Impact of copepod grazing on the red-tide flagellate Chattonella antiqua

Although planktonic copepods are major suspension feeders in the sea, the impact of their grazing pressure upon red-tide flagellates has not been fully investigated. In the present study, the grazing of adult females of several copepod species is examined using three food types: viz. natural suspended particles, natural suspended particles mixed with cultured Chattonella antiqua, and cultured C. antiqua. The functional response on C. antiqua was investigated for five species of copepods (Acartia erythraea, Calanus sinicus, Centropages yamadai, Paracalanus parvus and Pseudodiaptomus marinus). Ingestion rates increased linearly with increasing cell concentrations until a maximum level was reached, beyond which the rates were constant. This cell concentration was higher for larger copepods. The weight-specific maximum ingestion rates were higher in the small species. In general, copepods tended to feed selectively on larger particles when feeding on natural particles. This tendency was strongest in a simulated red-tide environment. Thus, it can be surmised that copepods may selectively graze on C. antiqua during the outbreak of a red tide. Grazing pressure by the natural copepod community in Harima Nada, the Inland Sea of Japan, was calculated by integration of the laboratory determined feeding rates and field measurements of zooplankton biomass. The daily removal rate was 3.4 to 30.8% (mean: 12.3%) of C. antiqua biomass at 20 cells ml^-1 and decreased to 0.6–4.3% (mean: 1.8%) at 500 cells ml^-1. Therefore, the grazing pressure by the copepod community is important at the initial stage of the red tide.     

Fate of domoic acid ingested by the copepod <Emphasis Type="Italic">Acartia clausi</Emphasis>

Two important issues in the studies of harmful algae include ecological role of the toxic compounds and their fate through the food web. The aims of this study were to determine whether the production of domoic acid is a strategy evolved to avoid predation and the role of copepods in the fate of this toxic compound through the food web. The copepod Acartia clausi was fed with single and mixed cultures of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia delicatissima. Ingestion rate as a function of diatom abundance was the same for the toxic and non-toxic Pseudo-nitzschia species, indicating no selective feeding behaviour against P. multiseries. The toxins ingested by the copepods did not affect mortality, feeding behaviour, egg production and egg hatching of the copepods. Copepods assimilated the 4.8% of the total domoic acid ingested. Although the amount of toxins daily detoxificated by the copepods was 63.6%, the copepods accumulated domoic acid in their tissues. We conclude that domoic acid is not toxic for copepods and, probably for this reason, this toxin does not act as feeding deterrent for copepods. However, even though the production of domoic acid has apparently not evolved to deter predation, copepods may play an important role on the fate of this toxic compound through the marine food web.     

Strain-related physiological and behavioral effects of <Emphasis Type="Italic">Skeletonema marinoi</Emphasis> on three common planktonic copepods

Three strains of the chain-forming diatom Skeletonema marinoi, differing in their production of polyunsaturated aldehydes (PUA) and nutritional food components, were used in experiments on feeding, egg production, hatching success, pellet production, and behavior of three common planktonic copepods: Acartia tonsa, Pseudocalanus elongatus, and Temora longicornis. The three different diatom strains (9B, 1G, and 7J) induced widely different effects on Acartia tonsa physiology, and the 9B strain induced different effects for the three copepods. In contrast, different strains induced no or small alterations in the distribution, swimming behavior, and turning frequency of the copepods. 22:6(n-3) fatty acid (DHA) and sterol content of the diet typically showed a positive effect on either egg production (A. tonsa) or hatching success (P. elongatus), while other measured compounds (PUA, other long-chain polyunsaturated fatty acids) of the algae had no obvious effects. Our results demonstrate that differences between strains of a given diatom species can generate effects on copepod physiology, which are as large as those induced by different algae species or groups. This emphasizes the need to identify the specific characteristics of local diatoms together with the interacting effects of different mineral, biochemical, and toxic compounds and their potential implications on different copepod species.     

