Prey Target Research Articles

Evolution of Three-Finger Toxin Genes in Neotropical Colubrine Snakes (Colubridae).

Snake venom research has historically focused on front-fanged species (Viperidae and Elapidae), limiting our knowledge of venom evolution in rear-fanged snakes across their ecologically diverse phylogeny. Three-finger toxins (3FTxs) are a known neurotoxic component in the venoms of some rear-fanged snakes (Colubridae: Colubrinae), but it is unclear how prevalent 3FTxs are both in expression within venom glands and more broadly among colubrine species. Here, we used a transcriptomic approach to characterize the venom expression profiles of four species of colubrine snakes from the Neotropics that were dominated by 3FTx expression (in the genera Chironius, Oxybelis, Rhinobothryum, and Spilotes). By reconstructing the gene trees of 3FTxs, we found evidence of putative novel heterodimers in the sequences of Chironius multiventris and Oxybelis aeneus, revealing an instance of parallel evolution of this structural change in 3FTxs among rear-fanged colubrine snakes. We also found positive selection at sites within structural loops or "fingers" of 3FTxs, indicating these areas may be key binding sites that interact with prey target molecules. Overall, our results highlight the importance of exploring the venoms of understudied species in reconstructing the full evolutionary history of toxins across the tree of life.

Investigation of the Dietary Preferences of Two Dorid Nudibranchs by Feeding-Choice Experiments and Chemical Analysis

Feeding-choice experiments were conducted under laboratory conditions with two dorid spongivorous nudibranchs, Goniobranchus aureomarginatus and Ceratosoma amoenum, collected from a sponge meadow off Tauranga, New Zealand with two sponge prey (Dysidea teawanui sp.nov. and an undescribed species from the Dictyodendrillidae family, possibly Dictyodendrilla tenella (Lendenfeld 1888). The first choice of prey, the total number of prey choices made, and the time spent on each prey target was recorded, results indicating that each nudibranch had strong preferences for specific prey species. Preferences were significant when the time spent grazing on prey was taken into consideration. Goniobranchus aureomarginatus had a strong preference for the undescribed Dictyodendrillid sponge, while Ceratosoma ameonum preferred Dysidea teawanui. The results of the feeding-choice experiments matched observations in the wild. Chemical analysis of the undescribed Dictyodendrillid sponge led to the isolation and characterisation of six known bioactive metabolites, dictyodendrin C (1), D (2) and F (3), as well as denigrin E (4), dactylpyrrole A (5) and lamellarin O1 (6). Two of the known compounds, dictyodendrins C (1) and F (3) were also isolated from G. aureomarginatus individuals. Chemical analysis of D. teawanui afforded ergosterol peroxide, 5α,8α-epidioxy-24-methylcholesta-6,22-dien-3β-ol (7). The structures of the isolated natural products were elucidated based on extensive analysis of 1D and 2D NMR data.

Bite Force in Four Pinniped Species from the West Coast of Baja California, Mexico, in Relation to Diet, Feeding Strategy, and Niche Differentiation

Behavioral foraging differences are known to aid in food resource partitioning in pinniped communities, but it is not known whether skull biomechanical efficiency also contributes to dietary niche partitioning. We tested this hypothesis in a community of four sympatric species of pinnipeds that co-occur along the coast of Baja California: California sea lion (Zalophus californianus), northern elephant seal (Mirounga angustirostris), harbor seal (Phoca vitulina), and Guadalupe fur seal (Arctocephalus townsendi). We tested whether their preferred prey items differed in resistivity to puncture and whether those differences were linked to the mass of the muscles of mastication and the biomechanical efficiency with which they can puncture prey items. For each prey species, we measure resistivity to puncture using texture profile analysis. We found that M. angustirostris consumes the most resistant prey and that A. townsendi consumes the least resistant. We estimated physiological cross-sectional area of the muscles of mastication for each pinniped and found that the same pair of species respectively has the largest and smallest theoretical value of muscular force. Finally, we estimated the bite force that each pinniped species requires to puncture its prey by solving Euler-Lagrange equations based on biomechanical lever model parameters measured from 3D digital models of the skulls. We also found differences in efficiency between the species. These data allowed us to classify the three ecomorphological types. Type 1 features a hydrodynamic skull with relatively low mandibular forces, characteristic of pelagic carnivore feeders such as A. townsendi. Type 2, represented by Z. californianus and M. angustirostris (both opportunistic feeders), is characterized by broad insertion areas for the mandibular muscles and strong teeth, permitting these predators to vary the prey target species as a function of prey availability. Type 3 features a less robust skull and a lower muscle efficiency, characteristic of benthic feeders such as P. vitulina. This evidence indicates that biomechanical differences between the species contribute to dietary niche construction.

