Optimal foraging constrains macroecological patterns: body size and dietary niche breadth in lizards

Aim  To explore and identify probable mechanisms contributing to the relationships among body size, dietary niche breadth and mean, minimum, maximum and range of prey size in predaceous lizards.
Location  Our data set includes species from tropical rainforests, semi-arid regions of Brazil, and from deserts of the south-western United States, Australia and the Kalahari of Africa.
Methods  We calculated phylogenetic and non-phylogenetic regressions among predator body size, dietary breath and various prey size measures.
Results  We found a negative association between body size and dietary niche breadth in 159 lizard species sampled across most evolutionary lineages of squamate reptiles and across major continents and habitats. We also show that mean, minimum, maximum and range of prey size were positively associated with body size.
Main conclusions  Our results suggest not only that larger lizards tend to eat larger prey, but in doing so offset their use of smaller prey. Reduction of dietary niche breadth with increased body size in these lizards suggests that large predators target large and more profitable prey. Consequently, the negative association between body size and niche breadth in predators most likely results from optimal foraging. Though this result may appear paradoxical and runs counter to previous studies, resources for predators may be predictably more limited than resources for herbivores, thus driving selection for more profitable prey.     

Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus)

1. Digital tags were used to describe diving and vocal behaviour of sperm whales during 198 complete and partial foraging dives made by 37 individual sperm whales in the Atlantic Ocean, the Gulf of Mexico and the Ligurian Sea. 2. The maximum depth of dive averaged by individual differed across the three regions and was 985 m (SD = 124.3), 644 m (123.4) and 827 m (60.3), respectively. An average dive cycle consisted of a 45 min (6.3) dive with a 9 min (3.0) surface interval, with no significant differences among regions. On average, whales spent greater than 72% of their time in foraging dive cycles. 3. Whales produced regular clicks for 81% (4.1) of a dive and 64% (14.6) of the descent phase. The occurrence of buzz vocalizations (also called 'creaks') as an indicator of the foraging phase of a dive showed no difference in mean prey capture attempts per dive between regions [18 buzzes/dive (7.6)]. Sperm whales descended a mean of 392 m (144) from the start of regular clicking to the first buzz, which supports the hypothesis that regular clicks function as a long-range biosonar. 4. There were no significant differences in the duration of the foraging phase [28 min (6.0)] or percentage of the dive duration in the foraging phase [62% (7.3)] between the three regions, with an overall average proportion of time spent actively encountering prey during dive cycles of 0.53 (0.05). Whales maintained their time in the foraging phase by decreasing transit time for deeper foraging dives. 5. Similarity in foraging behaviour in the three regions and high diving efficiencies suggest that the success of sperm whales as mesopelagic predators is due in part to long-range echolocation of deep prey patches, efficient locomotion and a large aerobic capacity during diving.     

It is time to move: linking flight and foraging behaviour in a diving bird

Although the adaptive value of flight may seem obvious, it is the most difficult behaviour of birds to monitor. Here, we describe a technique to quantify the frequency and the duration of flights over several months by implanting a data logger that records heart rate (fH), hydrostatic pressure (diving depth) and the body angle of a large sea duck species, the common eider (Somateria mollissima). According to the mean fH recorded during flight and the parameters recorded to identify the fH flight signature, we were able to identify all flights performed by 13 individuals during eight months. We cumulated local flight time (outside migrations) and found that activity occurs primarily during dawn and morning and that flying activities are strongly related to diving activities (Pearson's r=0.88, permutation test p<0.001). This relationship was interpreted as a consequence of living in a dynamic environment where sea currents move the ducks away from the food patches. We believe that the technique described here will open new avenues of investigation in the adaptive value of flight.     

The influence of preceding dive cycles on the foraging decisions of Antarctic fur seals

The foraging strategy of many animals is thought to be determined by their past experiences. However, few empirical studies have investigated whether this is true in diving animals. We recorded three-dimensional movements and mouth-opening events from three Antarctic fur seals during their foraging trips to examine how they adapt their behaviour based on past experience—continuing to search for prey in the same area or moving to search in a different place. Each dive cycle was divided into a transit phase and a feeding phase. The linear horizontal distance travelled after feeding phases in each dive was affected by the mouth-opening rate during the previous 244 s, which typically covered two to three dive cycles. The linear distance travelled tended to be shorter when the mouth-opening rate in the previous 244 s was higher, i.e. seals tended to stay in the same areas with high prey-encounter rates. These results indicate that Antarctic fur seals follow decision-making strategies based on the past foraging experience over time periods longer than the immediately preceding dive.     

