Elanor M. Bell

Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs

The majority of organisms can be grouped into those relying solely on photosynthesis (phototrophy) or those relying solely on the assimilation of organic substances (heterotrophy) to meet their requirements for energy and carbon. However, a special life history trait exists in which organisms combine both phototrophy and heterotrophy. Such “mixotrophy” is a widespread phenomenon in aquatic habitats and is observed in many protozoan and metazoan organisms. The strategy requires investment in both photosynthetic and heterotrophic cellular apparatus, and the benefits must outweigh these costs. In accordance with mechanistic resource competition theory, laboratory experiments revealed that pigmented mixotrophs combined light, mineral nutrients, and prey as substitutable resources. Thereby, they reduced prey abundance below the critical food concentration of competing specialist grazers [Rothhaupt, K. O. (1996) Ecology 77, 716–724]. Here, we demonstrate the important consequences of this strategy for an aquatic community. In the illuminated surface strata of a lake, mixotrophs reduced prey abundance steeply. The data suggest that, as a consequence, grazers from higher trophic levels, consuming both the mixotrophs and their prey, could not persist. Thus, the mixotrophs escaped from competition with and losses to higher grazers. Furthermore, the mixotrophs structured prey abundance along the vertical light gradient, creating low densities near the surface and a pronounced maximum of their algal prey at depth. Such deep algal accumulations are typical features of nutrient-poor aquatic habitats, previously explained by resource availability. We hypothesize instead that the mixotrophic grazing strategy is responsible for deep algal accumulations in many aquatic environments.

The ups and downs of benthic ecology: considerations of scale, heterogeneity and surveillance for benthic–pelagic coupling

Dave Raffaelli*, Elanor Bell, Guntram Weithoff, Asako Matsumoto, Juan Jose Cruz-Motta, Pete Kershaw, Ruth Parker, Dave Parry, Malcolm Jones Environment Department, University of York, Heslington, York YO10 5DD, UK b Institute for Biochemistry and Biology, University of Potsdam, Maulbeerallee 2, 14469 Potsdam, Germany Marine Ecosystems Research Department, Japan Marine Science and Technology Centre, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories, University of Sydney, Sydney NSW 2006, Australia The Centre for Fisheries, Environment and Aquaculture Science, Lowestoft Laboratory, Pakefield Road, Lowestoft NR33 0HT, UK Plymouth Environmental Research Centre, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK

MIXOTROPHY IN THE ANTARCTIC PHYTOFLAGELLATE, PYRAMIMONAS GELIDICOLA (CHLOROPHYTA: PRASINOPHYCEAE)1

Grazing by the planktonic phytoflagellate, Pyramimonas gelidicola McFadden (Chlorophyta: Prasinophyta), and heterotrophic nanoflagellates (HNAN) in meromictic saline Ace Lake in the Vestfold Hills, eastern Antarctica was investigated in the austral summers of 1997 and 1999. Up to 47% of the P. gelidicola population ingested fluorescently labeled prey (FLP). Ingestion rates varied with depth. In January 1997 and November 1999, maximum P. gelidicola ingestion rates of 6.95 and 0.79 FLP·cell−1·h−1, respectively, were measured at the chemocline (6–8 m) where a deep chl maximum composed of phototrophic nanoflagellates (PNAN DCM), predominantly P. gelidicola, persisted all year. During the summers of 1997 and 1999, the grazing P. gelidicola community removed between 0.4% and approximately 16% of in situ bacterial biomass, equivalent to between 4% and>100% of in situ bacterial production. Because of their higher abundance, the community clearance rates of HNAN in Ace Lake generally exceeded those of P. gelidicola, but HNAN removed approximately only 3%–4% of bacterial biomass, equivalent to between 28% and 32% of bacterial production. Pyramimonas gelidicola growth rates were highest at the PNAN DCM concomitant with the highest ingestion rates. It is estimated that during the summer P. gelidicola can derive up to 30% of their daily carbon requirements from bacterivory at the PNAN DCM. This study confirms mixotrophy as an important strategy by which planktonic organisms can survive in extreme, polar, lacustrine ecosystems.

