The importance of honeydew as food for larvae of Chrysoperla carnea in the presence of aphids

Larvae of the common green lacewing Chrysoperla carnea are predacious and feed on a wide range of small, soft‐bodied arthropods. In addition to their feeding on prey arthropods to cover their nutritional requirements for growth and development, the consumption of non‐prey foods such as honeydew has been reported. It is commonly believed that these food supplements are primarily exploited by the larvae when prey is scarce or of low nutritional quality. Here, we assess whether C. carnea larvae also use honeydew when high‐quality aphid prey are readily available. In a choice experiment, the feeding behaviour of C. carnea larvae was observed in the presence of both aphids and honeydew. The larvae were starved, aphid‐fed, or honeydew‐fed prior to the experiment. The time spent feeding on honeydew compared with feeding on aphids was highest for starved larvae and lowest for honeydew‐fed larvae. Among the three treatments, the aphid‐fed larvae spent the most time resting and the least time searching. In an additional experiment food intake was assessed in terms of weight change when larvae were provided with an ad libitum supply of either aphids or honeydew. Larvae yielded a significant lower relative weight increase on honeydew compared with aphids. The reduced weight increase on honeydew was compensated when larvae were subsequently provided with aphids, but not when honeydew was provided again. This study showed that (i) prior honeydew feeding reduces overall aphid consumption, and (ii) larvae do consume honeydew even after they have been given ad libitum access to aphids. The fact that larvae of C. carnea still use honeydew as a food source in the presence of suitable prey underlines the importance of carbohydrates as foods.     

The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae)

Abstract.  1. To clarify the use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L., searching behaviour of ladybird larvae for Aphis craccivora Koch and Acyrthosiphon pisum Harris and the abundance of honeydew under aphid colonies were examined in laboratory experiments.
2. More larvae responded by climbing the plants with aphids than responded to plants without aphids. When the plants were replaced with sticks, in order to exclude visual and olfactory cues from plants and aphids, more larvae of C. septempunctata climbed sticks above the area that contained honeydew than climbed sticks above the area that did not contain honeydew. Then, ladybird larvae use honeydew as a contact kairomone when foraging for aphids.
3.  Aphis craccivora deposited a larger number of honeydew droplets beneath the plants than did similar numbers of A. pisum. Thus, C. septempunctata larvae licked more frequently the honeydew of A. craccivora than that of A. pisum and spent longer searching on the area containing honeydew of A. craccivora than that of A. pisum . Consequently, a larger number of larvae climbed a stick above honeydew of A. craccivora than that of A. pisum.
4. It may be also considered that C. septempunctata larvae can distinguish honeydew of the two aphid species and respond more strongly to A. craccivora than A. pisum.     

Influence of aphid honeydew on the foraging behaviour of Hippodamia convergens larvae

1. Environmental cues associated with prey are known to increase predator foraging efficiency. Ladybird larvae are major predators of aphids. The sugary excretion of aphids (honeydew) has been proposed to serve as a prey‐associated cue for ladybird larvae. 2. Ladybird larvae are regularly found on the ground moving between plants or after falling off plants. The use of prey‐associated cues would be particularly beneficial for ladybird larvae on the ground in that such cues would help them to decide which plants to climb because aphids are patchily distributed within as well as amongst plants and, as a result, many plants are either not infested with aphids or do not host an aphid species of high nutritional value for ladybird larvae. 3. Laboratory experiments with larvae of Hippodamia convergens Guérin‐Méneville (Coleoptera: Coccinellidae) were carried out to explore whether honeydew accumulated on the ground is used as a foraging cue. The study also investigated whether, if honeydew is a foraging cue, larvae show differential responses to honeydew of high‐quality prey Acyrthosiphon pisum Harris compared with that of low‐quality prey Aphis fabae Scopoli (both: Homoptera: Aphididae). 4. Hippodamia convergens larvae stayed longer in areas containing honeydew but did not engage in longer bouts of searching. Furthermore, larvae did not distinguish between honeydew from high‐ and low‐quality aphid prey.     

Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata

Abstract. 1. Adult males of the two-spot ladybird beetle, Adalia bipunctata , did not show a functional response to increase in aphid abundance and consumed markedly fewer aphids than do the females.
2. At high densities of prey, females spent more time in area-restricted search than when prey was scarce. Males were always less active than females and they did not respond to an increase in prey abundance by a change in searching behaviour.
3. After a brief encounter with a female, a male showed area-restricted searching behaviour. This behaviour occurred in response to encountering a female's elytra and in particular to a chloroform-soluble component (sex pheromone) present on or in the elytra.
4. Males needed to encounter a female in order to respond to her presence, which indicated the pheromone is a contact pheromone.
5. The searching behaviour of males appeared to be mainly directed towards locating females; that of females towards locating aphids. This difference between the sexes should be taken into account when quantifying the predatory response of ladybirds to aphid abundance in the field.     

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.     

Honeydew: A food resource or arrestant for the mealybug predatorCryptolaemus montrouzieri?

The study investigated whether honeydew is a source of food or is an arrestant stimulus for adults and 4th instar larvae ofCryptolaemus montrouzieri. Adult predators fed on honeydew but produced few viable eggs. In the presence of honeydew the adult and larvae spent a significantly longer time searching and made more intensive searches on leaf surfaces than on clean parts of the leaf. We concluded that the honeydew was both a food resource and an arrestant.

---

Résumé Ce travail a pour but de déterminer si le miellat est une source de nourriture ou un stimulus d'arrêt pour les adultes et les larves de 4° stade deCryptolaemus montrouzieri. Les prédateurs adultes nourris de miellat produisent peu d'œufs viables. L'adulte et la larve de coccinelle font des recherches significativement plus longues et plus intensives sur les surfaces foliaires couvertes de miellat que sur les parties indemnes de miellat. L'étude conclut que le miellat constitue à la fois une source de nourriture et un stimulus d'arrêt.

     

Prey location and prey choice by the freshwater leech Erpobdella octoculata using foraging kairomones

1. The freshwater leech, Erpobdella octoculata , is a generalist predator feeding on prey organisms such as Tubifex spp., Chironomus spp. and Asellus aquaticus. Using different experimental designs, we studied the use of foraging kairomones by the leeches for prey location.
2. Leeches were attracted to living as well as to freshly killed larvae of Chironomus sp., to Tubifex sp., and to A. aquaticus offered in Petri dishes covered with gauze. The leeches also reacted to an extract of macerated Tubifex sp. presented in agar.
3. Using ion exchange chromatography, the presence of histidine and glutamic acid was demonstrated in water contaminated by living larvae of Chironomus sp. and Tubifex sp. Agar blocks containing a synthetic mixture of these compounds at concentrations above 5 mg mL⁻¹ were attractive to the leeches.
4. Choice tests showed that leeches preferred chemical signals from Tubifex sp. over larvae of Chironomus sp. No difference was found between chemicals from Tubifex sp. and A. aquaticus , and A. aquaticus and larvae of Chironomus sp.
5. The results demonstrate that E. octoculata uses specific foraging kairomones in searching for prey and indicate that amino acids serve as foraging kairomones.     

Foraging by the carabid Agonum dorsale in the field

Abstract. 1. Small arenas in the field were used for observing adult Agonum dorsale (Pont.) foraging in a wheat crop.
2. The carabid showed no significant change in behaviour between low and high aphid density arenas.
3. Individuals foraged nocturnally and spent most of their time on the ground searching for prey. They climbed infrequently and then not high enough to reach aphid aggregations on the ears and flag leaves of wheat.
4. Gut dissection showed that more individuals had eaten aphids in the high aphid density arena than the low. Recording of aphid distribution within the arenas showed that this increase in aphid consumption could be explained by A.dorsale capturing aphids on the ground. Prey availability per unit area was in fact higher on the ground than on the wheat.
5. The contribution of ground-zone predators such as A.dorsale to the control of cereal aphids will be determined by the frequency with which aphids arrive on the ground and the proportion of these which reclimb the wheat and reproduce in the absence of predation.     

