Energetic costs and efficiencies of ciliary filter feeding

The relationship between activity of the lateral cilia and oxygen consumption was studied in fragments of the gills of Mytilus edulis L., and the effects of stimulation with the nerve transmitters serotonin and dopamine were measured. Beat frequency, f, and oxygen consumption, M_{O 2}, increased with increasing doses of the transmitters. Serotonin increased f up to 26 Hz and the relationship with M_{O 2} could be described by M_{O 2} (l cm^-2 gill area h^-1)=0.44+0.35 f (r=0.99). The relationship after dopamine stimulation did not differ from that established by serotonin, but the maximum value of f was only 19 Hz. At the frequency of 10 Hz, characteristic of undisturbed pumping, the cells carrying the lateral cilia were estimated to account for one third of the total oxygen consumed, equivalent to 1.05×10^-10 mol ATP cm^-2 s^-1. This rate of synthesis of ATP was compared with the rate at which the active cilia hydrolyse ATP. ATP hydrolysis ranged from 58 to 87% of synthesis as the assumed ratio between number of ATP molecules hydrolysed per beat and number of dynein molecules ranged from 2 to 3. The rate at which ATP is hydrolysed by the active cilia was compared with the work done in pumping water. At two estimates available of the pumping pressure, 1.4 and 2.5 mm H₂O, the work amounted to 1.4×10^-6 or 2.5×10^-6 joule cm^-2 s^-1, equivalent to 2.9×10^-11 and 5.2×10^-11 mol ATP cm^-2 s^-1. The efficiencies of work thus corresponded to 48 or 86% at the ATP/dynein ratio of 2. The overall efficiencies of the mussel pump amounted to 18 or 32%.     

Form and feeding mechanism of a living Planctosphaera pelagica (phylum Hemichordata)

We describe aspects of the anatomy and suspension-feeding mechanism of a single Planctosphaera pelagica captured from the plankton in June 1992 off Bermuda in the western Atlantic. We also describe several unusual features of the larva, including its occurrence in surface waters, unusually large size, and limited swimming ability. Our account of the form and feeding behavior of P. pelagica is the first based on observations of a specimen captured and observed alive. Our limited observations suggest that the planctosphaera may use a suspension-feeding mechanism much like that of the other feeding deuterostome larvae (the pluteus and bipinnaria larvae of echinoderms and the tornaria larva of enteropneust hemichordates) known to capture food particles using a single ciliated band. Although we could not observe cilia directly, the movement of dye streams and food particles and the structure of the ciliated band suggest that some particles may be captured at the ciliated band by the reversal of ciliary beat. The planctosphaera possesses many prominent mucous glands near the food grooves. This suggests an important role of mucus in the biology of the larva, but we were not able to observe directly any role of mucus in particle capture.     

Function of lateral cilia in suspension feeding of lophophorates (Brachiopoda,Phoronida, Ectoprocta)

Suspension feeding by the brachiopod Laqueus californianus (Koch), the phoronid Phoronis vancouverensis Pixell, the ectoprocts Bugula sp., Membranipora villosa Hincks, and Schizoporella unicornis (Johnston), and actinotrocha and cyphonautes larvae was observed. Lophophorates retain particles on the upstream side of the band of lateral cilia, even after particles have moved lateral to the frontal surface. This suggests that these animals utilize an induced local reversal of beat of the lateral cilia for concentration and capture of suspended food particles. Retention of particles can cease while the current past the tentacles continues. Movement of particles down the frontal surface of the tentacles of L. californianus and the ectoproct species confirms previous observations that mucus strands are not used in particle capture. Possible functions of latero-frontal cilia or bristles are considered. Distribution of the feeding mechanism among phyla, clearance rates, and the lack of fusion of tentacles in brachiopods are discussed. The impingement mechanism previously suggested for lophophorates cannot account for the movements of particles observed here.     

