Stable isotope ratios indicate differential omnivory among syntopic rocky shore suspension-feeders

We utilised stable isotope ratios to assess differences in diet among three indigenous and syntopic rocky shore suspension-feeders (mussels Perna perna, barnacles Tetraclita serrata, and polychaetes Gunnarea gaimardi). We also determined the spatial and temporal variability in the suspension-feeder diets by collecting specimens on two occasions from two regions adjacent to hydrologically distinct river mouths (i.e. one with larger annual freshwater throughput than the other). The results showed that the isotopic niches (used as proxies for trophic niches) of the three species did not overlap and that the barnacles occupied a trophic position (3.4) well above those of the mussels (2) and polychaetes (2.6). We ascribed the interspecific differences primarily to the disparate feeding mechanisms used by the species. Large-scale regional (~50 km) differences in suspension-feeder diets were apparent, but not small-scale (up to a few km north and south of each estuary mouth). The regional differences in diet resulted from the increased availability of estuarine-origin suspended particulate matter (SPM) and zooplankton in the region adjacent to the river with relatively larger freshwater output, although overall incorporation of zooplankton versus mixed SPM into consumer diets was relatively consistent between regions and through time. Temporal shifts in suspension-feeder diets were apparent from stable carbon isotope ratios in the consumers. Our results showcase the measurable effects of regional-scale processes that can alter the food sources for dominant primary consumers in the rocky intertidal, thus potentially affecting entire food webs through bottom-up processes. The clear evidence for trophic niche partitioning offers valuable insights into how potentially strong competitors can coexist.     

Predictors of food-related aggression in wild Assamese macaques and the role of conflict avoidance

The quality, availability and distribution of food resources and their influence on types and levels of feeding competition play a central role in ecological models of female social structure in mammals. Here, we investigate the impact of social and ecological factors on rates of food-related aggression and the use of potential conflict avoidance mechanisms in wild Assamese macaques (Macaca assamensis) in northeastern Thailand. These questions were addressed by examining feeding competition at the level of individual food patches which provides detailed information on resource characteristics, aggression and feeding party composition. Results suggest that the frequency of aggression in food patches increases with increasing feeding group size and decreasing patch size but is not affected by ecological variables representing resource value (abundance and nutritional value of food items in a patch). Interestingly, females appear to employ several mechanisms to avoid direct conflicts, including the use of alternative feeding sites within food patches, delayed arrival at feeding sites, storing food in cheek pouches and co-feeding with individuals they share strong social bonds with. Conflict avoidance may be partially responsible for the absence of a rank-related skew in female energy intake in this population and may explain other cases where empirical data do not fit the predictions of socio-ecological theory. Our findings also inform the debate about the mechanisms generating fitness benefits from strong social bonds by suggesting that by increasing feeding tolerance, social bonds may enhance resource acquisition, reduce the risk of injuries and lower levels of agonism-related stress.     

Temporal shifts in the fatty acid profiles of rocky intertidal invertebrates

Fatty acid profiles were determined in rocky intertidal suspension-feeders (mussels and polychaetes) and grazers (limpets and sea urchins) on a monthly basis over 1 year to assess potential dietary overlap between consumers occupying the same trophic guild, and any temporal shifts in diets. Both reproductive and non-reproductive tissues were assessed in an attempt to separate influences of food quality with those of life cycle. Relative variability in fatty acids over time could not be predicted from the feeding guild occupied by a consumer, and influential factors of the temporal shifts included both dietary and reproductive dynamics (even in muscle tissues). Species in the same trophic guild occupied separate trophic niches throughout the year, hence minimising competitive interactions regarding food acquisition. Based on overall variation in fatty acid profiles of muscle tissues, the suspension-feeders Perna perna and Gunnarea gaimardi and the grazing limpet Cymbula oculus occupied narrower feeding niches relative to the grazing sea urchin Parechinus angulosus. Our results provide compelling evidence for potentially large changes in the lipid composition of intertidal invertebrate populations over relatively small temporal scales (i.e. month to month), and these have important implications for short-term field collections intended for assessing invertebrate diets.     

