Stable Isotope Diagrams of Freshwater Food Webs
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NOTES AND COMMENTS 2293 i.e., m, = d,ls,, where d, is the number of deaths during mortality rates, which have been described above, are the time interval i, and s, is the number of survivors approaches that can enable very short periods of time at the midpoint of the time interval i. to be identified when mortality risks differ substantially Gehan ( 1969) has derived an equation which enables between sets of plants. Although for the field ecologist the variance of the midpoint age-specific mortality to inferences about the causes of plant death will always be determined: be easier than proof, the ability to compare mortality rates over very short time intervals will allow more accurate interpretation of the causes of mortality and Var[m,] = (:/ {1 - ( ~')l promote a sharper understanding of the tolerance lim its of species in the field. d, . where q, = -, I.e., s, Acknowledgments: This work was undertaken while K. D. Booth was in receipt of a Science and Engineering 2 , (m,)' 2 {. ( m,' ) } Research Council studentship. We gratefully acknowl Var[m,] = T 1 - . 2 edge the helpful comments of four referees, including David Pyke and Dolph Schluter. This formula may be used to calculate 95% confidence intervals around m, values (Fig. 1), aiding the com Literature Cited parison of survivorship patterns in the cohorts (Lee Gehan, E. A. 1969. Estimating survival functions from the 1980). When this procedure is applied to the data of life table. Journal of Chronic Diseases 21:629-644. Pyke and Thompson ( 1986), the analysis shows that Lee, E. T. 1980. Statistical methods for survival data anal the mortality rates differ significantly in the two cohorts ysis. Lifetime Learning Publications, Belmont, California, during the intervals between days 0-10, 10-20, 30-40, USA. Mantel, N., and W. Haenszel. 1959. Statistical aspects of and 50-60, confirming the conclusions of the analysis the analysis of data from retrospective studies of disease. of the residuals generated during calculation of the lo Journal ofthe National Cancer Institute 22:719-748. grank statistic. Muenchow, G. 1986. Ecological use of failure time analysis. Ecology 67:246-250. Conclusions Peto, R., and M. C. Pike. 1973. Conservatism of the ap proximation ~ (C - E) 2/E in the logrank test for survival Despite the vigor with which plant demography has data or tumor incidence data. Biometrics 29:579-584. been pursued in the last twenty years, ecologists are Pyke, D. A., and J. N. Thompson. 1986. Statistical analysis still mostly ignorant of the causes of the deaths of in of survival and removal rate experiments. Ecology 67:240- dividual plants in the field and of the reasons why 245. Pyke, D. A., and J. N. Thompson. 1987. Erratum. Ecology mortality rates of species differ between sites and dif 68:232. ferent growing conditions. Common problems in in Tremlett, M., J. W. Silvertown, and C. Tucker. 1984. An terpreting the causes of mortality and the rates of mor analysis of spatial and temporal variation in seedling sur tality in populations stem from our ignorance of the vival of a monocarpic perennial, Conium maculatum. Oi exact times at which plants have died and of variations kos 43:41-45. in mortality rates through time. The analysis of resid Manuscript received 16 January 1991; uals, and comparison of confidence intervals about revised 20 May 1991; accepted 21 May 1991. Ecology, 72(6), 1991, pp. 2293-2297 organic matter is cycled in different ecosystems. For © 1991 by the Ecological Society of America example, a few measurements of isotopic compositions of dissolved nutrients, aquatic plants, and animals es tablish a chemical outline of food web structure (Fry STABLE ISOTOPE DIAGRAMS OF and Sherr 1984, Minagawa and Wada 1984). These tracer results can be used to check conventional ideas FRESHWATER FOOD WEBS about trophic structure in well-studied systems, and to test how food web structure varies in other systems Brian Fry' where conventional visual studies of trophic relations are difficult or lacking (Rau 1980). A dual-isotope ap Stable carbon and nitrogen isotopes are valuable proach is often useful in these studies, for example, tracers in ecological research (Runde! et al. 1988). One with nitrogen isotope measurements functioning as tro use of isotope measurements is to rapidly survey how phic level indicators, and carbon isotope measure 1 The Ecosystems Center, Marine Biological Laboratory, ments indicating which plants are important sources Woods Hole, Massachusetts 02543 USA. of nutrition for consumers (Peterson and Fry 1987). 