Feeding four species of pelagic copepods under experimental conditions

Different qualitative and quantitative aspects of feeding with varied compositions of diets have been studied in 4 species of pelagic copepods: Calanus helgolandicus, Centropages typicus, Temora stylifera and Acartia clausi. By feeding copepods different algal concentrations, it was shown that when food concentration increases grazing rate decreases; the ingestion rate remains fairly constant in the lower range of concentrations, but then increases, reaching a plateau at higher algal concentrations. There is a significant correlation between daily food intake and fecal pellet production. On a pluri-algal diet, selective grazing is observed: larger phytoplankton cells are more efficiently removed than smaller ones. Using Artemia nauplii, it is shown that the copepods studied are also able to eatch and ingest animal prey. Increased daily food intake affects respiration and oviposition. Metabolic requirements, gross growth-efficiency, and food assimilation have been ealculated in Calanus helgolandicus, Centropages typicus and T. stylifera for a large range of algal concentrations.     

In situ feeding rhythms of herbivorous copepods,and the effect of starvation

In situ diel variations in gut pigment contents of neritic (Acartia omorii andPseudocalanus minutus) and oceanic copepods (Calanus plumchrus andC. cristatus) were analyzed.A. omorii andP. minutus were sampled in Onagawa Bay on the east coast of Japan in May and August 1987, andC. plumchrus andC. cristatus were sampled in the Bering Sea in June 1986. Gut pigments were generally high at night, and bimodal feeding rhythms were observed in all species. The first peak of gut pigments occurred between sunset and midnight and was followed by a midnight decrease in gut pigment levels, resulting in eventual evacuation of the gut. The second peak was observed a few hours after sunrise. Incubation experiments indicated that ingestion rates of starved copepods were higher than those of acclimated copepods. This phenomenon was most notable at high food concentrations. Gut pigments of starved copepods rapidly increased after exposure to high concentrations of culturedThalassiosira decipiens. These findings suggest that in situ feeding behavior of herbivorous copepods includes periods of cessation or reduction in feeding during the night, and consequently, feeding activity is periodically enhanced with starvation. Starvation enhanced feeding behavior is most obvious in the large oceanic species,C. plumchrus andC. cristatus and is not distinct in small coastal species such asA. omorii.     

Measurement of copepod predation on nauplii using qPCR of the cytochrome oxidase I gene

A method to directly measure predation rates by older stage copepods upon copepod nauplii using species-specific primers for the mitochondrial cytochrome oxidase subunit one gene (mtCOI) and real-time quantitative PCR (qPCR) was developed. The general approach is to determine the mtCOI gene copy number of an individual prey organism and the copy number of the same gene in the stomachs of predatory copepods collected in the field. From the knowledge of DNA disappearance rates in the stomachs, ingestion rates can be calculated. In October 2006, laboratory experiments were carried out with Acartia tonsa N1 and N2 as prey and adult female Centropages typicus as predator. The copepods were collected in Narragansett Bay, USA. A. tonsa mtCOI copy numbers copepod⁻¹ were determined for stages N1–C1 and for adults. A. tonsa DNA was detectable in the guts of the predators for as long as 3 h. Exponential rates of decline in prey DNA from the stomachs of the predators are similar to those measured for gut pigments. Because of the very small amount of DNA in an individual N1 or N2 nauplius, procedures were developed to maximize the quantitative extraction and recovery of DNA and to increase the sensitivity of the method. Two quite divergent haplotypes of A. tonsa were found in Narragansett Bay, which required separate qPCR primers; one was present in summer (July) and the other in fall and winter (October and February). With modification, the methods in this study can likely be applied to a range of predator–prey systems.     

