David L. Macmillan

Victoria University Melbourne, Melbourne, Victoria, Australia

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Publications (51)89.22 Total impact

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    ABSTRACT: Abstract Effective communication requires reliable signals and competent receptors. Theoretical and empirical accounts of animal signaling focus overwhelmingly on the capacity of the signaler to convey the message. Nevertheless, the intended receiver's ability to detect a signal depends on the condition of its receptor organs, as documented for humans. The impact of receptor organ condition on signal reception and its consequences for functional behavior are poorly understood. Social insects use antennae to detect chemical odors that distinguish between nestmates and enemies, reacting aggressively to the latter. We investigated the impact of antennal condition, determined by the density of sensilla, on the behavior of the weaver ant Oecophylla smaragdina. Worker aggression depended upon the condition of their antennae: workers with fewer sensilla on their antennae reacted less aggressively to nonnestmate enemies. These novel data highlight the largely unappreciated significance of receptor organ condition for animal communication and may have implications for coevolutionary processes in animal communication.
    The American Naturalist 12/2013; 182(6):834-840. · 4.55 Impact Factor
  • B W Patullo, D L Macmillan
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    ABSTRACT: The five sensory modalities of humans are also found in a wide range of invertebrates. Other vertebrates have evolved additional special senses, such as the magnetic sense, which are also found in some invertebrates. However, there remain a few sensory abilities that curiously appear to be found in either vertebrates or invertebrates, but not both. For example, electrosensitivity - the ability to detect electric fields in water - which should benefit vertebrates and invertebrates alike, is apparently only used by vertebrates. However, recent reports suggest that some invertebrates could have an electric sense. Here we examine that possibility further and demonstrate a behavioural threshold to low-level electrical fields in two freshwater invertebrates. The responses are not low enough for them to detect the Earth's magnetic field as some other electroreceptive species can do, but sufficiently low for them to use in navigation or prey and predator detection. This finding challenges the current view of the sensory world of aquatic invertebrates and has implications for the evolution of this ability.
    Journal of Experimental Biology 02/2010; 213(4):651-7. · 3.24 Impact Factor
  • Edith Heußlein, Blair W. Patullo, David L. Macmillan
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    ABSTRACT: Biomimetic applications play an important role in informing the field of robotics. One aspect is navigation – a skill automobile robots require to perform useful tasks. A sub-area of this is search strategies, e.g. for search and rescue, demining, exploring surfaces of other planets or as a default strategy when other navigation mechanisms fail. Despite that, only a few approaches have been made to transfer biological knowledge of search mechanisms on surfaces along the ground into biomimetic applications. To provide insight for robot navigation strategies, this study describes the paths a crayfish used to explore terrain. We tracked movement when different sets of sensory input were available. We then tested this algorithm with a computer model crayfish and concluded that the movement of C. destructor has a specialised walking strategy that could provide a suitable baseline algorithm for autonomous mobile robots during navigation.
    Robotica 01/2010; 28:465-475. · 0.88 Impact Factor
  • Blair W. Patullo, Helena P. Baird, David L. Macmillan
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    ABSTRACT: Living in groups with conspecifics can increase an animal's fitness in the wild. A social environment may also be imposed by commercial farming industries. One important measure of competition and group dynamics is the level of aggressive interaction. This can also influence the level of damage or injury in cultured populations, a commercial issue at point of sale. There is considerable research into this issue in commercial species such as pigs, cattle and chickens but less is known about aquatic communal species such as decapod crustaceans. Here we manipulated group size in the freshwater crayfish Cherax destructor, a species that forms social groups in the wild and one that is also commercially farmed. Aggressive behaviour was scored during 1h of observation in replicates of groups of 4, 16 and 36 animals to analyse 11 variables of fight dynamics that ensued. The number of fights per crayfish (4.0±0.8 to 1.9±0.2 fights, P=0.017) and the time each crayfish was involved in a fight (113.9±32.6 to 21.6±2.6s, P=0.011) decreased as group size increased. Conversely, the number of failed tailflips elicited per crayfish increased from 0 to 0.08±0.03 tailflips in the largest groups (P=0.011). Together, the data suggest that despite C. destructor's different biology and habitat, compared to prior work that manipulates group size, the crayfish adjusts its fighting strategy when social circumstances change. Theory has proposed aggressive behaviour could change in groups of animals and our data indicates that this applies more broadly across species and more dynamically than previously demonstrated.