Visual Attack on the Moving Prey by Cuttlefish.

Visual attack for prey capture in cuttlefish involves three well characterized sequential stages: attention, positioning, and seizure. This visually guided behavior requires accurate sensorimotor integration of information on the target’s direction and tentacular strike control. While the behavior of cuttlefish visual attack on a stationary prey has been described qualitatively, the kinematics of visual attack on a moving target has not been analyzed quantitatively. A servomotor system controlling the movement of a shrimp prey and a high resolution imaging system recording the behavior of the cuttlefish predator, together with the newly developed DeepLabCut image processing system, were used to examine the tactics used by cuttlefish during a visual attack on moving prey. The results showed that cuttlefish visually tracked a moving prey target using mainly body movement, and that they maintained a similar speed to that of the moving prey right before making their tentacular strike. When cuttlefish shot out their tentacles for prey capture, they were able to either predict the target location based on the prey’s speed and compensate for the inherent sensorimotor delay or adjust the trajectory of their tentacular strike according to the prey’s direction of movement in order to account for any changes in prey position. These observations suggest that cuttlefish use the various visual tactics available to them flexibly in order to capture moving prey, and that they are able to extract direction and speed information from moving prey in order to allow an accurate visual attack.

Turning performance of brief squid Lolliguncula brevis during attacks on shrimp and fish.

Although squid are generally considered to be effective predators, little is currently known of how squid maneuver and position themselves during prey strikes. In this study, high-speed video and kinematic analyses were used to study attacks by the brief squid Lolliguncula brevis on both shrimp and fish. Squid attack success was high (>80%) and three behavioral phases were identified: (1) approach, (2) strike and (3) recoil. Lolliguncula brevis demonstrated greater maneuverability (i.e. a smaller length-specific turning radius) and employed more body adjustments (i.e. mantle angle posturing) during approaches toward shrimp versus fish. Squid exhibited higher linear approach/strike velocities and accelerations with faster-swimming fish prey compared with slower shrimp prey. Agility (i.e. turning rate) during prey encounters was comparable to performance extremes observed during non-predatory turns, and did not differ according to prey type or distance. Despite having the ability to modulate tentacle extension velocity, squid instead increased their own swimming velocity rather than increasing tentacle velocity when targeting faster fish prey during the strike phase, but this was not the case for shrimp prey. Irrespective of prey type, L. brevis consistently positioned themselves above the prey target prior to the tentacle strike, possibly to facilitate a more advantageous downward projection of the tentacles. During the recoil, L. brevis demonstrated length-specific turning radii similar to those recorded during the approach despite vigorous escape attempts by some prey. Clearly, turning performance is integral to prey attacks in squid, with differences in attack strategy varying depending on the prey target.

First capture success in two dimensions: The search for prey by a random walk predator in a comprehensive space of random walks

Random walk models are an important tool used for understanding how complex organisms redistribute themselves through space and time in search of targets such as food, shelter, or mates. These walks are easily studied with agent-based models, which can be used to ask which search strategy is best according to some efficiency metric. Current studies however, generally do not consider the full range of potential random walks, success metrics, and constraints on the walker, and implementation details vary widely. It is therefore difficult to compare results across studies. In this paper, we investigate predator search behaviour in a comprehensive space of key movement variables that allows the predator to select from a continuum of random walks ranging from Brownian walks (BWs) to correlated random walks (CorRWs) which include directional persistence, to composite random walks (ComRWs) which feature intensive and extensive search modes (ISMs and ESMs), and finally to more complex correlated composite random walks (CCRWs). We specifically focus on the search behaviour of a predator between the initiation of a search for a prey item and the first successful acquisition of a prey target: we call this interval the “search-to-capture” event. We measure the predator's success against three metrics of energetic cost: (1) the time elapsed, (2) the distance travelled, and (3) an equally weighted combination of time and distance. In addition, we explore the effect of three different constraints on the predator: (1) hunting success in the extensive search mode, (2) detection radius when in the extensive search mode, and (3) prey density. Our work confirms the broadly held notion that CCRW movement patterns should always outperform BWs, but find instructive cases where other walks are superior. We also show that, within the CCRW category, there is a wide range of possible walks and rank these according to measures of energetic cost. Our work also offers insights into the evolutionary pressures surrounding the “search-to-capture” event, and suggests that CCRW predators with low hunting success in one movement mode experience higher evolutionary pressures and are thus more likely to adopt a nearly optimal random walk. Our work highlights the need for comprehensive studies that examine several aspects of random walks simultaneously.

