Control of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica,flow environment,and siphon-cropping fishes

Macoma balthica (L.), an abundant clam, ubiquitous in temperate estuaries across the North Atlantic, is known to practice both alternative basic modes of feeding available to seafloor invertebrates. It either holds its feeding organ, the siphon, at a fixed position just above the sediment surface to filter out food particles suspended in the overlying water or else extends and moves its siphon around to vacuum up deposited food particles on the sediment surface. Previous laboratory experiments have established an understanding of the role of current flow in dictating the choice of whether suspension or deposit feeding will be used by marine invertebrates with the facultative flexibility to choose. Faster flows imply greater fluxes of suspended particles so that the energetic rewards of suspension feeding are enhanced. Slower flows imply reduced renewal rates of suspended foods in the bottom boundary layers and enhanced deposition of food particles on the seafloor so that a switch to deposit feeding is favored. Like early optimal foraging theory, this understanding is based on energetic considerations alone without incorporation of broader implications of how population interactions such as predation and competition influence individual foraging behavior. Feeding behavior of Macoma balthica is influenced in the Neuse River estuary by both hydrodynamics and siphon-cropping by juvenile demersal fishes. Under conditions of identical concentrations of suspended particulates in the water column and organic contents of surface sediments, Macoma exhibited much higher levels of deposit feeding where currents were slower. In addition, exclosure and fish inclosure experiments demonstrated that juvenile demersal fishes influence feeding behavior of Macoma by cropping exposed siphons and inducing reduction in deposit-feeding activity. Effects of croppers were substantial in early to midsummer, when juvenile fish abundances were greatest in trawl samples from this estuarine nursery and before the growing fish exhibited ontogenetic changes in diet away from early concentration on bivalve siphons. Field experiments in which siphon-cropping fish were caged at varying distances off the bottom failed to detect any effective behavioral avoidance by Macoma of cropping in response to proximity of fish. One might have hypothesized that under high risk of cropping, Macoma would switch to suspension feeding and away from deposit feeding, the feeding method entailing more risk of losses to croppers because of greater siphon activity and greater extension of siphons on the sediment surface. Consequently, partial predation by siphon-cropping fishes greatly reduces deposit-feeding activity by Macoma balthica during summer as an apparent direct effect of disfigurement and reduction of siphons, the organ required for efficient deposit feeding. Information on current flows alone would not suffice to predict feeding behavior of this marine invertebrate: the influence of partial predation must also be included.     

Regeneration of lost siphon tissues in the tellinacean bivalve Nuttallia olivacea

The inhalant siphon of the tellinacean bivalve Nuttallia olivacea is an important prey item for juvenile stone flounder Platichthys bicoloratus in estuaries in Japan. We examined quantitative siphon regeneration of N. olivacea in rearing experiments of siphon-removed bivalves (> 30 mm shell length) both in the laboratory and in their natural habitat. Under laboratory conditions, siphon-removed bivalves regenerated lost tissues quantitatively at 15 and 25 °C 1 mo after siphon removal, although regeneration was incomplete. A 3-mo caging experiment in the field showed that great regeneration occurred in siphon-removed bivalves. However, the siphon weight of removed bivalves was significantly smaller than that of non-amputated bivalves, suggesting the incomplete regeneration. In a 1-mo caging experiment, bivalves that had approximately 15% of their siphons amputated were selected at some intervals to illustrate the quantitative regeneration process. Estimated daily siphon production was remarkably high only a few days after amputation. It decreased greatly thereafter, but regeneration was not completed within 30 d. These results indicate that bivalves regenerate siphons rapidly just after losing siphon tissues and then regeneration is slowed down before it is completed.     

Protection against suspended sand: the function of the branchial membrane in the blue mussel Mytilus edulis

Blue mussels (Mytilus edulis) living in estuaries have to cope with varying concentrations of suspended sand. Sand flowing through the inhalant siphons comes into the infrabranchial chamber. The inhalant siphon can be partially closed by the branchial membrane. As a result the inward flow decreases, and suspended sand sinks and can be eliminated. Experiments with mussels from three ecologically different locations showed about the same response of the branchial membrane on contact with suspended sand. The presence and function of the branchial membrane appears to be an adaptation of mussels to their estuarine environment.     

