Oviposition site choice under conflicting risks demonstrates that aquatic predators drive terrestrial egg-laying

Laying eggs out of water was crucial to the transition to land and has evolved repeatedly in multiple animal phyla. However, testing hypotheses about this transition has been difficult because extant species only breed in one environment. The pantless treefrog, Dendropsophus ebraccatus, makes such tests possible because they lay both aquatic and arboreal eggs. Here, we test the oviposition site choices of D. ebraccatus under conflicting risks of arboreal egg desiccation and aquatic egg predation, thereby estimating the relative importance of each selective agent on reproduction. We also measured discrimination between habitats with and without predators and development of naturally laid aquatic and arboreal eggs. Aquatic embryos in nature developed faster than arboreal embryos, implying no cost to aquatic egg laying. In choice tests, D. ebraccatus avoided habitats with fish, showing that they can detect aquatic egg predators. Most importantly, D. ebraccatus laid most eggs in the water when faced with only desiccation risk, but switched to laying eggs arboreally when desiccation risk and aquatic predators were both present. This provides the first experimental evidence to our knowledge that aquatic predation risk influences non-aquatic oviposition and strongly supports the hypothesis that it was a driver of the evolution of terrestrial reproduction.     

Quantitative genetics of oviposition behaviour and interactions among oviposition traits in the sand cricket

We performed a quantitative genetic study of oviposition behaviours and oviposition traits in the sand cricket Gryllus firmus. Egg survival in crickets depends on the depth at which they are inserted into the soil with the ovipositor. We examined whether egg depth depends on ovipositor length alone, or on both morphological and behavioural traits associated with oviposition. Heritability estimates were high (h² >0.5) for ovipositor length and small (h²=0.2) for oviposition behaviours. Negative genetic correlations between ovipositor length and some behavioural traits (digging depth and the behavioural component of egg depth) indicated compensation between oviposition traits on egg depth. Because of behavioural compensation, females with different ovipositor lengths subject to stabilizing selection on egg depth could have equal fitnesses. Females laid their eggs deeper, and their eggs were marginally more evenly distributed in dry than in wet sand. This suggests adaptive phenotypic plasticity in laying behaviour, but may also result from physical constraints of the substrate on the insertion of the ovipositor. The absence of significant between-family variation in oviposition traits in response to sand moisture indicates low evolutionary potential for phenotypic plasticity in oviposition traits according to soil moisture. In highly unpredictable environments, females could spread the risk of desiccation by laying eggs at different depths independently of environmental conditions (bet hedging). Our results show significant additive genetic influences on the ability of a female to spread risks as measured by genetic variation in egg distribution, suggesting that a bet-hedging strategy of egg laying has the potential to evolve in this population. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Embryonic Development and Rates of Metabolic Activity in Early and Late Hatching Eggs of the Major Malaria Vector Anopheles gambiae

Anopheles gambiae eggs generally hatch at the completion of embryo development; two-three days post oviposition. However, staggered or delayed hatching has been observed whereby a single batch of eggs shows marked variation in time-to-hatch, with some eggs hatching 18 days post oviposition or later. The mechanism enabling delayed hatch has not been clearly elucidated but is likely mediated by environmental and genetic factors that either induce diapause or slow embryo development. This study aimed to compare metabolic activity and embryonic development between eggs collected from sub-colonies of the baseline Anopheles gambiae GAH colony previously selected for early or late time-to-hatch. Egg batches from early and late hatch sub-colonies as well as from the baseline colony were monitored for hatching. For both time-to-hatch selected sub-colonies and the baseline colony the majority of eggs hatched on day two post oviposition. Nevertheless, eggs produced by the late hatch sub-colony showed a significantly longer mean time to hatch than those produced by the early hatch sub-colony. The overall proportions that hatched were similar for all egg batches. CO₂ output between eggs from early and late hatch sub-colonies showed significant differences only at 3 and 7 days post oviposition where eggs from the early hatch and the late hatch sub-colony were more metabolically active, respectively. No qualitative differences were observed in embryo development between the sub-colonies. It is concluded that all viable embryos develop to maturity at the same rate and that a small proportion then enter a state of diapause enabling them to hatch later. As it has previously been shown that it is possible to at least partially select for late hatch, this characteristic is likely to involve genetic as well as environmental factors. Delayed hatching in An. gambiae is likely an adaptation to maximise reproductive output despite the increased risk of desiccation in an unstable aquatic environment.     