Nectar foraging behaviour is affected by ant body size in Camponotus mus

The nectivorous ant Camponotus mus shows a broad size variation within the worker caste. Large ants can ingest faster and larger loads than small ones. Differences in physiological abilities in fluid ingestion due to the insect size could be related to differences in decision-making according to ant size during nectar foraging. Sucrose solutions of different levels of sugar concentration (30% or 60%w/w), viscosity (high or low) or flow rate (ad libitum or 1microl/min) were offered in combination to analyse the behavioural responses to each of these properties separately. Differences were found depending on ant body size and the property compared. A regulated flow produced smaller crop loads for medium and large ants compared to the same solution given ad libitum. All foragers remained longer times feeding at the regulated flow source but larger ants often made longer interruptions. When sugar concentration was constant but viscosity was high, only large ants increased feeding time. Constant viscosity with different sugar concentration determined longer feeding time and bigger loads for the most concentrated solution for small but not for large ants. Small ants reached similar crop loads in a variety of conditions while large ants did not. These differences could be evidence of a possible specialization for nectar foraging based on ant body size.     

Thermal and digestive constraints to foraging behaviour in marine mammals

While foraging models of terrestrial mammals are concerned primarily with optimizing time/energy budgets, models of foraging behaviour in marine mammals have been primarily concerned with physiological constraints. This has historically centred on calculations of aerobic dive limits. However, other physiological limits are key to forming foraging behaviour, including digestive limitations to food intake and thermoregulation. The ability of an animal to consume sufficient prey to meet its energy requirements is partly determined by its ability to acquire prey (limited by available foraging time, diving capabilities and thermoregulatory costs) and process that prey (limited by maximum digestion capacity and the time devoted to digestion). Failure to consume sufficient prey will have feedback effects on foraging, thermoregulation and digestive capacity through several interacting avenues. Energy deficits will be met through catabolism of tissues, principally the hypodermal lipid layer. Depletion of this blubber layer can affect both buoyancy and gait, increasing the costs and decreasing the efficiency of subsequent foraging attempts. Depletion of the insulative blubber layer may also increase thermoregulatory costs, which will decrease the foraging abilities through higher metabolic overheads. Thus, an energy deficit may lead to a downward spiral of increased tissue catabolism to pay for increased energy costs. Conversely, the heat generated through digestion and foraging activity may help to offset thermoregulatory costs. Finally, the circulatory demands of diving, thermoregulation and digestion may be mutually incompatible. This may force animals to alter time budgets to balance these exclusive demands. Analysis of these interacting processes will lead to a greater understanding of the physiological constraints within which the foraging behaviour must operate.     

The diving behaviour of the Manx Shearwater Puffinus puffinus

The diving capabilities of the Procellariformes remain the least understood component of avian diving physiology. Due to their relatively small size, shearwaters may have high oxygen consumption rates during diving relative to their available oxygen stores. Dive performance in this group should be strongly limited by the trade‐off between oxygen consumption and oxygen stores, and shearwaters could be a good model group for testing predictions of dive theory. Many earlier measurements of shearwater dive behaviour relied on observations from the surface or potentially biased technology, and it is only recently that diving behaviour has been observed using electronic recorders for many of the clades within the family. The diving behaviour of Manx Shearwaters Puffinus puffinus breeding in Wales, UK, was studied on a large sample of birds using time–depth–temperature recorders deployed on chick‐rearing shearwaters in July and August over 3 years (2009–2011). Light availability apparently limited diving as dives only occurred between 04:00 and 19:00 h GMT. All individuals routinely dived deeper than traditionally assumed, to a mean maximum depth of 31 m and occasionally down to nearly 55 m. We compiled all available data for a comparison of the dive depth across shearwater species. There was a positive allometric relationship between maximum dive depth and body mass across Puffinus and Ardenna shearwater species, as expected, but only if samples of fewer than two individuals were excluded. The large intra‐specific range in maximum dive depth in our study illustrates that apparent diversity in diving performance across species must be interpreted cautiously.     

