- Email: [email protected]
Phylogenetic reconstructions of food catching among primates
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Abstracts / Comparative Biochemistry and Physiology, Part A 150 (2008) S93–S96
escape responses. The time between a startling stimulus and the animal's response (i.e. escape latency) is usually very short, i.e. of the order of a few milliseconds (1020 ms) in many invertebrates and lower vertebrates. However, recent work shows that escape latencies are not always minimized, possibly as a result of a graded system through which sub-maximal responses may be used when the threat is not maximal, or in extreme environmental conditions. Similarly, specific patterns of escape directions were found. While maximizing unpredictability would correspond to random directions of escape, work on various species shows that escape directions are not random. Theoretical work suggest that optimal trajectories for escape should span 90180° from the predator's attack, depending on the ratio between the speeds of predators and prey. Experimental results are in line with this prediction.
defensive strikes by snakes, including cobras. This suggests that the neck muscles capable of producing cephalic rotations have a fundamentally different role during striking and spitting. The kinematic and kinetic differences between spitting and striking suggest that during the latter the cervical muscles would have to play a much greater role in acceleration, momentum control, and bracing. These potential functional roles of the cervical muscles were examined in the puff adder (Bitis arietans), a large, heavy-bodied viper known for its rapid strikes. A combination of high-speed kinematics, electromyography, and basic biomechanics was used to investigate the functional integration of the neck and head during the strike.
doi:10.1016/j.cbpa.2008.04.181
doi:10.1016/j.cbpa.2008.04.179 A4.6 Prey-prehension modes in Gerrhosaurus major: Integration of the locomotor apparatus and trophic system A4.4 Sensory modulation of prey capture in frogs: Alternative strategies, biomechanical trade-offs, and sensory hierarchies
S. Montuelle (Muséum National d'Histoire Naturelle); A. Herrel (Harvard University); L. Reveret (INRIA); P. Libourel (Muséum National d'Histoire Naturelle); V. Bels (Muséum National d'Histoire Naturelle)
K. Nishikawa, J. Monroy (Northern Arizona University) Frogs exhibit complex repertoires of prey capture behavior that depend on visual analysis of prey size, shape, location, and velocity. Based on these cues, frogs modulate their prey capture strategies to maximize the probability of capture. Our studies reveal two organizational principles for modulation of prey capture: (1) alternative strategies are associated with biomechanical tradeoffs that arise from physical attributes of prey; and (2) processing of sensory information about prey attributes is hierarchical. When prey are small, ballistic tongue projection is used for capture. As prey become larger, they reach a mass at which the tongue can no longer be used to retrieve them, and frogs switch to jaw prehension. At the border between large and small prey, frogs switch randomly between alternative strategies. Because ballistic prey capture depends on momentum transfer from jaws to tongue, it cannot be used to power outofplane tongue movements. At an azimuth of ~40°, frogs switch from a strategy in which they aim only the head, to one in which both head and tongue are aimed. How much information about its prey can be deduced from the kinematics of a frog's prey capture behavior? Our results suggest that visual processing of prey attributes involves a hierarchical decisionmaking process. Biomechanical constraints prevent any given prey capture strategy from being effective for all types of prey under all conditions. Prey capture strategies are adjusted to prey attributes in a hierarchical fashion that maximizes the probability of capture. doi:10.1016/j.cbpa.2008.04.180
Within the Squamate lineage, scleroglossan lizards are typically considered to be active foragers that capture prey with their jaws only. In contrast, Iguanian lizards are described as ambush predators that use tongue to catch prey. However, this dichotomy appears oversimplified as some Scleroglossan lizards, especially many Scincomorphs, are able to use both modes of prey prehension. As feeding behaviour involves a locomotor approach, a bodyconfiguration phase and the actual strike phase, it is necessary to consider both the locomotor and trophic systems in an integrative context. Thus, we decided to quantify prey prehension behaviour in a scleroglossan model organism Gerrhosaurus major. We used a multiplecamera experimental setup involving three synchronized highspeedvideoscameras (200 fps) to reconstruct the movements of the locomotor elements (i.e., vertebral column bending and forelimbs