Foraging by Atta sexdens (Formicidae: Attini): seasonal patterns, caste and efficiency

Abstract. 1. Atta sexdens changes diel periods of foraging, the size of its foraging territory, the numbers and lengths of foraging trails, and its rate of foraging with respect to seasonality in subtropical Paraguay. Leaf loads are significantly larger in warmer months than loads carried in cooler months.
2. Foragers segregate into three labour groups in the field: a small subset climb trees, cut large quantities of vegetation, and drop them to the ground; the second subset of foragers searches out these leaf caches, cut diem into smaller pieces, and carry and deposit the leaf fragments on the foraging trail; the third subset of workers retrieves leaf fragments on the trail and carry them to the nest.
3. Pitfall trapping shows a large degree of patchiness in activity, with media workers dominating the foraging population, more so closer to vegetation which is being harvested.
4. The recovery efficiency of the multi-staged foraging behaviour is estimated to be only 49%, with the recovery of leaf caches near 50%. The impact of A. sexdens may, thus, be twice as great as previous estimates on their herbivory.     

Diel growth patterns of young soybean (Glycine max) leaflets are synchronous throughout different positions on a plant

Leaf growth is controlled by various internal and external factors. Leaves of dicotyledonous plants show pronounced diel (24 h) growth patterns that are controlled by the circadian clock. To date, it is still uncertain whether diel leaf growth patterns remain constant throughout the development of a plant. In this study, we followed growth from the primary leaves to leaflets of the seventh trifoliate leaf of soybean (Glycine max) on the same plants with a recently developed imaging‐based method under controlled conditions and at a high temporal resolution. We found that all leaflets displayed a consistent diel growth pattern with maximum growth towards the end of the night. In some leaves, growth maxima occurred somewhat later – at dawn – as long as the leaves were still in a very early developmental stage. Yet, overall, diel growth patterns of leaves from different positions within the canopy were highly synchronous. Therefore, the diel growth pattern of any leaf at a given point in time is representative for the overall diel growth pattern of the plant leaf canopy and a deviation from the normal diel growth pattern can indicate that the plant is currently facing stress.     

The ‘truck‐driver’ effect in leaf‐cutting ants: how individual load influences the walking speed of nest‐mates

The foraging behaviour of social insects is highly flexible because it depends on the interplay between individual and collective decisions. In ants that use foraging trails, high ant flow may entail traffic problems if different workers vary widely in their walking speed. Slow ants carrying extra‐large loads in the leaf‐cutting ant Atta cephalotes L. (Hymenoptera: Formicidae) are characterized as ‘highly‐laden’ ants, and their effect on delaying other laden ants is analyzed. Highly‐laden ants carry loads that are 100% larger and show a 50% greater load‐carrying capacity (i.e. load size/body size) than ‘ordinary‐laden’ ants. Field manipulations reveal that these slow ants carrying extra‐large loads can reduce the walking speed of the laden ants behind them by up to 50%. Moreover, the percentage of highly‐laden ants decreases at high ant flow. Because the delaying effect of highly‐laden ants on nest‐mates is enhanced at high traffic levels, these results suggest that load size might be adjusted to reduce the negative effect on the rate of foraging input to the colony. Several causes have been proposed to explain why leaf‐cutting ants cut and carry leaf fragments of sizes below their individual capacities. The avoidance of delay in laden nest‐mates is suggested as another novel factor related to traffic flow that also might affect load size selection The results of the presennt study illustrate how leaf‐cutting ants are able to reduce their individual carrying performance to maximize the overall colony performance.     

Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae)

Leaf‐cutter ants (Atta colombica) use trail following to travel between foraging sites and the home nest. However, this combination of pheromone and visual cues is likely to be complemented by a directional reference system such as a compass, used not only when foraging but also during colony formation, where foraging trails degrade or where ants become displaced. One candidate system is the magnetic polarity compass. We tested the orientation of leaf‐cutter ants under a magnetic field of reversed‐polarity, with the prediction that the ants would show 180° deflection compared with control ants in an unchanged geomagnetic field. When the sun's disc was unobstructed by clouds, orientation was the same as that of control ants, implying that magnetic cues were not used to orient. However, when the sky was overcast, ants in the experimental treatment significantly shifted their mean orientation both in comparison with controls and reversed‐polarity ants under the sun. Although a total reversal in orientation was not induced, the results demonstrate that Atta respond to magnetic reversal in the absence of sunlight cues, and suggest a role for magnetic cues in determining direction during orientation.     

Leaf caching in Atta leafcutting ants: discrete cache formation through positive feedback

We examined the occurrence, mechanism and costs and benefits of leaf caching in laboratory colonies of two species of leafcutting ants, Atta cephalotes and A. colombica. If foragers returning to the nest are unable to enter because of a temporary bottleneck caused by leaves building up they may deposit their leaf pieces outside the nest entrance, forming a leaf cache. Similar leaf caches occur in the field at foraging trail junctions, obstacles on the trail and within nest entrance tunnels. Foraging ants carrying leaves were presented with different-sized leaf caches and the number dropping their leaves on the cache was recorded. The probability of a forager dropping her leaf was positively correlated with the size of the cache that she encountered. Therefore, positive feedback played a role in the formation of nest entrance caches. Cached pieces were more likely to be retrieved than noncached pieces but the time taken to retrieve leaf pieces from a cache was greater than from scattered groups of leaves. We suggest that the strategy of flexible nest entrance caching is an adaptive response to fluctuating food availability and collection. Copyright 2000 The Association for the Study of Animal Behaviour.     

β-eudesmol-induced aggression in the leaf-cutting ant Atta sexdens rubropilosa

Leaf‐cutting ants are highly polyphagous insects, but some plants escape their attack due to the presence of secondary metabolites that are toxic to the ant–fungus symbiosis. Previous studies have demonstrated that the terpenoid β‐eudesmol extracted from Eucalyptus species (Myrtaceae) is responsible for the deleterious behavior in colonies of leaf‐cutting ant species. The objective of this study was to evaluate the effect of β‐eudesmol on workers of the leaf‐cutting ant Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae). This chemical caused behavioral modification in the colonies, leading to mutilation and death of workers. It is suggested that β‐eudesmol interferes with colony nestmate recognition. As a consequence, colony cohesion may be disrupted by β‐eudesmol what could be used as an additional control tactic against this important pest ant.     

Phase relations between the circadian leaf movement rhythm and its zeitgeber within the range of entrainment in the cotton plant,Gossypium hirsutum L.

Abstract

The leaf movement rhythm of Gossypium hirsutum L. (cv. Lakshmi) could be entrained to 24 h LD cycles with different photofractions varying from 4 to 20 h such that the night peak position of the rhythm occurred during darkness. The phase angle (ψ) of the rhythm varied in a regular manner with different photoperiods of a 24 h LD cycle. Under 24 h LD cycles with different photoperiods, the leaf movement shows probable evidences for the concurrent participation of a ‘light‐on’ and ‘light‐off rhythm.     

Quality versus quantity: Foraging decisions in the honeybee (Apis mellifera scutellata) feeding on wildflower nectar and fruit juice

Foraging animals must often decide among resources which vary in quality and quantity. Nectar is a resource that exists along a continuum of quality in terms of sugar concentration and is the primary energy source for bees. Alternative sugar sources exist, including fruit juice, which generally has lower energetic value than nectar. We observed many honeybees (Apis mellifera scutellata) foraging on juice from fallen guava (Psidium guajava) fruit near others foraging on nectar. To investigate whether fruit and nectar offered contrasting benefits of quality and quantity, we compared honeybee foraging performance on P. guajava fruit versus two wildflowers growing within 50 m, Richardia brasiliensis and Tridax procumbens. Bees gained weight significantly faster on fruit, 2.72 mg/min, than on either flower (0.17 and 0.12 mg/min, respectively). However, the crop sugar concentration of fruit foragers was significantly lower than for either flower (12.4% vs. 37.0% and 22.7%, respectively). Fruit foragers also spent the most time handling and the least time flying, suggesting that fruit juice was energetically inexpensive to collect. We interpret honeybee foraging decisions in the context of existing foraging models and consider how nest‐patch distance may be a key factor for central place foragers choosing between resources of contrasting quality and quantity. We also discuss how dilute solutions, such as fruit juice, can help maintain colony sugar–water balance. These results show the benefits of feeding on resources with contrasting quality and quantity and that even low‐quality resources have value.     

