Feeding behavior of Simulium vittatum larvae in response to various suspended materials: implications for control using biological larvicides

Biologically based larvicides used to suppress nuisance populations of black flies (Diptera: Simuliidae) require that the larvae ingest the larvicide for mortality to occur. Materials present in the habitat that alter larval feeding behavior may reduce the effectiveness of the larvicide. This study was conducted to determine the effects that commonly occurring materials in larval habitats have on Simulium vittatum Zetterstedt feeding behavior. Larvae were exposed to 50 p.p.m. of kaolinite clay and 4 p.p.m. of purified diatom frustules. Larvae were also exposed to 10 000 cells or colonies per ml of viable green algae, Chlorella vulgaris Pratt and Scenedesmus quadricauda (Turp) Bréb, and the diatom Cyclotella meneghiniana Kützing to determine the effects that these materials have on larval feeding behavior. Individual larvae were recorded using a digital camcorder to determine the average number of times the larvae extended and retracted their cephalic fans per min (flick rate) in each medium. Following exposure to the selected material, neon red particles (NRP) (DayGlo) were added to the larval medium for 20 min. A spectrophotometric analysis was conducted to determine the average quantity of NRP consumed by larvae per min in each medium. The flick rate and quantity of NRP consumed by larvae was not significantly affected by clay material or viable Chlorella cells. When Scenedesmus colonies or Cyclotella cells were present in the larval medium, larval flick rate and NRP ingestion was significantly reduced. The presence of diatom frustules in the medium resulted in the most severe reduction in larval flick rate and NRP ingestion. The results suggest that larval flick rate can change depending on environmental conditions, and that suppression programs using biologically based larvicides may benefit from investigating the potential correlation between algal counts and treatment efficacy.     

Functional response of suspension feeding anuran larvae to different particle sizes at low concentrations (Amphibia)

The influence of particle size, initial particle concentration and larval stage on the ingestion rate, ‘retention efficiency’, and filtering rate of anuran larvae with varying filter apparatus anatomy and different life histories was investigated for four species. Larvae of premetamorphic Stages 28 and 32 and prometamorphic Stage 40 were selected for filtering experiments on the basis of their different growth rates. Three different sizes of silica gel particles were offered as mock food. Particle concentration was measured photometrically. The Michaelis-Menten model was used to describe the dependency of ingestion rate, filtering rate, and ‘retention efficiency’ upon initial particle concentration, and to calculate maximum ingestion rate, threshold concentration, and the half-saturation constant. (1) The highest ingestion rates, filtering rates and ‘retention efficiencies’ were achieved by Xenopus laevis larvae, followed by Bufo calamita larvae. Bufo bufo larvae lay at the opposite end of the scale. Rana temporaria larvae were placed between B. calamita and B. bufo larvae. This order is attributed to differences in life histories, especially the different breeding environments in which these larvae occur. (2) The larger the particle size and the older the stage, the greater the tendency toward saturation of the ingestion rate, filtering rate and ‘retention efficiency’. These filtration parameters are graded according to particle size. The ingestion rate (number of particles), filtration rate and ‘retention efficiency’ are greatest for PS3. Ingestion volume is greatest for PS 1. The difference between PS3 and PS2 on the one hand, and PS1 on the other, is often great; for Stage 28 X. laevis it is very great. This shows that larvae ingest large particles more effectively, and that the most effective ingestion takes place at Stages 28 and 32, owing to the growth function of these stages. The ability of larvae to ingest large particles effectively is possibly a very basic phylogenetic characteristic. (3) The threshold concentration is lowest when the particles are at their largest. In accordance with conclusions drawn by other authors, threshold feeding is attributed to regulation by buccal pumping and mucus production. Considerable importance is attributed to threshold feeding with respect to larval adaptation to oligotrophic environments.     

