Environmental regulation of feeding and egg production by Acartia tonsa off southern California

Omnivory in the calanoid copepod Temora longicornis: feeding, egg production and egg hatching rates

Effect of diet on the coupling of ingestion and egg production in the ubiquitous copepod, Acartia tonsa

Many suspension-feeding copepods show omnivorous feeding behavior. However, the relative contribution to egg production of herbivorous and heterotrophic feeding in copepods remains an open question. In this study, we quantified pigment ingestion rates and egg production rates of the planktonic calanoid copepod Acartia tonsa from July to November of 1986 in Long Island Sound, a large temperate estuary. Pigment ingestion and egg production rates were better correlated to the > 10-µm chlorophyll size fraction than total chlorophyll. Maximum pigment ingestion and egg production rates were observed during the fall bloom in September. Pigment ingestion and egg production rates were linearly related. However, pigment ingestion rates accounted for only 48% of the variance in egg production rates. If female A. tonsa had fed entirely as herbivores over the course of the season, the observed gross efficiency of egg production, K'1 = egg production rate/pigment ingestion rate, in terms of nitrogen, would have been 0.68. This growth efficiency is considerably higher than the expected value, K 1 = 0.38, for this species based on laboratory studies of herbivorous feeding. We suggest that the ratio H = K 1/K' 1 is a measure of the fraction of egg production that is due to herbivorous feeding. Thus, we infer that herbivory accounted for 56% (0.38/0.68) of egg production in A. tonsa in this study. The ratio H is an useful tool in examining the relative contribution to egg production of herbivorous and heterotrophic feeding in copepods.

Negative effects of prey species on consumers could be due to deterrence, nutritional insufficiency, or toxicity of the prey. These effects can be discerned in experiments in which the suspect prey is offered to the consumers in a food mixture containing another prey item that is not toxic and in which the ingestion rates on the prey and the grazers’ responses (e.g., egg production) are measured. We used this framework to determine whether several algae that have been reported to have harmful effects on grazers (Prorocentrum minimum, low‐and high‐toxin Alexandrium sp., Heterosigma carterae, Thalassiosira rotula, and Phaeodactylum tricornutum) are toxic to females of the calanoid copepod Acartia tonsa. Ingestion, egg production, and egg‐hatching rates were measured for A. tonsa offered sole diets of the suspect alga and mixed diets containing the suspect alga and a control alga (the green flagellate Tetraselmis sp.) at an ecologically relevant concentration (250 µg C L-1) and duration (3 d). With the exception of the Alexandrium strain with the high‐toxin content (16.3 pgSaxitoxin [pgSTX] equivalents cell21), none of the diets studied can be considered toxic. The high‐toxin Alexandrium reduced A. tonsa’s total ingestion rate, and thus egg production, as the proportion of Alexandrium increased in the diet. A. tonsa exhibited significantly reduced ingestion and egg production rates when feeding on sole food diets of H. carterae and P. tricornutum relative to the mixed food diets. However, a comparison of ingestion rates among the diet mixtures revealed that H. carterae and P. tricornutum acted as feeding deterrents when provided as sole foods. These results stress the importance of using mixed food diets when examining putative toxic effects of preys on consumers.

Prorocentrum minimum(clone Exuv) is nutritionally insufficient, but not toxic to the copepod Acartia tonsa

Egg production by Paracalanus parvus, a particle‐grazing copepod, was investigated in relation to its food supply. The concentration of available food (P) and the rates of ingestion (I) and egg production (B) were measured simultaneously at intervals of 6 h to 2 d for periods of 2–10 d. Concentration, chemical composition (carbon and nitrogen), and species of phytoplankton were experimental variables.Egg production was related to the food ingested during the previous day. For one food type, I and B were rectilinear functions of P. The average maximum rates of ingestion and egg production were 1.1 µg N·female−1·d−1 and 53 eggs·female−1·d−1, equivalent to specific rates of 1.5 and 0.37·d−1. B was proportional to I below a critical ingestion rate, Ic, and independent of I above Ic. For I <Ic, the gross efficiency of egg production (B ·I−1) in terms of nitrogen was 0.37 while in terms of carbon it was a hyperbolic function of the ratio of C:N in the food, ranging between 0.41 (C:Nfood = 4.0) and 0.15 (C:Nfood = 11). For I >Ic, B·I−1 declined in terms of both carbon and nitrogen.These results, together with the ratio of C:N in particulate matter in the sea off southern California, suggest that nitrogen (hence protein) potentially limits egg production by adult female Paracalanus and that ingested carbon is used inefficiently.

