Fitness consequences for copepods feeding on a red tide dinoflagellate: deciphering the effects of nutritional value, toxicity, and feeding behavior

Phytoplankton exhibit a diversity of morphologies, nutritional values, and potential chemical defenses that could affect the feeding and fitness of zooplankton consumers. However, how phytoplankton traits shape plant–herbivore interactions in the marine plankton is not as well understood as for terrestrial or marine macrophytes and their grazers. The occurrence of blooms of marine dinoflagellates such as Karenia brevis suggests that, for uncertain reasons, grazers are unable to capitalize on, or control, this phytoplankton growth—making these systems appealing for testing mechanisms of grazing deterrence. Using the sympatric copepod Acartia tonsa, we conducted a mixed diet feeding experiment to test whether K. brevis is beneficial, toxic, nutritionally inadequate, or behaviorally rejected as food relative to the palatable and nutritionally adequate phytoplankter Rhodomonas lens. On diets rich in K. brevis, copepods experienced decreased survivorship and decreased egg production per female, but the percentage of eggs that hatched was unaffected. Although copepods showed a 6–17% preference for R. lens over K. brevis on some mixed diets, overall high ingestion rates eliminated the possibility that reduced copepod fitness was caused by copepods avoiding K. brevis, leaving nutritional inadequacy and toxicity as remaining hypotheses. Because egg production was dependent on the amount of R. lens consumed regardless of the amount of K. brevis eaten, there was no evidence that fitness costs were caused by K. brevis toxicity. Copepods limited to K. brevis ate 480% as much as those fed only R. lens, suggesting that copepods attempted to compensate for low food quality with increased quantity ingested. Our results indicate that K. brevis is a poor food for A. tonsa, probably due to nutritional inadequacy rather than toxicity, which could affect bloom dynamics in the Gulf of Mexico where these species co-occur.     

Chitobiase of planktonic crustaceans from South Atlantic coast (Southern Brazil): Characterization and influence of abiotic parameters on enzyme activity

Chitobiase is one of the enzymes involved in chitin degradation in nature. It is produced and released by a variety of organisms from bacteria to fish. In crustaceans, it is associated with digestive function and acts on the epidermis during the molting process. In the present study, the influence of water pH, temperature and salinity on maximum chitobiase activity (MCA), as well as the enzyme affinity (Km) for a substrate, the methylumbelliferyl N-acetyl-ß-d-glucosaminide (MUFNAG) was evaluated in the copepod Acartia tonsa. Km values for chitobiases of other crustaceans from the Patos Lagoon estuary and Cassino Beach (Southern Brazil) were also determined. For A. tonsa, MCA was observed at pH 5-6 and 30-35 °C. The range of pH was quite similar to that reported for other aquatic organisms. However, the range of temperature was lower than that previously reported. For salinity, no previous studies have considered the influence of this parameter on MCA. For A. tonsa, MCA was observed in freshwater, showing a significant linear decrease with increasing salinity. Considering that maximum copepod survival and growth rates are observed between 15 and 25 ppt, these findings suggest that the observed enzyme activity in this range of salinity (68 to 47% of that measured in freshwater) is not a limiting factor for A. tonsa growth. However, the extremely decreased enzyme activity observed in salinity 30 ppt (33% of that measured in freshwater) suggests that chitobiase activity might be one of the limiting factor for copepod growth at 30 ppt salinity or higher. Km values (μM) determined for organisms evaluated in the present study (copepod A. tonsa = 20.77; mysid Metamysidopsis elongata atlantica = 14.67; nauplii barnacle Balanus improvisus = 18.19; decapod zoea = 14.30; decapod megalopa = 24.77) were lower than those reported for other crustaceans from Northern Hemisphere. Also, they were much lower than those of organisms from different taxonomic groups like bacteria and fungi, but much higher than in protozoans and dinoflagelates. These findings suggest that chitobiase might be differentially evolved in each specific group of organism, and even within different ontogenetic stages of the same species, for a better adaptation to cope with its respective environmental needs.     

Acartia tonsa: a species new for the Black Sea fauna

The presence of Acartia tonsa in Black Sea waters (South Crimean coast, Ukraine) is reported for the first time. A. tonsa may be a recently introduced species in the Black Sea. Morphological features of the adults have been shown by S.E.M.     

