The abundance of mixotrophic algae drives the carbon isotope composition of the copepod Boeckella gracilipes in shallow Patagonian lakes (original) (raw)
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Copepods in Turbid Shallow Soda Lakes Accumulate Unexpected High Levels of Carotenoids
PLoS ONE, 2012
Carotenoids are protective pigments present in many aquatic organisms that reduce the photooxidative stress induced by short-wavelenght solar radiation, yet increase their susceptibility to predators. Arctodiaptomus spinosus, a calanoid copepod typically found in many fishless shallow soda lakes, shows large between-lake differences in pigmentation. Here, we attribute these differences to the environmental state of these ecosystems, namely, 'dark water' lakes with submersed vegetation and turbid 'white' lakes lacking macrophytes. Copepod carotenoid concentration in the turbid 'white' lakes was significantly (about 20-fold) higher than in the 'dark water' ones, although the latter systems were characterized by higher transparency. In addition, males had on a dry weight basis around three times higher carotenoid concentrations than females. Mycosporine-like amino acids (direct UV screening substances) were found in all cases, but in low concentration. The environmental conditions in these ecosystems were largely shaped by the presence/absence of submersed macrophytes Thus, in the turbid lakes, the strong wind-driven mixis allows for copepods to be brought to the surface and being exposed to solar radiation, whereas in 'dark water' ones, macrophytes reduce water turbulence and additionally provide shelter. Our results explain the counter-intuitive notion of strong red pigmentation in copepods from a turbid ecosystem and suggest that factors other than high UV transparency favor carotenoid accumulation in zooplankton.
Small copepods (<2 mm) are the most abundant metazoans in the world’s oceans, a keystone in pelagic food webs. Small copepods are considered to be omnivorous, feeding on unicellular protists and phytoplankton, with carnivorous feeding –i.e. preying on zooplankton- restricted to larger copepods and cyclopoid copepods. We developed a PCR based technique that detected a diverse range of zooplankton species (eight families of decapods, bivalves, fish, and also other copepods) within the digestive tract of copepods traditionally considered to be “herbivorous”. This finding provides evidences that a significant component of copepod diets has been overlooked owed to the methodologies traditionally been carried out –visual inspection and pigments analysis. Such predatory behaviour extends the trophic role of small copepods in upwelling food webs, affecting the mesozooplankton communities through intraguild predation. Furthermore, this study helps to explain the discrepancies found between quantified phyto/microzooplankton ingestion and metabolic demands of copepods. In order to infer the consequences of this overlooked predatory behaviour to the flux of Carbon in the whole pelagic ecosystem, we screened the literature to obtain an estimate of weight specific ingestion rates (WSIR) based on their averaged weight for adult calanoid (n=121) and cyclopoid copepods (n=41), in the field (n=125) and under laboratory conditions (n=37). By multiplying the estimated WSIR by the standing stock of adult copepods in the upper 100 m of the ocean -assuming that i) copepods are approximately 80% of the total zooplankton biomass ii) only 50% are adults and iii) calanoids comprise between 30 to 40% of total copepods (the rest being cyclopoid copepods) - our carbon budget estimates show that on a global scale, copepods process, between 3.41 - 3.70 up to 20.75 - 21.87 gigaton (Gt) C yr-1 through zooplankton predation based on field and laboratory measured WSIR, respectively. This conservative field estimate reveals that copepods are channeling 31.28 - 33.95% more carbon towards upper trophic levels than previous estimates focused on phytoplankton and microzooplankton consumption (10.9 Gt C yr-1). Hence, copepod intrigued predation should definitely be considered in oceanic biogeochemical cycles and ecosystem models.
