Allelopathy prevents competitive exclusion and promotes phytoplankton biodiversity

It has been hypothesized that allelopathy can prevent competitive exclusion and promote phytoplankton diversity in aquatic ecosystems, where numerous species coexist on a limited number of resources. However, experimental proof‐of‐principle is not available to support this hypothesis. Here we present the first experimental evidence to support this hypothesis by demonstrating that allelopathy promotes the coexistence of two phytoplankton species, Ankistrodesmus falcatus and Oscillatoria sp., that compete for a single limiting nutrient. By performing long‐term competition experiments in nitrate‐limited continuous cultures, and by describing the population dynamics using a mechanistic model, we demonstrate that when allelopathy comes into play, one of the following outcomes is possible depending on the relative initial abundances of the species: dominance of the stronger competitor for nitrate (the non‐allelopathic species), oscillatory coexistence, or dominance of the weaker competitor (the allelopathic species). Our model analysis revealed that sustained oscillatory coexistence of the two species would be a common outcome of this experiment. Our study confirms for the first time, based on laboratory experiments combined with mechanistic models, that allelopathy can alter the predicted outcome of inter‐specific competition in a nutrient‐limited environment and increase the potential for the coexistence of more species than resources, thereby contributing to the identification of endogenous mechanisms that explain the extreme diversity of phytoplankton communities.     

EFFECTS OF PHOTOCYCLES AND PERIODIC AMMONIUM SUPPLY ON THREE MARINE PHYTOPLANKTON SPECIES. I. CELL DIVISION PATTERNS1

Cell division patterns in Thalassiosira weissflogii (Grun.), Hymenomonas carterae (Braarud and Fagerl), and Amphidinium carteri (Hulburl) grown in cyclostat culture were analyzed as functions of the periodic supply of light and the limiting nutrient (ammonium) and of combinations of these two factors. In all three species, division patterns were phased by light/dark cycles in N–limited as well as N–replte conditions, and also to ammonium pulses in N–limited growth in continuous light. Both the degree and timing of the cell cycle phasing varied among species. When both stimuli were present, the influence of the photocycle overrode the N–pulse stimulus in H. carterae and A. carteri. while in T. weissflogii, division was always phased by the timing of the N–pulse regardless of the phase angle between the photocycle and the pulse.     

Biomass recycling and species competition in continuous cultures

A chemostat with cell feedback is analyzed for three kinds of limiting nutrient: a substrate dissolved in the inflow, a gas bubbled directly into the reactor, and light. The effects of recycle are distinct in each case, because the relationships between hydraulic detention time and nutrient inflow are different for each type of nutrient, Effluent recycle, in which the recycle stream is more dilute than the reactor, is discussed in terms of cell detention time and nutrient limitation. Results from chemostat cultures of the blue-green alga, Spirulina geitleri, demonsrtat cell feedback under light limitation. Maximum Productivity is fixed by the incident light intensity. At a particular dilution rate recycling increases or decreases productivity by taking cell density closer or further from the optimum density. Cell recycle with heterogeneous populations can change the outcome of species competition. Selective recycling of one species can reverse this outcome or stabilize coexistence by its selective effect on cell detention time. Experimental results from light-limited mixed cultures of S. geitleri and a Chlorella sp. verify this.     

IMPORTANCE OF RESTING STAGES IN DIATOM SEASONAL SUCCESSION1

The role of environmental factors in seasonal succession of six clones of marine diatoms was examined by testing effects of various combinations of temperature (5°, 10°, 15°, 20°C) and photoperiod (10, 12, 14, 16 h) on time to germination of resting stages and subsequent vegetative cell division rates. Resting stages were induced in batch cultures using a low nutrient medium and a cold, dark period. A three-factor ANOVA showed that species, temperature, daylength, and their interactions signficantly (P =0.0001) injuenced germination time and division rate. Resting stages of Chaetoceros similis Cleve and Odontella aurita (Lyngbye) Agardh were most successful in producing populations of cells on warm, long days (20°C/16 h). Chaetoceros didymus Ehrenberg and C. cinctus Gran were most successful under more moderate conditions (15°C/14 h). Resting stages of Ditylum bright-wellii (West) Grunow germinated and cells divided rapidly under all conditions. No consistent pattern was evident with Thalassiosira rotula Meunier. We compared results of the laboratory study with environmental conditions prevailing during the presence of these species in a British Columbia fjord. Favorable growth conditions determined for C. didymus, D. brightwellii, and T. rotula were similar to conditions present when these species were commonly found in the fjord.     