Space and time distribution of zooplankton in a Mediterranean lagoon (Etang de Berre)

In the Berre lagoon, a large brackish and swallow area near Marseille, the environmental factors (temperature, salinity, oxygen, suspended particulate matter and chlorophyll) generally display strong space and time variations. The rotifer Brachionus plicatilis and the copepod Acartia tonsa constitute the bulk of the zooplankton population during all the year. Their space and time distributions were studied in 23 stations distributed all over the lagoon, during four seasonal cruises (February, June, October, November), at surface and bottom layers. There is no marked difference in the horizontal and vertical distribution of the two species, (except in November when rotifers were prevailing in surface and copepods at depth) and in their time occurence. When the four series of data are pooled, correlation analysis show that A.tonsa is positively correlated with temperature, salinity and seston and negatively to oxygen and chlorophyll. B. plicatilis is positively correlated with temperature and seston, but also with chlorophyll, while salinity has a negative effect. The specific eggs number of both species is chlorophyll dependent. Considering seasonal cruises separately, some differences appear in the sense or the significance of these different correlations. The respective distribution of the two species is only partly dependent on the variation of the environmental factors: most of the variance remains unexplained, as indicated by the result of a stepwise multiple regression analysis using the most significant factors (temperature, salinity and oxygen explain 33 to 42% of the variance in Acartia, while temperature and salinity explain 27 to 28% of the variance in Brachionus). Thus, internal behavioral factors could also play a role in the distribution of organisms, particularly in some cases of aggregations of organisms observed during this study. As the two species occupied the same space habitat most of the year, they are potentially in competition for food. A way to optimize the food utilization could be the time separation of their feeding activity, nocturnal in Acartia and diurnal in Brachionus. Another way could be selective feeding upon food particles depending on their size (Brachionus being able to use finer particles than Acartia) or their quality (Brachionus being more herbivorous than Acartia) as demonstrated in some grazing experiments carried out in parallel.     

Egg production of the copepod Acartia tonsa: The influence of hypoxia and food concentration

Low dissolved oxygen conditions, or hypoxia, occur in estuaries and impact more than just the obvious commercially important species. Copepods are an important link in the food web, and the influence of hypoxia upon them is relatively unstudied. Using the copepod Acartia tonsa, a study of the impact of hypoxia on egg production was conducted. A. tonsa had reduced egg production at low dissolved oxygen concentrations (DO), with the lowest egg production occurring at 0.53-ml/l O₂ concentration. Another experiment was conducted to determine if, by increasing food concentration, the affect of hypoxia could be mitigated. The results indicate that increased food did not offset the impact that hypoxia had on egg production of A. tonsa. These results suggest that as A. tonsa experiences hypoxia in the wild, population numbers will decrease. Thus, if hypoxic conditions increase in scope and duration, declines in copepod abundance may lead to a decline in the abundance of species that depend on them as food. These species may be of commercial importance (e.g., fish, crabs, and oysters).     

Hypoxia and seasonal temperature: Short-term effects and long-term implications for Acartia tonsa dana

Far more attention has been given to the short-term lethal impacts of reduced dissolved oxygen on commercially important fish and crabs than to the long-term sublethal impacts on these same species, or on lower trophic levels. This study demonstrates that chronic, sublethal effects of hypoxia on the copepod Acartia tonsa, a critical component of many pelagic coastal food webs, can lead to significant decreases in population growth. The results of laboratory experiments conducted at 15 °C (winter) and 25 °C (summer), under conditions of normoxia (Controls), sublethal hypoxia (1.5 ml l^− 1) and lethal hypoxia (0.7 ml l^− 1) show that egg production female^− 1 day^− 1 was significantly lower at 0.7 ml l^− 1 compared to Controls at both temperatures, while egg production female^− 1 day^− 1 was significantly lower at 1.5 ml l^− 1 compared to controls in both summer experiments and in one of the two winter experiments. Survival was significantly decreased in the 0.7 ml l^− 1 treatment compared to Controls and the 1.5 ml l^− 1 treatment. Copepods developed more slowly and matured at smaller adult body sizes at both temperatures under both lethal and sublethal hypoxia compared to normoxia. Under summer temperatures, egg production was reduced by hypoxia exposure on two counts: (1) exposure to hypoxia during development resulted in smaller adults, which translated into lower egg production, and (2) egg production was still significantly lower in hypoxia treatments compared to Controls even when differences in body size were taken into account. While copepods collected in winter and exposed to winter temperatures and hypoxia also matured at smaller body sizes than copepods exposed to normoxia, egg production in winter was almost entirely attributable to this reduction in body size. These results suggest that coastal hypoxia may have a significantly greater impact in the summer months, when copepod populations are most abundant and growing at their most rapid rate of the year. With the anticipated increases in global temperatures, hypoxia may have even greater impacts on pelagic food webs.     