Atypical plant–herbivore association of algal food and a kleptoplastic sea slug (Elysia clarki) revealed by DNA barcoding and field surveys

The identity of food sources and feeding preferences of specialist herbivores have been commonly inferred from spatial associations between consumer and food items. However, such basic information for well-known marine herbivores, sacoglossans (sea slugs), and their algal diets remains disappointingly lacking, especially from field studies. The sacoglossan, Elysia clarki (Pierce et al. in Molluscan Res 26:23–38, 2006), is kleptoplastic and sequesters chloroplasts from algal food to photosynthesize, so DNA identification of sequestered chloroplasts was employed to verify the algal species fed upon by the slug across its geographic range. The molecular information on the algae consumed by E. clarki was combined with field surveys of slugs and algae in slug habitats in the Florida Keys in July and August of 2008 in order to evaluate whether the diet of this herbivore could be predicted based on its spatial association with algae in the field. A considerable mismatch between food availability and kleptoplast identity was recorded. E. clarki commonly occupied areas devoid of potential food and often contained symbiotic plastids from algal species different from those most frequently found in the surveyed habitats. In three of the four study sites, algal species present were poor predictors of slug diet. These findings suggest that the photosynthetic capability of E. clarki may release the slug from the constraint of requiring proximity to its food sources and may allow for the potential lack of spatial coupling between this herbivore and its algal food. This combination of field surveys and DNA barcoding provided critical and previously unavailable information on herbivore feeding in this marine system.     

Diet selection of the Chilean stone crab Homalaspis plana

Diet selection of the Chilean stone crab Homolaspis plana (Milne-Edwards, 1834) was studied using the optimal foraging theory to explain its feeding strategy. The hypothesis that H. plana prefers prey species of the highest prey (“energy”) value was experimentally tested on adult crabs during 1980–1981. Food value was defined as the ratio between caloric content and consumption time, according to energy maximization as the criterion to optimize diet selection. Diet composition of adult crabs from the littoral of Valparaíso (Chile) and ingestion under laboratory conditions were studied to determine type, size and quantity of food to be offered in experiments on prey-type preference. Porcellanid crabs, barnacles and bivalves were the most frequently occurring items in stomachs from in situ conditions. In the aquaria, daily ingestion rates were quite variable among crabs and among days. H. plana showed no size preference for molluscs (Tegula atra, Semimytilus algosus) but preferred larger sizes of porcellanids. The order of preference for prey type was S. algosus>T. atra> porcellanids. However, no differences between their energy values were found and, therefore, the optimal foraging hypothesis was rejected. By extension, the energy maximization criterion alone may not explain the diet selection of H. plana under experimental conditions.     

Ecology of the northern Red Sea crinoids and their Epi- and Endozoic fauna

Fourteen crinoid species are found along the coral reefs of the northern Red Sea that form aggregations of different species at various depths. The shallowest aggregation consists partly of Lamprometra klunzingeri and Capillaster multiradiatus, occurring subtidal to a depth of 2 to 5 m. Of this group, Heterometra savignii inhabits depths down to 12–15 m. Further down, another group of 10-armed crinoids occurs, dominated by Decametra chadwicki and Oligometra serripinna. The deepest aggregation of crinoids occurs at 45 m; its most common members are Colobometra arabica and Comaster distinctus. Feeding on micro- and nanoplankton, shallow-water crinoids show a circadian activity rhythm; in deeper aggregations (10 to 12 m), this behaviour changes with decreasing illumination, to a diurnal activity rhythm. The symbiotic animals living on crinoids comprise 27 taxons, among them Copepoda (6 species), Mollusca (2 species), Polychaeta (11 species, especially Myzostomida); Ophiurida (1 species), Crustacea, Decapoda (6 species); and the clingfish Lepadichthys lineatus. These symbiotic animals form food webs at various depths, according to the distribution of their crinoid host. The occurrence of Indo-West Pacific and Mediterranean commensals on the same crinoid in the Gulf of Aqaba is of special interest.     

