Social foraging in honey bees: how nectar foragers assess their colony's nutritional status

Summary A honey bee colony operates as a tightly integrated unit of behavioral action. One manifestation of this in the context of foraging is a colony's ability to adjust its selectivity among nectar sources in relation to its nutritional status. When a colony's food situation is good, it exploits only highly profitable patches of flowers, but when its situation is poor, a colony's foragers will exploit both highly profitable and less profitable flower patches. The nectar foragers in a colony acquire information about their colony's nutritional status by noting the difficulty of finding food storer bees to receive their nectar, rather than by evaluating directly the variables determining their colony's food situation: rate of nectar intake and amount of empty storage comb. (The food storer bees in a colony are the bees that collect nectar from returning foragers and store it in the honey combs. They are the age group (generally 12–18 day old bees) that is older than the nurse bees but younger than the foragers. Food storers make up approximately 20% of a colony members.) The mathematical theory for the behavior of queues indicates that the waiting time experienced by nectar foragers before unloading to food storers (queue length) is a reliable and sensitive indicator of a colony's nutritional status. Queue length is automatically determined by the ratio of two rates which are directly related to a colony's nutritional condition: the rate of arrival of loaded nectar foragers at the hive (arrival rate) and the rate of arrival of empty food storers at the nectar delivery area (service rate). These two rates are a function of the colony's nectar intake rate and its empty comb area, respectively. Although waiting time conveys crucial information about the colony's nutritional status, it has not been molded by natural selection to serve this purpose. Unlike signals, which are evolved specifically to convey information, this cue conveys information as an automatic by-product. Such cues may prove more important than signals in colony integration.     

Trunk trails and the searching strategy of a leaf-cutter ant,Atta colombica

Summary Atta colombica uses chemical mass recruitment that allows the rapid exploitation of resources. Most foragers thus search only within patches. Accumulation of extra foragers at patches results in sampling of alternate food items and area-restricted search as patch resources are depleted.Individual workers have a higher probability of removing a leaf fragment the earlier they arrive at a bait. Workers that arrive when much of the resource is gone travel further on the bait (within the patch) but do not spend significantly more time at the patch. They give up after 50–80s.Foraging effort is centered on the extensive trail system, not on the nest a predicted by time and energy foraging models. Search effort is also trail centered. The probability that an item will be discovered decreases with distance from the trail and increasing litter depth. Trail traffic and trail quality together mave no significant effect although this may be because they act antagonistically.Economic considerations predict that trials should be built to high quality and very productive sites. If trails are built as a result of recruitment and recruitment reflects patch quality and productivity, characteristics of forage sites are physically embodied in the trail system.Leaf cutter foraging is better understood as a long term optimization that effectively exploits resources over the lifetime of the colony than as prudent predation that husbands resources.     

Comparison of gut-evacuation rates of feeding and non-feeding Calanus marshallae

Gut-evacuation rates were compared for feeding and non-feeding Calanus marshallae collected near Yaquina Bay, Oregon (44°37N; 124°04W) from June 1986 through May 1987. Evacuation rates were measured at four concentrations of Thalassiosira weissflogii from the decline of gut-pigment fluorescence following transfer of copepods to filtered seawater and from the loss of cells labelled with 68-germanium, a radioactive analog of silicon. There was no significant difference between gut-evacuation rates of feeding and non-feeding copepods over both short-term (20 min) and long-term (90 min) evacuation times. Furthermore there was no difference between rates obtained using either pigment or ⁶⁸Ge as tracers of gut food-passage. These results are discussed in the light of possible dilution of tracer in the guts of feeding copepods due to mixing with unlabelled food. Gut-evacuation rates measured at food concentrations ranging from 500 to 4000 cells ml^-1 were not significantly different, regardless of the technique employed.     