Stone tool transport by wild Burmese long-tailed macaques (Macaca fascicularis aurea)

Archaeologists have used stone transport as a proxy to understand a variety of cognitive, logistical and social problems faced by human ancestors. In the same way, tool transport in our close relatives, non-human primates, has been seen as an important indicator of material selection proclivities, and as a contributing factor to the formation of activity sites as part of niche construction processes. Non-human primate transport behaviour also assists in framing evolutionary scenarios for the emergence of stone tool use in the hominin lineage. Here, we present the first study of directly observed stone tool transport in wild and unhabituated Burmese long-tailed macaques (Macaca fascicularis aurea) in Thailand. These macaques were observed during intertidal foraging activities, during which they pound open hard-shelled molluscs with stone tools. We recorded 2449 transport bouts, when a long-tailed macaque carried a stone tool from one prey target to the next, and found that on average the same tool was used to sequentially consume nine prey items in each foraging episode. The maximum number of prey items consumed in a single episode was 63. We found that tools used to open sessile oysters typically were used to consume more prey per episode than those employed on motile prey, and females transported tools further than males. Heavier tools (>200g) were rarely transported more than a few metres, but the longest transport distance was over 87m. Importantly for primate archaeological analysis of macaque tool use sites, we found that the median transport distance was 0.5m, meaning that tools are very often used in the immediate vicinity of the place they were collected by a macaque.

Marine teleost locates live prey through pH sensing.

We report that the Japanese sea catfish Plotosus japonicus senses local pH-associated increases in H(+)/CO2 equating to a decrease of ≤0.1 pH unit in ambient seawater. We demonstrated that these sensors, located on the external body of the fish, detect undamaged cryptic respiring prey, such as polychaete worms. Sensitivity is maximal at the natural pH of seawater (pH 8.1 to 8.2) and decreases dramatically in seawater with a pH <8.0.

Hold your breath or the catfish will find you

Sensory Biology Finding prey is hard enough in the light of day, but animals that are nocturnal or live in murky conditions face even greater challenges. Caprio et al. describe a sense that allows a marine catfish to detect the mere “breathing” of their prey target. External sensors on the

Scanning Behavior in the Medicinal Leech Hirudo verbana

While moving through their environment, medicinal leeches stop periodically and wave their head or body back and forth. This activity has been previously described as two separate behaviors: one called ‘head movement’ and another called ‘body waving’. Here, we report that these behaviors exist on a continuum, and provide a detailed description of what we now call ‘scanning’. Scanning-related behavior has been thought to be involved in orientation; its function has never before been assessed. While previous studies suggested an involvement of scanning in social behavior, or sucker placement, our behavioral studies indicate that scanning is involved in orienting the leech towards prey stimuli. When such stimuli are present, scanning behavior is used to re-orient the leech in the direction of a prey-like stimulus. Scanning, however, occurs whether or not prey is present, but in the presence of prey-like stimuli scanning becomes localized to the stimulus origin. Most likely, this behavior helps the leech to gain a more detailed picture of its prey target. The display of scanning, regardless of the presence or absence of prey stimuli, is suggestive of a behavior that is part of an internally driven motor program, which is not released by the presence of sensory stimuli. The data herein include first steps to understanding the neural mechanisms underlying this important behavior.

