Dietary specialization and infochemical use in carnivorous arthropods: testing a concept

For the location of hosts and prey, insect carnivores (i.e., parasitoids or predators) often use infochemical cues that may originate from the host/prey itself but also from the food of the host/prey, a food plant, or another feeding substrate. These cues can be either specific for certain host/prey complexes or generally present in various complexes, and the reaction of the carnivores to these cues is either innate or learned. According to the concept on dietary specialization and infochemical use in natural enemies, the origin and specificity of the infochemical cues used and the innateness of the behavioural response are dependent on the degree of dietary specialization of the carnivore and its host/prey species. This concept has been widely adopted and has been frequently cited since its publication. Only few studies, however, have been explicitly designed to test predictions of the concept. Thus, more than 10 years after publication and despite of its broad acceptance, the general validity of the concept is still unclear. Using data from about 140 research papers on 95 species of parasitoids and predators, the present literature study comparatively scrutinises predictions from the concept. In accordance with the concept, learning to react to infochemicals and the use of general host and host plant cues was more often found in generalists than in specialists. In addition, more specialists were using specific infochemicals than generalists. In contrast to the concept, however, there was no significant difference between specialists and generalists in the proportion of carnivore species that use infochemicals during foraging and also extreme generalists are using infochemical cues for foraging. Likewise, an innate reaction to infochemicals was found in both specialists and generalists. Several reasons why infochemical use, including an innate reaction to infochemicals, is adaptive in generalist carnivores are discussed . We conclude that the concept has been a useful paradigm in advancing the chemical ecology of arthropod carnivores, but needs to be modified: the use of infochemicals is expected in all arthropod carnivores, regardless of dietary specialization.     

海洋微型浮游动物对浮游植物和初级生产力的摄食压力

综述了国际上研究微型浮游动物对浮游植物和初级生产力摄食的方法,并重点介绍了稀释法的理论和在实践中遇到的问题。各种方法的微型浮游动物对浮游植物和初级生产力摄食压力的估计表明,微型浮游动物在海洋生态系统中的扮演重要角色。     

Grazing impact of micro- and mesozooplankton during a spring situation in coastal waters off the Gironde estuary

The aim of this study was to characterize the grazing link betweenphytoplankton and zooplankton. Quantifying rates of phytoplanktonutilization by micro- and mesozooplankton is an attempt to understandthe control of phytoplankton populations in marine ecosystemsand the export flux of organic matter to the depths. Sampleswere taken in the plume of dilution of the Gironde estuary duringspring (May 1995). The mesozooplankton community was dominatedby the heterotrophic dinoflagellate Noctiluca scintillans andby copepods. Our estimates showed that on average, 26% of thetotal primary production was grazed daily by mesozooplankton.However, the pressure exerted by microzooplankton on the primaryproduction was estimated to be approximately four times higher.As a consequence, during this spring situation in the plumeof dilution of the Gironde estuary when small cells dominated,microzooplankton represented the most important grazing communityand could potentially control the growth of phytoplankton.     

东海春季水华期浮游植物生长与微型浮游动物摄食

2005年4～6月在东海有害水华频发区14个站位采样,通过现场稀释法实验对春季东海水域浮游植物比生长率和微型浮游动物比摄食率进行了研究.结果表明东海有害水华频发区浮游植物群落以甲藻为优势.浮游植物比生长率在水华爆发前相对较低,平均为1.18 d~(-1);进入水华期后比生长率明显升高,但在水华站位随现存量增加而降低;非水华区比生长率近岸高、远岸低.微型浮游动物主要以急游虫和桡足类幼体为主,而种类上以砂壳纤毛虫居多.微型浮游动物比摄食率在水华爆发前波动较大,介于0.53～1.73 d~(-1),平均为0.90 d~(-1);在水华区比摄食率较为稳定,浮游植物比生长率的降低导致群落净生长率持续下降;在非水华区,比摄食率整体较高,近岸低而远岸高.微型浮游动物的摄食对浮游植物群落的生长有一定的控制作用,但在水华爆发后这种控制作用将减弱.     