Studies on the nutritional requirements of the larval stages of Penaeus japonicus using microencapsulated diets

Fatty acid biosynthesis in the larval stages of Penaeus japonicus Bate was examined by feeding microencapsulated diets containing (1-¹⁴C) palmitic acid, and fat-free diets supplemented with defined fatty acids. Highest larval growth rates were achieved on diets containing Tapes philippinarum lipid and, when defined fatty acids were substituted, on diets containing 20:63 fatty acid. The radioactive tracer experiments indicate that 16:17, 18:0 and 18:19 fatty acids may be synthesised from palmitic acid and that P. japonicus larvae may possess the ability to elongate 18:33 to 20:53 and 22:63, and 18:26 to 20:46. However, the rates of these reactions appear to be too slow to meet the larval requirements for essential fatty acids and the 3 series of polyunsaturated fatty acids must be provided in the diet.     

Optimal foraging and territorial defence in the Great Tit (Parus major)

Summary We describe an experiment designed to investigate the trade-off between foraging and territorial vigilance in the Great Tit. Captive territorial male Great Tits were observed while foraging in a large indoor aviary. They obtained food from two operant patches in which the supply of food was gradually depleted during a visit. We predicted that during control sessions the birds would switch between patches in such a way as to maximise their overall feeding rate. In experimental sessions, we introduced briefly a rival male as an intruder at the start of the test. The foraging male could see the rival only when travelling between patches and not while feeding within patches. We predicted that during experimental sessions birds would switch between patches more often than in control tests, sacrificing food intake for territorial vigilance. Three of the four males tested behaved in approximately the predicted manner. We discuss the use of an inverse optimality argument to provide a calibration of feeding against the benefit resulting from territorial vigilance.     

Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques

Tissue ¹³C of bowhead whale, Balaena mysticetus, varies seasonally in response to geographic variations in the ¹³C of prey organisms consumed along the annual migratory route between the Bering, Chukchi and Beaufort Seas. Seasonal changes in body ¹³C of whales taken in 1986 from Alaskan waters provide a means of estimating energy intake from the different habitats in which the whales feed. Adult bowheads do not show significant seasonal shifts in the ¹³C of muscle and visceral fat. Their enrichment in ¹³C relative to subadult whales suggests that they acquire most of their food from fall and winter feeding or from unsampled parts of the summer range where zooplankton are enriched in ¹³C. Young individuals however, undergo marked seasonal shifts indicating that they feed heavily both in the summer and autumn or winter. Oscillations in ¹³C along the length of the baleen also provide a measure of age. Baleen growth rates decline as the whales age and provide a means of correcting for wear loss and allow aging of individuals less than 12 yr old. Although body length is a poor indicator of age in young bowhead whales, baleen length is closely correlated. Growth rates of bowheads after Year 1 are slow ( 0.4m yr^-1) and up to 20 yr are required to reach the assumed length of sexual maturity at 13 to 14m.     

Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence

Stable carbon isotope measurements (¹³C) were used to assess the importance of kelp carbon (-13.6 to-16.5) versus phytoplankton carbon (-25.5 to-26.5) to resident fauna of an isolated kelp bed community on Alaska's north arctic coast from 1979 to 1983. The predominant kelp, Laminaria solidungula, showed some seasonal variation in ¹³C which was correlated with changes in the carbon content of the tissue. Animals that showed the greatest assimilation of kelp carbon (>=50%) included macroalgal herbivores (gastropods and chitons,-16.9 to-18.2), a nonselective suspension feeder (an ascidian,-19.0) and a predatory gastropod (-17.6). Animals that showed the least incorporation of kelp carbon into body tissues (<=7%) included selective suspension-feeders (hydroids, soft corals and bryozoans,-22.8 to-25.1). Sponges, and polychaete, gastropod and crustacean omnivores exhibited an intermediate dependence on kelp carbon (15 to 40%). Within some taxonomic groups, species exhibited a broad range in isotopic composition which was related to differences in feeding strategies. In the polychaete group alone, ¹³C values identified four major feeding habits: deposit-feeders (-18.0), omnivores (-20.4), predators (-22.2) and microalgal herbivores (-23.0). Distinct seasonal changes in the ¹³C values of several animals indicated an increased dependence on kelp carbon during the dark winter period when phytoplankton were absent. Up to 50% of the body carbon of mysid crustaceans, which are key prey species for birds, fishes and marine mammals, was composed of carbon derived from kelp detritus during the ice-covered period.     

