Ontogenetic niche shifts occur across diverse taxonomic groups, and can have critical implications for population dynamics, community structure, and ecosystem function. In this study, we provide a hypothesis-testing framework combining univariate and multivariate analyses to examine ontogenetic niche shifts using stable isotope ratios. This framework is based on three distinct ontogenetic niche shift scenarios, i.e., (1) no niche shift, (2) niche expansion/reduction, and (3) discrete niche shift between size classes. We developed criteria for identifying each scenario, as based on three important resource use characteristics, i.e., niche width, niche position, and niche overlap. We provide an empirical example for each ontogenetic niche shift scenario, illustrating differences in resource use characteristics among different organisms. The present framework provides a foundation for future studies on ontogenetic niche shifts, and also can be applied to examine resource variability among other population sub-groupings (e.g., by sex or phenotype).
Citation: Hammerschlag-Peyer CM, Yeager LA, Araújo MS, Layman CA (2011) A Hypothesis-Testing Framework for Studies Investigating Ontogenetic Niche Shifts Using Stable Isotope Ratios. PLoS ONE 6(11): e27104. https://doi.org/10.1371/journal.pone.0027104
Editor: Simon Thrush, National Institute of Water & Atmospheric Research, New Zealand
Received: November 23, 2010; Accepted: October 10, 2011; Published: November 3, 2011
Copyright: © 2011 Hammerschlag-Peyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors would like to thank their funding agencies, National Science Foundation (OCE #0746164, DEB #0842196; www.nsf.gov/) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (www.capes.gov.br/), and Florida International University Dissertation Year Fellowship (gradschool.fiu.edu/Fellowships.html) for their financial support. The funding agencies had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Changes in resource use with body size or age, i.e., ontogenetic niche shifts, may occur in 80% of animal taxa , and have been shown to affect the structure and dynamics of populations, communities and ecosystems –. For instance, species often feed at higher trophic levels as they mature ,  and thus, interactions with other species may shift from competition to predation through ontogeny , . Many organisms increase their foraging range with ontogeny , thereby changing the nature of nutrient and energy flow through different habitats or ecosystems . As such, ontogenetic niche shifts may render life stages as functionally distinct groups that should be considered as distinct nodes in food web models . Hence, the study of ontogenetic niche shifts is of core interest in the ecological sciences.
In a classic paper, Werner and Gilliam  proposed three possible scenarios for how an organism's resource use (e.g., diet, habitat use) may (or may not) change through ontogeny. First, a consumer may have no substantial ontogenetic changes in resource use (Fig. 1A, 1D). This scenario may occur in specialist taxa, such as phytophagus insects which are highly selective feeders throughout ontogeny . Second, the niche of a smaller size class may be a subset of the niche of a larger size class, e.g., because larger individuals expand their foraging range and incorporate prey items that smaller individuals do not encounter (Fig. 1B, 1E; opposite scenario can also be true, i.e., niche of larger size class can be a subset of a smaller size class) . Third, consumers may switch to a different resource pool during ontogenetic development (Fig. 1C, 1F), e.g., those organisms that have different diets following metamorphosis  or following shifts across habitat boundaries –. These different ontogenetic niche shift scenarios will translate into changes in niche width, niche position and/or niche overlap between size classes.
Horizontally adjacent panels represent the same ontogenetic niche shift scenario. (A–C) Multivariate illustration of potential differences in niche width (represented by convex hull polygons), niche position and niche overlap (see text for more details) between two size classes in δ13C-δ15N niche space. (D–F) Univariate representation of niche width (variance of isotope values) and niche position (mean isotopic value) of either δ13C or δ15N between size classes. Closed circles represent isotope data of small individuals and open circles of large individuals. For B & E, this could also be a niche reduction, i.e., small individuals would occupy larger niche width than large individuals. Solid line = constant niche width, dotted line = niche reduction, dashed line = niche expansion; S = small size class, L = large size class. In panel F, solid line = constant variance, dotted line = reduced variance, dashed line = increased variance.
Stable isotope analysis often is applied to investigate ontogenetic niche shifts because it provides a time- and space-integrated representation of diet and/or is useful for those organisms whose diets are difficult to characterize directly , . The majority of diet studies have employed stable isotope ratios of carbon (i.e., δ13C) and nitrogen (i.e., δ15N), as they provide information related to a consumer's basal resource pool and trophic position, respectively –. Most studies using stable isotopes to examine ontogenetic changes in diet rely on qualitative observations (i.e., drawing conclusions without using statistical descriptions or tests) or analyze δ13C and δ15N separately, either against a continuous body size gradient (e.g., regression analysis –) or among size/age groups (e.g., t-test, analysis of variance –; Fig. 1A–C). Yet, recent food web studies have shown the power of simultaneously analyzing δ13C and δ15N in order to better characterize overall patterns in niche variation –. For instance, bi- or multivariate analysis (e.g., simultaneous analysis of δ13C and δ15N) enables the detection of potential correlations between variables, which is not possible in univariate analysis .
Our aim was to provide a single hypothesis-testing framework that can delineate examinations of ontogenetic niche shift scenarios . Our proposed framework incorporates both univariate and multivariate analyses to investigate shifts in niche width, niche position and niche overlap through ontogeny. We developed specific criteria characterizing each ontogenetic niche shift category and provide empirical examples to illustrate each. We hope this provides a unified framework for extending the classic niche shift categorization defined by Werner and Gilliam .