Control of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica and interactions between competition and siphon cropping

Macoma balthica (L.) is a common clam of the estuarine seafloor, belonging to an important group of invertebrates possessing the capacity to choose between the two fundamental modes of feeding available, using its siphon to inhale either suspended food particles from the water or food particles deposited on the sediment surface. Field experiments demonstrate that intraspecific competition, effects of other competing benthic invertebrates, and complex interactions between competition and partial predation (siphon cropping by fishes) modify the foraging behavior of Macoma. When protected by caging from siphon nipping by fishes, Macoma demonstrated greater siphon regeneration at lower density, indicating the importance of competition for limited resources. In the absence of siphon croppers, these same clams also exhibited more deposit feeding at the lower density either because of improved ability to deposit-feed with longer siphons or because deposited foods become more rapidly depleted than suspended foods on local spatial scales. Addition of siphon-nipping fishes caused greater reductions in siphon size of clams at lower density, presumably because the intensity of nipping per clam was greater where clam targets were fewer and because deposit feeding, which was more intense at lower densities, confers a greater risk of cropping from greater siphon extension and activity than characterize suspension feeding. Deposit feeding by Macoma was reduced in the presence of siphon croppers at both high and low density of clams, but the intensity of deposit-feeding activity at low density was substantially higher than predicted by additive effects of clam density and cropping. This suggests operation of a balancing strategy in Macoma whereby it is accepting greater risks of partial predation when rewards of greater food harvest are larger. The surprising failure to adopt a risk-averse stratery may be explained by the non-lethal nature of partial predation, which renders siphon loss an energetic penalty replacable through regeneration. The presence of a bed of suspension-feeding Rangia cuneata also altered foraging behavior of Macoma by inducing a switch to more intense deposit feeding, in response either to the documented near-bottom depletion of suspended foods or to likely enhanced biodeposition from feces and pseudofeces. The induction of greater deposit feeding by the presence of this competing suspension feeder led to greater siphon losses during exposure to croppers because Macoma was practicing more risky feeding behavior. This enhanced loss of siphon tissues to croppers in the presence of the suspension-feeding Rangia induced an interaction between the effects of siphon croppers and Rangia, such that Macoma exhibited a larger switch away from deposit feeding in the presence of siphon croppers when Rangia were also present. Clearly, the foraging decisions made by individuals can only be understood in a broad holistic context of population, community, and ecosystem processes.     

Recovery from Siphon Damage in Donax vittatus (Da Costa) (Bivalvia: Donacidae)

Between 2.5% and 18% of Donax vittatus from a natural populationon West Sands beach, St Andrews on the Scottish east coast showeddamage to the siphons caused by non-lethal predation by juvenileflatfishes. The percentage with damaged siphons was greatestin summer. Either inhalant or exhalant siphons were affected,in varying proportions, or in some cases, both siphons. In experimentalaquaria, Donax vittatus that suffered non-lethal attack by juvenileplaice which resulted in their removal from the sand, rapidlyresumed normal activity as evidenced by reburrowing. Wound healing,followed by re-differentiation of siphonal tentacles, took placerapidly following experimental amputation of siphon tips, withthe newly-formed tentacles appearing almost normal after 10days. Re-differentiation of the siphonal tentacles was accompaniedby the development of their complement of three types of ciliated senseorgans. (Received 11 May 1998; accepted 9 July 1998)     

A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus)

