Assessment of patch quality by ladybirds: role of larval tracks

Gravid females of the two-spot ladybird, Adalia bipunctata (L.), were deterred from ovipositing when kept in petri dishes that had previously contained conspecific larvae but not conspecific adults, or the larvae of another two species of ladybird, Adalia decempunctata (L.) and Coccinella septempunctata L. The deterrent effect was density dependent and mediated via a chloroform-soluble contact pheromone present in the larval tracks. Similarly, gravid females of C. septempunctata were deterred from ovipositing by conspecific larval tracks and chloroform extracts of these tracks, but not by the tracks or extracts of tracks of A. bipunctata larvae. That is, in ladybirds the larvae produce a species-specific oviposition-deterring pheromone. In the field, the incidence of egg cannibalism in ladybirds increases very rapidly with the density of conspecific eggs or larvae per unit area. Thus, in responding to the species specific oviposition deterring pheromone female ladybirds reduce the risk of their eggs being eaten and spread their offspring more equally between patches. Received: 14 March 1997 / Accepted: 26 August 1997     

Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species

Abstract 1 Survival and development of hatchling larvae of three aphidophagous ladybirds (Coleoptera: Coccinellidae), Harmonia axyridis Pallas, Coccinella septempunctata brucki Mulsant and Adalia bipunctata Linnaeus, when fed their own and the other species eggs were recorded. 2 In all three species, the larvae survived when fed conspecific eggs. 3 The percentage of larvae of H. axyridis that survived decreased to 35% and 85% when fed eggs of A. bipunctata and C. s. brucki, respectively. All the larvae of A. bipunctata and C. s. brucki died after eating eggs of H. axyridis. None of the larvae of C. s. brucki died after eating eggs of A. bipunctata, whereas 46% of those of A. bipunctata died after eating eggs of C. s. brucki. 4 In general, larvae were reluctant to eat the eggs of other species. However, larvae of C. s. brucki showed less reluctance than H. axyridis to eat the eggs of A. bipunctata. 5 The consequence of this for invasive species of ladybird is discussed.     

The consequences of egg cannibalism inAdalia bipunctata [Coleoptera: Coccinellidae]

When eggs ofAdalia bipunctata L. are offered to larvae of their own species, these larvae are able to develop to adults. Reducing the daily egg supply results in decreased larval survival and pupal weight and especially fecundity of the adult females. The duration of larval development is significantly increased, the longevity of adults is shortened.     

Egg dumping by predatory insects

Synovigenic insects resorb oocytes when food is scarce and mature oocytes when food is plentiful. These two antagonistic processes allow an optimal allocation of resources to reproduction and somatic functions. Unlike hymenopteran parasitoids, ladybirds cannot resorb mature oocytes present in the oviducts. Is the energy contained in these oocytes lost or is there a mechanism for recovering it when needed? Females of two species of ladybird beetles Adalia bipunctata (L.) and Adalia decempunctata (L.) that are starved for >24 h lay single infertile eggs, which they immediately eat, and these eggs comprise the mature oocytes in the oviducts at the onset of starvation. This behaviour has some similarities to egg dumping reported in herbivorous insects and is part, in ladybird beetles, of a process to retrieve energy invested in reproduction. Such behaviour may exist in other predatory synovigenic insects species that do not invest in maternal care.     

Effects of food and temperature on development,fecundity and life‐table parameters of Adalia bipunctata (Coleoptera: Coccinellidae)

Development, reproduction and life tables of Adalia bipunctata (L.) were studied at three temperatures (19, 23 and 27°C) on a mixture of frozen pollen and Ephestia kuehniella Zeller eggs as a factitious food and on the aphids Myzus persicae (Sulzer) and Acyrthosiphon pisum (Harris) as natural foods. Development time of A. bipunctata on all tested diets decreased with increasing temperature. Mortality was lowest at 23°C, averaging 44.5%, 42.6% and 24.3% on factitious food, A. pisum and M. persicae respectively. The shortest developmental time from egg to adult at this temperature was observed on factitious food (18.55 days). However, the factitious food was inferior to the aphid diets in terms of reproduction, yielding the longest pre‐oviposition period, shortest oviposition period and lowest fecundity. The mean oviposition rate at 23°C varied from 19.94 to 25.03 eggs day^?1 on factitious food and M. persicae respectively. The intrinsic rate of increase (r_m) on different foods increased with increasing temperature and ranged from a minimum of 0.08 females/female/day on factitious food (19°C) to a maximum of 0.18 females/female/day on A. pisum (27°C). The results suggest that a mixture of E. kuehniella eggs and pollen fully support development of A. bipunctata larvae and can be used as an alternative to live aphids in the mass rearing of the pre‐imaginal stages of the predator. However, reproductive performance of a laboratory population may be better on aphids than on the factitious food.     

