Pre-oviposition Behaviour Research Articles

Pre-oviposition behavior of Aedes aegypti in field: First report of eggs laying on water surface in an artificial breeding site

This study presents the first report of Aedes aegypti laying eggs on the water surface of an artificial breeding site in the field. This report occurred in the city of Rio de Janeiro inside a white bucket containing 11 liters of rainwater. Conspecific larvae had previously been found in this bucket. From the 219 eggs obtained, 135 (61.6%) were laid on the water and 84 (38.3%) on the border of the bucket. Larvae (4th instar) and adults obtained from the eggs were identified as A. aegypti. This behavior may influence the population dynamics of A. aegypti and expands the knowledge about the species adaptation. This report confirms the species’ ability to lay eggs on the water surface of artificial breeding sites in the field and suggests the hypothesis that pheromones in the water may influence the females to lay eggs on water. KEY WORDS: Ethology; Aedes aegypti; adaptation; disease vectors; mosquito vectors.

The arms race between heliconiine butterflies and Passiflora plants - new insights on an ancient subject.

Heliconiines are called passion vine butterflies because they feed exclusively on Passiflora plants during the larval stage. Many features of Passiflora and heliconiines indicate that they have radiated and speciated in association with each other, and therefore this model system was one of the first examples used to exemplify coevolution theory. Three major adaptations of Passiflora plants supported arguments in favour of their coevolution with heliconiines: unusual variation of leaf shape within the genus; the occurrence of yellow structures mimicking heliconiine eggs; and their extensive diversity of defence compounds called cyanogenic glucosides. However, the protection systems of Passiflora plants go beyond these three features. Trichomes, mimicry of pathogen infection through variegation, and production of extrafloral nectar to attract ants and other predators of their herbivores, are morphological defences reported in this plant genus. Moreover, Passiflora plants are well protected chemically, not only by cyanogenic glucosides, but also by other compounds such as alkaloids, flavonoids, saponins, tannins and phenolics. Heliconiines can synthesize cyanogenic glucosides themselves, and their ability to handle these compounds was probably one of the most crucial adaptations that allowed the ancestor of these butterflies to feed on Passiflora plants. Indeed, it has been shown that Heliconius larvae can sequester cyanogenic glucosides and alkaloids from their host plants and utilize them for their own benefit. Recently, it was discovered that Heliconius adults have highly accurate visual and chemosensory systems, and the expansion of brain structures that can process such information allows them to memorize shapes and display elaborate pre-oviposition behaviour in order to defeat visual barriers evolved by Passiflora species. Even though the heliconiine-Passiflora model system has been intensively studied, the forces driving host-plant preference in these butterflies remain unclear. New studies have shown that host-plant preference seems to be genetically controlled, but in many species there is some plasticity in this choice and preferences can even be induced. Although much knowledge regarding the coevolution of Passiflora plants and heliconiine butterflies has accumulated in recent decades, there remain many exciting unanswered questions concerning this model system.

No effect of recent sympatry with invasive zebra mussel on the oviposition decisions and reproductive success of the bitterling fish, a brood parasite of unionid mussels

The presence of non-native species can affect coevolved relationships. However, rapid reciprocal changes in coevolutionary associations provide the potential to quickly respond to a new situation. We studied a system where bitterling fish (Rhodeus amarus) parasitize unionid mussels by laying their eggs onto their gills. This association is affected by the infestation of unionid shells by the non-native zebra mussel (Dreissena polymorpha). In a series of experiments under experimental, semi-natural and natural conditions, we compared the behavioural response to zebra mussel infestation of unionid shells, its effect on oviposition decisions and their population consequences between bitterling populations naive to zebra mussels and those recently sympatric with zebra mussels. We found no effect of recent sympatry on bitterling preoviposition behaviour and oviposition decisions and only a weak effect on their reproductive success. Bitterling from both populations inspected infested and non-infested mussels at the same rate but preferred to oviposit into non-infested unionid hosts. However, neither bitterling population completely avoided oviposition into infested unionids and three ovipositions into zebra mussels were observed. Overall, there was a clear negative relationship between the number of zebra mussels on unionid host shells and the number of juvenile bitterling emerging from the mussels. Our study demonstrated a lack of rapid evolutionary response to adaptively modulate oviposition choice after recent zebra mussel invasion.

