© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Taxonomic versus trophic structure of mesozooplankton: a seasonal study of species succession and stable carbon and nitrogen isotopes in a coastal upwelling ecosystem
Instituto Español de Oceanografía, Centro Oceanográfico de A Coruña Apdo. 130, 15080 A Coruña, Spain
*Correspondence to A. Bode: tel: +34 981 205362; fax: +34 981 229077. e-mail: antonio.bode{at}co.ieo.es; alvarez{at}co.ieo.es.
Seasonal variations in mesozooplankton (>200 µm) stable carbon and nitrogen isotope abundances were compared with the seasonal species succession pattern off A Coruña (Galicia, NW Spain). Mesozooplankton biomass, numerical abundance, species composition, and natural abundance of stable isotopes, along with water column temperature, salinity, chlorophyll a and dissolved nitrate concentrations, were studied in monthly samples during the years 2000 and 2001 at a coastal station (80-m depth). Biomass and abundance of mesozooplankton followed the annual cycle with maxima in spring and summer (year 2000) and occasionally also in autumn (year 2001). The succession pattern shown by the taxonomic assemblages was recognized in both years of study, despite differences in the timing of upwelling and the large input of continental water during most of 2000. Variations in neither carbon nor nitrogen isotopes were correlated with either abundance or biomass at annual time scales, but heavy isotopes significantly accumulated during periods of zooplankton increase (spring and early summer). The consumption of nitrate during the spring can explain in part the progressive accumulation of heavy nitrogen isotopes during this period. In addition, the abundance of carnivorous zooplankton (mainly carnivorous copepods, siphonophores, and chaetognaths) was linearly related to the increase in heavy isotopes during the spring and, in the case of nitrogen, also during the whole study period. The computed linear relationships between isotope abundances and plankton species composition provided a way to further analyse the pelagic foodweb through the estimation of isotope reference values for primary consumers.
Keywords: coastal ecosystem, foodweb, species succession, stable isotopes, upwelling, zooplankton
 |
Introduction |
|---|
 Top Introduction Materials and methodsResultsDiscussionReferences |
|---|
The study of the trophic relationships in pelagic ecosystems is complicated by the large variability in diet of most species, which leads to unstructured foodwebs (Isaacs, 1973). Omnivory is widespread among all organisms, but a particularly large number of zooplankton species may feed on similar diets composed of a mixture of phytoplankton, detritus, and microplankton (e.g. Stoecker and Capuzzo, 1990; Irigoien et al., 1998; Batten et al., 2001). Experimental determinations of the contribution of non-autotrophic prey to the diet of zooplankton (mostly copepods) suggest estimates ranging from purely carnivorous diets to a variety of mixtures of algae and animal prey (Gifford and Dagg, 1991; Fessenden and Cowles, 1994; Irigoien et al., 1998; Batten et al., 2001; Halvorsen et al., 2001). Such variety in the diet makes the quantification of flows between compartments or trophic levels difficult.
As heavy isotopes accumulate in consumers relative to their prey (Minagawa and Wada, 1984; Peterson and Fry, 1987), the value of natural abundance of stable isotopes in plankton has been used to analyse the trophic structure of various foodwebs (Mullin et al., 1984; Fry and Quiñones, 1994; Rolff, 2000). The relative enrichment in heavy isotopes between species or size classes can be interpreted as a measure of the complexity of a particular foodweb as it reflects the number of trophic steps from the primary producers. This is supported by the relative constancy of the isotopic fractionation between successive consumer levels found in several studies (Minagawa and Wada, 1984; Vander Zanden and Rasmussen, 2001; Post, 2002), particularly in the case of nitrogen isotopes (+3.4
). In this way, the trophic position of a particular compartment in the foodweb may be computed if we have an estimate of the isotopic value of the food at the base of the foodweb. However, the choice of an appropriate reference value is complicated because the isotopic abundance of the phytoplankton depends on the nutrient source (O'Reilly et al., 2002) and on the species composition (Fry and Wainright, 1991), particularly in upwelling ecosystems. In addition, the isotopic fractionation between primary producers and herbivores is highly variable (Vander Zanden and Rasmussen, 2001).