Measuring RNA:DNA ratios in individual <Emphasis Type="Italic">Acartia tonsa</Emphasis> (Copepoda)

Acartia tonsa Dana is a dominant copepod in coastal waters and is therefore an important link in the food web between microplankton and higher trophic levels. RNA:DNA ratios have been used to describe growth and nutritional condition of field-collected copepods and to show strong correlation between RNA:DNA ratios and group egg production (EP). A method was developed using a sensitive, nucleic acid-specific fluorescent dye, and automated microplate fluorometer to measure DNA, RNA, and the RNA:DNA ratio of individual A. tonsa. DNA, RNA, and RNA:DNA ratios and EP were all significantly higher in copepods fed Thalassiosira sp. compared to starved copepods. There was a general trend toward an increase in RNA:DNA ratios with increase in EP, but due to the high degree of variation in both RNA:DNA ratios and EP among individual copepods there was no significant correlation between RNA:DNA ratios and EP. Significant differences in RNA:DNA ratios between fed (7.2) and starved (3.3) copepods were found after 2 days. This assay may be applied to other species of copepods sampled in the field to provide an index of the health of planktonic food webs.     

Effects of water motion and prey behavior on zooplankton capture by two coral reef fishes

Water motion is an important factor affecting planktivory on coral reefs. The feeding behavior of two species of tube-dwelling coral reef fish (Chaenopsidae) was studied in still and turbulent water. One species of blenny, Acanthemblemaria spinosa , lives in holes higher above the reef surface and feeds mainly on calanoid copepods, while a second, A. aspera , lives closer to the reef surface, feeds mainly on harpacticoid copepods, and is exposed to less water motion than the first. In the laboratory, these two blenny species were video recorded attacking a calanoid copepod ( Acartia tonsa, evasive prey) and an anostracan branchiopod (nauplii of Artemia sp., passive prey). Whereas A. spinosa attacked with the same vigor in still and turbulent water, A. aspera modulated its attack with a more deliberate strike under still conditions than turbulent conditions. For both fish species combined, mean capture success when feeding on Artemia sp. was 100% in still water and dropped to 78% in turbulent water. In contrast, when feeding on Acartia tonsa, mean capture success was 21% in still water and rose to 56% in turbulent water. We hypothesize that, although turbulence reduces capture success by adding erratic movement to Artemia sp. (passive prey), it increases capture success of Acartia tonsa (evasive prey) by interfering with the hydrodynamic sensing of the approaching predator. These opposite effects of water motion increase the complexity of the predator-prey relationship as water motion varies spatially and temporally on structurally complex coral reefs. Some observations were consistent with A. aspera living in a lower energy benthic boundary layer as compared with A. spinosa: slower initial approach to prey, attack speeds modulated according to water velocity, and lower proportion of approaches that result in strikes in turbulent water.Communicated by P.W. Sammarco, Chauvin     

Effects of low oxygen concentrations on the hatching and viability of eggs of marine calanoid copepods

Hatching of the eggs of four species of copepods, Acartia tonsa, Labidocera aestiva, Tortanus discaudatus, and Centropages hamatus was suppressed at oxygen concentrations less than 0.02 ml O₂/l. When such eggs were subsequently exposed to normal oxygen concentrations, hatching varied among the species, indicating variability in the capacity of eggs to survive exposure to low oxygen. Incubation of eggs at low oxygen concentrations resulted in an increase in the duration of embryonic development. Experiments were conducted in closed systems and oxygen concentration was determined by thermal conductivity using gas chromatography.     

Trophic implications of cross-shelf copepod distributions in the Southeastern Bering Sea

