Patterns of photosynthetic carbon metabolism in light-limited phytoplankton

Patterns of phytoplankton carbon (C) metabolism were examined in å combined laboratory and field study to assess the influence of light conditions on ¹⁴C assimilation into photosynthetic end-products. Laboratory studies with three species representing distinct size classes and taxonomic groups tested the influence of low light on patterns of C flow. Prorocentrum mariae-lebouriae (dinoflagellate) and Ditylum brightwellii (diatom) showed decreased movement of photoassimilated ¹⁴C into protein following a shift to low light ¹⁴C assimilation into lipids and photosynthetic pigments increased in low light and was paralleled by increased chl a per cell. The proportion of ¹⁴C fixed into protein returned to the pre-shift level upon return to initial light conditions. Monochrysis lutheri (chrysophyte) did not show this pattern of reduced % ¹⁴C protein. Incubations of 12 and 24 h demonstrated significant rearrangements in labeling patterns at night, wherein ¹⁴C flow into protein in darkness was favored. % ¹⁴C protein at night was lower for M. lutheri than for the other species, suggesting some interspecific differences in the low light response. Measurements of ¹⁴C assimilation in phytoplankton assemblages from Chesapeake Bay demonstrated movement of a higher proportion of photo-assimilated C into protein in samples collected in the surface mixed layer than in those below the pycnocline. In comparison, phytoplankton collected below the pycnocline fixed a higher proportion of ¹⁴C into lipids, photosynthetic pigments, and low molecular weight metabolites, as was observed in low light laboratory cultures. A comparison of 12- and 24-h incubations for measuring patterns of C flow into photosynthetic end-products confirmed the inadequacy of short-term measurements, as significant changes in ¹⁴C allocation occurred in the dark phase of the photocycle. Together, these results suggest that ¹⁴C assimilation into photosynthetic end-products can be a useful measure of adaptive state in changing light conditions, but point out some difficulties in applying this approach in situ.     

Does interaction between bumblebees (Bombus ignitus) reduce their foraging area?: bee-removal experiments in a net cage

To examine whether the interaction between bumblebees, Bombus ignitus, reduces their foraging area, we conducted bee-removal experiments in a net cage. In the cage, we set potted Salvia farinacea plants, allowed bumblebees to forage freely on those plants, and followed their plant-to-plant movements to identify a bee with a relatively small foraging area. We then removed all the other foraging bees, except for the bee with a small foraging area, and observed the change of the foraging area of the focal bee under conditions of no interaction with other bees. After the removal of the other bees, all five bees tested enlarged their foraging areas, suggesting that the interaction between bees is an important determinant of their foraging areas. The result also means that bumblebees are able to adjust their foraging areas in response to other foragers, indicating the necessity for future studies to clarify what cues bees use to interact with other bees. Moreover, after the removal treatments, all five bees showed temporary increases in the number of flower probes per plant. This can be explained by their optimal foraging according to the old average intake rate for the plant population and by the delayed changes in response to the new high average energy intake rate after the bee-removal treatments.Communicated by M. Giurfa     

Dance dialects and foraging range in three Asian honey bee species

Summary We measured the distance dialects in the dance languages of three honey bee species in Thailand (Apis florea, A. cerana, and A. dorsata), and used these dialects to examine the hypothesis that a colony's dialect is adaptively tuned to enhance efficiency of communication over the distances that its foragers typically fly. in contrast to previous interspecific comparisons in Sri Lanka (Lindauer 1956; Punchihewa et al. 1985), we found no striking dialect differences among the Asian bees in Thailand. The adaptive tuning hypothesis predicts that the foraging ranges of the three species should also be similar, but comparisons of colonial foraging range using the forage mapping technique (Visscher and Seeley 1982) actually revealed marked differences. This raises the possibility that the link between ecology and distance code is more subtle than previously supposed, if a link exists at all. Offprint requests to: F.C. Dyer     

Carbon fixation in marine phytoplankton: carboxylase activities and stable carbon-isotope ratios; physiological and paleoclimatological aspects