Assessment of scale-dependent foraging behaviour in southern elephant seals incorporating the vertical dimension: a development of the First Passage Time method

1. Identifying the spatial scales at which top marine predators forage is important for understanding oceanic ecosystems. Several methods quantify how individuals concentrate their search effort along a given path. Among these, First-Passage Time (FPT) analysis is particularly useful to identify transitions in movement patterns (e.g. between searching and feeding). This method has mainly been applied to terrestrial animals or flying seabirds that have little or no vertical component to their foraging, so we examined the differences between classic FPT and a modification of this approach using the time spent at the bottom of a dive for characterizing the foraging activity of a diving predator: the southern elephant seal. 2. Satellite relayed data loggers were deployed on 20 individuals during three successive summers at the Kerguelen Islands, providing a total of 72 978 dives from eight juvenile males and nine adult females. 3. Spatial scales identified using the time spent at the bottom of a dive ( = 68.2 +/- 42.1 km) were smaller than those obtained by the classic FPT analysis ( = 104.7 +/- 67.3 km). Moreover, foraging areas identified using the new approach clearly overlapped areas where individuals increased their body condition, indicating that it accurately reflected the foraging activity of the seals. 4. These results suggest that incorporating the vertical dimension into FPT provides a different result to the surface path alone. Close to the Antarctic continent, within the pack-ice, sinuosity of the path could be explained by a high sea-ice concentration (restricting elephant seal movements), and was not necessarily related to foraging activity. 5. Our approach distinguished between actual foraging activity and changes in behaviour induced by the physical environment like sea ice, and could be applied to other diving predators. Inclusion of diving parameters appears to be essential to identify the spatial scale of foraging areas of diving animals.     

Slug foraging behaviour: Attraction to food items from a distance

Slug foraging paths recorded using time lapse video techniques under infra-red light were fitted to a correlated random walk model. Analyses were carried out on slugs in arenas where no food was present, as well as those containing commercial molluscicides at two rates of application. Slugs were found to search randomly in empty arenas and those containing commercial metaldehyde baits, but deviated from random search patterns when in the presence of commercial methiocarb bait. Differential attraction from a distance is suggested as a cause of these differences.     

Consequences of climate and body size on the foraging performance of seed‐eating ants

1. Changes in climatic factors could have major effects on the foraging performance of animals. To date, however, no study has attempted to examine the concurrent effect of different climatic factors on foraging performance of individual organisms. 2. In the present study, this issue was addressed by studying changes in foraging performance of seed‐eating ant colonies of the genus Messor in response to variation in precipitation and ambient temperature along a macroecological gradient. In addition, we examined the way three colony‐level attributes, foraging distance, forager number, and variance in worker‐size, could affect foraging performance in those ants. Foraging performance was measured as size matching, i.e. the correlation between forager size and load size. The study was carried out for 2 years in six sites along a south‐north productivity gradient in a semi‐arid region of the Eastern‐Mediterranean. 3. Size matching increased with increased precipitation as well as with an increase in worker‐size variability, but slightly decreased with increasing temperatures, as predicted by foraging‐decision models. In contrast, foraging distance had no effect on size matching. Interestingly, size matching showed a unimodal relationship with forager number. 4. These results indicate that interplay between climate and body size affects foraging performance either directly via physiological constraints, or indirectly through their effect on food availability. Moreover, this is one of the first evidences to support the assumption that ant colonies can differ in their ability to optimally allocate their workforce in natural environments. This emphasises the importance of studying the way foraging strategies vary across environmental gradients at macroecological scales.     

Field studies of foraging behaviour of an intertidal beetle

Abstract. 1. Adult staphylinid beetles Thinopinus pictus LeC. are noct turnal predators of sand beach amphipods, Orchestoidea califomiana (Brandt). I made continuous observations of Thinopinus near the drift patches on which amphipods feed.
2. Thinopinus alternated between active and ambush foraging modes.
3. Thinopinus had greater attack rates and captured smaller amphipods while in active foraging mode.
4. Thinopinus attacked 0.147 amphipods/min, and captured 9.1% of the amphipods attacked. The attack rate on amphipods increased with the proportion of time spent by Thinopinus in active mode.
5. Thinopinus remained longer near types of drift patches which were more attractive to amphipods.     

Biomechanics and foraging profitability: an approach to assessing trophic needs and impacts of diving ducks

A biomechanical model of underwater locomotion is described, and data required by the model presented for 3 species of diving duck (Aythya spp.). Based on field observations of behavior and foods consumed, the model is used to estimate energy costs of foraging and minimum food intake rates of canvasbacks (Aythya valisineria) in two habitats in North Carolina. Increased water depth from 0.5 m in Lake Mattamuskeet to 1.5 m in Pamlico Sound increased the net cost of time spent foraging at the bottom by 43%. Biomechanical calculations are combined with data on intake rates at different food densities (Takekawa, 1987) to determine minimum food densities for profitable foraging in Lake Mattamuskeet. Field observations of behavior are used to adjust minimum intake per dive for unsuccessful dives spent locating food patches. Density and dispersion of plant tuber foods in Lake Mattamuskeet, before and after the fall staging period, suggest that the fraction of habitat with tuber densities above a profitability threshold is more critical to canvasbacks than average tuber density. Such factors are important in relating bird energy requirements and benthic sampling data to carrying capacity and total area of usable habitat. The proportion of foods that can be fed upon profitably also determines the fraction of food organisms subject to depletion as components of trophic pathways.     

