Chemical Trails Research Articles

Biological Self-Organization by Way of Microtubule Reaction−Diffusion Processes

This article addresses the physical chemical processes underlying biological self-organization by which a homogeneous solution of reacting chemicals spontaneously self-organizes. Theoreticians have predicted that self-organization can arise from a coupling of reactive processes with molecular diffusion. In addition, the presence of an external field such as gravity, at a critical moment early in the process may determine the morphology that subsequently develops. The formation, in vitro, of microtubules, a constituent of the cellular skeleton, shows this type of behavior. Preparations spontaneously self-organize by reaction−diffusion, and the morphology that develops depends on the presence of gravity at a critical bifurcation time early in the process. Numerical simulations of a population of microtubules involving only reactive and diffusive terms reproduce this behavior. Microtubules can grow from one end while shrinking from the other. The shrinking end leaves behind itself a chemical trail of high tubulin concentration. Neighboring microtubules preferentially grow into these regions, while avoiding regions of low concentration. The chemical trails produced by individual microtubules thus activate and inhibit the formation of their neighbors, and this progressively leads to self-organization. Gravity acts by way of its directional interaction with the macroscopic density fluctuations present in the solution arising from microtubule disassembly. Evidence is presented that similar processes might occur both during the cell cycle and the early stages of Drosophila fruit fly embryogenesis.

Predatory behavior and chemical communication in two Metapone species (Hymenoptera:Formicidae)

Colonies of two species of Metapone (M. madagascarica, M. new species.) were collected in Madagascar and established in laboratory nests. It could be demonstrated that both species are specialist predators of termites (Cryptotermes kirbyi). During hunting the ants sting the termites and thereby paralyze and preserve the prey alive. In this way prey can be stored in the ant nest for extended periods. During foraging and colony emigrations the ants lay chemical trails with poison gland secretions. Among the seven compounds identified in the venom only methyl pyrrole-2-carboxylate elicits trail following behavior in both Metapone species.

The Ability of Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) to Locate and Attack the Pupae of the Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under Seminatural Conditions

In Latin America, the diapriid Coptera haywardi (Ogloblin) attacks the pupae of tephritid fruit flies. Anastrepha spp. are among its natural hosts, but in the laboratory it also develops in the exotic Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Field cage tests demonstrated that C. haywardi could locate and parasitize Mediterranean fruit fly pupae under seminatural conditions as found in a Guatemalan coffee plantation. A mean of 18.3% of the pupae buried artificially at depths of 5 mm were parasitized by C. haywardi, while those buried at 15 mm suffered 3.2% parasitism. In a laboratory experiment, larvae that buried themselves to pupate were not significantly more likely to be parasitized than artificially buried pupae, although they may have left a physical or chemical trail that betrayed their presence. Thus, the artificial burial of pupae is unlikely to grossly underestimate C. haywardi efficacy in the field. Another field cage test found that mortality levels due to unsuccessful parasitoid attacks were similar to those resulting from successful parasitism. Thus, the actual effect of a mass-release might be considerably greater than that suggested from parasitism data alone. The results are considered sufficiently positive to encourage further testing of C. haywardi as a biological control agent of the Mediterranean fruit fly. © 2002 Elsevier

Numerical simulations of microtubule self-organisation by reaction and diffusion.

This article addresses the physical chemical processes underlying biological self-organisation by which a homogenous solution of reacting chemicals spontaneously self-organises. Theoreticians have predicted that self-organisation can arise from a coupling of reactive processes with molecular diffusion. In addition, the presence of an external field, such as gravity, at a critical moment early in the process may determine the morphology that subsequently develops. The formation, in-vitro, of microtubules, a constituent of the cellular skeleton, shows this type of behaviour. The preparations spontaneously self-organise by reaction-diffusion and the morphology that develops depends upon the presence of gravity at a critical bifurcation time early in the process. Here, we present numerical simulations of a population of microtubules that reproduce this behaviour. Microtubules can grow from one end whilst shrinking from the other. The shrinking end leaves behind a chemical trail of high tubulin concentration. Neighbouring microtubules preferentially grow into these regions, whilst avoiding regions of low tubulin concentration. The chemical trails produced by individual microtubules thus activate and inhibit the formation of neighbouring microtubules and this progressively leads to self-organisation. Gravity acts by way of its directional interaction with the macroscopic density fluctuations present in the solution arising from microtubule disassembly.