We measured the activity of three carboxylases: RuBP carboxylase, PEP carboxylase and PEP carboxykinase of marine phytoplankton species in culture and in natural communities. Activities of the three carboxylases were measured simultaneously with stable carbon-isotope ratios. The enzymatic activities have been used to estimate the importance of carboxylation and its impact on the ¹³C:¹²C ratio (expressed as ¹³C). The marine phytoplankton species in culture were Fragilariopsis kerguelensis, Nitzschia turgiduloides, Skeletonema costatum, Phaeodactylum tricornutum, Isochrysis galbana, Dunaliella marina, and Prorocentrum micans, and the field samples were collected from different depths off the coast of Portugal (August/September, 1981). Our results indicate that, as in terrestrial plants, the ¹³C value is a good indicator of the extent of carboxylation. RuBP carboxylase activity was always predominant, whereas the ¹³C value never reached values typical of the C₄ pathway. The carboxylases could be PEP carboxylase (in dinoflagellates) or PEP carboxykinase (in diatoms). carboxylation increased at the end of the exponential growth phase in a diatom culture and with increased biomass in natural samples. We interpret these increases as an adaptative response mechanism to poor environmental conditions, especially to low light intensity.     

Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.)

Variability exists among worker honey bees for components of division of labor. These components are of two types, those that affect foraging behavior and those that affect life-history characteristics of workers. Variable foraging behavior components are: the probability that foraging workers collect (1) pollen only; (2) nectar only; and (3) pollen and nectar on the same trip. Life history components are: (1) the age the workers initiate foraging behavior; (2) the length of the foraging life of a worker; and (3) worker length of life. We show how these components may interact to change the social organization of honey bee colonies and the lifetime foraging productivity of individual workers. Selection acting on foraging behavior components may result in changes in the proportion of workers collecting pollen and nectar. Selection acting on life-history components may affect the size of the foraging population and the distribution of workers between within nest and foraging activities. We suggest that these components define possible sociogenic pathways through which colony-level natural selection can change social organization. These pathways may be analogous to developmental pathways in the morphogenesis of individual organisms because small changes in behavioral or life history components of individual workers may lead to major changes in the organizational structure of colonies. Correspondence to: R.E. Page, Jr.     

Elemental composition (C,N,H) in larval and crab-1 stages of Pagurus bernhardus (Decapoda,Paguridae) and Carcinus maenas (Decapoda,Portunidae)

Analyses of individual content of carbon (C), nitrogen (N), and hydrogen (H) were carried out for all larval stages of Pagurus bernhardus and Carcinus maenas, and for newly metamorphosed crabs. Maximum range in total larval development is 12.8 to 165.8 g C, 3.2 to 35.1 g N, and 1.9 to 24.9 g H in P. bernhardus and 3.1 to 43.2 g C, 0.7 to 10.1 g N, and 0.4 to 6.3 g H in C. maenas. From these data energy equivalents were calculated. Maximum range in total larval life is 0.43 to 6.38 J ind. ^-1 in P. bernhardus and 0.1 to 1.49 J ind. ^-1 in C. maenas. There is a 32.4% mean loss of energy in P. bernhardus megalopa development; this seems to describe the normal developmental pattern in this stage. Biomass was determined as fresh and dry weight respectively. Individual dry weight is about 3.6 to 5.6 times higher in P. bernhardus (44 to 340 g) than in C. maenas (12 to 93 g) larvae.Contribution to research project Experimentelle marine Ökosystemanalyse sponsored by Bundesministerium für Forschung und Technologie, Bonn (Grant No. MFU-0328/1)     

Effects of salinity fluctuation on the hemolymph composition of the blue crab Callinectes sapidus

The hemolymph of the blue crab Callinectes sapidus was hyperosmotic during 20-10-20 S and 30-10-30 S diurnal cycles. The hemolymph became isosmotic at 26 S and hyposmotic at 28 S in the 10-30-10 S diurnal cycle. Hemolymph Na⁺ was hyperionic to seawater throughout all cycles. Hemolymph Cl^- was hyperionic below 24 S and either isionic or hypoionic from 24 to 30 S. Hemolymph K⁺ concentrations were hyperionic below 26 S and either isionic or hypoionic from 26 to 30 S. Hemolymph Mg⁺⁺ values were hypoionic over the experimental salinity range (10 to 30). Hemolymph ninhydrin-positive substances (NPS) levels were directly related to ambient salinity.     