Prey finding by larvae and adult females of shape Episyrphus balteatus

The prey-location behaviour of larvae of Episyrphus balteatus DeG. (Dipt.: Syrphidae) was investigated in two different experimental set-ups. First instar larvae exhibited directed search over short distances, guided by olfactory cues from aphids, but not from honeydew. However, second and third instars did not respond to aphid-plant-complex odours in a 4-arm-olfactometer. Aphid extracts, honeydew and sucrose were found to be feeding stimulants for the larvae. The oviposition behaviour of female syrphids was investigated in a series of two-choice experiments: females were able to evaluate aphid numbers and adjust oviposition rates accordingly, with higher prey numbers eliciting increased oviposition, even when the aphids were removed at the start of the experiment. The presence of conspecific syrphid larvae did not inhibit oviposition when the females were deprived of suitable oviposition sides before the experiments were conducted.     

A fly larva (Syrphidae: Ocyptamus) that preys on adult flies

Predatory syrphid larvae feed on relatively immobile prey, but here we report the first case (as far as we are aware) of obligatory predation on very mobile prey. Larvae of an undescribed species of Ocyptamus (Diptera: Syrphidae) were found in whitefly (Hemiptera: Aleyrodidae) aggregations on the undersides of citrus leaves. However, instead of preying on the whitefly nymphs (as would be expected), the larvae preyed on adult flies (Diptera) that were attracted to the honeydew. In the laboratory, larvae captured significantly more flies on whitefly infested leaves than on washed leaves, and generally abandoned leaves that lacked whiteflies. Most cases of successful prey capture involved flies that probed the anterior part of the larva's body with its proboscis (as if it were honeydew). The syrphid larva lashed out at the fly and entangled it in sticky oral secretion. The prey did not recover when they were removed from the larva, suggesting that this new predatory species also employs venom to subdue its prey. Although the larvae consumed some honeydew, they were unable to complete their development on this diet. Two parasitoids were reared from Ocyptamus puparia, Proaspicera sp. (Hymenoptera: Figitidae) and Paracarotomus sp. (Hymenoptera: Pteromalidae), both of which are endoparasitic koinobionts.     

The role of honeydew as an ovipositional stimulant for two species of syrphids

The influence of honeydew contamination on egg laying by the syrphidsEpisyrphus balteatus (Deg.) andPlatycheirus albimanus (F.) on ears of wheat was investigated in a large laboratory flight cage. Artificially-applied honeydew elicited oviposition byE. balteatus but not byPlatycheirus albimanus.Episyrphus balteatus females landed more frequently on ears contaminated with honeydew than on clean ears, suggesting a response to honeydew volatiles. Honeydew from the rose-grain aphidMetopolophium dirhodum and from the pea aphidAcyrthosiphon pisum stimulatedE. balteatus to lay eggs, whereas honeydew from the nettle aphidMicrolophium carnosum did not. The number of eggs laid byE. balteatus increased with increasing honeydew concentration. At low honeydew concentrations the presence of aphids increased oviposition byE. balteatus, but aphid presence had little effect on the number of eggs laid at high honeydew concentrations.     

Plant effects on prey choice by a vespid wasp, Polistes arizonensis

1. The effects of sunflower, Helianthus annuus , and groundcherry, Physalis pubescens , eaten by the tobacco budworm ( Heliothis virescens ), on predation by paper wasps ( Polistes arizonensis ) were examined.
2. Polistes arizonensis foragers took more caterpillars from H. annuus plants than P. pubescens in paired-choice tests.
3. They took longer to locate prey and apparently gave up searching faster on artificial plants mimicking P. pubescens than on artificial plants mimicking H. annuus .
4. In paired-choice tests for chemical effects, wasps chose more caterpillars within H. annuus odour than in P. pubescens odour.
5. They also chose more H. annuus -reared larvae than P. pubescens -reared larvae when they were presented without plants. Handling time was not affected.     