    Applied Animal Behaviour Science - APPL ANIM BEHAV SCI. 01/2009; 120(3):231-237.
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    ABSTRACT: The capacity to associate stimuli underlies many cognitive abilities, including recognition, in humans and other animals. Vertebrates process different categories of information separately and then reassemble the distilled information for unique identification, storage and recall. Invertebrates have fewer neural networks and fewer neural processing options so study of their behavior may reveal underlying mechanisms still not fully understood for any animal. Some invertebrates form complex social colonies and are capable of visual memory-bees and wasps, for example. This ability would not be predicted in species that interact in random pairs without strong social cohesion; for example, crayfish. They have chemical memory but the extent to which they remember visual features is unknown. Here we demonstrate that the crayfish Cherax destructor is capable of visual recognition of individuals. The simplicity of their interactions allowed us to examine the behavior and some characteristics of the visual features involved. We showed that facial features are learned during face-to-face fights, that highly variable cues are used, that the type of variability is important, and that the learning is context-dependent. We also tested whether it is possible to engineer false identifications and for animals to distinguish between twin opponents.
    PLoS ONE 02/2008; 3(2):e1695. · 3.73 Impact Factor
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    B W Patullo, G Jolley-Rogers, D L Macmillan
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    ABSTRACT: Computer analysis of video footage is one option for recording locomotor behavior for a range of neurophysiological and behavioral studies. This technique is reasonably well established and accepted, but its use for some behavioral analyses remains a challenge. For example, filming through water can lead to reflection, and filming nocturnal activity can reduce resolution and clarity of filmed images. The aim of this study was to develop a noninvasive method for recording nocturnal activity in aquatic decapods and test the accuracy of analysis by video tracking software. We selected crayfish, Cherax destructor, because they are often active at night, they live underwater, and data on their locomotion is important for answering biological and physiological questions such as how they explore and navigate. We constructed recording arenas and filmed animals in infrared light. Wethen compared human observer data and software-acquired values. In this article, we outline important apparatus and software issues to obtain reliable computer tracking.
    Behavior Research Methods 12/2007; 39(4):783-8. · 2.12 Impact Factor
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    ABSTRACT: Periods of isolation during which animals have no social contact are common in the design of behavioral experiments. They are used, for example, to test memory and recognition responses, or to ensure a baseline condition before experimental manipulations commence. We investigated the effect of isolation periods on the aggressive behavior of matched pairs of the crayfish Cherax destructor in two contexts. The first experiment tested the effects of a period of isolation between two encounters. The second experiment tested the effects of isolation before an encounter by pairing one crayfish from a communal living environment with another crayfish from an isolated one. Fight outcome and aggression levels were analyzed, resulting in three conclusions about the social biology of C. destructor. First, encounters between familiar opponents are influenced by the outcome of the familiarization fight for about 2 weeks. Second, the level of aggression and the outcome of an encounter are affected over different time frames. Third, individuals that are isolated before an encounter can be disadvantaged. These data suggest that isolation, or events that occur during periods of isolation, affect multiple elements of social behavior in C. destructor. This suggestion has implications for the interpretation of previous results and future studies in crustaceans and other taxa.
    Biological Bulletin 11/2007; 213(2):187-95. · 1.23 Impact Factor
  • Blair W Patullo, David L Macmillan
    Current Biology 03/2007; 17(3):R83-4. · 9.49 Impact Factor
  • Helena P. Baird, Blair W. Patullo, David L. Macmillan
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    ABSTRACT: Most of our knowledge of social behaviour in crustaceans stems from observations of pairs of animals engaged in conflict. Less consideration has been given to the dynamics of group behaviour. We investigated whether chemical signals affect the dynamic of groups of Cherax destructor. Animals were exposed to odours collected from male, female, moulted or dominant crayfish, or from fish. We observed agonistic encounters in the group during a 15 min period after the introduction of the odour. There was a decrease in threat behaviours when the male odour was added. We conclude from this that an olfactory stimulus can affect the dynamic of group interactions and the results suggest that the outcome is likely to be different from that obtained with paired or single individuals.
