On the integration of individual foraging strategies with colony ergonomics in social insects: nectar-collection in honeybees

Summary We experimentally tested whether foraging strategies of nectar-collecting workers of the honeybee (Apis mellifera) vary with colony state. In particular, we tested the prediction that bees from small, fast growing colonies should adopt higher workloads than those from large, mature colonies. Queenright small colonies were set up by assembling 10 000 worker bees with approximately 4100 brood cells. Queenright large colonies contained 35 000 bees and some 14 500 brood cells. Thus, treatments differed in colony size but not in worker/brood ratios. Differences in workload were tested in the context of single foraging cycles. Individuals could forage on a patch of artificial flowers offering given quantities and qualities of nectar rewards. Workers of small colonies took significantly less nectar in an average foraging excursion (small: 40.1 ± 1.1 SE flowers; large: 44.8 ± 1.1), but spent significantly more time handling a flower (small: 7.3 ± 0.4 s ; large: 5.8 ± 0.4 s). When the energy budgets for an average foraging trip were calculated, individuals from all colonies showed a behavior close to maximization of net energetic efficiency (i.e., the ratio of net energetic gains to energetic costs). However, bees from small colonies, while incurring only marginally smaller costs, gained less net energy per foraging trip than those from large colonies, primarily as a result of prolonged handling times. The differences between treatments were largest during the initial phases of the experimental period when also colony development was maximally different. Our results are at variance with simple models that assume natural selection to have shaped behavior in a single foraging trip only so as to maximize colony growth. Offprint requests to: P. Schmid-Hempel     

Circadian rhythmicity of locomotor behavior and oviposition in female Teleogryllus commodus

Summary Locomotor activity of the Teleogryllus commodus is under circadian control, with _LL=25.3 h and _DD=23.4 h. In LD 12:12 h, running occurs either exclusively during darkness (57%), mainly in the dark phase (35%), or with substantial activity peaks in both phases (8%). For oviposition, _LL>24 h and _DD<24 h; in LD 12:12 h, 80% of the studied deposited their eggs mainly during the light phase and 20% primarily during darkness. In the discussion, a temporal correlation between stridulation, spermatophore formation, and locomotion, and oviposition is established, which serves to make an encounter and mating between the sexes as likely as possible.Dedicated to Prof. Dr. M. Gersch on the occasion of his 70th birthday     

Annual cycles in worker size of the seed-harvester antVeromessor pergandei (Hymenoptera: Formicidae)

Summary The seed-harvester antVeromessor pergandei Mayr is primitively polymorphic; workers are monophasically allometric. There is a distinct annual cycle in mean worker body size that replicates across colonies and habitats (Fig. 1); this cycle occurs through alteration of the worker size distribution (Fig. 2). There is little, if any, morphspecific task specialization by workers suggesting worker size variance is a colony-level adaptation permitting maintenance of a large and constant worker force during periods of resource fluctuation. Smaller workers appear in the foraging force following the triple crunch of reduced seed availability, reduced favorable times to forage, and alate production during winter months. Adult and startingV. pergandei colonies exhibit strong intraspecific territoriality, suggesting the selective advantage for maintenance of a large and constant worker force. Such selective pressures may have provided the initial variance in worker size distributions that led subsequently to specialized castespecific task performance in more distinctly polymorphic ant species.     

Division of labour in a crisis: task allocation during colony emigration in the ant Leptothorax unifasciatus (Latr.)

Division of labour during colony emigration is widespread in ants. An important problem is how tasks are allocated during colony movement from one nest site to another. The generally favoured view is that emigrations are organised by a minority group of individuals, which either work unusually hard at tasks (elites) or have the exclusive task of carrying out the emigration (moving specialists). Five consecutive emigrations of a Leptothorax unifasciatus (Latr.) colony showed that the number of transporters, i.e. the individuals that took an active part in the emigration by transporting brood and ants, was smaller than it would have been if allocation of this task was random during each emigration. However, single emigrations of another three colonies, for which the spatial distribution and behaviour of the workers had been observed for a week prior to the emigration, demonstrated that the transporters did not form a homogeneous group. They differed in their spatial positions and tasks before the emigration. There was also no evidence that transporters worked harder or less hard than their nestmates before the emigration. Therefore, the individuals which carry out emigrations in L. unifasciatus colonies appear to be neither moving specialists nor elites. We propose that task allocation during emigrations of L. unifasciatus colonies is based on a feedback mechanism that involves learning.     

