Notes on New Zealand mammals 6. Second report on the stomach contents of long‐finned pilot whales,Globicephala melas

Abstract

We report data on the stomach contents of the long‐finned pilot whale, Globicephala melas, recovered from a group of whales stranded on Ruakaka Beach, northeastern New Zealand, in November 2006. In nine whales for which identifiable stomach contents were recovered (three that stranded on 10 November and six that stranded on 11 November) prey remains comprised exclusively cephalopod beaks attributed to five squid species. The stomachs of a further two whales contained unidentifiable upper beaks only, while the stomachs of five whales were completely empty. No whale appeared to have been satiated immediately before stranding, given that the maximum biomass of prey recently consumed by any one whale was calculated to be <5 kg. All squids ingested represented oceanic species, found from 50 to 1000 m but more common towards the deeper end of this range. These data both complement and contrast with the only other dietary information available for this species in New Zealand waters, reported from stomach contents of whales stranded on Farewell Spit, South Island in December 2005.     

Utilization of stomach content DNA to determine diet diversity in piscivorous fishes

The objective of the study was to validate and apply DNA-based approaches to describe fish diets. Laboratory experiments were performed to determine the number of hours after ingestion that DNA could be reliably isolated from stomach content residues, particularly with small prey fishes (c. 1 cm, <0·75 g). Additionally, experiments were conducted at different temperatures to resolve temperature effects on digestion rate and DNA viability. The molecular protocol of cloning and sequencing was then applied to the analysis of stomach contents of wild fishes collected from the western basin of Lake Erie, Canada-U.S.A. The results showed that molecular techniques were more precise than traditional visual inspection and could provide insight into diet preferences for even highly digested prey that have lost all physical characteristics.     

Molecular identification of prey in the stomach contents of Harp Seals (Pagophilus groenlandicus) using species-specific oligonucleotides

All methods of diet analysis in marine mammals, including hard part analysis (HPA), have biases affecting the accuracy of prey-species identification and frequency in the estimated diet due to differential consumption, digestion and retention. Using PCR amplification of specific prey DNA with species-specific primers, we developed a DNA-based method that complements HPA and provides an alternative means to detect prey from stomach contents of Harp Seals (Pagophilus groenlandicus). The target size that could be reliably amplified was determined using a digestion time-series of Atlantic Cod (Gadus morhua) tissue in simulated seal stomachs. Various target lengths were trialed using general teleost primers; amplicons of approximately 800 bp or less were consistently obtained. Prey species-specific PCR primers for Atlantic Cod, Arctic Cod (Boreogadus saida) and Capelin (Mallotus villosus) were designed and tested with DNA from the stomach contents of 31 Harp Seals. Amplicons were obtained for all three species-specific primer sets. Amplification results compared with HPA revealed: (i) Atlantic Cod hard parts were found in five stomachs where no Atlantic Cod DNA amplified, suggesting that Atlantic Cod may be over-represented in the estimated diet, (ii) amplification of Arctic Cod DNA occurred for 17 stomachs, including all 12 stomachs with, and five stomachs without, Arctic Cod hard parts, and (iii) Capelin DNA amplified for four of five stomachs with Capelin hard parts and for one stomach without Capelin hard parts. We conclude that PCR amplification of specific prey DNA provides a viable means to complement Harp Seal diet analysis by HPA, but suggest that valuable information for quantitative diet analysis rests in a quantitative PCR approach.     

Gastric evacuation of mixed stomach contents in predatory gadoids: an expanded application of the square root model to estimate food rations

A mechanistic gastric evacuation model of mixed stomach contents was established. Its simple generic nature should prove useful for studying predator‐prey interactions in fish communities. Only prey lengths were required as additional input. Surface dependent digestive processes were considered to act on equal fractions of individual prey‐cylinder surfaces. Primary and interactive effects of size, energy density and resistance to digestion of individual prey in a stomach were described by the model. Model predictions of results from experiments on gastric evacuation of meals composed of different prey types demonstrated the capability of this model, as opposed to previously applied model principles, to predict evacuation of mixed stomach contents involving the three above‐mentioned prey characteristics. The study furthermore illustrated that estimates of food ration might be severely biased by using improperly formulated effects of prey characters on gastric evacuation, and demonstrated that the new model holds the potential to predict food ration and diet composition for wild populations of predatory fishes.     