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     

Vigilance and foraging substrate: anti-predatory considerations in a non-standard environment

Summary The commonly studied standard anti-predatory environment presents animals with spatially-distinct feeding sites and refuges from attack, neither of which necessarily obstructs predator detection. In contrast, tree-trunks provide animals with a markedly non-standard environment in which the foraging substrate itself may be a refuge from attack that unavoidably obstructs predator detection. Thus anti-predatory behavior in this environment should be influenced not only by a perceived risk of attack, but also by the nature of the refuge/foraging substrate itself. Downy woodpeckers (Picoides pubescens) are a common tree-trunk foraging animal, and an experimental analysis of their behavior suggests that they respond appropriately to their non-standard anti-predatory environment. In particular, anti-predatory vigilance varies strongly with changes in tree trunk diameter. Two modes of vigilance were apparent. In stationary vigilance, woodpeckers maintained the position of their feet while rotating their bodies side-to-side to peer around the trunk; mobile vigilance involved movement around the trunk itself. Both the frequency and angle of rotation of stationary vigilance increased with trunk diameter, as did the frequency of mobile vigilance. The woodpeckers also held their heads farther away from the trunk surface as diameter increased. All of these measures of vigilance increased under a greater perceived risk of predation. As might be expected given these results, downy woodpeckers avoided thick trunks; they did not, however, prefer the thinnest (least obstructive) available trunks. These preferences may reflect the influence of trunk diameter on thermo-ecological and/or anti-predator considerations not related to vigilance. Overall, this arboreal environment provides an unusual perspective on anti-predator decision-making with several implications for tree-trunk foraging animals in general.     

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     

Compositional topography of melon lipids in the Atlantic bottlenosed dolphin Tursiops truncatus: Implications for echo-location

Major variations in lipid composition exist within the fatty melon tissue of the Atlantic bottlenosed dolphin Tursiops truncatus. Topographical lipid analyses indicate a central inner melon core surrounded by distinctive outer melon, under melon, and blubber tissues. Acoustical considerations suggest that this melon-lipid topography may aid in collimation of the ultrasonic pulses used by the dolphin for echolocation.     

“Copper” granules in the barnacle Balanus balanoides

Balanus balanoides (L.) collected from an area with high heavy-metal run-off contained two different types of granule within the parenchyma cells of the prosoma. X-ray microprobe analysis shows one to be the familiar zinc granule made up of concentric layers and giving major peaks for phosphorus and zinc, and the other to be homogeneous and giving peaks for sulphur and copper. This latter granule is designated the copper granule. Whilst zinc granules are known to be composed of inorganic phosphate, various tests on copper granules in sections and in a granule-rich pellet have shown that the copper is probably complexed with organic matter. The tests also demonstrated the relatively, insoluble (inert) nature of these granules. Although zinc and copper granules were present together in the prosoma, atomic absorption analyses of whole bodies (prosoma+thorax) have shown the level of zinc (50.28 g/mg dry weight) to be much higher than that of copper (3.75 g/mg dry weight).     

The role of learning in the mating biology of a sweat bee Lasioglossum zephyrum (Hymenoptera: Halictidae)

Summary Results from experiments on the role of learning in the mating biology of a sweat bee, Lasioglossum zephyrum (Hymenoptera: Halictidae), are described in this paper. Male learning of individual female odors is important in natural populations (Table 1), as has been shown in the laboratory. Four other hypotheses are unlikely to account for the observed behavior: (1) Female odors dissipate rapidly; (2) Males learn and then avoid the study area; (3) Males or females produce repellents which are effective against other males; or (4) males recognize their own odor on previously-contacted females, which they subsequently avoid. Regarding questions of male preference and optimal outbreeding, Tables 2 and 3 show there are no consistent preferences for more novel or less novel female odors.     

Nutrient enrichment and the ultrastructure of zooxanthellae from the giant clam Tridacna maxima

The separate and combined effects of ammonium (10M) and phosphate (2M) on the ultrastructure of zooxanthellae (Symbiodinium sp.) from giant clams, Tridacna maxima, were examined in the field. Nitrogen addition significantly changed the ultrastructure of the zooxanthellae inhabiting the clams. After 9 mo exposure, the cross-sectional area of zooxanthellae from N-treated clams was significantly lower than that from other treatments [N=39.3 m²; C=47.9 m²; P=43.2m²; N+P=44.5 m²; (P=0.001)]. There was also a significant decrease in the size of starch bodies, especially around the pyrenoid of the zooxanthellae from N and N+P treatments [N=1.2 m²; C=2.0 m²; P=1.8 m²; N+P=1.2 m²; (P=2.08E-11)]. This presumably occurs as a result of the mobilization of organic carbon stores in response to stimulated amino acid synthesis under enriched nutrient conditions. These data strongly suggest that the symbiotic zooxanthellae of clams are limited to some extent by the availability of inorganic nitrogen, and that relatively minor changes to the nutrient loading of the water column can have substantial effects on the biochemistry of symbioses such as that which exists between clams and zooxanthellae.     