The enantiomeric composition of monoterpene hydrocarbons in the defensive secretions ofNasutitermes termites (Isoptera): Inter- and intraspecific variations

Summary Frontal gland secretions of termite soldiers of the speciesNasutitermes costalis, N. ephratae, N. nigriceps, N. rippertii, andN. hubbardii were analyzed. The chiral compositions of the monoterpene hydrocarbons were investigated by means of two-dimensional gas chromatography. Two of them, 3-carene and-pinene were present in the form of (–)-enantiomers of high purity in the majority of the samples. The other monoterpenes,-pinene, camphene, sabinene, limonene, and-phellandrene, exhibited a great variation in the enantiopurity between different species.-Pinene and limonene varied significantly even between different colonies within the species.N. costalis was the only species with an invariable composition of the secretion, independent of the locality or origin.     

Predation on zooplankton by the benthic anthozoans Alcyonium siderium (Alcyonacea) and Metridium senile (Actiniaria) in the New England subtidal

The Alcyonacean octocoral Alcyonium siderium Verrill and the sea anemone Metridium senile (L.), the only common perennial zooplanktivores on shallow (16-m depth) subtidal rock walls in much of northern New England, USA, are of similar heights and overlap in their habitat and microhabit distributions. The coelenteron contents of both species were sampled at four-hour intervals over a diel cycle and were compared to zooplankton available in the water at 1 to 5 cm from the rock wall, the height at which the cnidarians held their feeding tentacles. Prey in coelenterons of A. siderium were significantly smaller (means of 256 to 345 m), and those in coelenterons of M. senile were equal to or slightly greater in length (means of 415 to 1006 m) than the available zooplankton. The diets of A. siderium and M. senile differed significantly from each other and from the available zooplankton. A. siderium showed strong positive electivites for ascidian larvae and for foraminiferans, and strongly negative electivities for most crustaceans. M. senile had strong positive electivities for barnacle cyprids, ascidian larvae, and gammarid amphipods, and strong negative electivities for invertebrate eggs, foraminiferans, calanoid and harpacticoid copepods, and ostracods. Electivities may reflect tentacle avoidance or escape by motile prey as well as predator preference. Substratum-associated organisms (e.g. demersal crustaceans, larvae of benthic invertebrates) were the most common items in the diets of both species, suggesting a tight benthic food web, similar to the situation for coral reef anthrozoans which rely on reef-generated zooplankton. A. siderium ate large numbers of ascidian larvae which, as benthic adults, compete for space with A. siderium and can overgrow small colonies. Predation on the larvae of a competing species may alleviate competition by decreasing the competitor's recruitment.     

Spermatozoon structure of some North American prosobranchs from the families Lottiidae (Patellogastropoda) and Fissurellidae (Archaeogastropoda)

The spermatozoa of four species of the patellogastropod family Lottiidae (Lottia pelta, L. digitalis, L. strigatella, Tectura scutum) and one species of the archaeogastropod family Fissurellidae (Diodora aspera) were examined in 1990 using transmission electron microscopy. All have primitive or ect-aquasperm, typical of invertebrates using external fertilization. Sperm of the lottiid limpets are characterized by a 5 to 9 m-long head composed of a conical acrosome which constitutes >50% of the head length, and a cylindrical nucleus. The acrosome of all species of lottiids is differentiated internally, and has a posterior invagination 0.9 to 1 m in depth, into which an elongate acrosomal lobe protrudes. Between the posterior acrosomal lobe and the nucleus, the subacrosomal material is aggregated as a fibrous column. The midpiece of the sperm has a ring of 4 to 5 spherical mitochondria of 0.6 m diam, posterior to which is a collar of cytoplasm 1 m long, which sheaths the anterior portion of the axoneme. The size and morphology of the acrosome and large cytoplasmic collar clearly distinguish the spermatozoa of the Lottiidae from other families of Patellogastropoda. The sperm of D. aspera (Fissurellidae) is typical of the family of archaeogastropod; the head has a length to breadth ratio of 4:1, and the cylindrical nucleus is capped by a small acrosome, <25% of the total head length, which is deeply invaginated.     