Materials and Methods
We evaluated three niche aspects, including (1) niche width (variety in resources consumed), (2) niche position (types of resources consumed), and (3) niche overlap (similarity in resource use among individuals). We examined changes in niche width and niche position through ontogeny using multivariate and univariate analyses (see below). If niche width and/or niche position were found to differ through ontogeny using multivariate analysis, conventional univariate tests were performed to elucidate which niche axis (e.g., δ13C, δ15N) drove the observed niche shift (Fig. 1). For example, ontogenetic shifts in δ13C values could indicate dissimilar use of habitats or resource pools by different size classes , –, whereas changes in δ15N values typically imply a shift in trophic position , , . We then measured niche overlap between size classes in two-dimensional niche space (i.e., δ13C-δ15N-biplot space) using a % overlap measure . Niche width, niche position and niche overlap are important aspects to identify ontogenetic niche shifts and can be used to classify an organism into one of the three categories proposed in the classic paper of Werner and Gilliam . Following, we identify specific quantitative criteria that can be used for each of these niche shift scenarios.
The criteria for the first ontogenetic niche shift scenario, involving no change in diet through ontogeny are: no difference in (1) niche width and (2) niche position, imparting (3) a high degree of overlap in individuals' isotope values (Figs. 1A, 1D, 2). For the second scenario, breadth of resource use (i.e., diet or habitat use) is larger in one group than in the other, resulting in (1) a difference in niche width, irrespective of (2) niche position. More specifically, the isotopic niche width of one group is statistically larger than that of the other and the niche of the latter group is largely encompassed by the former, leading to (3) an asymmetry in niche overlap (Figs. 1B, 2). Niche position may or may not differ between groups, depending on whether resource expansion/reduction takes place from the center of the isotopic niche space (no niche shift) or is directed away from that center (Figs. 1B, 1E, 2). For the third scenario, involving a discrete ontogenetic diet shift, (1) niche width of one group can either be the same, smaller or larger than the other (Fig. 1C, 1F), with (2) a distinct shift in niche position, resulting in (3) little or no overlap in isotopic niche (Figs. 1C, 1F, 2).
Niche aspects (i.e., niche width, niche position, and niche overlap) are shown in rectangles, and test types in diamonds; “Yes” = niche width or niche position differs between size classes, “No” = niche width or niche position does not differ between size classes. The three possible scenarios are represented in ovals, with “No Niche Shift” = first scenario, “Niche Expansion/Reduction” = second scenario, and “Discrete Niche Shift” = third scenario. Low = low niche overlap for both size classes; High = high niche overlap for both size classes; High/Low = asymmetric niche overlap between two size classes.
We used empirical data to illustrate these different niche shift scenarios. We chose these examples specifically to illustrate the methodological framework discussed herein, and not as independent tests of the nature of niche shifts in these particular taxa. For these taxa, we collected direct diet data (or in one case, published diet information) to further help us characterize and understand niche variation. Post-metamorphic Eupemphix nattereri frogs (i.e., no tadpoles), gray snapper (Lutjanus griseus) and hardhead silversides (Atherinomorus stipes) constituted the model species.
Post-metamorphic Eupemphix nattereri specimens were collected from an area of Brazilian savannahs locally known as Cerrado in the municipality of Uberlândia (18°55′ S, 48°17′ W) in southeastern Brazil, a region characterized by shrubby grassland areas surrounding wet areas such as veredas (marshes with buriti-palms Mauritia flexuosa) or temporal and permanent ponds. Frogs were collected from October 1999 to October 2001 and immediately killed upon collection, preserved in 5% formalin and later transferred to 70% ethanol. Since all individuals were preserved in the same manner, differences in isotope values among individuals should have not been affected by preservatives . Gut content analysis was performed via dissection and prey items were counted and identified to the lowest taxonomic level. Gut content data of E. nattereri are published elsewhere . Upon dissection, individuals were sexed by examination of gonads and classified as adults if the gonads were fully developed (reproductive) or as juveniles if gonads were underdeveloped (non-reproductive). We used a piece of muscle from the thigh to measure δ13C and δ15N .
Gray snapper (Lutjanus griseus) were collected in the Loxahatchee River (26°57′ N, 80°06′ W) located on the southeast Atlantic coast of Florida, USA. Snappers were caught during the summers of 2007 – 2009 by angling and electrofishing in the mesohaline areas of the river. Fish were anesthetized using eugenol  and their standard length was measured. Each individual was forced to regurgitate their stomach contents by pressing on the abdomen while using a metal spatula to help invert the stomach . Stomach content data of L. griseus are published elsewhere . A small sample (∼1cm2) of dorsal fin tissue was taken from each fish for stable isotope analysis. After sampling their stomach contents, fish were returned to ambient water and allowed to recover before being released. Since the size range of L. griseus in the Loxahatchee River does not include reproductively mature adults, we a priori divided the individuals into juveniles (<100 mm SL) and sub-adults (≥100 mm SL) based on observed differences in habitat use between these two life-history stages , .
Hardhead silversides (Atherinomorus stipes) were collected by cast netting in a tidal creek (26°21′36.58″N, 77°00′58.91″W) on Abaco Island, Bahamas on November 15th 2009. This creek is lined by mangroves (primarily red mangrove, Rhizophora mangle) and supports extensive seagrass beds predominantly consisting of turtle grass, Thalassia testudinum. The creek is dominated by marine waters with relatively little topographic relief, a small watershed, and little freshwater input . All captured individuals were immediately put on ice and later frozen. The whole organism was used for stable isotope analysis. Diet information of A. stipes was obtained by Boveri and Quiros . Based on gonad inspections, A. stipes was divided into juveniles (underdeveloped gonads) and adults (fully developed gonads).
