The influence of larval density, food stress, and parasitism on the bionomics of the dengue vector Aedes aegypti (Diptera: Culicidae): implications for integrated vector management

New larval control strategies for integrated vector management of Aedes aegypti are in high demand, including the use of biological control agents. Exposure of Aedes aegypti to parasites, starvation, and overcrowded conditions during larval development reduces the probability of survival to eclosion, can directly affect fitness parameters such as adult size and fecundity, and can affect the size, provisioning, and viability of eggs produced by females. We compared these parameters after exposing larvae to 1) abundant food at low larval densities, 2) food deprivation and high larval density, and 2) infection with the endoparasite Plagiorchis elegans, an entomopathogenic digenean trematode. Female mosquitoes that eclosed from larval conditions of starvation and overcrowding were smaller and laid fewer and smaller eggs than controls. The proportion of females to complete an oviposition cycle was reduced in the P. elegans-infected treatment group. Parasite load was negatively correlated with wing length and egg size. Infection of Ae. aegypti with P. elegans has sublethal effects and may reduce population-level reproductive output, but one-time low-density P. elegans exposure does not have sufficient effect on Ae. aegypti fitness parameters to be considered a viable biocontrol option.     

Life-history responses of larviparous Boettcherisca formosensis (Diptera: Sarcophagidae) to larval competition for food, including comparisons with oviparous Hemipyrellia ligurriens (Calliphoridae)

Abstract. 1 The effect of larval rearing density on life-history parameters of Boettcherisca formosensis Kirner & Lopes (Sarcophagidae) was investigated. Increases in rearing density resulted in lowered larval survivorship, shortened larval development time and production of smaller, shorter-lived adults with reduced fecundity.
2. B. formosensis is larviparous. Average brood size was 17.5±1.0 (mean±M) larvae, which was much less than the average number of mature larvae inside gravid females. Females apparently produced a series of small broods, distributing their offspring over a number of carcasses.
3. Compared with the oviparous species Hemipyrellia ligurriens (Wiedemann) (Calliphoridae), B. formosensis adults were larger and longer-lived, with a longer larval development time but shorter larval feeding period. However, females had a shorter pre-reproductive period, were less fecund, and had a lower life time reproductive investment.
4. B. formosensis had lower relative performance (measured by the composite index of performance, r') than H. ligurriens over the larval rearing density range, and was more sensitive to increases in density. Although the r' values suggest that the sarcophagid may be a competitively inferior species, other features which are not included in the index (such as larvipary, short larval feeding period and spreading of offspring from a single brood among carcasses) may be of significant adaptive value to B. formosensis.     

Effect of Population Density and Female Body Size on Number and Size of Offspring in a Species with Size‐Dependent Contests over Resources

When size‐dependent contests over resources influence reproductive success, the trade‐off between number and size of offspring depends on the frequency of contests. Under these circumstances, clutch size should decrease and offspring size should increase as contests become more frequent. We tested these predictions with the burying beetle Nicrophorus pustulatus through manipulation of rearing densities. Burying beetles reproduce on small vertebrate carcasses, a rare but high quality food source for the larvae. Large beetles are more likely to win contests over carcasses and gain exclusive access to a carcass. The winner of a contest kills eggs and larvae already present on a carcass. As a result of the rarity of carcasses, burying beetles are unlikely to breed more than once. As predicted, brood size of N. pustulatus decreased with increasing rearing density. Despite a negative correlation between brood size and larval mass, larval mass did not increase with increasing rearing density. This may be due to the special biology of N. pustulatus which can use snake eggs for reproduction. Potentially larger supply of resources and generally small population densities of N. pustulatus may weaken selection on body size and thus the correlation between brood size and larval mass. As size‐dependent constraints can limit reproductive phenotypes, we examined whether female size influenced reproductive phenotype. Small females produced larger broods with smaller, but more variable, offspring than large females. Mechanical constraints of egg size seem an unlikely explanation for the differences because burying beetles can compensate for small egg size through parental care. Energetic constraints may impact small females because body mass and brood size of small females decreased with increasing density. Yet, at all density levels small females produced larger, not smaller, broods than large females. The larger and more variable broods of small females seem to be in agreement with a bet‐hedging strategy.     

