Distance Chemoreception Research Articles

Contact chemoreception in multi-modal sensing of prey by Octopus.

Octopuses have keen vision and are generally considered visual predators, yet octopuses predominantly forage blindly in nature, inserting their arms into crevices to search and detect hidden prey. The extent to which octopuses discriminate prey using chemo- versus mechano-tactile sensing is unknown. We developed a whole-animal behavioral assay that takes advantage of octopuses' natural searching behavior to test their ability to discriminate prey from non-prey tastes solely via contact chemoreception. This methodology eliminated vision, mechano-tactile sensing and distance chemoreception while testing the contact chemosensory discriminatory abilities of the octopus arm suckers. Extracts from two types of prey (crab, shrimp) and three types of non-prey (sea star, algae, seawater) were embedded in agarose (to control for mechano-tactile discrimination) and presented to octopuses inside an artificial rock dome; octopuses reached their arms inside to explore its contents - imitating natural prey-searching behavior. Results revealed that octopuses are capable of discriminating between potential prey items using only contact chemoreception,as measured byan increased amount of sucker contact time and arm curls when presented with prey extracts versus non-prey extracts. These results highlight the importance of contact chemoreception in the multi-modal sensing involved in a complex foraging behavior.

Distance chemoreception and the detection of conspecifics in Octopus bimaculoides

Distance chemoreception and the detection of conspecifics in Octopus bimaculoides

A comparative ultrastructural investigation of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda)

Cephalic sensory organs (CSOs) are specialised structures in the head region of adult Opisthobranchia involved in perception of different stimuli. The gross morphology of these organs differs considerably among taxa. The current study aims at describing the cellular morphology of the CSOs in order to reveal cellular patterns, especially of sensory epithelia, common for opisthobranchs. Transmission electron microscopy was used to characterise the fine structure of the organs and to compare the CSOs of four different opisthobranch species. The cellular composition of the sensory system is conserved among taxa. The epidermal cells in sensory regions are always columnar and ciliated cells are frequently apparent. The sensory cells are primary receptors arranged in subepidermal cell clusters. They extend dendrites which penetrate the epithelium and reach the surface. Some of the dendrites bear cilia, whereas others only build a small protuberance. Processing of sensory information takes place in the peripheral glomeruli of all species. Moreover, few taxa possess additional peripheral ganglia at the base of their CSOs. The results of the present study might support other investigations indicating that the posterior CSOs are primarily involved in distance chemoreception, whereas the anterior CSOs might be used for contact chemoreception and mechanoreception.

Morphology and distribution of antennular setae of scyllarid lobsters (Scyllarides aequinoctialis, S. latus, and S. nodifer) with comments on their possible function

Abstract. Lateral flagella of the antennules of scyllarid lobsters were examined for setal morphology and distribution via scanning electron microscopy. Setal distribution patterns were mapped directly for 3 regions of the antennule (base, tuft, and tip) and analyzed for differences: (1) between left and right antennules, (2) between males and females within a species, and (3) among species by comparing counts of setae per annulus in the ventral tuft region only. Six types of antennular setae were identified based on their external morphology: aesthetases, simple, modified simple, asymmetric, hemi‐plumose, and toothbrush setae. These different types were organized in a clear pattern over the ventral and dorsal surfaces of the lateral flagella of the antennule. Aesthetase, asymmetric, modified simple, and hemi‐plumose setae were found only on annuli in the tuft region between the distal and proximal ends of the flagellum. Simple setae were found on all annuli of all regions of the antennule, and toothbrush setae were mainly concentrated on all annuli of the base region and on proximal annuli of the tuft region. All species of scyllarids examined had the same general pattern of setal distribution and no differences were found between left and right, or male and female antennules. Similar setae located on the lateral antennules of species from the families Nephrophidae and Palinuridae (clawed and spiny lobsters) have been previously described as chemo‐ and/or mechanoreceptive for use in distance chemoreception (i.e., detection and orientation to olfactory stimuli). Based on work on clawed and spiny lobsters, we predict that the aesthetases on slipper lobsters have a chemoreceptive function and that simple and toothbrush setae may have a bimodal chemo‐ and mechanoreceptive function.

