Kelton W. McMahon

Using Isoscapes to Trace the Movements and Foraging Behavior of Top Predators in Oceanic Ecosystems

The stable isotope composition of animal tissues can provide intrinsic tags to study the foraging and migratory ecology of predators in the open ocean. Chapter 13 (this volume) demonstrated that by comparing the isotope values of an animal and its local prey or environment, the animal’s movements can be estimated, given that isotopic variation exists between habitats. The utility of using geographical variations in stable isotopes values, or isoscapes to study the movements of marine predators has been limited because of our lack of knowledge on the spatial variation of the carbon, nitrogen, and oxygen isotope values in the open ocean.

Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein.

1. Analysis of stable carbon isotopes is a valuable tool for studies of diet, habitat use and migration. However, significant variability in the degree of trophic fractionation (Delta(13)C(C-D)) between consumer (C) and diet (D) has highlighted our lack of understanding of the biochemical and physiological underpinnings of stable isotope ratios in tissues. 2. An opportunity now exists to increase the specificity of dietary studies by analyzing the delta(13)C values of amino acids (AAs). Common mummichogs (Fundulus heteroclitus, Linnaeus 1766) were reared on four isotopically distinct diets to examine individual AA Delta(13)C(C-D) variability in fish muscle. 3. Modest bulk tissue Delta(13)C(C-D) values reflected relatively large trophic fractionation for many non-essential AAs and little to no fractionation for all essential AAs. 4. Essential AA delta(13)C values were not significantly different between diet and consumer (Delta(13)C(C-D) = 0.0 +/- 0.4 per thousand), making them ideal tracers of carbon sources at the base of the food web. Stable isotope analysis of muscle essential AAs provides a promising tool for dietary reconstruction and identifying baseline delta(13)C values to track animal movement through isotopically distinct food webs. 5. Non-essential AA Delta(13)C(C-D) values showed evidence of both de novo biosynthesis and direct isotopic routing from dietary protein. We attributed patterns in Delta(13)C(C-D) to variability in protein content and AA composition of the diet as well as differential utilization of dietary constituents contributing to the bulk carbon pool. This variability illustrates the complicated nature of metabolism and suggests caution must be taken with the assumptions used to interpret bulk stable isotope data in dietary studies. 6. Our study is the first to investigate the expression of AA Delta(13)C(C-D) values for a marine vertebrate and should provide for significant refinements in studies of diet, habitat use and migration using stable isotopes.

Transequatorial migrations by basking sharks in the western Atlantic Ocean.

The worlds second largest fish, the basking shark (Cetorhinus maximus), is broadly distributed in boreal to warm temperate latitudes of the Atlantic and Pacific oceans from shallow coastal waters to the open ocean. Previous satellite archival tagging in the North Atlantic has shown that basking sharks move seasonally, are often associated with productive frontal zones, and may make occasional dives to mesopelagic depths. However, basking sharks are thought to be restricted to temperate latitudes, and the extent to which they exploit deeper-water habitat remains enigmatic. Via satellite archival tags and a novel geolocation technique, we demonstrate here that basking sharks are seasonal migrants to mesopelagic tropical waters. Tagged sharks moved from temperate feeding areas off the coast of southern New England to the Bahamas, the Caribbean Sea, and onward to the coast of South America and into the Southern Hemisphere. When in these areas, basking sharks descended to mesopelagic depths and in some cases remained there for weeks to months at a time. Our results demonstrate that tropical waters are not a barrier to migratory connectivity for basking shark populations and highlight the need for global conservation efforts throughout the species range.

Bivalves as indicators of environmental variation and potential anthropogenic impacts in the southern Barents Sea.

Identifying patterns and drivers of natural variability in populations is necessary to gauge potential effects of climatic change and the expected increases in commercial activities in the Arctic on communities and ecosystems. We analyzed growth rates and shell geochemistry of the circumpolar Greenland smooth cockle, Serripes groenlandicus, from the southern Barents Sea over almost 70 years between 1882 and 1968. The datasets were calibrated via annually-deposited growth lines, and growth, stable isotope (delta(18)O, delta(13)C), and trace elemental (Mg, Sr, Ba, Mn) patterns were linked to environmental variations on weekly to decadal scales. Standardized growth indices revealed an oscillatory growth pattern with a multi-year periodicity, which was inversely related to the North Atlantic Oscillation Index (NAO), and positively related to local river discharge. Up to 60% of the annual variability in Ba/Ca could be explained by variations in river discharge at the site closest to the rivers, but the relationship disappeared at a more distant location. Patterns of delta(18)O, delta(13)C, and Sr/Ca together provide evidence that bivalve growth ceases at elevated temperatures during the fall and recommences at the coldest temperatures in the early spring, with the implication that food, rather than temperature, is the primary driver of bivalve growth. The multi-proxy approach of combining the annually integrated information from the growth results and higher resolution geochemical results yielded a robust interpretation of biophysical coupling in the region over temporal and spatial scales. We thus demonstrate that sclerochronological proxies can be useful retrospective analytical tools for establishing a baseline of ecosystem variability in assessing potential combined impacts of climatic change and increasing commercial activities on Arctic communities.