Diet of copepods (Scopalatum vorax) associated with mesopelagic detritus (giant larvacean houses) in Monterey Bay,California

The feeding structures or houses of the giant larvacean Bathochordaeus sp. serve as both habitat and food for the calanoid copepod Scopalatum vorax. Gut contents of S. vorax include both microbial and metazoan associates of larvacean houses, and possibly the house-mucus matrix itself. Copepods were observed and collected from larvacean houses between 100 and 500 m in Monterey Bay, California, using a submersible ROV (remotely operated vehicle) from the Monterey Bay Aquarium Research Institute. Gut contents were compared to potential food items on the houses and in the open water (not associated with the house). Copepods were generalist feeders, with amorphous detritus, diatoms, and copepods or other crustacean parts dominating gut contents. Protozoans and algae other than diatoms were rarer in guts. Houses contained a diverse assemblage of microplankton and metazoans, both intact specimens and detrital remains of these. Numbers of diatoms and fecal pellets were enriched by 1 to 3 orders of magnitude on houses compared to numbers in surrounding water. Many of the abundant species of diatoms and copepods on houses occurred in S. vorax guts. This observation coupled with S. vorax feeding habits observed in situ and in the laboratory provide evidence for feeding on houses. S. vorax appears to possess special adaptations to living in a resource-limited environment, such as gorging as a feeding adaptation, chemosensory structures to help locate houses, and the ability to change feeding modes. Consumption of detritus at depth by S. vorax provides evidence that metazoans contribute to remineralization of particulate organic carbon in the mesopelagic zone.     

Food resource partitioning by the pufferfishes Sphoeroides spengleri and S. testudineus from Biscayne Bay,Florida

Partitioning of the food resources by two coexisting pufferfishes (Sphoeroides spengleri and S. testudineus) from Biscayne Bay, Florida, USA, was investigated. Gut contents from 453 bandtail and 339 checkered puffers were analyzed. The diets of both species consisted of a variety of benthic prey, but only crustaceans and molluscs were important prey groups. While differences were found in the proportions of general prey categories eaten by these fishes, both species consumed substantial quantities of brachyuran crabs, bivalves, and gastropods. Specific identification of the prey items within these three food categories revealed additional differences in prey between the two puffer species. This partitioning of the food resources by bandtail and checkered puffers was found between both species overall, between overlapping size ranges, and between both species' most abundant size group. Differences in food habits between these two fishes illustrate that congeners with virtually identical mouth structure and complete spatial overlap can significantly partition the food resources.Contribution No. 78-58M from the U.S. Department of Commerce, NOAA, National Marine Fisheries Service, Southeast Fisheries Center, Miami Laboratory, Miami, Florida, USA.     

Brood or broadcast? The adaptive significance of different reproductive strategies in the two intertidal sea stars Leptasterias hexactis and Pisaster ochraceus

This paper considers the adaptive significance of two different reproductive methods in two co-occurring, competing sea stars. The smaller (3 to 8 g mean wet weight) Leptasterias hexactis broods relatively few, large young in the winter, while the large (300 to 650 g mean wet weight) Pisaster ochraceus broadcasts relatively many, small eggs each spring. L. hexactis matures at a small size (2 g wet weight) in about 2 years, and P. ochraceus matures at a larger size (70 to 90 g wet weight) in about 5 years (Menge, 1974). As in many broadcasting asteroids, gonad and storage organ indices of P. ochraceus are inversely related over time, and maximum storage-organ index correlates with the summer feeding maximum (Mauzey, 1966). In contrast, both organ indices of L. hexactis and feeding increase and are positively correlated until early autumn, when feeding activity begins to decline. At this time the male gonad index continues to rise, and the storage-organ index drops. In contrast, both organ indices of females rise. Spawning occurs from November to January. Thereafter storage-organ indices decline in females, presumably because females draw upon energy reserves while brooding; storage-organ indices rise in males, presumably because males do not brood and can feed if food is available. The primary cause for the differences between annual reproductive cycles of P. ochraceus and L. hexactis is suggested to be patterns of food availability for the released young (planktonic food for the broadcasted young of P. ochraceus and benthic prey for the brooded young of L. hexactis. Estimates of pre-maturity survival and post-maturity longevity indicate that the probability of survival per individual of young P. ochraceus is vastly lower than that of L. hexactis. However, once mature, P. ochraceus has a much longer expected lifespan. Brooding is suggested to be a coadaptive consequence of competition-induced small size. Assuming planktonic mortality rates in this environment are roughly constant across broadcasting species, I suggest that a small broadcasting species could not produce enough offspring in its expected lifespan to replace itself. This hypothesis is partly supported by some simple simulations. Broadcasting is suggested to permit rapid location and utilization of spatially and temporally unpredictable, but highly desirable, resources by allowing rapid and widespread dispersal. Brooders presumably cannot disperse rapidly and must rely on more reliable, but perhaps less desirable, resources. Factors affecting reproductive patterns in marine invertebrates include (1) food availability for both adults and offspring, (2) planktonic mortality rates, (3) interactions between species and latitudinal changes in these factors, and (4) various physical factors. This paper suggests that competition and predation can have an important effect on the evolution of reproductive methods, a possibility heretofore largely ignored. Although several similar examples of co-occurring species' pairs which differ in reproductive method and size are available, the role of adult interactions is unknown in these examples.     

