Prey species and prey diet affect growth of invertebrate predators

1. The effects of prey species and leaf age used by prey on performance of two generalist invertebrate predators were studied. The focal plant was Plantago lanceolata , which contains iridoid glycosides.
2. Diet of the herbivorous prey influenced their growth rate.
3. The generalist herbivore ( Vanessa cardui ) and the novel-plant feeder ( Manduca sexta ) contained very low levels of iridoid glycosides in their haemolymph, whereas the specialist ( Junonia coenia ) levels were 50–150-fold higher.
4. Predatory stinkbugs ( Podisus maculiventris ) fed either the novel-plant feeder or the specialist exhibited similar developmental rates. However, stinkbugs ate less of the generalist but grew faster. The growth rate of the stinkbugs was higher when the caterpillar species were raised on the new-leaf powder diet, which contained twice as much protein and iridoid glycosides as the mature-leaf powder diet.
5. Jumping spiders ( Phidippus audax ) ate more mealworms ( Tenebrio molitor ) than specialist J. coenia caterpillars, fed either new- or mature-leaf powder diets, and could not gain weight when fed J. coenia.
6. These results indicate that prey quality was not determined solely by the iridoid glycoside concentration in the diet.     

Drug discovery and sea hares: bigger is better

Traditionally, small molecules (<1kDa) have dominated the study of the chemistry and chemical ecology of marine natural products. However, as reported in a recent publication, Yang and co-workers have isolated a 60-kDa antibacterial protein from the defensive secretions of the sea hare Aplysia californica. This protein, escapin, has been characterized as an l-amino acid oxidase with bacteriostatic and bacteriocidal activities. Their work highlights the largely untapped biomedical potential of marine organism-derived proteins and addresses the problems of supply associated with invertebrate natural products. It also leads to intriguing hypotheses about the ecological function(s) of the new protein.     

Antitumor and antimicrobial glycoproteins from sea hares

1. Novel antitumor and antimicrobial glycoproteins were found in the sea hares. These glycoproteins were purified to apparent homogeneity from Aplysia kurodai, Aplysia Juliana and Dolabella auricularia, and designated as aplysianins, julianins and dolabellanins, respectively.2. The nine isolated glycoproteins lysed all the tumor cells tested but did not lyse normal white and red blood cells.3. The glycoproteins completely inhibited the synthesis of DNA and RNA by tumor cells within 2 hr and caused tumor lysis within 15hr.4. Tumor lysis was inhibited by the presence of N-acetylneuraminic acid, suggesting that the recognition of the sugar moiety is a key step in the cytolysis by antitumor glycoproteins from sea hares.5. These antitumor glycoproteins, except dolabellanin P, also showed antimicrobial activities.6. The factors were active for Gram-positive and -negative bacteria and some fungi, and their action was not cytocidal but cytostatic.7. They exerted the antibacterial action by inhibiting nucleic acid synthesis, as does a DNA-inhibiting chemotherapeutic drug.8. The sequence of the N-terminal part of dolabellanin A was similar to other antibacterial peptides from arthropoda, amphibia and mammals, suggesting that dolabellanin-like antibacterial peptides are common throughout the animal kingdom.     

Growth of larval and juvenile perch: the importance of diet and fish density

In August, growth rate of young–of–the–year (YOY) Perch In lake enclosures could be explained by both YOY density and mean cladoceran biomass, suggesting that in a lake where YOY perch are dominant, growth may be density dependent in late summer and mediated through top–down control on daphnid biomass. In June, growth rate of YOY perch could not be fully explained by YOY density or by mean cladoceran biomass, suggesting that growth and survival during the first part of the summer is negatively affected by a diet of Bosmina and cyclopoid copepods only. The experiments also suggest why YOY perch have a slow growth and a low abundance in eutrophic lakes where small zooplankton dominate. The June experiment also indicated that growth of late larval or early juvenile perch improved when a larger cladoceran became available and was included in the diet.     

Profiling invasive fish species: the importance of phylogeny and human use

Understanding the ecological differences between native and invasive species is of considerable scientific and practical interest. We examined such differences between native and invasive inland fish species from the Iberian Peninsula in order to analyse the importance of phylogenetic correction and variability (in addition to central tendency). We collected 26 quantitative and qualitative variables on the ecology, life‐history traits and human use of the 69 inland fish species of the Iberian Peninsula, including native, invasive and migratory species. The taxonomic distribution of invasive fish species deviated significantly from world freshwater richness and in contrast to native species, invasive fish belongs to only five taxonomic orders but to a wide spectrum of families not native to the Iberian Peninsula. Because the life‐history traits were highly dependent on taxonomy, the results, with or without applying phylogenetic methods, differed and after accounting for phylogeny, invasive species displayed higher and wider latitude in general and a different reproductive season mainly among salmonids and cyprinids. Human use was also significantly different between native and invasive fish species and produced more variability in life‐history traits of invasive species and uneven taxonomic distribution because of the high diversity of species introduced. We show that accounting for taxonomy and studying variability in addition to central tendency is important in the comparison of life‐history traits between native and invasive species.     