Aquatic Microbial Ecology, 2004
Copepod and appendicularian grazing experiments using naturally occurring planktonic assemblages from a coastal embayment (Mejillones Bay, northern Chile upwelling system at 23º S) were conducted between October 2000 and October 2001. Total carbon ingestion rates based on sizefractioned chlorophyll data showed that dominant copepods (Acartia tonsa, Centropages brachiatus, Oithona similis and Paracalanus parvus) ingested between 2 and 8 µg C ind.-1 d-1 , while appendicularians (Oikopleura dioica and O. longicauda) ingested ~3 to 4 µg C ind.-1 d-1. Even when most copepods were feeding on larger cells (> 23 µm) at high rates, the smaller copepods also grazed at similar rates on nanoplankton (5 to 23 µm) and picoplankton (< 5 µm). In contrast, chain-forming diatoms were cleared at very low rates by copepods. Bacteria were cleared only by appendicularians (~170 tõ 400 ml ind.-1 d-1) but not by any copepod, while heterotrophic protists constituted a substantial proportion in the diet of both copepods and appendicularians (~10 to 100% body carbon d-1), particularly during austral spring. Occasionally, copepod C-specific ingestion on heterotrophs was similar to that on autotrophic cells. Large ciliates and dinoflagellates were cleared but not ingested by the appendicularian O. dioica, suggesting a mechanism of trapping large cells in their houses and implying a rapid export of fresh material. Since heterotrophs are a common component in the diet of these 2 groups (omnivory by copepods and bacterophagy by appendicularians), they can potentially affect microbial food webs in this upwelling system and thus carbon export.
Journal of Plankton Research, 2001
The calanoid copepod, Boeckella gracilipes, is the dominant crustacean zooplankton in South Andean deep ultra-oligotrophic lakes. Combining field and experimental data we explored the feeding of the copepod and its access to the mixotrophic ciliate, Ophrydium naumanni, in Lake Moreno Oeste (Patagonia, Argentina). Phytoplankton was dominated by nanoflagellates throughout the water column. Ophrydium naumanni, which accumulates much of the chlorophyll a, as do copepodites and adults of B. gracilipes, has a deep distribution during the day, with maximal abundances around 30 m depth. Mouth-part morphology analysis of B. gracilipes indicated that the copepod has an omnivorous diet. Laboratory experiments showed that B. gracilipes could access O. naumanni only when it is offered as a single food item. However, when natural phytoplankton and ciliate assemblages (including O.naumanni) are offered, B. gracilipes did not eat Ophrydium and preyed on the oligotrich, Strombidium viride, and phytoflagellates like Chrysochromulina parva. The range of ingested sizes was broad (3.9-33 µm of equivalent spherical diameter) but all selected particles were motile ones with distinctive movements, which would enhance the copepod particle detection. JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES -
Aquatic Microbial Ecology, 2004
Copepod and appendicularian grazing experiments using naturally occurring planktonic assemblages from a coastal embayment (Mejillones Bay, northern Chile upwelling system at 23º S) were conducted between October 2000 and October 2001. Total carbon ingestion rates based on sizefractioned chlorophyll data showed that dominant copepods (Acartia tonsa, Centropages brachiatus, Oithona similis and Paracalanus parvus) ingested between 2 and 8 µg C ind. -1 d -1 , while appendicularians (Oikopleura dioica and O. longicauda) ingested ~3 to 4 µg C ind. -1 d -1 . Even when most copepods were feeding on larger cells (> 23 µm) at high rates, the smaller copepods also grazed at similar rates on nanoplankton (5 to 23 µm) and picoplankton (< 5 µm). In contrast, chain-forming diatoms were cleared at very low rates by copepods. Bacteria were cleared only by appendicularians (~170 tõ 400 ml ind. -1 d -1 ) but not by any copepod, while heterotrophic protists constituted a substantial proportion in the diet of both copepods and appendicularians (~10 to 100% body carbon d -1 ), particularly during austral spring. Occasionally, copepod C-specific ingestion on heterotrophs was similar to that on autotrophic cells. Large ciliates and dinoflagellates were cleared but not ingested by the appendicularian O. dioica, suggesting a mechanism of trapping large cells in their houses and implying a rapid export of fresh material. Since heterotrophs are a common component in the diet of these 2 groups (omnivory by copepods and bacterophagy by appendicularians), they can potentially affect microbial food webs in this upwelling system and thus carbon export.