TROPHIC INTERACTIONS IN THE SEA: AN ECOLOGICAL ROLE FOR CLIMATE RELEVANT VOLATILES?1

When attacked by herbivores, land plants can produce a variety of volatile compounds that attract carnivorous mutualists. Plants and carnivores can benefit from this symbiotic relationship, because the induced defensive interaction increases foraging success of the carnivores, while reducing the grazing pressure exerted by the herbivores on the plants. Here, we examine whether aquatic phytoplankton use volatile chemical cues in analogous tritrophic interactions. Marine algae produce several classes of biogenic gases such as non‐methane hydrocarbons, organohalogens, ammonia and methylamines, and dimethylsulfide. The grazing‐induced release of marine biogenic volatiles is poorly understood, however, and its effect on the chemical ecology of plankton and the foraging behavior of predators is essentially unknown. We outline grazing‐induced defenses in algae and highlight the biogenic production of volatiles when phytoplankton are attacked by herbivores. The role of chemical signaling in marine ecology presents several possible avenues for future research, and we believe that progress in this area will result in better understanding of species competition, bloom development, and the structuring of food webs in the sea. This has further implications for biogeochemical cycles, because several key compounds are emitted that influence the chemistry of the atmosphere and global climate.     

Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea

Understanding the processes that regulate phytoplankton biomass and growth rate remains one of the central issues for biological oceanography. While the role of resources in phytoplankton regulation (`bottom up' control) has been explored extensively, the role of grazing (`top down' control) is less well understood. This paper seeks to apply the approach pioneered by Frost and others, i.e. exploring consequences of individual grazer behavior for whole ecosystems, to questions about microzooplankton–phytoplankton interactions. Given the diversity and paucity of phytoplankton prey in much of the sea, there should be strong pressure for microzooplankton, the primary grazers of most phytoplankton, to evolve strategies that maximize prey encounter and utilization while allowing for survival in times of scarcity. These strategies include higher grazing rates on faster-growing phytoplankton cells, the direct use of light for enhancement of protist digestion rates, nutritional plasticity, rapid population growth combined with formation of resting stages, and defenses against predatory zooplankton. Most of these phenomena should increase community-level coupling (i.e. the degree of instantaneous and time-dependent similarity) between rates of phytoplankton growth and microzooplankton grazing, tending to stabilize planktonic ecosystems. Conversely, phytoplankton, whose mortality in the sea is overwhelmingly due to microzooplankton grazing, should experience strong pressure to evolve grazing resistence. Strategies may include chemical, morphological, and `nutrient deficit' defenses. Successful deployment of these defenses should lead to uncoupling between rates of phytoplankton growth and microzooplankton grazing, promoting instability in ecosystem structure. Understanding the comparative ecosystem dynamics of various ocean regions will require an appreciation of how protist grazer behavior and physiology influence the coupling between rates of phytoplankton growth and microzooplankton grazing.     

Summer feeding activities of zooplankton in Prydz Bay, Antarctica

Grazing of dominant zooplankton copepods (Calanoides acutus, and Metridia gerlachei), salps (Salpa thompsoni) and microzooplankton was determined during the austral summer of 1998/1999 at the seasonal ice zone of the Prydz Bay region. The objective was to measure the ingestion rates of zooplankton at the seasonal ice zone, so as to evaluate the importance of different groups of zooplankton in their grazing impact on phytoplankton standing stock and primary production. Grazing by copepods was low, and accounted for <1% of phytoplankton standing stocks and 3.8-12.5% of primary production for both species during this study; even the ingestion rates of individuals were at a high level compared with previous reports. S. thompsoni exhibited a relatively high grazing impact on primary production (72%) in the north of our investigation area. The highest grazing impact on phytoplankton was exerted by microzooplankton during this investigation, and accounted for 10-65% of the standing stock of phytoplankton and 34-100% of potential daily primary production. We concluded that microzooplankton was the dominant phytoplankton consumer in this study area. Salps also played an important role in control of phytoplankton where swarming occurred. The grazing of copepods had a relatively small effect on phytoplankton biomass development.     

Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary,USA

Microzooplankton grazing can have significant impacts on the distribution and abundance of phytoplankton, thereby influencing the frequency and duration of algae blooms. Observations of high ciliate abundances in the Suwannee River estuary, Florida, suggest a significant potential for top-down pressure on the phytoplankton community by microzooplankton. We examined the composition of the microzooplankton and determined grazing mortality losses for phytoplankton within the Suwannee River estuary from 2001 to 2002. Our results indicated grazing mortality rates of 1.4 d⁻¹, equivalent to a loss of up to 76% of phytoplankton standing crop and up to 83% of total daily primary production. The microzooplankton community was primarily composed of ciliates, dinoflagellates, and copepod nauplii. The densities of ciliates in the estuary were comparable to densities reported in highly eutrophic ecosystems (9,400–72,800 ciliates l⁻¹). Grazing pressure on small phytoplankton may be further enhanced because ciliates and small dinoflagellates have growth rates similar to those of phytoplankton, and therefore can keep up with surges in abundance. Handling editor: Judit Padisak     

REACTIVE OXYGEN METABOLISM IN THE TROPICAL BROWN ALGA DICTYOTA DICHOTOMA

There is a growing understanding that phagotrophic ciliates are often important members of aquatic communities in terms of their trophic role and mobilization of small cell production to higher consumers. As formidable consumers of small phytoplankton species they are likely to be also important in determining the community composition of the pico- and nanophytoplankton assemblages. Dilution method experiments were conducted during the winter and summer in the South Slough, an arm of the Coos Bay on the southern Oregon coast, to assess the impact of ciliate grazing on two size fractions of chlorophyll (0.2 to 5 mm and> 5 mm) and on the growth and abundance of specific phytoplankton groups, particularly cryptophytes and Synechococcus sp. The premise of the dilution technique is that grazers are diluted with their food and the observed rate of change in chlorophyll or phytoplankton abundance is linearly related to the dilution factor. Results from previous studies using the dilution technique have been given in terms of the grazing impact of microzooplankton on total chlorophyll. The findings of the research presented using a more rigorous application of the dilution method suggest that ciliates are differential in their grazing of phytoplankton, targeting small phytoplankton biomass and preying selectively on components of the assemblage that constitute this biomass.     

Interactions between planktonic microalgae and protozoan grazers

For an algal bloom to develop, the growth rate of the bloom-forming species must exceed the sum of all loss processes. Among these loss processes, grazing is generally believed to be one of the more important factors. Based on numerous field studies, it is now recognized that microzooplankton are dominant consumers of phytoplankton in both open ocean and coastal waters. Heterotrophic protists, a major component of microzooplankton communities, constitute a vast complex of diverse feeding strategies and behavior which allow them access to even the larger phytoplankton species. A number of laboratory studies have shown the capability of different protistan species to feed and grow on bloom-forming algal species. Because of short generation times, their ability for fast reaction to short-term variation in food conditions enables phagotrophic protists to fulfill the function of a heterotrophic buffer, which might balance the flow of matter in case of phytoplankton blooms. The importance of grazing as a control of microalgae becomes most apparent by its failure; if community grazing controls initial stages of bloom development, there simply is no bloom. However, if a certain algal species is difficult to graze, e.g. due to specific defense mechanisms, reduced grazing pressure will certainly favor bloom development. The present contribution will provide a general overview on the interactions between planktonic microalgae and protozoan grazers with special emphasis on species-specific interactions and algal defense strategies against protozoan grazers.     

Microzooplankton grazing in the surface water of the Southern Ocean during an austral summer

Microzooplankton grazing was investigated in surface waters of the Indo-Pacific and Atlantic sectors of the Southern Ocean by the dilution method. Phytoplankton growth varied mainly between 0.1 and 0.4 day⁻¹, and microzooplankton grazing between 0.0 and 0.3 day⁻¹. Great fluctuations in phytoplankton growth rate were observed at one station within 3 weeks and between closely spaced stations. Microzooplankton grazing rates were similar to phytoplankton growth rate despite the variation of phytoplankton growth rates, although in some cases, phytoplankton growth overwhelmed microzooplankton grazing. These observations suggest that microzooplankton are the main consumers of primary producers, and that steady state between phytoplankton growth and microzooplankton grazing is usually established in the Southern Ocean in austral summer. Received: 5 November 1996 / Accepted: 4 March 1997     