Physiological responses of two marine diatoms to pulsed additions of ammonium

The effects of pulsed ammonium additions on the ammonium-limited marine diatoms, Chaetoceros gracile Schutt and Skeletonema costatum (Grev.) Cleve were studied. Two culture systems were maintained for each species. One culture was grown in a chemostat which provided a homogeneous distribution of the limiting nutrient. In the other continuous culture, ammonium was added once daily giving rise to a patchy distribution. Ammonium patchiness increased both the V'_max (from 4.1 ± 0.3 to 11.8 ± 0.9 · h^?1) and the V_i (from 0.19 ± 0.02 to 0.36 ± 0 0.04 · h^?1) for ammonium in S. costatum and the V'_max (from 0.91 ± 0.07 to 2.9 ± 0 0.2 · h^?1) and the V_i (from 0.16 ± 0.01 to 0.31 ± 0.05 · h^?1) for ammonium in Chaetoceros gracile. The once-per-day addition of ammonium also induced a diel periodicity in photosynthetic rate and fluorescence although these cultures were growing under continuous light. The relative amplitude of the periodicity was greater for Skeletonema than for Chaetoceros. These observations are considered with regard to the hypothesis that limiting nutrient patchiness may alter the growth kinetics of marine phytoplankton.     

Nutrient limitation of phytoplankton in a naturally acidic lake (Lake Caviahue, Argentina)

As a result of a low pH, the inorganic carbon of acidic lakes is present as CO₂ at air-equilibrium concentration and is substantially lower than the inorganic carbon concentration in higher-pH waters with bicarbonate. This situation is quite common in artificially acidified lakes and where inorganic carbon is considered the limiting factor in phytoplankton growth. Apart from low inorganic carbon content, Lake Caviahue in Argentina has low nitrogen and high phosphorus content. The aim of this work was to assess the importance of inorganic carbon, phosphorus, and nitrogen, relating data on lake nutrients to phytoplankton species requirements. Lake samples taken in the 2004–2006 period did not show any particular trend in the vertical distribution of the water column of ammonium, inorganic carbon, and phosphorus with reference to either seasonality or depth. A decrease of some 15% in the lake’s phosphorus concentration was observed over the same period. Although the total phytoplankton biomass in Lake Caviahue was similar throughout the period, a seasonal variation was observed. Lab bioassays were carried out with solutions of bicarbonates, ammonium, nitrates, and phosphate. We worked with three species separately, namely, two chlorophytes, Keratococcus rhaphidioides and Watanabea sp.; and one euglenophyte, Euglena mutabilis. Answers to specific nutrient requirements differed for each algal species: both chlorophytes prefer ammonium or nitrates added on their own, whereas the euglenophyte registered a higher growth rate with the joint addition of ammonium and phosphorus. Even when the limiting nutrient(s) for phytoplankton yield and rate varied between species, we observed a tendency for nitrogen limitation in Lake Caviahue.     

Variation in species light acquisition traits under fluctuating light regimes: implications for non‐equilibrium coexistence

Resource distribution heterogeneity offers niche opportunities for species with different functional traits to develop and potentially coexist. Available light (photosynthetically active radiation or PAR) for suspended algae (phytoplankton) may fluctuate greatly over time and space. Species‐specific light acquisition traits capture important aspects of the ecophysiology of phytoplankton and characterize species growth at either limiting or saturating daily PAR supply. Efforts have been made to explain phytoplankton coexistence using species‐specific light acquisition traits under constant light conditions, but not under fluctuating light regimes that should facilitate non‐equilibrium coexistence. In the well‐mixed, hypertrophic Lake TaiHu (China), we incubated the phytoplankton community in bottles placed either at fixed depths or moved vertically through the water column to mimic vertical mixing. Incubations at constant depths received only the diurnal changes in light, while the moving bottles received rapidly fluctuating light. Species‐specific light acquisition traits of dominant cyanobacteria (Anabaena flos‐aquae, Microcystis spp.) and diatom (Aulacoseira granulata, Cyclotella pseudostelligera) species were characterized from their growth–light relationships that could explain relative biomasses along the daily PAR gradient under both constant and fluctuating light. Our study demonstrates the importance of interspecific differences in affinities to limiting and saturating light for the coexistence of phytoplankton species in spatially heterogeneous light conditions. Furthermore, we observed strong intraspecific differences in light acquisition traits between incubation under constant and fluctuating light – leading to the reversal of light utilization strategies of species. This increased the niche space for acclimated species, precluding competitive exclusion. These observations could enhance our understanding of the mechanisms behind the Paradox of the Plankton.     