Hitchhiking and the removal of microbial contaminants by the leaf‐cutting ant Atta colombica

1. The ecologically dominant leaf‐cutting ants exhibit one of the most complex forms of morphological caste‐based division of labour in order to efficiently conduct tasks, ranging from harvesting fresh leaf material to caring for the vulnerable fungal crop they farm as food. While much of their division of labour is well known, the role of the smallest workers on foraging trails is puzzling. Frequently these minim workers hitchhike on leaf fragments and it has been suggested that they may act to reduce the microbial contamination of leaf material before they enter the nest. Here we investigated this potentially important role of minims with field colonies of Atta colombica. 2. We experimentally increased the microbial load of leaf fragments and found that this resulted in minims hitchhiking on leaf fragments for longer. Furthermore, we show that leaves naturally have a significant microbial load and that the presence of hitchhikers reduces the microbial load of both experimentally manipulated and natural leaf fragments. 3. Intriguingly, the microbial load of leaves high in the canopy where ants were foraging was much lower than closer to the ground where the ants avoided cutting leaves. This suggests that the often perplexing foraging patterns of leaf‐cutting ants may in part be explained by the ants avoiding leaves that are more heavily contaminated with microbes. 4. The removal of microbial contaminants is therefore an important role of hitchhiking minim workers in natural colonies of Atta leaf‐cutting ants, although other tasks such as trail maintenance and defence also explain their occurrence on trails.     

Foraging activity of leaf‐cutting ants changes light availability and plant assemblage in Atlantic forest

1. Leaf‐cutting ants (LCAs) have often been denoted as ecosystem engineers because of their multifarious effects on the vegetation, particularly via nest‐driven environmental changes. However, the non‐trophic impacts of LCAs on forest dynamics via foliage harvesting across sizeable foraging zones (so‐called associated ecosystem engineering) are still poorly investigated. 2. Here, light availability and sapling assemblages were assessed within foraging areas and ant‐free control zones of 16 Atta cephalotes colonies located in a large remnant of Atlantic forest in northeastern Brazil. 3. Canopy openness and total light transmission were 1.4 and 1.6 times higher in foraging zones than in control areas. In parallel, sapling density and species richness decreased constantly from control to foraging zone plots. Additionally, shade‐tolerant species exhibited reduced abundance across foraging zones. A non‐metric multidimensional scaling ordination based on taxonomic similarity primarily segregated foraging zone and control plots; foraging zone plots converged to be more similar to each other as well. Finally, some plant species emerged as indicators of LCA‐free zones. 4. These results suggest that LCA foraging activity in the forest canopy directly increases the light availability and indirectly affects the recruitment and the structure of local plant assemblages. 5. Such a biologically significant effect on the light environment and its cascades confirms LCAs as potent ecosystem engineers, particularly as a plant assembly force, which operates beyond the spatial reach of their well‐described nest effects.     

