Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus

Abstract.

• 1 The ability to use flexible decision rules can be an advantage to parasitoid females searching for patchily-distributed hosts. In a series of laboratory experiments the hypothesis that Opius dimidiatus, a solitary parasitoid of the chrysanthemum leafminer (Liriomyza trifolii), adjusts the time she allocates to searching for her larval hosts in response to both patch qualities and experiences with hosts was tested by varying such patch parameters as area, presence of host mines and density of host mines, and by allowing ovipositions and encounters with parasitized hosts.
• 2 Though leaf area was not a factor, the presence of host mines in a leaf did increase the time a female O.dimidiatus spent searching, over time spent on unmined leaves.
• 3 When host mine density was increased, females responded by increasing their search period in a density-dependent manner, suggesting a perception of patch quality.
• 4 Ovipositions in hosts caused females to reset their‘giving-up time’(GUT), or increase search intensity, by adding an amount of search time that increased with each successive oviposition. Conversely, encounters with parasitized (unsuitable) hosts incremented the GUT, but by an amount that decreased with each successive encounter.

     

Parasitoids use herbivore-induced information to adapt patch exploitation behaviour

Abstract.  1. Optimal foraging models ultimately predict that female parasitoids should exploit rich host patches for longer than poorer ones. At the proximate level, mechanistic models and experimental studies show that parasitoids use both chemicals produced by their hosts and direct encounters with their hosts to estimate patch quality. Although it has been extensively studied in the context of host location, the use of herbivore-induced plant response by insect parasitoids has never been considered in the context of patch time allocation.
2. In this study, the respective roles of herbivore-induced plant response and direct contact with hosts on the foraging behaviour of Lysiphlebus testaceipes females on an aphid patch were quantified. For this, the level of herbivore-induced plant response and the number of aphids on the leaf bearing the patch were manipulated independently. Different levels of plant response were obtained by varying the duration of infestation on another leaf.
3. Parasitoid residence time and number of attacks increased with both the level of plant response and the number of aphids.
4. These results suggest that L. testaceipes females use the combination of herbivore-induced response of plants and direct encounters with hosts to assess patch quality and adjust their patch use behaviour.     

Patterns of parasitism by insect parasitoids in patchy environments

Abstract. 1. This paper shows how the different spatial patterns of per cent parasitism in patches of different host density can be explained within a single model framework that takes into account the parasitoid's aggregative response, and the factors limiting the degree of host exploitation within patches.
2. Two contrasting laboratory examples are presented in which the distribution of searching parasitoids and the resulting levels of parasitism in different patches are both known for a range of parasitoid densities.
3. A model is described predicting the number of hosts parasitized per patch, in which the number of parasitoids searching is determined from a simple expression allowing different degrees of aggregation.
4. The model generates patterns of parasitism encompassing the two laboratory examples and a wide range of examples from the field.
5. The importance of density dependent spatial distributions of parasitism to population stability is briefly discussed.     

The ecological significance of differences in host detection behaviour in coexisting parasitoid species

1. Six species of drosophilid parasitoids of the genus Leptopilina (Hymenoptera: Eucoilidae) exist in Europe. Laboratory experiments reveal that the fundamental niches for most of these species overlap. Field collections indicate that overlap in their realised niches is much smaller.
2. Here data are presented for the little known species Leptopilina longipes. Field and laboratory observations indicate that its niche overlaps with both that of L. clavipes and L. heterotoma .
3. The host detection behaviour of L. longipes is examined and it is shown that L. longipes uses vibrotaxis to detect its hosts. This behaviour of L. longipes is compared with that of L. heterotoma and L. clavipes , which both use the ovipositor in host detection.
4. The ways in which differences in host searching behaviour can contribute to niche segregation and coexistence of these species are discussed.     