extension) and trophic system (i.e., head positioning and jaw displacements) in 3dimensions. Data were obtained for animals capturing 4 distinct foodtypes (1 cm3 piece of banana, giant mealworms, grasshoppers and pinkies). Three capture strategies were observed: (i) lingual prehension involving protrusion of the tongue out of the buccal cavity followed by retraction of the tongue with adhering food, (ii) lingual pinning with the tongue positioned at the tip of the mandible (but remaining in the buccal cavity) to retain the prey on the substratum while the jaws close, and (iii) jaw prehension with the tongue completely retracted into the buccal cavity. This analysis allows us to determine the contribution of locomotor and trophic elements to each of the observed prey prehension modes. doi:10.1016/j.cbpa.2008.04.182
A4.5 Why spitting cobras oscillate their heads and puff adders don’t: functional integration of the head and neck in snakes
A4.7 Phylogenetic reconstructions of food catching among primates
B.A. Young (Washburn University) While “spitting” venom, cobras perform cephalic oscillations in both the vertical and horizontal planes. These angular displacements are rapid (up to 30 degrees in 10 msec) and appear to be highly controlled. Similar rotations have never been described from either predatory or
E. Pouydebat (USTV, France); V. Bels (MNHN, France); M. Laurin (CNRS, UPMC, France) The prevailing hypothesis about grasping in primates stipulates an evolution from power toward precision grips within hominids. Here,
Abstracts / Comparative Biochemistry and Physiology, Part A 150 (2008) S93–S96
the evolution of grasping has been studied through a pluridisciplinary analysis on the basis of experimental studies. We compare the modes of food grasping to morphometric characters in one platyrrhine, nine catarrhines and humans. We determine if extant primates present morphometric characteristics linked to their modes of grasping, trace the evolution of these characteristics and point human specificities. The possible presence of a phylogenetic signal in the behavioural and relevant morphometric characters is investigated using squaredchange parsimony and through PVR. The correlation between some morphometric and behavioural characters is also determined using phylogenetic independent contrasts and variance partitioning with PVR. All these data are used to show the proximity between the platyrrhine and humans and to discuss the model of the evolution of grasping proposed in the literature. doi:10.1016/j.cbpa.2008.04.183
A4.8 Interaction between underwater and aerial body temperatures in influencing a top predator feeding rate in the intertidal S. Pincebourde (University of South Carolina, Department of Biological Sciences); E. Sanford (University of California Davis, Bodega Marine Laboratory); B. Helmuth (University of South Carolina, Department of Biological Sciences) Numerous studies reported the effects of a variation in a single abiotic variable (eg temperature) on biotic interactions. Very few, however, have attempted to ask if a variation in a given factor can dampen or amplify the effects of another factor. We measured the interactive effects of sea water temperature and aerial body temperature, when exposed at low tide, on the feeding rate of the keystone intertidal predatory starfish Pisaster ochraceus, when feeding on the Californian mussel. In laboratory trials, we reproduced temperature scenario measured in the field. Results suggest that cold water helps starfish to recover relatively quickly from aerial thermal stress, but warmer waters did not permit predators to acclimate to warmer aerial conditions. Moreover, starfishes performed surprisingly better when both aerial and water stressful conditions occurred simultaneously, followed by a period when both stress signals were released, compared to a situation with the two stress signals following each other in a non overlapping way. Overall, our results highlight (1) the importance of looking at the interaction between water and aerial abiotic conditions when studying the effects of environment on species performance in the intertidal, and (2) the importance of temporal pattern of multiple environmental stress signals, which is largely neglected in studies on determinants of variation in species interactions. doi:10.1016/j.cbpa.2008.04.184
S95