ALLELOPATHIC GROWTH INHIBITION OF SELECTED PHYTOPLANKTON SPECIES BY SUBMERGED MACROPHYTES1

Allelopathic effects of submerged macrophytes on the growth and photosynthesis of different unialgal cultures of planktonic cyanobacteria, a diatom, and a green alga were tested in coexistence experiments using dialysis cultures. The method applied allowed measurements under conditions similar to that in lakes but without nutrient and light limitation. Growth and photosynthesis were measured with a pulse amplitude modulated fluorometer as an increase of chl a fluorescence and activity of PSII, respectively. Eurasian water milfoil Myriophyllum spicatum L. and rigid hornwort Ceratophyllum demersum L. proved to inhibit the PSII activity and then growth of the investigated phytoplankton species, whereas sago pondweed Potamogeton pectinatus L. showed no effect. Growth inhibition was dependent on biomass of M. spicatum. Considerable differences between phytoplankton groups and among species of cyanobacteria were found regarding their response to M. spicatum. Members of the Oscillatoriales and Microcystis aeruginosa Kütz. emend. Elenkin were more sensitive than the cyanobacterium Aphanizomenon flos‐aquae Ralfs ex Born. et Flah., the diatom Stephanodiscus minutulus (Kütz) Cleve et Möller, and the green alga Scenedesmus armatus Chodat. A possible contribution of this result to changes in the phytoplankton succession of lakes after loss of macrophytes is discussed.     

Size scaling of photophysiology and growth in four freshly isolated diatom species from Ryder Bay,western Antarctic peninsula

Diatoms are one of the dominant groups in phytoplankton communities of the western Antarctic Peninsula (WAP). Although generally well‐studied, little is known about size dependent photophysiological responses in diatom bloom formation and succession. To increase this understanding, four Antarctic diatom species covering two orders of magnitude in cell size were isolated in northern Marguerite Bay (WAP). Fragilariopsis sp., Pseudo‐nitzschia cf. subcurvata, Thalassiosira cf. antarctica, and Proboscia cf. alata were acclimated to three different irradiances after which photophysiology, electron transport, carbon fixation, and growth were assessed. The small species Fragilariopsis sp., Pseudo‐nitzschia cf. subcurvata, and large species Proboscia cf. alata showed similar photoacclimation to higher irradiances with a decrease in cellular chlorophyll a and an increase in chlorophyll a specific absorption and xanthophyll cycle pigments and activity. In contrast, pigment concentrations and absorption remained unaffected by higher irradiances in the large species Thalassiosira cf. antarctica. Overall, the small species showed significantly higher growth rates compared to the large species, which was related to relatively high light harvesting capacity and electron transport rates in the smaller species. However, photophysiological responses related to photoinhibition and photoprotection and carbon fixation showed no relationship with cell size. This study supports the dominance of small diatoms at low irradiances during winter and early spring, but does not provide photophysiological evidence for the dominance of large diatoms during the phytoplankton bloom in the WAP. This suggests that other factors such as grazing and nutrient availability are likely to play a major role in diatom bloom formation.     

Allelopathic effects of Alexandrium fundyense (Dinophyceae) on Thalassiosira cf. gravida (Bacillariophyceae): a matter of size