Formation and fate of marine snow: small-scale processes with large- scale implications

Marine snow aggregates are believed to be the main vehicles for vertical material transport in the ocean. However, aggregates are also sites of elevated heterotrophic activity, which may rather cause enhanced retention of aggregated material in the upper ocean. Small-scale biological-physical interactions govern the formation and fate of marine snow. Aggregates may form by physical coagulation: fluid motion causes collisions between small primary particles (e.g. phytoplankton) that may then stick together to form aggregates with enhanced sinking velocities. Bacteria may subsequently solubilise and remineralise aggregated particles. Because the solubilization rate exceeds the remineralization rate, organic solutes leak out of sinking aggregates. The leaking solutes spread by diffusion and advection and form a chemical trail in the wake of the sinking aggregate that may guide small zooplankters to the aggregate. Also, suspended bacteria may enjoy the elevated concentration of organic solutes in the plume. I explore these small-scale formation and degradation processes by means of models, experiments and field observations. The larger scale implications for the structure and functioning of pelagic food chains of export vs. retention of material will be discussed.

The influence of the physical environment on the self-organised foraging patterns of ants

Among social insects such as ants, scouts that modulate their recruiting behaviour, following simple rules based on local information, generate collective patterns of foraging. Here we demonstrate that features of the abiotic environment, specifically the foraging substrate, may also be influential in the emergence of group-level decisions such as the choice of one foraging path. Experimental data and theoretical analyses show that the collective patterns can arise independently of behavioural changes of individual scouts and can result, through self-organising processes, from the physico-chemical properties of the environment that alter the dynamics of information transfer by chemical trails.

Trail Communication During Foraging and Recruitment in the Subterranean Termite Reticulitermes santonensis De Feytaud (Isoptera, Rhinotermitidae)

The search for food in the French subterranean termite Reticulitermes santonensis De Feytaud is organized in part by chemical trails laid with the secretion of their abdominal sternal gland. Trail-laying and -following behavior of R. santonensis was investigated in bioassays. During foraging for food termites walk slowly (on average, 2.3 mm/s) and lay a dotted trail by dabbing the abdomen at intervals on the ground. When food is discovered they return at a quick pace (on average, 8.9 mm/s) to the nest, laying a trail for recruiting nestmates to the food source. While laying this recruitment trail the workers drag the abdomen continuously on the ground. The recruitment trail is highly attractive: it is followed within a few seconds, by more nestmates, and at a quicker pace (on average, 6.4 mm/s) than foraging trails (on average, 2.9 mm/s). The difference between foraging and recruitment trails in R. santonensis could be attributed to different quantities of trail pheromone. A caste-specific difference in trail pheromone thresholds, with workers of R. santonensis being more sensitive to trails than soldiers, was also documented: soldiers respond only to trails with a high concentration of trail pheromone.

Fluid motion and solute distribution around sinking aggregates. II. Implications for remote detection by colonizing zooplankters

Marine snow aggregates are colonized by copepods, and encounter rates inferred from observed abundances of colonizers are high. We examined the potential for hydromechanical and chemical remote detection. The fluid disturbance generated by a sinking aggregate was described by solving the Navier-Stokes' equation for a sinking sphere at Reynolds numbers typical of marine snow (up to 20). Fluid deformation rate, the component of the flow that can be perceived by copepods, attenuates rapidly, and detection distances estimated from knowledge of the hydromechanical sensi- tivity in copepods are insufficient to account for the observed abundances of colonizers. We next solved the advection-diffusion equation to describe the chemical trail left by a leaking and sinking aggregate. The plume is long and slender and may be detected by a horizontally cruising copepod. From the model of the plume and literature-based estimates of size-dependent aggregate leakage rates of amino acids, we estimate that a threshold sensitivity to amino acids of 0.4 〈 10 -7 M is required to account for observed abundances of colonizers. This is consistent with knowledge of the amino acid concentrations needed to elicit behavioral responses in copepods.

Pattern formation and optimization in army ant raids.