Kinematics of the head, jaws and hyolingual complex during aquatic feeding were analysed using highspeed cinematography (500 and 1000 fr/s). In prey capture the hyoid protracts prior to jaw opening. The gape increases gradually, with no discrete phases leading to maximal jaw amplitude. Neck extension starts shortly prior to reaching peak gape. In initial prey capture, we detected a static phase in which maximum gape is briefly retained (here termed “MGphase). Such a gape phase is lacking in transport cycles. During the MGphase in ingestion, the hyoid retracts rapidly (Vmax = 26.5 cm/s). Prey transport is characterized by modulations in the kinematic patterns depending on the food position within the oral cavity. The first transport cycles immediately after prey capture involve “compensatory suction”. When the food is repositioned posteriorly toward the esophagus, the musk turtles use predominantly “inertial suction”. The hard pellets offered as food items are moved forward and backward within the buccal cavity by the waterflow and are crushed during this combined transport manipulation phase. Discrete pharyngeal packing cycles prior to swallowing can be recognised. Typical for these cycles is a hardly detectable gape and modest ventral hyoid depression. Swallowing starts with a hyoid elevation by contraction of the intermandibular muscles followed by activation of the cervical constrictors. doi:10.1016/j.cbpa.2008.04.185
A4.10 On the biochemical and bizarre mechanical defensive strategies of the salamandrid Pleurodeles waltl E. Heiss, N. Natchev, J. Weisgram (University of Vienna) When threatened, the Spanish ribbed newt, Pleurodeles waltl, displays relatively stereotypic immobile posturings that present armed body parts to potential predators. After predator like stimulation, young animals press their forebody to the ground while elevating the tail. Adults arch their body and present their neck and back regions towards the threatening stimulus. During both posturings, the newts release a viscous white poisonous fluid to the skin surface, especially in the neck, back and tail dorsum regions. Histological and ultrastructural investigations show three types of dermal glands that produce the skin secretion. While the mucous glands are randomly distributed, the conventional serous glands are concentrated in the neck and back regions. High numbers of a new type of giant serous glands were found only in the tail, especially along its dorsal edge. Adult newts develop an additional mechanical protective strategy. During the arched body posturing, their sharply pointed rib tips stretch the lateral orange warts, ultimately piercing them. The rib tips project up to 3 mm out of the body and are used, in combination with the poisonous secretion, to injure aggressors. Even if the newts wound themselves, they seem to be immune against their own poison and are also resistant against microbial pathogens that could easily enter through the selfinduced lesions. doi:10.1016/j.cbpa.2008.04.186
A4.9 Kinematic analysis of prey capture, prey transport and swallowing in the Common Musk Turtle Sternotherus odoratus (Chelonia, Kinosternidae) N. Natchev, E. Heiss, P. Lemell, J. Weisgram (University Vienna)
A4.11 Effect of simulated purse seine fishing on acclimated sardines and post-fishing interactions with predators
Musk Turtles are completely aquatic carnivorous species. Young animals are able to capture prey on land, but have to return to the water to transport the foot items through the oropharyngeal cavity.
A. Marçalo (INRB/IPIMAROlhão); J. Araújo (INRB/IPIMAROlhão); P. PousãoFerreira (INRB/IPIMAROlhão); K. Erzini (Universidade do Algarve); Y. Stratoudakis (INRB/IPIMARLisbon)
Abstracts / Comparative Biochemistry and Physiology, Part A 150 (2008) S93–S96
escape responses. The time between a startling stimulus and the animal's response (i.e. escape latency) is usually very short, i.e. of the order of a few milliseconds (1020 ms) in many invertebrates and lower vertebrates. However, recent work shows that escape latencies are not always minimized, possibly as a result of a graded system through which sub-maximal responses may be used when the threat is not maximal, or in extreme environmental conditions. Similarly, specific patterns of escape directions were found. While maximizing unpredictability would correspond to random directions of escape, work on various species shows that escape directions are not random. Theoretical work suggest that optimal trajectories for escape should span 90180° from the predator's attack, depending on the ratio between the speeds of predators and prey. Experimental results are in line with this prediction.
defensive strikes by snakes, including cobras. This suggests that the neck muscles capable of producing cephalic rotations have a fundamentally different role during striking and spitting. The kinematic and kinetic differences between spitting and striking suggest that during the latter the cervical muscles would have to play a much greater role in acceleration, momentum control, and bracing. These potential functional roles of the cervical muscles were examined in the puff adder (Bitis arietans), a large, heavy-bodied viper known for its rapid strikes. A combination of high-speed kinematics, electromyography, and basic biomechanics was used to investigate the functional integration of the neck and head during the strike.