Tradeoff Between Travel Speed and Olfactory Food Detection in Ring‐Tailed Coatis (Nasua nasua)

The distance at which an animal can detect food has important ramifications for foraging behavior. Although some studies have investigated the factors which affect visual food detection, very little is known about what influences olfactory food detection abilities in wild animals. The food discovery behavior of ring‐tailed coatis (Nasua nasua) was studied using experimental fruit plots. Coatis primarily used olfaction to detect these new food sources, and visual food discovery appeared plausible in only five of 148 trials. Coatis detected the fruit from longer distances when traveling compared with when foraging for invertebrates in the leaf litter. Travel speed had a negative effect on discovery distance. Coatis traveling slowly detected the fruit plots from further away, which demonstrated a tradeoff between speed and food detection. If this tradeoff is biologically important, slower groups should have visited more fruit trees per day, so data taken during full‐day coati group follows were analyzed to determine whether this pattern occurred. Slower moving groups visited more fruit trees than faster groups once confounding factors such as daily travel distance, group identity, group spread, and year were controlled for. These results are consistent with the hypothesis that coatis exhibit a speed‐accuracy tradeoff for olfactory food detection. This tradeoff appears to be an important factor influencing the movement ecology of animal groups.     

Long-term temporal changes of plant phenology in the Western Mediterranean

Plants are altering their life cycles in response to current climatic change around the globe. More than 200 000 records for six phenological events (leaf unfolding, flowering, fruit ripening, fruit harvesting, leaf falling and growing season) of 29 perennial species for the period 1943–2003 recorded throughout Spain provide the longest temporal and the broadest spatial assessment of plant phenology changes in the Mediterranean region. The overwhelming majority of the 118 studied phenophases shifted their dates in recent decades. Such changes differed among phenological events. Leaf unfolding, flowering and fruiting are markedly advancing (?0.48, ?0.59 and ?0.32 days yr^?1, respectively), but only since the mid‐1970s. Anemophilous have advanced more days their flowering than entomophilous. However, some species have delayed and others have advanced their leaf falling dates and as a result only a weak shift was observed in this event for the whole of the studied species (+0.12 days yr^?1). The growing season lengthened by 18 days, which implies an increase of 8% in the life of annual leaves. Such an increase was achieved mainly through the advance of leaf unfolding dates in the spring, one of the most productive times of year for vegetation in the Mediterranean. Shifts in the plant calendar were accompanied as well by long‐term changes in the range of onset dates in 39% of studied phenophases. Leaf unfolding, flowering and growing season tended to reduce spatial variability, reflecting a faster and more synchronized onset (or duration) of phenophases across the study area. Changes in spatial variability may aggravate calendar mismatching with other trophic levels resulting from changes in dates. Because temporal responses differed markedly among species, calendar guilds of plants have changed, which suggests alterations of interspecific relationships in plant communities from Mediterranean ecosystems.     

Seed hoarding by rodents of the Monte Desert,Argentina

Food storage is an important adaptation of several animal species to the temporally variable or unpredictable food supplies that are typical of desert environments. In the present study, whether Eligmodontia typus and Graomys griseoflavus inhabiting sand dunes in the Monte desert displayed scatter‐hoarding was investigated. Both rodent species prepared surface caches by digging small holes (1–3 cm deep) in the soil. Caches were partially covered with sand and dry leaves, which meant that all of the cache sites at each station could be found. Most caches were found below shrubs, that is, in a sheltered microhabitat rather than near the food source. The mean distance between caches and seed sources was significantly higher than the mean distance from food sources to shrubs. The proportion of caches was significantly higher in shrubs with high safety cover. The adaptive significance of this foraging behaviour could be a competitive tactic for the rapid sequestering of food from a rich and ephemeral source. Such behaviour would reflect predation risk, which constitutes an important foraging cost in deserts, and could also influence plant community dynamics.     

Extent of mismatch between the period of circadian clocks and light/dark cycles determines time‐to‐emergence in fruit flies