Army ant colonies display complex foraging raid patterns involving thousands of individuals communicating through chemical trails. In this article we explore, by means of a simple search algorithm, the properties of these trails in order to test the hypothesis that their structure reflects an optimized mechanism for exploring and exploiting food resources. The raid patterns of three army ant species, Eciton hamatum, Eciton burchelli, and Eciton rapax, are analyzed. The respective diets of these species involve large but rare, small but common, and a combination of large but rare and small but common food sources. Using a model proposed by Deneubourg et al. [4], we simulate the formation of raid patterns in response to different food distributions. Our results indicate that the empirically observed raid patterns maximize return on investment, that is, the amount of food brought back to the nest per unit of energy expended, for each of the diets. Moreover, the values of the parameters that characterize the three optimal pattern-generating mechanisms are strikingly similar. Therefore the same behavioral rules at the individual level can produce optimal colony-level patterns. The evolutionary implications of these findings are discussed.

Remote prey detection in Oithona similis: hydromechanical versus chemical cues

We quantified prey encounter rates and prey reaction distances in the ambush-feeding cyclopoid copepod Oithona similis by video recording freely swimming copepods at different concentrations of prey, the dinoflagellate Gymnodinium dominans. Prey encounter rate increased with prey concentration, and a maximal clearance rate of 0.42 ± 0.10 ml h–1 was estimated. The average distance (from the antennules) at which O.similis reacts to prey is 0.014 ± 0.007 cm. A simple prey encounter model was used to combine observed predator and prey velocities and prey reaction distance, and yielded a clearance rate similar to that estimated directly from prey encounter rates. The observed prey reaction distance was consistent with that estimated from a published model of hydromechanical prey perception. The possibility of remote chemodetection was examined by modeling the distribution of solutes leaking out of a swimming cell. The cell leaves a long slender chemical trail in its wake. However, since the ambush-feeding O.similis is essentially stationary when perceiving prey, it is the width rather than the length of the trail that matters. Owing to advection, the chemical signal vanishes almost instantaneously off the sides of the swimming flagellate, and solute concentrations are below any likely detection threshold within 40–50 μm from the flagellate. Our observations are thus inconsistent with remote chemodetection in O.similis. The considerations are generalized, and it is concluded that ambush-feeding copepods, unlike cruisers and suspension feeders, cannot utilize chemical signals for the detection of individual prey, but rely on either hydromechanical detection or direct interception of prey.

Social wasp swarm emigration: males stay behind

Many species of tropical social wasps initiate colonies by means of a swarm of queens and workers. Swarms either bud from mature colonies (reproductive swarms) or form from the entire adult population when it evacuates following destruction of the nest by predation or accident (absconding swarms). Colonies giving rise to founding swarms of either type may have males in their populations. Swarms emigrate along a chemical trail to a site selected by scouts, where the workers begin building a new nest. Published analyses of newly-founded colonies indicate that such colonies occasionally contain males. This raises the question of whether these are alien males who joined the new colony shortly after its founding, or are siblings of the females, having emigrated with them from the natal nest site. We used a double censusing technique to determine whether males of the Neotropical social wasp, Polybia occidentalis, emigrate with females in absconding swarms. Nine absconding swarms in Costa Rica were censused and sexed directly before they emigrated and were shown to contain males as well as females. When the swarms departed for the new site, males remained behind, and when the swarms were censused again soon after reaching their new sites, none contained males. Thus males of this species cluster temporarily with absconding females, but fail to emigrate with them. We suggest that the males’ failure to join pre-emergence colonies is in the best interest of both sexes.

HABITAT SELECTION AND PREY ODOR IN THE FORAGING BEHAVIOR OF WESTERN RATTLESNAKES (CROTALUS VIRIDIS)

AbstractWe tested the roles of prey odor and other habitat cues in the pre-strike movement patterns of two, ecologically distinct sub-species of the western rattlesnake in naturalistic arenas. In the first experiment, rattlesnakes preferred habitat containing prey odor and cover comprised of rocks, sticks and plants. While searching, rattlesnakes methodically investigated the edges and crevices within rock, areas rodents might frequent in nature. In the second experiment, rattlesnakes investigated sticks more than rocks arranged topographically similar to sticks. In the third experiment, rattlesnakes preferred habitat that included brush foliage and used chemical prey trails in pre-strike behavior via (i) trail-following, (ii) casting search patterns and (iii) scanning search patterns. Several snakes coiled in stereotyped ambush postures that allowed them to face chemical trails while resting against rocks and foliage. These results suggest that rattlesnake foraging exhibits qualities advantageous for hunting rodent prey in addition to providing protection from predators and perhaps promoting thermoregulation. Sub-species did not exhibit geographic variation in foraging behavior despite differences in natural history and morphology. Hence, the microevolutionary pattern suggests that generalized foraging repertoires are successful in numerous environments when coupled with locally specialized body patterns.