    Marine and Freshwater Behaviour and Physiology - MAR FRESHW BEHAV PHYSIOL. 01/2007; 40(3):183-188.
  • L M Koch, B W Patullo, D L Macmillan
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    ABSTRACT: Appendages are important sources of sensory information for all animals that possess them but they are commonly damaged in nature. We describe how the tactile system of the crayfish Cherax destructor functioned when subjected to the kind of damage found in wild-caught or cultured animals. Touch information was methodically varied by the removal of antennae and chelae. The resulting behaviour was analysed in a T-maze. Crayfish with a single antenna ablated turned toward the intact appendage, however, those with only a partial ablation did not, suggesting that a tactile information threshold exists for normal behaviour. When exposed to the same environment after an antennal ablation but with no prior experience in that terrain, crayfish also turned toward the side of the intact antenna. By contrast, when animals with experience obtained in a previous trial with intact antennae were tested after ablation of one antenna, they did not turn into one arm of the maze more than the other. These two outcomes indicate that behaviour is affected by an interaction between the time at which an injury occurs and an animal's knowledge of the topography, and that an injury may affect learning. We also tested to see if other appendages could provide tactile information to compensate for antennal loss. Input from the chelae did not affect the turning behaviour of crayfish in the maze.
    Journal of Experimental Biology 09/2006; 209(Pt 16):3226-33. · 3.24 Impact Factor
  • Helena P Baird, Blair W Patullo, David L Macmillan
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    ABSTRACT: The culture of decapod crustaceans occurs worldwide. Aggressive behaviour is common in many of the species, including crayfish. This is problematic when it physically damages stock and reduces quality. Numerous biological factors influence crayfish fighting behaviour but the influence of environmental factors is not well known. This study investigated the effect of habitat complexity on the agonistic interactions of Australian freshwater crayfish, more commonly referred to locally as ‘yabbies’ (Cherax destructor Clark). Solid objects that provided structure but not shelter were used to manipulate the complexity of the environment. The number, duration and dynamic of aggressive interactions within groups of animals were observed and recorded in simple and complex environments. Habitat complexity reduced both the number of agonistic interactions and the total time spent interacting. It is suggested that the structure in the environment distracts crayfish from the presence of others or physically blocks contact between them. These results extend our knowledge of crayfish social behaviour and may provide opportunities for reducing detrimental aggressive interactions in the aquaculture industry.
    Aquaculture Research 08/2006; 37(14):1419 - 1428. · 1.42 Impact Factor
  • B W Patullo, D L Macmillan
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    ABSTRACT: Touch is a principal sense in all animals. It is potentially important in species of freshwater crayfish that encounter murky waters or are nocturnal. Little is known about how tactile (touch) stimuli affect exploratory behaviour under these conditions. We placed animals in different tactile situations at the start of an exploration in a dark arena and tracked the position of the body and antennae to test whether subsequent search behaviour was affected. Individuals were exposed to differently textured walls, channelled out along a wall, or released in contact with no, one, or two walls. A corner arrangement of surfaces, where individuals started near two walls at right angles, produced behaviour that differed from that of other configurations; animals chose one wall and then maintained a close distance from the wall along which they were moving. The distance from a wall adopted by a crayfish walking parallel to it was affected by the texture of the wall. These results on the influence of tactile stimuli on crayfish exploratory behaviour may have implications for other taxa.
    Journal of Experimental Biology 03/2006; 209(Pt 3):567-75. · 3.24 Impact Factor
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    ABSTRACT: This study explored the distribution of parathyroid hormone-related protein (PTHrP) and its mRNA in tissues of the lamprey Geotria australis, a representative of one of the two surviving groups of an early and jawless stage in vertebrate evolution. For this purpose, antibodies to N-terminal and mid-molecule human PTHrP were used to determine the locations of the antigen. Sites of mRNA production were demonstrated by in situ hybridisation with a digoxigenin-labelled riboprobe to exon VI of the human PTHrP gene. The results revealed that antigen and its mRNA were widely distributed among similar sites of tissue localisation to those described for mammalian and avian species. However, some novel sites of localisation, such as in the gill and notochord, were also found. Some differences in PTHrP localisation were noted among individuals at different intervals of the life cycle, indicating that the distributions of PTHrP, and possibly its roles, change with the stage of development in this species. The widespread tissue distribution in G. australis implies diverse physiological roles for this protein. The presence of PTHrP in the lamprey, a representative of a group of vertebrates, which apparently evolved over 540 million years ago, strongly suggests that it is a protein of ancient origin. In addition, the successful use of antibodies and probes based on the human sequence in the lamprey also provides evidence that the PTHrP molecule may have been conserved from lampreys through to humans.