Recent studies with stable isotopes have demonstrated that the use of the natural abundance value of a primary consumer as the isotopic reference greatly reduces the uncertainty of estimations of trophic level in foodwebs of freshwater ecosystems (Vander Zanden and Rasmussen, 2001; Post, 2002; O'Reilly et al., 2002). In marine pelagic ecosystems of temperate latitudes these primary consumers can be found among the zooplankton, but because species composition and abundance vary seasonally (e.g. Colebrook, 1979) the selection of a single species as a reference may not be appropriate. Furthermore, several studies have shown that the isotopic composition of zooplankton size classes varies during the year ultimately due to changes in the sources of nutrients available for the primary producers (Goering et al., 1990; Montoya et al., 1990; Rolff, 2000).
In this study, we determined seasonal variations in stable carbon and nitrogen isotope abundances in zooplankton, which were compared with the seasonal species succession pattern off A Coruña (Galicia, NW Spain). The objective was to demonstrate the existence of trends in the isotopic composition of zooplankton over the annual species succession and productivity cycles. The results of this study may provide clues for the estimation of natural abundance values that can be used as the isotopic reference in the determination of trophic positions in marine pelagic ecosystems.
|
Materials and methods |
|---|
|
TopIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Zooplankton (>200 µm) was collected monthly during the years 2000 and 2001 at Station 2 off A Coruña (Figure 1). Samples were obtained by double oblique tows of a Juday-Bogorov net (200-µm mesh size) between the surface and the bottom (maximum depth 80 m). Aliquots were taken for the determination of biomass (dry weight), numerical abundance and species composition, and natural abundance of stable carbon and nitrogen isotopes. Temperature and salinity profiles were measured with a Seabird 25 CTD and water column chlorophyll a (Chl a) and dissolved nitrate concentrations were analysed. Details of the sampling and analytical methods for these variables can be found in Casas et al. (1997). Zooplankton were identified under the microscope to the species level where possible. Particular attention was paid to identify species or groups with potentially carnivorous diets (Greene, 1985). Succession of zooplankton taxa was summarized by means of non-metric multidimensional scaling (Clarke and Warwick, 2001). The analysis was run on the Bray–Curtiss similarity matrix obtained from log-transformed abundance values of taxa present in >20% of samples. Successional phases were further analysed by means of the SIMPER procedure (contribution of individual taxa to sample group separation by the similarity matrix) and ANOSIM (significance of differences in similarity between sample groups) of the PRIMER statistical package (Clarke and Warwick, 2001).
|
For stable isotope determinations, dried (60°C, 48 h) and finely ground aliquots of zooplankton were packed in tin capsules for conversion into CO2 and N2 in an elemental analyser (Carlo Erba CHNSO 1108) coupled to an isotope-ratio mass spectrometer (Finnigan Mat Delta Plus). Samples were not acidified to remove carbonates because other studies showed that the acidification may not cause substantial modification in carbon isotope results, but it may affect nitrogen determinations (Bunn et al., 1995; Bode et al., 2003). Carbon and nitrogen stable isotope abundance was expressed as
13C and 15N relative to VPDB (Vienna PeeDee Belemnite carbonate) and atmospheric N2 isotope standards. Precision (±1 standard error) of replicate determinations of both C and N stable isotopes was <0.03.