1. We investigated two possible proximate cues used for oviposition site choice by females of the bitterling ( Rhodeus sericeus ), a freshwater fish that spawns on the gills of live unionid mussels. The two cues were the flow velocity and/or oxygen content of water emerging from the exhalant siphon of a mussel.
2. Field observations showed that female bitterling always inspected the exhalant siphons of mussels before they spawned in them. Siphon inspection was not always a prelude to spawning and it may serve as a means of assessing mussel quality. Female skimming behaviour, swimming over a mussel without spawning, may also be used to assess mussel quality, although the mechanism for this is unclear.
3. Measurements of the flow velocity of water emerging from the exhalant siphons of four mussel species ( Anodonta anatina, A. cygnea, Unio pictorum and U. tumidus ) showed a significant difference among species, with U. tumidus having the highest mean flow velocity and U. pictorum the lowest.
4. Measurements of the change in oxygen concentration of water entering a mussel inhalant siphon and leaving its exhalant siphon in field and laboratory studies showed a significant difference among the four mussel species, with A. cygnea exhibiting a significantly higher change in oxygen concentration than the other species.
5. The presence of bitterling embryos in the gills of a mussel significantly increased its oxygen consumption whereas larval glochidia had no significant effect. We discuss oxygen availability as a possible proximate cue for oviposition site choice in bitterling.     

Life habits and functional morphology of the sediment infaunal spongesOceanapia oleracea andOceanapia peltata (Porifera,Haplosclerida)

Summary In the Santa Marta area of the northern coast of Colombia two species of sponges have been found living within the sediment. The only connection these sponges have with the open water consists of a number of protruding, tubule-like siphons. Through field observations and aquarium experiments, the life habits and the function of the water current system ofOceanapia oleracea andO. peltata have been studied. As an adaptation to life embedded in sediment, both species possess inhalant siphons which draw water from above the sediment surface and duct it to the central body. The inhalant system shows a most unusual separation and concentration of inhalant pores at the tips of the inhalant ducts. The exhalant water leaves the sponge through separate ducts at the opposite side of the central body. Based on the observations onOceanapia, the water flow model forDisyringa proposed by Fry and Fry (1979) is reconsidered.     

Discovery of ventrally directed spiralia in a Permian spiriferellid brachiopod and implications for its feeding system

Spiralia are lophophore‐supporting, coiled internal structures developed in some extinct brachiopods. In spite of considerable variations in their orientation, the spiralia of most spiriferide and spiriferinide taxa are known to be laterally directed. Recent studies have shown that these brachiopods consistently have a median inhalant and lateral exhalant feeding system. Here, we report a Permian spiriferellid brachiopod fossil (Spiriferella protodraschei) bearing ventrally directed spiralia in its interior. Using the serial sections of the specimen, we have reconstructed the detailed morphology and orientation of the spiralia. Each spiralium in the specimen does not show the apically tapering pattern supposedly universal in all the known types of spiralia: instead it maintains a similar diameter even at its last whorl. The spiralia appear to have directly developed from strong and anteriorly extended crura, consisting of ten whorls in one side and 13 whorls in the other side. As the morphology and orientation of spiralia are immediately associated with the arrangement of spirolophous lophophore within the mantle cavity, the extraordinary orientation and form of the spiralia indicate that this brachiopod likely had developed a considerably modified feeding pattern with respect to most other spirolophous brachiopods. It is postulated that the inhalant/exhalant current circulation of the species (and its descendants) would be considerably different from that of other spiriferide taxa. In particular, the combination of the vertically oriented life posture (free‐lying with thickened ventral apex bottom) and ventrally directed spiralia resembles both fossil atrypide and modern rhynchonellide brachiopods in the orientation of spirolophe, suggesting that some spiriferellid brachiopods may have developed a lateral inhalant/median exhalant feeding current system. A few spiriferide and spiriferinide brachiopod taxa with a weakly transverse but strongly convex ventral valve are noted to exhibit similar modifications in their spiralia, possibly due to the spatial limitation of their mantle cavities.     