Allelopathic interactions among phytoplankton are well documented. The potency of allelopathic species and responses of target species to allelochemicals are quite variable, however, limiting full understanding of the role these interactions may play in nature. One trait that may influence the sensitivity of an individual to allelochemicals is cell size. The few studies that have examined relationships between cell size and susceptibility to allelochemicals have compared different species and thus could not distinguish between the role of size and species‐specific physiological differences. Culturing an actively sexually reproducing diatom allowed us to focus on the influence of target cell size within a single species. We studied growth and nutrient acquisition by the chain‐forming Thalassiosira cf. gravida Clever in the presence and absence of allelochemicals released by Alexandrium fundyense Balech as a function of T. cf. gravida cell size. Upon exposure to filtrate of A. fundyense, T. cf. gravida cultures “bleached” and both growth and nutrient utilization ceased for up to 4 d. The magnitude of the effect was dependent on filtrate concentration and T. cf. gravida cell surface area:volume ratio. The greatest inhibition was observed on the smallest cells, while T. cf. gravida cultures that had undergone cell enlargement via sexual reproduction were least sensitive to A. fundyense filtrate. These results demonstrate that competitor cell size, independent from taxonomy, may influence the outcome of allelopathic interactions. The findings presented here suggest a potential ecological impact of diatom cell size reduction and sexual reproduction that has not yet been described and that may be important in determining diatom survival and success.     

SOME FACTORS IN THE COMPETITION OR ANTAGONISM AMONG BACTERIA, ALGAE, AND AQUATIC WEEDS

Field observations of changes in the populations of aquatic weeds and phytoplankton have confirmed that aquatic weeds have antagonistic activity toward phytoplankton. Nutritional studies in the laboratory indicate that cultures of the aquatic weeds, Myriophyllum sp., Ceratophyllum sp., and duckweed (Lemma minor L.); liquid cultures of barley (Hordeum vulgare L., Dickson variety); and cultures of the filamentous green algae, Cladophora sp. and Pithophora oedogonium (Mont.) Withrock, will remain relatively free of epiphytes or competing phytoplankton if the cultures are nitrogen-limited. Field observations of Cladophora sp. have confirmed that the growth of epiphytes on the Cladophora is related to conditions of surplus available nitrogen compounds. It is proposed that this antagonistic activity may be due to a “nitrogen sink” effect in which the aquatic weeds or filamentous green algae prevent the growth of contaminating algae by competition for the limited nitrogen compounds available. However, the presence of bacteria-sized organisms which have selective toxicity to certain algae indicates that perhaps multiple factors exist. Discussed are the ecological implications of associations of certain algae with bacteria that have selective toxicities for other species of algae under certain environmental conditions such as nitrogen-limited growth.     

Species-specific differences in phytoplankton responses to N and P enrichments and the N:P ratio in the Archipelago Sea, northern Baltic Sea

A nutrient enrichment experiment was conducted in order to studythe role of nitrogen (N), phosphorus (P) and the N:P ratio onthe early summer phytoplankton community in the ArchipelagoSea, northern Baltic Sea. The phytoplankton community was, interms of chlorophyll a and total biomass, primarily N-limited,but the individual species varied in their responses to thenutrient supply. The recorded overall N limitation was due tofast growth responses of a few N-limited species such as thediatom Chaetoceros wighamii (Brightwell) and the mixotrophicchrysophyte Uroglena sp. Another dominating diatom, Skeletonemacostatum (Greville) Cleve was most clearly P-limited. The N:Pratio had the strongest effect on Uroglena sp., which grew exponentiallyin the enrichments with a high N:P ratio. This can be explainedby the ability of the species to feed on P-rich bacteria, whichgives it a competitive advantage in P-limited conditions. Thespecies-specific differences in the responses to the nutrientenrichments can generally be explained by differences in thespecies physiology and they were consistent with the theoryof resource competition.     

Limiting nutrient patchiness and its rôle in phytoplankton ecology

Limiting nutrient patchiness is examined as a factor affecting the community structure and species succession of natural phytoplankton communities held in ammonia limited continuous culture at a dilution rate of 0.3 day^?1. It was found that under a homogeneous distribution of the limiting nutrient members of genus Chaetoceros dominated and when ammonia was added daily (patchy distribution), Skeletonema dominated. Intermediate patchiness gave rise to an assemblage dominated by both Chaetoceros and Skeletonema. The nutrient uptake ability of each assemblage was determined three weeks after experiment initiation. Each assemblage was best able to optimize uptake of ammonia under its particular patchy nutrient regime. Optimization of a patchy environment took place by an increased maximal uptake rate (V_max) while optimization of a homogeneous environment appeared to take place by increased substrate affinity (i.e., low K_s).This study demonstrates that limiting nutrient patchiness can alter the relative abundance of populations within a community based on each population's ability to exploit the limiting resource under a particular degree of patchiness. We also show that coexistence of two populations might be expected due to the patchiness of a single limiting nutrient. The importance of patchiness in relation to other factors which determine community structure is discussed.     