Oviposition preferences of a threatened butterfly Leptidea morsei (Lepidoptera: Pieridae) at the western border of its range

The oviposition preferences of Leptidea morsei at the western border of its range (SE Slovenia) were studied with the aim of integrating this information into species habitat management recommendations. The characteristics of egg-laying habitat were examined at the landscape, patch, plant and leaf levels. Because sightings of adults in the field were infrequent, intensive searching for previously laid eggs on Lathyrus niger plants was chosen as the survey method. The main oviposition habitats of L. morsei in Slovenia were found to be the forest edges and light stands of thermophilous oak, oak-hornbeam and mesic beech forests (landscape level). The egg-laying sites were L. niger plants growing individually or in small stands, and oriented mostly towards W, SW, and S. The oviposition plants were between 33 and 120 cm high, with those growing in half to full shade preferred. Eggs were deposited singly, mainly on the underside of leaflets of terminal leaves, located mostly on the top quarter of plants irrespective of their height and growth form. The most important factors affecting egg-placement are sun exposure and the size of L. niger stands at ovipositing sites (patch level), leaf exposure on the plant in vertical and horizontal directions (plant level), leaf age and the leaf parts where the risk of leaf and egg desiccation is lower (leaf level). Management strategies for the main egg-laying habitats of the species are proposed.     

Relative predation risk and risk of desiccation co-determine oviposition preferences in Cope’s gray treefrog, <Emphasis Type="Italic">Hyla chrysoscelis</Emphasis>

Habitat permanence and threat of predation are primary drivers of community assembly and composition in lentic freshwater systems. Pond-breeding amphibians select oviposition sites to maximize fitness and minimize risks of predation and desiccation of their offspring, typically facing a trade-off between the two as predation risk often increases as desiccation risk decreases. To experimentally determine if Hyla chrysoscelis partition oviposition along gradients of relative desiccation risk and predation risk, we tested oviposition site preference in a natural population of treefrogs colonizing experimental ponds that varied in water depth and contained predatory larvae of two Ambystoma salamander species. Hyla chrysoscelis selected habitats with both lower predation risk, avoiding A. talpoideum over A. maculatum, and lower desiccation risk, selecting ponds with three times greater depth. We demonstrate that adult oviposition site choices simultaneously minimize relative predation risk and desiccation risk and that closely related salamander species produce functionally different responses among colonizing animals.     

Oviposition pattern of several Drosophila species under various light environments

The oviposition pattern over two continuous days under constant light (LL) and light-and-dark (LD) conditions was studied by means of a special apparatus; four Drosophila species (D. lutescens, D. melanogaster, D. hydei, and D. virilis) were used. The results showed that: (1) Under the LL condition, the oviposition pattern was characteristic for each species. The number of eggs laid by D. lutescens was smaller than that laid by the other species, and the oviposition pattern of this species was rhythmical. Females of D. melanogaster laid eggs continuously, but at a low rate. In contrast, D. hydei and D. virilis laid eggs in clusters, the total numbers of eggs being larger than those of D. lutescens and D. melanogaster. (2) Females of three species (D. lutescens, D. melanogaster, and D. virilis) laid more eggs in the light phase than in the dark phase under the LD condition. However, no consistent trend was obtained with D. hydei, suggesting that the oviposition pattern of this species is indifferent to the light condition (i.e., it is independent of it). (3) No effects of pre-experimental light condition on the oviposition were found for any of the species. The light-dependency of the oviposition pattern is discussed from the viewpoint of adaptation.     

Desiccation of Pinus foliage induced by conifer sawfly oviposition: effect on egg viability

Abstract 1. Desiccation of needles following oviposition by Neodiprion lecontei in Pinus resinosa caused high egg mortality. Eight-five per cent of pine needles into which sawflies oviposited subsequently desiccated, compared with 2.5% of needles without eggs. No larval emergence occurred from desiccated needles.
2. Within affected shoots, the probability of desiccation increased with the extent of oviposition. In paired comparisons of needles, 41.2% of needle length was occupied by eggs in desiccated needles, compared with 24.0% of needles without desiccation.
3. Both density-dependent and density-independent factors may contribute to desiccation of egg-laden needles. The likelihood that needle vasculature will be severed by ovipositing females probably increases with population density. Drought, which was high during the observations, probably increases the incidence of needle desiccation following mechanical injury caused by oviposition.     