Effect of monosodium glutamate on apple leaf consumption by codling moth larvae

We have demonstrated that larvae of codling moth, Cydia pomonella (L) can successfully complete their first instar when fed apple leaves instead of fruit. Larvae fed leaves after hatching maximized their feeding intensity (about 320 g/larva/day) on day 2. Weight gain revealed a stereotypic sigmoid pattern that peaked on day 3. Although the maximum body weight of larvae fed leaves was 70–85% less than for larvae maintained on apples or on artificial diet, 100% of larvae fed leaves molted to the second instar 3–5 days after hatching. Our investigation revealed a diurnal pattern of leaf ingestion, and neonates' feeding intensity decreased significantly during the scotophase. We also demonstrated that monosodium glutamate (MSG) increased feeding on leaves by codling moth larvae. Depending on the duration of the bioassay, and larval age at time of initial exposure, 0.05 mg/ml and 0.1 mg/ml MSG increased apple leaf consumption by 25–60% over leaves alone. The effect of monosodium glutamate was best demonstrated during the first day following hatching. Exposure to MSG also accelerated molting to the second instar. Larvae exposed to MSG initiated consumption of leaf tissue significantly earlier than control neonates. The feeding stimulatory effect of MSG was not observed if exposure to this chemical was delayed until 3–4 h after hatch.The addition of feeding stimulants to pesticides that act via the alimentary tract may reduce the amount of active ingredients needed to maintain the efficacy of these formulations. Here, we postulate that first instar codling moth larvae are potential targets for treatment with pesticide formulations enhanced with monosodium glutamate.     

Oral exudate as a mediator of behavior in larval eastern and western spruce budworms (Lepidoptera: Tortricidae)

The production of oral exudate by larval eastern and western spruce budworms,Choristoneura fumiferana (Clem.) andChoristoneura occidentalis Free., respectively, was investigated in the laboratory. All larvae except those entering into a molt exhibited aggressive behavior and produced exudate in response to handling or intraspecific encounters. Larvae could be induced to produce exudate up to four times over 2–3 min and produced an average of 1.92±0.04 µl (X ± SE) per induction. Larvae on foliage spent much of their time maintaining their silken feeding tunnel, including spinning and combing silk and removing frass. Exposure to conspecific oral exudate deposited inside the tunnel, or released by agitated larvae inside the tunnel, increased the proportion of larvae that dispersed away from the tunnels and, apparently, increased the larval sensitivity to disturbances. The behavior induced by the oral exudate indicates that it acts as an epideictic (spacing) pheromone.     

Performance of pine looper Bupalus piniarius larvae under population build-up conditions

In the first year of an outbreak, Bupalus piniarius larvae, encounter intense crowding. In the later stages of larval development, they are forced to feed on the non-preferred current-year needles of Scots pine or even on alternative hosts. It was hypothesized that larval feeding on a non-preferred resource (current-year needles) will negatively affect B. piniarius performance. It was also hypothesized that larval mutual interference (crowding without competition for food) will have negative additive effects. These hypotheses were tested in laboratory and field experiments. Fourth instar larvae were reared singly and under crowded conditions in cohorts of ten. Larvae in both situations were reared on control branches (containing both mature and current-year shoots) and branches containing only current-year shoots. Crowded larvae were reared also on Norway spruce, an alternative host. Crowding and feeding on a non-preferred resource had opposite effects on B. piniarius larval performance. Crowding in the late larval instars enhanced larval performance while absence of the preferred resource had negative effects. Larval growth rate was higher and development time was shorter for larvae exposed to crowded conditions than for solitary larvae. There was, however, no difference between the groups in final pupal weights or survival. Survival was 25% lower for larvae feeding on non-preferred current-year needles and pupal weights 9% lower, compared with results for larvae feeding on mature needles. Larvae feeding on Norway spruce suffered greatly extended development time, 82% lower survival, and resulted in 60% lighter pupae compared with conspecifics on Scots pine. It was concluded that not only quantity but also quality of the available food resource is critical for B. piniarius development.     

Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea

A concern with the widespread use of insecticidal transgenic crops is their potential to adversely affect non-target organisms, including biological control agents such as larvae of the green lacewing, Chrysoperla carnea (Neuroptera: Chrysopidae). Since the insecticidal proteins expressed by the current transgenic plants are active only after ingestion, dietary bioassays are required to test direct effects on non-target organisms. After showing that C. carnea larvae utilize carbohydrate foods, we exposed them to insecticidal proteins dissolved in a sucrose solution. Feeding on snowdrop lectin (Galanthus nivalis agglutinin, GNA) as a model compound, the larvae were negatively affected in a number of life-table parameters. Interestingly, GNA caused a prolongation in first instar development, but had no effect on subsequent utilization of prey resulting in an increased weight of second instars. Comparable studies with avidin, a biotin-binding protein, revealed strong effects on C. carnea survival at the concentration tested. Despite the fact that the proteolytic digestion of C. carnea larvae is reported to be dominated by serine proteases, ingestion of soybean trypsin inhibitor (SBTI) did not cause any detrimental effects. Similarly, two Cry proteins derived from Bacillus thuringiensis (Cry1Ac and Cry1Ab) did not cause negative effects on C. carnea, what is consistent with earlier studies. The here presented bioassay provides a valuable tool to assess direct impacts of insecticidal proteins to C. carnea larvae and other predators that are known to feed on carbohydrate solutions.     

Xenopus laevis larvae (Amphibia,Anura) as model suspension feeders

Larvae of the South African clawed frog, Xenopus laevis (Daudin), are efficient, obligate suspension feeders. We examine the relationship between the ambient particle concentration offered these larvae as food and their filtering, ingestion, and buccal pumping rates. We demonstrate that: (i) the larvae can sense and respond to a broad range of particle concentrations, down to 0.2 mg 1^–1 (dry weight); (ii) their metabolic needs theoretically can be met by particle concentrations as low as 5 mg 1^–1; and (iii) their patterns of regulation of filtering and ingestion fit predictions from certain models used to describe zooplankton feeding dynamics. Two such models are discussed: the modified Monod (Michaelis-Menten) model, with a lower threshold below which the tadpoles do not feed, and an energy optimization model. Both the models and the observed behavior of the tadpoles allow for stability of populations of food organisms. Tadpole feeding dynamics apparently are compatible with both the predictions and assumptions of these models, suggesting similar regulation of feeding by tadpoles and zooplankton. However, the size, morphology, and behavior of X. laevis larvae make their feeding regulation uniquely accessible to direct observation.Contribution No. 223, Center for Great Lakes Studies, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin.Contribution No. 223, Center for Great Lakes Studies, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin.     

The physiology of digestion in fish larvae

Synopsis The acquisition, digestion, and assimilation of food is critical for the growth and survival of fish larvae; a fish larva either grows or it perishes. Fish larvae are characterized by digestive systems and diets that differ from adults. Larvae undergo a pattern of trophic ontogeny, changing diet with increasing size, and these changes result in differences in digestive requirements. At first feeding, the larval alimentary canal is functional, but is structurally and functionally less complex than that of adults. The larval alimentary canal remains unchanged histologically during the larval period before transformation. During transformation, major changes that result in the development of the adult alimentary canal occur. The ontogeny of the alimentary canal differs in different taxa, and experimental evidence suggests that functional differences exist as well. Assimilation efficiency may be lower in larvae than it is in adult fishes, due to a lack of a morphological and functional stomach in larvae, but the question of improving assimilation efficiencies during larval development before transformation remains unresolved.     

Effects of insect damage on photosynthesis,transpiration and SO2 uptake by sycamore

Summary The bilberry (Vaccinium myrtillus L.), is the dominant plant in the field layer of many boreal forests in northern Sweden. It is utilized by several herbivorous insect larvae as food (i.e. Lepidoptera: Geometridae, Tortricidae and Hymenoptera: Symphyta). Total density of insect larvae was 63% lower where birds had access to larvae compared to exclosures. Larvae with a feeding behaviour which exposes them to birds (geometrids and sawflies) showed a pronounced reduction in density when exposed to bird predators. Density of larvae with a concealed feeding behaviour (tortricids) was unaffected by birds. The frequency of larval damage to bilberry annual shoots was significantly higher in areas where larval density was high due to exclusion of birds. I concluded that birds have the potential to heavily modify the interaction between bilberry and insect larvae.     