Adaptive egg size plasticity for larval competition and its limits in the seed beetle Callosobruchus chinensis

Life‐history theory predicts that females who experienced stressful conditions, such as larval competition or malnutrition, should increase their investment in individual offspring to increase offspring fitness (the adaptive parental hypothesis). In contrast, it has been shown that when females were reared under stressful conditions, they become smaller, which consequently decreases egg size (the parental stress hypothesis). To test whether females adjust their egg volume depending on larval competition, independent of maternal body mass constraint, we used a pest species of stored adzuki beans, Callosobruchus chinensis (L.) (Coleoptera: Chrysomelidae: Bruchinae). The eggs of females reared with competitors were smaller than those of females reared alone, supporting the parental stress hypothesis; however, correcting for female body size, females reared with competitors produced larger eggs than those reared in the absence of competition, supporting the adaptive parental hypothesis, as predicted. The phenotypic plasticity in females' investment in each offspring in stressful environments counteracts the constraint of body size on egg size.     

Seasonal life cycle and autogeny in the mosquitoAedes togoi in northern Kyushu,Japan, with experimental analysis of the effects of temperature,photoperiod and food on life-history traits

We studied seasonal changes in the larval population structure, adult size, and autogeny (egg production without a bloodmeal) of the mosquitoAedes togoi on the seacoast of northern Kyushu, Japan. The effects of temperature, photoperiod and food conditions on larval development, adult size and autogeny were studied in the laboratory.Aedes togoi overwintered in both the egg and larval stages and was multivoltine. Adult size was greater in spring and autumn and smaller in summer. Autogeny occurred in spring and autumn but not in summer. Autogenous females were larger than anautogenous females, and larger autogenous females produced more eggs. Laboratory experiments showed that autogeny was promoted under low temperature and short-day conditions which corresponded with spring/autumn conditions in the field. Experimental food limitation in the larval stage greatly reduced adult size and autogenous egg production. In the field, large inter-pool variations in adult size and autogeny rate probably resulted from variations in nutrient and crowding conditions. Seasonal autogeny ofAedes togoi was discussed in terms of life-history strategy under fluctuating environmental conditions where relative advantages of autogenous and anautogenous reproduction alternate seasonally.     

Invasive mosquitoes, larval competition, and indirect effects on the vector competence of native mosquito species (Diptera: Culicidae)

Invasive arthropods that vector pathogens have the potential to influence pathogen transmission both directly, by becoming a novel pathogen vector, or indirectly, by interacting with native vectors. Adult mosquito size is influenced by food availability in the larval stage, and smaller, nutrient-deprived mosquitoes are, in some studies, more efficient viral vectors in the laboratory. This is the first study to examine the indirect impacts that larval competition between Aedes albopictus, an introduced mosquito species, and Ochlerotatus triseriatus, a native mosquito species and the primary vector for La Crosse virus (LACV) in the US, has on native mosquito larval survival, adult size, and vector competence. A. albopictus presence decreased Oc. triseriatus larval survival, but surviving Oc. triseriatus females were larger, potentially owing to a release from intraspecific competition. These larger, native females were more likely to develop both midgut and disseminated LACV infections than females emerging from monospecific treatments. Collectively, these results suggest a need to better understand the ecology of both native and invasive vector species, their interactions, and the potential for those interactions to alter vector-borne disease transmission.     

Consequences of larval intraspecific competition to stonefly growth and fecundity

Summary We conducted experiments in replicated circular streams to measure the effect of intraspecific larval density on growth rates, size at emergence, timing of emergence, and fecundity of two species of predatory stoneflies (Megarcys signata and Kogotus modestus, Perlodidae). Early instars of both species showed no significant effect of intraspecific larval density on mean growth rates, despite the observation that in the absence of competitors stoneflies ate on average, significantly more prey (Baetis bicaudatus, Ephemeroptera, Baetidae) than in the presence of competitors. However, larval size of stoneflies held at higher densities (two per chamber) diverged over time, resulting in a greater size variability (coefficient of variation) among Kogotus than in treatments with low densities of stoneflies (one per chamber). The effect of doubling the density of early-instar Megarcys larvae was also asymmetrical, resulting in one larger and one smaller individual. In contrast, doubling the density of last-instar stoneflies whose feeding rates declined significantly prior to emergence had few measurable consequences, except that male Megarcys, which continued to feed throughout the last instar, had lower average feeding rates in high-density than in low-density chambers, and emerged at a significantly smaller mean size. We conclude that competition between early-instar stonefly larvae results in an asymmetry of body sizes, but that competitive effects are reduced as larvae slow or cease feeding before emergence. Since larger females of both stonefly species produced more eggs, the probable cost to females of early-instar larval competition was a reduction in their potential contribution of offspring to the next generation. The cost of attaining a smaller body size for male stoneflies is unknown; but if, as in many other insects, larger males have greater reproductive success, larval competition may increase the opportunity for sexual selection among males. This hypothesis remains to be tested experimentally.     