Copepod and microzooplankton grazing in mesocosms fertilised with different Si:N ratios: no overlap between food spectra and Si:N influence on zooplankton trophic level

We hypothesized that the trophic level of marine copepods should depend on the composition of the protist community. To test this hypothesis, we manipulated the phytoplankton composition in mesocosms and measured grazing rates of copepods and mesozooplankton in those mesocosms. Twelve mesocosms with Northeast Atlantic phytoplankton were fertilised with different Si:N ratios from 0:1 to 1:1. After 1 week, ten of the mesocosms were filled with natural densities of mesozooplankton, mainly calanoid copepods, while two remained as mesozooplankton-free controls. Both before and after the addition of copepods there was a positive correlation of diatom dominance with Si:N ratios. During the second phase of the experiment, copepod and microzooplankton grazing rates on different phytoplankton species were assessed by a modification of the Landry-Hassett dilution technique, where the bottles containing the different dilution treatments were replaced by dialysis bags incubated in situ. The results indicated no overlap in the food spectrum of microzooplankton (mainly ciliates) and copepods. Ciliates fed on nanoplankton, while copepods fed on large or chain-forming diatoms, naked dinoflagellates, and ciliates. The calculated trophic level of copepods showed a significantly negative but weak correlation with Si:N ratios. The strength of this response was strongly dependent on the trophic levels assumed for ciliates and mixotrophic dinoflagellates.     

The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical

Information transfer influences food-web dynamics in the marine environment, but infochemicals involved in these processes are only beginning to be understood. Dimethylsulfoniopropionate (DMSP) is produced by phytoplankton and other marine algae, and has been studied primarily in the context of sulfur cycling and regulation of global climate. My laboratory has been investigating DMSP and its breakdown product, dimethyl sulfide as infochemicals associated with trophic interactions in marine habitats, including sub-Antarctic and coral reef ecosystems. Using a neuroecological approach, our work has established that these biogenic sulfur compounds serve as critical signal molecules in marine systems and provides us with a more mechanistic understanding of how climate change may impact information transfer within marine food webs.     

Mesozooplankton and microzooplankton grazing during cyanobacterial blooms in the western basin of Lake Erie

Lake Erie is the most socioeconomically important and productive of the Laurentian (North American) Great Lakes. Since the mid-1990s cyanobacterial blooms dominated primarily by Microcystis have emerged to become annual, late summer events in the western basin of Lake Erie yet the effects of these blooms on food web dynamics and zooplankton grazing are unclear. From 2005 to 2007, grazing rates of cultured (Daphnia pulex) and natural assemblages of mesozooplankton and microzooplankton on five autotrophic populations were quantified during cyanobacterial blooms in western Lake Erie. While all groups of zooplankton grazed on all prey groups investigated, the grazing rates of natural and cultured mesozooplankton were inversely correlated with abundances of potentially toxic cyanobacteria (Microcystis, Anabaena, and Cylindrospermopsis; p < 0.05) while those of the in situ microzooplankton community were not. Microzooplankton grazed more rapidly and consistently on all groups of phytoplankton, including cyanobacteria, compared to both groups of mesozooplankton. Cyanobacteria displayed more rapid intrinsic cellular growth rates than other phytoplankton groups under enhanced nutrient concentrations suggesting that future nutrient loading to Lake Erie could exacerbate cyanobacterial blooms. In sum, while grazing rates of mesozooplankton are slowed by cyanobacterial blooms in the western basin of Lake Erie, microzooplankton are likely to play an important role in the top-down control of these blooms; this control could be weakened by any future increases in nutrient loads to Lake Erie.     