Can stomach temperature telemetry be used to quantify prey consumption by seals? A re-examination

 To further determine the efficacy of stomach temperature probes in quantifying harp seal (Phoca groenlandica) feeding behaviour, captive seals were fed stomach temperature sensors and given pre-weighed meals of herring (Clupea harengus) and crushed ice. Ingestion of either substance caused a decrease in stomach temperature. Results suggested that the magnitude of the stomach temperature change could indicate whether an ingested substance was a prey item or ice. The duration of stomach temperature change was significantly related to the quantity of fish consumed, but it accounted for just 27% of the overall variation. This percentage was considerably less than previously reported, perhaps due to the more extensive sampling regime of this study. Both the magnitude and duration of temperature change were related to the quantity of ice consumed, accounting for 69% of the mass variation. However, subsequent modelling revealed that the relationship was not robust. Despite problems with quantification, combining the use of stomach temperature telemetry with time-depth and satellite recordings could provide valuable information on the location, timing and frequency of prey consumption by seals. Results indicate that, with sufficient samples, this technique may provide a valuable tool for investigating the feeding ecology of seals and other marine endotherms. Received: 8 February 1995/Accepted: 4 August 1995     

Stable isotope analysis as a tool to monitor dietary trends in little penguins Eudyptula minor

Long‐term dietary monitoring of seabirds can be used to relate population fluctuations to at‐sea events. Stomach flushing is a conventional dietary monitoring technique, but has a number of disadvantages. Stable isotope analysis (SIA) is a less invasive method that provides unbiased dietary information over a longer period. We evaluated stable isotope analysis as a potential tool for monitoring long‐term little penguin Eudyptula minor diet. We determined diet composition during the chick feeding stage using stomach flushing and SIA at three separate colonies, using spatial variation in diet as a surrogate for potential temporal variation. Bayesian isotopic mixing models were generated for blood and feathers to evaluate their ability to discriminate broad‐scale (fish, squid, crustaceans) and fine‐scale (individual prey species) diet composition. Differences in stable carbon and nitrogen isotope ratios were found between colonies: broad‐scale isotopic mixing models predicted different proportional contributions of broad taxa (fish, cephalopod, crustacean) to diet than was indicated by stomach samples, reflecting the bias incurred by one‐off stomach contents analysis. Fine‐scale isotopic mixing models predicted proportional contributions of prey items with less certainty. Blood isotopic mixing models had narrower confidence intervals than models for feathers, but trends in δ¹⁵N for feathers mirrored those for blood. Our results suggest that relying on stomach contents analysis to detect shifts in prey consumption in little penguins could be very misleading, resulting in a less‐than‐complete idea of total prey consumption. SIA of little penguin tissues could be used to monitor dietary shifts across dissimilar taxa that may affect population numbers, but would fail to detect shifts between fish species.     

Prey selection and diel feeding of the freshwater jellyfish, Craspedacusta sowerbyi

1. The diet of the invasive freshwater jellyfish, Craspedacusta sowerbyi (Lankester), was assessed by analysing its stomach contents. 2. The medusae ingested various zooplankton and benthic prey in the 0.1–3.0 mm size range. The selectivity indices for prey showed that larger zooplankton (0.4–1.4 mm) and active prey such as copepods were preferred; small potential prey, and the loricate rotifer Keratella cochlearis in particular, were almost never consumed. Measurements suggest that spacing between the tentacle branches could determine prey selection. Another possibility is that some prey are too small or slow to activate nematocysts after collision with the predator. Prey > 1.4 mm can probably escape or are otherwise too large to be handled. 3. The medusae of Craspedacusta medusae stayed in deep water during daytime and migrated upwards at night. The greatest number of prey in freshwater jellyfish stomachs was detected at night. 4. Calculation of consumption rates, based on mean stomach contents and digestion times of 4–5 h, showed that, on average, one medusa takes 190 zooplankton prey day^??1 at a mean prey density of about 100 L^??1. At the observed medusae density of 1 m^??3, the cropping rate was about 0.2 zooplankton prey L^??1 day^??1.     