Predation on zooplankton by the benthic anthozoans Alcyonium siderium (Alcyonacea) and Metridium senile (Actiniaria) in the New England subtidal

The Alcyonacean octocoral Alcyonium siderium Verrill and the sea anemone Metridium senile (L.), the only common perennial zooplanktivores on shallow (16-m depth) subtidal rock walls in much of northern New England, USA, are of similar heights and overlap in their habitat and microhabit distributions. The coelenteron contents of both species were sampled at four-hour intervals over a diel cycle and were compared to zooplankton available in the water at 1 to 5 cm from the rock wall, the height at which the cnidarians held their feeding tentacles. Prey in coelenterons of A. siderium were significantly smaller (means of 256 to 345 m), and those in coelenterons of M. senile were equal to or slightly greater in length (means of 415 to 1006 m) than the available zooplankton. The diets of A. siderium and M. senile differed significantly from each other and from the available zooplankton. A. siderium showed strong positive electivites for ascidian larvae and for foraminiferans, and strongly negative electivities for most crustaceans. M. senile had strong positive electivities for barnacle cyprids, ascidian larvae, and gammarid amphipods, and strong negative electivities for invertebrate eggs, foraminiferans, calanoid and harpacticoid copepods, and ostracods. Electivities may reflect tentacle avoidance or escape by motile prey as well as predator preference. Substratum-associated organisms (e.g. demersal crustaceans, larvae of benthic invertebrates) were the most common items in the diets of both species, suggesting a tight benthic food web, similar to the situation for coral reef anthrozoans which rely on reef-generated zooplankton. A. siderium ate large numbers of ascidian larvae which, as benthic adults, compete for space with A. siderium and can overgrow small colonies. Predation on the larvae of a competing species may alleviate competition by decreasing the competitor's recruitment.     

On the sociobiology of some hermaphroditic serranid fishes,the hamlets,in Puerto Rico

Three species of hamlets, Hypoplectrus chlorurus, H. unicolor, and H. puella (Pisces: Serranidae) were observed underwater off the west coast of Puerto Rico. They are predaceous fishes, feeding on small benthic organisms, and live in close association with the coral reef. Hamlets are highly aggressive and defend large territories, excluding their own and all other species of hamlets. They are synchronous hermaphrodites. In spawning, which occurs around sunset, one member of the pair ascends, the other joins it, each clasps the nape of the other with its tail, and gametes are released. Little color change occurs, but the black marking before the eye of H. unicolor fades when fixing on prey, proving it is not used as a sighting line. The all-black nominal species H. nigricans spawns with the yellow-tailed H. chlorurus, and is regarded here as a synonym of H. chlorurus.     

Assimilation,inter-organ transfer and excretion of americium in two teleost fish

Radiotracer experiments were performed (February–April, 1982) to study the assimilation and metabolism of the transuranium nuclide americium-241 in the marine teleosts Serranus scriba (Linnaeus, 1758) and Scorpaena notata Rafinesque, 1810, caught off the Monaco coast. Fish fed with ²⁴¹Am-labelled food showed that assimilation of this radionuclide takes place through the gastrointestinal walls and that the small fraction accumulated is incorporated mainly in the skin, muscle and skeleton. Gut-transfer coefficients were similar in both species and averaged 0.7% (range 0.1 to 1.7%) of the ingested activity. The calculated biological half-lives for loss of the absorbed fraction ranged between 49 and 61 d for Serranus scriba and 12 and 117 d for Scorpaena notata. Results from an intramuscular injection experiment indicated that ²⁴¹Am was retained mainly in the liver, skin and skeleton; the fraction accumulated by muscle was very low. Liver displayed a relatively short biological half-time for ²⁴¹Am loss of roughly 24 d. Routes of ²⁴¹Am excretion from the teleosts appear to be through the kidneys, gills and feces with bile serving as a possible excretion route from the liver. From the limited amount of published information available for comparison, experimental evidence is presented which suggests that ²⁴¹Am taken up via the food chain is more biologically available to marine fish than is plutonium.     