Enzymatic analysis of uricotelic protein catabolism in the mosquito Aedes aegypti

Excess protein ingested by blood meals of mosquitoes is catabolized by a uricotelic pathway. We have established enzyme activity profiles for xanthine dehydrogenase (XDH), the enzyme that catalyzes uric acid synthesis, and related it to intestinal proteolytic activities in female Aedes aegypti mosquitoes.During the first day after eclosion the meconium containing urate and urea of larval/pupal origin is discharged, together with XDH activity. Females of constant body size and of defined age were given measured blood meals by enema. XDH activity and uric acid synthesis correlate with the size of the blood meals. Upon completion of protein digestion and catabolism, XDH is excreted in an active form and its activity returns to the residual level. Maximal XDH activity always precedes intestinal proteolytic activities by a few hours. Regulation of XDH activity appears to be purely metabolic, independent of endocrine factors.Small females fed identical volumes of blood produce fewer eggs than their larger sisters and consequently catabolize a higher proportion of blood protein to uric acid.Old females are less fecund and show smaller investments of protein into yolk than younger ones. Despite reduced XDH activities, they excrete equal amounts of urate as young females. Obviously in young females XDH activity is in excess of biochemical requirements.     

Harem size and oviposition behaviour in a polygynous bark beetle

Abstract. 1. Harem polygyny can have fitness benefits and costs on females. In bark beetles of the genus Ips the latter may include within‐harem competition between larvae. However, earlier competition between females for male care and mating opportunities may also influence oviposition behaviour. There has been relatively little investigation into the relationship between harem size and initial egg output. The present study investigated this relationship in the bark beetle Ips grandicollis. 2. The measure of egg output used was the number of eggs in the gallery with the most eggs in each harem. Mean (±SE) harem size of 242 observed harems was 3.25 ± 0.10. A curvilinear relationship was found between egg output and harem size, with females in smaller harems (one to four females) laying more eggs with increased harem size. However, females in larger harems (five to seven females) laid fewer eggs as harem size increased. The optimal harem size (in terms of number of eggs laid) was close to four females. 3. We found no evidence from a behavioural assay that females could preferentially choose unmated males over mated males with harems of two females. Additionally, the distribution of harem sizes suggests that females distribute themselves among males randomly. 4. The results suggest that harem size has effects on female reproduction that extend beyond larval competition and influence patterns of oviposition. The mechanism that determines why egg laying is greatest at intermediate levels is unknown. There is no evidence that smaller harems belong to lower quality males, but females may adjust egg‐laying behaviour in large harems as a result of reduced male attendance or anticipated larval competition.     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Comparative fecundity and associated factors for two sibling species of the Anopheles gambiaecomplex occurring sympatrically in The Gambia

Abstract. For two sibling species of mosquitoes belonging to the Anopheles gambiae complex of malaria vectors, the effects of body size (wing length) and bloodmeal size (haematin excretion) on fecundity of wild females were investigated in The Gambia, West Africa. Freshly blood-fed individuals from sympatric populations of An.arabiensis and An.gambiae sensu stricto were sampled by collection at 07.00–09.00 hours from within bednets during July/August 1993, at the beginning of the rainy season. The possible confounding effect of infection with Plasmodium parasites was removed by eliminating infected mosquitoes from the study samples. An.arabiensis females comprised 75% of the An.gambiae sensu law population and were significantly larger (greater mean wing length) than those of An.gambiae s.s. mosquitoes. Mean egg production per female (for the subsequent gonotrophic cycle, excluding pre-gravids) for the two species was not significantly different, though the relationship between wing length and egg production showed An.gambiae s.s. to be more fecund than the An.arabiensis of the same size. Pre-gravid An.gambiae s.s. had consumed significandy smaller bloodmeals than gravid females but the mean wing length of these two gonotrophic categories was not significantly different. In contrast, An.arabiensis pre-gravids were smaller and had consumed smaller bloodmeals than the gravids.     

Adaptive plasticity of egg size in response to competition in the cowpea weevil,Callosobruchus maculatus (Coleoptera: Bruchidae)