Importance of the fatty acids 20:5ω 3 and 22:6ω 3 in the diet of plaice (Pleuronectes platessa) larvae

The requirement of plaice (Pleuronectes platessa L.) larvae for the fatty acids 20:5 3 and 22:6 3 was studied. Larvae were reared from first feeding to beyond metamorphosis on Artemia sp. nauplii (EG brand), whose nutritional content had been manipulated by enrichment. Some larvae were fed Artemia rich in 20:5 3 and 22:6 3, and others were fed nauplii with no 22:6 3 and low levels of 20:5 3 (1.9% of the total fatty acids). The differences in diet had no significant difference on growth or survival of the plaice larvae. The results indicate that the plaice larvae in this study did not require 22:6 3 in their diet, even when the levels of 20:5 3 were low.     

Division of labor during honey bee colony defense

Summary Some worker honey bees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. We use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and we propose that the non-guard defenders be called soldiers, due to their important role in colony defense.Offprint requests to: M.D. Breed     

Worker size variability and foraging efficiency in Veromessor pergandei (Hymenoptera: Formicidae)

Summary As foragers of the harvester ant, Veromessor pergandei, travel further from their nest they spend significantly more time sampling seeds in experimental patches. Although accepted seeds are heavier than offered seeds, mass of accepted seed is not correlated with sampling time. Variably sized V. pergandei workers do not size-match; little, if any, variance in size of seed selected can be attributed to body size of forager. The lack of size-matching in V. pergandei suggests individual performance may be an inadequate measure of colony foraging success.     

Feeding factors for the sea anemone Anthopleura midorii

The carnivorous feeding behavior of the sea anemone Anthopleura midorii was found to be a sequence of successive feeding motions, which consisted of several separate actions: (1) tentaculation on any solid matter; (2) retention of prey by tentacles; (3) mouth opening; (4) ingestion of food; (5) digestion of food; (6) extrusion of indigestible waste material. Hot water extract of a natural prey induced the entire feeding sequence when extract was given in the form of an artificial food by mixing with -potato starch and water. The fractionated extract induced only a limited feeding action. Several amino acids induced feeding. Alanine, glycine or histidine stimulated the retention of artificial food by tentacles, and proline evoked mouth opening. Cysteine or reduced glutathione (GSH) induced food ingestion. Unnatural food stuff such as -potato starch was ingestible, if an appropriate amount of a chemical substance was added.     

Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton

In our field study we analyzed the C and H isotopic and biochemical (C, N, P, protein, lipid, carbohydrate) composition of the jellyfish Pelagia noctiluca (collected from the Gulf of Trieste in 1985 to 1986) and its presumed diet-net zooplankton. The mean ¹³C (-18.8) and D (-58.4) ratios of P. noctiluca showed enrichment in heavy isotopes relative to net zooplankton (2 for carbon and 30 for hydrogen). Both the jellyfish and net zooplankton were characterized by a linear correlation between ¹³C and D. C. N, P, protein, lipid, and carbohydrate contents of P. noctiluca were low on a dry weight basis as compared to net zooplankton. Significantly lower C:N and C:P ratios were found in jellyfish indicating a greater loss of carbon relative to nitrogen and phosphorus along the passage to a higher trophic level. Isotopic and biochemical evidence indicate that, though collected in nearshore waters, P. noctiluca depended on autochthonous marine organic matter.     