Diet and movement of the killifish,Fundulus heteroclitus, in a Maine salt marsh assessed using gut contents and stable isotope analyses

Killifish are ecologically important components of salt marsh ecosystems, but no studies have determined the importance of locally produced versus allochthonous food sources on a scale of less than multiple kilometers. The goal of our study was to examine diet and movement of the killifish,Fundulus heteroclitus, collected from a Maine salt marsh to assess the importance of locally produced versus allochthonous food sources on a scale of several hundred meters. We compared the gut contents and stable isotope signatures ofF. heteroclitus from four regions along the central river of a Maine salt marsh to the distinct food sources and isotopic signatures of the region of the marsh in which they were caught.F. heteroclitus were relying on locally produced food sources even on the scale of several hundred meters. They fed daily in a small area less than 6 ha and maintained relatively strong site fidelities over the course of several months. Phytoplankton and salt marsh detritus both contributed to the high production ofF. heteroclitus; terrestrial plant detritus was not an important component of their diet. The diet and feeding patterns ofF. heteroclitus from this small Maine salt marsh were similar to the patterns found in much larger salt marshes, suggesting that locally produced organic matter is essential to the production of these ecologically important fish.

Linking habitat mosaics and connectivity in a coral reef seascape

Tropical marine ecosystems are under mounting anthropogenic pressure from overfishing and habitat destruction, leading to declines in their structure and function on a global scale. Although maintaining connectivity among habitats within a seascape is necessary for preserving population resistance and resilience, quantifying movements of individuals within seascapes remains challenging. Traditional methods of identifying and valuing potential coral reef fish nursery habitats are indirect, often relying on visual surveys of abundance and correlations of size and biomass among habitats. We used compound-specific stable isotope analyses to determine movement patterns of commercially important fish populations within a coral reef seascape. This approach allowed us to quantify the relative contributions of individuals from inshore nurseries to reef populations and identify migration corridors among important habitats. Our results provided direct measurements of remarkable migrations by juvenile snapper of over 30 km, between nurseries and reefs. We also found significant plasticity in juvenile nursery residency. Although a majority of individuals on coastal reefs had used seagrass nurseries as juveniles, many adults on oceanic reefs had settled directly into reef habitats. Moreover, seascape configuration played a critical but heretofore unrecognized role in determining connectivity among habitats. Finally, our approach provides key quantitative data necessary to estimate the value of distinctive habitats to ecosystem services provided by seascapes.

Carbon and nitrogen isotope fractionation of amino acids in an avian marine predator, the gentoo penguin (Pygoscelis papua)

Compound-specific stable isotope analysis (CSIA) of amino acids (AA) has rapidly become a powerful tool in studies of food web architecture, resource use, and biogeochemical cycling. However, applications to avian ecology have been limited because no controlled studies have examined the patterns in AA isotope fractionation in birds. We conducted a controlled CSIA feeding experiment on an avian species, the gentoo penguin (Pygoscelis papua), to examine patterns in individual AA carbon and nitrogen stable isotope fractionation between diet (D) and consumer (C) (Δ13CC-D and Δ15NC-D, respectively). We found that essential AA δ13C values and source AA δ15N values in feathers showed minimal trophic fractionation between diet and consumer, providing independent but complimentary archival proxies for primary producers and nitrogen sources respectively, at the base of food webs supporting penguins. Variations in nonessential AA Δ13CC-D values reflected differences in macromolecule sources used for biosynthesis (e.g., protein vs. lipids) and provided a metric to assess resource utilization. The avian-specific nitrogen trophic discrimination factor (TDFGlu-Phe = 3.5 ± 0.4‰) that we calculated from the difference in trophic fractionation (Δ15NC-D) of glutamic acid and phenylalanine was significantly lower than the conventional literature value of 7.6‰. Trophic positions of five species of wild penguins calculated using a multi-TDFGlu-Phe equation with the avian-specific TDFGlu-Phe value from our experiment provided estimates that were more ecologically realistic than estimates using a single TDFGlu-Phe of 7.6‰ from the previous literature. Our results provide a quantitative, mechanistic framework for the use of CSIA in nonlethal, archival feathers to study the movement and foraging ecology of avian consumers.