LABORATORY DIGESTION OF PREY AND INTERPRETATION OF WALRUS STOMACH CONTENTS

A new approach for evaluating the potential biases of walrus ( Odobenus rosmarus ) diet data derived from stomach contents was examined based on the rates at which different prey types were digested. In this study controlled digestion experiments on polychaetes, echiurid and sipunculid worms, clams, snails, and crabs demonstrated that these prey items did not remain equally identifiable during digestion. Polychaetes, echiurids, and sipunculids were the least persistent prey. All worms became unidentifiable during the six-hour digestion trials. Over 50% of the clams maintained their diagnostic tissues ( i. e. , foot and/or siphon). Clam viscera did not survive hour 2. Snails and crustaceans were the most persistent prey. Without a consideration of the state of digestion, a stomach sample may not accurately reflect the species composition and size of prey consumed. Volume is not a reliable measure of a prey's relative importance, as the diagnostic fragments of invertebrate prey in a stomach vary greatly in physical composition. Walruses probably consume all of the soft tissues of clams, not solely the foot and siphon.     

Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay

Parasites that are transmitted through predator–prey interactions may be used as indicators of trophic relationships between organisms. Yet, they are rarely used as such in the construction of topological (predator–prey) food webs. We constructed food webs of vertebrate trophic interactions using observed diet alone, trophically transmitted parasites alone, and the combination of the two based on data from 31 species of fish from the Bothnian Bay, Finland. The fish food web contained 530 links derived from observed diet, 724 links inferred from parasitism, and 1,058 links calculated from a combination of both stomach contents and parasites. This sub-web constructed from stomach contents had a mean of 17.1 links per fish species, while that using parasites had 23.4 links per fish. Combining the two diet indicators yielded 34.1 links per fish species, illustrating the complementarity of the two methods. Mean number of prey species per fish species was 12.5 using observed diet items, 15.8 using parasites, and 24.5 using both measures together. Mean number of predators per fish species was 7.4 using observed diet, 11.7 using parasites and 15.0 using both. A positive correlation was found between the mean number of parasites and the number of prey taxa in the diet among the fishes. Omnivorous fish had the highest diversity of both parasite species and prey items, while benthophagous fish had among the lowest. Mean total abundance and mean total prevalence of parasites correlated positively with fish size, with piscivores being the largest with the highest abundance and prevalence, while planktivores and benthivores had the lowest. Trophically transmitted parasites may be used to help construct vertebrate sub-webs and derive information about food web processes. Parasites alone provided equivalent if not more information than observed diet. However, resolution is improved by using parasites and observed diet together.     

STOMACH CONTENTS OF LONG-FINNED PILOT WHALES (GLOBICEPHALA MELAS) STRANDED ON THE U.S. MID-ATLANTIC COAST

Ten prey taxa were recorded from the stomach contents of eight long-finned pilot whales ( Globicepbala melas ) independently stranded along the U.S. mid-Atlantic coast. Relative importance of prey species was determined by methods that incorporate prey frequencies of occurrence, proportions of numerical abundance, and proportions of reconstructed mass. Separate analyses of trace (free, durable body parts representing well-digested prey items) and non-trace (relatively intact prey specimens) food material were conducted in order to address biases caused by differential rates of digestion and passage through the gastrointestinal tract. Different measures of prey importance yielded varying results, but the long-finned squid ( Loligo pealei ) was the most important prey species regardless of how prey importance was defined. Fishes were relatively unimportant in the diet. Our results indicate that the diets of western North Atlantic long-finned pilot whales differ substantially from what has been previously reported in the literature and that results from food-habits studies that utilize different techniques may not be comparable.     

The role of escape reactions in determining the size distribution of prey captured by herring larvae

Synopsis Fish larvae are selective planktivores, and size is an important factor in prey selection. However, for herring larvae, a selection model based solely on the principle of optimising calorific gain per unit energy expenditure consistently overestimates the mean size of ingested prey. Most such models ignore the escape capabilities and shape of the prey, and the potential role of escape on capture success. In this paper, a static foraging model incorporating both selection and escape is described and tested against published data on the composition of herring larvae stomach contents. The results indicate that prey escape is a major factor structuring the diet composition of the larvae.     