Circadian clocks time developmental stages of fruit flies Drosophila melanogaster, while light/dark (LD) cycles delimit emergence of adults, conceding only during the “allowed gate.” Previous studies have revealed that time‐to‐emergence can be altered by mutations in the core clock gene period (per), or by altering the length of LD cycles. Since this evidence came from studies on genetically manipulated flies, or on flies maintained under LD cycles with limited range of periods, inferences that can be drawn are limited. Moreover, the extent of shortening or lengthening of time‐to‐emergence remains yet unknown. In order to pursue this further, we assayed time‐to‐emergence of D. melanogaster under 12 different LD cycles as well as in constant light (LL) and constant dark conditions (DD). Time‐to‐emergence in flies occurred earlier under LL than in LD cycles and DD. Among the LD cycles, time‐to‐emergence occurred earlier under T4–T8, followed by T36–T48, and then T12–T32, suggesting that egg‐to‐emergence duration in flies becomes shorter when the length of LD cycles deviates from 24 h, bearing a strong positive and a marginally negative correlation with day length, for values shorter and longer than 24 h, respectively. These results suggest that the extent of mismatch between the period of circadian clocks and environmental cycles determines the time‐to‐emergence in Drosophila.     

GPS tracking of the foraging movements of Manx Shearwaters Puffinus puffinus breeding on Skomer Island, Wales

We report the first successful use of miniature Global Positioning System loggers to track the ocean‐going behaviour of a c. 400 g seabird, the Manx Shearwater Puffinus puffinus. Breeding birds were tracked over three field seasons during the incubation and chick‐rearing periods on their foraging excursions from the large colony on Skomer Island, Pembrokeshire, UK. Foraging effort was concentrated in the Irish Sea. Likely foraging areas were identified to the north, and more diffusely to the west of the colony. No foraging excursions were recorded significantly to the south of the colony, conflicting with the conclusions of earlier studies based on ringing recoveries and observations. We discuss several explanations including the hypothesis that foraging may have shifted substantially northwards in recent decades. We found no obvious relationship between birds’ positions and water depth, although there was a suggestion that observations at night were in shallower water than those during the day. We also found that, despite the fact that Shearwaters can be observed rafting off‐shore from their colonies in the hours prior to making landfall at night, breeding birds are usually located much further from the colony in the last 8 h before arrival, a finding that has significance for the likely effectiveness of marine protection areas if they are only local to the colony. Short sequences of precise second‐by‐second fixes showed that movement speeds were bimodal, corresponding to sitting on the water (most common at night and around midday) and flying (most common in the morning and evening), with flight behaviour separable into erratic (indicative of searching for food) and directional (indicative of travelling). We also provide a first direct measurement of mean flight speed during directional flight (c. 40 km/h), slower than a Shearwater's predicted maximum range velocity, suggesting that birds are exploiting wave or dynamic soaring during long‐distance travel.     

Comparative proteomics reveal characteristics of life-history transitions in a social insect

Background  

Honey bee (Apis mellifera) workers are characterized by complex social behavior. Their life-history is dominated by a period of within-nest activity followed by a phase of long-distance flights and foraging. General insights into insect metabolism imply that foraging onset is associated with fundamental metabolic changes, and theory on social evolution suggests metabolic adaptations that are advantageous for the colony as a whole.     

Environmental heterogeneity amplifies behavioural response to a temporal cycle

Resource acquisition is integral to maximise fitness, however in many ecosystems this requires adaptation to resource abundance and distributions that seldom stay constant. For predators, prey availability can vary at fine spatial and temporal scales as a result of changes in the physical environment, and therefore selection should favour individuals that can adapt their foraging behaviour accordingly. The tidal cycle is a short, yet predictable, temporal cycle, which can influence prey availability at temporal scales relevant to movement decisions. Here, we ask whether black‐legged kittiwakes Rissa tridactyla can adjust their foraging habitat selection according to the tidal cycle using GPS tracking studies at three sites of differing environmental heterogeneity. We used a hidden Markov model to classify kittiwake behaviour, and analysed habitat selection during foraging. As expected for a central‐place forager, we found that kittiwakes preferred to forage nearer to the breeding colony. However, we also show that habitat selection changed over the 12.4‐h tidal cycle, most likely because of changes in resource availability. Furthermore, we observed that environmental heterogeneity was associated with amplified changes in kittiwake habitat selection over the tidal cycle, potentially because environmental heterogeneity drives greater resource variation. Both predictable cycles and environmental heterogeneity are ubiquitous. Our results therefore suggest that, together, predictable cycles and environmental heterogeneity may shape predator behaviour across ecosystems.     

