Feeding mechanisms and feeding strategies of Atlantic reef corals

The feeding behaviour of 35 species of Atlantic reef corals was examined in the laboratory and in the field. Observations were made during the day and at night, using freshly hatched brine shrimp nauplii and finely ground, filtered fresh fish as food sources. Three feeding strategies were observed: Group I–feeding by tentacle capture only; Group II–feeding by entanglement with a mucus net or mucus filaments; Group III–feeding by a combination of tentacle capture and mucus filament entanglement. Group I included corals of the families Poritidae and Pocilloporidae which were normally expanded during both day and night. Group II included corals of the family Agaricidae which were normally expanded at night and contracted during the day. Group III included corals of the other families examined which, with the exception of Dendrogyra cylindrus , were normally expanded only at night.
Feeding responses were elicited by both chemical and tactile stimuli. A preparatory feeding posture was assumed in response to chemical stimuli and consisted of horizontal positioning of the tentacles, elevation of the oral disk to form a cone-like mouth, a wide mouth opening and secretion of mucus by the epidermis of the oral disk. Following the assumption of the preparatory feeding posture, food capture and ingestive movements were elicited by tactile stimuli. However, food capture and ingestive movements were also elicited by chemical stimuli alone in those species which were normally contracted during the day.
While expanded corals captured food with their tentacles or with mucus filaments, contracted corals were able to feed by capturing fine particulate matter with mucus filaments only and thus acted as suspension feeders. By a combination of feeding strategies, reef corals were able to feed both day and night and a wide range of potential food ranging from fine particulate matter to large zooplankton was available to them.     

Heterotrophy in Tropical Scleractinian Corals

The dual character of corals, that they are both auto- and heterotrophs, was recognized early in the twentieth Century. It is generally accepted that the symbiotic association between corals and their endosymbiotic algae (called zooxanthellae) is fundamental to the development of coral reefs in oligotrophic tropical oceans because zooxanthellae transfer the major part of their photosynthates to the coral host (autotrophic nutrition). However, numerous studies have confirmed that many species of corals are also active heterotrophs, ingesting organisms ranging from bacteria to mesozooplankton. Heterotrophy accounts for between 0 and 66% of the fixed carbon incorporated into coral skeletons and can meet from 15 to 35% of daily metabolic requirements in healthy corals and up to 100% in bleached corals. Apart from this carbon input, feeding is likely to be important to most scleractinian corals, since nitrogen, phosphorus, and other nutrients that cannot be supplied from photosynthesis by the coral's symbiotic algae must come from zooplankton capture, particulate matter or dissolved compounds. A recent study showed that during bleaching events some coral species, by increasing their feeding rates, are able to maintain and restore energy reserves.
This review assesses the importance and effects of heterotrophy in tropical scleractinian corals. We first provide background information on the different food sources (from dissolved organic matter to meso- and macrozooplankton). We then consider the nutritional inputs of feeding. Finally, we review feeding effects on the different physiological parameters of corals (tissue composition, photosynthesis and skeletal growth).     

Within-colony feeding selectivity by a corallivorous reef fish: foraging to maximize reward?

Foraging theory predicts that individuals should choose a prey that maximizes energy rewards relative to the energy expended to access, capture, and consume the prey. However, the relative roles of differences in the nutritive value of foods and costs associated with differences in prey accessibility are not always clear. Coral‐feeding fishes are known to be highly selective feeders on particular coral genera or species and even different parts of individual coral colonies. The absence of strong correlations between the nutritional value of corals and prey preferences suggests other factors such as polyp accessibility may be important. Here, we investigated within‐colony feeding selectivity by the corallivorous filefish, Oxymonacanthus longirostris, and if prey accessibility determines foraging patterns. After confirming that this fish primarily feeds on coral polyps, we examined whether fish show a preference for different parts of a common branching coral, Acropora nobilis, both in the field and in the laboratory experiments with simulated corals. We then experimentally tested whether nonuniform patterns of feeding on preferred coral species reflect structural differences between polyps. We found that O. longirostris exhibits nonuniform patterns of foraging in the field, selectively feeding midway along branches. On simulated corals, fish replicated this pattern when food accessibility was equal along the branch. However, when food access varied, fish consistently modified their foraging behavior, preferring to feed where food was most accessible. When foraging patterns were compared with coral morphology, fish preferred larger polyps and less skeletal protection. Our results highlight that patterns of interspecific and intraspecific selectivity can reflect coral morphology, with fish preferring corals or parts of coral colonies with structural characteristics that increase prey accessibility.     