The ecology and functional morphology of Trigonothracia jinxingae (Bivalvia: Anomalodesmata: Thracioidea) from Xiamen, China

All anomalodesmatans are 'rare' but Trigonothrucia jinxingae is relatively common in Xiamen Harbour, Fujian Province, China. This is because the species has a life span of approximately one year and is a simultaneous hermaphrodite, probably with either a short or absent planktonic larval stage. That is, success results from rapid maturation, self-fertilization, direct development and within-habitat recruitment over an extended period in early summer.
Trigonothracia jinxingae is interesting in another way, however. The Thraciidae is the Mesozoic stem group of the Thracioidea which also contains the more modern (Caenozoic) Laternulidae and Periplomatidae. Features of the anatomy of T. jinxingae , such as the method of hydraulically moving the foot by the pumping of blood into a capacious pallial haemocoel, and the structure of the stomach, are reminiscent of the earliest (Palaeozoic) anomalodesmaans, i.e. the Pholadomyoidea, represented today by Pholadomya candida. The thraciid Asthenothaerus sp. (Pelseneer, 1911) even has, like P. cundida , an opisthopodium on its visceral mass. P. candida , however, fed on sub-surface deposits using its foot. T. jinxingae is also a deposit feeder, but on surface deposits using the inhalant siphon.
Modern periplomatids resemble thraciids in their separate siphons, but both representatives of this family and the Laternulidae are suspension feeders with extensive sorting areas on the wall of the stomach to process such material. The Thraciidae thus form a link between the oldest, pedal feeding, pholadomyoidean anomalodesmatan and the most advanced, suspension feeding, laternulids and periplomatids.     

On the reorientation of non-spherical prey particles in a feeding current

Potentially, non-spherical prey can be re-oriented in a flowfield and impact on the predator's feeding structures in a non-randommanner. Herein, we quantify a process whereby this passive reorientationoccurs, and present a model that predicts the orientation ofa spheroidal prey as a function of its shape, size and the characteristicsof the fluid flow. For a radial flow field, elongated prey tendto align with their long axis parallel to streamlines. Thistheory is well supported by our results from a laboratory studyof cylindrical particles in a siphon flow. The model is extendedto a more realistic representation of copepod feeding currents.In this context, the spatial scale over which this process isactive is proportional to     

As good as dead? Sublethal predation facilitates lethal predation on an intertidal clam

Although ecologists have speculated that sublethal predation can impact prey dynamics, consequences of these predator effects have seldom been experimentally tested. In soft‐sediment marine communities, fishes crop extended feeding siphons of buried clams, potentially causing clams to reduce their burial depth, thereby enhancing their susceptibility to excavating lethal predators. We simulated cropping of the confamilial clams, Protothaca staminea and Venerupis philippinarum, by removing the top 40% of siphons, which caused each species to burrow 33–50% shallower than conspecifics with intact siphons. To examine subsequent consequences of reduced burial depth, we exposed cropped and intact clams to natural levels of predation in the field. Because of a naturally longer siphon, Protothaca, even after cropping, remained at relatively safe burial depths. In contrast, siphon cropping nearly doubled the mortality rate of Venerupis. Thus, while sublethal predation facilitates lethal predation, this linkage depends on specific life history characteristics, even among ecologically similar species.     

SOME BEHAVIOURAL AND ELECTRICAL RESPONSES OF SCROBICULARIA PLANA (BIVALVIA:TELLINACEA) TO SIPHONAL WOUNDING

Water pumping, valve movements and heart rate have been recordedfrom Scrobicularia for short periods of normal behaviour andthen after siphonal wounding. Scrobicularia exhibits regularand repetitive pumping periods interrupted for only 2–3s after siphonal wounding, without the regularity of these periodsbeing affected. Wounding does not prevent animals from usingtheir inhalant siphons for deposit feeding. A preliminary investigationof neural responses to stimulation has shown that wounding thesiphon causes minimal disturbance to the animal, a brief (2s)burst of nerve activity occurs, the siphon is retracted, butvalve adduction does not occur. In contrast to this tactilestimulation of the mantle edge always elicits a large burstof impulses in the posterior adductor nerve, valve closure results,usually for 14–15 s. ¹Present address: Dept of Zoology, University of Cape Town,Rondebosch 7700, South Africa. (Received 2 February 1981;     