Life history theory predicts that larger propagules should be produced when the offspring are expected to experience intense competition. This study tested whether female cowpea weevils responded to high larval or adult density by producing larger eggs. In a splitbrood design I measured the effect of density experienced by females at their larval stage (1 vs. 4–6 larvae/cowpea) on the size of eggs produced just after emergence. The females were then kept either at low adult density (1 female+1 male per vial), or at high adult density (10 females+10 males) for 2 days, and tested for the effect of this adult density treatment on the size of eggs laid subsequently. I measured egg length and width, as well as the diameter of the entrance tunnel made by the larva, which can be regarded as a crude measure of larval size. Females that experienced high adult density subsequently laid slightly wider eggs than those kept at low density. This difference, albeit small (about 1–4% after correction for female weight and the effect of family, depending on the statistical model used), was statistically significant and robust to alterations of the statistical model. It may be a remnant of a larger plastic response of egg size to competition that has become eroded during many generations in high-density laboratory cultures. There was no difference in egg length or the diameter of the entrance tunnel. Eggs laid just after emergence by females reared at high larval density also tended to be wider than those produced by females that had no competitors. This effect was only marginally significant, however, and sensitive to the statistical model. Both egg length and width and the diameter of the entrance tunnel increased with female weight and decreased with female age. The tunnel diameter was positively correlated with both egg length and width, but the effect of width was larger.     

Local Competition Between Foraging Relatives: Growth and Survival of Bruchid Beetle Larvae

Kin selection theory states that when resources are limited and all else is equal, individuals will direct competition away from kin. However, when competition between relatives is completely local, as is the case in granivorous insects whose larval stages spend their lives within a single seed, this can reduce or even negate the kin-selected benefits. Instead, an increase in competition may have the same detrimental effects on individuals that forage with kin as those that forage with non-kin. In a factorial experiment we assessed the effects of relatedness and competition over food on the survival and on fitness-related traits of the bruchid beetle Callosobruchus maculatus. Relatedness of competitors did not affect the survival of larvae. Larval survival substantially decreased with increasing larval density, and we found evidence that beetles maturing at a larger size were more adversely affected by competition, resulting in lower survival rates. Furthermore, females showed a reduction in their growth rate with increasing larval density, emerging smaller after the same development time. Males increased their growth rate, emerging earlier but at a similar size when food was more limited. Our results add to the growing number of studies that fail to show a relationship between relatedness and a reduction in competition between relatives in closed systems, and emphasize the importance of the scale at which competition between relatives occurs.     

She’s a femme fatale: low-density larval development produces good disease vectors

Two hypotheses for how conditions for larval mosquitoes affect vectorial capacity make opposite predictions about the relationship of adult size and frequency of infection with vector-borne pathogens. Competition among larvae produces small adult females. The competition-susceptibility hypothesis postulates that small females are more susceptible to infection and predicts frequency of infection should decrease with size. The competition-longevity hypothesis postulates that small females have lower longevity and lower probability of becoming competent to transmit the pathogen and thus predicts frequency of infection should increase with size. We tested these hypotheses for Aedes aegypti in Rio de Janeiro, Brazil, during a dengue outbreak. In the laboratory, longevity increases with size, then decreases at the largest sizes. For field-collected females, generalised linear mixed model comparisons showed that a model with a linear increase of frequency of dengue with size produced the best Akaike’s information criterion with a correction for small sample sizes (AICc). Consensus prediction of three competing models indicated that frequency of infection increases monotonically with female size, consistent with the competition-longevity hypothesis. Site frequency of infection was not significantly related to site mean size of females. Thus, our data indicate that uncrowded, low competition conditions for larvae produce the females that are most likely to be important vectors of dengue. More generally, ecological conditions, particularly crowding and intraspecific competition among larvae, are likely to affect vector-borne pathogen transmission in nature, in this case via effects on longevity of resulting adults. Heterogeneity among individual vectors in likelihood of infection is a generally important outcome of ecological conditions impacting vectors as larvae.     

Female size and fitness in the leaf-cutter bee Megachile apicalis

1. The effects of female size on fitness of the leaf-cutter bee Megachile apicalis Spinola (Hymenoptera: Megachilidae) were examined using artificial nesting sites in the field.
2. Although female size had no significant effect on female longevity or sex ratio of progeny, it did have a significant effect on fecundity; larger females attained greater realized fecundity than did smaller females.
3. This significant effect of female size on fecundity occurred because larger females produced cells faster than did smaller females.
4. Female size also had a significant effect on egg size; larger females laid larger eggs than did smaller females.
5. Female size had a significant effect on the size of investment in each progeny. The size of investment estimated by brood cell weight was greater for larger females than for smaller females. This pattern was largely absent, however, when the size of investment was estimated by adult progeny weight.
6. Female size had a significant effect on nest usurpation behaviour; larger females had a higher capacity to usurp nests than did smaller females.     