Impact of hypoxia on the survival, egg production and population dynamics of Acartia tonsa Dana

Concern for the increasing occurrence of coastal zone hypoxia has generally focused on the direct, short-term impact of reduced dissolved oxygen (DO) concentrations on the survival of commercially important species such as fish and crabs. Copepods, especially the naupliar stages, are important pelagic food web components, yet only a few studies have considered the effect of reduced DO concentrations on their survival and population dynamics. This study considers the impact of both lethal and sublethal DO concentrations on copepods. Acartia tonsa were reared at 25 °C at saturating DO (normoxic control) and reduced (hypoxic) DO concentrations of 1.5 or 0.7 ml l⁻¹. Oxygen concentrations were maintained in replicate flasks, by bubbling seawater with air (control), or mixtures of nitrogen and oxygen. Egg production, but not survival, was significantly higher in the controls compared to the 1.5 ml l⁻¹ DO treatment. Survival and egg production were significantly lower at 0.7 ml l⁻¹ DO compared to the control. The results suggest that the sublethal as well as the lethal effects of hypoxia may have important repercussions on population and community dynamics in coastal systems.     

Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching

Recent literature suggests that heterotrophic protists could improve the biochemical constituents of poor quality algae for subsequent use by higher trophic levels, a phenomenon dubbed “trophic upgrading”. We conducted experiments to test trophic upgrading effects on the omnivorous calanoid copepod Acartia tonsa. Two heterotrophic protists, Oxyrrhis marina and Gymnodinium dominans, were grown on three algal species of different nutritional qualities: Dunaliella tertiolecta, Isochrysis galbana and Rhodomonas salina. In parallel incubations, the copepods were fed the heterotrophic protists or the algae that the protists grew on. We measured the ingestion rate, egg production rate and egg hatching success of the copepods in each treatment. Comparison of the egg production efficiency (EPE; egg carbon production/carbon ingestion×100%) between parallel diet treatments allowed us to calculate the trophic upgrading index (TUI; ratio of EPE-heterotrophic protist to EPE-alga). The copepods ingested similar amount, or 20-30% more algae than heterotrophic protists. Daily rations ranged 50-122% of body C per day. Copepods feeding on O. marina that grew on D. tertiolecta had higher egg production rate and egg hatching success than copepods feeding on D. tertiolecta directly, and the resultant TUI between the two treatments was 19.7. Similarly, the copepod egg production was improved by G. dominans that grew on D. tertiolecta and the resultant TUI was 23.3. TUI was near 1 between I. galbana treatment and the parallel heterotrophic protist treatments, indicating no or little trophic upgrading effects on the copepod's egg production. However, egg hatching success was significantly lower with G. dominans growing on I. galbana. O. marina that grew on R. salina induced a lower EPE relative to the alga itself, yielding a TUI of less than 1. Biochemical data showed that the heterotrophic protists contained eicosapentanoic acid (EPA) and docosahexanoic acid (DHA) even when they fed on alga that lacked these essential fatty acids, which may explain some of the observed trophic upgrading effects and species-specific differences in our experiments. However, our data also suggested that dietary EPA and DHA could not be the sole factors regulating the copepod's reproductive output, and that egg production and egg hatching appeared to have different nutritional requirements and respond differently to the copepod's diets.     

Feeding rates and productivity of the copepod Acartia bifilosa in a highly turbid estuary; the Gironde (SW France)

Acartia spp. are the dominant copepod species in the Gironde estuary, seaward of the turbidity maximum area. Acartia bifilosa develop a large population in spring and early summer whereas Acartia tonsa appear in late summer. High values and high variability of chlorophyll a/suspended particulate matter ratio are found seaward of the turbidity maximum area. Feeding rates of A. bifilosa were measured by fluorometry. Phytoplankton ingestion was found to be highly variable, between 8 to 80% of copepod carbon body weight. Except for adult females, copepods were heavier in summer than in winter. PB ratios, estimated by the instantaneous growth rate method, varied from 0.03 d^–1 to 0.14 d^–1. The gut contents and P/B ratios of Acartia bifilosa were related to chl a/SPM ratio. From those data, and a few obtained for A. tonsa, it is concluded that only in summer months phytoplankton ingestion is enough to maintain secondary production.     