Zooplankton response to organic carbon level in lakes of differing trophic states
Knowledge and Management of Aquatic Ecosystems, 2014
Water eutrophication is associated with an increase in the organic carbon content (both particulate and dissolved forms), which may affect the functioning of the zooplankton community. Mesotrophic and eutrophic lakes in the Masurian Lake District (Poland) were selected to evaluate the relationship between the organic carbon level and the zooplankton community. The lakes differed significantly in most environmental variables. RDA analysis was performed to evaluate the impact of environmental variables on zooplankton. The variables that significantly explained the variance in the zooplankton community abundance (Monte Carlo permutation test) included dissolved and particulate organic carbon, Secchi disc visibility, soluble reactive phosphorus and total nitrogen. The response of zooplankton to an increasing level of organic carbon is functional rather than quantitative. In the mesotrophic system, the results of the redundancy analysis indicated relatively strong positive relationships between dissolved organic carbon and zooplankton biomass, and negative correlations between chlorophyll a and zooplankton biomass. The above suggests that indirect organic carbon utilization by zooplankton could partly compensate for the poor feeding conditions of planktonic animals (decreased phytoplankton availability). In the eutrophic lake, elevated organic carbon levels are partly limited by zooplankton, which is suggested by the positive relationship between particulate organic matter and the total zooplankton biomass (RDA results). The positive relationship between the biomass of copepods and organic carbon in particulate and dissolved forms implies that copepods benefit from the increased heterotrophic carbon flow that is activated in the eutrophic lake. RÉSUMÉ Réponse du zooplancton au niveau de carbone organique dans des lacs de statuts trophiques différents
Biogeosciences Discussions, 2007
Within the frame of the Pelagic Ecosystem CO 2 Enrichment (PeECE III) experiment, reproduction and feeding of the copepod Calanus finmarchicus was monitored in relation to phytoplankton development in two mesocosms, at present 1× (350 µatm) and ca 3× present (1050 µatm) CO 2 concentrations, respectively. Both mesocosms showed rapid 5 phytoplankton growth after the initial nutrient additions and reached maximum chlorophyll (Chl) a concentrations around day 10. Flow-cytometry and specific pigment analysis (HPLC-CHEMTAX), showed that diatoms and prymnesiophyceae (Emiliania huxleyi (Ehux) and other nanoplankton) dominated the biomass. Feeding and egg production rates of C. finmarchicus developed similarly in both mesocosms, and were positively 10 correlated with Chla, Ehux, diatom and prymnesiophyceae concentrations. Although the total number of copepod nauplii recruited during the experiment was similar in 1× and 3×, significantly less nauplii were recruited in 3× during the peak of the bloom compared to in 1×. We conclude that the algae responsible for the higher biomass in 3× during the peak of the bloom (diatoms and Ehux), may have been relatively inferior 15 food for C. finmarchicus naupliar recruitment, possibly due to a high C:N ratio (>8). Nevertheless, the 3 fold increase in CO 2 concentration did not show any clear overall effect on bulk phytoplankton or zooplankton development over the whole experiment, suggesting a more complex coupling between increased CO 2 and the nutritional status of the system. 20 25 depending on the consumption of fossil fuels (Houghton et al., 2001). If uncertainties 3914 BGD Abstract Introduction Conclusions References Tables Figures Back Close Full Screen / Esc Printer-friendly Version Interactive Discussion
Stable isotope variability of meso-zooplankton along a gradient of dissolved organic carbon
Freshwater Biology, 2009