Host location by larvae of a parasitic barnacle: larval chemotaxis and plume tracking in flow

Numerous studies describe stimulation and/or enhancement of larval settlement by distance chemoreception in response to chemical factors emitted by conspecific adults, host and prey species and microbial films. However, active upstream tracking of odor plumes, needed in order to locate specific, spatially limited settlement sites, has thus far received little scientific attention. This study examines host location in flow and still water by larvae of the parasitic barnacle Heterosaccus dollfusi, which inhabits the brachyuran crab Charybdis longicollis. Experiments included analysis of larval motion patterns under four conditions: still water, in flow, in still water with waterborne host metabolites and in flow with host metabolites. Our results show that H. dollfusi larvae are capable of actively and effectively locating their host in still water and in flow, using chemotaxis and rheotaxis and modifying their swimming pattern, direction, velocity, determination and turning rate to accommodate efficient navigation in changing environmental conditions.

The sensory epithelium of the tentacles and the rhinophore of Nautilus pompilius L. (cephalopoda, nautiloidea).

Nine intraepithelial ciliated cell types that are presumed to be sensory cells were identified in the epithelium of the pre- and postocular tentacles, the digital tentacles, and the rhinophore of the juvenile tetrabranchiate cephalopod Nautilus pompilius L. The morphological diversity and specialization in distribution of the different ciliated cell types analyzed by SEM methods suggest that these cells include receptors of several sensory functions. Ciliated cell types in different organs that show similar surface features were combined in named groups. The most striking cell, type I, is characterized by a tuft of long and numerous cilia. The highest density of this cell type occurs in ciliary fields in the epithelium of the lamellae of the pre- and postocular tentacles, in the olfactory pits of the rhinophores, and in the lamellae of four pairs of lateral digital tentacles, but not in the epithelium of the medial digital tentacles. The similar morphological data, together with behavioral observations on feeding habits, suggest that this cell type may serve in long-distance chemosensory function. The other ciliated cell types are solitary cells with specific spatial distributions in the various organs. Cell types with tufts of relatively short, stiff cilia (types III, IV, VIII), which are distributed in the lateral and aboral areas of the tentacles and at the base of the tentacle-like process of the rhinophore, are considered to be employed in mechanosensory transduction, while the solitary cells with bristle-like cilia at the margin of the ciliary fields (type II) and at the base of the rhinophore (type IX) may be involved in chemoreception. Histological investigation of the epithelium and the nerve structures of the different organs shows the proportion and distribution of the sensory pathways. Two different types of digital tentacles can be distinguished according to their putative functions: lateral slender digital tentacles in four pairs, of which the lowermost are the so-called long digital tentacles, participate in distance chemoreception, and the medial digital tentacles, whose terminal axial nerve cord may represent a specialized neuromechanosensory structure, appear to have contact chemoreceptive abilities.

Behavioural responses of competent lobster postlarvae to odor plumes

We determined the ability of competent laboratory-reared Homarus americanus postlarvae to use odor plumes as a potential mechanism of orientation during the habitat selection process at settlement. In a Y-maze apparatus, both swimming direction (upstream or downstream) and arm selection (control or experimental) were strongly influenced by the nature of the chemical stimulus tested. In control conditions (unconditioned water in both proximal arms of the experimental device), postlarvae swam predominantly upstream (61:39) but displayed no arm preference (48:52). When submitted to a metabolite solution of adult conspecifics or macroalgae, postlarvae swam consistently upstream (≥73%) and showed a significant preference for the arm providing these stimuli (≥69%). In contrast, postlarvae submitted to cunner (Tautogolabrus adspersus) metabolites swam predominantly downstream (68:32), and those that did swim upstream significantly avoided the experimental arm (30:70). In repeated trials with the same individuals, postlarvae behaved similarly in ≥80% of the assays, suggesting a low intra-individual variability in behavioural responses. It is concluded that distance chemoreception may play a role in habitat selection by lobster postlarvae at settlement.