We employed ratios of 15N to 14N and of 13C to 12C, and the stable isotope values are reported in the δ notation where δ13C = [(Rsample /Rstandard) – 1] ×1000, and where R is 13C / 12C and 15N / 14N, respectively. We focused on ratios of δ15N and δ13C because each reveals a distinct aspect of the consumer's long-term trophic niche (see above). PDB (PeeDee belemnite) and AIR (atmospheric nitrogen) are the global standards of δ13C and δ15N, respectively. Isotope sample preparation and analysis followed Post et al.  and was conducted at the Yale Earth System Center for Stable Isotopic Studies using a ThermoFinnigan DeltaPlus mass spectrometer (for L. griseus and A. stipes) and at the Centro de Energia Nuclear na Agricultura of the Universidade de São Paulo using a Micromass 602E mass spectrometer (for E. nattereri).
To evaluate for which ontogenetic niche shift scenario the model species met the criteria, we performed multivariate analyses, using δ13C and δ15N simultaneously, and “post-hoc” univariate analyses, separately on δ13C and δ15N. For the multivariate analyses, we first examined significant differences in (1) niche width and (2) niche position between the two groups, and then (3) niche overlap (Fig. 2). To do so, we performed a test for differences in dispersion and central tendency, respectively, following Turner et al.  in R version 2.12.2. In the context of this study, difference in dispersion represents a change in niche width because this metric measures the average trophic variability within size classes. More precisely, using analysis of nested linear models and residual permutation procedure, the mean distance to centroid (bivariate mean) was computed for each size class separately, and then the absolute value of the difference was evaluated between size classes. An absolute value greater than zero indicates a difference in niche width between size classes . Similarly, the difference in central tendency represents a shift in isotopic niche position and was measured by computing the Euclidean distance between the centroids of the two groups . The isotopic niche position was considered to be different if the Euclidean distance between the two groups was significantly greater than zero (R codes for the test of dispersion and central tendency are provided in the Appendix of Turner et al. ). The test statistics for dispersion and central tendency are herein referred to as “mean distance to centroid” and “Euclidean distance”, respectively.
Conventional univariate analysis was applied after significant results from multivariate analysis to provide additional detail. To this end, we first tested all data for normality (Shapiro-Wilk test) and square-root transformed them when applicable. Then, we examined shifts in niche width and niche position for each stable isotope element by measuring (1) homogeneity of variance between size classes using Bartlett's test and (2) by comparing mean isotopic values between size classes using t-test for independent samples (for normally distributed data) or Wilcox test (for non-normally distributed data). All tests were performed in R version 2.12.2. Significance was declared at α≤0.05.
We measured niche overlap between groups by quantifying, for each group, the percentage of individuals that were encompassed by the other group's convex hull , which is the area of the smallest convex polygon that contains all individuals of a group in a δ13C-δ15N-biplot (Figs. 1, 3) .The convex hull approach offers some advantages for characterizing niche width when compared to alternative analyses. The convex hull approach is powerful because it incorporates each individual of the population's sub-sample, and thus includes information about the niche width of the population including every sampled individual. Conversely, other approaches are targeted at identifying the “core” niche of the population, a niche metric which could exclude particular individual niches from the characterization of the population niche . Either of these approaches may be more relevant with respect to a particular question of interest and/or the nature of the underlying data set. Herein, we chose to measure niche overlap based on the convex hull approach, as the importance of individual level niche variation is increasingly recognized as an important component of ecological dynamics and evolutionary trajectories , .
Differences in niche width (for illustration purposes represented by convex hull polygons) of a small (solid line) and large (dashed line) size class of A) Eupemphix nattereri, B) Lutjanus griseus, and C) Atherinomorus stipes represented in a δ13C-δ15N niche space. Closed circles represent isotope data of individual juveniles and open circles individual adults (or sub-adults in case of L. griseus).
Since for many organisms body size is more important in determining life history characteristics than age per se , we used body size as a proxy for ontogenetic stage. More specifically, we used categorical size classes instead of continuous body size data (Fig. 1). Yet, for the univariate analyses, our framework could easily be applied to a continuous body size gradient, e.g., using linear regression (to test for non-zero slope, instead of comparing means between groups) when examining shifts in niche position. When categorical size groups are used, biologically meaningful size classes should be chosen (as in this study), or a break point analysis  could be performed, to determine the size at which change in resource use occur.
In this paper we use a traditional, frequentist approach (i.e., null hypothesis significance testing based on P-values) to evaluate which ontogenetic niche shift models best represent our empirical examples. Yet, our analytical framework can easily be applied to alternative statistical approaches (e.g., information theory or likelihood ratios) – to select which model (i.e., ontogenetic niche shift scenario) fits best the empirical data used.
For the illustration of the first ontogenetic niche shift scenario, we used 25 post-metamorphic juveniles (size range: 13–33mm Snout-Vent Length (SVL)) and 26 adults (size range: 34–47mm SVL) of E. nattereri. Juvenile and adult E. nattereri did not statistically differ in their (1) niche widths (mean distance to centroid = 0.08, P = 0.87), and (2) isotopic niche position (Euclidean distance = 0.41, P = 0.58; Fig. 3A). Individuals of both groups (3) overlapped substantially with each other (juveniles = 92% overlap with adults, adults = 85% overlap with juveniles, Fig. 3A).