An empirical model of carbon flow through marine viruses and microzooplankton grazers

Viruses and microzooplankton grazers represent major sources of mortality for marine phytoplankton and bacteria, redirecting the flow of organic material throughout the world's oceans. Here, we investigate the use of nonlinear population models of interactions between phytoplankton, viruses and grazers as a means to quantitatively constrain the flow of carbon through marine microbial ecosystems. We augment population models with a synthesis of laboratory-based estimates of prey, predator and viral life history traits that constrain transfer efficiencies. We then apply the model framework to estimate loss rates in the California Current Ecosystem (CCE). With our empirically parameterized model, we estimate that, of the total losses mediated by viruses and microzooplankton grazing at the focal CCE site, 22 ± 3%, 46 ± 27%, 3 ± 2% and 29 ± 20% were directed to grazers, sloppy feeding (as well as excretion and respiration), viruses and viral lysate respectively. We identify opportunities to leverage ecosystem models and conventional mortality assays to further constrain the quantitative rates of critical ecosystem processes.     

THE IMPACT OF DIFFERENTIAL GRAZING BY PHAGOTROPHIC CILIATES ON PHYTOPLANKTON BIOMASS AND COMMUNITY STRUCTURE

There is a growing understanding that phagotrophic ciliates are often important members of aquatic communities in terms of their trophic role and mobilization of small cell production to higher consumers. As formidable consumers of small phytoplankton species they are likely to be also important in determining the community composition of the pico‐ and nanophytoplankton assemblages. Dilution method experiments were conducted during the winter and summer in the South Slough, an arm of the Coos Bay on the southern Oregon coast, to assess the impact of ciliate grazing on two size fractions of chlorophyll (0.2 to 5 mm and> 5 mm) and on the growth and abundance of specific phytoplankton groups, particularly cryptophytes and Synechococcus sp. The premise of the dilution technique is that grazers are diluted with their food and the observed rate of change in chlorophyll or phytoplankton abundance is linearly related to the dilution factor. Results from previous studies using the dilution technique have been given in terms of the grazing impact of microzooplankton on total chlorophyll. The findings of the research presented using a more rigorous application of the dilution method suggest that ciliates are differential in their grazing of phytoplankton, targeting small phytoplankton biomass and preying selectively on components of the assemblage that constitute this biomass.     

Prey preference of top predators manipulates the functioning and stability of multi-trophic ecosystems

The relationship between biodiversity and ecosystem functioning, and the mechanisms underpinning the food web stability, have been intensively investigated in ecological research. The ubiquities of generalists in natural food webs and its important role in dictating these ecosystem properties have been generally recognized. However, how competition between multiple top predators shape these ecosystem properties and determine the success of invasive predators remain largely unexplored. Here, we use a well-developed food web model to investigate the effects of prey preference of top predators on ecosystem functioning and food web stability in both local and invasive conditions. We design several modeling scenarios to mimic combinations of different types of top predators (specialist/generalist) and their origins (local/invasive). Our model theoretically shows that lower exploitation competition for prey between top predators (with distinct prey preferences featured by higher attack rates) would be beneficial for the ecosystem functioning and food web stability. We also demonstrate that the success of top predator invasion depends on the prey preference of both local and invasive top predators. Sensitivity analysis on the model further supports our findings. Our results highlight the importance of prey preference of multiple top predators in manipulating the properties of multi-trophic ecosystems. Our findings may have important implications because the current ongoing global changes profoundly change the phenology of many biological systems and create trophic mismatch, which may manipulate prey preference of top predators and in turn deteriorate ecosystem functioning and food web stability.     