Oviposition behaviour in Paysandisia archon (Lepidoptera: Castniidae)

SummaryPaysandisia archon (Burmeister, 1880) (Lepidoptera: Castniidae) is a South American insect developing on palms and recently introduced in Europe where it damages most palm species. Understanding the oviposition behaviour would be decisive for risk assessment and pest management but key points on oviposition behaviour are missing. Using wind tunnel and field experiments, we investigated the oviposition timing, the attraction behaviour of mated females to palms and the different steps of oviposition behaviour. Results showed that oviposition behaviour occurred between 3 pm and 6 pm. In the field, gravid females were significantly more attracted by the palm crown than virgin females. The ovipositing females exhibited distinctive steps before ovipositing. Subsequent to alighting on the crown, pre-oviposition behaviour was characterized by two main behavioural steps: walking and probing the surface with antennae and ovipositor. After the choice of oviposition place, the gravid female remains motionless and the extendible ovipositor is deeply introduced into the upper fibrous part of the crown. About 10 eggs can be lays at the same place. Finally, the female starts to walk again and reinitiates the same behavioural sequences. This paper supports the hypothesis that odours from the crown may play a key role in gravid female attraction. The study assessed that P. archon lays on the palm crown, the part of the palm that should be treated for population monitoring.

Ovoviviparity in Macrocheles glaber (Müller) (Acari: Macrochelidae), with notes on parental care and egg cannibalism

In Macrocheles glaber (Müller), oviposition can involve either oviparity or egg production followed by immediate hatching of the larva, a process that may be called ovoviviparity. We observed three phases in the process of ovoviviparity: preoviposition behaviour, oviposition followed by holding the egg under the gnathosoma and hatching of the larva assisted by the female. Two factors appear to favour the occurrence of ovoviviparity in this species: poor feeding and poor substrate quality. We witnessed egg cannibalism four times in two of the four females that we observed. We discuss the consequences of variable oviposition strategy, parental care and egg cannibalism in M. glaber in the context of maximization of reproductive success.

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

Although aggregation in non‐social arthropods is common, its adaptive value is not always clear. Oviposition behaviour of the viburnum leaf beetle (Pyrrhalta viburni) is aggregative, with females preferring to lay eggs on twigs already infested by conspecifics. We previously showed that aggregative oviposition aided in overcoming host plant defences. Here we explore two additional benefits of this behaviour: reduction of time investment in oviposition; and improvement of host use by larval group feeding. In video‐recorded trials, the presence of conspecific egg masses did not have an impact on the time associated with oviposition, but it did affect females' pre‐oviposition behaviour: the length of foraging movements was 21% shorter on infested than on non‐infested twigs, and was concentrated near the infested area. In two separate studies of insect performance, larvae were reared to maturity in groups of different densities (five or 10, and five or 20, respectively) on several hosts (four and 17 Viburnum spp., respectively). Independent of host species, adults were > 13% heavier (groups of 10 vs. five), and pupation success was 27% higher (groups of 20 vs. five) at higher larval density. Two additional effects were dependent on host species: larval survivorship (groups of 10 vs. five), and adult mass (groups of 20 vs. five). These effects were not associated with plant defensive traits (i.e. trichomes or leaf toughness), but adult mass was associated with host nutritional quality (i.e. foliar nitrogen content). These results show that several traits of P. viburni larval performance are positively density‐dependent, and suggest that benefits of group feeding could have played a role in the evolution of oviposition behaviour in P. viburni. Our results also demonstrate that plant quality can mediate benefits of aggregation, underscoring the importance of ecological context in understanding the feeding strategies of insects.

Water vapour is a pre-oviposition attractant for the malaria vector Anopheles gambiae sensu stricto

BackgroundTo date no semiochemicals affecting the pre-oviposition behaviour of the malaria vector Anopheles gambiae sensu lato have been described. Water vapour must be the major chemical signal emanating from a potential larval habitat, and although one might expect that gravid An. gambiae s.l. detect and respond to water vapour in their search for an aquatic habitat, this has never been experimentally confirmed for this species. This study aimed to investigate the role of relative humidity or water vapour as a general cue for inducing gravid An. gambiae sensu stricto to make orientated movements towards the source.MethodsThree experiments were carried out with insectary-reared An. gambiae s.s. One with unfed females and two with gravid females during their peak oviposition time in the early evening. First, unfed females and gravid females were tested separately in still air where a humidity difference was established between opposite ends of a WHO bioassay tube and mosquitoes released individually in the centre of the tube. Movement of mosquitoes to either low or high humidity was recorded. Additionally, gravid mosquitoes were released into a larger air-flow olfactometer and responses measured towards collection chambers that contained cups filled with water or empty cups.ResultsUnfed females equally dispersed in the small bioassay tubes to areas of high and low humidity (mean 50% (95% confidence interval (CI) 38-62%). In contrast, gravid females were 2.4 times (95% CI 1.3-4.7) more likely to move towards high humidity than unfed females. The results were even more pronounced in the airflow olfactometer. Gravid females were 10.6 times (95% CI 5.4-20.8) more likely to enter the chamber with water than a dry chamber.ConclusionsWater vapour is a strong pre-oviposition attractant to gravid An. gambiae s.s. in still and moving air and is likely to be a general cue used by mosquitoes for locating aquatic habitats.