A quantified ethogram for oviposition behavior and oviposition preference in the hemipterophagous butterfly Spalgis epius (Westwood) (Lepidoptera: Lycaenidae)

In this study, we examined the oviposition behavior and preference of Spalgis epius, a potential predator of mealybug crop pests. An ethogram of oviposition behavior was constructed based on observations made in an oviposition cage. Ovipositional behavioral acts were catalogued and separated into two behavioral repertoires: searching and egg laying. Gravid females of S. epius oviposited similar numbers of eggs on three mealybug species. Females preferred eggs and adults to nymphs of mealybugs for oviposition. Among three species of mealybugs attended by ants, females laid fewer eggs in the mealybug mass attended by Oecophylla smaragdina than on mealybugs attended by Tapinoma melanocephalum and Camponotus variegatus. Females preferred mealybug masses already containing conspecific eggs to mealybug masses containing conspecific larvae or Cryptolaemus montrouzieri larvae for egg deposition. Gravid females laid larger numbers of eggs under bright sunlight than in diffused sunlight or shade. The results of this study showed that S. epius can effectively attack any species of mealybugs, avoid intra- and interspecific competition, and co-exist with some species of ants attending mealybugs. With the knowledge of these behaviors, this predator can be effectively utilized as a major biological control agent of mealybugs.     

Host plant use for oviposition by Trigonotylus caelestialium (Hemiptera: Miridae) and Stenotus rubrovittatus (Hemiptera: Miridae)

The main hosts and sites of oviposition for the two bugs, Trigonotylus caelestialium (Kirkaldy) (Hemiptera: Miridae) and Stenotus rubrovittatus (Matsumura) (Hemiptera: Miridae), that cause pecky rice were investigated in 24 poaceous plants. Nymphs of T. caelestialium emerged from both spikelets and leaf sheaths, while nymphs of S. rubrovittatus emerged almost exclusively from spikelets. Suitable plants for oviposition by T. caelestialium are Lolium multiflorum, Digitaria violascens and Hordeum murinum, while Poa annua, Anthoxanthum odoratum, Alopecurus aequalis and D. violascens were preferentially used by S. rubrovittatus. There was a greater difference in the number of nymphs emerging from different plants for S. rubrovittatus than for T. caelestialium. This difference may be because T. caelestialium can oviposit on leaf sheaths if the spikelets are not suitable for oviposition, whereas S. rubrovittatus only oviposits on spikelets. Although both bugs oviposited on spikelets, the internal oviposition sites were different. In D. ciliaris, T. caelestialium laid all eggs between the lemma of the first floret and the second floret, whereas S. rubrovittatus laid eggs almost exclusively inside the second floret. In contrast, in P. annua, T. caelestialium laid all eggs inside the florets, whereas S. rubrovittatus laid eggs both between and inside the florets.     

A first step towards successful conservation: understanding local oviposition site selection of an imperiled butterfly, mardon skipper

Lack of basic biological information is a key limiting factor in conservation of at-risk butterflies. In the Puget prairies of Washington State little is known about the habitat requirements of mardon skipper (Polites mardon, federal candidate, WA endangered). We investigated oviposition site selection and used our results to assess oviposition habitat quality at a restored site with reintroduction potential. During the 2009 flight season we marked eighty-eight eggs and sampled vegetation at oviposition and random locations, measuring habitat variables with respect to the oviposition plant, vegetation structure, and vegetation cover. Eighty-six of the eighty-eight eggs were laid on Festuca roemeri, a native, perennial bunchgrass. Discriminant function analysis revealed selection of oviposition sites based on habitat structure; females laid eggs in small F. roemeri tufts in sparsely vegetated areas of the prairie. These results are contrary to results from a previous study in the Cascade Mountains of WA where females are generalists and selected densely vegetated areas, suggesting that the species has geographically specific habitat requirements. To assess oviposition habitat at a potential reintroduction site we measured the six variables most important for oviposition at the occupied site and a proposed reintroduction site. Results revealed differences in habitat quality between locations and suggest a need for further habitat management at the reintroduction site. Our results highlight the importance of understanding the local habitat use of a rare species where restoration activities occur and increase our ability to target habitat management where it is most needed for the persistence of the species.     