Attack strategy of ladybird beetles (Coccinellidae): factors shaping their numerical response

Summary Temporal changes in aphid abundance pose a considerable challenge to ovipositing aphidophagous ladybirds, as in order to maximize their fitness they need to synchronize their reproduction with the early development of aphid populations. Field census data and laboratory experiments were used to determine how ovipositing females of the two-spot ladybird, Adalia bipunctata (L.), assess whether an aphid population is suitable for exploitation. In the field, two-spot ladybirds usually laid eggs well before aphid populations peaked in abundance. In the laboratory they showed a marked reduction in their reproductive numerical response in the presence of larvae of their own species but not of other aphidophagous ladybirds. At the highest aphid density this was not a consequence of competition for food between larvae and ovipositing females. In the presence of conspecific larvae gravid females were very active and as a consequence more likely to leave an area, and when confined with other conspecific females or larvae laid fewer eggs and later than females kept on their own. The extent of the inhibition of egg laying is negatively correlated with the rate of encounter with larvae. Thus it is proposed that gravid females appear mainly to use the presence of conspecific larvae to assess the potential of an aphid colony for supporting the development of their offspring.     

Why do ladybirds (Coleoptera: Coccinellidae) cannibalize?

Cannibalism of eggs by larvae ofAdalia bipunctata, an aphidophagous species of ladybirds, is important for survival when aphids are scarce. Ladybirds survive longer by eating eggs of their own species rather than aphids. Since it costs less, in terms of larval growth, to eat eggs rather than aphids, cannibalism has a strong advantage under conditions of prey scarcity.     

Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues

The quality of different species of aphids as food for aphidiphagous ladybird beetles varies greatly. The optimal oviposition theory predicts that a female should lay eggs preferentially in patches of suitable prey and should be reluctant to oviposit in patches of less suitable prey. A no‐choice experiment was used to test whether aphids (Homoptera: Aphididae) of different suitability influence the oviposition behaviour of the two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). The results indicate that A. bipunctata females are not more reluctant to lay eggs in the presence of moderately suitable compared to highly suitable aphids. However, females laid fewer eggs in the presence of toxic aphids.     

Developmental stage of failed eggs in the red-legged partridge <Emphasis Type="Italic">Alectoris rufa</Emphasis>

Understanding whether egg failure occurs more frequently during laying or during incubation is important for determining the most vulnerable period of the egg phase in bird species with long laying and incubation periods. However, most studies compare nest failure during the egg stage and the hatchling stage. In this study we examined whether egg failure was higher during the laying period and early development than during the final stages of development in a population of red-legged partridge (Alectoris rufa) from northeast Spain. We collected 216 abandoned eggs in the field. Only 12% (n = 26) of the eggs were sufficiently intact to enable direct assessment of developmental stage, showing that 81% of 26 eggs were lost during early stages. The majority of eggs were depredated (n = 154, 71%), as evidenced by an opening hole. To take advantage of information contained in these eggs, we propose a simple method to assess their developmental stage by measuring the size of the opening of their hole. Based on this method, we estimated that the proportion of eggs lost during early stages ranged from 72 to 83%. We validated this result of a high percentage of egg failure during early developmental stages with a larger experimental sample. Nest losses in the partridge are higher during the laying period or early development. This result is important in that the direction of conservation efforts and their seasonal application should be adjusted to account for the most important factors affecting egg failure.     

A study on the energy source in the developing embryo of the mangrove horseshoe crab,Carcinoscorpius rotundicauda (Latreille)

The mangrove horseshoe crab, Carcinoscorpius rotundicauda, is an Asian species found in Malaysia. This ancient arthropod has a long incubational period during which it depends on various energy sources for both embryogenesis and organogenesis. This study describes the trend of energy utilization from the endogenous reserves by the developing embryos from 0 to 40 days of incubation (until the hatching of the larvae). The dry weight, insoluble protein, carbohydrate, glycogen and lipid showed a declining trend from 0 to 40 days of incubation, whereas the wet weight, water content, ash content and soluble protein showed an increasing trend. Selected micro-elements such as Cu²⁺, Fe²⁺ and Zn²⁺ also demonstrated an interesting trend in the developing eggs when the egg mass was subjected to inductively coupled plasma mass spectrometry analysis, where these elements showed a high correlation with the moulting stages and egg development. Maximum variations within the micro-elements were observed during the 1st (10 days after fertilization) and 2nd (35–36 days after fertilization) moulting stages within the developing eggs. This study clearly indicated that the moulting cycles of C. rotundicauda during embryonic development influence energy utilization in the form of carbohydrates, lipids, proteins, glycogen and other micro-elements.     