False feedings at the nests of carrion crows<Emphasis Type="Italic"> Corvus corone corone</Emphasis>

False feedings, when individuals visit the nest but refrain from feeding the chicks, occur in some cooperative species and have been interpreted in the white-winged chough (Corcorax melanorhamphos) as active deception by helpers towards the rest of the group. In a cooperatively breeding population of carrion crows (Corvus corone corone) 81.5% of the individuals that provided nestling care showed various kinds of false feedings: arriving at the nest with no food, consuming part or all the food brought to the nest, or taking back from a chicks gape the food that had just been delivered. False feedings occurred on average during 16.3% of nest visits, with some individuals performing them at very high rates (up to 64% of nest visits). False feedings occurred at similar rates in unassisted pairs and groups with helpers, and breeding females showed false feeding at significantly higher rates than other group members. Furthermore, individuals showed false feedings regardless of whether they were alone on the nest or in the presence of other group members, and false feedings did not provoke aggression by the rest of the group. False feedings are not likely to represent deceptive help in the carrion crow. We suggest that crows evaluate the chicks condition during nest visits and that false feedings occur as result of a trade-off between their own hunger and the chicks needs.Communicated by W.A. Searcy     

Lipid biochemistry and reproductive biology in two species of Gammaridae (Crustacea: Amphipoda)

Gammarus oceanicus Segerstråle, 1947 and Echinogammarus marinus (Leach, 1815) were sampled during the breeding season from Oslofjord in 1984, and their lipid composition examined in relation to reproductive condition. In G. oceanicus, female lipid content increased as the ovary matured. Both the amount of lipid stored and the rate of accumulation were greater in spring than in winter. Spring eggs contained 12.4 g lipid, of which 63% was triacylglycerol and 27% phospholipid. Both fractions decreased steadily during embryonic development. Winter eggs contained 19.2g lipid, of which 52% was triacylglycerol and 43% phospholipid. During the early stages of embryonic development the amount of phospholipid decreased sharply, whereas that of triacylglycerol increased, suggesting that some of the fatty acid released from phospholipid was sequestered temporarily as triacylglycerol. When newly spawned, both winter and spring eggs were richer in monoenoic fatty acids than adult amphipods and these acids were the major fuel consumed during development. 6 fatty acids were utilised more slowly than 3 acids, and egg carotenoid pigment content remained constant. Female E. marinus increased in lipid content as the ovary matured. Spring eggs contained 14.7 g lipid when newly spawned and this increased to 16.6 g during the early stages of development. This increase was entirely triacylglycerol, which declined in later stages; the source of the extra lipid was unclear. Eggs contained very little phospholipid or sterol, and both of these components remained at a steady low level during development. E. marinus eggs were not significantly rich in thonoenoic acids compared with adults, and saturated, monoenoic and polyenoic acids were utilised about equally during development. Both adults and eggs were rich in 20.46, which was utilised at a slower rate than the 3 polyunsaturated acids during embryonic development; again, egg carotenoid pigment content remained constant. In both species there was a decrease in the size of the egg (and as a result, of the newly hatched juvenile), but an increase in total reproductive output (i.e., the total weight of the egg clutch) per female as the breeding season proceeded. The reproductive output of an individual female is probably related to food availability during the period of ovarian maturation, whereas the size of an individual egg is dictated largely by feeding conditions for the juveniles once they are independent of the female. The different patterns of lipid utilisation during development found in this study emphasize the flexibility of response in the reproductive biology of gammarid amphipods. It is not yet possible, however, to relate the differing patterns in a simple way either to egg size or total female reproductive output. Two outstanding problems are the source of extra triacylglycerol during the early stages of development of E. marinus and the metabolic cost of brooding eggs.     