Probopyrus pandalicola (Packard) (Isopoda; Epicaridea): swimming responses of cryptoniscus larvae in water conditioned by hosts Palaemonetes pugio (Holthuis) (Decapoda; Palaemonidae)

Swimming responses of Probopyrus pandalicola (Packard) cryptoniscus larvae to water solutions either conditioned or unconditioned by hosts were determined using a simple Y-tube choice apparatus. Results document that larvae swim at random or downstream with respect to water current in unconditioned control solutions. In the presence of either “crude extract” or “host-metabolite” solution, prepared using definitive hosts Palaemonetes pugio (Holthuis), cryptonisci are strongly rheopositive. However, upstream swimming cryptonisci swam toward the source of the host-conditioned water (i.e., made the correct ‘choice’) only when it was rather concentrated; when ‘host-metabolite’ solution was employed, rheopositive parasite larvae swam toward control solution as frequently as toward the experimental solution. We conclude that distance chemoreception may play a role in host finding by P. pandalicola.

Feeding biology and ecological impact of an introduced nudibranch,Tritonia plebeia, New England, USA

The nudibranchTritonia plebeia (Johnston) was first observed in New England in 1983, on vertical rock walls at 7 m depth off Nahant, Massachusetts. This northern European species preys exclusively on the soft coralAlcyonium digitatum (Linneaus) in its natural habitat. At Nahant, it preyed primarily on the closely relatedAlcyonium siderium Verrill. Laboratory studies indicated that it could locate its prey by distance chemoreception and by visual orientation towards tall dark surfaces which could help it find the vertical walls, overhangs, and boulder sides where the soft corals occur. Field studies showed thatT. plebeia fed primarily on colony bases, causing extensive damage and whole colony mortality. The most important endemic predator onA. siderium, Coryphella verrucosa (Sars), preyed preferentially on hydroids, but would graze polyps off the top portions ofA. sederium colonies, causing little permanent damage to the colony, during the winter months when hydroids were scarce. AlthoughC. verrucosa occasionally behaved agonistically towardT. plebeia, there was no indication in laboratory or field studies that either nudibranch had an effect on the other's foraging through interference competition. Extensive predation byT. plebeia caused the disappearance ofA. siderium at two sites (Outer and Inner Shag Rocks) and a sharp reduction at a third site (Inner East Point). The higher mortalities at the Shag Rocks sites most likely occurred because of a simultaneous urchin (Strogylocentrotus droebachiensis) population expansion. As space among aggregates ofA. siderium opened up due toT. plebeia predation, urchins were able to forage on the vertical walls and scrape off remaining colonies. At a fourth site, Halfway Rock, whereT. plebeia were seldom present,A. siderium colonies also suffered high mortalities. This increae in mortality began nearly a year before urchin populations increased, and during a summer of abnormally high water temperatures at Halfway Rock. The high temperatures, followed by urchin predation on remaining colonies could account for the disappearance of allA. siderium colonies at this site.T. plebeia disappeared at all sites by summer 1986 andA. siderium populations have since stabilized, but community-level changes at all sites whereA. siderium were removed have persisted.

Operculum closing as a defence against predatory leeches in four British freshwater prosobranch snails

The defence reaction of operculum closing in response to the presence of the molluscivorous leech Glossiphonia complanata (L.) and the non-molluscivorous Erpobdella octoculata (L.) was studied in four species of freshwater prosobranch gastropod. Bithynia tentaculata (L.) and Valvata piscinalis (Muller) can distinguish between the leeches, reacting only to G. complanata. V. piscinalis is capable of a greater degree of distance chemoreception of the leech ‘scent’. Valvata cristata Muller and Potamopyrgus jenkinsi (Smith) did not react to either leech. V. cristata may not be a potential prey item for G. complanata, while P. jenkinsi is fed on by the leech, but is a relative newcomer to the freshwater fauna.