The behavioral regulation of monogamy in gibbons (Hylobates muelleri)

Summary Responses of mated individuals to playbacks of the songs of solitary females and males permit evaluating the behavioral mechanisms maintaining monogamy in gibbons. When female songs are played back from the centers of their ranges, mated female gibbons typically initiate duets and group approaches toward playback sites. Female songs played back from range boundary locations elicit duetting responses. Responses to solitary female songs do not differ from responses to song duets used by established mated pairs to mediate patterns of intergroup spacing. Mated males lead silent group approaches toward the sites of male song playbacks. These results suggest that range defense by female gibbons forces males into accepting monogamous mating relationships and that monogamy in gibbons is regulated by intersexually-supported, intrasexual aggression.     

Patterns of trace-metal distribution in tissues of Pleoticus muelleri (Crustacea: Decapoda: Solenoceridae)

Trace-metal distribution in tissues of the shrimp Pleoticus muelleri Bate from the Patagonian region, Argentina, was related to sex, size and physiological condition. Concentrations of cadmium, copper, manganese and zinc were determined in the digestive gland, male reproductive system and muscle of adult specimens. Significant (p<0.01) sex-dependent differences in mean metal concentrations (g g^-1 wet wt) were found in the following tissues of males and females, respectively: digestive gland, Cu, 82.9 and 30.8; Zn, 32.5 and 44.9; reproductive system, Zn, 12.8 and 38.6; Mn, 1.7 and 3.1; Cd, 0.29 and 0.58. Metal levels of muscle showed no significant differences between sexes. Cadmium was not detected in muscle, suggesting that its incorporation into this tissue was strictly regulated. Metal concentrations in the male reproductive system were in general weakly correlated (0.001<p<0.05) with either body size or the concentration of metals in the digestive gland. The developing ovary incorporated substantial amounts of zinc, while cadmium and copper levels decreased at proportional rates (p<0.001). The patterns of the variations in the concentrations of these metals in the ovary strongly suggested that a regulatory mechanism operated throughout oogenesis. Manganese was not involved in this presumptive mechanism. The results of this study are discussed in terms of concentrations and in absolute amounts for standardized individuals.     

Nutrition studies in the nauplius larva of Calanus pacificus (Copepoda: Calanoida)

Nauplii of Calanus pacificus were raised on a mixture of algae. Details of the mouth-parts, such as denticles, labial palps and lobes, setations and structure of the masticatory teeth were examined by scanning electron microscopy (SEM). Under the experimental conditions (15°C and 300 gC l^-1), exponential growth coefficients for the period Nauplii II–VI were 0.179 for carbon and 0.228 for nitrogen. C:N ratios dropping from 5.1 to 4.7. Growth was isochronous, each stage lasting 1.5 days. Respiratory losses were 15 to 19.6% of body carbon daily. Nauplii raised on a given alga showed higher rates of ingestion in the presence of this food, compared to nauplii switched to other algae. Minimal threshold concentrations for feeding were found, depending on the size of the food offered and ranging from 5.8 gC I^-1 for Lauderia borealis (28.7 m spherical diameter) to 47.1 gC 1^-1 for Chlamydomonas sp. (11.0 m). Unlike the Copepodite I stage, Nauplii II–VI larvae were not able to ingest small cells such as Isochrysis galbana (4.3 m), or very large ones such as Ditylum brightwellii (47.5 m) at more than maintenance rations. Below the critical concentration for maximal feeding, ingestion was clearly dependent on size of the cells offered, but the size-dependent relationship was different for diatoms and non-diatoms. Filtering rates increased from a threshold concentration to a maximal rate at about 50 gC 1^-1, and decreased at higher concentrations. Critical concentrations ranged from 125 gC 1^-1 for L. borealis to 1000 gC 1^-1 for Chlamydomonas sp. Maximal daily rations ranged between 100 and 150% of body carbon.     

