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.     

Reproductive toxicity of metals in calanoid copepods

This study investigated the effect of exposure route on metal accumulation, tissue distribution, and toxicity in the marine copepods Acartia hudsonica and A. tonsa. Sublethal toxicity was measured as decreases in egg production, hatching rate, ovarian development and protein (yolk) content of the egg. When algal food, exposed to Hg at 1 nM or Cd at 5 nM resulting in cells containing 34 and 64 nmol metal g^-1 dry weight, respectively, was ingested over a 4-h period by copepods, the total copepod body burden increased nine-fold for Hg and two-fold for Cd over background concentrations, and egg production decreased by 50%. Sublethal concentrations of metals were >2 orders of magnitude lower than LC₅₀ concentrations. Hatching rate, ovarian development and egg protein content all decreased following trophic exposure to metals, implying that the process of yolk accumulation (vitellogenesis) was affected. Exposure to dissolved Cd had no effect, but dissolved Hg at concentrations as low as 0.25 nM did affect egg production. Different toxic effects following different exposure routes were related to different metal distributions in the copepods: exposure to dissolved metal resulted in metal deposition in the exoskeleton, whereas exposure to dietary metal resulted in metal deposition in internal tissues. These findings indicate that enrichment of metal concentrations in internal tissues, which occurs primarily after exposure to dietary metal, affects vitellogenesis. The reproduction rate decreases by about 75% at metal concentrations only moderately higher than levels in coastal waters. Toxicity tests involving aquatic animals need to consider effects following uptake by different pathways, including the trophic transfer of metals.     

Morphogenesis of opal teeth in calanoid copepods

Opal teeth of calanoid copepods develop early in the premolt phase of the molt cycle. They form in the apolysis space beneath the old tooth row on the mandibular gnathobase. We examined stages of tooth formation inNeocalanus spp. andCalanus pacificus. Apolysis occurs early in the distal gnathobase, then several epidermal cell types participate sequentially in formation of new teeth. Fibrous molds in the shapes of the new teeth are extruded onto the epidermal surface, then additional materials, probably proteinaceous, are secreted into them. Tooth molds next are linked to a gland in the proximal part of the gnathobase by ducts of an unusual type, lamellar-walled ducts. Silicification follows, apparently using highly osmiophilic material supplied by the proximal gland. Opal is laid down at the outer periphery of the mold then thickens toward the attachment of the mold to newly formed chitin at its base. During apolysis the epidermal cells move proximally without breaking ducts that connect small dermal glands with pores in the sides of the opal teeth. The molds for the new teeth form surrounding these ducts, and new pores result. The glands are like the ciliary exocrine glands seen in other Crustacea, with the duct deriving from fusion of the axonemes of a cilium. Presumably the glands secrete a substance into food newly broken by the teeth. This could be a toxin or a digestive enzyme.     

Feeding of calanoid copepods in relation to Phaeocystis pouchetii blooms in the German Wadden Sea area off Sylt

Surface sediments from the Svartnes basin (195 m deep) in Balsfjorden, northern Norway (ca. 70°N), were partially characterized to assess the nature and origin of the organic material present and its potential nutritive value for sediment-ingesting animals. Seasonal analyses were carried out on material collected between May 1979 and August 1980 for total organic matter, organic C and N, acid-extractable amino acids and lipids extractable with chloroform:methanol. Little or no seasonal variation was seen in any of the parameters analysed. The mean apparent organic content was 9.3% of sediment dry weight, the organic C content was 2.38%, the organic N content was 0.26% and the C:N ratio was 9.1:1. Acid hydrolysis of sediment yielded 575 mg of amino acids and 41 mg of NH₃ per 100 g sediment dry weight, the composition of the amino acids being similar to that of nutritionally highquality animal or microbial protein. Glucoseamine was not detected in acid hydrolysates of sediment, consistent with the absence of chitin. Chloroform:methanol extraction yielded 133 mg of material per 100 g sediment dry weight, 62% of which was accounted for by saponifiable lipids (fatty acids) and non-saponifiable lipids present in approximately equal amounts. Fatty alcohols accounted for 30% of the non-saponifiable lipids and phytol accounted for 40% of the fatty alcohols. Small amounts of very long-chain fatty alcohols characteristic of terrestrial plants were present, but long-chain monounsaturated fatty alcohols characteristic of marine zooplankton were essentially absent. Very small quantities of long-chain ketones characteristic of marine coccolithophores were detected. The major fatty acids present in sediments were 16:0, 14:0, 16:1 (n-7) and 18:1 (n-9), and 11% of the total fatty acids were comprised of a mixture of odd-numbered straight-chain and branched-chain moieties characteristic of micro-organisms. The data point to small amounts of material characteristic of marine and terrestrial photosynthetic organisms being present in sediments at any given time, whereas material characteristic of marine zooplankton is not present. The presence of material characteristic of micro-organisms is consistent with conversion of sedimenting material into a pool of sediment micro-organisms. Although the biological availability to sediment-ingesting organisms of the esterified fatty acids and the acid-extractable amino acids in sediments remains to be assessed, the maximum amounts available are equivalent to approximately 60 mg of polar lipid and 575 mg of protein per 100 g sediment dry weight. These amounts are small in relation to the production rates in the photic zone of the fjord, implying that the bulk of the energy flow in Balsfjorden occurs in its relatively short pelagic food chains.     