The Pieris napi /bryoniae hybrid zone at Pont de Nant, Switzerland: broad overlap in the range of suitable host plants

1. The butterflies Pieris napi and Pieris bryoniae hybridize in a narrow zone at ≈ 1200 m in the Alps and Carpathians of Europe. They feed as larvae on a variety of hosts in the Brassicaceae, and few host species occur on both sides of the hybrid zone.
2. Females were captured on either side of the hybrid zone at Pont de Nant, Switzerland, eggs obtained, and larvae were offered plants from nineteen species of Brassicaceae and Reseda lutea (Resedaceae).
3. Nine of the hosts were found to have eggs or larvae already on them. Only Capsella bursa-pastoris and R. lutea were unsuitable.
4. Significant survivorship differences among suitable hosts were found. There was no interaction between butterfly species and host plant, which would indicate adaptation by these taxa to their respective suites of hosts.
5. Among suitable hosts, larvae of both taxa had higher mortality on plants with hairy leaves and on older plants beginning to senesce.
6. Differential selection on host use, if it occurs at all, is likely to be a very minor factor in the dynamics of the Pieris napi / bryoniae hybrid zone.     

Patch departure mechanisms and optimal host exploitation in an insect parasitoid

1. Patch-leaving decisions are of utmost importance in determining parasitoid foraging success. Parasitoids are known to use both marks left by hosts (chemical or otherwise) and ovipositions to assess host availability and to decide when to leave a host patch.
2. Previous studies have shown that, depending on the species, ovipositions either increase (an incremental mechanism) or decrease (a decremental mechanism) the patch residence times of parasitoids. Reports in the literature conflict on which mechanism is used by Venturia canescens , a parasitoid of pyralid moth larvae.
3. We hypothesize that, as a consequence of saturation in the capacity of the parasitoid to discriminate between host densities at high host numbers, V. canescens uses a decremental mechanism at low host numbers and an incremental one at high host numbers. We call this a 'switching mechanism'.
4. Our experiments show that even if discrimination capacity saturates, V. canescens uses a decremental mechanism over a wide range of host densities.
5. The distribution of hosts in different fruits species under field conditions suggests a switching mechanism would not evolve in natural situations.
6. A model of patch departure in V. canescens is constructed and tested using an independent set of experiments. The model suggests that the patch leaving mechanism in V. canescens is a stochastic decremental one. As might be expected from Weber's Law, the initial leaving tendency is a convex decreasing function of kairomone concentration. The leaving tendency increases exponentially with the time spent in the patch without ovipositing. Ovipositions cause a sudden increase in leaving tendency.
7. Simulations suggest that a decremental mechanism would be out-competed by either one indifferent to ovipositions or an incremental one, only when travel times are much larger than those that are likely to occur in the field.     

Learning pays off: influence of experience on host finding and parasitism in Lariophagus distinguendus

Abstract. 1. The influence of experience on egg maturation, parasitism rate, and behaviour during host searching was investigated for Lariophagus distinguendus (Först.) (Hymenoptera: Pteromalidae) parasitizing larvae of the granary weevil Sitophilus granarius (L.) in grains of wheat Triticum aestivum L.
2. Dissection of female parasitoids and parasitism bioassays at high host density revealed that experience with hosts (e.g. by oviposition or by host feeding) is not required either for triggering oogenesis or for oviposition.
3. In parasitism experiments at low host density, when single host-infested grains were offered within a bulk of healthy grains, host finding and parasitism rate were increased by experience.
4. Behavioural observations revealed that searching time required for finding an infested grain was shorter for experienced parasitoids than for naive parasitoids, because travel time from grain to grain is shorter for experienced parasitoids, and because experienced parasitoids spend less time than naive parasitoids on non-infested grains.
5. In conclusion, experience due to host exposure increases parasitism and thereby the fitness of the parasitoids. It is discussed that this increase is more likely due to learning than to different egg load dynamics of experienced parasitoids.     

Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles

Abstract 1 When searching for suitable hosts in flight, especially in mixed forests, conifer‐inhabiting bark beetles will encounter not only suitable host trees and their odours, but also unsuitable hosts and nonhost trees. Rejection of these trees could be based on an imbalance of certain host characteristics and/or a negative response to some nonhost stimuli, such as nonhost volatiles (NHV). 2 Recent electrophysiological and behavioural studies clearly indicate that conifer‐inhabiting bark beetles are not only able to recognize, but also to avoid, nonhost habitats or trees by olfactory means. Green leaf volatiles (GLV), especially C₆‐alcohols, from the leaves (and partly from bark) of nonhost angiosperm trees, may represent nonhost odour signals at the habitat level. Specific bark volatiles such as trans‐conophthorin, C₈‐alcohols, and some aromatic compounds, may indicate nonhosts at the tree species level. Flying bark beetles are also capable of determining whether a possible host is unsuitable by reacting to signals from conspecifics or sympatric heterospecifics that indicate old or colonized host tree individuals. 3 Combined NHV signals in blends showed both redundancy and synergism in their inhibitory effects. The coexistence of redundancy and synergism in negative NHV signals may indicate different functional levels (nonhost habitats, species, and unsuitable hosts) in the host selection process. Combinations of NHV and verbenone significantly reduced the number of mass attacked host trees or logs on several economically important species (e.g. Dendroctonus ponderosae, Ips typographus, and I. sexdentatus). 4 We suggest a semiochemical‐diversity hypothesis, based on the inhibition by NHV of bark beetle host‐location, which might partly explain the lower outbreak rates of forest insects in mixed forests. This ‘semiochemical‐diversity hypothesis’ would provide new support to the general ‘stability‐diversity hypothesis’. 5 Natural selection appears to have caused conifer‐inhabiting bark beetles to evolve several olfactory mechanisms for finding their hosts and avoiding unsuitable hosts and nonhost species. NHV and unsuitable host signals have potential for use in protecting trees from attack. The use of these signals may be facilitated by the fact that their combination has an active inhibition radius of several metres in trap test, and by the observation of area effects for several trees near inhibitor soruces in tree protection experiments. Furthermore, incorporation of negative signals (such as NHV and verbenone) and pheromone‐based mass‐trapping in a ‘push–pull’ fashion may significantly increase the options for control against outbreaks of conifer‐inhabiting bark beetles, especially in high risk areas.     

Analysis of Foraging Behaviour of the Whitefly Parasitoid Encarsia formosa on a plant: A Simulation Study

The foraging behaviour of Encarsia formosa was analyzed using a stochastic simulation model of the parasitoid's behaviour. Parasitoids were allowed to search during a day on a tomato plant infested with immatures of the greenhouse whitefly, Trialeurodes vaporariorum. The model simulates searching, host selection, host handling and patch leaving behaviour, and the physiological state of the parasitoid. The outputs of the model are the number of visited leaflets and the number of hosts encountered, parasitized or killed by host feeding. The simulation results agreed well with observations of parasitoids foraging on tomato plants. The number of encounters and ovipositions on the plant increased with host density according to a type II functional response. At a clustered host distribution over leaflets and low host densities, the most important parameters affecting the number of ovipositions were the leaf area, the parasitoid's walking speed and walking activity, the probability of oviposition after encountering a host, the initial egg load and the ratio of search times on both leaf sides. At high densities, the maximum egg load and the giving-up time on a leaflet since latest host encounter were the most essential parameters.     

The Quest for a Suitable Host: Size Distributions of Host Trees and Secondary Hemiepiphytes Search Strategy