2294 NOTES AND COMMENTS Ecology, Vol. 72, No.6 Ecologists from Long Term Ecological Research ll 13C and ll'5N values are reported relative to carbon (LTER) sites in the United States and Puerto Rico in the Peedee belemnite (PDB) limestone and nitrogen recently used isotope analysis to test ideas about aquat in air, respectively, in parts per thousand (o/oo). ic food-web structure and terrestrial nitrogen cycling. This note reports an overview of the food-web results 1Jl3C or IJlSN = [Rsample - R,.andard] X 103, and discussed at a workshop in September 1989, and in Rstandard 5 cludes a ll' N survey of terrestrial materials that con R = 13C/' 2C or 15N/14N. tribute to freshwater food webs as allochthonous or ganic matter. A list of isotopic analyses from each site High-purity tank carbon dioxide and nitrogen gases is available.2 were used as working standards during sample analysis. These working standards had been calibrated against National Bureau of Standards (NBS) isotope standards Study Areas NBS-20 limestone and NBS-21 graphite for /l 13C, at Samples for studies offood webs were collected from mospheric nitrogen and N-1 ammonium sulfate for streams (sites I, 3, 8, and 17, Fig. 1) and lakes (sites ll'5N (Coplen et a!. 1983, Mariotti 1983, Minagawa et 1, 10, and 16). To determine generality of /l 15N values a!. 1984, Nevins et a!. 1985). PDB and nitrogen in air in plants and soils, samples were also collected at sev have by definition ll values of Oo/oo; samples enriched eral sites in forests (sites 2, 9, 12, 15, 16, and 17), in 13C or 15 N are "heavy" and have higher /l 13C and grasslands and deserts (sites 4, 5, and 7), at a coastal ll'5N values, while samples enriched in 12C and 14N dune site (site 14), and at a high-altitude tundra site have lower ll values. (site 6). Food Webs Methods Nitrogen isotopic compositions of plants and vari Soils, plant leaf material, plant litter, and whole an ous types of animal consumers showed remarkable imals or muscle tissue from fish were collected in the similarity in eight lake and stream sites sampled (Fig. 15 summer of 1989, dried at 60°C, and ground to fine 2). Plants had lowest ll N values of typically -4 to 5 powders. Most samples were composites of > 5 indi + 3o/oo, and ll' N values of aquatic and terrestrial plants vidual samples. Samples were combusted at 750°C were generally similar (Fig. 2). A broad analysis of 15 overnight (soils) or 900°C for 1 h (plants, animals) in plants and soil fractions showed that ll N values of evacuated sealed Vycor high temperature glass tubes terrestrial materials at the lake and stream sites were (Corning Glass, Corning, New York) containing 1 g of fairly typical and could be expected to occur at most CuO and 0.5 g Cu metal (Minagawa eta!. 1984). Sam other LTER sites where streams and lakes were often ple sizes were typically 5 mg for animals, 15 mg for present, but not sampled (Figs. 2 and 3). Plants and plants, and 50-1000 mg for soils. To obtain accurate soils in these relatively undisturbed L TER sites also 15 ll'5N values, it was necessary to grind soils, but not had generally lower ll N values than previously ana plant or animal samples, with CuO prior to combus lyzed agricultural plants and soils of North America tion. (Feigin eta!. 1974, Shearer eta!. 1978). Only samples 15 Combustion gases were cryogenically separated and from arid sites 4 and 5 had higher average /l N values similar to those found in agricultural sites (Fig. 3). pure C02 and N 2 measured for carbon and nitrogen isotope values with a Finnigan 251 stable isotope ratio Animals from L TER lakes and streams had higher 5 15 mass spectrometer. Molecular sieve (0.5 nm, Alltech ll' N values than did plants, and animal /l N values Associates, Deerfield, Illinois) was used during collec increased with increasing trophic level (Fig. 2). There was an average ll'5N increase of2-3o/oo per trophic level tion and transfer of N 2 gas between vacuum prepara tion lines and the mass spectrometer. Replicates usu (Fig. 2), and at all sites top predators, such as small ally fell within a 0.2o/oo range for both carbon and mouth bass and giant salamanders, had highest values nitrogen isotope measurements; an increased range of (up to 9o/oo higher than algae at the base of the food 15 ten resulted if samples had not been finely ground to web). Using the assumption of a 3.3o/oo increase in /l N 15 a flour-like consistency. per trophic level (Minagawa and Wada 1984), the /l N results indicate that there are 2.5-3.5 trophic levels in all stream and lake ecosystems (Fig. 2). 2 See ESA Supplementary Publication Service Document The estimate of 2.5-3.5 trophic levels agrees fairly No. 9102 for 32 pages of supplementary material. This doc well with estimates of trophic complexity in other ument is available on microfiche or in printed form.