Photoacclimation of Ulva rotundata (Chlorophyta) under natural irradiance

Two vegetative clones (designated 11/85 and 7/86 in accordance with month/year of collection) of the green macroalga Ulva rotundata were collected in the vicinity of Beaufort, North Carolina, USA. Each was grown in an outdoor continuous-flow system in summer (20°C) of 1986 and late winter (10° to 17°C) of 1987, in irradiances ranging from 9 to 100% of full sunlight, with and without NH ₄ ⁺ enrichment. Continuous enrichment of influent estuarine water (dissolved inorganic nitrogen 2 M, N:P5) to 8–12 M NH ₄ ⁺ had only a slight effect on growth rate. Temperature changes of 2 to 3°C had a much greater effect. Prolonged exposure to a given daily irradiance resulted in acclimation, exposure to a given daily irradiance resulted in acclimation, indicated by faster growth of conditioned plants relative to those transferred from a different irradiance. Most of the difference in growth rates between transferred and control plants was attributed to differences in thallus absorptance. Growth was photoinhibited above 40% sunlight at temperatures below 15°C, but not above 20°C. Following interday irradiance transfers, thallus percent dry weight changed in a manner that suggests different response times for photosynthesis and cell division.     

Brood reduction in the American white pelican (Pelecanus erythrohynchos)

Summary American white pelicans (Pelecanus erythrorhynchos) breeding in colonies at East Shoal Lake, Manitoba, Canada exhibited a mean hatching asynchrony of 2.5 days in 2-egg clutches. This resulted in a size difference between chicks which facilitated sibling dominance, harassment and lack of food for the subordinate chick. Only one young survived per nest. In marked broods, the secondhatched chick survived in 20% of successful nests. Manipulated clutch sizes (1, 2 and 3 eggs or chicks per nest) revealed that the presence of a second chick contributes significantly to the reproductive success of the parents. Results support the hypothesis that the second egg functions as a form of insurance against early loss of the first egg or chick. The parents, by establishing hatching asynchrony, by nonintervention in sibling aggression, and by selectively feeding the dominant chick, maximize their chance of rearing the most viable young.     

Effect of inhibitors of carbonic anhydrase activity on photosynthesis in the red alga Soliera filiformis (Gigartinales: Rhodophyta)

The effect of light intensity, pH and carbonic anhydrase (CA) inhibitors on photosynthesis of the red marine macroalgae Solieria filiformis (Kützing) Gabrielson, collected from Taliarte (Gran Canaria, Canary Islands) in 1991, has been investigated. Plants taken from the sea (wild phenotype) developed spherical morphology (ball phenotype) after 2 mo culture in aerated tanks. The photosynthetic oxygen evolution in the wild phenotype was saturated at 100 mol photons m^-2s^-1, while the ball phenotype displayed saturation at 200 mol photons m^-2s^-1. The inhibitors of total CA activity (6-ethoxizolamide) and extracellular CA activity (dextran-bound sulfonamide) inhibited photosynthesis at pH 8.2, to 90 and 50% respectively, in both phenotypes. No inhibition of the photosynthetic oxygen evolution was detected at pH 6.5. CA activity was associated with both supernatant and pellet fractions of crude extracts of S. filiformis. The rate of alkalization of the medium by the algae was dependent on light intensity. We suggest that carbon dioxide is the general form of inorganic carbon transported across the plasmamembrane in S. filiformis. HCO₃ transport into the cell takes place simultaneously by an indirect mechanism (dehydration to CO₂ catalyzed by CAext) and by direct uptake. Extracellular (CAext) and intracellular (CAint) CAs are involved in the mechanisms of inorganic carbon assimilation by S. filiformis.     