Deposit feeding in Abra tenuis (Bivalvia: Tellinacea)

Deposit feeding in Abra tenuis is described in terms of the size of particles utilized.
Material is collected by the inhalant siphon performing a circular motion sucking in sediment from beneath and on the surface.
The size distribution of silica admitted into the mantle cavity is described and shown to be controlled by physical parameters. The density of a particle does not affect its uptake by the inhalant siphon. The size distribution of the sediment affects the size distribution of particles admitted to the mantle cavity.
No selection of material for ingestion in terms of size occurs after it has been taken into the mantle cavity. Thus the range of material ingested is ultimately controlled by a physical parameter, the inhalant opening.     

Autocatalysis in Reaction Networks

The persistence conjecture is a long-standing open problem in chemical reaction network theory. It concerns the behavior of solutions to coupled ODE systems that arise from applying mass-action kinetics to a network of chemical reactions. The idea is that if all reactions are reversible in a weak sense, then no species can go extinct. A notion that has been found useful in thinking about persistence is that of “critical siphon.” We explore the combinatorics of critical siphons, with a view toward the persistence conjecture. We introduce the notions of “drainable” and “self-replicable” (or autocatalytic) siphons. We show that: Every minimal critical siphon is either drainable or self-replicable; reaction networks without drainable siphons are persistent; and nonautocatalytic weakly reversible networks are persistent. Our results clarify that the difficulties in proving the persistence conjecture are essentially due to competition between drainable and self-replicable siphons.     

Feeding activity, absorption efficiency and suspension feeding processes in the ascidian, Halocynthia pyriformis (Stolidobranchia: Ascidiacea): responses to variations in diet quantity and quality

The benthic suspension feeding ascidian, Halocynthia pyriformis (Rathke, 1806), is often exposed to high concentrations of resuspended sediment in the Bay of Fundy. Resuspended sediment can change diet quantity and quality that may alter the ascidian's ability to feed and gain energy. The feeding activity of H. pyriformis exposed to bottom sediment was examined using standard physiological techniques and video endoscopy. Ascidians were exposed to natural seston plus additions of bottom sediment ranging in concentration from 0 to 46 mg l(-1). For each sediment concentration, clearance rate, ingestion rate, and retention efficiency of the ascidians was estimated using flow-through feeding chambers. Samples of suspended particles and feces were collected to estimate absorption efficiency and absorption rate. Results indicate that with increasing sediment concentration, ingestion rate increased to a constant level, absorption rate increased linearly despite a logarithmic decrease in absorption efficiency, and the retention of small particles (2-5 &mgr;m) increased while retention of larger particles (5-15 &mgr;m) decreased. As sediment concentration increased, squirting frequency increased and diameter of the siphon was reduced. Endoscopic observation of feeding structures and processes and the measurement of particle velocity was performed on ascidians exposed to 0 and 10 mg l(-1) of bottom sediment. An increase in squirting frequency at the high concentration facilitated the rejection of unwanted material and altered the structure and transport velocity of mucus. Mucus velocity was five times slower at 10 mg l(-1) than at 0 mg l(-1), however, the overall distance of mucus travel and the probability of clogging was reduced at 10 mg l(-1). H. pyriformis appears to compensate for episodic changes in the quantity and quality of available food particles by altering siphon-opening diameter, squirting frequency, structure and transport of mucus, and retention efficiency to maintain constant clearance rates.     

Influence of current speed on clearance rate, algal cell depletion in the water column and resuspension of biodeposits of cockles (Cerastoderma edule)