Amoebic grazing of freshwater Synechococcus strains rich in phycocyanin

Fifteen strains of naked amoebae were presented with 19 strains of Synechococcus on an agar surface. After 14 days of incubation, each of the 285 combinations yielded one of three responses. 42.1% of combinations showed clearing (digestion) of the Synechococcus (C), 56.5% of combinations showed no clearing of the Synechococcus (N) while 1.4% of combinations showed partial clearing of the Synechococcus (P). In general, the Synechococcus strains showed variability in their susceptibility to digestion by the amoebae and the amoebae showed variability in their ability to digest the Synechococcus strains. There was no evidence for amoebae actively selecting profitable prey and equivalent-sized Synechococcus strains were ingested at the same rate, irrespective of their fate. There was some evidence of 'size-selective' grazing in that amoebae ingested the smaller Synechococcus strains at higher rates than the larger strains. However, there was no correlation between prey size and their ultimate fate. These data suggest that amoebae are not selective with regard to the ingestion of synechococci, but that 'selection' occurs at the digestion stage, i.e. whether the synechococci are digested or not.     

How are feathers digested by raptors?

In order to determine the cause of the evident degradation of feathers from ingested prey in pellets regurgitated by raptors, in vitro digestions of whole feather barbs by pellet extracts, pepsin or trypsin were carried out. The material was analysed by using biochemical and electron microscopic methods. The results show that the changes in the feathers which occur in the stomach of the Falconidae do not arise from digestion of keratin but from hydrolysis of protein acting as a cement matter in the feather.     

A surface-dependent gastric evacuation model for fish

A gastric evacuation curve expresses how fast prey disappear from the stomach, and empirical models are used generally for the relationship between weight of prey remaining ( W_t ) and time ( t ) after a meal. Unfortunately, empirical models are likely to have restricted applicability because their parameters often represent limited biological mechanisms. This paper develops a simple digestion model. The simplest form of the model has four parameters; the digestion velocity (expressing enzymatic breakdown of prey), prey length, initial prey radius and the density of the prey. Two more parameters are included in an extended version; a time-delay before digestion starts and environmental temperature. The approach is based on the assumption that prey digestion is a surface process in that digestive enzymes attack progressively deeper into a prey of known size and shape so that the average digestion rate is proportional to the prey radius r (m). This process is characterized by the digestion velocity d_s (m s ^–1). Unknown parameters are estimated with uncertainty using the maximum likelihood technique. Model evaluation using published data sets demonstrated that the new model is flexible. Prey geometry is incorporated into the model and temperature effects upon gastric evacuation are linked directly to the digestion velocity.     

A nematomorph parasite explains variation in terrestrial subsidies to trout streams in Japan

Nematomorph parasites alter the behavior of their orthopteran hosts, driving them to water and creating a source of food for stream salmonids. We investigated whether nematomorphs could explain variation in terrestrial subsidies across several streams. In nine study streams, orthopterans comprise much of the stomach contents of trout (46 ± 31% on average). Total mass of ingested prey per trout biomass positively correlated with the mass of orthopterans ingested, suggesting that the orthopterans enhanced absolute mass of prey consumption by the trout population. The orthopterans ingested per trout biomass positively correlated with the abundance of nematomorphs in the stream, but not with the abundance of camel crickets (the dominant hosts) around the streams. Streams in conifer plantations had fewer nematomorphs than streams in natural deciduous forests. These results provide the first quantitative evidence that a manipulative parasite can explain variation in the allochthonous energy flow through and across ecosystems.     

Methods of estimating marine mammal diets: A review of validation experiments and sources of bias and uncertainty

Diet estimation in marine mammals relies on indirect methods including recovery of prey hard parts from stomachs and feces, quantitative fatty acid signature analysis (QFASA), stable isotope mixing models, and identification of prey DNA in stomach contents and feces. Experimental evidence (9 species/13 studies) shows that digestion strongly influences the proportion and size of otoliths that can be recovered in feces. Number correction factors (NCF) and digestion coefficients have been experimentally determined to reduce the biases in fecal analysis. Correction factors and coefficients have not been determined for diet estimated from stomach contents. QFASA estimates which prey species and amounts must have been eaten to account for the fatty acid composition of the predator. Experimental studies on mammals and seabirds (9 species/10 studies) indicate that accurate estimates of diet can be determined using QFASA. Stable isotope mixing models provide rather coarse taxonomic resolution of diet composition. Prey DNA analysis shows promise as a method to estimate the species composition of diet, but further development and testing is needed to validate its use. Obtaining a representative sample from marine mammal populations is a significant challenge. Therefore, the use of complementary methods is recommended to obtain the most informative results.     