Egg cannibalism by ladybird larvae is less frequent than expected from the nutritional benefit accrued to cannibals

Egg cannibalism is a widespread phenomenon in predatory arthropods. However, conflicting results have been reported regarding the nutritional value of conspecific eggs. Therefore, evaluation of the value of a mixed diet of conspecific eggs and aphids for survival and growth of Adalia bipunctata (Coccinellidae) larvae was tested. Subsequently, the propensity for cannibalism of naive and experienced larvae was assessed in two experiments in which the relative density and quality of conspecific eggs were manipulated in an experimental arena. It was found that larvae that were fed a mixed diet of conspecific eggs and aphids moulted into larger adults than those fed either aphids or eggs, and those that fed on conspecific eggs lost less mass than those fed only aphids during pupal stage. Additionally, in an experimental arena, attacks on aphids were more frequent than expected when conspecific eggs occupied 50% and 75% of the patches. When 50% of patches were occupied by conspecific eggs, the preference for aphids was less marked when larvae had previously experienced cannibalism (76% vs. 52% respectively) or when offered in the arena conspecific egg the cuticular hydrocarbons of which had been removed (76% vs. 48%, respectively). However, cannibalism was not enhanced if larvae experienced heterospecific prey shortages, but were supplemented with an artificial diet. Given that prey choice in A. bipunctata larvae is driven by chemical cues and that hydrocarbons on the egg surfaces and in larval tracks are very similar, we hypothesize that the naive larvae avoid eggs because of the uncertainty that those hydrocarbons indicate either eggs or conspecific larvae.     

Laboratory study of cannibalism and interspecific predation in ladybirds

Abstract.

• 1 In the absence of aphids, adult females of Adalia bipunctata (L.) showed a greater reluctance to eat eggs than males.
• 2 Eggs and young larvae were more vulnerable to cannibalism than older larvae and starved larvae were more vulnerable than well-fed larvae.
• 3 Both egg and larval cannibalism is inversely related to the abundance of aphids.
• 4 Eggs are a better food, in terms of larval growth and survival, than aphids.
• 5 In the absence of aphids interspecific predation occurred, but not equally, between the coccinellids A.bipunctata, A.decempunctata (L.), Coccinella septempunctata L. and C.undecempunctata L.
• 6 Larvae and adults of A. bipunctata and C.septempunctata were reluctant to eat conspecific eggs painted with a water extract of the other species' eggs and larvae of C. septempunctata were more likely to die after eating a few eggs of A.bipunctata than vice versa.
• 7 These results indicate that cannibalism occurs mainly when aphid prey is scarce and is adaptive in that it improves the chances of survival, and coccinellids, to varying degrees, are defended against interspecific predation.

     

Eat or be eaten: prevalence and impact of egg cannibalism on two-spot ladybirds, Adalia bipunctata

Ladybirds commonly engage in cannibalistic behaviour. Egg cannibalism by first instars is considered advantageous to the cannibal, because it not only results in direct metabolic gain but also a reduction in potential competitors. In this study, we quantified the effect of cannibalism on the development rate and survival of Adalia bipunctata (L.) (Coleoptera: Coccinellidae) larvae through development to the adult stage. We also assessed the synchrony of egg‐hatching in relation to laying order and compared the proportion of eggs cannibalized in egg batches laid as clusters or linearly. Larvae that had consumed a conspecific egg after hatching reached the adult stage 1.65 days earlier than those larvae that had not. Larval and pupal mortality was lower for cannibals compared to non‐cannibals; only 46% of non‐cannibalistic individuals reached the adult stage whereas 81% of cannibals pupated successfully. Egg cannibalism is undoubtedly advantageous to A. bipunctata larvae both in terms of faster development and increased survival. There is a positive correlation between laying and hatching order for eggs laid linearly or in a cluster. There was no significant difference in the proportion of eggs hatching in clusters or in a line (80 and 77%, respectively). The remaining eggs were either cannibalized or did not hatch. The ecological implications of these results are discussed with particular reference to trophic egg plasticity.     