Strong vertical differences in the plankton composition of an extremely acidic lake

Vertical differences in food web structure were examined in an extremely acidic, iron-rich mining lake in Germany (Lake 111; pH 2.6, total Fe 150 mg L -1 ) during the period of stratification. We tested whether or not the seasonal variation of the plankton composition is less pronounced than the differences observed over depth. The lake was strongly stratified in summer, and concentrations of dissolved organic carbon and inorganic carbon were consistently low in the epilimnion but high in the hypolimnion. Oxygen concentrations declined in the hypolimnion but were always above 2 mg L -1 . Light attenuation did not change over depth and time and was governed by dissolved ferric iron. The plankton consisted mainly of single-celled and filamentous bacteria, the two mixotrophic flagellates Chlamydomonas sp. and Ochromonas sp., the two rotifer species Elosa worallii and Cephalodella hoodi, and Heliozoa as top predators. We observed very few ciliates and rhizopods, and no heterotrophic flagellates, crustaceans or fish. Ochromonas sp., bacterial filaments, Elosa and Heliozoa dominated in the epilimnion whereas Chlamydomonas sp., single-celled bacteria and Cephalodella dominated in the hypolimnion. Single-celled bacteria were controlled by Ochromonas sp. whereas the lack of large consumers favoured a high proportion of bacterial filaments. The primarily phototrophic Chlamydomas sp. was limited by light and CO 2 and may have been reduced due to grazing by Ochromonas sp. in the epilimnion. The distribution of the primarily phagotrophic Ochromonas sp. and of the animals seemed to be controlled by prey availability. Differences in the plankton composition were much higher between the epilimnion and hypolimnion than within a particular stratum over time. The food web in Lake 111 was extremely species-poor enabling no functional redundancy. This was attributed to the direct exclusion of species by the harsh environmental conditions and presumably enforced by competitive exclusion. The latter was promoted by the low diversity at the first trophic level which, in turn was attributed to relatively stable growth conditions and the independence of resource availability (inorganic carbon and light) from algal density. Ecological theory suggests that low functional redundancy promotes low stability in ecosystem processes which was not supported by our data.

Benthic recruitment of zooplankton in an acidic lake

In recent years, most studies of the benthic microbial food web have either been descriptive or were restricted to the measurement of within sediment process rates. Little is known about benthic–pelagic coupling processes such as recruitment. We, therefore, developed an ex situ core incubation procedure to quantify the potential for microbial recruitment from the benthos to the pelagic in an acidic mining lake, Mining Lake 111 (ML 111; pH 2.6), in eastern Germany. Our data suggest that considerable zooplankton recruitment from the benthos takes place. Heliozoan and rhizopod recruitment in both summer and winter sediment cores was highest when they were incubated at 20 °C. Maximum heliozoan recruitment was 23 (±9 S.E.) individuals cm−2 day−1 (40% initial standing stock daily) in the winter 20 °C incubation. Maximum rhizopod recruitment was 6 (±2 S.E.) individuals cm−2 day−1 in the summer 20 °C incubation. Little or no recruitment was apparent for either taxa when winter cores were incubated at 5 °C, implying a temperature cue. Conversely, the rotifer, Cephalodella hoodi, exhibited a maximum recruitment of 6 (±2 S.E.) individuals cm−2 day−1 during the winter 5 °C incubation, representing 30% of initial standing stock daily, but little recruitment when incubated at 20 °C. Cephalodella may have responded to an increased winter benthic food supply; in situ winter Chl a concentrations in the benthos were 3.4 times higher than those in the summer. The importance of this was reinforced by the poor pelagic food supply available in ML 111. In situ, Heliozoa, rhizopods and Cephalodella were first observed in the epilimnion of ML 111 in spring or early summer, suggesting active or passive recruitment following lateral transport from littoral sediments. Benthic–pelagic coupling via recruitment is potentially important in understanding the pelagic food web in ML 111 and warrants further investigation in this and other aquatic environments.

Detection of a novel ecotype of Pfiesteria piscicida (Dinophyceae) in an Antarctic saline lake by real-time PCR

The heterotrophic dinoflagellate Pfiesteria piscicida was detected in Ace Lake in the Vestfold Hills, eastern Antarctica by using real-time PCR based on 18S rDNA sequences. Antarctic water samples collected in 2004 were tested by species-specific real-time PCR assays for the identification of P. piscicida and P. shumwayae. Positive results were shown with P. piscicida-specific real-time PCR, and PCR products were examined by sequence analysis for confirmation. A phylogenetic tree made from partial 18S rDNA sequences showed that the Antarctic clone clustered with P. piscicida. This result suggests that P. piscicida is present in the extreme conditions of an Antarctic saline lake which has not contained fish for thousands of years.