As climbing plants lack the capacity to hold themselves upright, they need to encounter a suitable host. Vines, lianas, and secondary hemiepiphytes need, therefore, an effective searching strategy. Various hypotheses have been put forward on searching strategies, including ‘skototropism’—growth toward darkness—and random searching. We studied host searching strategies of three secondary hemiepiphyte species belonging to the genus Heteropsis. We recorded information on the diameter distribution of host and evaluated whether these hosts were ‘suitable’, i.e., sufficiently tall for Heteropsis individuals to reach reproductive size. The diameter distribution of host trees bearing Heteropsis seedlings was similar to that of the trees in our study plots. Also, we found that 72–81 percent of the Heteropsis seedlings were present on unsuitable hosts (seedlings, saplings, herbs). These results suggest that Heteropsis seedlings search hosts in a random manner and not by skototropism. We found quite a distinct pattern for adult Heteropsis individuals, which predominantly occur on host trees bigger than 10 cm dbh. Host diameter distribution for Heteropsis adults differed significantly from that of the entire tree community. This difference suggests that Heteropsis individuals may change hosts if they are initially present on nonsuitable hosts. We observed that Heteropsis seedlings and juveniles on unsuitable hosts often produced vegetative shoots that searched for another host. In many cases, such shoots did not find a suitable host. For Heteropsis, our results suggest that host tree searching is a long‐term trial and error process that is governed by a random searching strategy. Abstract in Spanish is available in the online version of this article.     

Potential novel hosts for the lily leaf beetle Lilioceris lilii Scopoli (Coleoptera: Chrysomelidae) in eastern North America

Abstract.  1. Introduced insects often incorporate native plants into their diets and might be expected to show a predilection for novel hosts that are phylogenetically related to their normal hosts. The lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae), is an introduced pest of cultivated lilies. Oviposition behaviour, larval behaviour, and development of L. lilii was examined on a range of potential host plants, as well as on the normal host, Asiatic hybrid lilies Lilium sp.
2. Neonate larval feeding behaviour was quantified on 15 food plant species: 10 from the Liliales, three from the Asparagales and two eudicots. Larvae fed plants closely related to the genus Lilium were more likely to initiate feeding, less likely to abandon their food leaf, and consumed more leaf area.
3. In no-choice tests, females oviposited on the novel hosts Lilium philadelphicum , Medeola virginiana , Clintonia borealis , Streptopus amplexifolius , and Polygonatum biflorum ; however, all but L. philadelphicum received very few eggs. Non- Lilium novel hosts were not used for oviposition when presented along with Asiatic lilies in choice tests.
4. A single individual was reared to the adult stage on the novel host S. amplexifolius . Several larvae survived to the pupal stage on M. virginiana , although no adults emerged from those pupae. Larvae reared on the native wood lily L. philadelphicum performed equally well or better than on the Asiatic cultivar.
5. Our results indicate that the lily leaf beetle poses a threat to native Liliaceae. Several native Lilium species, including L. philadelphicum , are threatened or endangered in certain jurisdictions throughout their range; these species should be monitored closely for colonisation by the beetle.     

Active defence of herbivorous hosts against parasitism: Adult parasitoid mortality risk involved in attacking a concealed stemboring host

Phytophagous insects have several defence strategies to defend themselves against attack by parasitic wasps. Larval lepidopteran hosts can defend themselves actively to prevent oviposition by the parasitoid. Among the aggressive kinds of behaviour exhibited by hosts against parasitoids are violent wriggling, biting and spitting. The behaviour of the braconid parasitoid Cotesia sesamiae attacking stemboring larvae inside their feeding tunnel in the plant stem was investigated in maize and sugarcane stem pieces and transparent artificial tunnels. Attacking a defending stemborer host inside the confined space of a tunnel was shown to be risky for the female parasitoid. A considerable proportion (25%) of female wasps were killed in their attempt to attack the spitting and biting host. No difference was found in the behaviour of C. sesamiae attacking the suitable host Sesamia calamistis or the unsuitable host Eldana saccharina. The consequences of this high mortality risk involved in each host attack is discussed in relation to the ecology of the parasitoid.     