Swimming and feeding in Periphylla periphylla (Scyphozoa, Coronatae)

Some western Norwegian fjords host extraordinarily abundant and persistent populations of the mesopelagic, coronate scyphomedusa, Periphylla periphylla. In these environments, from late autumn to spring, the medusae undertake regular diel vertical migrations into surface waters. From unique observations obtained with a remotely operated vehicle (ROV), including observations made without artificial light, we observed that 90% of the medusae swam with their tentacles in aboral position. Stomach content analyses of surface-collected specimens revealed that the medusae ate mainly calanoid copepods, but ostracods and large euphausiids were also prominent components of their diets. The clearance rate potential of P. periphylla, assessed from in situ observations and stomach contents, was comparable to that of similar-sized, epipelagic gelatinous species. Our findings suggest that P. periphylla behave as active predators in surface waters.     

Particle capture in the crown of the ciliary suspension feeding polychaete Sabella penicillus: videotape recordings and interpretations

An experimental setup was designed for in situ videotape recording of the particle capture process in the crown of the polychaete Sabella penicillus. Intact individuals of S. penicillus (collected in the Gullmornfjord, Sweden in 1992) were exposed to either 6 m Latex spheres or Rhodomonas sp. flagellate cells (6 m). The capture of the added particles was recorded on video. From frameby-frame analyses particle velocities were estimated and the shape of the three-dimensional particle paths was inferred. The mean velocity of particles approaching the crown was estimated to be ca. 1 mm s^-1, increasing to ca. 1.7 mm s^-1 in the interpinnule channel. At the moment of capture the particles were seen to follow a curved, near circular path close to the tips of the latero-frontal cilia. The transport velocities on the frontal side of the pinnules and filaments were estimated to be up to 0.15 and 0.5 mm s^-1, respectively. Counting captured particles relative to particles arriving within the area of the pinnules gave a rough, direct estimate of nearly 100% retention rate when the polychaete was feeding undisturbed. Together with results from clearance measurements in the literature this implies that the worm is able to capture particles down to 3 m entering the interpinnule channel almost 100% effectively. In view of the 80-m wide interpinnule channel and 40-m spacing between the tips of the latero-frontal cilia on both sides of the channel, this result cannot be explained by mechanisms based solely on direct mechanical contact between cilia and particles but must involve fluid mechanical mechanisms. The present work is the experimental basis for ongoing numerical simulations of the particle motion in the interpinnule channel.     

Begging calls and parental feeding decisions in tree swallows (Tachycineta bicolor)

We conducted playback experiments to examine how parent tree swallows (Tachycineta bicolor) use nestling begging calls to distribute feedings to individuals within broods. In a first study, we used a paired-choice test to determine if parents discriminated between the taped begging calls of nestlings deprived of food and those of nestlings that had been recently fed. Our results showed that parents directed their first feeding attempt towards model nestlings near speakers playing deprived calls significantly more often than to models near speakers playing fed calls. They also made more feeding attempts overall to models with deprived calls. In the second study, we varied call rate and amplitude to examine which call features parents might use to discriminate begging calls. Parents directed significantly more first feeding attempts and more feeding attempts overall towards non-begging nestlings near speakers playing high call rates than to nestlings near speakers playing low call rates. They did not, however, discriminate between calls differing in amplitude. Previous studies have shown that parent birds use begging calls to regulate overall feeding rates to the brood. Our results suggest that parent tree swallows also use begging calls when feeding individual nestlings and, in particular, prefer calls associated with increased levels of nestling hunger. Received: 14 February 2000 / Revised: 6 October 2000 / Accepted: 16 October 2000     

Distribution and feeding in the onuphid polychaete,Diopatra cuprea (Bosc)

Population density of the onuphid polychaete Diopatra cuprea is poorly correlated with particle size distribution of the substratum. It varies directly, however, with current velocity. Measurements of the volume of oxygen drawn through the tube by the inhabitants' rhythmic activities, and the volume consumed under similar conditions, indicate that the rate of oxygen utilization is unusually low; therefore, the influence of current velocity cannot be exerted through its effect on oxygen supply. We suggest that the worm's tube, which protrudes several centimeters above the substratum in the form of an inverted hook, is a food-catching device whose efficiency is governed by the volume of water flowing past. This hypothesis is supported by the identity of many species found both in the gut and on the tube. We also suggest that the tube-irrigating activities permit the animal to test the medium for the presence of chemical stimuli emanating from food caught by the tube; supra-threshold concentrations of these stimuli elicit the feeding response.     