Priority resource access mediates competitive intensity between an invasive weevil and native floral herbivores

Mechanisms underlying invasive species impacts remain incompletely understood. We tested the hypothesis that priority resource access by an invasive biocontrol weevil, Rhinocyllus conicus, intensifies and alters the outcome of competition with native floral herbivores over flower head resources of the non-target, native host plant Cirsium canescens, specifically with the predominant, synchronous tephritid fly Paracantha culta. Four main results emerged. First, we documented strong, asymmetric competition, with R. conicus out-competing P. culta. Second, weevil priority access to floral resources accelerated competitive suppression of P. culta. Evidence for competitive suppression with increased weevil priority included decreases in both the numbers and the total biomass of native flies, plus decreases in individual P. culta fly mass and, so, potential fitness. Third, we found evidence for three concurrent mechanisms underlying the competitive suppression of P. culta by R. conicus. Prior use of a flower head by R. conicus interfered with P. culta pre-oviposition behavior. Once oviposition occurred, the weevil also reduced fly post-oviposition performance. Preemptive resource exploitation occurred, shown by the significant effect of flower head size on the total number of insects developing and in the magnitude of R. conicus effects on P. culta. Interference also occurred, shown by a spatial shift of surviving P. culta individuals away from the preferred receptacle resources as R. conicus priority increased. Finally, fourth, using an individual-based model (IBM), we found that the competitive interactions documented have the potential for imposing demographic consequences, causing a reduction in P. culta population sizes. Thus, priority resource access by an invasive insect increased competitive impact on the predominant native insect in the invaded floral guild. This study also provides the first experimental evidence for non-target effects of a weed biological control agent on an associated native insect herbivore.

Morphological characteristics of sensilla on the female ovipositor of Lype phaeopa (Psychomyiidae; Trichoptera)

An important aspect of the association of Lype phaeopa (Stephens) with submerged wood is the oviposition behavior of adult females, which preferably oviposit their eggs on moist emergent or submerged parts of woody debris with a structured surface. The eggs are commonly deposited in cracks and crevices using the elongated ovipositor. Ovipositor morphology and various sensilla on the tip and along the ovipositor were studied by scanning electron microscopy and their possible function discussed. Structure of these sensilla and pre-oviposition behavior of the females point to a preference for certain oviposition sites on woody debris. This may be a key factor for the distribution and development of the larvae.

Morphological characteristics of sensilla on the female ovipositor of Lype phaeopa (Psychomyiidae; Trichoptera)

An important aspect of the association of Lype phaeopa (Stephens) with submerged wood is the oviposition behavior of adult females, which preferably oviposit their eggs on moist emergent or submerged parts of woody debris with a structured surface. The eggs are commonly deposited in cracks and crevices using the elongated ovipositor. Ovipositor morphology and various sensilla on the tip and along the ovipositor were studied by scanning electron microscopy and their possible function discussed. Structure of these sensilla and pre-oviposition behavior of the females point to a preference for certain oviposition sites on woody debris. This may be a key factor for the distribution and development of the larvae.

Specialist weevil, Rhyssomatus lineaticollis, does not spatially avoid cardenolide defenses of common milkweed by ovipositing into pith tissue