Indirect multi-trophic interactions mediated by induced plant resistance: impact of caterpillar feeding on aphid parasitoids

Cotton produces insecticidal terpenoids that are induced by tissue-feeding herbivores. Damage by Heliothis virescens caterpillars increases the terpenoid content, which reduces the abundance of aphids. This effect is not evident in Bt-transgenic cotton, which is resistant to H. virescens. We determined whether induction of terpenoids by caterpillars influences the host quality of Aphis gossypii for the parasitoid Lysiphlebus testaceipes and whether this interaction is influenced by Bt cotton. The exposure of parasitoids to terpenoids was determined by quantifying terpenoids in the aphids. We detected several terpenoids in aphids and found a positive relationship between their concentrations in plants and aphids. When L. testaceipes was allowed to parasitize aphids on Bt and non-Bt cotton that was infested or uninfested with H. virescens, fewer parasitoid mummies were found on infested non-Bt than on Bt cotton. Important parasitoid life-table parameters, however, were not influenced by induced resistance following H. virescens infestation, or the Bt trait. Our study provides an example of a tritrophic indirect interaction web, where organisms are indirectly linked through changes in plant metabolites.     

Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities

BACKGROUND: Carnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs. PITCHER: Fluid as a Habitat The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O(2) and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water. INQUILINE: Diversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. MUTUALISTIC: Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N(2). CONCLUSIONS: There is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.     

Oxygenation of anoxic sediments triggers hatching of zooplankton eggs

Many coastal marine systems have extensive areas with anoxic sediments and it is not well known how these conditions affect the benthic–pelagic coupling. Zooplankton lay their eggs in the pelagic zone, and some sink and lie dormant in the sediment, before hatched zooplankton return to the water column. In this study, we investigated how oxygenation of long-term anoxic sediments affects the hatching frequency of dormant zooplankton eggs. Anoxic sediments from the brackish Baltic Sea were sampled and incubated for 26 days with constant aeration whereby, the sediment surface and the overlying water were turned oxic. Newly hatched rotifers and copepod nauplii (juveniles) were observed after 5 and 8 days, respectively. Approximately 1.5 × 10⁵ nauplii m⁻² emerged from sediment turned oxic compared with 0.02 × 10⁵ m⁻² from controls maintained anoxic. This study demonstrated that re-oxygenation of anoxic sediments activated a large pool of buried zooplankton eggs, strengthening the benthic–pelagic coupling of the system. Modelling of the studied anoxic zone suggested that a substantial part of the pelagic copepod population can derive from hatching of dormant eggs. We suggest that this process should be included in future studies to understand population dynamics and carbon flows in marine pelagic systems.     

Colour learning when foraging for nectar and pollen: bees learn two colours at once

Bees are model organisms for the study of learning and memory, yet nearly all such research to date has used a single reward, nectar. Many bees collect both nectar (carbohydrates) and pollen (protein) on a single foraging bout, sometimes from different plant species. We tested whether individual bumblebees could learn colour associations with nectar and pollen rewards simultaneously in a foraging scenario where one floral type offered only nectar and the other only pollen. We found that bees readily learned multiple reward–colour associations, and when presented with novel floral targets generalized to colours similar to those trained for each reward type. These results expand the ecological significance of work on bee learning and raise new questions regarding the cognitive ecology of pollination.     

Predator feeding choice on conspicuous and non-conspicuous carabid beetles: first results

Insects use various types of behaviour, chemical defences, mimetic, aposematic or cryptic appearances as anti-predatory strategies. Among insects, carabid beetles of the genus Brachinus are distasteful prey because they discharge an irritating "cloud" of quinones when threatened. These beetles live in aggregations and adopt warning (conspicuous pattern) colours and chemicals to create a template that is easily learnt by predators. Another carabid beetle, Anchomenus dorsalis, mimics the colours and cuticular profile of Brachinus and is usually found in Brachinus aggregations. In this paper we report results from laboratory observations on feeding choice of the following natural predators - Crocidura leucodon (Insectivora: Soricidae), Ocypus olens (Coleoptera: Staphylinidae) and Podarcis sicula (Reptilia: Lacertidae) - on carabid beetle species. Comparing the number of attacks of predators towards aposematic and non-aposematic prey, there was a statistically significant preference towards non-aposematic prey.     