Juvenile (n = 31, size range: 40–96mm Standard Length (SL)) and sub-adult (n = 89, size range: 101–204mm SL) L. griseus differed significantly in their (1) niche width (mean distance to centroid = 1.22, P = 0.006, Fig. 3B), which was driven by a difference in variance of δ13C values (Bartlett: K2 = 10.37, df = 1, P = 0.001), not δ15N (Bartlett: K2 = 1.07, df = 1, P = 0.3). There was no shift in (2) isotopic niche position (Euclidean distance = 0.94, P = 0.13; Fig. 3B) and (3) most juvenile L. griseus overlapped with the niche width of sub-adults (97% of individuals), whereas only 35% of sub-adults were encompassed by the convex hull of the juveniles (Fig. 3B).
Juveniles (n = 16, size range: 23–35mm SL) and adults (n = 14, size range: 40–61mm SL) of A. stipes differed significantly in (1) niche width (mean distance to centroid = 0.51, P = 0.01; Fig. 3C), which was caused by differences in variance of δ15N (Bartlett: K2 = 10.6, df = 1, P = 0.001), as well as δ13C (Bartlett: K2 = 3.85, df = 1, P = 0.05). In addition, the (2) isotopic niche position changed significantly between juvenile and adult A. stipes (Euclidean distance = 1.5, P<0.0001; Fig. 3C), which was driven by a change in their mean δ15N values (Wilcox: W = 224, P<0.001), but not mean δ13C values (t-test: t = 0.29, df = 20.3, P = 0.77). (3) No individuals were encompassed by the convex hull of the other group (Fig. 3C).
Because of the significant effects ontogenetic niche shifts can have on the structure and dynamics of populations, communities and ecosystems, it is important to identify the nature of these dietary shifts using quantitative techniques –. Stable isotope analysis is especially useful for this purpose because of its time- and space-integrated representation of diet , , . Yet, most studies using stable isotope ratios have examined ontogenetic niche shifts either qualitatively or by analyzing stable isotope elements separately , –. Quantitative measures analyzing isotope elements simultaneously are advantageous in identifying the nature of dietary shifts through ontogeny, offering increased knowledge of potential shifts in niche width, niche position and niche overlap, and can detect possible correlations among these elements . This study provides a hypothesis-testing framework to investigate ontogenetic niche shifts in organisms by applying univariate and multivariate analyses simultaneously on stable isotope elements. In doing so, we provide a foundation for exploring ontogenetic niche shifts in any organism of interest.
Post-metamorphic juveniles and adults of E. nattereri illustrate the first ontogenetic niche shift scenario: there were no differences in niche width and niche position between the two size classes, and they overlapped greatly (Fig. 3A). Since frogs can grow substantially after metamorphosis, they could be expected to experience considerable diet shifts during the terrestrial phase of their life cycle , but this was not found to be the case. Stomach content analysis supported the isotope analysis findings by showing that both juvenile and adult E. nattereri tend to specialize on ants and termites . Since stable isotope ratios of muscle tissue represent diet over a long time period (weeks to months, ), it can be inferred that the observed diet specialization was long-term, and not just based on local prey availability at the time of sampling (an advantage of stable isotope analysis over stomach content analysis, ).
Gray snapper illustrate the second ontogenetic niche shift scenario: sub-adult L. griseus expanded their isotopic niche to include diet items with more depleted δ13C values (Fig. 3B). Direct diet analysis confirmed that the feeding of juvenile L. griseus was essentially confined to the oyster reef matrix of the Loxahatchee River, where their diet was composed almost entirely of oyster reef-associated prey items (i.e., mud crabs, Eurypanopeus sp. and Panopeus sp.). Conversely, sub-adult L. griseus move to the adjacent mangrove habitats to feed on mangrove-associated prey (i.e., green mangrove tree crab, Aratus pisonii) . Prey items in oyster reef habitats are largely supported by microalgae- and phytoplankton-based trophic pathways that are more enriched in δ13C values (∼ -18 0/00), whereas prey from mangrove-based food web modules are more depleted (δ13C ∼ -27 0/00) , . Sub-adults most likely increased their foraging area because of decreased predation pressure or increased mobility due to larger body size . Such foraging and predation risk trade-offs and/or increase in mobility with body size can drive many ontogenetic niche shifts, and stable isotope ratios can be a prime tool to reflect such long-term feeding shifts when isotopic signatures of sources are distinct.
Juvenile and adult A. stipes displayed a distinct niche shift, mainly along the δ15N axis (Fig. 3C). Since A. stipes is a visual feeder that actively selects zooplankton , no major ontogenetic niche shift would be expected for that species. Yet, our stable isotope data suggest that adults likely fed exclusively on larger-sized zooplankton prey, as larger zooplankton are often more enriched in δ15N . Since adult and juvenile A. stipes share the same resources (i.e., habitat and diet), adults might shift to larger prey sizes as a means to reduce intrapopulation niche competition .
Our empirical examples highlight the benefit of using both univariate and multivariate measures, as each was useful to identify different aspects of the niche differences. For example, in the case of gray snapper, multivariate approaches were useful in identifying degree of niche width and niche overlap, whereas univariate analysis was important to elucidate niche expansion in the larger size class primarily along the carbon axis. It would be difficult to differentiate among the three major niche shift scenarios by using univariate analyses alone (Fig. 1D–F).