Effect of carnivory on larvae and adults of a detritivorous caddisfly, Lepidostoma complicatum: a laboratory experiment

Lepidostomatid caddisfly larvae are typical detritivores, but they occasionally eat small dead animals. A laboratory feeding experiment was conducted with Lepidostoma complicatum (Kobayashi) larvae using two different feeding treatments: leaves or leaves and dead chironomids. L. complicatum larvae showed significantly higher growth rates and adult emergence weight and a significantly earlier emergence for the leaves and dead chironomids treatment than for the leaves alone treatment. However, the adult emergence rate was not different between the two feeding treatments. Thus, it is apparent that ingestion of dead chironomids by detritivorous L. complicatum larvae positively influences larval growth rates, adult emergence weight, and larval development time.     

Onion maggot feeding and development on heterogeneous sections of the onion bulb

When given a choice of feeding sites in laboratory arenas, Delia antiqua (Meigen) larvae exhibited a 3: 1 bias for internal vs outer sections of onion bulbs and distributed themselves non-randomly among identical preferred onion sections. Larval clustering did not appear to be correlated with increased fitness in the laboratory; larval development was identical across the range of densities from 1 to 50 larvae per onion. Larvae feeding on preferred internal sections developed 14% faster, were 38% heavier upon pupation, and were two times more likely to survive to the adult stage than larvae feeding on outer sections. D. antiqua larval food preference was therefore positively correlated with increased fitness.     

Determinants of ingestion rates in filter-feeding larval blackflies (Diptera: Simuliidae)

SUMMARY 1. The functional response of the filter-feeding blackfly larva Frosimulium mixtum/fuscum was examined in laboratory experiments. We focused on the relationship between a component of the particle handling process (the cephalic fan flick rate) and ingestion rate, to determine whether ingestion rate is limited by handling-time. The influence of food deprivation on ingestion rate and feeding efficiency also was assessed. 2. Ingestion rate rose asymptotically with increasing food availability, leveling off at a concentration of about 100 mg1^?1. Satiation did not account for this plateau. Flick rate (the frequency with which larvae open and close their cephalic fans) increased in a similar fashion, though flick rate only accounted for about two-thirds of the variation in ingestion rate. 3. A simple equation describing the components of the feeding process in blackfly larvae was developed to investigate alternate flick rate ‘decision rules’ capable of predicting relationships between food concentration, flick rate and ingestion rate. The flick rate did not follow a fixed time rule, in which larvae allow particles to accumulate in the fan for a fixed amount of time prior to retraction. For most food densities, flick rate patterns more closely approximated a fixed number rule, in which fans are retracted after a fixed number of particles accumulate. 4. Flick rate rose with increasing food concentration even after the ingestion rate had levelled off, whereas several optimal filter-feeding models predict that filtering rate should decline as food concentration increases above this level. This predicted behavior was not observed because the number of particles ingested per flick failed to increase with increasing food concentration. 5. The efficiency of particle ingestion (number ingested × number available^?1× 100) was very low (<0.1%), and declined with increasing food concentration. 6. An increase in food deprivation time prior to a feeding trial produced a significant increase in flick rate, ingestion rate and feeding efficiency. This adjustment of feeding behaviour allowed animals to replace their gut contents more quickly following longer periods of food deprivation, which agrees with the qualitative predictions of optimal digestion-time models.     

Temperature and food quality influences feeding behavior,assimilation efficiency and growth rate of arctic woolly-bear caterpillars