Sex ratio regulation in Coccygomimus turionella Linnaeus (Hymenoptera: Ichneumonidae) and its ecological implications

Abstract. 1. Sex regulation and its relevance to the ecology of a k-selected pupal parasitoid was investigated in Coccygomimus turionellae.
2. The ratio varied with host size, females predominating in large hosts.
3. Egg transfer experiments and comparative mortality rates among the progeny of virgin and inseminated females demonstrated that the phenomenon was due to parental behaviour.
4. The study of the mechanism confirmed Aubert's hypothesis of host size estimation with the addition that the host had to be exposed from the poles and had to contain the proper host kairomones.
5. Host size was highly correlated to parasitoid fecundity via influences on size and longevity but not the number of ovarioles per female or daily egg production.
6. Host encounters are more limiting than egg production and host size had no effect on host acceptance.
7. Sex regulation allows a maximal host encounter rate at the same time that it maximizes the reproductive potential of female progeny.
8. Low host density increased the production of female progeny resulting in more offspring searching for the limited resource. Concealed hosts and a high host density resulted in a shift towards a Fisher 1:1 sex ratio.     

Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Density-related foraging behaviour in Closterocerus tricinctus, a parasitoid of the leaf-mining moth, Cameraria hamadryadella

• 1 We examined the foraging behaviour of the parasitoid wasp, Closterocerus tricinctus (Ashmead) (Chalcidoidea: Eulophidae), as it visited larvae of the leaf-mining moth, Cameraria hamadryadella (Lepidoptera: Gracillariidae), in an outbreak population.
• 2 We tracked females of C.tricinctus, recording the time spent searching for mines and handling host larvae. The density of leaf-mines (host larvae) and their condition were recorded for each leaf visited. A subset of leaves visited by C.tricinctus was enclosed in fine mesh bags so that foraging success could be determined by rearing or dissection. The average density of mines and the average leaf-area mined was estimated for a random sample of leaves from each tree.
• 3 The selection of leaves upon which to forage appears to be density-dependent. C.tricinctus visits leaves with leaf-mine densities twice the average, and when switching leaves lands directly on leaf-mines 5 times more often than expected assuming random landings.
• 4 The total time spent foraging on a leaf, the average time spent handling hosts, and the total search time within leaves tend to decline on leaves with many hosts, but the observed declines are not statistically significant.
• 5 The proportion of leaf-mines visited within a leaf is strongly inversely density-dependent. 30% of visits to leaf-mines are re-visits and 29% of handling time is spent re-handling previously visited hosts. Furthermore, only 21% of visits to mines lead to successful parasitism. We suggest that self-interference and the avoidance behaviour of the host may reduce the number of visits of leaf-mines by C.tricinctus within a leaf.
• 6 The effect of the strongly inversely density-dependent foraging investment within leaves is to offset the observed density-dependent pattern of leaf visitation making the overall spatial pattern of visitation by C.tricinctus to mines of C.hamadryadella inversely density-dependent.
• 7 We suggest that the uncertainty of C.tricinctus surviving on multiply mined leaves because of density-dependent host mortality due to intraspecific competition in high-density host populations, the rarity of high-density host populations, and the rarity of multiply-mined leaves in low-density host populations combine to select against an aggregative response within leaves by C.tricinctus.

     

A hierarchical multi‐scale analysis of the spatial relationship between parasitism and host density in urban habitats

Studies on spatial density dependence in parasitism have paid scarce attention to how changes in host density at different hierarchical scales could influence parasitism in an herbivore at a particular scale. Here, we evaluated if rates of parasitism per leaf (by the whole parasitic complex and by dominant species) of the specialist leaf miner Liriomyza commelinae (Diptera: Agromyzidae) respond to variations in host density at the leaf, plant patch and site levels in an urban setting. We used multi‐level Bayesian models that incorporate the spatial hierarchy occurring in this system, as well as habitat factors previously found to have an effect on the L. commelinae parasitoid community in an urban context (patch size, patch isolation and urbanization level). According to the fitted model, overall parasitism rates decreased with increasing number of mines per leaf, being independent of host‐density variations at patch and site level. Patch structure was found to have a strong effect on parasitism rates per leaf. The analysis of parasitism by parasitoid species separately showed consistent results with the response at community level. These results suggest that parasitism of the parasitoid community here studied would be sensitive to hierarchical cues related to the host at the leaf level and to the host habitat at the patch level.     