Reproductive biology of deep-water calanoid copepods from the Arctic Ocean

Reproductive modes and egg production were studied in 15 species of meso- and bathypelagic copepods from nine Calanoida families in the Arctic Ocean. During shipboard incubation, females of seven species released eggs freely into the water and females of three species produced membrane-bound egg sacs. One species, Aetideopsis rostrata, produced a mass of eggs looking like an egg sac, but the “sac” lacked a membrane and disintegrated within 2 h. Females of four additional species were encountered with membrane-bound egg sacs in the preserved samples. In most families, only one reproductive mode, either egg-carrying (the Euchaetidae, Augaptilidae), or broadcast spawning (the Heterorhabdidae, Spinocalanidae, Scolecitrichidae, Tharybidae, Bathypontiidae) was observed. In contrast, different genera of the Aetideidae family demonstrated different reproductive modes, with broadcast spawning predominant in the benthopelagic species, and both broadcast spawning and egg-brooding in the planktonic species. Clutch size and egg diameter varied widely between species in both broadcast spawners and egg-brooders. In broadcast spawners, the clutch size varied from 1 to 95 eggs female⁻¹, while the average egg diameter ranged from 152 to 440 μm. The clutch size for egg brooders varied between 3 and 82, while average egg diameter varied from 258 to 732 μm. Deep-water broadcast spawners produced much larger eggs compared to surface-dwelling broadcast spawning species. This larger egg size may result in a reduction, or elimination, of feeding during naupliar stages, thereby improving the survival potential of deep-water species.     

Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern Britain

Eggs of the calanoid copepodsLabidocera wollastoni (Lubbock) andCentropages hamatus (Lilljeborg) and others, which could not be reliably assigned to species, were identified from sediment samples taken during three cruises in December 1984, January 1986, and February 1987 in the southern North Sea, the English Channel, the Irish Sea and the Celtic Sea. Eggs were most abundant in sediment samples taken between 20 and 80 m depth, with bottom stress less than 10 dyn cm^–2, and near to the positions of tidal fronts. It is suggested that sedimentation, resuspension and sediment transport contribute to the causes of these distributions, which have been found to be consistent with the distributions of species which are known to produce diapause eggs as an overwintering strategy. Nauplii ofL. wollastoni, C. hamatus, C. typicus (Krøyer)Temora longicornis (Müller) andAcartia sp. hatched from incubated sediment samples. The last noted hatchings ofL. wollastoni, Centropages spp. andT. longicornis all occurred more than 1 yr after the start of the incubation experiments.     