Spring distributions of some numerically dominant copepods reflect associations with two distinct water masses separated along the 80- to 100-m isobaths. Seaward of this middle shelf front, the oceanic Bering Sea hosts populations of Calanus cristatus, C. plumchrus, and Eucalanus bungii bungii; Metridia pacifica, Oithona similis, and Pseudocalanus spp. are also present. The large oceanic species are much less abundant in waters shallower than 80 m where the community is seasonally dominated by smaller copepods, O. similis, Acartia longiremis, and Pseudocalanus spp. Experimental and field-derived estimates of carbon ingestion indicate that the oceanic/outer shelf copepods can occasionally graze the equivalent of the daily plant production and probably routinely remove 20–30% of the primary productivity. Conversely, stocks of middle shelf copepods rarely ingest more than 5% of the plant carbon productivity. During 45 d between mid April to late May, 1979, approximately three times more organic matter was ingested m^-2 by the outer shelf/oceanic copepod community than by middle shelf species. This imbalance in cross-shelf grazing permits middle shelf phytoplankton stocks to grow rapidly to bloom proportions, and to sink ungrazed to the seabed. Over the outer shelf and particularly along the shelf break, a much closer coupling to phytoplankton supports a large biomass of oceanic grazers. Here, copepod stocks approaching 45 g dry wt m^-2 occur in late spring as a narrow band at the shelf break.Supported by National Science Foundation Grant DPP 76-23340Contribution no. 485, Institute of Marine Science, University of Alaska, Fairbanks     

Orientation affects the sensitivity of Acartia tonsa to fluid mechanical signals

Nearly all organisms show directional bias in sensitivity to environmental signals. In this study, the behavioral sensitivity of a common estuarine copepod, Acartia tonsa, varies significantly with respect to their orientation to a well-characterized fluid mechanical signal. Maximum sensitivity occurs at an angle of 25°–30° and lowest sensitivity occurs at angles of 60°–90° relative to the source. These results support the hypothesis that copepods are not uniformly sensitive to fluid signals and show directional bias in mechanosensitivity. The data also show that large copepods initiate their escape reaction further from the source than small copepods. There is, however, an uncharacteristically large increase in sensitivity at the transition between the nauplii and C1 stage despite being similar in size. This suggests that the mechanosensory system of the naupliar stages is less sensitive to fluid signals and helps to explain the higher predation rates experienced by nauplii.     

Survival and sex ratios of the intertidal copepod,Tigriopus californicus,following ultraviolet-B (290–320 nm) radiation exposure

The marine harpacticoid copepod, Tigriopus californicus (Baker), is a successful colonizer of supralittoral splash pools from Torch Bay, Alaska, to Baja California, Mexico. As these pools are subject to abundant amounts of direct solar radiation, it was of interest to determine the sensitivity of T. californicus to ultraviolet-B (UV-B, 290 to 320 nm) radiation. During 1980, copepods were raised under diurnal conditions in the laboratory and fed a mixture of unicellular algae and bacteria. Larval and adult stages were irradiated for 0 to 26 h on a rotating turntable under enhanced ultraviolet radiation. Following irradiation, the copepods were maintained in the culture area and checked daily for survival. All life stages of T. californicus tolerated enhanced UV-B radiation irrespective of exposure period; in contrast, survival of an irradiated planktonic copepod, Acartia clausii (Giesbrecht), was significantly lower. Additionally, there appeared to be asex ratio shift in adults that developed from the youngest naupliar stages (N₁/N₂) of T. californicus that were irradiated. Extraction and tentative identification of the pigment(s) responsible for the bright orange color of the carapace of T. californicus were performed. These pigments may function to absorb UV radiation and protect internal structures from photochemically induced damage.     

Subitaneous, diapause, and delayed-hatching eggs of planktonic copepods from the northern Gulf of Mexico: morphology and hatching success

Experiments were conducted to examine the morphology and hatching success of eggs, either spawned by freshly caught planktonic copepods or recovered from bottom sediments in the northern Gulf of Mexico. Collections were made between August 1992 and September 1995. Eggs of nine species were described and these differed in their diameter, color and surface attributes. Three types of eggs were distinguished: subitaneous, diapause, and delayed-hatching. Three species, Labidocera aestiva Wheeler, Acartia tonsa Dana, and Centropages velificatus (Oliveira) produced only subitaneous eggs. Hatching success varied greatly among these species. Two species, Labidocera mirabilis Fleminger and Centropages hamatus (Lilljeborg) produced diapause eggs and subitaneous eggs. The length of the refractory phase of the diapause eggs differed greatly both within and between these two species. A third type of dormant egg, delayed-hatching, was recognized in Labidocera scotti Giesbrecht and Pontella meadi Wheeler. The existence of delayed-hatching eggs may be an adaptive response of subtropical species to less seasonal fluctuation. Based upon morphological characteristics of the eggs and rearing of nauplii to an identifiable stage, benthic dormant eggs of eight species of calanoid copepods were also identified. Received: 9 September 1996 / Accepted: 1 October 1996     