Carbon isotopes in otolith amino acids identify residency of juvenile snapper (Family: Lutjanidae) in coastal nurseries

This study explored the potential for otolith geochemistry in snapper (Family: Lutjanidae) to identify residency in juvenile nursery habitats with distinctive carbon isotope values. Conventional bulk otolith and muscle stable isotope analyses (SIA) and essential amino acid (AA) SIA were conducted on snapper collected from seagrass beds, mangroves, and coral reefs in the Red Sea, Caribbean Sea, and Pacific coast of Panama. While bulk stable isotope values in otoliths showed regional differences, they failed to distinguish nursery residence on local scales. Essential AA δ13C values in otoliths, on the other hand, varied as a function of habitat type and provided a better tracer of residence in different juvenile nursery habitats than conventional bulk otolith SIA alone. A strong linear relationship was found between paired otolith and muscle essential AA δ13C values regardless of species, geographic region, or habitat type, indicating that otolith AAs recorded the same dietary information as muscle AAs. Juvenile snapper in the Red Sea sheltered in mangroves but fed in seagrass beds, while snapper from the Caribbean Sea and Pacific coast of Panama showed greater reliance on mangrove-derived carbon. Furthermore, compound-specific SIA revealed that microbially recycled detrital carbon, not water-column-based new phytoplankton carbon, was the primary carbon source supporting snapper production on coastal reefs of the Red Sea. This study presented robust tracers of juvenile nursery residence that will be crucial for reconstructing ontogenetic migration patterns of fishes among coastal wetlands and coral reefs. This information is key to determining the importance of nursery habitats to coral reef fish populations and will provide valuable scientific support for the design of networked marine-protected areas.

Millennial-scale plankton regime shifts in the subtropical North Pacific Ocean

Community changes centuries in the making How might climate change affect the base of the marine food chain? Phytoplankton, the foundation of the marine ecosystem, depend on ambient oceanographic conditions such as temperature, salinity, and nutrient availability, which affect ocean chemistry and isotopic distributions. McMahon et al. report carbon isotopic composition changes in the North Pacific Ocean over the past 1000 years, which reflect changes in the community composition of phytoplankton in the region (see the Perspective by Vogt). An ongoing trend toward greater prevalence of nitrogen-fixing cyanobacteria that began 100 years ago might lead to a more efficient carbon pump and remove increasing amounts of CO2 from the atmosphere. Science, this issue p. 1530; see also p. 1466 Phytoplankton communities in the Pacific have changed markedly over the past thousand years. [Also see Perspective by Vogt] Climate change is predicted to alter marine phytoplankton communities and affect productivity, biogeochemistry, and the efficacy of the biological pump. We reconstructed high-resolution records of changing plankton community composition in the North Pacific Ocean over the past millennium. Amino acid–specific δ13C records preserved in long-lived deep-sea corals revealed three major plankton regimes corresponding to Northern Hemisphere climate periods. Non–dinitrogen-fixing cyanobacteria dominated during the Medieval Climate Anomaly (950–1250 Common Era) before giving way to a new regime in which eukaryotic microalgae contributed nearly half of all export production during the Little Ice Age (~1400–1850 Common Era). The third regime, unprecedented in the past millennium, began in the industrial era and is characterized by increasing production by dinitrogen-fixing cyanobacteria. This picoplankton community shift may provide a negative feedback to rising atmospheric carbon dioxide concentrations.

Functional connectivity of coral reef fishes in a tropical seascape assessed by compound-specific stable isotope analyses

Analysis of stable carbon isotopes is a valuable tool for studies of diet, habitat use, and migration. However, significant variability in the degree of trophic fractionation (ΔCC-D) between consumer (C) and diet (D) has highlighted our lack of understanding of the biochemical and physiological underpinnings of stable isotope ratios in tissues. An opportunity now exists to increase the specificity of dietary studies by analyzing the δC values of amino acids (AAs). Common mummichogs (Fundulus heteroclitus, Linnaeus 1766) were reared on four isotopically distinct diets to examine individual AA ∆CC-D variability in fish muscle. Modest bulk tissue ΔCC-D values reflected relatively large trophic fractionation for many non-essential AAs and little to no fractionation for all essential AAs. Essential AA δC values were not significantly different between diet and consumer (ΔCC-D = 0.0 ± 0.4‰), making them ideal tracers of carbon sources at the base of the food web. Stable isotope analysis of muscle essential AAs provides a promising tool for dietary reconstruction and identifying baseline δC values to track animal movement through isotopically distinct food webs. Non-essential AA ΔCC-D values showed evidence of both de novo biosynthesis and direct isotopic routing from dietary protein. We attributed patterns in ΔCC-D to variability in protein content and AA composition of the diet as well as differential utilization of dietary constituents contributing to the bulk carbon pool. This variability illustrates the complicated nature of metabolism and suggests caution must be taken with the assumptions used to interpret bulk stable isotope data in dietary studies. Our study is the first to investigate the