Metabarcoding for the parallel identification of several hundred predators and their prey: Application to bat species diet analysis

Assessing diet variability is of main importance to better understand the biology of bats and design conservation strategies. Although the advent of metabarcoding has facilitated such analyses, this approach does not come without challenges. Biases may occur throughout the whole experiment, from fieldwork to biostatistics, resulting in the detection of false negatives, false positives or low taxonomic resolution. We detail a rigorous metabarcoding approach based on a short COI minibarcode and two‐step PCR protocol enabling the “all at once” taxonomic identification of bats and their arthropod prey for several hundreds of samples. Our study includes faecal pellets collected in France from 357 bats representing 16 species, as well as insect mock communities that mimic bat meals of known composition, negative and positive controls. All samples were analysed using three replicates. We compare the efficiency of DNA extraction methods, and we evaluate the effectiveness of our protocol using identification success, taxonomic resolution, sensitivity and amplification biases. Our parallel identification strategy of predators and prey reduces the risk of mis‐assigning prey to wrong predators and decreases the number of molecular steps. Controls and replicates enable to filter the data and limit the risk of false positives, hence guaranteeing high confidence results for both prey occurrence and bat species identification. We validate 551 COI variants from arthropod including 18 orders, 117 family, 282 genus and 290 species. Our method therefore provides a rapid, resolutive and cost‐effective screening tool for addressing evolutionary ecological issues or developing “chirosurveillance” and conservation strategies.     

Influence of multiple predators decreases body condition and fecundity of European hares

1. We assessed the hypothesized negative correlation between the influence of multiple predators and body condition and fecundity of the European hare, from 13 areas in the Netherlands.
2. Year‐round abundance of predators was estimated by hunters. We quantified predator influence as the sum of their field metabolic rates, as this sum reflects the daily food requirements of multiple individuals. We determined the ratio between body mass and hindfoot length of hares as an index of body condition and the weight of their adrenal gland as a measure of chronic exposure to stress, and we counted the number of placental scars to estimate fecundity of hares.
3. As hypothesized, we found that the sum of field metabolic rate of predators was negatively correlated with body condition and the number of placental scars, whereas it was positively related to the weight of the adrenal glands. In contrast to the sum of the field metabolic rate, the total number of predators did not or weakly affect the investigated risk responses.
4. The sum of the field metabolic rate can be a useful proxy for the influence of multiple predators and takes into account predator abundance, type, body weight, and food requirements of multiple predators.
5. With our findings, our paper contributes to a better understanding of the risk effects of multiple predators on prey fitness. Additionally, we identify a potential contributor to the decline of European hare populations.

     

Integrative biology: sea hares saved by a delicious distraction

When threatened, sea hares secrete ink and opaline. This mixture has now been shown to act on peripheral chemosensory neurons of spiny lobsters, stimulating feeding-related behaviours as a deceptive method of avoiding predation.     

Morphological characteristics in relation to diet in five coexisting Thai fish species

Morphological characteristics and intestinal content were analysed for five species of coexisting freshwater fishes in Thailand: Rasbora caudimaculata , Schistura desmotes , Dermogenys pusillus , Xenentodon cancila and Monopterus albus (all found in riffle habitats in Thai streams). Rasbora caudimaculata , S. desmotes and D. pusillus fed predominantly on ephemeropterans, hymenopterans and dipterans, X. cancila fed predominantly on fishes, and larger aquatic invertebrates such as Odonata, and M. albus fed on detritus as well as invertebrate prey such as crustaceans and Odonata. Intestine length, mouth height, mouth width, eye position and mouth orientation varied among all five species. Canonical analysis of discriminance of mouth height, width and intestine length showed a clear dispersion of species, which was supported by intestine content. Evolutionary processes leading to the present differences in morphological characters resulted in each of the five species consuming a different portion of the available resource base, thereby facilitating coexistence.     

PCR enrichment techniques to identify the diet of predators

The increasing sensitivity of PCR has meant that in the last two decades PCR has emerged as a major tool in diet studies, enabling us to refine our understanding of trophic links and to elucidate the diets of predators whose prey is as yet uncharacterized. The achievements and methods of PCR-based diet studies have been reviewed several times, but here we review an important development in the field: the use of PCR enrichment techniques to promote the amplification of prey DNA over that of the predator. We first discuss the success of using group-specific primers either in parallel single reactions or in multiplex reactions. We then concentrate on the more recent use of PCR enrichment techniques such as restriction enzyme digests, peptide nucleic acid clamping, DNA blocking and laser capture microdissection. We also survey the vast literature on enrichment techniques in clinical biology, to ascertain the pitfalls of enrichment techniques and what refinements have yielded some highly sensitive methods. We find that while there are several new approaches to enrichment, peptide nucleic acid clamping and DNA blocking are generally sufficient techniques for the characterization of diets of predators and highlight the most important considerations of the approach.     