Accumulation of paralytic shellfish poisoning toxins in planktonic copepods during a bloom of the toxic dinoflagellate<Emphasis Type="Italic"> Alexandrium tamarense</Emphasis> in Hiroshima Bay,western Japan

Concentrations of paralytic shellfish poisoning (PSP) toxins in toxic dinoflagellate cells and in marine planktonic copepods were monitored during the bloom of Alexandrium tamarense in Hiroshima Bay, western Japan. Concentration of the toxins retained by copepods was a function of the ambient toxin concentration, i.e. the product of A. tamarense cell density and cellular toxicity. The toxin concentration in copepods increased with the increase of toxicants in the seawater then leveled off, but decreased significantly at higher concentrations. In the field, the maximum toxin concentration was 1.2 pmol ind^-1, whereas in the laboratory, the copepod Acartia omorii accumulated a much higher concentration of PSP toxins (24 pmol ind^-1). Feeding avoidance against Alexandrium tamarense and a shift to alternative food sources such as diatoms in the field might keep their toxin levels lower than their potentially maximum level. The copepod toxin levels in the field were not so high as to cause an instantaneous lethal effect on their predator fishes but may reach possibly lethal levels after a few days' continuous feeding. Overall toxin retention by copepods after 12 h feeding and 2 h starvation was only 2.5% of total ingested toxins, which suggested that a significant amount of toxins was released into the seawater. Measurements of toxin reduction and gut evacuation suggested that the toxins were removed through both fecal evacuation and metabolism (e.g. excretion, decomposition and transformation). The results, as a whole, imply that copepods can be a link for PSP toxin flux in both pelagic and benthic food webs and can also be a sink for toxins by metabolizing and removing them from the environment.Communicated by T. Ikeda, Hakodate     

Influence of cultivation and food concentration on body length of calanoid copepods

The cephalothorax length of the marine pelagic Copepoda Acartia clausi Giesbrecht, Temora longicornis (Müller), Centropages hamatus (Lilljeborg) and Pseudocalanus sp. was monitored at 15°C during prolonged cultivation through up to 55 filial generations and at different concentrations of food. The length of T. longicornis decreased considerably during the first 15 generations and remained rather constant thereafter. In the other species, body length increased slightly or remained almost constant. Genetic changes are probably involved. Food concentration influenced body size of all species, particularly C. hamatus, in which 80% of the natural size range may be explained by differences in food concentration. The idea that temperature is a dominant factor in determining the length of copepods should be reconsidered.     

The progressive changes of the copepod community from the eastern Adriatic coast caused by eutrophication

In 1976–1985 period, some changes have been found during long‐term monitoring of physical, chemical and biological parameters in front of the largest harbours of the eastern Adriatic coast. For that reason, the control has been continued in 1985–1988 period.

This paper presents some recent results about copepods‐dominant mesozooplankton group—as they respond very quickly (both by composition and biomass) to the changes of the environment they inhabit. Besides the increased copepod density, further increasing of maximal values of Acartia clausi was found at the whole investigated area in 1987 and 1988, caused by progressive eutrophication of the eastern Adriatic coastal waters.     

