Trapline foraging by bumble bees: III. Temporal patterns of visitation and foraging success at single plants

We analyzed the temporal structure of visitation by bumble beeworkers to a single Penstemon strictus plant growing in an arrayof conspecifics. When tested against a null distribution usinga randomization model, the observed pattern of arrivals forthe whole group of bees was random, but departures were clusteredin time. Certain individuals visited the plant repeatedly andfrequently throughout the day. These showed significantly regulararrival and departure schedules, which were likely producedby traplining. We explored whether these more frequent and regularforagers gained a higher reward than random or incidental plantvisitors. Using an analytical model, Possingham predicted thata dominating forager that visited a simple, renewing resourcein a regular pattern would garner higher and less variable rewardsthan random visitors. Inspired by these results, but interestedin plant-level visitation, we constructed a simulation modelof resource dynamics for a multiflowered plant with high visitation.The model incorporates the observed visitation schedules ofall bees and independent reward dynamics for each flower onthe plant. We calculated the rewards that observed bees wouldhave collected given a range of resource-renewal parameters.More frequent visitors did not return to the plant when whole-plantresource levels were higher, but these visitors did get greaterrewards. Their increased reward resulted from greater foragingefficiency, primarily through selecting (on average) more rewardingflowers than those selected by less frequent, random visitors.     

Trapline foraging by bumble bees: IV. Optimization of route geometry in the absence of competition

Foraging on resources that are fixed in space but that replenishover time, such as floral nectar and pollen, presents animalswith the problem of selecting a foraging route. What can flowervisitors such as bees do to optimize their foraging routes,that is, reduce return time or route distance? Some repeatedlyvisit a set of plants in a significantly predictable sequence(so-called "trapline foraging"), which may also enhance theirforaging efficiency. A moderate level of optimization and repetitionof foraging routes can be reached by following simple movementrules for choosing the distances and turning angles of successiveflights, without the use of spatial memory. If pollinators canlearn the locations of patches and choose among possible foragingroutes or paths, however, even better performance may be achieved.We tested whether and how bumble bees can optimize and repeattheir foraging routes in laboratory experiments with artificialflowers that secreted nectar at a constant rate. With increasingexperience, foraging routes of bees became more repeatable andefficient than expected from a combination of simple movementrules between successive flowers. We suggest that trapline foragingis a more sophisticated pattern of spatial use than searchingand is based on memory. On the other hand, certain spatial configurationsof flowers hampered optimization by the bees; bees preferredto choose short distances over straight moves and showed littleplasticity in this regard. Developing an efficient trapline,therefore, may require prior selection of a set of plants withan appropriate spatial configuration.     

Trapline foraging by bumblebees: I. Persistence of flight-path geometry

By setting out arrays of potted plants of Penstemon strictus,I tested whether freely foraging bumblebee (Bombus spp. ) workerswould establish regular foraging routes that reflected the geometryof the array. They did, passing through an asymmetrical arrayin a pattern that minimized interplant flight distances. Afterthe array was changed to a symmetrical pattern, however, theexperienced bees continued to show their previous asymmetricalflight patterns. New bees without experience on the asymmetricalarray showed no asymmetry on the symmetrical array. I term thispersistence of flight-path geometry "trapline holdover, " anddiscuss its implications for the study of animals' learningand foraging behavior.     

Heritable allometric variation in bumble bees: opportunities for colony-level selection of foraging ability

Different characters of an organism may be correlated if genes control the allometric relationship between them. If genetic variation exists for such genes then the allometric relation itself is potentially subject to change by selection. In social insects allometric relations represent colony-level characters. If colonies differ in these relations and this variation leads to differential productivity among colonies, then selection on allometric relations can operate at the level of the colony. We assessed the extent of heritable, between-colony variation for the allometric coefficients relating proboscis ( = glossa) length to wing length for two bumble bee species (Bombus huntii and B. occidentalis). We found that in both species colonies did not differ significantly in slope (b) but did differ significantly in intercept (a) of the regression of glossa length on wing length. Within-colony variation of the intercept was estimated by randomly constituting groups of five workers from each colony and calculating the regression for each group. The intraclass correlation was then calculated from the between- and within-colony mean squares. We found significant intraclass correlations in both species, giving heritabilities of 0.5 ± 0.3 in B. hunti and 0.7 ± 0.3 in B. occidentalis. If this allometric relation affects colony foraging success and foraging environments vary geographically, then the intercept should exhibit corresponding geographic variation. We tested this prediction by comparing intercepts calculated using wild-caught B. vagans workers from Alberta, Ontario and Maine. We found that the intercepts did differ significantly between sites, with the bees from Alberta having a significantly smaller intercept than the bees from eastern North America. Our results illustrate the opportunity for selection on an allometric relation that directly affects the foraging success of individual bumble bee colonies.     