Chemoreception in Luidia clathrata (Echinodermata: Asteroidea): qualitative and quantitative aspects of chemotactic responses to low molecular weight compounds

Chemoreception was studied in Luidia clathrata (Say), collected from Old Tampa Bay, Florida, USA, in June 1983. L. clathrata has chemotactic responses to compounds associated with its preferred dietary items. This seastar responded most strongly to L-cysteine, L-cystine, L-isoleucine and L-glutamic acid, compounds associated with fleshy animal foods. Sugars (sucrose, maltose and lactose), compounds associated with plant and detrital foods, were also stimulatory, but less so than the aminoacids. The seastar showed a strong response to the freshtissue component, betaine. The excretory product ammonium, indicative of metabolic activity of live prey, elicited a weak response. Chemotactic responses were concentration-dependent. Concentration-response curves for L-cysteine, L-isoleucine, and L-glutamic acid are steeply sloped and have response-dose50 values within the range of 1×10-8 and 1×10-5 M. L. clathrata is adapted to sensing concentration gradients at levels which could be expected in its environment. Distance chemoreception is an important component of both search behavior and food discrimination for this seastar.

Ventilation rate and arousal in the Octopus

Observations on undisturbed, individually isolated, Octopus vulgaris Cuvier show that ventilation rate is strongly related to “arousal” or activation. Ventilation rate may be recorded visually by a screened observer or remotely, using carbon electrodes connected to a pen recorder via an impedance coupler to register the associated water movements in a small experimental chamber. The method allows a quantifiable behavioural characteristic to be measured objectively. It has been used to demonstrate that O. vulgaris responds to certain chemical stimuli in flowing sea water with a sharply increased ventilation rate. This result is taken to show distance chemoreception in this cephalopod.

Chemoreception by the asteroid Cross aster papposus (L.)

Chemoreception abilities were demonstrated in the solasterid asteroid Crossaster papposus (L.) from a level substratum in the current-swept Crouch Estuary, England. C. papposus showed wide variability of positive and negative responses to crude extracts of prey species and (unattractive) conspecifics. C. papposus has an olfactory (distance chemoreception) ability to whole, live potential prey and conspecifics. This was confirmed by contact chemoreception responses, which are stronger, to the same stimuli. The olfaction tests in the Y-maze yielded variable results in which the initial (rheopositive or rheonegative) responses demonstrated that conspecifics and prey species were avoided yet subsequent arm choices of rheopositive individuals showed significant selection for prey over controls and no avoidance of conspecifics. The arm choices for prey relate to a priority of orientation to food and feeding over intraspecific avoidance in hungry asteroids. Intraspecific avoidance functions more in dispersion than prevention of cannibalism and is less important than feeding to hungry asteroids. Interpretation of chemically-mediated responses of asteroids requires appreciation of their innate behavioural variability which has led to confusion in the literature. This is the first experimental study of contact and distance chemoreception among solasterids. Their chemosensory abilities have previously been contradictory which may be due to intraspecific avoidance in satiated individuals of some species.