Grazing rates of the Atlantic menhaden Brevoortia tyrannus as a function of particle size and concentration

The feeding behavior of adult Atlantic menhaden (Brevoortia tyrannus) upon 5 species of phytoplankton and 2 species of zooplankton has been studied. Four recognizable feeding stages which were a function of the concentration and size of the food particles were observed. During rapid feeding the fish swam at a constant speed for a prolonged period over a wide range of particle concentrations. Particle and food carbon-concentrations at the threshold for initiation and termination of feeding were inversely related to particle size. Carteria chuii (13.2 μ) was not grazed at a significant rate, while two-cell chains of Skeletonema costatum (16. 5 μ) were filtered from the water, indicating a minimum-size threshold for filtration of between 13 and 16 μ. The most rapid filtering rates were observed for the copepod Acartia tonsa ( \(\bar x\) volume swept clear = 24.8 l/fish/min). The maximum food-particle size acceptable to a menhaden appears to be between Acartia tonsa (1200 μ) and adult Artemia salina (10 mm). These results suggest that the large schools of menhaden found in Atlantic coastal waters could have a significant effect on the plankton, selectively grazing zooplankton, larger phytoplankton, and the longer chains of chain-forming diatoms.     

Competition for food and other niche-related studies of three species of salt-marsh foraminifera

The niches of 3 species of salt-marsh foraminifera, Allogromia laticollaris, Rosalina leei, and Spiroloculina hyalina were assessed in the laboratory. The 3 species reproduce within the following ranges: temperature (10° to 33°C), salinity (12 to 45‰) and pH (5 to 10). Competition for food among the 3 species was evaluated. S. hyalina did not compete with other species. Intraspecific competition (crowding) appears to be an important factor limiting the reproduction of A. laticollaris. Crowding seems to have little effect on the other 2 species. The feeding of foraminifera is affected by the quality and quantity of food organisms. The feeding rate of the species tested is directly related to concentration within a range of 10² to 10⁶ cells fed. S. hyalina is a bacterial feeder. A. laticollaris is a rare species which may become locally abundant when dominant species are missing. S. hyalina is also a rare species, which can bloom where the density of bacteria is relatively high and in the absence of competing species. R. leei is a stable, conspicuous species, whose moderate numbers are relatively unaffected by physical stress and competition. Some new laboratory data on Ammonia beccarii were obtained so that this species could be compared with the other studied. Differences in niches are graphically presented.     

Feeding strategies and diets of breeding grey-headed and wandering albatrosses at South Georgia

The foraging areas and diets of the grey-headed albatross Thalassarche chrysostoma and wandering albatross Diomedea exulans were studied in March/April 2000 at Bird Island, South Georgia, during their respective chick-rearing and brood-guard periods. Oceanographically, March/April 2000 was abnormal, with warm conditions close to South Georgia. These conditions affected albatross foraging behaviour, particularly that of grey-headed albatrosses. Both species tended to forage in different areas of the ocean, with significant differences in trip durations. Grey-headed albatrosses (n=9) foraged mainly in Antarctic waters (predominantly shelf waters of the South Shetland Islands and Antarctic Peninsula, and also in oceanic waters around South Georgia), feeding mainly on krill (Euphausia superba; 77% by mass). Foraging trips lasted 13.3 days (range: 5–26 days), far longer than the 1–3 days found in previous studies. Only one grey-headed albatross was associated with the APF (Antarctic Polar Front), a reported foraging area in recent studies. Wandering albatrosses (n=9) foraged in Antarctic (South Georgia Shelf) and Antarctic Polar Frontal Zone (APFZ) waters, with trips of 1–4 days trip duration (usual for this species), feeding on fish (46% by mass) and cephalopods (32%). One bird was associated with the APF, and two birds foraged on the shelf/shelf break over the Patagonian shelf. These findings suggest that sea surface temperature anomalies, produced by movement of the APF closer to South Georgia or by eddies, may have had an effect on the foraging strategy of grey-headed albatrosses that year (the main prey of grey-headed albatrosses in previous studies, the ommastrephid Martialia hyadesi, is known to be associated with the APF). Also, when both albatross breeding periods overlap, their foraging areas were complementary, which reflected the prey taken.     