The effect of larval and adult nutrition on successful autogenous egg production by a mosquito

Females of most mosquito species require a blood meal to provision eggs and can be medical problems because of this dependency. Autogenous mosquitoes do not require blood to mature an initial egg batch and, instead, acquire nutrients for egg provisioning as larvae. We studied the importance of larval and adult nourishment for Ochlerotatus atropalpus which is obligatory autogenous for its first egg cycle but may ingest blood for subsequent cycles. Larval nourishment strongly influenced autogenous egg production: female larvae that were nutritionally stressed emerged as smaller adults, produced fewer eggs and emerged with less protein, lipid and glycogen stores. Female Oc. atropalpus are 100% autogenous, regardless of larval diet quality or whether females are fed sugar or water at emergence. Upon completion of the first egg batch, only females emerging from a poor larval diet ingested blood and produced a second egg batch.     

Larval Competition, Adult Fitness, and Reproductive Strategies in the Acoustically Orienting Ormiine Homotrixa alleni (Diptera: Tachinidae)

Homotrixa alleni is a gregarious endoparasitoid fly that attacks adult male Sciarasaga quadrata (Orthoptera: Tettigoniidae) in southwestern Western Australia. Gravid female flies acoustically orient to their host's call and deposit live first-instar larvae upon or near their calling host. Up to 16 larvae may be found developing in the one host, and since only calling adult male S. quadrata are parasitized, host size and hence larval resources are essentially fixed at parasitism. This study examines parasitism by H. alleni in relation to intraspecific larval competition and adult fitness. The mean number of larvae emerging per host failed to increase significantly beyond a clutch size of four. Mean pupal weight and survival to the adult stage decreased linearly with increasing clutch size across the entire range of clutch sizes examined. Within a clutch, heavier pupae successfully completed pupal development significantly more often than lighter pupae. Pupal weight was directly related to adult size, with adult males being significantly larger than adult females at any given pupal weight. Female body size was positively correlated with fecundity. The size distribution of emerging females was normally distributed, while the distribution of searching gravid females collected at acoustic traps in the field was significantly skewed toward larger flies, suggesting yet another fitness benefit associated with large size. Using fecundity and survival to adulthood as our measure of fitness we calculated the optimal clutch size maximizing fitness per host to be seven, which exceeds the majority of observed clutch sizes in the field. Uncertainties associated with larvae successfully entering the host following larviposition are likely to reduce clutch sizes of H. alleni below this optimum in the field.     

The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition

The effect of competition between ovipositing females on theirclutch size decisions is studied in animals that lay their eggsin discrete units of larval food (hosts). In such species theeffect of competition depends on the form of the larval competitionwithin such units. In insect parasitoids, there might eitherbe contest (solitary parasitoids) or scramble competition (gregariousparasitoids) between larvae within a host For gregarious parasitoids,a decreasing clutch size with increasing competition betweenforagers is predicted. This prediction is tested in experimentsusing the parasitoid Aphaertta minuta. Parasitoids were eitherkept alone or in groups of four before the experiment, in whichthey were introduced singly in a patch containing unparasitizedhosts. Animals kept together laid on average clutches of 0.74eggs smaller than females kept alone (average clutch is 5.3),thereby confirming the prediction. Clutch size decreased withencounter number, which might be due to the adjustment of thefemale's estimate of the encounter rate with hosts. Finally,the results are compared with those reported for solitary parasitoids(that have scramble larval competition), for which it is predictedthat the clutch size will increase with increasing levels ofcompetition between females.     

The relationship between female body size and survival rate of the malaria vector Anopheles arabiensis in Ethiopia

Abstract. The relationship between female mosquito body size and survival rate was studied in field populations of Anopheles arabiensis in the Awash valley, central Ethiopia. Body size was quantified by measuring the wing-length. Highly significant correlations were found between size, parousness and insemination. It was concluded that larger An.arabiensis females have a higher probability of survival, being inseminated and producing more egg batches than smaller adults. Implications for vectorial capacity and vector competence of mosquitoes are discussed.     

Body size influences mating success of the Eucalyptus longhorned borer (Coleoptera: Cerambycidae)

Both sexes of adultPhoracantha semipunctata F. (Coleoptera: Cerambycidae) congregate on stressedEucalyptus that are the larval hosts. In a field study, 721 adultP. semipunctata captured on host trees varied considerably in body size with the largest individuals being about twice the length of the smallest. Females that were paired with a mate were similar in size to solitary females, suggesting that the probability of a female being mated was not affected by her size. However, large males had greater success than smaller males in obtaining mates. MaleP. semipunctata rely on antennal contact to locate and identify females on the larval host. Therefore, the rate at which males search for mates is a function of the area swept by their antennae per unit time. Because of their greater antennal spread, large males were able to search for females at double the rate of the smallest males. Large males also dominated in aggressive contests for females. The superior abilities of large maleP. semipunctata in both locating and defending mates account for the influence of body size on mating success.