    Development Genes and Evolution 12/2005; 215(11):553-63. · 1.70 Impact Factor
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    Adrian McMahon, Blair W Patullo, David L Macmillan
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    ABSTRACT: Many crayfish species inhabit murky waters or have a crepuscular lifestyle, which forces them to rely on chemical and mechanical information rather than visual input. Information on how they use one form of mechanical information-tactile cues-to explore their local environment is limited. We observed the exploratory behavior of the crayfish Cherax destructor in a T-maze under red light. Animals moved forward along the long arm of the maze and then moved equally in one of two available directions. The arm chosen by one crayfish did not affect that selected by a second crayfish tested immediately after in an unwashed maze. Previous experience in the maze also did not affect the choice. We found, however, that crayfish with one antenna denervated or splinted back to the carapace turned more often toward the unaltered side. Our data support the hypothesis that crayfish bilaterally compare information from their antennae.
    Biological Bulletin 07/2005; 208(3):183-8. · 1.23 Impact Factor
  • Daniela Lupone, David L. Macmillan
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    ABSTRACT: The morphology and physiology of the MC1 mero-carpopodite organ of the crayfish Cherax destructor was compared with those of the better known northern hemisphere species and found to be closely similar. The nerves to the organ were prepared using a fine dissection technique and backfilled with Cobalt chloride to reveal the central endings. This first description of the central endings of a crayfish proprioceptor reveals that it has relatively restricted distribution in the ventral, ipsilateral hemiganglion. The similarity with results from insects is discussed.
    Journal of Experimental Zoology 06/2005; 249(3):241 - 246.
  • D. L. Macmillan, J. S. Altman, J. Kien
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    ABSTRACT: Stein ('71, '74) demonstrated that lesions in areas 78 and 81 of the nerve cord of the crayfish Procambarus affected intersegmental coordination. In these areas he found neurons which appeared to be local interneurons and whose discharge was correlated with motor discharge in the swimmeret roots. He suggested that these neurons might be responsible for intersegmental coordination and termed them coordinating fibres. We reexamined the same areas of the ventral nerve cord in the crayfish Cherax by recording extracellularly from small bundles of axons during rhythmic activity in the swimmeret motor nerves. All the units we located that exhibited correlated discharge appeared to be plurisegmental. Physiological examination revealed that such units may be sensory, motor, or interneurons. We confirmed this finding morphologically by staining some of the units intracellularly with cobalt. Deafferentation experiments and the effects of stimulating units showing correlated discharge suggest that all three types of neurons may be involved in intersegmental coordination. We conclude that the that the present coordinating fibre model should be abandoned.
    Journal of Experimental Zoology 05/2005; 228(1):157 - 162.
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    R Crook, B W Patullo, D L Macmillan
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    ABSTRACT: There is some evidence that macrurans recognize each other as individuals. In freshwater crayfish there are conflicting reports and there is limited information about the sensory mechanisms involved. To determine the extent to which the crayfish Cherax destructor is capable of individual recognition, we performed experi-ments that familiarized animals with each other and then manipulated their recent success in dominance con-tests. Crayfish were more likely to win an encounter when paired against a familiar opponent than an unfamiliar one after the manipulation stage. In other experiments, animals were attracted to familiar conspe-cifics when only visual or chemical cues were present. This demonstrates that C. destructor is able to discrimi-nate between a familiar and an unfamiliar opponent. The results highlight the complex nature of intraspecific communication in crayfish and suggest elements likely to be of importance in the social interactions of groups in the wild state.