Winter browsing of brown hares: evidence for diet breadth expansion

Foraging theory predicts that diet breadth should expand as food availability decreases. We tested this by looking at the winter browsing behaviour of the brown hare Lepus europaeus. We predicted selective feeding on different woody plant species, diet generalisation under increasingly severe winter conditions and a rank preference between the different food items. Following a period of severe winter conditions, we censused browsing marks of brown hares on woody plants at six sites situated at different altitudes (340 – 600 m a. s. l.) in Upper Franconia, Germany. We assumed that access to ground vegetation, which is the general diet of brown hares, was more restricted at sites with higher snow cover. The results provided support for all of our predictions: Feeding intensity varied strongly between the different plant species indicating selectivity of feeding. The number and also the percentage of browsed woody plant species was positively correlated with the altitude of the study site indicating a wider diet breadth in situations where less food was available. On the basis of a rank model on the food choice of brown hares, which was evaluated by an independent data set, we conclude that brown hares show a rank preference with regard to different groups of woody plant species. Our findings support the assumption that food restricted hares increasingly include unfavourable, low quality items into the diet.     

Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay

Recent studies of aquatic food webs show that parasite diversity is concentrated in nodes that likely favour transmission. Various aspects of parasite diversity have been observed to be correlated with the trophic level, size, diet breadth, and vulnerability to predation of hosts. However, no study has attempted to distinguish among all four correlates, which may have differential importance for trophically transmitted parasites occurring as larvae or adults. We searched for factors that best predict the diversity of larval and adult endoparasites in 4105 fish in 25 species studied over a three-year period in the Bothnian Bay, Finland. Local predator–prey relationships were determined from stomach contents, parasites, and published data in 8,229 fish in 31 species and in seals and piscivorous birds. Fish that consumed more species of prey had more diverse trophically transmitted adult parasites. Larval parasite diversity increased with the diversity of both prey and predators, but increases in predator diversity had a greater effect. Prey diversity was more strongly associated with the diversity of adult parasites than with that of larvae. The proportion of parasite species present as larvae in a host species was correlated with the diversity of its predators. There was a notable lack of association with the diversity of any parasite guild and fish length, trophic level, or trophic category. Thus, diversity is associated with different nodal properties in larval and adult parasites, and association strengths also differ, strongly reflecting the life cycles of parasites and the food chains they follow to complete transmission.     

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.     

New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning

Introduced species can alter the topology of food webs. For instance, an introduction can aid the arrival of free-living consumers using the new species as a resource, while new parasites may also arrive with the introduced species. Food-web responses to species additions can thus be far more complex than anticipated. In a subarctic pelagic food web with free-living and parasitic species, two fish species (arctic charr Salvelinus alpinus and three-spined stickleback Gasterosteus aculeatus) have known histories as deliberate introductions. The effects of these introductions on the food web were explored by comparing the current pelagic web with a heuristic reconstruction of the pre-introduction web. Extinctions caused by these introductions could not be evaluated by this approach. The introduced fish species have become important hubs in the trophic network, interacting with numerous parasites, predators and prey. In particular, five parasite species and four predatory bird species depend on the two introduced species as obligate trophic resources in the pelagic web and could therefore not have been present in the pre-introduction network. The presence of the two introduced fish species and the arrival of their associated parasites and predators increased biodiversity, mean trophic level, linkage density, and nestedness; altering both the network structure and functioning of the pelagic web. Parasites, in particular trophically transmitted species, had a prominent role in the network alterations that followed the introductions.     

Summer diet selection of snowshoe hares: a test of nutritional hypotheses

We examined summer diet selection by snowshoe hares in the southwestern Yukon, Canada, and attempted to explain how plant qualities such as nutritional content (protein, energy, fiber, water) and defensive compounds affect hare food choice. Male hares were placed in enclosures in natural vegetation areas dominated by shrubs and in both open and closed spruce forests. Each site contained a variety of herbaceous plant species. After 24 h, hares were sacrificed, their stomachs collected, and the contents removed and analyzed. Of the 30 plant species recorded in the enclosures only 10 were identified in the stomach contents of the hares. The summer diet is composed predominantly of five plant species; Lupinus arcticus, Salix spp. Shepherdia canadensis, Betula glandulosa and Festuca altaica. The selection of these species changes between sampling times. Protein, energy and water contents were highest in leaf tissues of most species early in the season, and most species had an increase in fiber through the summer. Protein content consistently explains the largest amount of variation in diet selection, although protein selection is modified by extremely high concentrations of defence compounds. It is likely that hares are not protein limited and are selecting for other plant characteristics correlated with protein content such as energy content. It is significant that hares continue to ingest heavily defended species (e.g. Shepherdia canadensis, B. glandulosa and L. arcticus) when many less defended plants are available to be eaten (e.g. F. altaica, Epilobium latifolium and Anemone parviflora). Our results support the idea that hares are selecting dietary items on the basis of energy content. No single plant species can satisfy all of the hares’ nutritional requirements and the selection patterns may reflect the need to balance many conflicting plant qualities.     