doi:10.1016/j.cbpa.2008.04.181
doi:10.1016/j.cbpa.2008.04.179 A4.6 Prey-prehension modes in Gerrhosaurus major: Integration of the locomotor apparatus and trophic system A4.4 Sensory modulation of prey capture in frogs: Alternative strategies, biomechanical trade-offs, and sensory hierarchies
S. Montuelle (Muséum National d'Histoire Naturelle); A. Herrel (Harvard University); L. Reveret (INRIA); P. Libourel (Muséum National d'Histoire Naturelle); V. Bels (Muséum National d'Histoire Naturelle)
K. Nishikawa, J. Monroy (Northern Arizona University) Frogs exhibit complex repertoires of prey capture behavior that depend on visual analysis of prey size, shape, location, and velocity. Based on these cues, frogs modulate their prey capture strategies to maximize the probability of capture. Our studies reveal two organizational principles for modulation of prey capture: (1) alternative strategies are associated with biomechanical tradeoffs that arise from physical attributes of prey; and (2) processing of sensory information about prey attributes is hierarchical. When prey are small, ballistic tongue projection is used for capture. As prey become larger, they reach a mass at which the tongue can no longer be used to retrieve them, and frogs switch to jaw prehension. At the border between large and small prey, frogs switch randomly between alternative strategies. Because ballistic prey capture depends on momentum transfer from jaws to tongue, it cannot be used to power outofplane tongue movements. At an azimuth of ~40°, frogs switch from a strategy in which they aim only the head, to one in which both head and tongue are aimed. How much information about its prey can be deduced from the kinematics of a frog's prey capture behavior? Our results suggest that visual processing of prey attributes involves a hierarchical decisionmaking process. Biomechanical constraints prevent any given prey capture strategy from being effective for all types of prey under all conditions. Prey capture strategies are adjusted to prey attributes in a hierarchical fashion that maximizes the probability of capture. doi:10.1016/j.cbpa.2008.04.180
Within the Squamate lineage, scleroglossan lizards are typically considered to be active foragers that capture prey with their jaws only. In contrast, Iguanian lizards are described as ambush predators that use tongue to catch prey. However, this dichotomy appears oversimplified as some Scleroglossan lizards, especially many Scincomorphs, are able to use both modes of prey prehension. As feeding behaviour involves a locomotor approach, a bodyconfiguration phase and the actual strike phase, it is necessary to consider both the locomotor and trophic systems in an integrative context. Thus, we decided to quantify prey prehension behaviour in a scleroglossan model organism Gerrhosaurus major. We used a multiplecamera experimental setup involving three synchronized highspeedvideoscameras (200 fps) to reconstruct the movements of the locomotor elements (i.e., vertebral column bending and forelimbs extension) and trophic system (i.e., head positioning and jaw displacements) in 3dimensions. Data were obtained for animals capturing 4 distinct foodtypes (1 cm3 piece of banana, giant mealworms, grasshoppers and pinkies). Three capture strategies were observed: (i) lingual prehension involving protrusion of the tongue out of the buccal cavity followed by retraction of the tongue with adhering food, (ii) lingual pinning with the tongue positioned at the tip of the mandible (but remaining in the buccal cavity) to retain the prey on the substratum while the jaws close, and (iii) jaw prehension with the tongue completely retracted into the buccal cavity. This analysis allows us to determine the contribution of locomotor and trophic elements to each of the observed prey prehension modes. doi:10.1016/j.cbpa.2008.04.182
A4.5 Why spitting cobras oscillate their heads and puff adders don’t: functional integration of the head and neck in snakes
A4.7 Phylogenetic reconstructions of food catching among primates
B.A. Young (Washburn University) While “spitting” venom, cobras perform cephalic oscillations in both the vertical and horizontal planes. These angular displacements are rapid (up to 30 degrees in 10 msec) and appear to be highly controlled. Similar rotations have never been described from either predatory or
E. Pouydebat (USTV, France); V. Bels (MNHN, France); M. Laurin (CNRS, UPMC, France) The prevailing hypothesis about grasping in primates stipulates an evolution from power toward precision grips within hominids. Here,
Abstracts / Comparative Biochemistry and Physiology, Part A 150 (2008) S93–S96
the evolution of grasping has been studied through a pluridisciplinary analysis on the basis of experimental studies. We compare the modes of food grasping to morphometric characters in one platyrrhine, nine catarrhines and humans. We determine if extant primates present morphometric characteristics linked to their modes of grasping, trace the evolution of these characteristics and point human specificities. The possible presence of a phylogenetic signal in the behavioural and relevant morphometric characters is investigated using squaredchange parsimony and through PVR. The correlation between some morphometric and behavioural characters is also determined using phylogenetic independent contrasts and variance partitioning with PVR. All these data are used to show the proximity between the platyrrhine and humans and to discuss the model of the evolution of grasping proposed in the literature. doi:10.1016/j.cbpa.2008.04.183