Discrimination between Envenomated and Nonenvenomated Prey by Western Diamondback Rattlesnakes (Crotalus atrox): Chemosensory Consequences of Venom

Snake venoms have multiple consequences on prey, ranging from immobilizing and digestive effects to enhancing the salience of envenomated prey and their chemical trails. Although the toxic and lytic effects are reasonably well understood, the chemosensory effects have been little studied. Experiment 1 showed that western diamondback rattlesnakes (Crotalus atrox) preferred envenomated (E) over nonenvenomated (NE) prey in a standardized choice situation, as other species have done in previous studies. In Experiment 2, E prey were prepared by injecting reconstituted lyophilized venom, so that dosage could be controlled, something not possible when snakes envenomated prey as in Experiment 1 and in most previous studies of rattlesnake response to E and NE prey. Prey injected with 10 mg of lyophilized venom were reliably discriminated from NE prey by C. atrox. A dose-response curve was established in Experiment 3 to assess the lowest dose to produce E prey that were preferred over NE prey. Two statistical techniques were used to estimate minimum perceptible dose (MPD), giving values of 6.0 and 7.1 mg, respectively. These values were compared with the amount of venom snakes actually injected during predatory strikes and with various measures of lethality. Chemosensory effects of venom probably facilitate rattlesnake predatory behavior in that adult rodents are usually released after envenomation, requiring that the snake follow the prey's trail to recover the carcass. This trail-following task depends upon the snake's ability to discriminate trails of E prey from those deposited in the vicinity by other (NE) rodents as they engaged in foraging activities.

Recruitment and trail communication in two species of Messor ants (Hymenoptera, Formicidae)

Behavioural patterns and chemical signals mediating recruitment communication of the harvesting ants M. minor and M. was‐manni were studied. Recruitment towards a food source was investigated in the laboratory. Bioassays showed that successful scouts induce nestmates to leave the nest by substances from Du‐four's gland. This gland was also found to be the source of the chemical trails by which foragers reach newly discovered feeding sites. Glandular secretions from the last abdominal tergites as well as from the poison gland induced typical alarm reactions, suggesting their involvement in alarm communication and recruitment towards a source of danger. Production of stridulations by scouts and recruited foragers was also recorded on the food items under both field and laboratory conditions. The possible role of such vibrational signals in foraging communication is discussed. Finally, a comparison of the communication systems employed by both species was made and some ecological implications are discussed.

Following the invisible trail: kinematic analysis of mate-tracking in the copepod Temora longicornis.

We have analysed the fine-scale kinematics of movement of male and female copepods, Temora longicornis, to resolve how these small animals find their mates. Location of the trail initially involves rapid random turning and high rates of directional change. Males subsequently increase their rate of movement as they follow the trail, and execute a regular pattern of counter turns in both x,z and y,z planes to stay near or within the central axis of the odour field. Pursuit behaviour of males is strongly associated with female swimming behaviour, suggesting that quantifiable variations in the structure of the odour signal released by females affects male tracking. The behavioural components of mate tracking in Temora are very similar to those of other animals that employ chemically mediated orientation in their search for mates and food, and we conclude that male Temora find their mates using chemoperception. The kinematic analysis indicates both sequential and simultaneous taxis mechanisms are used by Temora to follow the odour signal. This, in turn, indicates that rather than responding to a diffuse plume, males are following a signal more accurately characterized as a chemical trail, and copepods appear to use mechanisms that are similar to those employed by trail-following terrestrial insects such as ants. While Temora expresses similar behaviours to those of a variety of chemosensory organisms, the ability to track a three-dimensional odour trail appears unique, and possibly depends on the persistence of fluid-borne odour signals created in low Reynolds number hydrodynamic regimes.