Asymmetric intraspecific competition among larvae of the damselfly Ischnura elegans (Zygoptera: Coenagrionidae)

Abstract. 1. A laboratory competition experiment is described in which the growth and development rates of larvae of the damselfly Ischnura elegans (Lind.) were measured over an entire instar.
2. Two larval instars which commonly occur together in the field were used in the experiment; they were maintained with a superabundance of prey and either larvae from the same or the larger/smaller instar.
3. Small larvae suffered increased development times and decreased size increases at the moult in the presence of large larvae but similar interference effects were not evident when these smaller larvae were in the presence of other small larvae.
4. Development time and size increases of large larvae were not significantly affected by the presence of small larvae.
5. Irrespective of the instar combinations investigated, interference effects were reduced when there were more perches available, although in only a few cases was this reduction significant.
6. The consequences of the asymmetric competition reported in the experiment for the study of lifetime reproductive success in damselflies are discussed. Late emerging adults may incur reduced reproductive success.     

Ant mutualists alter the composition and attack rate of the parasitoid community for the gall wasp Disholcaspis eldoradensis (Cynipidae)

Abstract.  1. The strength or density dependence of pairwise species interactions can depend on the presence or absence of other species, especially potential mutualists.
2. The gall wasp Disholcaspis eldoradensis induces plant galls that secrete a sweet honeydew from their top surfaces while the wasp larvae are active. These galls are actively tended by Argentine ants, which collect the honeydew and drive off parasitoids attempting to attack the gall wasp.
3. When ants were excluded, the total rate of parasitism by seven species of parasitoids increased by 36%, and the rate of gall-wasp emergence decreased by 54%.
4. The total percentage parasitism was affected by gall density when ants were excluded but not when ants were unmanipulated, suggesting a change in parasitoid functional responses due to ant tending.
5. In addition, excluding ants significantly altered the proportions of different parasitoid species that emerged from galls; one parasitoid species increased from 1% to 34%, and another decreased from 46% to 19%.
6. The invasive Argentine ants studied are capable of maintaining the mutualism with the gall wasps that evolved in the presence of different ant species and also act as a selective filter for the local community of generalist parasitoids trying to attack this gall species.     

Searching behavior and time budgets of the predator Podisus maculiventris

Searching behavior of the predaceous insect Podisus maculiventris (Say) (Heteroptera: Pentatomidae) was investigated in the laboratory to verify assumptions made in a predator search model. Female predators were placed into an arena containing 30 lima bean plants (Phaseolus lunatus L.), each having five numbered leaflets. Prey were third-instar larvae of Mexican bean beetle (Epilachna varivestis Mulsant) at two densities. Predators were observed for 4 h periods as they searched the plant canopy. Results showed that predators searched a greater area and for longer at low prey density than at high prey density. Predators apparently searched plants without using cues, did not search areas of the canopy repeatedly after attacks, and spent approximately 1 h handling prey. Predators spent more time resting than searching, and attack rates were negatively correlated with rest time, but were not correlated with search time. Long resting periods by predators may be a result of energy conservation. The implications for using predators such as P. maculiventris against pests in crops are (i) the predators' searching behavior limits the number of prey attacked, and (ii) the predator may be able to persist at low prey densities better than species with different searching behaviors.     

Dealing with food shortage: larval dispersal behaviour and survival on non‐prey food of the hoverfly Episyrphus balteatus

1. Predatory larvae often have to face food shortages during their development, and thus the ability to disperse and find new feeding sites is crucial for survival. However, the dispersal capacity of predatory larvae, the host finding cues employed, and their use of alternative food sources are largely unknown. These aspects of the foraging behaviour of the aphidophagous hoverfly (Episyrphus balteatus De Geer) larvae were investigated in the present study. 2. It was shown that these hoverfly larvae do not leave a plant as long as there are aphids available, but that dispersing larvae are able to find other aphid colonies in the field. Dispersing hoverfly larvae accumulated on large aphid colonies, but did not distinguish between different pea aphid race–plant species combinations. Large aphid colonies might be easier to detect because of intensified searching by hoverfly larvae following the encounter of aphid cues like honeydew that accumulate around large colonies. 3. It was further shown that non‐prey food, such as diluted honey or pollen, was insufficient for hoverfly larvae to gain weight, but prolonged the survival of the larvae compared with unfed individuals. As soon as larvae were switched back to an aphid diet, they rapidly gained weight and some pupated after a few days. Although pupation and adult hatching rates were strongly reduced compared with hoverflies continuously fed with aphids, the consumption of non‐prey food most probably increases the probability that hoverfly larvae find an aphid colony and complete their development.     