Alloimmune memory for glycoproteid recognition molecules in sea anemones competing for space

A highly specific recognition system, capable of distinguishing between allogeneic (non-clonemates) and syngeneic (clonemates) conspecifics, exists in Anemonia sulcata (Coelenterata: Anthozoa). During a competitive interaction between allogeneic individuals, specialized structures (acrorhagi) are exposed and used to sting opponents. This complex behavior is called the acrorhagial response. In order to quantify this behavior we measured the acrorhagial response time (period from first contact with opponent to full expansion of acrorhagi). More than 320 reciprocal histoincompatibility responses were recorded. These histoincompatibility (H) markers are free components of the sea anemone mucus: they were characterized as glyco-proteins of a molecular weight <18 KD (Kilo-Dalton) containing terminal -d-glucose and/or -d-mannose. In alloimmune memory testing experiments, the memory trace in A. sulcata was found to persist for 5 d.     

Feeding,growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi

Feeding, growth and bioluminescence of the thecate heterotrophic dinoflagellate Protoperidinium huberi were measured as a function of food concentration for laboratory cultures grown on the diatom Ditylum brightwellii. Ingestion of food increased with food concentration. Maximum ingestion rates were measured at food concentrations of 600 g C l^-1 and were 0.7 g C individual^-1 h^-1 (1.8 D. brightwelli cells individual^-1 h^-1). Clearance rates decreased asymptotically with increasing food concentration. Maximum clearance rates at low food concentration were ca. 23 l ind^-1 h^-1, which corresponds to a volume-specific clearance rate of 5.9x10⁵ h^-1. Cell size of P huberi was highly variable, with a mean diameter of 42 m, but no clear relationship between cell size and food concentration was evident. Specific growth rates increased with food concentration until maximum growth rates of 0.7 d^-1 were reached at a food concentration of 400 g C l^-1 (1000 cells ml^-1). Food concentrations as low as 10 g C l^-1 of D. brightwellii (25 cells ml^-1) were able to support growth of P. huberi. The bioluminescence of P. huberi varied with its nutritional condition and growth rate. Cells held without food lost their bioluminescence capacity in a matter of days. P. huberi raised at different food concentrations showed increased bioluminescence capacity, up to food concentration that supported maximum growth rates. The bioluminescence of P. huberi varied over a diel cycle, and these rhythmic changes persisted during 48 h of continuous darkness, indicating that the rhythm was under endogenous control.     

Collective decision-making in honey bees: how colonies choose among nectar sources

Summary A honey bee colony can skillfully choose among nectar sources. It will selectively exploit the most profitable source in an array and will rapidly shift its foraging efforts following changes in the array. How does this colony-level ability emerge from the behavior of individual bees? The answer lies in understanding how bees modulate their colony's rates of recruitment and abandonment for nectar sources in accordance with the profitability of each source. A forager modulates its behavior in relation to nectar source profitability: as profitability increases, the tempo of foraging increases, the intensity of dancing increases, and the probability of abandoning the source decreases. How does a forager assess the profitability of its nectar source? Bees accomplish this without making comparisons among nectar sources. Neither do the foragers compare different nectar sources to determine the relative profitability of any one source, nor do the food storers compare different nectar loads and indicate the relative profitability of each load to the foragers. Instead, each forager knows only about its particular nectar source and independently calculates the absolute profitability of its source. Even though each of a colony's foragers operates with extremely limited information about the colony's food sources, together they will generate a coherent colonylevel response to different food sources in which better ones are heavily exploited and poorer ones are abandoned. This is shown by a computer simulation of nectar-source selection by a colony in which foragers behave as described above. Nectar-source selection by honey bee colonies is a process of natural selection among alternative nectar sources as foragers from more profitable sources survive (continue visiting their source) longer and reproduce (recruit other foragers) better than do foragers from less profitable sources. Hence this colonial decision-making is based on decentralized control. We suggest that honey bee colonies possess decentralized decision-making because it combines effectiveness with simplicity of communication and computation within a colony. Offprint requests to: T.D. Seeley     

Nutrition studies in the nauplius larva of Calanus pacificus (Copepoda: Calanoida)