Interspecific trail following and commensalism between the ponerine ant Gnamptogenys menadensis and the formicine ant Polyrhachis rufipes

Gnamptogenys menadensis (subfamily Ponerinae) foragers use chemical trails to home to their nests. Although prey capture and retrieval are generally performed solitarily, trails seem to enhance foraging to areas rich in prey or to sugar sources. Trail laying and following are most conspicuous during nest migration. These trails are laid down by tapping the sting onto the substrate. In laboratory tests, only extracts from the Dufour's gland were readily followed. Workers of Polyrhachis rufipes (Formicinae) use the trails of G. menadensis to gain access to otherwise nonavailable sugar sources. When they encounter Gnamptogenys foragers, P. rufipes workers show a typical aggressive antennal boxing, to which Gnamptogenys reacts with a submissive behavior. This is the first report of commensalism between a ponerine and a formicine ant.

Orientation ofPolyergus rufescens(Hymenoptera, Formicidae) during slave-making raids

We investigated the factors involved in the orientation of raiders of the European Amazon ant,Polyergus rufescensand how these factors are used by raiders during the different phases of slave-making expeditions. Ants at the head of the raiding column did not follow previously deposited chemical trails but oriented by celestial cues. Raiders in the middle of the column used celestial factors but were also strongly affected by the recruiting activity of the ants that preceded them. During the return trip, raiders used both chemical and celestial cues. The latter allowed the ants to assume the correct home direction while following the chemical trail. Perception of the ultraviolet band of the light spectrum was of crucial importance for the orientation of the raiders, during both the outbound and inbound journeys. This supports the hypothesis thatP.rufescensworkers, like other ants, perceive the pattern of polarized skylight in the ultraviolet range.

Scavenging byPheidole pallidulaa key for understanding decision-making systems in ants

The usual evolutionary and ecological approaches to foraging in social insects often lack an investigation at the level of both individual behavioural complexity and social mechanisms ruling the emergence of adaptive collective strategies. The prey scavenging behaviour of the dimorphic antPheidole pallidulawas used in this study to investigate (1) how individuals estimate the size of prey, (2) how they modulate their behaviour and communication and (3) how these modulations generate the diversity of collective foraging patterns. For a pile of small prey (fruit flies), the recruitment of foragers was slow because of the weak intensity of individual trail-laying behaviour and the long time spent by ants wandering around the food. In contrast, for a large prey item (a cockroach), strong recruitment was induced by ants that dashed back to the nest laying a more continuous chemical trail. Experiments with small immovable prey showed that the tractive resistance of prey was the key parameter the foragers used to estimate prey size and that it ruled their trail-laying intensity. These data allow us to generate a model about decision making in scavenging. The rules leading to collective choice in a foraging or an agonistic context are discussed. On the basis of these findings, some theoretical stances in sociobiology and some shortcomings in current approaches to cooperation in social insects are considered.

Oviposition behaviour inOstrinia nubilaus (Lep.: pyralidae) and consequences on host location and oviposition inTrichogramma brassicae (Hym.: Trichogrammatidae)

Before oviposition, Ostrinianubilalis Hubner females sweep the surface of the plant with their abdominal tip extruded. The consequences of such behaviour were studied on host searching and oviposition behaviours of the parasitoidTrichogramma brassicae Bezdenko. Egg-masses ofO. nubilalis, associated or not with sweeping, were submitted toT. brassicae females. The behaviour ofT. brassicae females appeared to be very different between the two situations. The parasitoid in the vicinity of an egg-mass associated with sweeping spent more time on the corn leaf. Ninety percent of females located the egg-mass with sweeping, whereas only 40% located the egg-mass without sweeping. Eighty three percent ofT. brassicae females parasitized egg-masses with sweeping, but only 10% in the case without sweeping. Although no deposit was visible, a chemical trail was probably left behind and was found to arrest the parasitoid, to promote host recognition and to trigger oviposition. The amount of the scales left behind on the corn leaf during the sweeping behaviour was also taken into account but did not appear to constitute the trail. The passage over the trail followed by the egg-mass examination constituted behavioural steps which seemed necessary for oviposition in theT. brassicae female

Communication in the migratory termite-hunting ant Pachycondyla (= Termitopone) marginata (Formicidae, Ponerinae)

The Neotropical species Pachycondyla marginata conducts well-organized predatory raids on the termite species Neocapritermes opacus and frequently emigrates to new nest sites. During both activities the ants employ chemical trail communication. The trail pheromone orginates from the pygidial gland. Among the substances identified in the pygidial gland secretions, only citronellal was effective as a trail pheromone. Isopulegol elicited an increase in locomotory activity in the ants and may function as a synergist recruitment signal. The chemical signal is enhanced by a shaking display performed by the recruiting ant.