Optimum body size in aphids

Abstract.

• 1 Smallness in British plant-sucking bugs is associated with feeding on the contents of individual plant cells, especially phloem.
• 2 The sizes of species of aphids living in similar habitats and the rates of water loss from those that have and lack a filter chamber do not support the contention that small size in aphids is a means of maximizing the loss of water by cuticular transpiration.
• 3 An optimum energy partitioning model, previously developed for aphids, was used to predict the interspecifie relation between adult weight and birth weight that would maximize the population growth rate, r_m. Using the observed r_m/IRGR ratio (0.8–0.9) and that the gonads are smaller than the soma at birth the predicted relation between the logarithm of the adult weight and the logarithm of the birth weight is linear and has a slope of 1.
• 4 The relation between the logarithm of the adult weight and the logarithm of the birth weight for eighteen species of aphids is linear and has a slope of 1.
• 5 Birth size differs between species of aphids and in each species is assumed to be the minimum size necessary for feeding. Accepting this constraint then the optimum adult size for maximizing r_m is approximately 15 times the birth size.

     

Early diving behaviour in juvenile penguins: improvement or selection processes

The early life stage of long-lived species is critical to the viability of population, but is poorly understood. Longitudinal studies are needed to test whether juveniles are less efficient foragers than adults as has been hypothesized. We measured changes in the diving behaviour of 17 one-year-old king penguins Aptenodytes patagonicus at Crozet Islands (subantartic archipelago) during their first months at sea, using miniaturized tags that transmitted diving activity in real time. We also equipped five non-breeder adults with the same tags for comparison. The data on foraging performance revealed two groups of juveniles. The first group made shallower and shorter dives that may be indicative of early mortality while the second group progressively increased their diving depths and durations, and survived the first months at sea. This surviving group of juveniles required the same recovery durations as adults, but typically performed shallower and shorter dives. There is thereby a relationship between improved diving behaviour and survival in young penguins. This long period of improving diving performance in the juvenile life stage is potentially a critical period for the survival of deep avian divers and may have implications for their ability to adapt to environmental change.     

Nutrient balance affects foraging behaviour of a trap-building predator

Predator foraging may be affected by previous prey capture, but it is unknown how nutrient balance affects foraging behaviour. Here, we use a trap-building predator to test whether nutrients from previous prey captures affect foraging behaviour. We fed orb-weaving spiders (Zygiella x-notata) prey flies of different nutrient composition and in different amounts during their first instar and measured the subsequent frequency of web building and aspects of web architecture. We found that both the likelihood of web building and the number of radii in the web were affected by prey nutrient composition while prey availability affected capture area and mesh height. Our results show that both the balance of nutrients in captured prey and the previous capture rate may affect future foraging behaviour of predators.     

Empirical evidence for an optimal body size in snakes

Abstract The concept of optimal size has been invoked to explain patterns in body size of terrestrial mammals. However, the generality of this phenomenon has not been tested with similarly complete data from other taxonomic groups. In this study we describe three statistical patterns of body size in snakes, all of which indicate an optimal length of 1.0 m. First, a distribution of largest body lengths of 618 snake species had a single mode at 1.0 m. Second, we found a positive relationship between the size of the largest member of an island snake assemblage and island area and a negative relationship between the size of the smallest member of an island snake assemblage and island area. Best-fit lines through these data cross at a point corresponding to 1.0 m in body length, the presumed optimal size for a one-species island. Third, mainland snake species smaller than 1.0 m become larger on islands whereas those larger than 1.0 m become smaller on islands. The observation that all three analyses converge on a common body size is concordant with patterns observed in mammals and partial analyses of four other disparate animal clades. Because snakes differ so strikingly from mammals (ectotherms, gape-limited predators, elongate body shape) the concordant patterns of these two groups provide strong evidence for the evolution of an optimal body size within independent monophyletic groups. However, snakes differ from other taxonomic groups that have been studied in exhibiting a body size distribution that is not obviously skewed in either direction. We suggest that idiosyncratic features of the natural history of ectotherms allow relatively unconstrained distributions of body size whereas physiological limitations of endotherms constrain distributions of body size to a right skew.