1. The d 13 C and d 15 N signatures of zooplankton vary with dissolved organic carbon (DOC), but inconsistent and limited taxonomic resolution of previous studies have masked differences that may exist among orders, genera or species and are attributable to dietary and ⁄ or habitat differences. Here we investigate differences among the isotopic signatures of five zooplankton taxa (Daphnia, Holopedium, large Calanoida, small Calanoida and Cyclopoida) in Precambrian shield lakes with a sixfold range of DOC concentration. 2. d 13 C signatures of Daphnia, small calanoids and large calanoids became more depleted with increasing lake DOC, whereas Holopedium and cyclopoid d 13 C became enriched with increasing DOC concentration. 3. The variability of d 13 C and d 15 N isotopic signatures among zooplankton groups was reduced in high-DOC, compared to low-DOC lakes, especially for d 13 C. Differences in d 13 C and POM-corrected d 15 N accounted for up to 33.7% and 19.5% of the variance, respectively, among lakes of varying DOC concentration. 4. The narrow range of signatures found in higher DOC lakes suggests that different taxa have similar food sources and ⁄ or habitats. In contrast, the wide range of signatures in low-DOC lakes suggests that different taxa are exploiting different food sources and ⁄ or habitats. Together with the variable trends in zooplankton isotopic signatures along our DOC gradient, these results suggest that food web dynamics within the zooplankton community of temperate lakes will change as climate and lake DOC concentrations change.
Carbon Flow In the Littoral Food Web of An Oligotrophic Lake
Hydrobiologia, 2000
Benthic food web dynamics and carbon flow were examined in the littoral zone of Lake Coleridge, a large deep oligotrophic lake, using radioactive and stable isotope techniques in conjunction with analyses of stomach contents of the fauna. We specifically address two hypotheses: (1) that macrophytes only contribute to the carbon flow to higher trophic levels when they have decayed; and (2) that epiphytic algae is the major source of carbon for macroinvertebrates, and thus fish, with only minor contributions from phytoplankton or terrestrial sources. Epiphytic diatoms were a major component of the stomach contents of the gastropod snail Potamopyrgus antipodarum, and of chironomids. Animal remains were also common in the diet of some chironomids, while amorphous organic matter predominated in the stomachs of oligochaetes. A variety of epiphytic algal taxa was found in trichopteran larvae. Feeding rate of P. antipodarum measured with radioactive tracers increased by 10× on decayed macrophytes (Elodea) compared with live material, while feeding rates on characean algae increased by a factor of 3 when decayed material was presented. However, assimilation rates were less than 20% on decayed material compared with 48-52% on live material. Potential carbon sources were easily distinguished based on their δ 13 C values, although isotopic ratios showed significant variation among sites. Epiphytic algae showed less variation among sites than macrophytes and were depleted by 4-5‰ compared with macrophytes. Detrital material, organic matter in the sediments and plankton were significantly depleted in δ 13 C relative to macrophytes and slightly depleted relative to epiphytic algae. Most macroinvertebrate taxa showed a similar pattern among sites to macrophytes and epiphytic algae. P. antipodarum and chironomids were slightly enriched compared with epiphytic algae. Ratios for the common bully (Gobiomorphus cotidianus) were generally consistent with a diet dominated by chironomids, while there was some evidence for terrestrial inputs for koaro (Galaxias brevipinnis) and juvenile brown trout. Epiphytic algae appear to underpin much of the production in the littoral zone of this oligotrophic lake, with trichopteran and chironomid larvae mediating carbon flows from algae to fish. Macrophytes do not make a major contribution directly to carbon flow to higher trophic levels even when decayed. The lack of a direct link between macrophytes and higher trophic levels is due to the faunal composition, including a lack of large herbivores.