Diets of calanoid copepods on the West Florida continental shelf: Relationships between food concentration,food composition and feeding activity

Bottle incubations were conducted in March, July/August and October 1992. to measure the daily rations (R) and objectively characterize the diets of the calanoid copepodsEucalanus elongatus, Undinula vulgaris, Centropages velificatus andTemora stylifera from the west Florida continental shelf. Daily rations,R, were clustered around two, order-of-magnitude different means, 1.3 and 11.2% of body C d^–1, representative of quiescent and active feeding modes, respectively. The food concentration at which the transition from quiescent to active mode occurred was influenced by food particle size. In the quiescent mode, diets were dominated by nanoplankton, whereas no food type dominated the diet in the active mode. Selective feeding, defined as a statistically significant difference between the frequency distributions of foods in the diet and environment, occurred in both quiescent and active copepods. However, what appeared to be selective feeding in quiescent copepods could be explained by processes that passively modified the distribution of the diet relative to that of the food supply. Conversely, selective feeding in active copepods apparently resulted from foraging for particles >5 m in diameter in food environments dominated by nanoplankton (<5 m).     

Food resource utilization among five species of embiotocids at King Harbor,California, with preliminary estimates of caloric intake

The diets of 5 species of embiotocids (Rhacochilus vacca, Embiotoca jacksoni, Hypsurus caryi ryi, Phanerodon furcatus and Micrometrus minimus) from King Harbor, Redondo Beach, California, USA, are examined by means of a dietary survey, field feeding observations and bomb calorimetry of prey items. Each species is shown to have statistically different diets from all others, with the exception of H. caryi which apparently is a dietary intermediate between E. jacksoni and P. furcatus. Dietary overlap between E. jacksoni and H. caryi appears to have resulted in some competitive exclusion along other niche parameters. Estimated caloric intakes suggest that R. vacca has the highest caloric yield per bite and the lowest feeding rate of the species studied. Possible energetic advantages are found for diet specialization in R. vacca.     

Dimethyl disulfide and dimethyl trisulfide: so similar yet so different in evoking biological responses in saprophilous flies

Dimethyl disulfide (DMDS) and dimethyl trisulfide (DMTS) are used by saprophilous insects to locate breeding sites (decaying organic matter), and by brood-site deceptive flowers to attract such insects. However, little is known about the relative importance of these two compounds in eliciting electrophysiological and behavioral responses in the insects. Here, we compared the relative attractiveness of DMDS and DMTS to saprophilous flies in field choice experiments and tested whether potential differences in field responses can be explained by differences in electrophysiological antennal responses to these compounds. Field experiments revealed that the attractiveness of a mixture of these compounds is due to DMTS alone. This result was confirmed by electroantennographic recordings in which flies of four tested species of Calliphoridae (Lucilia sericata, L. caesar, Calliphora vicina, Protocalliphora azurea) and one Muscidae (Musca domestica) respond clearly to DMTS, but not to DMDS. In house flies, however, DMTS elicited electrophysiological responses only, not reflected in behavioral assays. Despite the fact that DMTS and DMDS exhibit similar chemical structures, both the electroantennographic and field responses from saprophilous flies to these two compounds strongly differed. Our study suggests that oligosulfide-responsive saprophilous flies rely on DMTS and not DMDS for finding appropriate breeding sites and that DMTS and not DMDS could act as a key mediator for pollinator attraction in brood-site deceptive plants.     

Shell parameters in relation to zonation in mediterranean limpets

The relation of shell form to habitat in the Mediterranean limpets Patella caerulea (L.) and P. lusitanica (Gmelin) was investigated. P. caerulea shells were significantly longer, broader, but lower in height than P. lusitanica shells. The regression of the ratio (length plus breadth)/2 on the height of the shell was found to characterize the two limpet populations, with a small degree of overlap reflecting the distribution of the two limpets on the shore.