Role of kin recognition in oviposition preference and cannibalism by the predatory mite <Emphasis Type="Italic">Gynaeseius liturivorus</Emphasis>

Animals often select oviposition sites to minimize the predation risk for eggs and juveniles, which are more vulnerable to predation than adults. When females produce eggs in clusters, the eggs and juveniles are likely to suffer from cannibalism. Although cannibalism among siblings is known to be lower than among non-siblings, there have been few investigations into the possibility that females select oviposition sites that reduce the risk of cannibalism for the offspring. To test this possibility, we examined oviposition preference by adult females of the predatory mite Gynaeseius liturivorus in response to the presence of her own eggs and to eggs of other females, offering plastic discs as oviposition substrates. Although females did not clearly show a preference for plastic discs on which they had oviposited, they avoided plastic discs on which other females had oviposited. When eggs of other females were artificially placed on clean plastic discs, adult female mites avoided these discs, suggesting that the eggs were used as cues for oviposition preference. Cannibalism among juvenile siblings was lower than among non-siblings. These observations show that adult females and juveniles of G. liturivorus discriminate kin relationships among conspecific individuals. Therefore, oviposition preference by adult female G. liturivorus may lead to the reduced risk of cannibalism among offspring.     

Suitability of non-fertilized eggs of Homalodisca vitripennis for the egg parasitoid Gonatocerus morrilli

Gonatocerus morrilli (Howard) (Hymenoptera: Mymaridae) is an egg parasitoid used in California, USA to control glassy-winged sharpshooter (GWSS), Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). Virgin GWSS females deposit non-fertilized eggs and mated females can exhaust sperm reserves for egg fertilization. However, nothing is known about Gonatocerus spp. performance when using non-fertilized GWSS eggs as hosts. Host age preference for oviposition and suitability of non-fertilized GWSS eggs as hosts for G. morrilli reproduction were investigated to determine whether non-fertilized eggs on sentinel plants could be used to monitor egg parasitoid populations. Gonatocerus morrilli parasitized all ages of GWSS eggs (1–8 days old) regardless if the host egg was fertilized or not. In choice tests (fertilized versus non-fertilized eggs), parasitoids failed to emerge as adults from non-fertilized eggs more often than from fertilized eggs. The results indicate that non-fertilized eggs were accepted by G. morrilli as suitable hosts for oviposition, but were less suitable for immature development compared to fertilized eggs.     

Oviposition deterrence associated with larval frass of the Japanese pine sawyer,Monochamus alternatus (Coleoptera: Cerambycidae)

To determine the effect of larval frass of Monochamus alternatus on oviposition preference of the female adults, three tests were performed in the laboratory. Individual females were provided with a frass-coated, Pinus densiflora bolt and an untreated bolt simultaneously and were allowed to oviposit for 24 h. They deposited a significantly smaller number of eggs on frass-coated bolts. The females supplied with frass-coated bolts deposited no eggs on them, indicating that the larval frass deterred the females from oviposition. When individual females were provided simultaneously with a pine bolt applied with a methanol extract of larval frass and another bolt applied with methanol alone, they deposited a significantly smaller number of eggs on frass extract-applied bolts for 24 h. These results suggest the presence of a putative oviposition deterrent in larval frass of M. alternatus. Each test was replicated 19-20 times using different females.     