Vulnerability and body size: tetrapods versus fish

The relationship between body size and risk of extinction has been the focus of much recent attention; however, it has only been stated for a few groups inhabiting restricted areas. Based on the IUCN list and other public records, we suggest that the relationship between vulnerability and body size is a trend among all vertebrates, especially tetrapods. In the case of fish, our results show that body size may be subordinate to another factor that we named concealment. Other plausible explanations about this difference could be the human preference for large terrestrial vertebrates and/or the inappropriateness of the current IUCN listing criteria for fish species.     

Spatial variation in sea urchins, fish predators, and bioerosion rates on coral reefs of Belize

Although sea urchins are critical for controlling macroalgae on heavily fished coral reefs, high densities threaten reefs, as urchins are also prodigous bioeroders. This study examined urchin population characteristics, bioerosion rates, their fish predators (Labridae), and potential competitors (Scaridae) on unprotected reefs and a reef within a marine protected area (MPA) in the lagoonal regions off Belize. Urchin density (<1 m⁻²) and bioerosion rates (∼0.2 kg CaCO₃ m⁻² year⁻¹) were lowest and members of the Labridae were the highest (∼20 fish 200 m⁻³) within the MPA, while several unprotected reefs had higher (∼18–40 m⁻²) urchin densities, lower Labridae abundances (1–3 fish 200 m⁻³), and bioerosion rates ranging from ∼0.3–2.6 kg CaCO₃ m⁻² year⁻¹. Urchin abundances were inversely related to Labridae (wrasses and hogfish) densities; however, on reef ridges, low algal cover (∼15%), small urchin size (∼14 mm), and low proportion of organic material in urchin guts suggested food limitation. Both top–down (predation) and bottom–up factors (food limitation) likely contribute to the control of urchins, predominantly Echinometra viridis, off Belize, thereby potentially diminishing the negative impacts of bioerosion activities by urchins.     

The chemosensory responses of young cichlid fish to parents and predators

The chemosensory responses of the fry of the Midas cichlid, Cichlasoma citrinellum (Pisces: Cichlidae), were tested in a Y-maze during their first 11 days of free-swimming. Fry preferred all conspecific females to blank water but did not distinguish between their own mother, another mother or a non-parental, adult female. Fry preferred females to males. Similar results were obtained for males. Fry preferred their siblings and (unrelated) juveniles to blank water. However, while they failed to show a preference between siblings and their mother, they preferred their mother to juveniles. Fry were able to any of three heterospecifics (C. managuense, C. nigrofasciatum and the allopatric Sarotherodon mossambicus). The chemosensory responses demonstrated in the Y-maze are hypothesized to aid the fry in staying near the centre of the guarded territory and away from predators, particularly under murky or nocturnal conditions.     

Vulnerability of Bemisia tabaci immatures to phytoseiid predators: Consequences for oviposition and influence of alternative food

An earlier study showed that two phytoseiid species, Euseius scutalis (Athias‐Henriot) and Typhlodromips swirskii (Athias‐Henriot) (Acari: Phytoseiidae), are capable of suppressing populations of Bemisia tabaci (Gennadius) (Hemiptera: Aleurodidae) on isolated cucumber plants supplied with Typha latifolia L. pollen. However, the predators did not exterminate their prey, and this may be caused by the existence of invulnerable B. tabaci stages. Little is known of the differential vulnerability of the immature B. tabaci stages. Here, we quantified their vulnerability by assessing the rate of predation on each of the immature stages when offered alone at a density high enough to allow for a maximal predation rate. All immature stages of B. tabaci were vulnerable to predation by each of the two predator species. However, the per capita predation rates, the oviposition rates of phytoseiids, as well as the percentage of predators feeding and the percentage ovipositing decreased with increasing stages of B. tabaci. Compared to that of eggs and 1st instars, the vulnerability of 2nd and later B. tabaci instars is an order of magnitude lower. To investigate how the presence of alternative food changes the rates of predation, we added pollen to a diet of 1st instars, one of the most vulnerable instars. This resulted in a decrease in the predation rate of E. scutalis, but not of T. swirskii, while the oviposition rate of both phytoseiid species remained equally high. The decreased predation of the 1st instars probably resulted from E. scutalis switching to pollen feeding.