Grazing in juvenile stages of some estuarine calanoid copepods

The grazing of juvenile Eurytemora affinis, Acartia tonsa and A. clausi from the Chesapeake Bay (USA) was investigated using natural particle distributions and freshly caught copepods, live-sorted into stages. Data were analyzed in 110 size channels using an electronic particle counter, and filtering rates (FR) were estimated based on total particle removal (mean FR), and that for each size channel (giving maximum FR). Mean and maximum filtering rates increased from NVI (Nauplius Stage VI) through CVI (Copepodid Stage VI). Both rates plotted against weight satisfied a log fit best for A. tonsa, and a linear fit best for E. affinis. Results for A. tonsa were quite variable, apparently due to differences in temperature between experiments. Particle selection was investigated from the shape of the filtering rate curve over particle size. We define selective feeding by a FR curve which is higher in some size categories, and non-selective feeding by a flat FR curve. The general pattern was one of selective feeding in all copepodid stages of the three calanoid copepods investigated. E. affinis tended to track biomass peaks while Acartia spp.'s feeding was more variable, including feeding in size ranges of greatest particle concentration, on larger particles, and in other size categories as well. Experiments with nauplii tended to yield flat FR curves, and it may be that selective grazing appears with, or is greatly accentuated by, metamorphosis from NVI to CI (Copepodid Stage I).University of Maryland, Center for Environmental and Estuarine Studies Contribution No. 762.     

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     

Spatial variability in lipid composition of calanoid copepods from Fram Strait,the Arctic

The calanoid copepods Calanus hyperboreus and C. finmarchicus were investigated in view of their lipid and wax ester content and their fatty acid and alcohol composition. Analyses were performed in females and copepodid stages V and IV from the Fram Strait region between Greenland and Spitsbergen in 1984. This region offers different food conditions like diatom blooms in the North East Water Polynya, food shortage in areas with very close ice cover, high phytoplankton biomass in the marginal ice zone and lower biomass in the open Atlantic water. Lipids contained generally more than 70% wax esters. Highest levels were found in C. hyperboreus with more than 90%. This percentage was not very variable, in spite of large differences in dry weight and lipid content. Copepods with particularly high weight and lipid content were found in the North East Water Polynya. The lightest individuals were found under the pack ice. Lipid proportions per unit dry weight were higher in C. hyperboreus than in C. finmarchicus, whose lowest values were found in the open Atlantic water. Spatial variability in fatty acid composition was much higher than in alcohol composition. The principle alcohols, 20:1 and 22:1, generally accounting for more than 80% of total alcohols. In the North East Water Polynya, the predominant monounsaturated fatty acid was 16:1, while under the ice 20:1 and 22:1 dominated. In the marginal ice zone and in the open water, the 18:4 acid reached percentages up to 30% of total fatty acids. These changes were related to the different food conditions. C. hyperboreus appears to be best adapted to the cold water and unfavourable conditions of polar regions because of its high lipid and wax ester store with long-chain wax esters of high calorific value.     

Distribution,structure and importance of the cephalic dorsal hump,a new sensory organ in calanoid copepods

The occurrence, external morphology and internal ultrastructure of a cephalic integumental organ in calanoid copepods were studied, using the specimens from the Pacific, Indian and Atlantic Oceans. This organ is located on the dorsoanterior surface of the cephalosome, and a name, cephalic dorsal hump (CDH) is proposed. Externally, it usually has two pores, anterior and apical, a dorsal plate, and a thin cuticle along the sides. CDH is found only in the male of Calanidae, Megacalanidae, Mecynoceridae and Paracalanidae, and showed some variation between species or species groups both in size and shape. Transmission electron microscopy (TEM) on the specimens from Sagami Bay, Central Japan, revealed that the CDH of Paracalanus parvus and Calanus sinicus consists of two dermal glands and a receptor, which is assumed to be chemosensory. A comparison of the distributions of CDH and prehensile fifth legs of male calanoid copepods suggests that it plays an important role in mate recognition.     

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.     

Zooplankton responses to hypoxia: behavioral patterns and survival of three species of calanoid copepods