Effects of meadow suitability on female behaviour in the alpine butterfly Parnassius smintheus

Abstract  1. Many butterfly populations persist in networks of naturally fragmented habitat patches. Movement and reproductive decisions made by adult females are critical to the persistence of these populations because colonisation of extinct habitat patches in the network requires emigration of fecund adult females from their natal meadow and their subsequent establishment in the extinct patch.
2. Movement and oviposition behaviours of mated Parnassius smintheus females released in suitable meadows (a good- and a poor-quality meadow) and an unsuitable meadow were compared, to determine whether adult females consider meadow suitability for their offspring despite frequent oviposition events off the larval host plant.
3. Bootstrap and correlated random walk analyses of female step lengths and turn angles demonstrated that females flew more randomly in the unsuitable meadow than in the suitable meadows. Although females tended to turn the sharpest angle between landing sites in the good-quality meadow, and fly the smallest distance between landing sites and displace the smallest distance from the release site in the suitable meadows, no significant differences were detected in turn angle, step length, and dispersal rates between suitable and unsuitable meadows.
4. Results from female flight observations and a caged oviposition study suggest that females lay significantly more eggs in suitable habitat than in unsuitable habitat despite not ovipositing on the host plant, and support the above findings.
5. Movement and oviposition behaviours of adult female P. smintheus promote their retention within meadows that can support their offspring.     

Plant cues influence searching behaviour and parasitism in the egg parasitoid Trichogramma nr. brassicae

Abstract. 1. The effect of experience of plant cues at emergence on searching behaviour and parasitism was investigated in two strains of Trichogramma nr. brassicae (Hymenoptera: Trichogrammatidae).
2. Wasps reared on Sitotroga cereallela were allowed to emerge on a tomato plant or in a vial, with or without food. For one of the strains, females emerging on tomato searched significantly longer on a tomato seedling than females emerging in a vial.
3. The experience effect lasted between 1 and 2 days. It involves associating plant stimuli with the remains of the host, because females emerging from their host on a tomato plant had an increased searching response to tomato, but females transferred to the plant immediately after emergence did not.
4. The effect of emergence environment on parasitism of the host Helicoverpa punctigera on tomato and lettuce seedlings was tested. Wasps were allowed to emerge on seedlings of tomato or lettuce, or in an empty vial. For one strain, females experienced with tomato at emergence parasitized significantly more hosts on tomato than did females emerging on lettuce or in a vial. Parasitism on lettuce was not influenced by the treatments.     

The biology and host searching behaviour of a Cynipoid parasite of aphidophagous syrphid larvae

Abstract. 1. Callaspidia defonscolombei was found to be a common, solitary, thelytokous parasitoid of aphidophagous syrphid larvae. In 1977 it was bivoltine with adults being most numerous in early August and late September. It is probably polyphagous.
2. An analysis of host searching behaviour suggests that females respond to an aphid odour bringing them to the region of an aphid colony.
3. Syrphid hosts are located within the aphid colony by response to a contact chemical. There is a host size preference, only larger second and third instar larvae being attacked.
4. Females inject a venom, which temporarily paralyses host larvae, and place the egg inside a cerebral ganglion.     

Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae)

Abstract. 1. A study of searching behaviour on wheat and host preference of Aphidius rhopalosiphi (DeStefani-Perez) is described.
2. Parasitoids divided their time equally between the leaves but spent very little time on the ear.
3. After contact with honeydew or an aphid host, parasitoids were arrested in a particular area and increased the time spent searching.
4. Aphids feeding on the ear were parasitized less successfully, since their position between the grains protected them from parasitoid attacks.
5. A.rhopalosiphi exhibited no preference for Metopolophium dirhodum (Walker) or Sitobion avenae (Fabricius), although the handling time for the latter was significantly longer; this resulted in fewer S.avenae being parasitized when it was abundant. Parasitoids did not switch between hosts in these experiments.
6. As a result of its searching behaviour, A.rhopalosiphi will encounter and parasitize M.dirhodum feeding on the leaves more frequently than S.avenae, which feeds on the ear. This will limit the parasitoid's ability to regulate populations of the cereal aphid S. avenae.