The relationships between environmental, plankton, and stable isotope variables were analysed by non-parametric rank correlation coefficients (Spearman's 
) and by robust regression (Least Trimmed Squares regression, see Venables and Ripley, 1997), the latter aimed at reducing the uncertainty in the estimations due to outliers, particularly when there are few observations. For these procedures, the statistical packages SPSS and S-Plus were employed.
|
Results |
|---|
|
TopIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Environmental dynamics
The ecosystem studied is characterized by a typical seasonal cycle with minimum temperatures in winter throughout the water column and maximum values in summer, when maximum stratification arises as a consequence of solar heating of the surface (Figure 2a). Salinity changes are generally low, as there are no large rivers nearby, but in the period between March 2000 and April 2001 there was a large influence of low salinity water in the surface layer due to run-off; it was an unusually rainy year (Figure 2b). However, coastal upwelling superimposes on the seasonal cycle by keeping the water near the bottom at <14°C for most of the year and by introducing nitrate to the surface during the spring and summer (Figure 2c), which produces a series of phytoplankton blooms as a result of temporary breakdown of stratification (Figure 2d). Also, in this study, the run-off water in the winter of 2001 left an unusual amount of nitrate in the surface, exceeding the values found in bottom layers. The changes in surface waters during most of 2001 were restricted to a narrow layer near the surface and apparently did not affect bulk biological variables, as the water column averaged chlorophyll followed the pattern found in previous studies in the same area (Valdés et al., 1991; Casas et al., 1997). Primary productivity increased during spring–early summer (from March to June), following the depletion of nitrate in the surface waters. This is illustrated by the significant negative correlation between surface nitrate and the Julian day for the spring–early summer period, whereas there was no significant correlation using all data (Table 1). Chlorophyll concentrations generally increased during spring, but because of the high variability found in the year 2000 we did not find significant correlations between mean chlorophyll and the Julian day (Figure 2d).
|
|
Zooplankton species succession
Mesozooplankton abundance (Figure 3a) followed an annual cycle with maximum values in spring and summer (year 2000) and occasionally also in autumn (year 2001). These maxima generally followed those of the phytoplankton and were caused mainly by the reproduction of holoplanktonic species such as Cladocera (Figure 3b) and copepods (Figure 3c), as well as the influx of meroplanktonic larvae into the community (Figure 3e). Taxa with potentially carnivorous diets included copepods (Aetideus armatus, Paraeuchaeta hebes, Metridia lucens, Pleuromamma gracilis, and Candacia armata), siphonophores, and ctenophores. Carnivores also displayed two annual abundance peaks, but in this case maximum numbers were generally reached by early summer (Figure 3d). Most of the variation in the abundance of carnivores was due to carnivorous copepods, significantly correlated with total carnivore abundance (Spearman's
=0.598, p<0.01). Similarly, variations in zooplankton biomass (not shown) were significantly correlated with those in total abundance (Spearman's =0.851, p<0.01). The seasonal pattern coincides with previous studies of zooplankton succession and biomass seasonality at the same station (Valdés et al., 1990, 1991; Bode et al., 1998) and in nearby areas of the NW Iberian Peninsula (Colebrook, 1979; Cabal, 1993).
|
Using multidimensional scaling, the succession pattern of the taxonomic assemblages was arranged in two main phases of high and low plankton abundance, respectively (Figure 4). Such phases were recognized in both years of study despite the differences in the input of continental water. The separation of samples into these groups was confirmed by the analysis of the similarity matrix with the ANOSIM procedure (global R statistic = 0.592, p<0.001). Small-sized (e.g. Acartia clausii) and juvenile stages of copepods contributed to >50% of similarity of samples within each of the phases of high and low total zooplankton abundance. In contrast, the contribution of the abundance of carnivorous taxa to average similarity in these groups was <1% (SIMPER analysis). The high zooplankton abundance phase occurred from February to October, when surface temperature generally increased and surface nitrate decreased, and coincided with the period of high chlorophyll concentration in the water column (Figure 2).
|
Stable isotope variability
Both
13C and 15N displayed maximum values in late spring (May 2000) or early summer (June 2001), but high values were found also in autumn of 2001 (Figure 5). Natural abundance values of both isotopes were significantly correlated either when considering all samples or samples from the spring–early summer period (Table 1). Values of 13C (but not of 15N) showed a significant increase with mean Chl a (Figure 6; Table 2). In contrast, a significant increase of 15N values (but not of 13C) was found during the spring, coinciding with a decrease of surface nitrate concentrations. No significant correlations were found between either 13C or 15N and temperature or nitrate considering all sampling dates (Table 1).