夏季胶州湾微型浮游动物摄食初步研究

2002年6月至7月间对胶州湾内、外和港口3个典型站位进行了微型浮游动物对浮游植物的摄食研究．按陆基半现场方式进行了4次稀释法实验,对湾外相同的站位进行了两次实验,对湾内和港口各进行了一次实验,获取了研究站位浮游植物和微型浮游动物种类、丰度、体积转换浮游植物碳含量、碳／叶绿素比率、浮游植物净生长率、微型浮游动物摄食率、对潜在初级生产力的摄食压力、对浮游植物现存量的摄食压力以及碳摄食通量等参数．湾外和湾内站位的浮游植物组成相似,优势种为新月柱鞘藻(Cylindrotheca closterium)和中肋骨条藻(Skeletonema costatum),港口浮游植物优势种类为中肋骨条藻、浮动湾角藻(Eucampia zodiacus)和旋链角毛藻(Chaetoceros curvisetus)．湾外微型浮游动物的优势种为百乐拟铃虫(Tintinnopsis beroidea),而在湾内为百乐拟铃虫和急游虫(Strombidium sp．),港口主要为急游虫,也有少数的百乐拟铃虫．微型浮游动物对浮游植物的摄食率和对潜在初级生产力的摄食压力,在湾内最高,其次在湾外,港口最低．微型浮游动物对浮游植物的摄食率,在湾外,分别为0．96和1．20d^-1,在湾内为1．33d^-1,在港口为0．36d^-1．微型浮游动物对潜在初级生产力的摄食压力,在湾外,分别为74％和84％,在湾内为93％,在港口为53％．微型浮游动物的碳摄食通量在港口最高达到281mgC·m^-3·d^-1,在湾内为102mgC·m^-3·d^-1,在湾外最低范围在31～49mgC·m^-3·d^-1．浮游植物的细胞大小和两种微型浮游动物的摄食习性的不同是造成研究站位微型浮游动物摄食率和摄食压力不同的主要原因．同世界其它内湾相比,胶州湾微型浮游动物的摄食压力处于中等水平。     

“Windows of opportunity” for dinoflagellate blooms: Reduced microzooplankton net growth coupled to eutrophication

Links between eutrophication, plankton community structure, microzooplankton grazing and dinoflagellate abundance were investigated in two tributaries of the Chesapeake Bay, the Choptank and Patuxent Rivers (MD, USA). Sampling and experiments were conducted during the spring of consecutive dry (below average freshwater flow) and wet (above average freshwater flow) years. During the wet year (2003), dissolved inorganic nitrogen, phytoplankton, and copepod biomass, but not microzooplankton abundance, were greater than in the dry year. In 2003, but not 2002, small cell size photosynthetic dinoflagellates were abundant and blooms occurred in both rivers. Average potential microzooplankton grazing pressure on small dinoflagellates was spatially and temporally variable, but was not significantly different between years. Our data suggest that the variability in microzooplankton grazing pressure provided “windows of opportunity” for net growth of dinoflagellates in response to nutrient loading. The lack of net population growth of micrograzers in response to increases in dinoflagellate prey allowed dinoflagellate blooms to reach relatively high densities, however grazing also appeared to be important in limitation or demise of some blooms. We hypothesize that uncoupling of micrograzer–prey dynamics was partly due to strong top-down control by copepods of microzooplankton in the proportionately more eutrophic year, and perhaps also due to inhibition of microzooplankton grazing/growth once dinoflagellate densities are high.     

Selectivity and grazing impact of microzooplankton on phytoplankton in two subtropical semi-enclosed bays with different chlorophyll concentrations

Microzooplankton grazing rates were compared between two sites (S1 and S2) in the coastal seas of eastern Hong Kong with similar physio-chemical parameters, but different chlorophyll concentrations. During the period from March 2007 to January 2008, six sets of dilution experiments, combined with high performance liquid chromatography and phytoplankton size fractionation (< 200 μm, < 20 μm and < 5 μm), were carried out to study the microzooplankton grazing rate on phytoplankton of different taxonomic groups and sizes. Although total chlorophyll a concentrations were much higher in S1 (4.98-18.42 μg l^− 1) than in S2 (0.29-1.68 μg l^− 1), size composition of phytoplankton was relatively similar between the two sites. Measured as chlorophyll a, phytoplankton growth rates (− 0.84-1.91 d^− 1 in S1; 0.03-2.85 d^− 1 in S2) and microzooplankton grazing rates (0.00-2.26 d^− 1 in S1; 0.00-1.49 d^− 1 in S2) for all three size fractions were similar between the two bays. Phytoplankton growth rates and microzooplankton grazing rates measured as other pigments for phytoplankton of different size fractions did not show strong variations. Microzooplankton grazing impact, expressed as the ratio of microzooplankton grazing rate to phytoplankton growth rate, was generally higher in S1 than in S2, although the difference was not statistically significant. High microzooplankton grazing impact on alloxanthin (1.00-45.85) suggested strong selection toward cryptophytes. Our results provided no evidence for size selective grazing on phytoplankton by microzooplankton.