Trophic status and feeding selectivity of blennies (Blenniidae: Salariini)

An evaluation of the dietary resources available to, and selected by, blennies of the tribe Salariini was used to assess their trophic status on the Great Barrier Reef. Gut-content analysis of nine species of blennies found detrital aggregates to be the dominant item ingested. Samples of the dietary resources available to one of these species, Salarias patzneri, were compared biochemically. Of the two main dietary categories (detrital aggregates and filamentous algae), detrital aggregates were the major resource available, accounting for 53 ± 4.6% (SE) of the organic matter present. The mean C:N values for detrital aggregates (17.2 ± 0.8) and filamentous algae (20.0 ± 1.8) were very similar, as were protein concentrations (1.8 ± 0.1 and 2.1 ± 0.1 μg mg⁻¹, respectively). However, mean carbohydrate concentrations were much lower in the aggregates than the filamentous algae (19 ± 2 and 76 ± 13 μg mg⁻¹, respectively). Comparison of the inorganic particles ingested to those available indicated that S. patzneri selectively fed on particles <125 μm, (predominantly detrital aggregates) and avoided particles >250 μm, (predominantly algal filaments). The patterns of resource availability, nutritional quality and selectivity suggest that salariin blennies utilise detrital aggregates as their primary dietary resource. Received: 24 May 1999 / Accepted: 29 November 1999     

Particle-size selection by Pseudopolydora paucibranchiata (Polychaeta: Spionidae) in suspension feeding and in deposit feeding: influences of ontogeny and flow speed

Pseudopolydora paucibranchiata Okuda suspension feeds and deposit feeds at the sediment-water interface, where it is exposed to a variety of particles differing in physical characteristics and nutritional value. In flume experiments (conducted in August 1994 and May 1995) with two sizes of either suspended or deposited beads, I measured particle-size selection separately in each feeding mode. The same influences of palp width and of ambient flow speed were observed in each mode. At velocities 0.74 cm s^-1 there were no relationships between palp width and the proportion of gut contents composed of large beads. At velocities 1.8 cm s^-1 worms with narrower palps ingested relatively fewer large beads (and more small beads) than did worms with wider palps. Palp width and body length were linearly related, and results were similar when analyzed with body length as the independent variable. As flow speed increased, selectivity changed in a worm-size-specific manner: worms with a palp width -1. Assuming that in the field (1) particle size is the principle criterion for selection, and (2) the amount of digestible food component in deposited and suspended particles, respectively, is related to particle surface area and volume, I hypothesize that changes in selectivity as velocity rises can cause juveniles to experience a decreasing profitability of suspension feeding and a simultaneously increasing profitability of deposit feeding. Juveniles could maintain a diet of high food value despite flow variations by adjusting the proportion of time they spend suspension feeding relative to deposit feeding.     

Mating and its effect on acoustic signalling behaviour in a primitive orthopteran,Cyphoderris strepitans (Haglidae): the cost of feeding females