|
|
|
Similarly, variations in carbon and nitrogen isotopes in zooplankton were not correlated with either total abundance or abundance of the dominant taxa, copepods (p>0.05). No significant correlations were found either when considering only samples from spring and early summer. However, abundance of carnivorous zooplankton was linearly related to the variations in
13C and 15N (Figure 6). Even when the determination coefficients were low, the regressions improved notably when using only spring–early summer data (Table 2). Furthermore, the regressions between 13C or 15N and carnivore abundance allow for estimation of the natural abundance values expected in a zooplankton community without predators (i.e. composed only from primary consumers). These values can be estimated from the intercepts of the robust regression lines relating isotope and carnivore abundances (Table 2). |
Discussion |
|---|
|
TopIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
This study has shown that zooplankton annual succession patterns in NW Spain based on the taxonomic composition of the community are different compared with those taking into account trophic aspects. On the one hand, species succession is characterized by the rapid increase in numbers of almost all taxa from the late autumn and winter period to spring, mostly dominated by copepods (Valdés et al., 1990, 1991; Cabal, 1993; Bode et al., 1998). For most of the year (spring to early autumn) a series of abundance peaks of various taxa, including meroplanktonic larvae, contributes to maintaining high abundance and biomass values in the water column, with maximum values in spring and autumn. On the other hand, heavy carbon and nitrogen stable isotopes accumulate in zooplankton during the spring–early summer period, but decrease thereafter. Such a trend is shown particularly by nitrogen, while the abundance of carbon isotopes was more variable. These results contrast with those from ecosystems where the annual primary production is characterized by a single spring bloom that supports the subsequent growth of zooplankton (e.g. Goering et al., 1990), but also with the pattern displayed by ecosystems with phytoplankton blooms in autumn (Montoya et al., 1990) and in summer (Rolff, 2000). The growth of phytoplankton during spring is fuelled mostly by dissolved nitrate, which is expected to become progressively enriched in 15N as it is consumed by phytoplankton because of isotopic fractionation (Wada and Hattori, 1991). The decrease in dissolved nitrate concentration is generally accompanied by an increase in
15N values (Montoya et al., 1990). Correspondingly, the phytoplankton becomes progressively enriched in 15N as dissolved nitrate is removed from the water in the upper mixed layer (Montoya et al., 1990) and this has been related to the enrichment of zooplankton (Goering et al., 1990; Montoya et al., 1990; Rolff, 2000). The linear increase in zooplankton 15N from spring to early summer, as surface temperature increases and nitrate decreases in our study, fits well with the nutrient depletion process described. In turn, the decrease in 15N values from the annual maximum in early summer can be explained by the progressive use of regenerated nitrogen by phytoplankton (mostly ammonium excreted by zooplankton), which is depleted in 15N (Montoya et al., 1990). However, the absence of a clear increase in 15N from zooplankton as a response to phytoplankton blooms during summer and autumn in our study suggests that the accumulation of 15N during spring and early summer is due to a combination of trophic and species succession processes.
First, most of the nitrate used by phytoplankton during the spring is likely to be supplied by the winter mixing of Eastern North Atlantic Central Waters (ENACW) with shelf waters (e.g. Casas et al., 1997). Upwelling events of ENACW replace some of the depleted nitrate in the subsurface layers, thus maintaining relatively high levels of phytoplankton biomass during the spring and summer. In contrast, nutrients provided by run-off seem of low importance in the study area, despite the clear signal of low salinity water found in the surface during the year 2000. The upwelled nitrate is expected to originate from regeneration in deep oceanic layers and thus to be relatively enriched in 15N (e.g. Wada and Hattori, 1991). Previous measurements in the study area during the spring indicate that the isotopic signature of deep-water nitrate is consistently displayed by surface phytoplankton (Bode et al., 2003) thus favouring enrichment of the zooplankton consumers, as observed during the spring in this study. Despite the occurrence of upwelling events also in summer, phytoplankton growth during summer and autumn in this region depends mainly on regenerated nitrogen (Bode and Varela, 1994; Joint et al., 2001), which would explain the general decrease in the values of zooplankton 15N observed.