Foraging dynamics of bumble bees: correlates of movements within and between plant species

What rules determine whether bumble bees continue exploitingplants of the species just visited or switch to another species?To tackle this question, we recorded handling times and flighttimes from bees foraging in a natural meadow containing fiveplant species. Inter- and intra-specific plant distances werequantified. The bee-subjective colors of the five species weredetermined; two of these species had similar colors and structures,while three species were distinct from all others. The followingrules were identified: (1) The decision to switch species wascorrelated with previous flower handling time, which we assumeis a function of the reward amount received at the flower. Aftershort handling times, the probability of switching to anotherspecies increased, whereas it decreased after long handlingtimes. This difference became even greater if the bee had hada run of several short or several long handling times. (2) Constantflights (those between flowers of the same species) and transitionflights (those between flowers of different species) followedstereotyped temporal patterns independent of the distances betweenflowers. Constant flights within five plant species consistentlyhad median durations of about 2 seconds, whereas median transitiontimes between species took 3–6 seconds. (3) This temporalrule broke down, however, if the flowers of two species hadsimilar colors, in which case transition flights had equal dynamicsas constant flights. (4) Bees switched more frequently fromrare than from common species but even more frequently betweensimilar species. We conclude that the bees' choices were determinedby a set of rules that guided them to stay with the currentplant species as long as flowers were rewarding and availablewithin close distance but to switch to another species if flowersoffered low rewards or were not encountered at close range     

The genetic control of seven isozymic loci in Vicia faba L. Identification of lines and estimates of outcrossing rates between plants pollinated by bumble bees

A simplified and non-destructive method using starch gel electrophoresis has been developed on seeds to identify inbred lines of Vicia faba and assess outcrossing rates and gene dispersal in pollination experiments. Six enzyme systems (Alcohol dehydrogenase, Aspartate aminotransferase, Glucose-6-phosphate isomerase, Isocitrate dehydrogenase, Phosphogluconate dehydrogenase and Shikimate dehydrogenase) were analysed from parental lines, crosses performed between lines bearing dissimilar isozyme patterns in pollination cages with Bombus and F₂ progenies obtained from manual selfing of F₁ hybrids. The allozymes at each of the seven studied loci segregated in the expected Mendelian fashion and behaved in a co-dominant manner except for the Adh-2 locus where the only variant was a null allele. No evidence of genetic linkage was observed between at least 13 of the 15 pairs of the studied loci. Percentage of cross fertilisation by Bombus between seven pairs of inbred lines ranged between 1.7% and 28.3%. Pollen transfer between a donor line and a recipient line by two species of Bombus did not lead to differences in outcrossing rates (both about 8%). The new PGD marker with two loci at three alleles each is particularly discriminating and valuable in pollination studies and breeding of V. faba.     

Energetics and foraging behaviour of the European seed harvesting ant Messor capitatus: II. Do ants optimize their harvesting?

Abstract The preference in seed selection by Messor capitatus (Latreille) was studied with artificial seeds (weighted styropore spheres) in the laboratory and with natural seeds in the field. The laboratory experiments showed no strong preference for size of the artificial seeds in the range 3–8 mm (diameter). A mass of about 400 mg was selected when artificial seeds of 5-5.5 mm were offered at different distances from the nest.
In the field experiments, crushed seeds were placed 2 m from the nest and ants showed a clear preference for the size class 2.0–3.0 mm in diameter, which is much smaller and lighter than the preference for the artificial seeds. The preference of seeds from different plants showed very big variability. There was no correlation between the preference and any of the following variables of the seeds: fresh mass, dry mass, water content, energy content, and nitrogen content. No evidence for energy optimizing in food selection in Messor capitatus was found.
The energetic reward of bringing any seed back to the nest will, under all normal conditions, be much higher than the energetic expenditure. For example, the energetic content in a wheat seed is about 650 Joule, which is sufficient energy for a worker ant of Messor capitatus to carry the seed for a distance of 6.5 km at a temperature of 30^oC.     

Inference of selection and recombination from nucleotide sequence data*

Two techniques for obtaining information about population structure from nucleotide sequences in DNA are summarized. The first focuses on the selection or neutrality of enzyme polymorphisms, the second on the detection of recombination. Neither method requires phylogeny estimation.     