Egg production and development rates of Centropages typicus (Kroyer) were studied in the laboratory under carying food and temperature conditions. Egg production rates in the laboratory ranged from 0 to 124 eggs female-1 d-1 and increased with food concentration up to a critical food concentration (Pc) above which egg production was constant. Egg production rates were influenced by temperature, with more eggs being produced at 15°C than at 10°C. Thalassiosira weisflogii and Prorocentrum micans were determined to be equally capable of supporting egg production at concentrations above Pc at 15°C. Rate of egg production was independent of adult female size when food and temperature were constant. Egg production rates of freshly captured females ranged from 0 to 188 eggs female-1 d-1 and were higher in April and May than in June or July. Hatching rates of eggs increased with increased temperature; 95% of the eggs at 15°C hatched within 48 h, while only 8% of the eggs at 10°C hatched within 48 h. Development rates, determined at 10°C in excess concentrations of T. weisflogii, were 23.0 d from egg release to copepodid state I, 27.0 d to stage II, 29.5 d to stage III, 32.2 d to stage IV, 38.5 d to stage V and 49 d to adulthood based on the average time required for 50% of the organisms in an experiment to attain a given stage. Adult males were usually observed 2 to 4 d before adult females, and therefore have a slightly faster rate of development. The effects of temperature, food type and food concentration on egg production and the seasonal appearances of diatoms in the New York Bight may account for the observed seasonal cycles in abundance of C. typicus in these coastal waters.

In marine food webs, copepods are the major producers of a carotenoid pigment astaxanthin, which is an important antioxidant. The availability of astaxanthin for higher trophic levels can be affected by changes in phytoplankton stocks and copepod feeding; however, the functional relationship between food availability and astaxanthin production is poorly understood. We hypothesized that with a given food type and quality, astaxanthin content in copepods is positively related to feeding and egg production rates. The hypothesis was tested by measuring astaxanthin accumulation in concert with ingestion and egg production rates in the copepod Acartia bifilosa exposed to different algal concentrations (Tetraselmis suecica; 0 to 1200 μg C L−1). Egg production and ingestion rates increased with increasing food availability and reached a plateau at ≥400–600 μg C L−1. In contrast, increasing accumulation of astaxanthin with increasing food availability was observed only at concentrations ≤150 μg C L−1. Contrary to our hypothesis, at 600–1200 μg C L−1 copepods had maximal ingestion and egg production rates, but low astaxanthin contents. It is suggested that this low accumulation of astaxanthin at high food concentrations results from a food-dependant decrease in assimilation efficiency. These findings are important for the understanding of astaxanthin dynamics within marine food webs, where increases in phytoplankton biomass may translate to a trade-off between zooplankton quantity and its nutritional quality for zooplanktivores.

As part of an ongoing study of changes in the trophic pathways of Florida Bay's pelagic ecosystem, the nutritional environment (seston protein, lipid and carbohydrate levels), diet (taxon-specific microplankton ingestion rates) and egg production rate of the important planktonic copepod Acartia tonsa were measured off Rankin and Duck Keys in July and September 1997 and in January, March and May 1998. Rankin Key has been the site of extensive sea grass mortality and persistent ultraplankton blooms since 1987. Duck Key has experienced neither of these perturbations. Protist (auto-plus heterotroph) biomass was approximately twice as high off Rankin as off Duck Key. Diatoms, dinoflagellates and heterotrophic protists dominated the food environment off Rankin Key, while cells <5 μm diam often predominated off Duck Key. Protein and carbohydrate concentrations were higher off Rankin Key than Duck Key, while average lipid levels were usually low at both stations. Ingestion rates at both stations frequently approached temperature- and food-dependent maxima for the species, exceeding 100% of estimated body C d−1 on 3 of 5 occasions off Rankin Key. Egg production rates, however, were consistently low (Rankin: 3 to 16 eggs copepod−1 d−1; Duck: 1 to 12 eggs copepod−1 d−1), and gross egg production efficiencies (100% × egg production C/ingested C) averaged <10%. At Duck Key, egg production rate varied with temperature and food concentration, while off Rankin Key, egg production was strongly correlated with seston protein content. The efficiency with which lipids (which were scarce in the seston) were transferred from the diet to the eggs increased exponentially with decreasing seston lipid content. Egg production efficiencies based on protein, however, were independent of seston protein content and never exceeded 10%.