Summary The energy budget for feeding activity and growth of larval Gynaephora groenlandica was investigated on the tundra and in the laboratory. Larvae fed only in June when the buds and young leaves of Salix arctica, its principal host plant, contained the highest concentrations of macro-nutrients and total nonstructural carbohydrates (TNC). The mid-summer hiatus in larval feeding was coincident with an abrupt decline in the TNC content of leaves and a buildup of plant secondary metabolites in the leaves of S. arctica. Following cessation of feeding, the larvae remained concealed from the sun within crevices and vegetation mats. Growth rates of larvae incubated at 15 and 30°C were similar (4.7–5.0 mg/larva/day), but the assimilation efficiency at 15°C was four times greater (40%) than at 30°C. Growth rates were lowest at 5°C (0.22mg/larva/day) as was the assimilation efficiency (6.6%), because of the extended residence time of food in the gut. The high rate of ingestion and excretion at 30°C was caused by elevated maintenance metabolism. Changes in metabolic state influenced oxygen consumption, which was highest for feeding larvae (0.29 ml/g/h) and significantly lower for each, digesting, moving, starved larvae, and lowest for inactive larvae (0.06 ml/g/h). An influence of temperature and leaf quality on digestion rate and maintenance metabolism is the most likely cause of the feeding behavior pattern in G. groenlandica. The larvae may undergo voluntary hypothermia in order to avoid an energy, deficit resulting from high maintenance metabolism during mid-season when the energy content and food quality declines. The restriction of growth and development to a very short period prior to mid-summer may have contributed, to the extended 14-year life cycle of this species.     

Embryogenesis and early larval development in wild-caught Levantine scraper,Capoeta damascina (Valenciennes, 1842)

Levantine scraper, Capoeta damascina is a candidate species for future stock assessments, conservation studies, and hatchery efforts. Herein, we documented embryonic and early larval development, from egg activation to the exogenous feeding period, using morphological and histological landmarks. Embryos were obtained by in vitro fertilization from hormonally induced wild-caught broodstock, and subsequent development was monitored at temperatures coinciding with native conditions. Embryonic development from fertilization to hatch lasted ~105–110 hr. Larvae emerged with unpigmented eyes and body morphology, as well as an undifferentiated digestive tract. The mouth was closed at hatch by the oropharyngeal membrane and opened by the early endogenous feeding period. Trabeculae cartilage, quadrate bone, and Meckel's cartilage of the endoskeleton were present during the endogenous feeding period. During this period, the larvae underwent considerable changes in craniofacial morphology, locomotion, and organogenesis of the digestive tract. The cartilaginous floor of the neurocranium developed and the first four ceratobranchials appeared simultaneously at the end of endogenous feeding period. The digestive tract was differentiated into buccopharynx, esophagus, and small intestine during the endogenous feeding period. The intestinal valve and numerous longitudinal folds at the posterior region of the intestine formed together by the endo–exogenous feeding period. Major developmental events in retinogenesis occurred during the endogenous feeding period. When larvae entered exogenous feeding the mouth was fully-functional. Additionally, liver size and eye diameter increased. Our analysis of embryonic and early larval development in Levantine scraper aligned with other freshwater fishes.     

Effects of food,water depth,and temperature on diving activity of larval Anopheles gambiae sensu stricto: evidence for diving to forage

Anopheles gambiae larvae have frequently been observed to dive, but the ecology of this behavior has not been extensively examined. We manipulated food level, water depth, and temperature for individually‐reared larvae and observed diving activity. Larvae dived more often under low food, which suggests that they dive to forage. There was only weak evidence for effects of water depth or temperature on diving. Experimental results are discussed in the context of energy budgets. Understanding larval ecology of this species is important for predicting how it will respond to environmental change. Further study is needed to assess the role that larval diving plays in both feeding ecology and thermal regulation of this and other medically important species.     

Cuterebra buccata: immune response in myiasis of domestic rabbits

Naturally infected rabbits (Oryctolagus) were used to define further the nature of the immune response in myiasis due to Cuterebra buccata. Third instar larvae were dissected into four fractions; (1) alimentary tract with attached organs, (2) hemolymph, (3) fat body with tracheae, and (4) cuticle with attached muscles. The antigens provoking immune phenomena in naturally infected rabbits were found to reside in the alimentary tract and hemolymph fractions only. All rabbits which were skin tested were found to exhibit delayed hypersensitivity and to have serum precipitins with specificity against these antigens. Passive cutaneous anaphylaxis activity was demonstrated only in sera from rabbits also exhibiting reaginic and/or Arthus-type skin hypersensitivities. With the use of immunoelectrophoresis four separate antigens were demonstrated in alimentary tract fractions. Larval dissections revealed the alimentary tract to be filled with cellular elements of rabbit whole blood. The immunologic findings are discussed in relation to this newly recognized feeding pattern and it is proposed that sensitization of the host occurs as a consequence of exogenous larval secretions injected at the time of feeding.     