Seasonal variation in the balance between physiological mechanisms of feeding and digestion in Mytilus edulis (Bivalvia: Mollusca)

Seasonal variations in the balance between physiological mechanisms of feeding and digestion are considered among 45 to 57 mm shell length Mytilus edulis L. from southwest England. Mussels had been acclimated to standardised conditions of food availability in March, June and October, 1981. Results indicate that despite showing a negative relationship (P<0.001) with the efficiency of ¹⁵N absorption, coincident alterations of both ingestion rate (0.17 to 0.54 mg total Phaeodactylum tricornutum h^-1) and organic gut content (1.00 to 1.80 mg) represent significant mechanisms effecting the seasonal regulation of nutrient acquisition. Concurrent changes in absorption efficiency alone clearly exerted a relatively minor influence upon seasonal rates of absorption. Associated gut residence times of ¹⁵N-labelled material varied between 4 and 10 h. Furthermore, despite the ensuing deleterious effects, together with increased gut contents, absorption efficiencies among mussels that had been starved throughout acclimation were consistently maintained equivalent to those among individuals feeding normally. Such constancy was at least partially achieved by an increased residence time of material within diverticulae, relative to the digestive system as a whole. Finally, comparison of isotopic absorption efficiencies with those recorded for total organics and organic nitrogen has demonstrated differences of as much as 30% between gross and net uptake due, we suggest, to excretion of metabolically derived material within the alimentary canal.     

Développement larvaire de deux Tellinacea,Scrobicularia plana (Semelidae) et Donax vittatus (Donacidae)

Scrobicularia plana Da Costa and Donax vittatus L. were reared in the laboratory through settlement. Fertilizable eggs were obtained by perfusing the ovary with 5% 0.1 M ammonium hydroxyde in sea water. S. plana eggs have a thick chorion, inside which the early larval stages develop; they hatch as straight-hinge larvae more than 60 h after fertilization. This brood protection is considered to be an adaptation to osmotic pressure changes and pollution in the environment. D. vittatus eggs have a very thin chorion and are unprotected. Further development is planktotrophic and very similar for the two species. Under laboratory conditions, the pediveliger stage is attained 3 weeks after fertilization and settlement occurs 1 week thereafter. S. plana spat stop growing until a suitable substratum is available. Meanwhile they undergo a byssus drifting important for postlarval dispersion. Post larvae resume growth as soon as a small quantity of fine sand is added to the rearing jar. The exhalant siphon is developed first, when the post larvae reach a length of 600 m; the inhalant siphon is formed later, at a length of approximately 900 m. Evolution from the larval hinge to the juvenile hinge stage occurs sooner in S. plana than in D. vittatus. Comparison of laboratory larval development with field development indicates that spawning occurs in June and August for S. plana in North Wales (UK).     

Carotenoids versus retinoids (Vitamin A) as essential growth factors in penaeid prawns (Penaeus semisulcatus)

Penaeus semisulcatus de Haan adult gravid females, eggs and non-feeding early larvae, including Protozoea I, were used to test the hypothesis that retinoid (Vitamin A) is not required in early decapod crustacean development. In the adult gravid females, retinoids were detected only in the eyes (1.56±0.23 g g^-1 wet mass), whereas there were up to 97 g g^-1 wet mass total carotenoid in digestive gland and epidermis. This was mostly esterified, except in the ovaries, where free astaxanthin predominated (30 g g^-1). No retinoids could be detected in the eggs, the naupliar stages or Protozoea I, but free astaxanthin was metabolised exponentially, falling from 19 g g^-1 in the eggs to 4 g g^-1 in Protozoea I. This suggests that retinoid is not essential in early development and that carotenoid could be taking its place. Also, including retinoids in artificial diets appears to be unnecessary, provided adequate carotenoid is supplied.     

Levels of intracellular free amino acids used for salinity tolerance by oysters (Crassostrea virginica) are altered by protozoan (Perkinsus marinus) parasitism