Aleutian Islands beaked whale echolocation signals

Beaked whales are an elusive group of marine mammals. They are infrequently encountered as they are pelagic, deep diving foragers with short surface intervals between long dives (Tyack et al. 2006). In recent years, research has shown that beaked whales produce frequency modulated (FM) upsweep echolocation signals (Zimmer et al. 2005, Johnson et al. 2006, Gillespie et al. 2009, McDonald et al. 2009, Baumann-Pickering et al. 2010), which appear to be species specific in their spectral and temporal characteristics. Their typical echolocation behavior during foraging consists of FM pulses with very regular interpulse intervals (IPIs) while searching for prey, and discrete click series with short IPIs when closing in on a potential prey target, called a buzz (Johnson et al. 2004, Madsen et al. 2005). Around the Aleutian Islands, only three species of beaked whales are currently known to occur. Sightings or strandings of Baird’s beaked whales (Berardius beardii), Cuvier’s beaked whales (Ziphius cavirostris), and Stejneger’s beaked whales (Mesoplodon stejnegeri) have been reported (Jefferson et al. 2008). Stejneger’s beaked whales are found in cold-temperate and subpolar waters, and they are endemic to the northern North Pacific. Based on stranding records because live sightings are rare, the central Aleutian Islands are considered to be the center of this species’ range (Loughlin et al. 1982, Walker and Hansen 1999). Stejneger’s beaked whale are mostly encountered in small groups of two or three animals and occasionally in larger groups up to 15 animals (Loughlin and Perez 1985). These groups make coordinated dives with a series of five to six short dives, followed by a longer dive of 10–15min (Loughlin et al. 1982). The species is most often found in water depths ranging from 730 to 1,560 m. Their habitat is the steep slope of the continental shelf, which drops off into the Aleutian Basin to the north and into the Aleutian Trench to the south, but they are not likely to occur in the shallow northern or eastern Bering Sea (Mead 1989). Investigative effort to study the behavior of beaked whales has increased due to several mass strandings, which have been linked to military sonar exercises (Cox et al. 2006). Numerous mass strandings of Stejneger’s beaked whales in the Aleutian Islands have been documented since 1975 (Walker and Hansen 1999), yet to date, no correlation between these strandings and human activities has been established. Passive acoustic monitoring provides a cost-effective technique to investigate the behavioral ecology of these animals over long periods and in remote locations, particularly for species whose echolocation signals are distinguishable (McDonald et al. 2009, Baumann-Pickering et al. 2010).

Nota sobre la dieta de Ameiva edracantha (Squamata, Teiidae) en el Parque Nacional Cerros de Amotape, Tumbes, Perú

The diet of Ameiva edracantha Bocourt 1874, a terrestrial diurnal teiid lizard distributed in northwestern Peru and southwestern Ecuador is described for the first time. Stomach contents of fifteen individuals collected from quebrada La Angostura were analyzed. Lepidopteran larvae, coleopterans, orthopterans and spiders were the dominant preys in the lizard’s diet. Snout-vent length and head length, width and height were not correlated to prey length, width and volume. Other parameters such as profitability and prey target selection could be involved in prey selection by A. edracantha.

Adaptive echolocation sounds of insectivorous bats, Pipistrellus abramus, during foraging flights in the field

Echolocation pulses emitted by wild Pipistrellus abramus were investigated while foraging for insects in the field. Similar to other European pipistrelles, the frequency structure during foraging varied. During the search phase, the bats emitted long shallow frequency-modulated pulses 9-11 ms in duration, whereas the maximum pulse duration of the bats approaching a large target wall in the laboratory was 3 ms. No significant difference was observed between decreases in the interpulse interval during these two approach flights. It is concluded that the bats use a long quasi-constant frequency pulse to find a weak echo from a small prey target.

Echolocation behaviour adapted to prey in foraging Blainville's beaked whale (Mesoplodon densirostris)

Toothed whales echolocating in the wild generate clicks with low repetition rates to locate prey but then produce rapid sequences of clicks, called buzzes, when attempting to capture prey. However, little is known about the factors that determine clicking rates or how prey type and behaviour influence echolocation-based foraging. Here we study Blainville's beaked whales foraging in deep water using a multi-sensor DTAG that records both outgoing echolocation clicks and echoes returning from mesopelagic prey. We demonstrate that the clicking rate at the beginning of buzzes is related to the distance between whale and prey, supporting the presumption that whales focus on a specific prey target during the buzz. One whale showed a bimodal relationship between target range and clicking rate producing abnormally slow buzz clicks while attempting to capture large echoic targets, probably schooling prey, with echo duration indicating a school diameter of up to 4.3m. These targets were only found when the whale performed tight circling manoeuvres spending up to five times longer in water volumes with large targets than with small targets. The result indicates that toothed whales in the wild can adjust their echolocation behaviour and movement for capture of different prey on the basis of structural echo information.