Relating the ontogeny of functional morphology and prey selection with larval mortality in Amphiprion frenatus

Survival during the pelagic larval phase of marine fish is highly variable and is subject to numerous factors. A sharp decline in the number of surviving larvae usually occurs during the transition from endogenous to exogenous feeding known as the first feeding stage in fish larvae. The present study was designed to evaluate the link between functional morphology and prey selection in an attempt to understand how the relationship influences mortality of a marine fish larva, Amphiprion frenatus, through ontogeny. Larvae were reared from hatch to 14 days post hatch (DPH) with one of four diets [rotifers and newly hatched Artemia sp. nauplii (RA); rotifers and wild plankton (RP); rotifers, wild plankton, and newly hatched Artemia nauplii (RPA); wild plankton and newly hatched Artemia nauplii (PA)]. Survival did not differ among diets. Larvae from all diets experienced mass mortality from 1 to 5 DPH followed by decreased mortality from 6 to 14 DPH; individuals fed RA were the exception, exhibiting continuous mortality from 6 to 14 DPH. Larvae consumed progressively larger prey with growth and age, likely due to age related increase in gape. During the mass mortality event, larvae selected small prey items and exhibited few ossified elements. Cessation of mass mortality coincided with consumption of large prey and ossification of key elements of the feeding apparatus. Mass mortality did not appear to be solely influenced by inability to establish first feeding. We hypothesize the interaction of reduced feeding capacities (i.e., complexity of the feeding apparatus) and larval physiology such as digestion or absorption efficiency contributed to the mortality event during the first feeding period. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Does Cry1Ac Bt‐toxin impair development of worker larvae of Africanized honey bee?

The western honey bee (Apis mellifera L.) is a widespread pollinator species. The present study aimed to test if Africanized honey bee larvae are negatively affected by the ingestion of diet contaminated with the Bacillus thunringiensis toxin Cry1Ac, which is expressed in GM cotton plants. The toxin activity was confirmed in bioassays with the velvetbean caterpillar (Anticarsia gemmatalis), a soybean pest species susceptible to Cry1Ac. The honey bee larvae were subjected to ingestion of either pure larval diet (control), diluted larval diet (diluted control) or larval diet diluted in a Cry1Ac solution at a concentration compatible with the maximum possible field exposure. Although diluted diet slightly increased larval mortality, Cry1Ac ingestion did not affect survival, developmental time, and neither adult body mass nor size, indicating that GM plants are unlikely to significantly impair the development of honey bee larvae. The larval‐rearing system reported here was suitable to assess the lethal and sub‐lethal effects of GM expressed toxins against honey bee larvae.     

Predator feeding vibrations encourage mosquito larvae to shorten their development and so become smaller adults

1. Water‐borne predator kairomones are known to allow mosquito larvae to detect and identify the presence of a specific predator, so that they can deploy defences tailored to that predator. Kairomones, however, have limitations, and detection of specific water‐borne vibrations produced by a predator would allow fine‐tuning of their anti‐predator defences. 2. Larvae of the mosquito Culiseta longiareolata have previously been shown to recognise the specific vibration pattern of a feeding dragonfly nymph and respond by altering their feeding behaviour from active bottom‐scraping to a more passive surface filter‐feeding, while other water vibrations did not produce this response. Culex perexiguus larvae also responded, but to a much lesser extent. 3. In this study, C. perexiguus larvae responded strongly to dragonfly vibrations by reducing their larval duration from 9.8 to 8.7 days, but this resulted in significantly smaller (and thus probably less successful) adults. However, Culiseta longiareolata larvae did not alter their larval duration in response to dragonfly vibrations.