Optimal traits when there are several costs: the interaction of mortality and energy costs in determining foraging behavior

I analyzed the interaction of different types of costs in determiningoptimal behavior using mathematical models. The analysis concentrateson foraging behavior and asks (1) whether the cost factor thathas the greatest effect on fitness generally has the greatesteffect on optimal trait values and (2) whether increasing thesize of one type of cost makes the optimal behavior absolutelyor relatively more sensitive to that cost. The foraging costsconsidered are energy expenditure, predation risk, and othermortality factors. It is shown that increasing the magnitudeof one cost often decreases the relative and absolute sensitivityof the optimal foraging strategy to that cost. The relativefitness effects of different costs generally differ from therelative sensitivities of the optimal strategies to the costfactors. Researchers should therefore measure the shapes ofcost curves rather than their average magnitudes to determinewhich of several costs can be ignored in cost-benefit analyses.     

Taking movement data to new depths: Inferring prey availability and patch profitability from seabird foraging behavior

Detailed information acquired using tracking technology has the potential to provide accurate pictures of the types of movements and behaviors performed by animals. To date, such data have not been widely exploited to provide inferred information about the foraging habitat. We collected data using multiple sensors (GPS, time depth recorders, and accelerometers) from two species of diving seabirds, razorbills (Alca torda, N = 5, from Fair Isle, UK) and common guillemots (Uria aalge, N = 2 from Fair Isle and N = 2 from Colonsay, UK). We used a clustering algorithm to identify pursuit and catching events and the time spent pursuing and catching underwater, which we then used as indicators for inferring prey encounters throughout the water column and responses to changes in prey availability of the areas visited at two levels: individual dives and groups of dives. For each individual dive (N = 661 for guillemots, 6214 for razorbills), we modeled the number of pursuit and catching events, in relation to dive depth, duration, and type of dive performed (benthic vs. pelagic). For groups of dives (N = 58 for guillemots, 156 for razorbills), we modeled the total time spent pursuing and catching in relation to time spent underwater. Razorbills performed only pelagic dives, most likely exploiting prey available at shallow depths as indicated by the vertical distribution of pursuit and catching events. In contrast, guillemots were more flexible in their behavior, switching between benthic and pelagic dives. Capture attempt rates indicated that they were exploiting deep prey aggregations. The study highlights how novel analysis of movement data can give new insights into how animals exploit food patches, offering a unique opportunity to comprehend the behavioral ecology behind different movement patterns and understand how animals might respond to changes in prey distributions.     

Benefits of recruitment in honey bees: effects of ecology and colony size in an individual-based model

Why do some social insects have sophisticated recruitment systems,while other species do not communicate about food source locationsat all? To answer this question, it is necessary to identifythe social or ecological factors that make recruitment adaptiveand thus likely to evolve. We developed an individual-basedmodel of honey bee foraging to quantify the benefits of recruitmentunder different spatial distributions of nondepleting resourcepatches and with different colony sizes. Benefits of recruitmentwere strongly dependent on resource patch quality, density,and variability. Communication was especially beneficial ifpatches were poor, few, and variable. A sensitivity analysisof the model showed that under conditions of high resource densityrecruitment could even become detrimental, especially if foragingduration was short, tendency to scout was high, or recruitsneeded a long time to find communicated locations. Colony size,a factor often suspected to influence recruitment evolution,had no significant effect. These results may explain the recentexperimental findings that in honey bees, benefits of waggledance recruitment seem to vary seasonally and with habitat.They may also explain why some, but not other, species of socialbees have evolved a strategy to communicate food locations tonest mates.     

Molecular systematics of the caracaras and allies (Falconidae: Polyborinae) inferred from mitochondrial and nuclear sequence data

The Polyborinae is the most diverse subfamily of the Falconidae in terms of both morphology and behaviour, and includes falconet‐shaped birds (Spiziapteryx), arboreal omnivores (Daptrius, Ibycter), as well as terrestrial generalists and scavengers (Caracara, Milvago and Phalcoboenus). The Polyborinae are endemic to the New World, with all but one species (Caracara cheriway) being restricted to Central and South America. Using over 7300 bp of mitochondrial and nuclear sequence data, we aim to clarify the taxonomy and biogeography of the Polyborinae. The genus Milvago was unexpectedly found to be polyphyletic, with Chimango Caracara Milvago chimango being related to the genus Phalcoboenus and Yellow‐headed Caracara Milvago chimachima being sister to Daptrius. Furthermore, very low genetic divergence was found among the four species of the genus Phalcoboenus, with the lowest divergence being between White‐throated Caracara Phalcoboenus albogularis and Mountain Caracara Phalcoboenus megalopterus. Our divergence time analyses revealed that the Polyborinae started to diversify in the Miocene, at about 14 Ma, and that the generalist/scavenger behaviour in the Falconidae appeared between 14 and 6.6 Ma. All speciation events within the caracaras occurred during the Pleistocene. This situation differs from the general pattern described for forest birds, in which most diversification events are older, occurring primarily in the Pliocene and Miocene.     