Placental transfer of nutrients during gestation in the viviparous lizard, Pseudemoia spenceri

Energy, ionic, protein and lipid contents and fatty acid profiles for the major lipid classes of freshly ovulated eggs and neonates of the viviparous lizard, Pseudemoia spenceri, were measured. Litter size is 1.7 ± 0.1, with larger females producing larger neonates. Placentotrophy results in approximately 23% more dry matter in the neonates than in the fresh egg. The increase in the quantity of protein and lipid during development is not significant and is reflected in the similarity of energy densities of eggs and neonates. As a percentage of dry matter, neonates have slightly lower proportions of lipid and protein than eggs because of significant uptake of ash, calcium, potassium and sodium, but not of magnesium, across the placenta. The amounts of triacylglycerol and phospholipid are not significantly different between the egg and the neonate, but neonates contain significantly more cholesterol and cholesteryl ester. The amounts of the major fatty acids, palmitic and oleic acids, recovered from the total lipids of the neonate do not differ significantly from the amounts present in the egg lipids, but the neonates contain significantly less linoleic and α-linolenic acids and more palmitoleic, stearic and arachidonic acids than the eggs. The amount of docosahexaenoic acid recovered from the lipids of the neonate is 2.6-times greater than the amount initially present in the egg. P. spenceri has a relatively larger egg and a smaller reliance on placentotrophy than other species in the same genus, all of which have a similar placental morphology. Nevertheless, the pattern of embryonic nutrition includes both obligative and facultative placentotrophy. All the major components of yolk of oviparous species are present in eggs of P. spenceri, but most are augmented during development by placental transfer. Accepted: 8 April 1999     

Lipid composition and utilization in developing eggs of two tropical marine caridean shrimps (Decapoda: Caridea: Alpheidae, Palaemonidae)

Changes in biomass and lipid biochemistry during egg development were studied in the tropical shrimps, Alpheus saxidomus and Palaemonetes schmitti, from Pacific Costa Rica. Freshly-laid eggs of P. schmitti were substantially smaller than those of A. saxidomus; dry mass decreased during embryogenesis in the former species but remained almost constant in the latter one. Water content of eggs close to hatching were similar among both species (roughly 75%). Newly-produced eggs of the two species contained ≈20% fatty acids per egg dry mass; a comparison with data concerning decapods inhabiting tropical and temperate waters revealed that eggs produced by shrimps inhabiting tropical waters tend to have a higher lipid egg content per dry mass than those from temperate regions. Major lipid classes in the eggs of both species were phospholipids and triacylglycerols which increased and decreased during the incubation period, respectively. The predominant fatty acids of P. schmitti eggs were 16:0, 20:5(n-3) and 22:6(n-3) whereas eggs of A. saxidomus showed high amounts of 16:0, 20:5(n-3) and 16:1(n-7), and remarkably low values of 22:6(n-3) fatty acid. Lipid utilization was more pronounced in P. schmitti; in A. saxidomus, eggs close to hatching still contained 70% of the initially deposited fatty acid content which may indicate an enhanced independence of the newly-hatched larvae on external energy resources. The observed differences may partially be related to different habitat preferences, however, the role of adaptation and phylogeny as determinants of egg lipid biochemistry in caridean shrimps remains to be clarified.     

Ladybirds as a model system for the study of male-killing symbionts

Maternally inherited bacteria that kill male but not female hosts during embryogenesis occur in a number of aphidophagous coccinellids. Work on EnglishAdalia bipunctata (L.), has shown the causative agent of male-killing to be a member of the bacterial genusRickettsia. In coccinellids, the primary advantage of male-killing behaviour to the bacterium has been identified. Following male death, resource reallocation occurs through sibling egg cannibalism: female neonate larvae of infected mothers gain a significant survival advantage by eating the soma of their dead male siblings. In addition, daughters of infected females suffer a reduced risk of cannibalism as a result of the lower egg hatch rate in infected clutches. Predictions as to which species of coccinellid are liable to harbour male-killers may be made on the basis of the selective advantages of male-killing identified inA. bipunctata. Species which may harbour male-killers are likely to lay eggs in clutches, show sibling egg cannibalism, and exhibit high neonate mortality. Recent work has shown male-killing to occur in a number of other aphidophagous coccinellids with the predicted characteristics. Molecular genetic analysis has putatively identified three bacterial symbionts associated with male-killing, coming from three phylogenetically distant bacterial taxa. We therefore suggest that within coccinellids that possess these features, male-killing may evolve in a taxonomically diverse range of inherited bacteria. The implications of the presence of male-killing bacteria on the population demography of host coccinellids, and on host mitochondrial DNA variability are discussed. The aphidophagous coccinellids are proposed as a model system for studying the evolution and consequences of infection with male-killers.     