The food and feeding habits of the Torrent frog, Amolops larutensis

The stomach contents of 661 Amolops larutensis (Blgr.) showed that this frog feeds on a wide range of terrestrial and aquatic animals of which insects form the greater part. Feeding was confined to the rocks and vegetation bordering the water-falls. Although adult frogs were capable of ingesting large prey up to a maximum length of 47.0 mm, they showed a definite preference for prey animals within the size-range of 1 to 6.5 mm length. No clear seasonal variation in the diet was found and it was suggested that the monthly fluctuations in the amount and type of prey ingested depend largely on the activity of the prey.     

A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators

Accurate identification of species that are consumed by vertebrate predators is necessary for understanding marine food webs. Morphological methods for identifying prey components after consumption often fail to make accurate identifications of invertebrates because prey morphology becomes damaged during capture, ingestion and digestion. Another disadvantage of morphological methods for prey identification is that they often involve sampling procedures that are disruptive for the predator, such as stomach flushing or lethal collection. We have developed a DNA-based method for identifying species of krill (Crustacea: Malacostraca), an enormously abundant group of invertebrates that are directly consumed by many groups of marine vertebrates. The DNA-based approach allows identification of krill species present in samples of vertebrate stomach contents, vomit, and, more importantly, faeces. Utilizing samples of faeces from vertebrate predators minimizes the impact of dietary studies on the subject animals. We demonstrate our method first on samples of Adelie penguin (Pygoscelis adeliae) stomach contents, where DNA-based species identification can be confirmed by prey morphology. We then apply the method to faeces of Adelie penguins and to faeces of the endangered pygmy blue whale (Balaenoptera musculus brevicauda). In each of these cases, krill species consumed by the predators could be identified from their DNA present in faeces or stomach contents.     

The feeding strategy of dab Limanda limanda in the southern North Sea: linking stomach contents to prey availability in the environment

The feeding strategy of dab Limanda limanda was investigated within a predefined research area in the southern North Sea for 2 years. The aims were: 1) to establish the relationship between prey availability and dab abundance, distribution, body condition and prey selection, and 2) to determine the underlying functional processes of prey choice in dab. Temporal and spatial trends of prey availability in relation to dab abundances, distribution, condition and prey selection were analysed. Temporal trends in dab condition, percentage of empty stomachs and numbers of ingested prey were apparent. In particular in the winter period 2000–2001 dab were in poor condition and prey items were only rarely found in stomachs. Similarly prey availability decreased in the environment while the abundance of dab increased. Thus, temporal changes in the nutritive state were partly thought to be attributed to density‐dependent effects. The stomach composition of dab during the two consecutive summers was mainly dominated by Pariambus typicus and Ophiura albida while in the winter period only O. albida made a significant contribution to the stomach content. Analysis of prey characteristics indicated that only prey densities in the environment significantly influenced prey choice in dab, while other characteristics such as the position of the prey in the habitat, its palatability or mobility did not have significant effects. The feeding strategy of dab thus was highly opportunistic, although trends were apparent that suggested that buried living fauna was less likely to be ingested, which was also observed in previous studies.     

Digestibility of chitin in cod,Gadus morhua,in vivo

Sixteen cod,Gadus morhua (L.), were individually fed a single ration of shrimps,Crangon allmanni. Four fish were killed and examined 6, 12, 24 and 48 h after the fish had been fed. Chitinase activities were measured in the extracts of stomach contents, stomach tissue, pyloric caecae, intestinal contents and intestinal tissue. The level of enzyme activity in different parts of the digestive tract was shown to be dependent on the phase of the digestive process. High concentrations of the chitin degradation product N-acetyl-D-glucosamine were determined in the stomach and in the intestinal contents. Based on the chitin concentration in the food organisms and the individual food uptake, the amount of chitin consumed by each fish could be calculated. Only up to 9% of the ingested chitin was recovered from the intestinal contents of the fish at any given time after feeding (6, 12, 24 and 48 h). In addition, only 2.4% of the chitin consumed with the food could be recovered in the collected faeces of the fish. The 4 cod killed 48 h after feeding had completely emptied their stomach. Chitin digestion in these fish was calculated to have been 90%.