Tracing horizontal Wolbachia movements among bees (Anthophila): a combined approach using multilocus sequence typing data and host phylogeny

The endosymbiotic bacterium Wolbachia enhances its spread via vertical transmission by generating reproductive effects in its hosts, most notably cytoplasmic incompatibility (CI). Additionally, frequent interspecific horizontal transfer is evident from a lack of phylogenetic congruence between Wolbachia and its hosts. The mechanisms of this lateral transfer are largely unclear. To identify potential pathways of Wolbachia movements, we performed multilocus sequence typing of Wolbachia strains from bees (Anthophila). Using a host phylogeny and ecological data, we tested various models of horizontal endosymbiont transmission. In general, Wolbachia strains seem to be randomly distributed among bee hosts. Kleptoparasite‐host associations among bees as well as other ecological links could not be supported as sole basis for the spread of Wolbachia. However, cophylogenetic analyses and divergence time estimations suggest that Wolbachia may persist within a host lineage over considerable timescales and that strictly vertical transmission and subsequent random loss of infections across lineages may have had a greater impact on Wolbachia strain distribution than previously estimated. Although general conclusions about Wolbachia movements among arthropod hosts cannot be made, we present a framework by which precise assumptions about shared evolutionary histories of Wolbachia and a host taxon can be modelled and tested.     

Intraspecific aggression, colony identity and foraging distances in Sudanese Microtermes spp. (Isoptera: Termitidae: Macrotermitinae)

Abstract. 1. Intraspecific aggression between termite major workers was used to obtain estimates of foraging distances for three Microtermes species in Sudan.
2. Maximum foraging distance recorded for M. sp. nr albopartitus (Sjöstedt) in Khartoum was 11.3 m, giving an estimated minimum colony area of 100 m². This is probably an underestimate. In the Tokar Delta, individuals from single colonies of M. najdensis Harris were encountered up to 42 m apart, giving a colony area of 1390 m².
3. Intraspecific aggression could not be used reliably to distinguish members of different colonies of M. lepidus Sjöstedt. Soil barrier formation between groups of workers in petri dishes may be of use as a supplementary technique, especially for species showing no clear aggression.
4. Experiments on isolated laboratory colonics of M. sp. Nr lepidus Sjöstedt, established from alates collected in Khartoum, further confirmed the value of inter-colony aggression for indicating colony identity.
5. The complications introduced into estimation of subterranean termite foraging areas by overlap and interdigitation of colonies are discussed.     

Characterization of null mutants of the glyoxylate cycle and gluconeogenic enzymes in S. cerevisiae through metabolic network modeling verified by chemostat cultivation.

Biomass yields for several null mutants in Saccharomyces cerevisiae were successfully predicted with a metabolic network model. Energetic parameters of the model were obtained from growth data in C-limited aerobic chemostat cultures of the corresponding wild-type strain, which exhibited a P/O ratio of 1.46, a non-growth-related maintenance of 56 mmol ATP/C-mol biomass/h, and a growth-related requirement of 655 mmol ATP/C-mol biomass. Biomass yields and carbon uptake rates were modeled for different mutants incapacitated in their glyoxylate cycle and their gluconeogenesis. Biomass yields were calculated for different feed ratios of glucose to ethanol, and decreases for higher ethanol fractions were correctly predicted for mutants with deletions of the malate synthase, the isocitrate lyase, or the phosphoenolpyruvate carboxykinase. The growth of the fructose- 1,6-bisphosphatase deletion mutant was anticipated less accurate, but the tendency was modeled correctly.     

Specific and sensitive detection of Nosema bombi (Microsporidia: Nosematidae) in bumble bees (Bombus spp.; Hymenoptera: Apidae) by PCR of partial rRNA gene sequences