Second, the rapid increase in the number of carnivorous groups during the spring, following the peak in omnivorous species (mostly copepods) is consistent with the progressive enrichment in 15N in zooplankton, as consumer species are enriched in heavy isotopes relative to their prey (Minagawa and Wada, 1984; Peterson and Fry, 1987). In our study, the contribution of carnivores to 15N values appears to be higher than the contribution of regenerated nitrogen, because there is a positive correlation between carnivore abundance and 15N not only when considering samples for the spring period but also when considering samples from all seasons (Figure 6). It can be argued that the regression of 15N with zooplankton abundance values may lead to misleading interpretations of isotopic enrichment during zooplankton succession because of possible changes in the average size of individuals. Although the use of direct biomass estimates of the various zooplankton taxa would be desirable, we do not expect a large deviation from the actual patterns when using abundance values, because we found a highly significant correlation between total abundance and biomass but also because previous studies in the same sampling area showed that most of the variations in total zooplankton biomass and abundance were due to copepods with a mean individual size of 0.9 mm throughout the year (Valdés et al., 1990, 1991). According to these studies, meroplanktonic larvae and juvenile stages of copepods have a modal size of 0.4 mm, while large zooplankton (such as siphonophores) may reach several millimetres in length. Neither the occasional high number of small zooplankton nor the generally low number of large specimens seem to affect the biomass–abundance relationship in the study area (Valdés et al., 1990).
Given the large variability found in both carbon and nitrogen isotope abundances in mesozooplankton through the annual cycle, there is not a simple way to estimate a single natural abundance value to use as a reference value when computing trophic positions, as was proposed for freshwater ecosystems (Vander Zanden and Rasmussen, 2001; Post 2002; O'Reilly et al., 2002). One approach is to use the mean value of natural abundance measured in the size fraction that likely contains primary producers (e.g. Bode et al., 2003). Another approach would be to measure the natural abundance of isotopes in selected herbivore species, but it is difficult to identify exclusive herbivores among marine zooplankton, as most grazers identified in the study region are omnivores (Batten et al., 2001; Halvorsen et al., 2001). Furthermore, the separation under the microscope of zooplankton by species, and subsequent determination of natural abundance values is a labour-intensive procedure. In this study we propose the use of the intercept of the line relating isotope abundances and carnivore abundance in the estimation of isotope reference values for this ecosystem. Use of the regression model allows for elimination of the effect of true carnivores on 15N values, as they are always present in the samples from the whole zooplankton community. For instance, we can use the value of the intercept for 15N using data from the spring–early summer period (+3.9) as an estimate of the isotopic reference value for a zooplankton community composed only of primary consumers (i.e. excluding species that almost exclusively prey on other mesozooplankton). Such consumers may not be full-time herbivores (e.g. most copepods), but their isotopic signatures are expected to be close to those of phytoplankton, as the isotopic enrichment in microbial and protozoan foodwebs is generally small (e.g. Rau et al., 1990). Using the reference value (which would indicate a trophic position value of 2 if we consider that the primary producers have a trophic position value equal to 1), the trophic position of other pelagic compartments in the foodweb could be estimated (e.g. Vander Zanden and Rasmussen, 2001). For instance, taking into account the mean values of 15N from sardines (Sardina pilchardus), a planktivorous fish, and from the common dolphin (Delphinus delphis), a piscivorous predator, measured near the study area by Bode et al. (2003), the reference value for zooplankton without carnivores determined in this study (+3.9), and a trophic fractionation factor between successive consumers of 3.4 (Vander Zanden and Rasmussen, 2001; Post, 2002), we can estimate that the sardines (15N = +6.7) have a trophic position of 2.8, which is consistent with the omnivorous diet of this species. In turn, dolphins (15N = +8.6) would have a mean trophic position of 3.4, equivalent to a primary carnivore. These figures are 0.5 trophic levels lower than those derived from previous estimations made by using the 15N value of the phytoplankton as the reference (Bode et al., 2003), which were subject to large uncertainties (e.g. Vander Zanden and Rasmussen, 2001). In this way, the results of this study may facilitate the interpretation of trophic analysis of the pelagic ecosystem through the measurement of stable isotopes in various compartments of the foodweb. However, the relationships given, although significant, do not account for a large fraction of the observed variability in isotope composition. Future studies will demonstrate the validity of the proposed regression approach by examining in greater detail some aspects not considered here, as the biomass-specific values of natural abundance of C and N isotopes in selected zooplankton species.