Rhyssomatus lineaticollis is a milkweed specialist whose larvae feed upon pith parenchyma in ramet stems of the common milkweed, Asclepias syriaca. Compared with other specialist insect herbivores on milkweeds, this curculionid beetle is unusual in that it is cryptically colored and does not sequester cardenolides characteristic of milkweed chemical defense. Based upon optimal defense theory, we predicted that pith tissue would be low in defensive compounds and that oviposition into the pith would spatially avoid cardenolides. We rejected this hypothesis because we found that pith tissue has a relatively high cardenolide concentration compared to cortex, epidermis, and leaf tissues. Moreover, we found total plant cardenolide concentration was lower in plants that contained the beetle eggs. Cardenolide concentrations were different among tissues in intact stems without the pith herbivore compared to stems where it was present. Furthermore, the overall polarity of the cardenolides present varied among plant tissues and between plants with and without R. lineaticollis eggs. Although we found lower concentrations of cardenolide in piths where the eggs were present, the cardenolides present in the pith contained more nonpolar forms, indicating that the plant may be responding to herbivory by increasing toxic efficacy of cardenolide defenses while lowering the total concentration. We suggest that preoviposition behavior by female beetles, which includes feeding on new leaves of the plant, is a mechanism by which females manipulate plant chemistry and assess quantitative and qualitative changes in cardenolide chemistry in response to herbivory prior to oviposition.

New Pseudacteon (Diptera: Phoridae) from North America That Parasitizes the Native Fire Ant Solenopsis geminata (Hymenoptera: Formicidae)

A new species, Pseudacteon bifidus, is described from Travis County, TX. It differs from all other North American Pseudacteon species by the structure of the ovipositor in females and the shape of antennal flagellomere 1 in males. Females attack ants of the species Solenopsis geminata and have distinctive preoviposition behavior.

Egg size variation in European Satyrine butterflies (Nymphalidae, Satyrinae)

The interspecific relationships between egg size and female size, sexual size dimorphism, latitude, preoviposition and egg-laying behaviour, was investigated in European Satyrine butterflies by controlling for taxonomic relatedness and by simple cross-species comparisons. Egg size scales positively to female size, although the relationship is not significant (but nearly so) when taxonomic effects are controlled for. Egg size is correlated with latitude. When the effects of latitude are removed, the relationship between egg and female size becomes more evident. Sexual size dimorphism is negatively correlated with egg size, but the effect disappears when adult size is controlled for. Small egg size is related to long preoviposition. No relationship between egg laying mode and egg size appears. The results are interpreted as evidence for positive scaling of egg to female size, with superimposed effects of egg size radiation. The correlation of egg size with latitude suggests that temperature, or season length, is likely to have made an important contribution to egg size selection within this geographic area.

Egg size variation in European Satyrine butterflies (Nymphalidae, Satyrinae)

The interspecific relationships between egg size and female size, sexual size dimorphism, latitude, preoviposition and egg-laying behaviour, was investigated in European Satyrine butterflies by controlling for taxonomic relatedness and by simple cross-species comparisons. Egg size scales positively to female size, although the relationship is not significant (but nearly so) when taxonomic effects are controlled for. Egg size is correlated with latitude. When the effects of latitude are removed, the relationship between egg and female size becomes more evident. Sexual size dimorphism is negatively correlated with egg size, but the effect disappears when adult size is controlled for. Small egg size is related to long preoviposition. No relationship between egg laying mode and egg size appears. The results are interpreted as evidence for positive scaling of egg to female size, with superimposed effects of egg size radiation. The correlation of egg size with latitude suggests that temperature, or season length, is likely to have made an important contribution to egg size selection within this geographic area.

Probing and Oviposition-Related Activity of Summerform Pear Psylla (Homoptera: Psyllidae) on Host and Nonhost Substrates

Effects of host and nonhost substrates on probing and preoviposition activity were monitored for adult summerform pear psylla, Cacopsylla pyricola Foerster. Tendency to initiate probing activity during a 15-min observation period was similar on a susceptible pear (Pyrus communis L. ‘Bartlett’), a presumed nonsusceptible pear (P. calleryana Decne.), and apple, but was reduced on quince. Depriving pear psylla access to pear for 4–6 h or 14–16 h before the observation period increased the percentage of psylla that probed during the observation period; effects of host deprivation on tendency to probe were independent of substrate. Tendency to initiate probing on P. communis was greater on lower leaf surfaces than upper leaf surfaces, which may suggest that probing is initiated in response to cues received at the leaf surface. The percentage of pear psylla that probed during the observation period was not affected by age of P. communis foliage. Mean probe duration and mean percentage of the 15-min observation period spent probing were unaffected by substrate; both measures increased linearly with amount of time that pear psylla were deprived of pear before the observation period. Mean percentage of the observation period spent in contact with the leaf surface was higher for P. communis and P. calleryana than non-Pyrus species. Despite extensive probing activity on apple, very little preoviposition behavior was noted; similarly, age of P. communis foliage did not affect tendency to initiate probing behavior, but did affect preoviposition activity. These two results suggest that probing and preoviposition activities were released by different cues.

