. The ants inhabiting V. erioloba are an effective deterrent against hemipteran and coleopteran, but not lepidopteran herbivores. Defensive services do not vary among ant species, but only Crematogaster ants exhibit aggression towards G. postica. This highlights the potential of the V. erioloba–ant mutualism for studying ant–plant interactions that involve multiple, simultaneously resident thorn‐dwelling ant species.     

Effects of habitat fragmentation on the three-way interaction among ants,aphids and larvae of the giant purple emperor, <Emphasis Type="Italic">Sasakia charonda</Emphasis> (Hewitson), a near-threatened butterfly

Survival rates of both early and middle instar larvae of the nymphalid butterfly, Sasakia charonda, were estimated to be lowest on test trees planted in a meadow (site A), intermediate in a small, narrow secondary deciduous broadleaf forest (small patch, site B) and highest in a large secondary deciduous broadleaf forest (large forest, site C). The larval mortality rates due to predation by tree-climbing predators from the ground (tree climbing predator) such as ants and the larvae of carabids were estimated to be greater at sites A and B than those at site C. The number of predatory ants climbing test trees was significantly greater at sites A and B than at site C, and the ants harvested honeydew from aphids living on tree leaves at those two sites. Aphid densities were significantly higher on trees at sites A and B than at site C, and aphid densities and numbers of predatory ants were significantly and positively correlated at sites A and B. In an experiment controlling aphid density per branch on test trees, the numbers of ants and the mortality rates of S. charonda larvae were greater on branches with high aphid densities than on those with low aphid densities at both sites A and B. These results suggest that the aphid density per host tree was higher in the meadow and the small patch than in the large forest; at both sites these higher aphid densities attracted higher numbers of predatory ants to test trees, and as a result, mortality rates of S. charonda larvae were increased.     

Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.     

Haemolymph Defense Capacity of the Neotropical sawfly <Emphasis Type="Italic">Aneugmenus merida</Emphasis> against Ant Predation

The defensive characteristics of the sawflies have received special attention due to the involvement of toxic compounds obtained from host plants. In this context, the haemolymph-based defense is one of the strategies known in sawflies to dissuade the attack of predators. Aneugmenus merida is a neotropical sawfly whose larvae are herbivorous on the toxic bracken fern Pteridium spp. The present study examines the defensive properties of the A. merida larval haemolymph and its possible link with the chemistry of its host plant. We report the behavior of the solitary hunter ant Odontomachus chelifer towards A. merida larvae under laboratory conditions. In addition, we studied the liquid intake behavior of the ants provided with solutions of crude haemolymph, bracken extracts, and its fractions. A. merida larvae showed a marked defensive capacity against the ants. The inhibition of the attack was observed during the stages of antennal contact and mandibular blow, suggesting that larval defensive capacity is due to factors present in the integument and haemolymph. Aqueous and methanolic fractions of haemolymph and bracken also deterred feeding. Although some common compounds were detected in the haemolymph and bracken fractions, they were in very small quantities, suggesting that they are not responsible for the bioactivity. Therefore, the hypothetical connection between the host plant chemistry and larval defensive capacity could not be evidenced. We suggest that the deterrent compounds present in the haemolymph and integument could be jointly acting in the sawfly’s defensive strategy.     

Impact of cocoon predation and parasitism on endemic populations of the common pine sawfly, Diprion pini (L.) (Hymenoptera, Diprionidae) in different forest types

1 Predation and parasitism on litter‐buried cocoons of the common pine sawfly Diprion pini (L.) were compared in different forest types with endemic sawfly populations by field exposure of laboratory‐reared cocoons during three consecutive years (1993–1995). 2 The impact of cocoon predation was dependent on season and forest type. The highest predation (up to 95%) was found during autumn in forest stands with a dense understory vegetation. 3 Cocoon parasitism varied between year, season and forest type. The highest parasitoid attack was observed in pure pine forests with more or less barren soils, but did not exceed 24% of exposed cocoons. 4 Cocoons were exposed in small patches. Predators tended to exploit all cocoons of a patch, whereas parasitoids only attacked a few cocoons of a patch. Predation was similar on cocoons placed in the litter and those buried more deeply in the soil, whereas parasitism of soil‐buried cocoons was rare. 5 These results indicate that predators can have a remarkable potential for limiting endemic sawfly densities, if habitat conditions in a forest maintain their population and support their foraging behaviour. A notable effect of parasitoids on sawfly cocoons deposited in the litter is obviously restricted to typical pure and barren pine forests, but may play there a similar role as predation.     

Does group feeding by toxic prey confer a defensive benefit? Aristolochic acid content,group size and survival of first‐instar pipevine swallowtail (Battus philenor L.) larvae

1. Aggregative feeding of larvae is widespread in the Lepidoptera, and many hypotheses have been proposed to explain the adaptive significance of this trait. Group feeding occurs disproportionately more in species with aposematic, chemically defended larvae compared with species with cryptic, non‐chemically defended larvae, consistent with the hypothesis that group feeding provides an enhanced aposematic signal to natural enemies. Most species characterised as having chemically defended larvae are cryptic during the first instar, when they are most highly aggregated and most vulnerable to predation. 2. The benefits of group feeding in terms of decreased predation were explored for first‐instar larvae of the pipevine swallowtail, Battus philenor, a species that sequesters aristolochic acids from its Aristolochia host plant and exhibits aposematism in later instars and as adults. We found that groups of larvae with experimentally enhanced aristolochic acid content had significantly lower survivorship due to predation both in the field and in laboratory experiments compared with groups of larvae without enhanced chemical defence. 3. A laboratory experiment found that aristolochic acid does not deter the generalist predator Hippodamia convergens. 4. No evidence was found that was consistent with the hypothesis that group feeding and increased sequestered chemical defence interact to decrease rates of larval mortality in non‐aposematic, first‐instar larvae. Future research on chemical defence, aposematism, and aggregative feeding should continue to appreciate that particular chemical defences and feeding behaviours are not universally effective against all natural enemies.     