Seasonally recurrent and persistent hypoxic events in semi-enclosed coastal waters are characterized by bottom-water dissolved oxygen (d.o.) concentrations of < 2.0 ml l⁻¹. Shifts in the distribution patterns of zooplankters in association with these events have been documented, but the mechanisms responsible for these shifts have not been investigated. This study assessed interspecific differences in responses to hypoxia by several species of calanoid copepods common off Turkey Point, Florida, USA: Labidocera aestiva (Wheeler) (a summer/fall species), Acartia tonsa (Dana) (a ubiquitous year-round species), and Centropages hamatus (Lilljeborg) (a winter/spring species). Under conditions of moderate to severe hypoxia 24-h survival experiments were conducted for adults and nauplii of these species from August 1994 to October 1995. Experiments on adults used a flow-through system to maintain constant d.o. concentrations. Adults of A. tonsa showed no decline in survival with d.o. as low as 1.0 ml l⁻¹, sharp declines in survival at d.o. = 0.9 to 0.6 ml l⁻¹, and 100% mortality with d.o. = 0.5 ml l⁻¹. Adults of L. aestiva and C. hamatus were more sensitive to oxygen depletion: both species experienced significant decreases in survival for d.o. = 1.0 ml l⁻¹. Nauplii of L. aestiva and A. tonsa showed no significant mortality with d.o. = 1.1 to 1.5 ml␣l⁻¹ and d.o. = 0.24 to 0.5 ml l⁻¹, respectively. In addition, experiments investigating behavioral avoidance of moderate to severe hypoxia were carried out for adults of all three species. None of the three species effectively avoided either severely hypoxic (d.o. < 0.5 ml l⁻¹) or moderately hypoxic (d.o. ≈ 1.0 ml l⁻¹) bottom layers in stratified columns. These results suggest that in␣nearshore areas where development of zones of d.o. < 1.0 ml l⁻¹ may be sudden, widespread, or unpredictable, patterns of reduced copepod abundance in bottom waters may be due primarily to mortality rather than avoidance. Received: 31 August 1996 / Accepted: 24 September 1996     

Characterizing dietary variability and trophic positions of coastal calanoid copepods: insight from stable isotopes and fatty acids

The spring zooplankton community in the Strait of Georgia (British Columbia, Canada) is characterized by the presence of several calanoid copepod species which collectively make up ~90% of the mezozooplankton biomass. Here, we investigate interspecific, interannual, and geographic variability in the diets and trophic positions of these copepods using a combination of fatty acids and stable isotopes. To characterize geographic variability in diet, we compare our findings from the Strait of Georgia with similar data from Ocean Station P in the subarctic northeast Pacific. Both fatty acid and stable isotope signatures indicate the existence of three trophic levels, even within the limited size range of these copepods: Neocalanus plumchrus and Calanus marshallae are primarily omnivorous, while Euchaeta elongata is carnivorous and Eucalanus bungii is herbivorous. Fatty acid markers of trophic position (e.g., DHA/EPA, 18:1n-9/18:1n-7) correlate significantly with δ¹⁵N, while markers indicating the proportion of diatoms to flagellates in the diet (e.g., 16PUFA/18PUFA and DHA/EPA) correlate significantly with δ¹³C, after the effect of lipid concentration on δ¹³C is accounted for. Despite the general correlation between stable isotopes and fatty acids, the former are not sensitive enough to capture the range of interannual variability observed in the latter, and can only capture substantial shifts in the diet over geographic scales. However, regardless of variability in food quality, the relative trophic positions of these copepods do not change significantly either spatially or temporally.     

Overwintering strategies of dominant calanoid copepods in the German Bight, southern North Sea

Abundance, stage composition and reproductive parameters (egg production, egg viability, proportion of spawning females) of the four copepod species Acartia clausi, Centropages hamatus, C. typicus and Temora longicornis were measured at the long term sampling station Helgoland Roads (German Bight, southern North Sea) from September 2003 to May 2004 to study their overwintering strategies. A. clausi was overwintering as females with arrested reproduction from November to January. T. longicornis, which is known to produce resting eggs in the North Sea, had a pelagic population with all developmental stages present during winter and reproductive rates closely related to food concentrations. Although their females produced eggs in response to ambient food conditions, both C. hamatus and C. typicus were rare in the pelagic. The C. hamatus population returned in May, probably from resting eggs, whereas C. typicus depended on advection. The Centropages species seemed to be less adapted to pelagic life in winter than A. clausi and T. longicornis. Sporadic occurrence of large numbers of nauplii and young copepodids of A. clausi and Centropages spp. pointed to different overwintering strategies or more successful survival in adjacent regions and advection of them into the waters around Helgoland island. While A. clausi was decoupled from environmental conditions in late autumn and winter, the other species were able to respond to variations in the food environment. Thus, egg production of T. longicornis increased during an unusual autumn diatom bloom.     