The endogenous regulation of mosquito reproductive behavior

Most female mosquitoes require a meal of blood that provides protein for egg maturation. For reproduction to occur, two behavioral sequences are essential. One is concerned with finding a host for the blood meal and the other in finding a site on which to lay the eggs that result. Stimuli from both hosts and oviposition sites initiate the reproductive behaviors of host-seeking and pre-oviposition, respectively, that are discussed in this review. After sensory receptors perceive these stimuli, the central nervous system must integrate the information and associate it with a biologically appropriate response. Host-seeking appears to be the default behavior, expressed whenever host stimuli are present. However, if the female is successful in locating a host and ingesting blood, subsequent host-seeking is inhibited when the meal distends the abdomen above a certain threshold. Host-seeking inhibition continues during egg development as a result of a humoral mechanism even after the blood volume has been reduced by digestion. At the time when eggs are maturing and host-seeking is inhibited, pre-oviposition behavior predominates if the central nervous system receives oviposition site stimuli. This behavior is also initiated by a humoral factor. Several physiological states, including insemination, age, and nutrition, can modulate both host-seeking and pre-oviposition behaviors.

Effects of male accessory gland substances on the pre-oviposition behaviour of Aedes aegypti mosquitoes

Secretions of the male accessory glands of Aedes aegypti (L.) induce gravid virgin females to engage in pre-oviposition behaviour. Normal mating, the implantation of whole glands, or the injection of male accessory gland homogenates, all induced pre-oviposition behaviour in gravid virgin females, but implants of testes did not. Injection of male accessory gland extracts from other mosquito species, including A. albopictus, A. sierrensis, A. taeniorhynchus and Anopheles nr. salbaii into gravid virgin A. aegypti females did not induce pre-oviposition, suggesting that the male components were species-specific. Male accessory gland substances retained their biological activity when stored at 4°C for 24 h or when maintained at −10°C for 2 weeks, but lost their activity after longer periods and were inactivated by heating.

Influence of the ovaries and fat body on the initiation and termination of pre-oviposition behavior in the mosquito, Aedes aegypti

Pre-oviposition behavior, or the attraction to oviposition-site stimuli by female Aedes aegypti mosquitoes, generally accompanies egg maturation. When ovariectomy occurred after blood ingestion, even as soon as 3 h afterwards, pre-oviposition behavior was still initiated at 3 days after the meal. Ovariectomized A. aegypti hosts engaged in pre-oviposition behavior when they were implanted with ovaries from Culex quinquefasciatus or A. taeniorhynchus and then fed blood, but ovaries of Anopheles nr. salbaii could not initiate this behavior. Fat body from gravid females induced pre-oviposition behavior when it was injected into non-gravid recipients, but not to the same extent as in a gravid mosquito. Pre-oviposition behavior was terminated after oviposition occurred, even if a denervated mature ovary implant was still present, suggesting that the behavior is terminated by a nervous signal.

Humoral control of pre-oviposition behaviour in the mosquito, Aedes aegypti

Pre-oviposition behaviour, the attraction of mosquitoes to oviposition-site stimuli, is induced by a haemolymph-borne substance. A large proportion of gravid mosquitoes was attracted to a solution of methyl propionate in a laboratory olfactometer, but non-gravid females were also attracted if they were first injected with haemolymph from gravid females. Ovariectomized blood-fed mosquitoes failed to respond, but the reimplantation of denervated ovaries or as few as six mature follicles still triggered pre-oviposition after a blood meal.

Color Stimuli and Oviposition Behavior of the Onion Fly, Delia antiqua (Meigen) (Diptera: Anthomyiidae)1

When presented with oviposition dishes containing a range of colored surrogate onion stems, Delia antiqua (Meigen) laid the most eggs around yellow stems. Response to yellow was elicited by hue and saturation, rather than brightness, and was reduced when either white or black was added to yellow. Differences in egg numbers on stimulatory and nonstimulatory colors reflected differences in preoviposition behaviors. Alighting on stems, stem walks, and probing with the ovipositor occurred more frequently on yellow than on blue or gray stems. The effect of yellow on post-alighting behaviors was independent of its effect on alighting. After alighting on a yellow stem, females performed three times more stem walks than on blue or gray stems and were twice as likely to probe with their ovipositors after a stem walk. Thus, color is one of the diverse variables influencing alighting and post-alighting preoviposition behavior of D. antiqua.