Free amino acid (FAA) levels were measured from May through October 1991 in gill tissues of two groups of juvenile oysters (Crassostrea virginica Gmelin), one transferred from a low salinity field site (8) to a field site of high salinity (20) and high Perkinsus marinus (Mackin, Owen, and Collier) prevalence, the other kept at the low salinity field site. Within 24 h, glycine levels in the oysters transferred to high salinity increased 8-fold, taurine concentrations doubled and the total FAA pool rose from 150 mol g^–1 dry wt to 400 mol g^–1 dry wt. Taurine levels reached a plateau within 20 d after transfer to high salinity and remained at that level until P. marinus infections were detected 85 d after transfer. Taurine and glycine levels declined by 40% in the high salinity population as infection intensity increased between 70 and 105 d. Total FAA declined by approximately 33% over this period. The oysters kept at low salinity were not infected and continued to grow while the infected high salinity oysters showed no increase in shell length after Day 85. FAA levels in the low salinity group remained relatively constant throughout the experiment except for an initial rise triggered by an increase in ambient salinity from 8 to 12. The results suggest that salinity tolerance mechanisms in C. virginica may be impaired by P. marinus infection.     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary The phenotypic cues that provide for rejection of non-nestmates by workers of the ant genus Camponotus could derive from any or all of four sources: (1) environmental odors; (2) the individual's own genetically-determined recognition pheromones or discriminators; (3) a gestalt or mixture of transferable discriminators, produced by each nestmate and absorbed by all; and/or (4) the discriminators of the queen applied to all nestmates. To test these hypotheses, four series of small experimental colonies were created: inter- and intraspecific mixed colonies containing queens, queenless worker groups, and pairs of worker groups between which a single queen was repeatedly switched. Intraspecific mixed colonies and queenless groups were further divided into groups receiving different diets. Aggression of workers in 165 experimental colonies was assayed in a total of 4064 neutral arena tests. Workers adopted into inter- and intraspecific mixed colonies with queens were highly aggressive to unfamiliar kin from pure colonies, independent of diet and of the proportion of different kin groups in the colony. However, queenless workers exhibited less aggression to unfamiliar kin than to non-kin, demonstrating the existence of worker discriminators. Diet differences slightly enhanced aggression among unfamiliar queenless kin. Non-kin sharing a switched queen were as unaggressive to one another as were sisters. The ability to adopt queenless workers between colonies gradually declined over 1–2 wks following their emergence from pupae. We propose a hierarchy of importance of cue sources in determining nestmate discrimination in small Camponotus colonies: Queen discriminators> worker discriminators>environmental cues. A flow-diagram model of social insect kin recognition, based on the phenotype matching concept of Holmes and Sherman (1983), is discussed.     

Nutritional value of Phaeocystis pouchetii (Prymnesiophyceae) and other phytoplankton for Acartia spp. (Copepoda): ingestion,egg production,and growth of nauplii

Ingestion and egg production by Acartia hudsonica (5°C) and A. tonsa (10°C) from Narragansett Bay, Rhode Island, USA, was measured in the laboratory over a range of concentrations of the prymnesiophyte Phaeocystis pouchetii and the diatom Skeletonema costatum. Both Acartia species reproduced well when fed unialgal diets of S. costatum. Egg production by females fed P. pouchetii, either as gelatioous colonies (primarily >200 m in diameter) or solitary cells (3 to 5 m), was not significantly different than that of starved females. Acartia spp. fed selectively on S. costatum in multialgal treatments. The presence of P. pouchetii did not reduce ingestion of S. costatum; the availability of S. costatum did not increase ingestion of P. pouchetii. Nauplii of A. hudsonica grew equally well on separate diets of P. pouchetii and Isochrysis galbana, two flagellates of similar size. Adult Acartia spp. reproduced poorly when fed these phytoplankton, suggesting that particle size may be more important than food quality in describing the responses. Grazing by Acartia spp. does not directly impact the dynamics of P. pouchetii, but may indirectly contribute to blooms of this prymnesiophyte by removal of competing phytoplankton.     

An energy budget for Porites porites (Scleractinia)

An energy budget for Porites porites (Pallas) was determined for specimens from 10 m depth on the Fore Reef of Discovery Bay, Jamaica, between July 1984 and July 1985. Evidence for habitual zooplankton ingestion was not obtained, and P. porites appears to be largely autotrophic. Out of the daily photosynthetically fixed energy, 26% is used for animal respiration and growth, 22% for zooxanthellae respiration and growth, and <1% for colony reproduction as mature planulae; 45% remains unaccounted for. Colony respiration, net photosynthesis, colony skeleton and tissue growth, zooplankton ingestion, reproductive effort and energy content of tissues were measured. Energy loss as continuous mucus secretion was not detected, but may occur by an alternative route via mucus tunics, which occur periodically in situ and in the laboratory. The energy budget suggests that a considerable excess of photosynthetically fixed energy is produced on an ideal sunny day at 10 m depth. This surplus may be required for periodic rather than continuous energy demands, or may be essential to survive less-than-ideal days, when net photosynthetic input is reduced.Contribution No. 357 of the Discovery Bay Marine Laboratory, University of the West Indies     