Effects of coral bleaching on the feeding response of two species of coral-feeding fish

Coral bleaching is an increasingly prominent threat to coral reef ecosystems, not only to corals, but also to the many organisms that rely on coral for food and shelter. Coral-feeding fishes are negatively affected by coral loss caused by extensive bleaching, but it is unknown how feeding behaviour of most corallivorous fishes changes in response to coral bleaching. In this study, coral bleaching was experimentally induced in situ to examine the feeding response of two obligate corallivorous fish, Labrichthys unilineatus (Labridae) and Chaetodon baronessa (Chaetodontidae). Feeding rates were monitored before, during, and immediately after experimental bleaching of prey corals. L. unilineatus significantly increased its feeding on impacted corals during bleaching, but showed a steady decline in feeding once corals were fully bleached. Feeding response of L. unilineatus appears to parallel the expected stress-induced mucous production by bleaching colonies. In contrast, C. baronessa preferentially fed from healthy colonies over bleached colonies, although bleached colonies were consumed for five days following manipulation. Feeding by corallivorous fishes can play an important role in determining coral condition and mortality of corals following stress induced bleaching.     

A forceful upper jaw facilitates picking-based prey capture: biomechanics of feeding in a butterflyfish,Chaetodon trichrous

Biomechanical models of feeding mechanisms elucidate how animals capture food in the wild, which, in turn, expands our understanding of their fundamental trophic niche. However, little attention has been given to modeling the protrusible upper jaw apparatus that characterizes many teleost species. We expanded existing biomechanical models to include upper jaw forces using a generalist butterflyfish, Chaetodon trichrous (Chaetodontidae) that produces substantial upper jaw protrusion when feeding on midwater and benthic prey. Laboratory feeding trials for C. trichrous were recorded using high-speed digital imaging; from these sequences we quantified feeding performance parameters to use as inputs for the biomechanical model. According to the model outputs, the upper jaw makes a substantial contribution to the overall forces produced during mouth closing in C. trichrous. Thus, biomechanical models that only consider lower jaw closing forces will underestimate total bite force for this and likely other teleost species. We also quantified and subsequently modeled feeding events for C. trichrous consuming prey from the water column versus picking attached prey from the substrate to investigate whether there is a functional trade-off between prey capture modes. We found that individuals of C. trichrous alter their feeding behavior when consuming different prey types by changing the timing and magnitude of upper and lower jaw movements and that this behavioral modification will affect the forces produced by the jaws during prey capture by dynamically altering the lever mechanics of the jaws. In fact, the slower, lower magnitude movements produced during picking-based prey capture should produce a more forceful bite, which will facilitate feeding on benthic attached prey items, such as corals. Similarities between butterflyfishes and other teleost lineages that also employ picking-based prey capture suggest that a suite of key behavioral and morphological innovations enhances feeding success for benthic attached prey items.     

Meeting nutrient requirements: the roles of power and efficiency

Conclusions We have attempted to illustrate the importance of nutrient transfer functions and their key quantitative parameters, power and efficiency. While this brief account has focused on one aspect of nutritional behaviour, the duration of intermeal intervals, the models are equally useful for understanding other components of feeding behaviour such as meal size and food switching. Like-wise, they provide a framework for formulating quantitative predictions about the dynamics of the physiological processes involved in digestion, absorption and the utilisation of food. These aspects are dealt with more fully elsewhere.     

Towards more efficient longline fisheries: fish feeding behaviour,bait characteristics and development of alternative baits

Better knowledge of food search behaviour in fish is essential for studies that aim to improve longline fishing, particularly through bait development. This review provides an overview of our understanding of how fish detect and locate sources of food odour, focusing on the stimuli and sensory modalities involved, and on factors that affect feeding activity. Studies that identify feeding attractants and efforts to develop alternative longline baits are presented. The review reveals that such studies are few in number, and that to date there are no alternatives to traditional baits in commercial longlining despite the growing demand for these resources, which are also used for human consumption. The chemical compounds that elicit food search behaviour differ from species to species, and species selectivity could be improved by incorporating specific feeding attractants in manufactured baits. The unique properties of chemical stimuli and odour dispersal form the basis for improving longline efficiency through the development of a long-lasting bait. Vision is important in prey capture, and manufactured baits can be made more visible than natural baits by increasing the contrast (e.g. via fluorescent or polarising coatings) and creating motion through buoyancy. Physical properties such as size, shape, texture and strength can also be manipulated in a manufactured bait to improve catch efficiency. Knowledge obtained from studies of various aspects of food search behaviour is of paramount importance for future research aimed at alternative bait development and improving longline fishing.     

Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids,sterols, and alcohols in the scleractinian coral <Emphasis Type="Italic">Turbinaria reniformis</Emphasis>

This study assesses the combined effect of feeding and short-term thermal stress on various physiological parameters and on the fatty acid, sterol, and alcohol composition of the scleractinian coral Turbinaria reniformis. The compound-specific carbon isotope composition of the lipids was also measured. Under control conditions (26°C), feeding with Artemia salina significantly increased the symbiont density and chlorophyll content and the growth rates of the corals. It also doubled the concentrations of almost all fatty acid (FA) compounds and increased the n-alcohol and sterol contents. δ¹³C results showed that the feeding enhancement of FA concentrations occurred either via a direct pathway, for one of the major polyunsaturated fatty acid (PUFA) compounds of the food (18:3n-3 FA), or via an enhancement of photosynthate transfer (indirect pathway), for the other coral FAs. Cholesterol (C₂₇Δ⁵) was also directly acquired from the food. Thermal stress (31°C) affected corals, but differently according to their feeding status. Chlorophyll, protein content, and maximal photosynthetic efficiency of photosystem II (PSII) decreased to a greater extent in starved corals. In such corals, FA concentrations were reduced by 33%, (especially C16, C18 FAs, and n-3 PUFA) and the sterol content by 27% (especially the C₂₈∆^5,22 and C₂₈∆⁵). The enrichment in the δ¹³C signature of the storage and structural FAs suggests that they were the main compounds respired during the stress to maintain the coral metabolism. Thermal stress had less effect on the lipid concentrations of fed corals, as only FA levels were reduced by 13%, with no major changes in their isotope carbon signatures. In conclusion, feeding plays an essential role in sustaining T. reniformis metabolism during the thermal stress.     

Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos Vireo olivaceus

Corticosterone is thought to play an important role in food caching and foraging behaviour. However, the direct influence of increased plasma corticosterone on feeding behaviour is still unclear. In this study the effect of increased corticosterone on feeding behaviour in migratory active red-eyed vireos Vireo olivaceus was investigated. We hypothesized that if increased corticosterone levels facilitate foraging behaviour, an increased number of visits to the food bowl by corticosterone treated birds would be seen. In addition to ad lib food during the experiment, the vireos were fed every full hour between 09.00–13.00 h with one meal worm injected either with 4 μg corticosterone dissolved in 20 μl DMSO, or with DMSO only as a control treatment. The presence or absence of a bird in the food bowl was recorded by a motion detector between 09.00–15.00 h. The non-invasive corticosterone treatment increased plasma corticosterone levels and caused vireos to visit the food bowl more frequently compared to control treated individuals between 11.00–12.00 h and 13.00–15.00 h. Our data indicate that corticosterone has an effect on feeding behaviour in birds.     

Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis

This study aimed at investigating changes in feeding rates of three scleractinian coral species (Stylophora pistillata, Turbinaria reniformis and Galaxea fascicularis) between control (26 °C) and short-term stress conditions (31 °C), and to assess the effect of feeding on the photosynthetic efficiency of the corals. Feeding rates varied according to the feeding effort of the corals, itself depending on the environmental conditions. Indeed, S. pistillata significantly decreased its feeding rates at 31 °C, while rates of T. reniformis and G. fascicularis were increased between 26 and 31 °C. Independently of the feeding rates, food supply helped in preventing damage to the photosynthetic apparatus of the zooxanthellae. Indeed, starved corals from the three species showed significant decrease in both the electron transport rates and in the photosynthetic rates, following a loss in the amount of chlorophyll and experiencing photoinhibition of the photosystem II. However, no bleaching was observed in heated fed corals, with no decrease in their photosynthetic efficiency or performance.     

Is feeding behaviour in crucian carp mediated by the lateral olfactory tract?

Experiments were performed to investigate which bundle of the olfactory tract was essential for mediating feeding behaviour in crucian carp. Fish were divided in three groups: control fish, fish with only the lateral olfactory tracts (LOTs) intact and fish with the LOTs cut. The fish were maintained in physiological saline after surgery to preserve the remaining tracts and postoperative inspections revealed the functional status of the remaining tracts. With the injection of food odour into the aquaria the scores for various feeding behaviours--biting, snapping, mouth openings and vertical posture--were not significantly different between those of the control fish and the fish with the LOT intact. Those fish that had the LOT cut but the medial and lateral parts of the medial olfactory tract (mMOT, lMOT) intact had significantly lower feeding-related scores than the other two groups of fish. The results of the present study indicate that the LOT is necessary to maintain the full qualitative and quantitative extent of feeding behaviour in crucian carp.     