Advances in Marine Biology, 2004
We compare the nature of copepod outfluxes of nonliving matter, the factors controlling their rate and their fate, and finally their role, particularly their relative importance in the carbon and nitrogen cycle. Copepods release dissolved matter through excretion and respiration and particulate matter through production of faecal pellets, carcasses, moults, and dead eggs. Excretion liberates several organic C, N, and P compounds and inorganic N and P compounds, with inorganic compounds constituting the larger part. The faecal pellets of copepods are covered by a peritrophic membrane and have a highly variable size and content. There is less information on the nature of other copepod particulate products. The weight-specific rates of posthatch mortality, respiration, excretion, and faecal pellet production have similar C or N levels and are higher than those of moulting and egg mortality. In general, most important factors controlling these rates are temperature, body mass, food concentration, food quality, and faunistic composition. Physical and biological factors govern the vertical fate of copepod products by aVecting their sedimentation speed and concentration gradient. The physical factors are sinking speed, advection, stratification, turbulent diVusion, and molecular diVusion. They influence the sedimentation speed and degradation of the copepod products. The biological factors are production, biodegradation (by zooplankton, nekton, and microorganisms) and vertical migration of copepods (diel or seasonal). Physical degradation and biodegradation by zooplankton and nekton are faster than biodegradation by microorganisms. The most important copepod outfluxes are excretion and faecal pellet production. Excretion oVers inorganic nutrients that can be directly used by primary producers. Faecal pellets have a more important role in the vertical transport of elements than the other particulate products. Most investigation has focused on carbon burial in the form of copepod faecal pellets, measured by sediment traps, and on the role of ammonia excretion in nutrient recycling. Full evaluation of the role of copepod products in the transport and recycling of elements and compounds requires a quantification of all copepod products and their diVerent fates, particularly detritiphagy, remineralization, and integration as marine snow. 254 C. FRANGOULIS ET AL. closely linked, as nutrient and light availability drive the biogenic components of the carbon cycle. The oceans are likely to be a major sink for released anthropogenic carbon on a long-term basis (Wollast, 1991). Marine flora incorporate inorganic carbon into organic molecules, constituting 40% of the total organic carbon production of the earth, and 95% of this production is by phytoplankton (Duarte and Cebrian, 1996). The carbon entering the upper ocean can be transferred to deep waters via three pathways; a physical one (the solubility pump; i.e., the transport of inorganic and organic carbon by deep convection) and two biological ones (the carbonate pump and the biological CO 2 pump; i.e., active and passive vertical transport of biogenic particles; Sundquist, 1993). The biological CO 2 pump largely relies on zooplankton. Despite the small size of zooplankton organisms (mm to mm size scale), their total biomass is estimated to be greater than that of other marine consumers such as zoobenthos and zoonekton (Conover, 1978). Herbivorous zooplankters consume more than 40% of the phytoplankton production (Duarte and Cebrian, 1996, and references therein) and release into the surrounding water a variety of liquid and solid materials that contribute to the dissolved matter (DM) and particulate matter (PM), respectively. DM and PM can accelerate the vertical transport of carbon and nutrients to deep water. An important process accelerating vertical fluxes of phytoplankton organic matter is the compaction and packing of this matter into faecal pellets by herbivorous zooplankton (e.g., Smayda, 1971; Turner, 2002). The intensity of this process varies according to the faecal pellet and zooplankton characteristics as well as environmental factors, so that carbon and nutrients will either be rapidly transported out of the eutrophic zone or be recycled in their production zone (Turner, 2002). These diVerent fates of carbon and nutrients transported through zooplankton products highlight the ''switching'' role of zooplankton in the cycle of these elements. The fact that zooplankton can drive the carbon and nutrient cycles by recycling or export of their products makes study of the fates of these products necessary. Furthermore, zooplankton outfluxes give information on the fates of pollutants, as zooplankters can transport elements and unassimilated organisms (even still living) through the sinking of their products (Fowler and Fisher, 1983). Pollutants can be concentrated in these products and transferred by ingestion to other organisms (Fowler, 1977). Reviews already exist on zooplankton-dissolved products (Corner and