Quantitative PCR to estimate copepod feeding

Copepods play a central role in marine food webs as grazers of plankton and as key prey for many predators. Therefore, quantifying their specific trophic interactions is critical for understanding the role of copepods in ocean processes. However, because of methodological constraints, it remains difficult to investigate in situ copepod feeding without reliance on laborious intrusive and potentially biased incubation approaches. Recent advances in PCR-based methodologies have demonstrated the feasibility of directly identifying copepod diets based on prey DNA sequences. Yet, obtaining quantitative information from these approaches remains challenging. This study presents results of systematic efforts to develop a quantitative PCR (qPCR) assay targeted to 18S rRNA gene fragments to estimate copepod gut content of specific species of prey algae. These results were first compared to gut content estimates based on fluorescence in the copepod Calanus finmarchicus fed monocultures of two different microalgae species in controlled laboratory studies. In subsequent field studies, we compared feeding rates obtained by microscopy and qPCR for Temora longicornis and Acartia clausi feeding on the haptophyte Phaeocystis globosa in natural blooms. These investigations demonstrate a semi-quantitative relationship between gut content estimates derived from qPCR, gut pigment, and direct microscopy. However, absolute estimates of gut content based on qPCR methodology were consistently lower than expected. This did not appear to be explained by the extraction methods used, or interference by non-target (predator) DNA in the PCR reactions, instead suggesting digestion of prey-specific nucleic acids. Furthermore, the 18S rDNA target gene copy number of the phytoplankton varied with growth phase. Nonetheless, when prey target gene copy number in the ambient water is quantified, the qPCR-approach can be compared to other methods, and then used to semi-quantitatively estimate relative copepod grazing on specific prey in situ without involving further incubations. A distinct advantage of a DNA-based molecular approach compared to gut fluorescence and direct microscopic observation, is the ability to detect non-pigmented and macerated prey. Future studies should aim to correct for breakdown in prey DNA and perform extensive calibrations to other methods in order to achieve a quantitative measure of feeding rates in situ.

Intensity control during target approach in echolocating bats; stereotypical sensori-motor behaviour in Daubenton's bats, Myotis daubentonii.

When approaching a prey target, bats have been found to decrease the intensity of their emitted echolocation pulses, called intensity compensation. In this paper we examine whether intensity compensation in the echolocation of bats is flexible or stereotyped. We recorded the echolocation calls of Daubenton's bats (Myotis daubentonii) while the animals attacked targets of different dimensions. Myotis daubentonii reduced the peak sound pressure level emitted by about 4dB for each halving of distance, irrespective of the target presented (mealworms and two different sizes of spheres). The absolute sound pressure level emitted by the bat is not or only a little affected by target strength. Furthermore, the decrease in emitted intensity over distance shows less scatter than the same intensity over time for the last 20 cm of target approach. The bats matched the emitted intensity to target distance equally well for the spheres (aspect-invariant target strength) as for the mealworms (aspect-dependent echo strength). We therefore conclude that intensity compensation does not rely on feedback information from received intensity, but instead follows a stereotyped pattern.

Prototype rechargeable tag for acoustical neural telemetry.

overshooting in response to stimuli placed on the side of the lesion (P < 0.001 for both animals, Fig. IC). In contrast to VIIIth nerve lesions, turn amplitude did not increase on the side opposite the lesion. Complete VIIIth nerve lesions disrupt input from all end organs which may result in more widespread turning deficits. For escape, preand post-lesion turn amplitudes were not significantly different (Fig. 1D). While lesions to the peripheral vestibular system did not affect the turning component of escape, they may affect the airborne phase and landing. Following PC nerve lesion, the amplitudes of prey capture and escape turns did not change (data not shown). This result implies that the turning deficits described here for prey capture are specific to horizontal canal nerve lesion and not a result of non-specific damage to the nervous system or to general surgical trauma. These data support the idea that on-line vestibular input is required for prey capture turning and not required for escape turning. This is consistent with the fact that turn accuracy is of greater importance for prey capture than for escape. Since the HC measures angular acceleration in the horizontal plane, it is well suited to supply the animal with on-line information about the actual position and velocity of the body in space. This information could be used to guide the centrally generated movement of the body and head toward the prey target. For escape turns, the spatial organization is more variable and the peak velocity is greater than for prey capture turns (4). This suggests that the speed of the escape turn is more important than accuracy; thus vestibular input may not be required. The initial phase of the escape response, the turn, may be truly ballistic in nature allowing the frog to maximize the speed of the response. This work was supported by the Grass Foundation.