Enclosure Experiments with Low-dose Additions of Phosphorus and Nitrogen in the Acidified Lake Njupfatet,Central Sweden

Experiments involving low-dose additions of phosphate, ammonium, nitrate and ADP, one by one and in combination, were performed in small (350 litre) in-situ enclosures in a moderately acid (pH 5.4) lake. Before manipulation, all large filter-feeding animals were removed by filtration. Phytoplankton responded to the nutrient additions only when both phosphorus and nitrogen were added, thus indicating a close balance between phosphorus and nitrogen limitation in the system. Variation of the inorganic nitrogen-source resulted in species-specific responses by phytoplankton. With ammonium as the nitrogen source Merismopedia tenuissima was favoured, regardless of whether this species was dominant in the phytoplankton community at the beginning of the experiment or not. With nitrate as nitrogen source Peridinium inconspicuum, which was never particularly common at the beginning of the experiments, was favoured. No other species of phytoplankton present in the bags was able to outcompete these two species as long as inorganic nutrients were added. With ADP as phosphorus source together with nitrate, a third species, Dictyosphaerium cf. botrytella, was favoured and reached dominance. The zooplankton community remaining in the bags, dominated by rotifers and calanoid nauplii, did not respond to the fertilization-induced increases in the total biomass of phytoplankton.     

Responses of Phytoplankton to in‐situ Nutrient Enrichment; Potential Influences on Species Dominance in a River

The Hawkesbury River at Sackville, New South Wales, Australia is fresh and vigorously mixed by tidal movement. The location has frequent blooms of Microcystis aeruginosa, which have been recorded occurring throughout the year, including winter temperatures as low as 13 °C. Nutrient enrichment tests were performed in‐situ on the natural phytoplankton population in 1997 and 1998 while Microcystis aeruginosa dominated (covering both summer and winter periods). These experiments compared population changes under the ambient nutrient regime with those after additions of ortho‐phosphate, nitrate, ammonia and various combinations of these nutrients. Under ambient conditions, the Microcystis population was able to grow significantly (P < 0.05) while most non‐cyanobacterial phytoplankton did not. Nutrient additions induced a variety of nutrient limitation responses that often varied between genera of major groups i.e. in the Chlorophyceae (Actinastrum sp. responded to phosphorus while Psephonema sp. responded to nitrogen). The possibility that shifts in population dominance from Chlorophyceae to the Cyanobacteria (M. aeruginosa) at Sackville are in response to competition for limiting nutrients is discussed.     

Nitrogen as a Factor Affecting Algal Growth Potential of an Oligotrophic Coastal Environment of Eastern Mediterranean Sea

Potential nitrogen limitation to chl a production in surface waters of Saronicos Gulf, Aegean Sea was assayed using the alga Pavlova lutheri as the test organism. The oligotrophic and eutrophic water types of this area were compared by in situ and in vitro chl a production estimations. Additions of ammonium alone as well as in combination with complete nutrient enrichment were made to the oligotrophic waters and the algal growth yield was determined and compared with the corresponding yield in unenriched water cultures. The results from routine nutrient analysis and bioassay experimentation support the view that nitrogen has a priority among the factors limiting phytoplankton growth in the Eastern Mediterranean Sea.     

INTERACTIONS OF PHYTOPLANKTERS CULTURED FROM A POLLUTED SALINE LAKE,ONONDAGA LAKE,NEW YORK1,2,3

Two-membered cultures of 3 phytoplankters isolated from Onondaga Lake, grown in defined media under laboratory conditions, were analyzed by electronic particle counts and statistical methods to determine antagonistic, neutral, or stimulatory relationships. Over the range studied (exponential phase of growth, nutrients not limiting), growth of Staurastrum paradoxum is markedly reduced in the presence of Chlamydomonas sp. Growth of Chlamydomonas is not affected by presence of Staurastrum. The initial concentration of Staurastrum has an effect on its subsequent growth. The initial concentration of Chlamydomonas does not have an effect on its subsequent growth nor that of Staurastrum. These effects are not mediated by a filterable factor (unless highly labile) or by competition for a nutrient. They resemble, and perhaps describe, fluctuations of these species in the lake.     