A polymerase chain reaction (PCR) based method was developed for the specific and sensitive diagnosis of the microsporidian parasite Nosema bombi in bumble bees (Bombus spp.). Four primer pairs, amplifying ribosomal RNA (rRNA) gene fragments, were tested on N. bombi and the related microsporidia Nosema apis and Nosema ceranae, both of which infect honey bees. Only primer pair Nbombi-SSU-Jf1/Jr1 could distinguish N. bombi (323bp amplicon) from these other bee parasites. Primer pairs Nbombi-SSU-Jf1/Jr1 and ITS-f2/r2 were then tested for their sensitivity with N. bombi spore concentrations from 10(7) down to 10 spores diluted in 100 microl of either (i) water or (ii) host bumble bee homogenate to simulate natural N. bombi infection (equivalent to the DNA from 10(6) spores down to 1 spore per PCR). Though the N. bombi-specific primer pair Nbombi-SSU-Jf1/Jr1 was relatively insensitive, as few as 10 spores per extract (equivalent to 1 spore per PCR) were detectable using the N. bombi-non-specific primer pair ITS-f2/r2, which amplifies a short fragment of approximately 120 bp. Testing 99 bumble bees for N. bombi infection by light microscopy versus PCR diagnosis with the highly sensitive primer pair ITS-f2/r2 showed the latter to be more accurate. PCR diagnosis of N. bombi using a combination of two primer pairs (Nbombi-SSU-Jf1/Jr1 and ITS-f2/r2) provides increased specificity, sensitivity, and detection of all developmental stages compared with light microscopy.     

Female and male Texas cichlids (Herichthys cyanoguttatum) do not fight by the same rules

Selection usually acts differently on males and females duringintrasexual competition for resources and/or mates. Nevertheless,agonistic behavior has been examined both theoretically andempirically mostly in males. Our research questions whethermales and females follow the same rules of engagement in intrasexualcontests as predicted by the sequential assessment model (SAM).The SAM predicts negative correlations between contest intensityand duration and the magnitude of asymmetry in resource holdingpower (RHP) between the contestants, such that the most escalatedcontests are those between similarly endowed individuals. Westaged male and female intrasexual contests with varying degreesof body size asymmetry under a round robin design using themonogamous Texas cichlid fish (Herichthys cyanoguttatum) asa study case. We used Mantel's matrix analysis to compare howthe behavioral content, duration, structure, and outcome ofmale and female contests were affected by the relative bodysize of the contestants. In the case of males, relative sizein each contest predicted outcome, duration, and frequency ofconventional and escalated behaviors according to prevailingtheory. Female contest structure and outcome, however, werenot predicted by the relative size of contestants. We discussour results in terms of other asymmetries that might be importantin structuring female contests, and we propose potential approachesto study female–female aggression.     

The evolution of nocturnal behaviour in sweat bees,Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies?

Evolutionary transitions to dim-light foraging (predawn matinal, crepuscular, nocturnal) have occurred repeatedly in bees, and may be associated with an escape from enemies or competitors. To date, however, little information has been available to test these hypotheses. Here we provide the first detailed information on the nesting behaviour of two species of Neotropical, nocturnal sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae). Females are facultatively social or solitary, and construct nests in dead wood. Nocturnal foraging behaviour is bimodal. Bees began foraging after sunset (∼18:30 h) and ceased foraging approximately 1 h later even though nocturnal flowers with pollen were still abundant; a second foraging bout occurred in the predawn morning, which began at ∼04:45 h and ended around sunrise (∼06:15 h) when diurnal-blooming flowers were abundant. Bees are capable of controlled flight in full light. They utilized pollen from both canopy and understory plant species, which have diurnal or nocturnal pollen anthesis. Megalopta nests are attacked by generalist predators such as ants, as well as the endoparasitic fly Melaloncha sp. nov. (Phoridae), the beetle Macrosaigon gracilis (Rhipophoridae), the parasitic wasp Lophostigma cincta (Mutillidae), and the brood parasite Megalopta byroni (Halictidae). Overall nest survivorship rates were comparable to those for diurnal relatives, but rates of cell parasitism for Megalopta (< < 5%) were substantially lower than they are for day-flying relatives, offering some support for the hypothesis that the evolution of nocturnal behaviour enables escape from natural enemies.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 377–387.     

PseqIP: a nonredundant and exhaustive protein sequence data bank generated from 4 major existing collections

Four major protein sequence data collections (NBRF-PIR, PSD-Kyoto, PGtrans, and NEWAT) have been merged into a single nonredundant data bank called PseqIP. The data bank entries were automatically matched by a heuristic computer program relying on the fast computation of the number of tetrapeptides shared by two sequences. PseqIP 1.0 includes 6,068 different protein sequences for a total of 1,357,067 residues, representing most of the available sequence information to date. During the course of this work, we found about 600 occurrences of a protein sequence recorded with a one-amino-acid variation in at least two different data banks. A flat file (ASCII computer-readable format) version of PseqIP 1.0, well-suited for exhaustive homology searches and statistical sequence analysis, is available from our laboratory.