When applying the proposed framework, it is important to consider that the three ontogenetic niche shift scenarios outlined in this study should be understood as endpoints of a continuum. Many organisms might fall between the endpoint scenarios. In addition, statistical significance does not always equate to biological importance, and vice versa , and thus caution should be exerted when interpreting empirical data. The much discussed limitations of isotopes must also be considered when interpreting their application to study ontogenetic diet shifts , , . For instance, source pools need to have distinct isotopic signatures for stable isotopes to be useful, and δ values can be particularly sensitive to spatial and temporal variation in isotope values of source pools. As such, scattering among consumers in a δ13C-δ15N biplot could be the result of a broad resource use among individuals, or due to high variation in isotope values of source pools. Consequently, the use of a complimentary method such as stomach content analysis (as applied in this study), fecal analysis, or direct observations are useful to interpret and better understand patterns in isotope signatures. When stable isotope ratios are put in the proper context, they can be a very powerful tool  and provide insights that would not be possible with some conventional methods .
Intrapopulation resource variation has critical ecological, evolutionary and conservation implications , , and ontogenetic niche shifts are one primary driver of this variation . Our approach provides a framework for exploring questions related to ontogenetic diet shifts, as well as other among-group (e.g., sex or phenotype) comparisons. Such studies are critical for understanding interactions among individuals at population, community and ecosystem levels.
We thank all people that helped with field work, data analysis, and manuscript editing, especially J. Vaudo, A. Mercado, A. Yoc-Kim, C. Villegas, and T. Turner.
Conceived and designed the experiments: CMHP CAL. Performed the experiments: CMHP LAY MSA CAL. Analyzed the data: CMHP LAY MSA. Contributed reagents/materials/analysis tools: CMHP LAY MSA CAL. Wrote the paper: CMHP CAL.
- 1. Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill - the foraging rate predation risk trade-off. Ecology 69: 1352–1366.EE WernerDJ Hall1988Ontogenetic habitat shifts in bluegill - the foraging rate predation risk trade-off.Ecology6913521366
- 2. Claessen D, Van Oss C, de Roos AM, Persson L (2002) The impact of size-dependent predation on population dynamics and individual life history. Ecology 83: 1660–1675.D. ClaessenC. Van OssAM de RoosL. Persson2002The impact of size-dependent predation on population dynamics and individual life history.Ecology8316601675
- 3. Polis GA, Strong DR (1996) Food web complexity and community dynamics. American Naturalist 147: 813–846.GA PolisDR Strong1996Food web complexity and community dynamics.American Naturalist147813846
- 4. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation - potential competitiors that eat each other. Annual Review of Ecology and Systematics 20: 297–330.GA PolisCA MyersRD Holt1989The ecology and evolution of intraguild predation - potential competitiors that eat each other.Annual Review of Ecology and Systematics20297330
- 5. Stein RA, Threlkeld ST, Sandgren CD, Sprules WG, Persson L, et al. (1988) Size-structured interactions in lake communities. In: Carpenter SR, editor. Complex interactions in lake communities. New York, USA: Springer-Verlag. pp. 161–180.RA SteinST ThrelkeldCD SandgrenWG SprulesL. Persson1988Size-structured interactions in lake communities.SR CarpenterComplex interactions in lake communitiesNew York, USASpringer-Verlag161180
- 6. Olson MH, Mittelbach GG, Osenberg CW (1995) Competition between predator and prey - resource-based mechanisms and implications for stage-structured dynamics. Ecology 76: 1758–1771.MH OlsonGG MittelbachCW Osenberg1995Competition between predator and prey - resource-based mechanisms and implications for stage-structured dynamics.Ecology7617581771
- 7. Persson L (1988) Asymmetries in competitive and predatory interactions in fish populations. In: Ebenman B, Persson L, editors. Size-structured populations: ecology and evolution. Berlin, Germany: Springer-Verlag. pp. 203–218.L. Persson1988Asymmetries in competitive and predatory interactions in fish populations.B. EbenmanL. PerssonSize-structured populations: ecology and evolutionBerlin, GermanySpringer-Verlag203218
- 8. Minns CK (1995) Allometry of home-range size in lake and river fishes. Canadian Journal of Fisheries and Aquatic Sciences 52: 1499–1508.CK Minns1995Allometry of home-range size in lake and river fishes.Canadian Journal of Fisheries and Aquatic Sciences5214991508
- 9. Subalusky AL, Fitzgerald LA, Smith LL (2009) Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems. Biological Conservation 142: 1507–1514.AL SubaluskyLA FitzgeraldLL Smith2009Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems.Biological Conservation14215071514
- 10. Olson MH (1996) Ontogenetic niche shifts in largemouth bass: Variability and consequences for first-year growth. Ecology 77: 179–190.MH Olson1996Ontogenetic niche shifts in largemouth bass: Variability and consequences for first-year growth.Ecology77179190