EFFECTS OF NO. 2 FUEL OIL ON CHEMICALLY-EVOKED FEEDING BEHAVIOR OF THE MUD SNAIL, ILYANASSA OBSOLETA

ABSTRACT Chemically-mediated feeding responses of the mud snail, Ilyanassa obsoleta, were evaluated after exposure to various fractions and concentrations of No. 2 fuel oil in a continuous flow-through seawater system. This type of feeding response involves chemical perception of and movement toward a point source of food followed by feeding through an extended proboscis. To investigate the effects of oil on this behavior, two types of bioassays were employed. In the first, arousal was used as a criterion to document effects on initial perception of food (olfaction or distance chemoreception). This initial phase of the feeding response is particularly susceptible to disruption by oil, with significant inhibition occurring after 48 hours exposure to concentrations as low as 0.015 ppm of an oil-in-water dispersion (OWD) and 0.43 ppm of the water-accommodated fraction (WAF). In the second bioassay, extension of the proboscis was used as a criterion to document effects on subsequent tasting or contact chemoreception. This later phase of feeding is less sensitive to oil, with significant inhibition occurring only after one month exposure to 0.49 ppm WAF, or after 48 hours exposure to concentrations in excess of 1 ppm (1.45 ppm OWD and 5.97 ppm WAF). Other, more obvious effects, including mortality, were observed at these two higher dose levels. This work illustrates the ability of extremely low levels of petroleum hydrocarbons to impair vital behavioral processes in marine organisms.

Distance Chemoreception and Vision in the Selection of Prey by American Lobster (Homarus americanus)

Lobsters responded positively to the waterborne odor of intact living crabs (Carcinus maenas), sea urchins (Strongylocentrotus droebachiensis), and mussels (Mytilus edulis). The frequency of response was higher and the response time shorter to crabs than to sea urchins or mussels. Lobsters also responded to the sight of moving crabs or moving sea urchins, but not to the sight of stationary specimens. Crabs are probably more attractive to lobsters because of their odor and their greater activity, compared with sea urchins or mussels. Key words: lobsters, prey, chemoreception, vision, crabs, sea urchins, movement, odor

Chemoreception in the antennule of the lobster,Homarus americanus

Chemoreceptors in the lobster antennule respond electrophysiologically to a large range of pure chemical substances including amino acids, sugars, alcohols, amines and fatty acids, in several cases down to thresholds below 10−6 or 10−7 M. Test substances were introduced by pipette into a current of sea water flowing over the isolated antennule and responses were recorded by hook electrode from small nerve fibre bundles in the antennular nerve. In many nerve bundles the responses consisted of multiunit activity, no individual nerve spikes being identifiable, while in other bundles large spikes due to one or more single receptor neurones were present. There are striking differences in response spectrum between the single and multiunit responses, which with other evidence suggest the presence of two major classes of antennular chemoreceptor. The results support the idea that in the lobster and other Crustacea the antennules are the site of sensitive chemoreceptors mediating such distance chemoreception responses as seen in trapping behaviour.

THE NUTRITION OF PARANEMERTES PEREGRINA (RHYNCHOCOELA: HOPLONEMERTEA). I. STUDIES ON FOOD AND FEEDING BEHAVIOR.

1. Paranemertes peregrina, an abundant hoplonemertean in rocky and muddy intertidal habitats of Washington, feeds on polychaetes during low tide periods. 2. Feeding by Paranemertes involves three steps. The first stage is a recoil of the Paranemertes' head upon contact with a prey. Contact must be made with the prey; Paranemertes does not find prey by distance chemoreception. The proboscis is everted and wraps around the prey in step two. The prey is temporarily paralyzed or is killed. In step three the prey is ingested by means of sucking motions from muscles around the mouth. Defecation occurs from 12 to 33 hours after feeding. 3. Specimens of Paranemertes ate mainly nereid polychaetes at the three study areas where nereids were available. At the fourth study area the nemerteans ate a wider variety of polychaetes. Experiments to test food preference showed that specimens of Paranemertes from all study areas strongly preferred nereids to members of other polychaete families. 4. Nereid polychaetes have a swimming escape response from Paranemertes.

Homing and "ortsteue" (attachment to place) in Patella L. (Gastropoda, Prosobranchia)