Individual complexity and self-organization in foraging by leaf-cutting ants

Leaf-cutting ants cut vegetation into small fragments that they transport to the nest, where a symbiotic fungus cultivated by the ants processes the material. Since the harvested leaf fragments are incorporated into the fungus garden and not directly consumed by the workers, it is expected that foraging workers select plants by responding to those physical or chemical traits that promote maximal fungal growth, irrespective of the potential direct effects of these leaf features on them. In this paper I summarize experimental work focusing on the decision-making processes that occur at the individual level, and discuss to what extent individual complexity contributes to the emergence of collective foraging patterns. Although some basic features of self-organizing systems, such as the existence of regulatory positive and negative feedback loops, are expected to be involved in the collective organization of leaf-cutting ant foraging, I contend that they are combined with complex individual responses that may result from the integration of local information during food collection with an assessment of colony conditions.     

Production of greenhouse tomatoes (Lycopersicon esculentum) using Nannotrigona perilampoides, Bombus impatiens and mechanical vibration (Hym.: Apoidea)

Importation of exotic bumblebees for greenhouse pollination may be restricted in México, thus making it necessary to evaluate the potential of native species as pollinators in enclosures. We studied the foraging activity and fruit production of tomato using one colony of Nannotrigona perilampoides (NP) and one colony of Bombus impatiens (BI) in greenhouses with ≈1000 plants. Mechanical vibration (MV) was included as a test treatment. The foraging activity was measured as the number of flowers visited within 5 min, the time spent on a flower collecting pollen, the number of visits that a flower received and the duration of a foraging trip. BI collected pollen more rapidly, visited more flowers within 5 min and did more visits per flower when compared with NP that also lasted longer in their trips. Significant correlations were found between environmental variables and the number of bees entering the hive and the number of bees on the flowers. For NP, the highest correlation was found for light intensity whilst in BI a negative effect of environmental temperature was detected. Regarding the quantity of fruit, BI resulted in higher fruit set when compared with NP, but the latter performed similarly to MV. However, the weight of the fruit and seed number was significantly higher for BI when compared with NP, and this was higher than for MV. Our results demonstrate that at the densities of tomato plants tested, one colony of BI was more efficient pollinator when compared with NP. We suggest that pollination efficiency of NP could have been limited by a reduced number of foragers on the plants at a given time and their limited flight range when compared with BI. Therefore, it will be necessary to evaluate if increasing densities of colonies of NP could improve tomato yield in tropical greenhouses.     

Influence of leaf herbivory,root herbivory,and pollination on plant performance in Cucurbita moschata

Abstract 1. Plants experience herbivory on many different tissues that can affect reproduction directly by damaging tissues and decreasing resource availability, or indirectly via interactions with other species such as pollinators. 2. This study investigated the combined effects of leaf herbivory, root herbivory, and pollination on subsequent damage, pollinator preference, and plant performance in a field experiment using butternut squash (Cucurbita moschata). Leaf and root herbivory were manipulated using adult and larval striped cucumber beetles (Acalymma vittatum F.), a cucurbit specialist. 3. Leaf herbivory reduced subsequent pistillate floral damage and powdery mildew (Sphaerotheca fuliginea) infection. In spite of these induced defences, the overall effect of leaf herbivory on plant reproduction was negative. Leaf herbivory reduced staminate flower production, fruit number, and seed weight. In contrast, root herbivory had a minimal impact on plant reproduction. 4. Neither leaf nor root herbivory altered pollinator visitation or floral traits, suggesting that reductions in plant performance from herbivory were as a result of direct rather than indirect effects. In addition, no measured aspect of reproduction was pollen limited. 5. Our study reveals that although leaf herbivory by the striped cucumber beetle can protect against subsequent damage, this protection was not enough to prevent the negative impacts on plant performance.