- 11. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annual Review of Ecology and Systematics 15: 393–425.EE WernerJF Gilliam1984The ontogenetic niche and species interactions in size structured populations.Annual Review of Ecology and Systematics15393425
- 12. Bernays EA (2001) Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation. Annual Review of Entomology 46: 703–727.EA Bernays2001Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation.Annual Review of Entomology46703727
- 13. Hammerschlag-Peyer CM, Layman CA(In Revision) Factors affecting resource use variation in an abundant coastal fish predator, Lutjanus apodus, in a Bahamian wetland system. Bulletin of Marine Science. CM Hammerschlag-PeyerCA Layman(In Revision) Factors affecting resource use variation in an abundant coastal fish predator, Lutjanus apodus, in a Bahamian wetland system.Bulletin of Marine Science
- 14. Wilbur HM (1980) Complex life-cycles. Annual Review of Ecology and Systematics 11: 67–93.HM Wilbur1980Complex life-cycles.Annual Review of Ecology and Systematics116793
- 15. Grossman GD (1980) Ecological aspects of ontogenetic shifts in prey size utilization in the bay goby (Pisces:Gobiidae). Oecologia 47: 233–238.GD Grossman1980Ecological aspects of ontogenetic shifts in prey size utilization in the bay goby (Pisces:Gobiidae).Oecologia47233238
- 16. Keast A (1977) Mechanisms expanding niche width and minimizing intraspecific competition in two centrarchid fishes. In: Hecht MK, Steere WC, Wallace B, editors. Evolutionary Biology. New York: Plenum. pp. 333–395.A. Keast1977Mechanisms expanding niche width and minimizing intraspecific competition in two centrarchid fishes.MK HechtWC SteereB. WallaceEvolutionary BiologyNew YorkPlenum333395
- 17. Werner EE (1979) Niche partitioning by food size in fish communities. In: Stroud RH, Clepper H, editors. Predator-Prey Systems in Fisheries Management. Washington DC: Sport Fish. Inst. pp. 311–322.EE Werner1979Niche partitioning by food size in fish communities.RH StroudH. ClepperPredator-Prey Systems in Fisheries ManagementWashington DCSport Fish. Inst311322
- 18. Hentschel BT (1998) Intraspecific variations in delta C-13 indicate ontogenetic diet changes in deposit-feeding polychaetes. Ecology 79: 1357–1370.BT Hentschel1998Intraspecific variations in delta C-13 indicate ontogenetic diet changes in deposit-feeding polychaetes.Ecology7913571370
- 19. Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, et al. (In Press) Applying Stable Isotopes to Examine Food Web Structure: An Overview of Analytical Tools. Biological Reviews (Cambridge). CA LaymanMS AraujoR. BoucekCM Hammerschlag-PeyerE. Harrison(In Press) Applying Stable Isotopes to Examine Food Web Structure: An Overview of Analytical Tools.Biological Reviews (Cambridge)
- 20. Newsome SD, del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5: 429–436.SD NewsomeCM del RioS. BearhopDL Phillips2007A niche for isotopic ecology.Frontiers in Ecology and the Environment5429436
- 21. Peterson BJ, Fry B (1987) Stable isotopes in ecoysystem studies. Annual Review of Ecology and Systematics 18: 293–320.BJ PetersonB. Fry1987Stable isotopes in ecoysystem studies.Annual Review of Ecology and Systematics18293320
- 22. Cocheret de la Morinière E, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, et al. (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Marine Ecology-Progress Series 246: 279–289.E. Cocheret de la MorinièreBJA PolluxI. NagelkerkenMA HemmingaAHL Huiskes2003Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis.Marine Ecology-Progress Series246279289
- 23. Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84: 1298–1310.DM Post2003Individual variation in the timing of ontogenetic niche shifts in largemouth bass.Ecology8412981310
- 24. Rolff C (2000) Seasonal variation in delta C-13 and delta N-15 of size-fractionated plankton at a coastal station in the northern Baltic proper. Marine Ecology-Progress Series 203: 47–65.C. Rolff2000Seasonal variation in delta C-13 and delta N-15 of size-fractionated plankton at a coastal station in the northern Baltic proper.Marine Ecology-Progress Series2034765
- 25. Quevedo M, Olsson J (2006) The effect of small-scale resource origin on trophic position estimates in Perca fluviatilis. Journal of Fish Biology 69: 141–150.M. QuevedoJ. Olsson2006The effect of small-scale resource origin on trophic position estimates in Perca fluviatilis.Journal of Fish Biology69141150
- 26. Young HS, Shaffer SA, McCauley DJ, Foley DG, Dirzo R, et al. (2010) Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean. Marine Ecology-Progress Series 403: 291–301.HS YoungSA ShafferDJ McCauleyDG FoleyR. Dirzo2010Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean.Marine Ecology-Progress Series403291301
- 27. Zimmerman MS, Schmidt SN, Krueger CC, Vander Zanden MJ, Eshenroder RL (2009) Ontogenetic niche shifts and resource partitioning of lake trout morphotypes. Canadian Journal of Fisheries and Aquatic Sciences 66: 1007–1018.MS ZimmermanSN SchmidtCC KruegerMJ Vander ZandenRL Eshenroder2009Ontogenetic niche shifts and resource partitioning of lake trout morphotypes.Canadian Journal of Fisheries and Aquatic Sciences6610071018
- 28. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.AL JacksonR. IngerAC ParnellS. Bearhop2011Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R.Journal of Animal Ecology80595602