The power of the seasons: rainfall triggers parental care in poison frogs

The quality of breeding sites is of great importance for the reproductive success and accordingly the fitness of many animal species. Hence, individuals should decide carefully where to rear their offspring. Often parents have to account for multiple characteristics of habitat quality at once, which in turn might change over time. Specimens confronted with such variability may evolve the ability to display context-dependant decision plasticity. Anuran amphibians breeding in ephemeral pools largely face two risks for their offspring: desiccation and predation. The Neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. These small tadpole nurseries lower the risk of offspring predation. However, because most poison frog tadpoles are cannibalistic, even these pools need to be surveyed for predators, and parents tend to avoid deposition with conspecifics. We tested if this avoidance behaviour does change in parental R. variabilis depending on seasonal circumstances. Over several months we provided the frogs the option to deposit their eggs or tadpoles in pools that did and did not contain chemical cues of cannibalistic conspecifics, respectively. During the rainy season, frogs strongly avoided conspecific cues for both eggs and tadpoles. Anyway, with the change to the dry season, parental preferences changed such that parent frogs were more likely to deposit tadpoles (but not eggs) in pools containing cues of conspecific tadpoles. We suggest that R. variabilis, a species that typically isolates its cannibalistic offspring, has evolved a plastic feeding behaviour with regard to the risk of phytotelmata desiccation. We interpret that parents provide older tadpoles with younger ‘trophic’ tadpoles in order to accelerate their development and save them from impending desiccation.     

Oviposition site selection of the Alcon blue butterfly at the northern range margin

Female oviposition decisions in insects may strongly affect offspring growth and survival, and thus determine population performance. In this study, we examined oviposition site selection in the xerophilous ecotype of the endangered myrmecophilous butterfly Phengaris (=Maculinea) alcon (Lepidoptera, Lycaenidae) in Estonia, at the northern distribution margin of both the butterfly and its host plant, Gentiana cruciata L. Egg distribution on individual host plants appeared to be highly uneven: plants carrying high egg loads contrasted to a high proportion of host plants without any or with a few eggs. Host plant use for oviposition was strongly dependent on plant characteristics and environmental context. Host plant height relative to the surrounding vegetation rather than the absolute height of host plants was a key factor determining the use of particular host plant individuals for oviposition. In particular, plants protruding above surrounding vegetation had a higher probability of being used for oviposition, and carried more eggs. Additionally, the number of eggs laid on individual host plants was positively associated with the presence of flowers and the number of shoots. More aggregated host plants received fewer eggs than those with less conspecifics around. Feeding damage by wild herbivores, found in a substantial proportion of the butterfly’s host plants, strongly reduced the number of eggs on individual plants. Our results underline the need to assure that butterfly’s host plants do not become overgrown by surrounding vegetation. Best practices for opening vegetation around host plants may need further studies that explicitly account for butterfly’s host ants—their abundance in relation to vegetation height and their response to opening vegetation.     

Does the Polyphagous Egg Parasitoid <Emphasis Type="Italic">Trichogramma platneri</Emphasis> Nagarkatti (Hymenoptera: Trichogrammatidae) Display Behavioral Plasticity When Parasitizing Different Hosts?

Trichogramma platneri oviposition behavior on Amorbia cuneana egg masses was investigated under laboratory conditions. No relationship was detected between host surface area, number of edge turning on host eggs, and parasitoid clutch size. It was also observed that females parasitized the egg mass randomly by drilling into the egg mass and parasitizing individual eggs without using stereotypical behaviors to assess individual hosts (i.e. drumming and turning). However, clutch size did change due to ovipositional experience as naïve wasps with little or no ovipositional experience (<6 eggs parasitized), allocated significantly more progeny per host than wasps with longer ovipositional experience (24-h oviposition experience on a single egg mass). Moreover, naïve wasps parasitized significantly more eggs on the outer edge of the egg mass than experienced wasps. We contend that the physical characteristics of A. cuneana eggs and egg masses preclude T. platneri from completely discriminating between individual eggs. However, because T. platneri may be using kairomones from the egg mass, this described oviposition strategy remains effective.     

Temperature-dependent oviposition model of Scopula subpunctaria (Lepidoptera: Geometridae)

Scopula subpunctaria, is one of important defoliating insect pests of tea plants in China. However, the effect of temperature on its longevity and fecundity had not been reported, and the temperature-dependent oviposition model is lacking. The reproductive characteristics of S. subpunctaria were investigated under eight constant temperatures (13, 16, 19, 22, 25, 28, 31, and 33℃), with a 14L: 10D photoperid and 65–85% RH. The results showed that temperature significantly influence oviposition period, longevity, and fecundity of S. subpunctaria. The mean longevity of female adults increased from 10.8 days (33℃) to 33.9 days (13℃). Male lived shorter than female did. The mean longevity of males was shortest at 33℃ (8.1 days) and longest at 23.8℃ (17.6 days). Total fecundity of S. subpunctaria females ranged from 15.4 eggs at 33℃ to 279.9 eggs at 22℃. The temperature-dependent oviposition model of S. subpunctaria was constructed based on four sub-models (developmental rate model, total fecundity model, oviposition rate model, and survival rate model). The results of this study would be helpful in forecasting and predicting population occurrence of S. subpunctaria in tea plantations.     