The influence of copepod and krill grazing on the species composition of phytoplankton communities from the Scotia Weddell sea

The influence of copepods (mainly Oithona sim-ilis) and krill (Euphausia superba) grazing on the species composition of plankton communities in ship board con tainers was investigated during the spring and post spring period in the Scotia Weddell Sea in the Antarctic ocean. Numbers of grazers were experimentally manipulated in containers with natural phytoplankton assemblages. With ratural levels of copepods but no krill a high (700–950 g C·l¹, ca 30 g chl a·.l¹) phytoplankton biomass developed. In these cultures large diatoms, e.g. Corethron criophilum and chains of Thalassiosira sp., made up 80% of total phytoplankton cell carbon at the end of the experiment. In cultures with elevated numbers of copepods (5X or 10X the natural level) phytoplankton biomass was somewhat reduced (ca 23 g chl a · l¹) compared to cultures with natural copepod abundance, but still high. Phytoplankton species composition was on the other hand greatly influenced. Instead of large diatoms these cultures were dominated by Phaeocystis pouchetii (70%) together with small Nitszchia sp. and Chaetoceros neogracile (20%). In containers with krill (both juveniles and adults), but without elevated numbers of copepods, phytoplankton biomass rapidly approached zero. With 10X the in situ level of copepods, krill first preyed on these before Corethron criophilum and Thalassiosira sp. were grazed. When krill were removed a plankton community dominated by flagellates (60–90%), e.g. Pyramimonas sp. and a Cryptophycean species, grazed by an unidentified droplet-shaped heterothrophic flagellate, developed. These flagellates were the same as those which dominated the plankton community in the Weddell Sea after the spring bloom. A similar succession was observed in situ when a krill swarm grazed down a phytoplankton bloom in a few hours. Our experiments show that copepods cannot control phytoplankton biomass in shipboard cultures even at artificially elevated numbers. Krill at concentrations similar to those in natural swarms have a great impact on both phytoplankton biomass and species composition in shipboard cultures. Both copepods and krill may have an impact on phytoplankton species composition and biomass in situ since the rates of phytoplankton cell division were probably artificially increased in shipboard cultures compared to natural conditions, where lower growth rates make phytoplankton more vulnerable to grazing. A similarity between phytoplankton successions in containers and in situ, especially with respect to krill grazing, supports the conclusion that grazing may structure phytoplankton communities in the Scotia-Weddell Sea.Data presented here were collected during the European Polarstern Study (EPOS) sponsored by the European Science Foundation     

The effects of initial population density on the competition for limiting nutrients in two freshwater algae

Eighteen long-term competition experiments were performed on two freshwater algae, a blue-green alga, Anabaena flos-aquae, and a diatom, Cyclotella sp., under controlled light and temperature conditions and various nutrient limitations. As predicted, Anabaena displaced Cyclotella when nitrate was in short supply to both species, whereas Cyclotella became dominant when both species were phosphate-limited. The two species stably coexisted when phosphate and silicate were limited. Anabaena either displaced or coexisted with Cyclotella when nitrate and phosphate or nitrate, phosphate and silicate were limited, depending on their initial density ratios. This study revealed strong effects of initial population densities on the outcomes of algal competition for limiting nutrients.     

Some Factors Influencing the Diversity and Species Composition of Benthic Invertebrate Communities in Twenty Arctic and Subarctic Lakes

The factors influencing the density, diversity and species composition of benthic invertebrate communities in 20 lakes in the Canadian arctic and subarctic were determined during 1975, 1976 and 1977. Despite small differences in nutrient and phytoplankton levels among the lakes, there was a strong positive correlation between these parameters and the density and diversity of the communities. Other factors, including maximum summer water temperature, lake depth and surface area had little overall effect on the communities. The densities of 2 ultra-oligotrophic chironomids (Heterotrissocladius oliveri and Micropsectra cf. groenlandica) increased markedly in cold deep lakes. However the abundance of the majority of species, most notably Procladius denticulatus, Tanytarsus sp., and Stictochironomus sp., was not effected by temperature. Other species, (Pontoporeia affinis, Monodiamesa bathyphila and Dicrotendipes nervosus) were probably restricted in their northern distribution by temperature. Surface area usually had little effect on the densities of all common species.