- 29. Semmens BX, Ward EJ, Moore JW, Darimont CT (2009) Quantifying Inter- and Intra-Population Niche Variability Using Hierarchical Bayesian Stable Isotope Mixing Models. PLoS ONE 4: BX SemmensEJ WardJW MooreCT Darimont2009Quantifying Inter- and Intra-Population Niche Variability Using Hierarchical Bayesian Stable Isotope Mixing Models.PLoS ONE4
- 30. Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecology Letters 10: 937–944.CA LaymanJP QuattrochiCM PeyerJE Allgeier2007Niche width collapse in a resilient top predator following ecosystem fragmentation.Ecology Letters10937944
- 31. Quevedo M, Svanback R, Eklov P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90: 2263–2274.M. QuevedoR. SvanbackP. Eklov2009Intrapopulation niche partitioning in a generalist predator limits food web connectivity.Ecology9022632274
- 32. Zar JH (1999) Biostatistical Analysis. Delhi, India: Pearson Education. JH Zar1999Biostatistical Analysis.Delhi, IndiaPearson Education
- 33. France RL, Peters RH (1997) Ecosystem differences in the trophic enrichment of C-13 in aquatic food webs. Canadian Journal of Fisheries and Aquatic Sciences 54: 1255–1258.RL FranceRH Peters1997Ecosystem differences in the trophic enrichment of C-13 in aquatic food webs.Canadian Journal of Fisheries and Aquatic Sciences5412551258
- 34. Layman CA (2007) What can stable isotope ratios reveal about mangroves as fish habitat? Bulletin of Marine Science 80: 513–527.CA Layman2007What can stable isotope ratios reveal about mangroves as fish habitat?Bulletin of Marine Science80513527
- 35. Rounick JS, Winterbourn MJ (1986) Stable carbon isotopes and carbon flow in ecosystems. Bioscience 36: 171–177.JS RounickMJ Winterbourn1986Stable carbon isotopes and carbon flow in ecosystems.Bioscience36171177
- 36. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica Et Cosmochimica Acta 45: 341–351.MJ DeNiroS. Epstein1981Influence of diet on the distribution of nitrogen isotopes in animals.Geochimica Et Cosmochimica Acta45341351
- 37. Minagawa M, Wada E (1984) Stepwise enrichment of N-15 along food-chains - Further evidence and the relation between Delta-N-15 and animal age. Geochimica Et Cosmochimica Acta 48: 1135–1140.M. MinagawaE. Wada1984Stepwise enrichment of N-15 along food-chains - Further evidence and the relation between Delta-N-15 and animal age.Geochimica Et Cosmochimica Acta4811351140
- 38. Vaudo JJ, Heithaus MR (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology-Progress Series 425: 247–260.JJ VaudoMR Heithaus2011Dietary niche overlap in a nearshore elasmobranch mesopredator community.Marine Ecology-Progress Series425247260
- 39. Araujo MS, Bolnick DI, Martinelli LA, Giaretta AA, dos Reis SF (2009) Individual-level diet variation in four species of Brazilian frogs. Journal of Animal Ecology 78: 848–856.MS AraujoDI BolnickLA MartinelliAA GiarettaSF dos Reis2009Individual-level diet variation in four species of Brazilian frogs.Journal of Animal Ecology78848856
- 40. Cotter PA, Rodruck KJ (2006) Differential effects of anesthetics on electrical properties of the rainbow trout (Oncorhynchus mykiss) heart. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology 145: 158–165.PA CotterKJ Rodruck2006Differential effects of anesthetics on electrical properties of the rainbow trout (Oncorhynchus mykiss) heart.Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology145158165
- 41. Yeager LA, Layman CA (2011) Energy flow to two abundant consumers in a sub-tropical oyster reef food web. Aquatic Ecology 45: 267–277.LA YeagerCA Layman2011Energy flow to two abundant consumers in a sub-tropical oyster reef food web.Aquatic Ecology45267277
- 42. Hammerschlag N, Serafy JE (2009) Nocturnal fish utilization of a subtropical mangrove-seagrass ecotone. Marine Ecology-an Evolutionary Perspective 31: 364–374.N. HammerschlagJE Serafy2009Nocturnal fish utilization of a subtropical mangrove-seagrass ecotone.Marine Ecology-an Evolutionary Perspective31364374
- 43. Faunce CH, Serafy JE (2007) Nearshore habitat use by gray snapper (Lutjanus griseus) and bluestriped grunt (Haemulon sciurus): environmental gradients and ontogenetic shifts. Bulletin of Marine Science 80: 473–495.CH FaunceJE Serafy2007Nearshore habitat use by gray snapper (Lutjanus griseus) and bluestriped grunt (Haemulon sciurus): environmental gradients and ontogenetic shifts.Bulletin of Marine Science80473495
- 44. Boveri MB, Quiros R (2002) Tropic interactions in pampean shallow lakes: evaluation of silverside predatory effects in mesocosm experiments. Verhandlungen des Internationalen Verein Limnologie 28: 1–5.MB BoveriR. Quiros2002Tropic interactions in pampean shallow lakes: evaluation of silverside predatory effects in mesocosm experiments.Verhandlungen des Internationalen Verein Limnologie2815
- 45. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, et al. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.DM PostCA LaymanDA ArringtonG. TakimotoJ. Quattrochi2007Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.Oecologia152179189
- 46. Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91: 2227–2233.TF TurnerML CollyerTJ Krabbenhoft2010A general hypothesis-testing framework for stable isotope ratios in ecological studies.Ecology9122272233
- 47. Layman CA, Arrington DA, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.CA LaymanDA ArringtonCG MontanaDM Post2007Can stable isotope ratios provide for community-wide measures of trophic structure?Ecology884248