|
Acknowledgements |
|---|
Samples were obtained with the collaboration of the crew of RV "Lura" as part of IEO-1007 project (Instituto Español de Oceanografía, Spain). We are grateful to all scientists and technicians participating in the project. Special mention is made of I. González and E. Rey for their assistance in the collection and processing of zooplankton samples. The comments and suggestions by Professor T. Ikeda and by an anonymous referee greatly improved an earlier version of the manuscript. Isotopic analyses were made at SXAIN of the Universidad de A Coruña (Spain). This is contribution number 161 of project IEO-1007.
|
References |
|---|
|
TopIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
-
Batten S., Fileman E.S., Halvorsen E. (2001) The contribution of microzooplankton to the mesozooplankton diet in an upwelling filament off the northwest coast of Spain. Progress in Oceanography 51:385–398.[CrossRef][Web of Science]
Bode A., Alvarez-Ossorio M.T., González N. (1998) Estimations of mesozooplankton biomass in a coastal upwelling area off NW Spain. Journal of Plankton Research 20:1005–1014.
Bode A., Carrera P., Lens S. (2003) The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: natural abundance of stable carbon and nitrogen isotopes. ICES Journal of Marine Science 60:11–22.
Bode A. and Varela M. (1994) Planktonic carbon and nitrogen budgets for the N–NW Spanish shelf: the role of pelagic nutrient regeneration during upwelling events. Scientia Marina 58:221–231.
Bunn S.E., Loneragan N.R., Kempster M.A. (1995) Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: implications for food-web studies using multiple stable isotopes. Limnology and Oceanography 40:622–625.[Web of Science]
Cabal J. A. (1993) Estructura y dinámica de las poblaciones de copépodos planctónicos en la costa central de Asturias. PhD thesis, Universidad de Oviedo, Spain. 349 pp.
Casas B., Varela M., Canle M., González N., Bode A. (1997) Seasonal variations of nutrients, seston and phytoplankton, and upwelling intensity off La Coruña (NW Spain). Estuarine, Coastal and Shelf Science 44:767–778.[CrossRef]
Clarke K.R. and Warwick R.M. (2001) Change in marine communities: an approach to statistical analysis and interpretation(PRIMER-E Ltd, Plymouth, UK) 171 pp.
Colebrook J.M. (1979) Continuous plankton record: seasonal cycles of phytoplankton and copepods in the North Atlantic Ocean and North Sea. Marine Biology 51:23–32.[CrossRef]
Fessenden L. and Cowles T.J. (1994) Copepod predation on phagotrophic ciliates in Oregon coastal waters. Marine Ecology Progress Series 107:103–111.[Web of Science]
Fry B. and Quiñones R.B. (1994) Biomass spectra and stable isotope indicators of trophic level in zooplankton of the northwest Atlantic. Marine Ecology Progress Series 112:201–204.[Web of Science]
Fry B. and Wainright S.C. (1991) Diatom sources of 13C-rich carbon in marine food webs. Marine Ecology Progress Series 76:149–157.[Web of Science]
Gifford D.J. and Dagg M.J. (1991) The microzooplankton-mesozooplankton link: consumption of planktonic protozoa by the calanoid copepod Acartia tonsa Dana and Neocalanus plumchrus Murukawa. Marine Microbial Food Webs 5:161–177.