Serotonin depresses feeding behaviour in ants

Feeding behaviour is a complex functional system that relies on external signals and the physiological state of the animal. This is also the case in ants as they vary their feeding behaviour according to food characteristics, environmental conditions and - as they are social insects - to the colony's requirements. The biogenic amine serotonin (5-HT) was shown to be involved in the control and modulation of many actions and processes related to feeding in both vertebrates and invertebrates. In this study, we investigated whether 5-HT affects nectar feeding in ants by analysing its effect on the sucking-pump activity. Furthermore, we studied 5-HT association with tissues and neuronal ganglia involved in feeding regulation. Our results show that 5-HT promotes a dose-dependent depression of sucrose feeding in Camponotus mus ants. Orally administered 5-HT diminished the intake rate by mainly decreasing the volume of solution taken per pump contraction, without modifying the sucrose acceptance threshold. Immunohistochemical studies all along the alimentary canal revealed 5-HT-like immunoreactive processes on the foregut (oesophagus, crop and proventriculus), while the midgut and hindgut lacked 5-HT innervation. Although the frontal and suboesophageal ganglia contained 5-HT immunoreactive cell bodies, serotonergic innervation in the sucking-pump muscles was absent. The results are discussed in the frame of a role of 5-HT in feeding control in ants.     

The Effect of Feeding History on Prey Capture Behaviour in the Orbweb Spider Argiope keyserlingi Karsch (Araneae: Araneidae)

The prey capture behaviour of the orb-web spider Argiope keyserlingi Karsch was examined experimentally by subjecting spiders to two different feeding regimes (food deprived and food satiated) and three types of prey: Drosophila, blowflies (Lucilia cuprina) and bees (Apis mellifera). The attack behaviour of the spiders was influenced by both their foraging history and the type of prey. Food deprived spiders attacked Drosophila and bees more frequently than food satiated spiders, and food satiated spiders travelled more slowly to any of the prey types than food deprived spiders. Furthermore, Drosophila were never wrapped in silk but only grasped with the chelicerae, whereas both blowflies and bees were always wrapped. This provides experimental confirmation that feeding history affects the decision of orb-web spiders to accept or reject any given prey.     

Nitrogen and photosynthetic function of hermatypic corals. Oxygen exchange of Stylophora pistillata coral under artificial feeding

The change of Stylophora pistillata coral photosynthetic function (oxygen exchange and biomass of symbionts) under starvation and food enrichment was studied to understand the role of heterotrophy in nitrogen supplements of zooxanthellae. The starvation caused the decrease of frequency of zooxanthellae cells division in 7-10 times. The number of degraded algae cells increased in same proportion and, as a result, the density of zooxanthellae in corals decreased about two times during one-two weeks. Under starvation corals kept their photosynthetic capacity at the level of corals in situ by means of enhancing the zooxanthellae gross photosynthesis. The respiration rate of coral had tendency to increase and the dry mass of polyp tissue to decrease. Under artificial feeding which was following starvation the zooxanthellae density increased in 1.5-2 times, and particular food caused more intensive accumulation of zooxanthellae comparing to dissolved inorganic ammonium. The feeding regime did not affect dry mass of polyp tissue and chlorophyll content as well as respiration and gross productivity of the corals. The conclusion about high effectiveness of particular feeding for supplying symbiotic algae with nitrogen was made and trophic status of zooxanthellae in hospite was determined as unlimited by nitrogen.     

Methods for Studying the Ecological Physiology of Feeding in Free-Ranging Howlers (Alouatta palliata) at La Pacifica, Costa Rica

We lack a general understanding of how primates perform physiologically during feeding to cope with the challenges of their natural environments. We here discuss several methods for studying the ecological physiology of feeding in mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. Our initial physiological effort focuses on recording electromyographic activity (EMG) from the jaw muscles in free-ranging howlers while they feed in their natural forest habitat. We integrate these EMG data with measurements of food material properties, dental wear rates, as well as spatial analyses of resource use and food distribution. Future work will focus on incorporating physiological measures of bone deformation, i.e., bone strain; temperatures; food nutritional data; and hormonal analyses. Collectively, these efforts will help us to better understand the challenges that howlers face in their environment and the physiological mechanisms they employ during feeding. Our initial efforts provide a proof of concept demonstrating the methodological feasibility of studying the physiology of feeding in free-ranging primates. Although howlers offer certain advantages to in vivo field research, many of the approaches described here can be applied to other primates in natural habitats. By collecting physiological data simultaneously with ecological and behavioral data, we will promote a more synthetic understanding of primate feeding and its evolutionary history.     