A4.8 Interaction between underwater and aerial body temperatures in influencing a top predator feeding rate in the intertidal S. Pincebourde (University of South Carolina, Department of Biological Sciences); E. Sanford (University of California Davis, Bodega Marine Laboratory); B. Helmuth (University of South Carolina, Department of Biological Sciences) Numerous studies reported the effects of a variation in a single abiotic variable (eg temperature) on biotic interactions. Very few, however, have attempted to ask if a variation in a given factor can dampen or amplify the effects of another factor. We measured the interactive effects of sea water temperature and aerial body temperature, when exposed at low tide, on the feeding rate of the keystone intertidal predatory starfish Pisaster ochraceus, when feeding on the Californian mussel. In laboratory trials, we reproduced temperature scenario measured in the field. Results suggest that cold water helps starfish to recover relatively quickly from aerial thermal stress, but warmer waters did not permit predators to acclimate to warmer aerial conditions. Moreover, starfishes performed surprisingly better when both aerial and water stressful conditions occurred simultaneously, followed by a period when both stress signals were released, compared to a situation with the two stress signals following each other in a non overlapping way. Overall, our results highlight (1) the importance of looking at the interaction between water and aerial abiotic conditions when studying the effects of environment on species performance in the intertidal, and (2) the importance of temporal pattern of multiple environmental stress signals, which is largely neglected in studies on determinants of variation in species interactions. doi:10.1016/j.cbpa.2008.04.184
S95
Kinematics of the head, jaws and hyolingual complex during aquatic feeding were analysed using highspeed cinematography (500 and 1000 fr/s). In prey capture the hyoid protracts prior to jaw opening. The gape increases gradually, with no discrete phases leading to maximal jaw amplitude. Neck extension starts shortly prior to reaching peak gape. In initial prey capture, we detected a static phase in which maximum gape is briefly retained (here termed “MGphase). Such a gape phase is lacking in transport cycles. During the MGphase in ingestion, the hyoid retracts rapidly (Vmax = 26.5 cm/s). Prey transport is characterized by modulations in the kinematic patterns depending on the food position within the oral cavity. The first transport cycles immediately after prey capture involve “compensatory suction”. When the food is repositioned posteriorly toward the esophagus, the musk turtles use predominantly “inertial suction”. The hard pellets offered as food items are moved forward and backward within the buccal cavity by the waterflow and are crushed during this combined transport manipulation phase. Discrete pharyngeal packing cycles prior to swallowing can be recognised. Typical for these cycles is a hardly detectable gape and modest ventral hyoid depression. Swallowing starts with a hyoid elevation by contraction of the intermandibular muscles followed by activation of the cervical constrictors. doi:10.1016/j.cbpa.2008.04.185
A4.10 On the biochemical and bizarre mechanical defensive strategies of the salamandrid Pleurodeles waltl E. Heiss, N. Natchev, J. Weisgram (University of Vienna) When threatened, the Spanish ribbed newt, Pleurodeles waltl, displays relatively stereotypic immobile posturings that present armed body parts to potential predators. After predator like stimulation, young animals press their forebody to the ground while elevating the tail. Adults arch their body and present their neck and back regions towards the threatening stimulus. During both posturings, the newts release a viscous white poisonous fluid to the skin surface, especially in the neck, back and tail dorsum regions. Histological and ultrastructural investigations show three types of dermal glands that produce the skin secretion. While the mucous glands are randomly distributed, the conventional serous glands are concentrated in the neck and back regions. High numbers of a new type of giant serous glands were found only in the tail, especially along its dorsal edge. Adult newts develop an additional mechanical protective strategy. During the arched body posturing, their sharply pointed rib tips stretch the lateral orange warts, ultimately piercing them. The rib tips project up to 3 mm out of the body and are used, in combination with the poisonous secretion, to injure aggressors. Even if the newts wound themselves, they seem to be immune against their own poison and are also resistant against microbial pathogens that could easily enter through the selfinduced lesions. doi:10.1016/j.cbpa.2008.04.186
A4.9 Kinematic analysis of prey capture, prey transport and swallowing in the Common Musk Turtle Sternotherus odoratus (Chelonia, Kinosternidae) N. Natchev, E. Heiss, P. Lemell, J. Weisgram (University Vienna)
A4.11 Effect of simulated purse seine fishing on acclimated sardines and post-fishing interactions with predators
Musk Turtles are completely aquatic carnivorous species. Young animals are able to capture prey on land, but have to return to the water to transport the foot items through the oropharyngeal cavity.
A. Marçalo (INRB/IPIMAROlhão); J. Araújo (INRB/IPIMAROlhão); P. PousãoFerreira (INRB/IPIMAROlhão); K. Erzini (Universidade do Algarve); Y. Stratoudakis (INRB/IPIMARLisbon)