Summary Males of the primitive orthopteran, Cyphoderris strepitans, provide their mates with two types of nuptial food gift during mating: 1) females feed while coupled on the fleshy metathoracic wings of the male and the resultant flow of haemolymph and 2) the spermatophore transferred by the male includes a gelatinous spermatophylax which the female eats after mating. During the peak breeding interval, virgin males secure significantly more matings than their numbers relative to non-virgin males would predict. We tested the hypothesis that non-virgin males, having lost a substantial portion of available energy through previous investment in females, call significantly less than virgin males. Reduced calling should result in the attraction of fewer females and/or a greater risk of intrusion from competing males and consequently, a lowered mating success. Calling activity of male C. strepitans of varying mating status was monitored with a sound activated relay apparatus for two consecutive nights following their capture. Males were of three experimental groups, virgin, freshly wounded males (mated on the same night of capture), and old-wound males (mated at least one night prior to capture). Our cata showed a significant short-term reduction in signalling activity as a consequence of mating. Whereas there was no difference in the time spent calling by virgins on the first and second nights following capture, freshly wounded and oldwound males called significantly less on the first night than on the second. Furthermore, the proportion of males calling on both nights was significantly greater for the virgin and old-wound groups than for freshly wounded males. When the duration over which males called on the first night was compared with that of the second, virgin males showed no difference whereas old-wound males called for significantly shorter intervals on the first night. These results indicate that the cost of a large nutrient investment in females lowers the energy level in males below the threshold required for a prolonged signalling period. After a refractory interval during which males feed and replenish their energy reserves, calling levels equivalent to those which occur prior to mating are regained. Active female choice may also contribute to the reduced mating success of non-virgins, but this possibility remains untested.     

Functional morphology and feeding behavior of Scolelepis squamata (Polychaeta: Spionidae)

Functional morphology and feeding behavior of Scolelepis squamata (Müller) were studied. Gut contents consisted of unconsolidated sedimentary particles, fecal pellets of other species, and a wide variety of embryos, larvae, and juveniles. Unlike other spionid polychaetes the palps of S. squamata lack a median, ciliated groove. Particles captured by the palps were brought to the pharynx by a complete contraction of the palp. In the presence of a current, S. squamata helically coiled their palps, and fed almost exclusively on suspended and resuspended particles. In contrast to most spionid polychaetes the palps of S. squamata are not deciduous. Various aspects of the morphology and feeding behavior of S. squamata are discussed in terms of their functional and ecological significance.     

Functional morphology and feeding behavior of Paraprionospio pinnata (Polychaeta: Spionidae)

The functional morphology and feeding behavior of Paraprionospio pinnata (Ehlers) were studied. The tentacular feeding palps of P. pinnata possess four groups of cilia: laterals, latero-frontal cirri, frontals and basal transverse rows. The lateral cilia beat in metachronal waves creating in current that flows toward the frontal surface of the palp. The latero-frontal cirri deflect suspended particles onto the frontal surface and potentially resuspend deposited particles. The frontal cilia line the groove of the palp and transport particles to the ciliated pharynx. The basal transverse cilia also beat in metachronal waves and together with the frontal cilia of the branchiae produce a U-shaped current that removes particles rejected by the pharynx from the burrow. The significance of particle selection at the site of the pharynx in spionid polychaetes is hypothesized to be constrained by the interaction of specific morphologies and behaviors that reduce the effects of epifaunal predation and browsing. The relationship between sediment permeability and type of respiratory or ventilation current is hypothesized to be a potentially important factor in understanding the distribution of spionid polychaetes.     

Comparison of the feeding habits of migratory and non-migratory Stenobrachius leucopsarus (Myctophidae)

Stenobrachius leucopsarus, the most abundant species of myctophid fishes off Oregon, USA, has a bimodal distribution at night, with a peak of abundance in the upper 100 m composed of diel vertical migrants, and another peak at 300 to 500 m composed of fish that did not migrate the night they were caught. We compared the feeding habits of these two groups of fish in an attempt to learn if deep fish migrated to surface waters. Low similarity of diets, differences in the rank order of common prey, and similar states of stomach fullness and digestion of prey suggest that fish captured in deep water at night probably did not feed exclusively in shallow water on previous nights. They probably fed in deep water. The similarity in food habits between deep and shallow fish is most readily explained by daytime feeding by fish in deep water and by broad vertical distributions of prey.     