Intentional partial beaching in a coral reef fish: a newly recorded hunting behaviour of titan triggerfish,Balistoides viridescens

Coral reef fishes use a multitude of diverse feeding behaviours to increase their ability to successfully capture a wide range of prey. Here, this study reports a novel hunting behaviour in a coral reef fish, the titan triggerfish, Balistoides viridescens, where an individual was seen partially beaching itself while attempting to catch a Red Sea ghost crab, Ocypode saratan. This is the first report of this behaviour in the order Tetraodontiformes and represents an astonishing capability of this species to exploit food resources outside their typical assumed ecological niche.     

The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia Danae Milne Edwards & Haime 1849

The coral Astrangia danae Milne Edwards & Haime 1849 occurs naturally with and without symbiotic algae and thus may have two sources of nourishment: (1) particles captured by the coral polyps, and (2) photosynthetic products translocated from their zooxanthellae. Symbiotic colonies may have both sources, and nonsymbiotic ones certainly have only the former. The relative importance of these two food sources was studied in the laboratory by examining the tissues of corals fed with frozen brine shrimp. Stock corals were fed once per week. Two to three weeks prior to each experiment, selected corals were placed on one of three feeding schedules: starved (S), fed once per week (1/wk), and fed three times per week (3/wk). The coral tissues were analyzed for protein, lipid, carbohydrate, and zooxanthellae content. Increased feeding frequency (1/wk → 3/wk) resulted in an increased tissue biomass and lipid to protein (L/P) ratio; starvation (1/wk → S) caused a decrease in these parameters. Symbiosis with zooxanthellae had an effect similar to increased feeding frequency in that the S and 1/wk symbiotic corals had a higher L/P ratio than comparable nonsymbiotic ones. There were no significant differences in L/P ratios between the 3/wk symbiotic and nonsymbiotic corals. Freshly collected colonies had a tissue composition most similar to the laboratory animals fed 3/wk. This result is consistent with the hypothesis that ingestion of solid food is the major nutritional source for A. danae in Narragansett Bay, Rhode Island, but our experiments suggest that the algae can have an important effect on tissue L/P ratios during times of food scarcity.     

Adaptive velocity-based six degree of freedom load control for real-time unconstrained biomechanical testing

Robotic biomechanics is a powerful tool for further developing our understanding of biological joints, tissues and their repair. Both velocity-based and hybrid force control methods have been applied to biomechanics but the complex and non-linear properties of joints have limited these to slow or stepwise loading, which may not capture the real-time behaviour of joints. This paper presents a novel force control scheme combining stiffness and velocity based methods aimed at achieving six degree of freedom unconstrained force control at physiological loading rates.     

Oxygen and Heterotrophy Affect Calcification of the Scleractinian Coral Galaxea fascicularis

Heterotrophy is known to stimulate calcification of scleractinian corals, possibly through enhanced organic matrix synthesis and photosynthesis, and increased supply of metabolic DIC. In contrast to the positive long-term effects of heterotrophy, inhibition of calcification has been observed during feeding, which may be explained by a temporal oxygen limitation in coral tissue. To test this hypothesis, we measured the short-term effects of zooplankton feeding on light and dark calcification rates of the scleractinian coral Galaxea fascicularis (n = 4) at oxygen saturation levels ranging from 13 to 280%. Significant main and interactive effects of oxygen, heterotrophy and light on calcification rates were found (three-way factorial repeated measures ANOVA, p<0.05). Light and dark calcification rates of unfed corals were severely affected by hypoxia and hyperoxia, with optimal rates at 110% saturation. Light calcification rates of fed corals exhibited a similar trend, with highest rates at 150% saturation. In contrast, dark calcification rates of fed corals were close to zero under all oxygen saturations. We conclude that oxygen exerts a strong control over light and dark calcification rates of corals, and propose that in situ calcification rates are highly dynamic. Nevertheless, the inhibitory effect of heterotrophy on dark calcification appears to be oxygen-independent. We hypothesize that dark calcification is impaired during zooplankton feeding by a temporal decrease of the pH and aragonite saturation state of the calcifying medium, caused by increased respiration rates. This may invoke a transient reallocation of metabolic energy to soft tissue growth and organic matrix synthesis. These insights enhance our understanding of how oxygen and heterotrophy affect coral calcification, both in situ as well as in aquaculture.