Overwintering, phenology and fecundity of Harmonia axyridis in comparison with native coccinellid species in Italy

Classical biological control is generallyunderstood as an environmentally safe practiceof insect pest management. However, questionshave been raised about possible negativeeffects for native species. As part of a riskassessment study a semi-field trial was carriedout in northern Italy in order to compare theoverwintering of the native species Propylea quatuordecimpunctata (L.) and Adalia bipunctata (L.) (Coleoptera:Coccinellidae) with the exotic Harmoniaaxyridis (Pallas) (Coleoptera: Coccinellidae).All the experiments were carried out from April1998 to April 2001. Harmonia axyridis wasable to overwinter successfully in northernItaly. Fecundity, oviposition rate, longevityand rate of increase of overwintering femaleswere calculated and the phenology of the threespecies was studied. Harmonia axyridisoverwintering mortality (31.9%) was lower incomparison with mortality of native species(68.9% for P. quatuordecimpunctata and61.3% for A. bipunctata). As aconsequence, post-overwintering rate ofincrease of the exotic species was higher.Longevity of overwintered females was similaramong the species. Mean fecundity of H. axyridis (783.8 eggs per female) was slightlyhigher than A. bipunctata (720.2 eggs perfemale), and much higher than P. quatuordecimpunctata (193.7 eggs per female). H. axyridis and A. bipunctatacompleted four generations and P. quatuordecimpunctata three generations in a year. The results show that H. axyridisappears to posses a high potential for establishment in Italy.     

Calculating egg volume when shape differs: when are equations appropriate?

ABSTRACT Egg volume is often calculated from length and breadth, assuming little variation in egg shape within species. However, egg shape may vary among females, over time, or within clutches. If this variation is not predictable, volume should be estimated using another method. For example, in some species, egg shape changes consistently with laying order and volume can be estimated using laying‐order specific equations. We measured the length, breadth, volume, and mass of 249 Magellanic Penguin (Spheniscus magellanicus) eggs and regressed volume on length and breadth for first and second eggs separately. Differences between measured and calculated volume averaged <1% for both eggs. Using linear measurements, we calculated egg volume for 7085 clutches from 1983 to 2006. First and second eggs had similar calculated volumes (P > 0.05) in 19 of 24 yr; when they differed, the second egg was larger. In contrast, using single equations typically employed to compute egg volume, we erroneously concluded that first eggs were usually (20 of 24 yr) significantly larger than second eggs. Our regression equations should be applicable to other Spheniscus penguins because ratios of elongation coefficients (length divided by breadth) of first and second eggs are similar among these species. In other species of birds where egg shape changes with laying order, the volume of a sample of eggs should be measured to develop regression equations specific to the species and laying order. Slight variation in egg volume can have important evolutionary and ecological implications that would be erroneously interpreted without field tests to measure volume.     

The effects of age and weather on egg laying inDanaus plexippus L. (Lepidoptera: Danaidae)

The effects of age and weather conditions on egg laying in D. plexippus were determined for caged females. Age (measured in physiological time), temperature and solar radiation influence egg laying in this species of butterfly. An algorithm taking these factors into account in presented and accounts for 88% of the daily variation in egg laying. Caged D. plexippus begin to lay eggs six—seven days after emergence, peak egg production (about 60 eggs/♀) occurs about 15 days later. Females continue to lay eggs throughout their adult life, which in a flight cage was about 40 days. This egg laying pattern is compared with other published fecundity schedules. The effect and importance of a female being prevented from laying her eggs, on her life-time egg production, is also discussed.     

Intraspecific and Interspecific Variation of the Mitochondrial Gene of Cytochrome Oxidase I in Ladybirds (Coleoptera: Coccinellidae)

Intergeneric, interspecific, and intraspecific genetic variation of the 310-bp 3-end region of the mitochondrial gene of cytochrome oxidase I (COI) has been assessed in ladybirds (Coleoptera: Coccinnellidae). The phylogenetic distances between eight species of ladybirds have been determined. Mitochondrial DNA (mtDNA) nucleotide sequences have been compared in Adalia bipunctata L. differing in the elytron and pronotum colors that have been sampled from several geographically remote populations. The taxonomic statuses of two morphs from the genus Adalia, A. bipunctata bipunctata and A. bipunctata fasciatopunctata, have been identified.