We examined the relationship between egg production rate (£) and pigment ingestion rate (/, from gut content corrected for 33% loss) for adult female Temora longicornis in Long Island Sound on 47 occasions. Linear regression of E on / [both variables expressed in mass of nitrogen (N) female day] was: £N = 0.0016 + 0.770 x /N. The slope, 0.77, is the apparent gross efficiency of egg production, equivalent to the gross growth efficiency (GGE) assuming that females partition all nitrogen for growth into egg production. Published work suggests that a GGE of 0.37 would be expected for herbivorous copepods. The discrepancy between the expected value of 0.37 and observed value of 0.77 could result from unquantified losses of gut pigment or because T.longicomis ingested a significant amount of nitrogen by feeding as a carnivore. We suggest that if T.longicomis females derive all of their nitrogen for growth by feeding on phytoplankton, and if no correction for pigment loss is employed, then the gut pigment method underestimates pigment ingestion by no more than a factor of two. There is disagreement among zooplanktologists about whether measurements of gut pigments can be used to provide a quantitative measure of feeding rates. Some laboratory experiments have shown that measurements of gut pigment content (GPC) do not yield accurate estimates of ingestion rates because of high and variable amounts of pigment destruction—losses of 75-99% have been reported (Conover et al., 1986; Lopez et al., 1988; Penry and Frost, 1991; Cary et al., 1992). On the other hand, others have shown that pigment losses range from 0 to 30% (Dagg and Walser, 1987; Ki0rboe and Tiselius, 1987; Pasternak and Drits, 1988; Peterson etal., 1990; Penry and Frost, 1991). One reason for such a broad range in results is that laboratory experiments can be influenced by a copepod's feeding pre-history and by the degree to which an animal is acclimated to experimental conditions (Penry and Frost, 1991; Mayzaud and Razouls, 1992). An associated problem is that when one attempts to evaluate the GPC method by constructing a pigment budget, inaccuracies can arise because pigments can be lost easily during an experiment. The puzzle is that when one compares ingestion rates measured by GPC to ingestion rates estimated from another independent method (such as measuring ingestion rate from the disappearance of phytoplankton cells), the GPC method does not yield underestimates of ingestion rate (Ki0rboe et al, 1985a; Durbin et al, 1990; Peterson et al, 1990). Clearly, we have a problem here: does the gut pigment method produce accurate results or not? Can the gut pigment method be used for the purpose for which it was originally proposed (Nemoto, 1968; Mackas and Bohrer, 1976), i.e. to estimate ingestion rates of zooplankton feeding on phytoplankton? In this paper, we evalu© Oxford University Press 855 W.T.Peterson and H.G.Dam ated the GPC technique by comparing ingestion estimated from GPC to ingestion estimated by measuring egg production rates of adult female copepods in Long Island Sound. Egg production is related to ingestion through gross growth efficiency (GGE) by:

Biochemical proxies are becoming increasingly common for growth assessment in zooplankton. Their suitability is often unknown, however, and proper calibration is lacking. We investigated correlations between physiological variables (ingestion, egg production, and respiration rates) and biochemical indices related to protein synthesis (RNA content, RNA:DNA ratio, RNA:protein ratio, and protein specific aminoacyl‐tRNA synthetases [spAARS] activity) in copepods Acartia bifilosa exposed to different algal concentrations (0–1200 µg C L−1). All variables assayed increased with increasing food concentration either linearly (spAARS) or nonlinearly (all other variables). Egg production and ingestion rates were significantly and positively correlated with RNA content and RNA:protein ratio, whereas correlations with spAARS and RNA:DNA ratio were weaker or nonsignificant. However, when RNA:DNA ratio and spAARS activity were used as predictors of ingestion, together they had higher explanatory value than did either variable separately. As there were substantial differences in saturating food concentrations among the assayed variables, applicability of biomarkers as proxies of physiological rates will be more reliable if restricted to the nonsaturated phase of the functional response of either variable, unless both variables saturate simultaneously. These findings contribute to methodology of zooplankton growth assessment and to our understanding of biochemical processes underlying growth and metabolism in copepods.

Egg and faecal pellet production rates, and their functional response to food and temperature, were measured for the Antarctic copepod Metridia gerlachei during January 1996. The study area comprised the Gerlache and Bransfield Straits and Drake Passage. The highest rates of “in situ” egg and faecal pellet production were observed in Gerlache stations, coinciding with chlorophyll a concentrations approaching food saturation levels. In the Bransfield and Drake stations, with very low chlorophyll concentrations, the rates of egg production were either very low, or no eggs were produced. Egg production rates, although well correlated with “in situ” chlorophyll values, appeared to be independent of food concentration on a short time-scale (24-h incubations), while the production of faecal pellets was closely related to food abundance in the same experiments. In general, the rates of egg production were low, even at food saturation, with a very high individual variability. Although in the majority of Gerlache stations about 50% of total chlorophyll a corresponded to the phytoplankton size-fraction >10 μm, M. gerlachei feeds preferentially on the <10-μm fraction. Temperature had no clear effects on egg production rate but had a significant effect on pellet production rates, with maximum values at 2.5°C. These features appear to agree with the reproductive strategy attributed to the species, based on a relatively low rate of egg production extended over a long reproductive period.

Experiments to determine egg production and feeding rates of Oithona davisae were carried out under controlled laboratory conditions. From copepodite IV stage on, the animals were fed the heterotrophic dinoflagellate Oxyrrhis marina in a wide range of concentrations (from 10 µg C L−1to 286 µg C L−1), and adult females were daily monitored to study different aspects of their fecundity. Both clutch and egg‐production rate increased with food concentration, with values from 8 to 20 eggs for the clutch size, and from 1.8 eggs to 6.3 eggs female−1 d−1 for the egg production. In addition, to assess the efficiency of conversion of food intake into egg mass, two feeding experiments were conducted. Maximum weight‐specific ingestion rates (≈ 80% body C d−1) and the egg‐production efficiency (16%) were lower than those reported for free‐spawning calanoid copepods. The fact that satiating food concentrations for feeding and egg production of adult females of Oithona davisae were rather low suggests an adaptation to exploit oligotrophic environments, and might explain the ecological success of the genus in situations when food becomes limiting for other groups of copepods.

CCEIII: Persistent functional relationships between copepod egg production rates and food concentration through anomalously warm conditions in the California Current Ecosystem

We measured ingestion rate (IR), egg production rate (EPR) and egg hatching success (EHS) at increasing prey concentrations and calculated egg production efficiency (EPE) and maintenance rate (MR) in the estuarine copepod Acartia tonsa fed three different algal diets. EPR and EHS were relatively more affected by prey species than by prey concentration. EPEs were constant among carbon concentrations (C) on a diet of Rhodomonas baltica (0.202 ± 0.055, mean ± SD) and Dunaliella tertiolecta (0.034 ± 0.015), but decreased significantly from 0.371 ± 0.062 (mean of two lowest prey concentrations) to 0.200 ± 0.019 at the highest concentration of Thalassiosira weissflogii. In general it seems that other requirements than C demand limit EPE and EHS in A. tonsa. The MR (IR when EPR = 0) was significantly higher on D. tertiolecta, which also yielded the lowest EPEs, and it seems that variations in maintenance requirements may have been instrumental in evoking EPE variations as well.