Influence of artificial honeydew on larval development and survival inChrysoperla carnea [Neur., Chrysopidae]

The effects of providing (a) an artificial honeydew consisting of yeast autolysate, sugar and water in the ratio 4∶7∶10 live prey (eggs ofEphestia kuehniella), and (b) water and life prey, on larval development and survival in the green lacewingChrysoperla carnea were examined. Compared with larvae provided with eggs and water, those given eggs and artificial honeydew were more likely to complete their development and did so significantly more rapidly.     

Searching efficiency of the lady beetleCoccinella septempunctata larvae in uniform and patchy environments

Experiments were conducted on the searching behavior and searching efficiency of the lady beetleCoccinella septempunctata bruckii Mulsant under conditions of various prey distributions and prey densities. The larvae changed their searching behavior before and after feeding. Before feeding the larvae moved quickly and the searching paths were nearly linear. But after feeding the speed decreased and turning angle increased. The speed and turning angle reverted gradually and recovered the initial pattern 95 s after feeding. The searching efficiency differed depending on the prey distribution. At low prey density, searching was most efficient when prey were distributed uniformly. But at middle and high prey densities, searching was most efficient when prey items were highly aggregated. The observed searching behavior of 4th instarC. septempunctata larvae was likely to be optimal considering the natural distribution of colonies of their prey, aphids.     

Interspecific differences in movement and hunting success in damselfly larvae (Zygoptera: Insecta): responses to prey availability and predation threat

SUMMARY. 1. Freshwater invertebrate predators can alter their hunting behaviour in response to prey availability and threat from their own enemies. Movement patterns and hunting success of the larvae of two species of damselfly (Zygoptera: Insecta), Enallagma cyathigerum (L.) and L. sponsa (Hansemann), were monitored in four combinations of prey availability and enemy threat. Aeshna juncea (L.) (Anisoptera: Insecta) larvae acted as predator and Daphnia magna Straus (Cladocera: Crustacea) as prey in the combinations: no predator/no prey; one Aeshna present/no prey; no predator/thirty Daphnia present; one Aeshna present/ thirty Daphnia present.
2. E. cyathigerum showed significantly reduced movement in the +Aeshna/no prey treatment but hunting success was not significantly affected. No other treatment effects were noted. L. sponsa movement patterns differed significantly across all four treatments and hunting success was significantly reduced in the presence of Aeshna .
Interspecifically, movement patterns of the two species differed markedly in all four treatments. L. sponsa larvae were much more active, and caught many more prey. Despite their activity L. sponsa larvae did not appear markedly more vulnerable than the immobile E. cyathigerum .
3. The interspecific differences between the two damselflies reflect predictions based on larval life-history. Activity patterns and ability to capture adequate prey under varying levels of predation may be important in the ecology of damselfly species.     

Cleaning Up After a Meal: The Consequences of Prey Disposal for Pit‐Building Antlion Larvae

Predators use a variety of strategies for capturing prey. Trap‐building predators can save on searching and encountering costs by investing in the construction and maintenance of traps such as webs and pits. However, what to do with partially consumed prey poses a potential problem. Antlion larvae (Myrmeleon acer) catch ants in conical pits, and dispose of partially consumed carcasses by flicking them a short distance away. We tested whether this prey‐disposal behaviour affects the effectiveness of antlion pits. We observed ant behaviour around artificially constructed pits and compared falls into pits with clean margins to those with conspecific ant carcasses or control objects around the pit edge. The presence of objects near pits affected the behaviour of live ants, and reduced the effectiveness of pits. Live ants spent the most time examining fresh ant carcasses, but the presence of any object near pits deterred pitfalls. Ants fell into pits significantly more often when pit edges were clean, suggesting that antlions could incur a prey capture cost from flicking carcasses from pits as well as from the accumulation of other debris around pit margins.