Nauplii of Calanus pacificus were raised on a mixture of algae. Details of the mouth-parts, such as denticles, labial palps and lobes, setations and structure of the masticatory teeth were examined by scanning electron microscopy (SEM). Under the experimental conditions (15°C and 300 gC l^-1), exponential growth coefficients for the period Nauplii II–VI were 0.179 for carbon and 0.228 for nitrogen. C:N ratios dropping from 5.1 to 4.7. Growth was isochronous, each stage lasting 1.5 days. Respiratory losses were 15 to 19.6% of body carbon daily. Nauplii raised on a given alga showed higher rates of ingestion in the presence of this food, compared to nauplii switched to other algae. Minimal threshold concentrations for feeding were found, depending on the size of the food offered and ranging from 5.8 gC I^-1 for Lauderia borealis (28.7 m spherical diameter) to 47.1 gC 1^-1 for Chlamydomonas sp. (11.0 m). Unlike the Copepodite I stage, Nauplii II–VI larvae were not able to ingest small cells such as Isochrysis galbana (4.3 m), or very large ones such as Ditylum brightwellii (47.5 m) at more than maintenance rations. Below the critical concentration for maximal feeding, ingestion was clearly dependent on size of the cells offered, but the size-dependent relationship was different for diatoms and non-diatoms. Filtering rates increased from a threshold concentration to a maximal rate at about 50 gC 1^-1, and decreased at higher concentrations. Critical concentrations ranged from 125 gC 1^-1 for L. borealis to 1000 gC 1^-1 for Chlamydomonas sp. Maximal daily rations ranged between 100 and 150% of body carbon.     

The erect ‘penis’ is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas

In East Africa, spotted hyenas live in large clans in a highly structured society dominated by females. A clan is a fission-fusion society where members are often solitary or in small groups. Spotted hyenas have a ritualized greeting during which two individuals stand parallel and face in opposite directions. Both individuals usually lift their hind leg and sniff or lick the anogenital region of the other. The unique aspect of greetings between individuals is the prominent role of the erect penis in animals of both sex. Female spotted hyenas have fused outer labiae and a pseudo-penis formed by the clitoris which closely resembles the male penis and can be erected. During greetings subordinates signalled submission with gestures which were not necessarily reciprocated by the dominant participant. Asymmetries were most pronounced in greetings between adult females where the probability of asymmetries increased with the divergence in rank between partners. Greetings between adult females and males were uncommon and restricted to males above median rank, principally the alpha male. Models of primate affiliative behavior assume that benefits derived from social relationships with different individuals are not equal and that individuals are selected to maximize the benefits they receive from social relationships with others. The observed distribution of greetings between partners of different rank matched the predictions of these models. An examination of non-adaptive hypotheses on the evolution of the pseudo-penis demonstrated that the conventional scenario linking (initial) virilization of female genitalia with selection for female dominance does not explain either the initial virilization, nor the evolution of the pseudo-penis to its current form and use. We sketch a new scenario that links (1) initial virilization to the occurrence of neonatal siblicide amongst members of a twin litter, and (2) costs of maintenance, pseudo-penile control over copulation and male submission. Our analysis confirms previous adaptive hypotheses on the function of the pseudo-penis in greetings and suggests new hypotheses to account for hitherto unexplained features. Correspondence to: M.L. East     

Mercury budget estimates for the State of New York

The development of two comprehensive modelling systems and a test application to estimate the mercury budget for the State of New York is discussed in the present study. The modelling tools developed are based on two well known meteorological modelling systems namely, RAMS and SKIRON/Eta. Both models have been modified and the developed modules describing the physico-chemical processes of mercury have been incorporated in each modelling system. Model calculations and measurements have been compared during the 14 to 26 August 1997 simulation period. Two different simulations were performed, scenario1 where all available sources of mercury were used and scenario2 where the New York State mercury sources were excluded. An attempt was made to identify and quantify critical gaps in the current understanding of regional scale transport deposition and fate of mercury in New York State, improving modelling capabilities and understanding of mercury as an air pollutant, and provide a tool for policy makers in mitigating the impacts of mercury pollution.