Osmoacclimation in Enteromorpha intestinalis: long-term effects of osmotic stress on organic solute accumulation

The fate of the protease trypsin in intestines of individual herring larvae Clupea harengus L. was studied following digestion of the copepod Acartia tonsa. Trypsin was retained in the intestine during two consecutive pulses of feeding and defaecation of copepods. Quantification of herring trypsin in digested, defaecated copepods showed that ca. 1% of larval intestinal enzyme was defaecated along with 1 to 3 copepods. Following ingestion of a single meal, the level of intestinal trypsin post-ingestion declined to pre-ingestion levels within 1 to 2 d of starvation. All enzyme data thus indicated that trypsin, released in response to ingestion of a meal, was retained. In addition, analysis of fed subgroups of starved larvae clearly indicated that release of trypsin from the pancreas stopped after 6 to 8 d of starvation. As the fish still contained substantial amounts of trypsinogen, the underlying cause might be defective release mechanisms. Daily secretion of trypsin and processes responsible for enzyme retention in the gut are discussed. Assimilation efficiency in herring larvae was estimated for copepodite prey. Average carbon assimilation was 90%.     

Calanoid copepod eggs in sea-bottom muds

We have found numerous eggs of neritic copepods in sea-bottom sediments. Eggs of 6 species of calanoid copepods: Tortanus forcipatus Giesbrecht, Calanopia thompsoni A. Scott, Acartia erythraea Giesbrecht, A. clausi Giesbrecht, Centropages abdominalis Sato and C. yamadai Mori are described and illustrated. The possibility that these eggs “rest” in the sediments, and their biological significance, are briefly discussed.     

Vulnerability of the copepod Acartia tonsa to predation by the scyphomedusa Chrysaora quinquecirrha : effect of prey size and behavior

Although scyphomedusae have received increased attention in recent years as important predators in coastal and estuarine environments, the factors affecting zooplankton prey vulnerability to these jellyfish remain poorly understood. Current models predicting feeding patterns of cruising entangling predators, such as Chrysaora quinquecirrha (Desor, 1948), fail to account for the selection of fast-escaping prey such as copepods. Nevertheless, our analysis of gastric contents of field-collected medusae showed that this scyphomedusa fed selectively on the calanoid copepod Acartia tonsa (Dana, 1846) and preferentially ingested adult over copepodite stages. We measured feeding rates in a planktonkreisel while simultaneously videotaping predator–prey interactions. C. quinquecirrha consumed adult A. tonsa ten times faster than copepodites. Differences in prey behavior, in the form of predator–prey encounter rates or post-encounter escape responses, could not account for the elevated feeding rates on adults. Prey size, however, had a dramatic impact on the vulnerability of copepods. In experiments using heat-killed prey, feeding rates on adults (1.5 times longer than copepodites) were 11 times higher than on copepodites. In comparison, medusae ingested heat-killed prey at only two to three times the rate of live prey. These results suggest that during scyphomedusan–copepod interactions, prey escape ability is important, but ultimately small size is a more effective refuge from predation. Received: 26 September 1997 / Accepted: 20 May 1998     

Variability in the gut contents of individual A cartia tonsa from waters off Southern California

The gut contents of 169 individual Acartia tonsa from Los Angeles Harbor, California, USA, were measured during a 24 h period (16–17 June 1986) by gut pigment (fluorescence) and microscopic analyses. Individual gut-pigment levels varied 10-fold or more within sampling intervals. Some copepods with moderate (0.2 to 0.5 ng) to high (>0.5 ng) gut-pigment levels were present in samples from both day and night collections. While the percentage of copepods containing>0.5 ng pigment was about the same during the day (8%) as at night (10%), the percentage of copepods with 0.2 to 0.5 ng pigment rose from 17% during the day to 55% at night. Significant differences between pigment levels in copepods collected before and after evening twilight were suggestive of a nocturnal feeding habit regardless of intense individual variability in gut-pigment content. Food in the gut was distributed in parcels, indicative of intermittent feeding that potentially contributes to individual variability. Feeding was not synchronized during most of the day and night, but synchrony increased at evening and morning twilights. Although synchrony declined after evening twilight, individual gut-pigment contents were relatively elevated in most of the nighttime samples. Thus, active feeding seems neither to require nor to imply synchrony.