Host specificity and host recognition in a chemically-defended herbivore, the tenthredinid sawfly Rhadinoceraea nodicornis

The sawfly Rhadinoceraea nodicornis Konow (Hymenoptera: Tenthredinidae) is a member of a closely related group of species, the tribe Phymatocerini, which feed on the Liliales and Ranunculales. It is known to sequester steroid alkaloids from its host plants, species in the genus Veratrum (Liliales: Melanthiaceae), and to use them as a defence against predators. There are known chemical relationships between the hosts of R. nodicornis and hosts of related sawfly species. We tested whether the R. nodicornis larvae would accept hosts of closely- and more distantly-related sawflies, but found that they accepted only plant species in the genus Veratrum. This specificity was apparently innate, as it was independent of early larval experience. A feeding bioassay showed that the steroid alkaloids from Veratrum nigrum were phagostimulatory for R. nodicornis larvae, suggesting that they may be involved in host recognition. We discuss the possibility that the evolution of recognition of specific compounds may represent the mechanism of host radiation within the Phymatocerini.     

Proximate effects of maternal oviposition preferences on defence efficacy and larval survival in a diet‐specialised tortoise beetle. Who knows best: mothers or their progeny?

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Trade‐offs in oviposition choice? Food‐dependent performance and defence against predators of a herbivorous sawfly

The sawfly Athalia rosae L. (Hymenoptera: Tenthredinidae) is a feeding specialist on plant species of the Brassicaceae, which are characterised by secondary metabolites, called glucosinolates. The larvae can take up the respective glucosinolates of their hosts and concentrate them in their haemolymph to protect themselves against predators. Oviposition preferences of naïve females were tested for three species, Sinapis alba L., Brassica nigra (L.) Koch, and Barbarea stricta Andrz., and were related to larval performance patterns. Larvae were reared on either one of these plants and it was investigated how host‐plant quality influences both the developmental times and growth of larvae (bottom‐up) and the defence efficiency against predators (top‐down). Innately, almost all adult females avoided B. stricta for oviposition and clearly preferred B. nigra over S. alba. On average, larvae developed best on B. nigra. Female larvae reached similar final body masses on all host‐plant species, but males reared on S. alba were slightly lighter. The developmental time of larvae reared on B. stricta was significantly longer than on the other two plants. However, larvae reared on B. stricta were best protected against the predatory wasp Polistes dominulus Christ (Hymenoptera: Vespidae). The wasps rejected these larvae most often, while they attacked larvae reared on S. alba most frequently. Thus, larvae feeding on B. stricta theoretically run a higher risk of predation due to a prolonged developmental time, but in practice they are better protected against predators. Overall, oviposition preferences of A. rosae seem to be more influenced by bottom‐up effects on larval performance than by top‐down effects.     

Contributions of female oviposition patterns and larval behavior to group defense in conifer sawflies (hymenoptera: diprionidae)

We studied the effects of adult oviposition and larval interactions on the defensive potential of gregarious behavior in conifer sawflies. Aggregation size and distribution initially reflected adult host plant selection and oviposition behavior. The contagious distribution of egg clusters resulted in part from the utilization of individual trees by multiple females, and of single host shoots by several females. Trees with the greates degree of prior defoliation received the most eggs, even though the potential for larval crowding made resource depletion possible. Foliar monoterpene and nitrogen contents explained only a small proportion of variability in female host utilization. Conifer needle architecture restricted the size of larval subgroups within aggregations, and limited the degree of defensive cohesiveness between subgroups. Subgroup turnover was frequent and independent of local food depletion. Risk of predation from wood ants varied with larval aggregation size and predator foraging level. When ant activity was high, large aggregations suffered greater numerical losses, but showed lower per capita predatory risk, than small groups. Results suggest that female oviposition patterns are influenced in part by the defensive benefits gained by offspring in large aggregations. Against ants, dilution effects and defensive synchrony due to gregariousness contribute to the overall antipredator strategy of sawfly larvae.     

Effects of neem oil on feeding behaviour and development of the pear sawfly, Caliroa cerasi

Neem oil deterred feeding by pear sawfly, Caliroa cerasi L., larvae (Hymenoptera: Tenthredinidae), both in choice and in no-choice cherry leaf disk bioassays. Deterrence was greater in the choice tests, with 50% inhibition occurring at 0.49% aqueous neem oil compared with 1.11% in the no-choice tests. Antifeedant activity towards pear sawfly larvae is slightly less than has been observed for Lepidoptera, but is higher than deterrence to other insects such as aphids. Topical application of neem oil to sawfly larvae resulted in reduced feeding, increased mortality, and a trend towards slower development. Most larval mortality after neem treatment resulted from incomplete subsequent moults. The potential utilization of neem insecticides for control of pear sawfly in tree fruit pest management is discussed.