Anatomy of structures associated with air-breathing in Orchestia gammarellus (Crustacea: Amphipoda: Talitridae): coxal plates and gills

The structure of the coxal gills and coxal plates of the semi-terrestrial beachflea Orchestia gammarellus (Pallas) (Crustacea: Amphipoda: Talitridae) is described in relation to their possible use for aerial gas exchange and ion exchange. Anatomical evidence is presented to support the hypothesis that the medial surface of the coxal plates functions as an extrabranchial aerial gas-exchange site in O. gammarellus. Thus, the effective diffusion distance across the medial (or inside-facing) surface of O. gammarellus coxal plates (mean±SD=5.4±0.3 m; n=9, cuticle thickness 4.4±0.5 m, n=21) is only a third of the equivalent distance across both the coxal gills (18.4±6.0 m, n=10; cuticle thickness 1.7±0.6 m, n=7) and the lateral (or external) surface of the coxal plates (19.4±0.7 m, n=5; cuticle thickness 8.7±0.8 m, n=7). Chloride-ion-permeable areas were located using a silver-staining technique. All ten coxal gills appeared to be equally permeable to chloride ions after examination with a light microscope. However, the coxal plates and the rest of the integument do not appear to be chloride-permeable.     

Behavioral ecology of the neotropical termite-hunting ant Pachycondyla (= Termitopone) marginata: colony founding,group-raiding and migratory patterns

This study provides the first detailed field account of colony founding, group-raiding and migratory habits in the neotropical termite-hunting ant rPachycondyla marginata, in a semi-deciduous forest in south-east Brazil. New colonies can originate by haplometrosis, pleometrosis, or colony fission. Incipient colonies with multiple foundresses persisted longer in the field, and most excavated nests contained more than one dealated female. A total of 202 group raids by P. marginata were registered, and in all cases the raided termite species was Neocapritermes opacus. Nearly 20% of the workers within a colony engage with raiding activity. Colonies of P. marginata hunt for termites approximately every 2–3 weeks, and group-raids may last for more than 24 h. Target termite nests are up to 38 m from the ant colony, and occasionally two nests are simultaneously raided by one ant colony. Raiding ants carry 1 or 2 paralysed prey, and nearly 1600 termites can be captured during a 9-h raid. Migration by P. marginata colonies lasted over 2 days and covered distances of 2-97 m (n = 48). Average residence time at a given location was 150 days. Three basic migratory patterns were noted: colony fission (only part of the colony moves), long-distance migrations, and short-distance migrations. Both raiding and migratory activities appeared to be strongly affected by seasonal factors. The group raiding and migratory patterns of P. marginata are compared with other ant taxa with similar habits. It is concluded that P. marginata presents a rudimentary form of the so-called army ant behavior, which is highly developed in the subfamilies Dorylinae and Ecitoninae. The extremely specialized diet of P. marginata and the associated high costs of migration are features likely to prevent it from evolving a full army ant life pattern.     

Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay

In situ grazing rates for the mixotrophic dinoflagellate Gymnodinium sanguineum Hirasaka feeding on nanociliate populations of Chesapeake Bay were determined in June and October of 1990 using a gut clearance/gut fullness approach. Recently ingested prey were digested beyond the point of recognition at a rate of 23% h^-1. Estimates of in situ ingestion and clearance ranged from 0 to 0.06 prey dinoflagellate^-1 h^-1 and 0 to 5.8 l dinoflagellate^-1 h^-1, respectively, with daily removal of ciliate biomass representing 6 to 67% of the 20-m oligotrich standing stock. Daily consumption of ciliate biomass by G. sanguineum averaged 2.5% of body carbon and 4.0% of body nitrogen with maximal values of 11.6 and 18.5%, respectively. Ingestion of ciliates may help balance nitrogen requirements for G. sanguineum and give this species an advantage over purely photosynthetic dinoflagellates in nitrogen limited environments. By preying on ciliates, these dinoflagellates reverse the normal flow of material from primary producer to consumer and thereby influence trophodynamics of the microbial food web in Chesapeake Bay.