Factors influencing particle selection and feeding rate in the polychaete Cistenides (Pectinaria) gouldii

Feeding behavior of the deposit feeding polychaete Cistenides (Pectinaria) gouldii was examined to determine factors affecting particle selection and feeding rate. Worms were found to select large particles preferentially and particle size selection increased with worm size. Particle selection behavior was unaffected by changes in sediment bacterial abundance. Feeding rates were affected by sediment size, bacterial density and worm size. Generally feeding rates increased in sediment containing more food, although the response was worm size specific. When viewed in a theoretical construct these results were inconsistent with predictions of deposit feeder optimal foraging models. Alternative explanations, such as morphological constraints placed upon the polychaete, may explain C. gouldii feeding behavior.     

Digestive mechanics and gluttonous feeding in the feather starOligometra serripinna (Echinodermata: Crinoidea)

The movement and digestion of food in the gut ofOligometra serripinna (Carpenter) were studied at Lizard Island (14°3842S; 145°2710E) in the austral winter of 1986. Feather stars in the laboratory were fed a brief, small meal of brine shrimp nauplii and killed at increasing time intervals thereafter. Histological reconstructions showed that the ingested nauplii progressed along the digestive tract surprisingly quickly. Some nauplii were found in the mid and hind intestine in only 30 min, and all of the nauplii had reached the hind intestine and rectum in 1 h. Digestion of the nauplii had started at 1 h, and only a few fragments of naupliar exoskeleton remained in the hind intestine and rectum 5 h after the start of feeding. Videotape analysis showed that no fecal pellets were released during this experiment. In the natural environment ofO. serripinna, ingested particles may similarly be transported quickly to the hind part of the gut and digested there — when feather stars were fixed in the field, most of the gut contents were found in the hind intestine and rectum.O. serripinna, which efficiently rejects inert particles before they are ingested, usually defecates infrequently (probably not more than once over a span of many hours) and differs from some other feather stars that ingest numerous inert particles and defecate much more frequently. When specimens ofO. serripinna were fed continuously on brine shrimp nauplii,Artemia sp. (San Francisco strain), in the laboratory, the feather stars fed gluttonously, packing their guts with several hundred nauplii in 1 to 2 h. Thereafter, superfluous feeding began (i.e., further ingestions appeared to force undigested nauplii, some of them still living, out of the anus). These observations suggest thatO. serripinna usually feeds at relatively modest rates in its natural habitat, but can feed gluttonously to take advantage of infrequent patches of highly concentrated, nutritious particles (e.g. copepod swarms, migrating demersal zooplankton, and invertebrate gametes from mass spawnings). It is likely that such patches of nutritious particles are usually small enough to drift out of reach of the feather stars before gluttonous feeding proceeds to superfluous feeding. Opportunities for superfluous feeding in nature are probably very infrequent (e.g. ingestion of coral gametes and embryos after a mass spawning), and the feather stars evidently have no behavior that stops further ingestions after the gut becomes filled to capacity.     

Food composition and feeding behavior of shallow-water crinoids at Eilat (Red Sea)

The food of 3 feather-stars, Lamprometra klunzingeri Hartlaub, 1890), Heterometra savignii (J. Müller, 1841) and Capillaster multiradiatus (Linnaeus, 1758), from the shallow water of Eilat (Red Sea) was found to be composed of planktonic and semi-benthalic organisms with a strong dominance of zooplankton. Monthly analyses of stomach contents showed seasonal changes in the participation of various systematic units in the diet. Food-comprising organisms were found to be selected according to size, and those measuring up to 400 formed 90% of the diet.This research has been sponsored partly by the Oceanic Biology Branch, Office of Naval Research, U.S.A. under contract N 62558-4556 and contract F 671052 67C 0043 between the Office of N.R. and the Tel-Aviv University. It represents part of the M.Sc. thesis of the first named author (in the framework of Red Sea investigations headed by Dr. L. Fishelson).