- 48. Bolnick DI, Amarasekare P, Araujo MS, Burger R, Levine JM, et al. (2011) Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution 26: 183–192.DI BolnickP. AmarasekareMS AraujoR. BurgerJM Levine2011Why intraspecific trait variation matters in community ecology.Trends in Ecology & Evolution26183192
- 49. Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, et al. (2003) The ecology of individuals: Incidence and implications of individual specialization. American Naturalist 161: 1–28.DI BolnickR. SvanbackJA FordyceLH YangJM Davis2003The ecology of individuals: Incidence and implications of individual specialization.American Naturalist161128
- 50. Kirkpatrick M (1984) Demographic-models based on size, not age, for organisms with indeterminate growth Ecology 65: 1874–1884.M. Kirkpatrick1984Demographic-models based on size, not age, for organisms with indeterminate growth Ecology6518741884
- 51. Gomez KA, Gomez AA (1984) Statistical Procedures for Agricultural Research. New York: Wiley Interscience. 680 p.KA GomezAA Gomez1984Statistical Procedures for Agricultural Research.New YorkWiley Interscience680
- 52. Hobbs NT, Hilborn R (2006) Alternatives to statistical hypothesis testing in ecology: A guide to self teaching. Ecological Applications 16: 5–19.NT HobbsR. Hilborn2006Alternatives to statistical hypothesis testing in ecology: A guide to self teaching.Ecological Applications16519
- 53. Burnham KP, Anderson DR (2002) Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach. New York: Springer. 496 p.KP BurnhamDR Anderson2002Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach.New YorkSpringer496
- 54. Anderson DR (2008) Model Based Inference in the Life Sciences: A Primer on Evidence. New York: Springer. 208 p.DR Anderson2008Model Based Inference in the Life Sciences: A Primer on Evidence.New YorkSpringer208
- 55. Royall RM (1997) Statistical evidence: a likelihood paradigm. London: Chapman & Hall. 191 p.RM Royall1997Statistical evidence: a likelihood paradigm.LondonChapman & Hall191
- 56. Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73: 1007–1012.S. BearhopCE AdamsS. WaldronRA FullerH. Macleod2004Determining trophic niche width: a novel approach using stable isotope analysis.Journal of Animal Ecology7310071012
- 57. Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83: 703–718.DM Post2002Using stable isotopes to estimate trophic position: Models, methods, and assumptions.Ecology83703718
- 58. Landman NH, Rye DM, Shelton KL (1983) Early ontogeny of eutrephoceras compared to recent nautilus and mesozoic ammonites - evidence from shell morphology and light stable isotopes. Paleobiology 9: 269–279.NH LandmanDM RyeKL Shelton1983Early ontogeny of eutrephoceras compared to recent nautilus and mesozoic ammonites - evidence from shell morphology and light stable isotopes.Paleobiology9269279
- 59. Lukeneder A, Harzhauser M, Mullegger S, Piller WE (2010) Ontogeny and habitat change in Mesozoic cephalopods revealed by stable isotopes (delta O-18, delta C-13). Earth and Planetary Science Letters 296: 103–114.A. LukenederM. HarzhauserS. MulleggerWE Piller2010Ontogeny and habitat change in Mesozoic cephalopods revealed by stable isotopes (delta O-18, delta C-13).Earth and Planetary Science Letters296103114
- 60. Mueller-Lupp T, Erlenkeuser H, Bauch HA (2003) Seasonal and interannual variability of Siberian river discharge in the Laptev Sea inferred from stable isotopes in modern bivalves. Boreas 32: 292–303.T. Mueller-LuppH. ErlenkeuserHA Bauch2003Seasonal and interannual variability of Siberian river discharge in the Laptev Sea inferred from stable isotopes in modern bivalves.Boreas32292303
- 61. Taylor MD, Mazumder D (2010) Stable isotopes reveal post-release trophodynamic and ontogenetic changes in a released finfish, mulloway (Argyrosomus japonicus). Marine and Freshwater Research 61: 302–308.MD TaylorD. Mazumder2010Stable isotopes reveal post-release trophodynamic and ontogenetic changes in a released finfish, mulloway (Argyrosomus japonicus).Marine and Freshwater Research61302308
- 62. Sweeting CJ, Jennings S, Polunin NVC (2005) Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Functional Ecology 19: 777–784.CJ SweetingS. JenningsNVC Polunin2005Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory.Functional Ecology19777784
- 63. Araujo MS, Bolnick DI, Machado G, Giaretta AA, dos Reis SF (2007) Using delta C-13 stable isotopes to quantify individual-level diet variation. Oecologia 152: 643–654.MS AraujoDI BolnickG. MachadoAA GiarettaSF dos Reis2007Using delta C-13 stable isotopes to quantify individual-level diet variation.Oecologia152643654
- 64. Kieckbusch DK, Koch MS, Serafy JE, Anderson WT (2004) Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons. Bulletin of Marine Science 74: 271–285.DK KieckbuschMS KochJE SerafyWT Anderson2004Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons.Bulletin of Marine Science74271285
- 65. Jones D, Matloff N (1986) Statistical hypothesis-testing in biology - a contradiction in terms. Journal of Economic Entomology 79: 1156–1160.D. JonesN. Matloff1986Statistical hypothesis-testing in biology - a contradiction in terms.Journal of Economic Entomology7911561160
- 66. Layman CA, Post DM (2008) Can stable isotope ratios provide for community-wide measures of trophic structure? Reply. Ecology 89: 2358–2359.CA LaymanDM Post2008Can stable isotope ratios provide for community-wide measures of trophic structure? Reply.Ecology8923582359