Biosynthesis of trimethylamine oxide in calanoid copepods. seasonal changes in trimethylamine monooxygenase activity

Live copepods, Calanus finmarchicus (Gunnerus) and C. hyperboreus (Krøyer), exposed to dissolved ¹⁴C-labeled trimethylamine (TMA) in seawater, oxidized TMA to trimethylamine oxide (TMAO), which accumulated in the organisms. The amount of TMAO synthesized was dependent on the time of exposure to TMA and the concentration of TMA in the seawater. It was inferred that copepods can produce TMAO by oxidation of TMA found in their plant food. Choline and methionine did not appear to be of importance as precursors of TMAO. There were large seasonal changes in TMA monooxygenase activity of both copepods. The activity was high in spring, and decreased through summer and autumn to a winter low in October to March. The changes in TMAO content of C. finmarchicus were, in comparison, small (this aspect was not tested for C. hyperboreus).     

Effects of dissolved cyanobacterial toxins on the survival and egg hatching of estuarine calanoid copepods

Toxic cyanobacteria occur in fresh, brackish, and marine waters worldwide. Harmful effects of intact cyanobacterial cells on zooplankton are well known, but only a few studies have focused on the effects of dissolved toxins. We investigated experimentally how the cyanobacterial toxins anatoxin-a, microcystin-LR, and nodularin affect estuarine calanoid copepods, by monitoring effects on egg hatching and survival in Eurytemora affinis. We also investigated effects of nodularin on the survival of Acartia bifilosa. All exposures were carried out using purified dissolved toxins. We found that the egg hatching was unaffected by these toxins, whereas survival was marginally affected by high concentrations of anatoxin-a and nodularin. For microcystin-LR, we found reduced survival at concentrations that were lower than those known to affect other meso-zooplankton.     

Comparative life histories of three species of planktonic calanoid copepods in Dabob Bay,Washington

The life history patterns of Calanus marshallae Frost, C. pacificus Brodsky, and Metridia lucens Boeck were determined in Dabob Bay, Washington, USA, during 1973 and October 1981–September 1982. C. marshallae emerged from diapause and moulted to adults in January–February. One major generation was observed, having been produced mainly during early to mid-March. Most surviving individuals spawned in March, arrested development at the C5 stage, and were in diapause by late May. However, some individuals developed to adults by late April and produced a very minor second generation. C. pacificus emerged from diapause and moulted to adults in February–March. The first generation produced during the spring lagged slightly behind the C. marshallae generation. C. pacificus produced two additional generations, one in late spring and one in the fall. The production of the three generations coincided with or closely followed phytoplankton blooms. Some C. pacificus arrested development at the C5 stage and entered diapause during the summer, but the majority of the population did not do so until fall. M. lucens did not appear to enter a diapause state. The fall and winter population was chiefly adult females which mostly remained at depth and were reproductively immature. Nevertheless, naupliar M. lucens were found on all sampling dates, indicating that reproduction never ceased as it did for the two Calanus species. M. lucens produced generations in late winter/early spring, late spring, and late summer/early fall. Interspecific comparisons between the life histories observed in Dabob Bay and intraspecific comparisons between the life histories in Dabob Bay and other locations are made. The advantages or disadvantages conferred to the copepods by their differing life histories are also discussed.     

Occurrence,viability and significance of resting eggs of the calanoid copepod Labidocera aestiva

Field and laboratory observations on the occurrence and viability of eggs of Labidocera aestiva Wheeler show that eggs of this temperate species which are laid in late fall remain viable on the bottom and hatch in late spring. These eggs thereby provide the means of repopulating temperate areas with this species after its winter disappearance from the plankton.     

Calanoid copepod eggs in sea-bottom muds. V. Seasonal changes in hatching of subitaneous and diapause eggs of Tortanus forcipatus

A warm-water neritic calanoid copepod, Tortanus forcipatus, has been found to lay two physiologically different types of eggs (subitaneous and diapause eggs), which are separately spawned in response to different seasonal environmental conditions. Subitaneous eggs are produced when the planktonic populations are at their numerical maxima, and are only shed until late summer. After peak spawning, true resting eggs are spawned which undergo diapause for 1 to 3 months. The eggs recover from their diapause around mid-winter, but hatching does not take place until the water temperature at the sea bottom exceeds 15°C in early summer.