Goering J., Alexander V., Haubenstock N. (1990) Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a North Pacific bay. Estuarine, Coastal and Shelf Science 30:239–260.[CrossRef]
Greene C.H. (1985) Planktivore functional groups and patterns of prey selection in pelagic communities. Journal of Plankton Research 7:35–40.
Halvorsen E., Hirst A.G., Batten S.D., Tande K.S., Lampitt R.S. (2001) Diet and community grazing by copepods in an upwelled filament off the NW coast of Spain. Progress in Oceanography 51:399–421.[CrossRef][Web of Science]
Irigoien X., Head R., Klenke U., Meyer-Harms B., Harbour D., Niehoff B., Hirche H.-J., Harris R. (1998) A high frequency time series at weathership M, Norwegian Sea, during the 1997 spring bloom: feeding of adult female Calanus finmarchicus. Marine Ecology Progress Series 172:127–137.[Web of Science]
Isaacs J.D. (1973) Potential trophic biomasses and trace-substance concentration in unstructured marine food webs. Marine Biology 22:97–104.[Medline]
Joint I., Rees A., Woodward M. (2001) Primary production and nutrient assimilation in the Iberian Upwelling in August 1998. Progress in Oceanography 51:303–320.[CrossRef][Web of Science]
Minagawa M. and Wada E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochimica et Cosmochimica Acta 48:1135–1140.[CrossRef][Web of Science]
Montoya J.P., Horrigan S.G., McCarthy J.J. (1990) Natural abundance of 15N in particulate nitrogen and zooplankton in the Chesapeake Bay. Marine Ecology Progress Series 65:35–61.[Web of Science]
Mullin M.M., Rau G.H., Eppley R.W. (1984) Stable nitrogen isotopes in zooplankton: some geographic and temporal variations in the North Pacific. Limnology and Oceanography 29:1267–1273.[Web of Science]
O'Reilly C.M., Hecky R.E., Cohen A.S., Plisnier P.-D. (2002) Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnology and Oceanography 47:306–309.[Web of Science]
Peterson B.J. and Fry B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293–320.[CrossRef][Web of Science]
Post D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.[CrossRef][Web of Science]
Rau G.H., Teyssie J.-L., Rassoulzadegan F., Fowler S.W. (1990) 13C/12C and 15N/14N variations among size-fractionated marine particles: implications for their origin and trophic relationships. Marine Ecology Progress Series 59:33–38.[Web of Science]
Rolff C. (2000) Seasonal variation in 13C and 15N of size-fractionated plankton at a coastal station in the northern Baltic Proper. Marine Ecology Progress Series 203:47–65.[Web of Science]
Stoecker D.K. and Capuzzo J.M. (1990) Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12:891–908.
Valdés L., Alvarez-Ossorio M.T., Varela M. (1990) Relación entre la estructura de tallas y la biomasa del zooplancton nerítico en la plataforma de La Coruña (NO de España). Boletín del Instituto Español de Oceanografía 6:97–106.
Valdés L., Alvarez-Ossorio M.T., Lavin A., Varela M., Carballo R. (1991) Ciclo anual de parámetros hidrográficos, nutrientes y plancton en la plataforma continental de La Coruña (NO, España). Boletín del Instituto Español de Oceanografía 7:91–138.[Medline]
Vander Zanden M.J. and Rasmussen J.B. (2001) Variation in 15N and 13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46:2061–2066.[Web of Science]
Venables W.N. and Ripley B.D. (1997) Modern and Applied Statistics with S-PLUS(Springer-Verlag, New York) 548 pp.
Wada E. and Hattori A. (1991) Nitrogen in the sea: forms, abundances, and rate processes(CRC Press, Boca Raton) 208 pp.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. B. Richoux and P. W. Froneman Plankton trophodynamics at the subtropical convergence, Southern Ocean J. Plankton Res., September 1, 2009; 31(9): 1059 - 1073. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Koppelmann, R. Bottger-Schnack, J. Mobius, and H. Weikert Trophic relationships of zooplankton in the eastern Mediterranean based on stable isotope measurements J. Plankton Res., June 1, 2009; 31(6): 669 - 686. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||