Oviposition choice by the Onopordum capitulum weevil Larinus latus (Coleoptera: Curculionidae) and its effect on the survival of immature stages

Female Larinus latus lay eggs into the capitula of their Onopordum spp. host plants from the onset of capitulum development until the completion of flowering. This tight linkage between insect life-history and plant development optimised larval survival, apart from some initial asynchrony between the readiness of the females to oviposit and the suitability of the very small capitula to physically support eggs. Eggs were laid on bracts and stems of capitula or directly in the florets, when these became available. Both the location of the egg and time of oviposition influenced mortality factors such as egg and larval parasitism, egg desiccation and larval establishment. Overall, survival of eggs laid later in the season into florets was higher, although the adults that emerged were smaller. The change in choice of oviposition site that occurs at the onset of flowering, not only favours survival, but ensures more efficient resource use by the larvae. This occurs because sequential flowering of Onopordum spp. drives a sequential oviposition pattern and spreads the egg load more evenly over the available capitula, reversing a trend earlier in the season to clump eggs that were laid directly on the bracts. Other potential constraints, such as capitulum size, absolute egg density and previous egg-laying do not play a major role in determining the oviposition pattern of L. latus. Larval survival was positively correlated with capitulum size and not strongly influenced by egg density. Competition for resources only appeared to play a role in smaller capitula, and manifested itself in a reduction in the size of emerging adults rather than the death of immatures. In the absence of strong interspecific competition, the oviposition behavior of L. latus has become geared to maximising resource use for larvae (i.e. its own potential competitiveness) rather than minimising interactions with other members of the capitulum endophage guild.     

Oviposition behaviour of Phlebotomus argentipes - A laboratory-based study

The breeding habitat of sandflies is a little studied and poorly understood phenomenon. More importantly, oviposition behaviour is a largely neglected aspect of sandfly biology and this knowledge gap further undermines our understanding of the biology of sandflies. Pheromones released by the eggs play an important role in identifying good sites for oviposition by female insects. Several recent studies have examined the oviposition pheromone. The present study provides a preliminary report on the oviposition behaviour of Phlebotomus argentipes, the only vector of kala-azar (or visceral leishmaniasis) on the Indian sub-continent. Sandflies prefer to oviposit their eggs on surfaces that contain organic substances, especially substances with an odour of decaying animal products and the remains of conspecific eggs. The results presented here suggest that the odour released by the organic substances of old sandfly colony remains that contain dead flies, old unhatched eggs, larval food containing vertebrate faeces, frass and other organic matter serves as an attractant for the ovipositing females of P. argentipes and hence greatly increases the number of oviposited eggs compared to eggs deposited in controlled oviposition pots. This result will be helpful in maintaining an efficient colony of P. argentipes and may be a promising tool for monitoring and controlling the target insect as part of a synergistic approach.     

Egg Placement by Anopheles gambiae (Diptera:Culicidae) as Influenced by Resting Surface Slope and Enclosure

In these experiments, oviposition by laboratory-reared Anopheles gambiae s.s. was as likely to occur from a vertical perch, as from a horizontal sitting position on a substrate of moist mud or open water. Tall cylinders with moist, dark walls provided an enclosed vertical resting surface from which An. gambiae deposited eggs. Similar numbers of eggs were deposited in these cylinders as on dark and moist horizontally-positioned ovipositional substrates. Likewise, An. gambiae oviposited equally from a vertical perch among emergent surrogate reeds vs. sitting horizontally on mud. Open ovipositional resources with exposed resting surfaces presenting 45°, 90°, and 135° angles relative to the cage floor received fewer eggs than a horizontally positioned, moist and dark ovipositional dish, even though more An. gambiae females settled on these angled resting surfaces post-oviposition. We conclude that vertical resting sites are adequate perches from which oviposition can occur if they provide high humidity and the paramount dark and wet ovipositional cues for An. gambiae oviposition.