Memory dynamics and foraging strategies of honeybees

Summary The foraging behavior of a single bee in a patch of four electronic flower dummies (feeders) was studied with the aim of analyzing the informational components in the choice process. In different experimental combinations of reward rates, color marks, odors and distances of the feeders, the behavior of the test bee was monitored by a computer in real time by several devices installed in each feeder. The test bee optimizes by partially matching its choice behavior to the reward rates of the feeders. The matching behavior differs strongly between stay flights (the bee chooses the feeder just visited) and shift flights (the bee chooses one of the three alternative feeders). The probability of stay and shift flights depends on the reward sequence and on the time interval between successive visits. Since functions describing the rising probability of stay flights with rising amounts of sucrose solution just experienced differ for the four feeders, it is concluded that bees develop feeder-specific memories. The choice profiles of shift flights between the three alternative feeders depend on the mean reward rate of the feeder last visited. Good matching is found after visits to the low-reward feeders and poor matching following departure from the high-reward feeders. These results indicate that bees use two different kinds of memories to guide their choice behavior: a transient short-term working memory that is not feeder-specific, and a feeder-specific long-term reference memory. Model calculations were carried out to test this hypothesis. The model was based on a learning rule (the difference rule) developed by Rescorla and Wagner (1972), which was extended to the two forms of memories to predict this operant behavior. The experiments show that a foraging honeybee learns the properties of a food source (its signals and rewards) so effectively that specific expectations guide the choice behavior. Correspondence to: R. Menzel     

Why are bumble bees risk-sensitive foragers?

Summary In a controlled laboratory experiment, we re-examined the question of bumble bee risk-sensitivity. Harder and Real's (1987) analysis of previous work on bumble bee risk aversion suggests that risk-sensitivity in these organisms is a result of their maximizing the net rate of energy return (calculated as the average of expected per flower rates). Whether bees are risk-sensitive foragers with respect to minimizing the probability of energetic shortfall is therefore still an open question. We examined how the foraging preferences of bumble bees for nectar reward variation were affected by colony energy reserves, which we manipulated by draining or adding sucrose solution to colony honey pots. Nine workers from four confined colonies of Bombus occidentalis foraged for sucrose solution in two patches of artificial flowers. These patches yielded the same expected rate of net energy intake, but floral volumes were variable in one patch and constant in the other. Our results show that bumble bees can be both risk-averse (preferring constant flowers) and risk-prone (preferring variable flowers), depending on the status of their colony energy reserves. Diet choice in bumble bees appears to be sensitive to the target value a colony-level energetic requirement. Offprint requests to: R.V. Cartar     

Effects of salinity fluctuations on the respiration rate of the southern oyster drill Thais haemastoma and the blue crab Callinectes sapidus

Respiration rates of Thais haemastoma and Callinectes sapidus were determined as a function of salinity with a flow-through respirometer at 20°C. Respiration rates were measured at 10, 20 and 30 S for acclimated animals. The effects of 10-5-10, 20-10-20, 30-10-30 and 10-30-10 S semidiurnal cycles (12 h) of fluctuating salinity on the rate of respiration of the oyster drill were studied. During each cycle, salinity was changed from the acclimation salinity over a 4 h interval, held at that salinity for 2 h, returned to the acclimation salinity over 4 h and held at that salinity for 2 h. The effects of diurnal (24.8 h) salinity cycles on respiration in the oyster drill and blue crab were also studied. Salinity was changed from the acclimation salinity over a 10.4 h interval, held at that salinity for 2 h, then returned to the acclimation salinity over 10.4 h and held at that salinity for 2 h. The respiration rate of 30 S acclimated oyster drills (679 l O₂ g dry weight^–1 h^–1) was significantly higher than for individuals acclimated to 10 S (534 l O₂ g dry weight^–1 h^–1). Blue crab respiration was 170 l O₂ g dry weight^–1 h^–1 at 30 S, and was significantly higher at 10 and 20 S than at 30 S. With the exception of the 20-10-20 S semidiurnal cycle, the respiration rate of oyster drills declined as salinity fluctuated in either direction from the acclimation salinity and increased as ambient salinity returned to the acclimation salinity. Semidiurnal cycles (12 h) of fluctuating salinity produced greater changes in the respiration rate of snails than analogous diurnal cycles (24.8 h). A 10-30-10 S pattern of fluctuation caused a greater percentage reduction in the steady state respiration rate of oyster drills than the 30-10-30 S pattern. The respiration rate of blue crabs varied inversely with fluctuating salinity. Relatively minor changes occurred in blue crab respiration rate with fluctuating salinity. Blue crab respiration rate characteristically dropped during the initial phase of declining salinity at a rate directly proportional to the rate of salinity decrease, perhaps representing a metabolic adjustment period by the blue crabs. The respiratory response of T. haemastoma to salinity is consistent with its incomplete volume regulation, while the response of C. sapidus is compatible with its ability to regulate extracellular fluid osmotic and ionic composition.     