The main objectives of this study were: 1) to determine the influence of water currents on the suspension feeding rate of cockles (Cerastoderma edule); 2) to quantify the interaction between cockle feeding and flow on algal cell depletion in the overlying water column, and 3) to measure the effect of flow on resuspension of their pseudofaeces and faeces. Flume experiments demonstrated that suspension feeding rate (i.e. clearance rate) of C. edule was not significantly affected by increasing current speed, at least between 5 and 35 cm s^− 1. Measurement of vertical profiles in algal cell concentrations within the water column showed a marked depletion above the bed, and the size of this was inversely related to currents' speeds below 5 cm s^− 1. At 2 cm s^− 1 the algal cell depletion was maximum immediately above the bed. However, below currents of 1 cm s^− 1 the maximum depletion was at 10 cm above the bed. This was a result of the exhalent jet of the cockle pumping filtered water (i.e. algal free) vertically into the water column and above the intake level of the inhalant siphon. Such stratification of the water column would appear to be beneficial to the cockle because it reduces the degree of re-filtration of algal cell depleted water at times of low flow, when there is poor mixing and thus poor replenishment of phytoplankton to the boundary layer. Critical erosion thresholds for cockle biodeposits, produced from a diet of silt and unicellular algae, were recorded at current velocities of 15 and 25 cm s^− 1, or shear velocities of 0.6 and 1.0 cm s^− 1, for pseudofaeces and faeces respectively.     

Ascidian suspension feeding

Ascidians are a diverse group of benthic suspension feeders. This review presents and discusses the current literature on ascidian suspension feeding including the different structures involved in feeding as well as how feeding responds to variation in environmental parameters like water temperature and particle concentration. It is concluded that clearance rates in different species at identical conditions will not vary more than within the same species of different sizes, and that variation in clearance rate in ascidians in relation to temperature and particle concentration involves different regulatory mechanisms. Finally ascidian and mussel suspension feeding is compared. It is concluded that the two pumps are very alike with regard to pump performance and specific clearance rate, but whereas ascidian suspension feeding is characterised by high efficiency in terms of particle range and costs of pumping, mussel suspension feeding is more adapted to turbid conditions.     

The food and feeding ecology of Gerreidae, Bleeker 1859, in the estuaries of Natal

The food and feeding ecology of five species of Genes in the estuaries of Natal, were investigated from 1978 to 1980. The Kosi system, consisting of an estuary and three main lakes was selected as the main study area due to an abundance of Genes . Four other estuarine systems were sampled.
At Kosi polychaetes were important at the estuary, siphon tips (distal ±5 mm) of the bivalve Hiatula lunulata were most commonly taken in Lakes Makhawulani and Mpungwini, while chironomid larvae were important in Lake Nhlange. Ivlev's electivity test showed that Genes positively selected bivalve siphon tips when searching for food. The food taken by Genes from other estuaries was similar to that at Kosi, although the proportions of the different prey varied. At Kosi between three and five species occurred sympatri-cally. Resource segregation was through differences in diet and feeding periodicity and a superabundance of food ( H. lunulata siphon tips) during summer and autumn. During winter and spring when food may be limiting, most Genes leave shelf areas of the Kosi system, only G. acinaces remains in large numbers. Little is known of the diet of other fish which feed on benthic invertebrates in Kosi but there is probably little direct competition with Gerreidae, although Acanthopagrus berda and Pomadasys commersonni have been recorded feeding on the siphons of the bivalve Solen corneus , the former in Durban Bay and the latter at Kosi. In areas where the bivalve H. lunulata occurs it is suggested that Gerreidae have developed optimal foraging techniques which enhance resource partitioning.     

Feeding Currents and Particle Capture Mechanisms in Suspension Feeding Animals

The apparent diversity of suspension feeding animals is, inone sense, more apparent than real. Virtually all suspensionfeeders capture particles from the water at low Reynolds numberswith cylindrical filtering elements, so, at the level of thefiltering elements, flow patterns are identical and viscousforces dominate the situation. Six particle capture mechanismsare likely to be operating alone or in combination: (1) scanand trap (isolation of a parcel of fluid containing the particle),(2) sieving, (3) direct interception, (4) inertial impaction,(5) gravitational deposition, and (6) diffusive deposition.To insure that all variables relevant to the suspension feedingprocess are recorded, future work on suspension feeding shouldreport the diameter and spacing of the filtering elements, flowspeeds, diameter of particles available and captured, particlesettling velocities, particle mobility (active or passive),and particle surface properties.