Low intensity surface fire instigates movement by adults of Calosoma frigidum (Coleoptera, Carabidae)

The genus Calosoma (Coleoptera: Carabidae) is a group of large, sometimes ornate beetles, which often voraciously attack caterpillars. Many studies have reported Calosoma beetles being highly conspicuous during defoliator outbreaks. Based on observations of individual beetle behavior, patterns of activity density and phenology we provide a hypothesis on how environmental cues may synchronize Calosoma activity with periods of high defoliation. We have observed that adults of Calosoma frigidum construct underground burrows similar to those reported to be created by larvae for pupation. We propose that small increases in soil surface temperature caused either by defoliation events or decreased albedo of blackened, burned soil causes beetles to leave their underground burrows and begin foraging. Indirect support for this hypothesis comes from high levels of adult Calosoma frigidum collected in relatively small patches of burned forest (<200m(2)) relative to the surrounding mosaic of unburned forest shortly after a prescribed surface burn.     

Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers

Animals exploiting their familiar food items often avoid spatio-temporal aggregation with others by avoiding scents, less rewarding areas or visual contacts, thereby minimizing competition or interference when resources are replenished slowly in patches. When animals are searching or assessing available food sources, however, they may benefit from reducing sampling costs by following others at food sites. Therefore, animals may adjust their responses to others depending on their familiarity with foraging situations. Here, we conducted field experiments to test whether nectar-collecting bumble bees make this adjustment. We allowed free-foraging bees to choose between two inflorescences, one occupied by a conspecific bee and another unoccupied. When bees were presented with flowers of a familiar type, they avoided occupied inflorescences. In contrast, bees visited an occupied inflorescence when the flower type was unfamiliar. To our knowledge, this is the first report suggesting that animals adjust their responses to feeding conspecifics depending on their familiarity with food sources. Such behavioural flexibilities should allow foragers to both explore and exploit their environments efficiently.     

Respiration rates of subitaneous eggs from a marine calanoid copepod: monitored by nanorespirometry

The oxygen consumption rate during embryogenesis of Acartia tonsa subitaneous eggs were measured at different temperatures (10, 15, 17, 21, 24 and 28°C) with nanorespirometry. The oxygen consumption was constant during the embryogenesis but increased rapidly at hatching time. The mean ± SD oxygen consumption rate increased exponentially with temperature and ranged from 0.09 ± 0.04 (10°C) to 0.54 ± 0.09 nmol O₂ egg⁻¹ h⁻¹ (28°C). The mean ± SD Q₁₀-value was 2.51 ± 0.15. Calculations of energy consumption during embryogenesis ranged from 1.86 to 18.28 mJ depending on temperature and development time. We conclude that the effect of temperature on oxygen consumption rate was far less important than the prolonged development time when calculating the energy consumed during embryogenesis.     

The predation impact of juvenile herring Clupea harengusand sprat Sprattus sprattus on estuarine zooplankton

The consumption of estuarine copepods by juvenile herring and sprat during estuarine residency was estimated using fish biomass data and daily rations calculated from two models of feeding in fish: a bioenergetic model and a gastric evacuation model. The bioenergetic model predicted daily rations that were, on average, three times higher than those estimated by a model based on field records of stomach contents. The biomass of herring and sprat in the estuary was negatively correlated with the daily ration suggesting that the clupeid fish populations were resource-limited. Copepod production decreased towards the winter and peaked in spring and summer. The relative importance of predation changed seasonally in function of the migration pattern of herring and sprat. In the spring and the summer, in situ production ofcopepod biomass was higher than the in situ consumption by fish. During the fall and the winter, consumption exceeded production. This suggests that top–down control exerted by marine pelagic fish may be an important force structuring estuarine copepod populations.     

Liparid and macrourid fishes of the hadal zone: in situ observations of activity and feeding behaviour

Using baited camera landers, the first images of living fishes were recorded in the hadal zone (6000–11 000 m) in the Pacific Ocean. The widespread abyssal macrourid Coryphaenoides yaquinae was observed at a new depth record of approximately 7000 m in the Japan Trench. Two endemic species of liparid were observed at similar depths: Pseudoliparis amblystomopsis in the Japan Trench and Notoliparis kermadecensis in the Kermadec Trench. From these observations, we have documented swimming and feeding behaviour of these species and derived the first estimates of hadal fish abundance. The liparids intercepted bait within 100–200 min but were observed to preferentially feed on scavenging amphipods. Notoliparis kermadecensis act as top predators in the hadal food web, exhibiting up to nine suction-feeding events per minute. Both species showed distinctive swimming gaits: P. amblystomopsis (mean length 22.5 cm) displayed a mean tail-beat frequency of 0.47 Hz and mean caudal : pectoral frequency ratio of 0.76, whereas N. kermadecensis (mean length 31.5 cm) displayed respective values of 1.04 and 2.08 Hz. Despite living at extreme depths, these endemic liparids exhibit similar activity levels compared with shallow-water liparids.