It is known that numerous gastropods show homing ability. Many limpets return to well defined sites. Patella L. acquires a home spot also on the smooth glass surfaces of aquarium. Before leaving, the limpet scrapes its home, particularly the anterior part of the footprint. After each return it makes characteristic movements with its shell.When homing Patella nearly always retraces its outward track, at least in part; sometimes it reaches its home over the shortest route possible.Site and tracks are marked by chemical substances. The animal orientates itself by contact chemoreception on the track and by distance chemoreception when near its home. Apparently there also exists a kinesthetic mechanism of orientation based on a measurement of distance on the outward journey.At the home spot Patella always manoeuveres exactly into the same position. Often it has to turn or to glide around slightly. It finally settles down with small movements of its shell.The footprint shows chemical differences in a wide marginal zone. Probably, different chemoreceptors on the sole of the foot are associated to the various regions of the footprint.The chemical differentiation of the footprint has the same orientation-value for all individuals of the same size group. In addition there exists an individual marking, shown e.g. by avoidance reactions of alien animals.The individual specificity of the foot's secretum is particularly marked on the tracks, for each Patella follows its own trail only and thus normally reaches its own home. On an uneven substratum this is the only place where the margin of its shell fits the ground exactly.For establishing a home site and keeping to it, several environmental conditions have to be met. Patella settles only on surfaces overgrown with small algae. In an aquarium it favours the sides most exposed to light. On vertical walls the animal is gravity-oriented. Most limpets are attached head-end down. Patella is able to perceive the distance from the water-line, and may orient itself with respect to fixed objects in the aquarium by means of a "Ferntastsinn". When first choosing a home spot on an uneven substratum, the limpet often adjusts its position by turning movements, so that the contacts between shell and ground are as close as possible. Selective growth at the shell's margin then results in a perfect fit to the irregularities of the ground.All prerequisites for the establishment of a home site are also determining the animal's keeping to its home. If changes are introduced with respect to the fitting of the shell to the ground, to the position of neighbouring objects, to water-level, light, or direction of gravity, the animal may leave its home site and reorient itself in an equivalent new one. The attractiveness of the chemical markings of the old site nevertheless compete with all these conditions for some time.Rest and activity are controlled by light-dark and tidal cycles. - Inter-and intraspecific differences were obtained under experimental conditions. Almost all individuals were preferentially active in darkness. P. caerulea moved at high tide; P. vulgata was active either at low tide only, or both at high and low tide, or - rarely-at high tide only. All animals reacting to tidal rhythms were synchronized even by unnaturally frequent changes in the water-level. The tidal dependence of the activity of individual P. vulgata may perhaps be interpreted as the persistence of an adaptation to drought and submergence acquired at the original habitat. The reactive ability towards high and low tide can be modified. The activity-phase may be stopped prematurely by changing light or tidal conditions. Animals keeping constantly to their homes returned to them at once, whereas others - having no defined home -generally prolonged their excursions. When light and water-level are kept constant the locomotory activity of P. vulgata and P. caerulea has the characteristics of an endogenous tidal rhythm. Changes in water-level soon approximately catch the freerunning periodicity, alteration of light and darkness synchronize it less readily but more precisely.

Escape responses of three herbivorous gastropods to the predatory gastropod Conus textile

Summary The herbivorous gastropods Strombus canarium, Lambis lambis, and Trochus pyramis evince escape responses, probably mediated by distance chemoreception, in the presence of the predatory gastropod Conus textile. In Strombus and Lambis, the response has two components: increase in the absolute rate of locomotion, and direction of locomotion away from the predator. When placed in the presence of C. textile, T. pyramis began moving, generally in the direction it faced. In control observations, a specimen of S. canarium moved at a mean rate of 2·7 mm/sec, by the leaping mode of locomotion characteristic of this and related genera. In the presence of C. textile, the rate increased to 6·8 mm/sec, due primarily to shortening of the lag or recovery period between leaps. In the presence of C. textile, a specimen of L. lambis moved at a rate of 11·9 mm/sec in the same manner as Strombus. In the presence of C. textile, a specimen of T. pyramis progressed at a rate of 1·9 mm/sec, by pedal locomotory waves. Comparison with absolute rates of locomotion by pedal locomotory waves in other marine gastropod molluscs leads to the conclusion that the leaping of Strombus and Lambis does not enable these gastropods to maintain a more rapid long-term rate of movement, but it confers a striking increase in agility, and a single leap provides an almost instantaneous increase in distance from a potential predator.