    Marine and Freshwater Behaviour and Physiology 12/2004; 37:271-285. · 0.88 Impact Factor
  • Blair W Patullo, David L Macmillan
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    ABSTRACT: Aquatic animals generate electrical field potentials which may be monitored by predators or conspecifics. Many crustaceans use rapid, forceful contractions of the flexor and extensor muscles to curl and extend their abdomens during swimming in escape and locomotion. When crayfish swim they generate electrical field potentials that can be recorded by electrodes nearby in the water. In general, it is reasonable to assume that larger bodied crayfish will generate signals of greater amplitude because they have larger muscles. It is not known, however, how activity in particular muscles and nerves combines to produce the compound electrical waveform recorded during swimming. We therefore investigated the relationship between abdominal muscle, body size and the amplitude of nearby tailflip potentials in the freshwater crayfish (Cherax destructor). We found that amplitude was correlated positively with abdominal muscle mass. The mean amplitude recorded from the five smallest and five largest individuals differed by 440 microV, a difference sufficiently large to be of significance to predators and co-inhabitants in the wild.
    Comparative Biochemistry and Physiology - Part A Molecular & Integrative Physiology 10/2004; 139(1):77-81. · 2.17 Impact Factor
  • B McCarthy, A Daws, D L Macmillan
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    ABSTRACT: Recordings were made from the nerve innervating the stretch receptors of the abdominal muscle receptor organs and slow extensor muscles of tethered crayfish, Cherax destructor, during so-called "non-giant swimming". The stretch receptors were active during the flexor phase of swimming but the duration and pattern of activity varied from cycle to cycle. Their pattern of firing was modified by the activity of the large accessory neurons which make direct inhibitory synapses upon them. Neither the stretch receptors nor the accessory neurons were active during the extensor phase of the cycle. The timing and extent of tailfan movements during the period of stretch receptor activity were measured from video records before and after the stretch receptor nerves were cut in the second to fifth segments. The promotion of the tailfan during flexion was significantly delayed and the minimum angle to which the uropods were remoted at the end of flexion significantly larger in denervated animals. We propose that afferent information from the stretch receptors coordinates the timing and extent of tailfan movements according to variations in the positioning and movement of the abdominal segments such that the hydrodynamic efficiency of the tailfan is enhanced on a cycle by cycle basis during non-giant swimming.
    Journal of Comparative Physiology 05/2004; 190(4):291-9. · 1.86 Impact Factor
  • Joanne M Drummond, David L Macmillan
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    ABSTRACT: Associated with the abdominal muscle receptor organs of crayfish are accessory neurons that inhibit the activity of the stretch receptors. Cobalt infusion into their cut axons reveals four accessory somata associated with each hemiganglion in the abdomen of the crayfish Cherax destructor. These conform to the pattern described previously for these neurons: The cell bodies are in the ganglion posterior to the one from which they exit. We recorded intracellularly from the largest accessory neurons, Acc-1 and Acc-2, and stained them with intracellular dye to establish unambiguously the characteristics defining their identity and structure. We describe their branching patterns in the ganglion of origin and the ganglion of exit. This morphological information permitted us to distinguish all four accessory neurons in preparations with dye infused through their cut axons, and we propose a revised, unambiguous nomenclature for the two smaller ones. Our intracelluar recordings allowed us to reexamine the physiological relationships of Acc-1 and Acc-2, the only accessory neurons for which there are data in the literature. In general, the connections and inputs described in previous studies were substantiated, although there has clearly been confusion between the two, and they differ in a number of significant ways. We found that they are seldom active together, have different firing patterns, and may operate with different clusters of extensor and flexor motorneurons. The results illustrate the level at which the accessory neurons operate within the abdominal control system but do not distinguish between competing hypotheses concerning their role in behavior. The data are consistent with the view that accessory neurons assist in timing between adjacent segments.
    The Journal of Comparative Neurology 03/2004; 469(4):548-58. · 3.66 Impact Factor

Publication Stats

291 Citations
89.22 Total Impact Points

Institutions

  • 2003–2010
    • Victoria University Melbourne
      Melbourne, Victoria, Australia
  • 1983–2010
    • University of Melbourne
      • Department of Zoology
      Melbourne, Victoria, Australia
  • 2002
    • University of Vic
      Vic, Catalonia, Spain