Acute toxicity of mercury and selenium to Crassostrea gigas embryos and Cancer magister larvae

The possible modification of mercury toxicity by selenium in embryos of the Pacific oyster Crassostrea gigas and the larvae of the crab Cancer magister was investigated. Mercury concentration eliciting abnormal development in 50% of the oyster embryos (EC₅₀) was 5.7 g l^-1 (48 h) and mortality in 50% of the crab larvae (LC₅₀) occurred with 6.6 g l^-1 (96 h). The 48 h EC₅₀ for selenium was greater than 10,000 g l^-1 for oyster embryos and the 96 h LC₅₀ for crab zoeae was 1040 g l^-1. The response from each species, when exposed to both toxicants, revealed, that a high level of selenium (5,000 g l^-1) increased mercury toxicity. Moderate selenium concentrations (10 to 1,000 g l^-1) tended to decrease mercury toxicity, although no statistical verification could be made. The order of administration of toxicants had no effect on the response of Crassostrea gigas embryos. Early developmental stages (8 h) of C. gigas embryos were most sensitive to dissolved Hg; toxicant administration 24 h after fertilization resulted in no apparent abnormalities in development.     

Compositional topography of melon and spermaceti organ lipids in the pygmy sperm whale Kogia breviceps: Implications for echolocation

The forehead of the pygmy sperm whale Kogia breviceps contains a large melon of fatty tissue in front of a small, fat-filled, cornucopia-shaped spermaceti organ. This unique anatomical structure may possibly play an acoustical role in the whale's echolocation system, similar to the fatty melon sound lens postulated for dolphins. To better understand its function, we have studied the compositional topography of the K. breviceps melon and spermaceti organ lipids. The fatty head tissues of an adult K. breviceps were serially sectioned into 9 transverse slices. Appropriate tissue samples were cut from every other slice, and analyzed for % lipid and lipid class composition. Wax esters and triglycerides were the only major lipids present; their average carbon number in each sample was determined by gas-liquid chromatography (GLC). Our topographical analyses of K. breviceps melon indicate 3 regions of distinctive lipid composition: a fat-poor melon exterior, an outer melon of medium fat content having % triglyceride>% wax ester, and a fat-rich inner melon having % wax ester>% triclyceride. The spermaceti organ contains a fat-rich core of very high wax-ester content (84 to 99%), surrounded by a fat-poor case. Average carbon numbers of both wax esters and triglycerides were lowest in the inner melon and the spermaceti organ. At the rear of the spermaceti organ lies the museau de singe, an apparent sound generator. The lipid topography data plus anatomical and acoustical considerations suggest that the K. breviceps melon/spermaceti organ system may function as an acoustical transducer, directing and refracting sound waves from this source for the purpose of echolocation.     

Genetic evidence that the “Padstow mussel” is Mytilus galloprovincialis

Electrophoretic analysis of loci controlling a variety of enzymes has been applied to samples of the Padstow mussel and typical Mytilus edulis L. living strictly sympatrically at Rock, Cornwall, England, in order to resolve the disputed status of the Padstow mussel. Small samples indicated similar monomorphic states at the GPDH, TO, MDH-2 loci and weak polymorphism at the 6 PGD locus in both types of mussel. The MDH-1 locus may be weakly polymorphic in the Padstow mussel and monomorphic in M. edulis. Large samples assayed for AP, LAP, PGM, and PHI produced data showing very large and highly significant differences in allele frequencies at three of these loci between the two groups of mussels separated on anatomical characters. At the LAP locus, significant deficiencies of heterozygotes were observed in both groups of mussels. A small percentage of mussels from Rock are difficult to assign with certainty to one or other group on anatomical and morphological criteria, but the genetic evidence indicates that most, if not all, such specimens are M. edulis. These genetic differences make it highly improbable that any significant degree of genetic exchange occurs between the two groups in nature and, taken together with the evidence of genetic resemblance of the Padstow mussel to M. galloprovincialis from Venice and that of Rock M. edulis to M. edulis, from the Gower peninsula of Wales we conclude that the Padstow mussel is indeed M. galloprovincialis.