Bulk tissue and amino acid stable isotope analyses reveal global ontogenetic patterns in ocean sunfish trophic ecology and habitat use

Phillips, Natasha D.; Smith, Emma A. Elliott; Newsome, Seth D.; Houghton, J. D. R.; Carson, Carol D.; Alfaro‐Shigueto, Joanna; Mangel, Jeffrey C.; Eagling, Lawrence E.; Kubicek, Lukas; Harrod, Chris

doi:10.3354/meps13166

Cited by 19 publications

(8 citation statements)

References 73 publications

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“…It is possible that phytoplankton‐derived detritus either settled on the surface of macroalgae, or was utilized by epiphytes that were subsequently consumed by Aplodactylus . Alternatively, it may be a result of our undersampling of benthic microalgae, which is currently poorly characterized in terms of EAA δ 13 C (Phillips et al 2020). The suggested reliance of individuals of both Aplodactylus and Engraulis on Ulva presents more of a challenge to explain, as Ulva is not a dominant macroalgae at our sites in terms of biomass, although Aplodactylus are known to consume Ulva in large volumes when available (Caceres et al 1994).…”

Section: Discussionmentioning

confidence: 99%

Intraspecific variation and energy channel coupling within a Chilean kelp forest

Smith

Harrod

Docmac

et al. 2020

Ecology

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The widespread importance of variable types of primary production, or energy channels, to consumer communities has become increasingly apparent. However, the mechanisms underlying this “multichannel” feeding remain poorly understood, especially for aquatic ecosystems that pose unique logistical constraints given the diversity of potential energy channels. Here, we use bulk tissue isotopic analysis along with carbon isotope (δ13C) analysis of individual amino acids to characterize the relative contribution of pelagic and benthic energy sources to a kelp forest consumer community in northern Chile. We measured bulk tissue δ13C and δ15N for >120 samples; of these we analyzed δ13C values of six essential amino acids (EAA) from nine primary producer groups (n = 41) and 11 representative nearshore consumer taxa (n = 56). Using EAA δ13C data, we employed linear discriminant analysis (LDA) to assess how distinct EAA δ13C values were between local pelagic (phytoplankton/particulate organic matter), and benthic (kelps, red algae, and green algae) endmembers. With this model, we were able to correctly classify nearly 90% of producer samples to their original groupings, a significant improvement on traditional bulk isotopic analysis. With this EAA isotopic library, we then generated probability distributions for the most important sources of production for each individual consumer and species using a bootstrap‐resampling LDA approach. We found evidence for multichannel feeding within the community at the species level. Invertebrates tended to focus on either pelagic or benthic energy, deriving 13–67% of their EAA from pelagic sources. In contrast, mobile (fish) taxa at higher trophic levels used more equal proportions of each channel, ranging from 19% to 47% pelagically derived energy. Within a taxon, multichannel feeding was a result of specialization among individuals in energy channel usage, with 37 of 56 individual consumers estimated to derive >80% of their EAA from a single channel. Our study reveals how a cutting‐edge isotopic technique can characterize the dynamics of energy flow in coastal food webs, a topic that has historically been difficult to address. More broadly, our work provides a mechanism as to how multichannel feeding may occur in nearshore communities, and we suggest this pattern be investigated in additional ecosystems.

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Section: Discussionmentioning

confidence: 99%

Intraspecific variation and energy channel coupling within a Chilean kelp forest

Smith

Harrod

Docmac

et al. 2020

Ecology

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“…Such an evolutionary constraint is supported by none of the known regionally endothermic fishes consuming a primarily gelativorous diet (Ates, 1988; Hetherington et al ., 2022), as well as the physiology and morphology of the largest gelativorous marine predators. The apparently ectothermic ocean sunfish Mola mola (Linnaeus 1758) (Watanabe & Davenport, 2021), which does not swim continuously (Nakamura et al ., 2015) because it is not an obligate ram ventilator as a predominantly gelata‐consuming adult (Phillips et al ., 2020), is the only other fish species with internalized red muscle (but powering the dorsal and anal fin) and no known retia (Davenport et al ., 2018). Similarly, the only homeothermic gelativore is the leatherback sea turtle Dermochelys coriacea (Vandelli 1761), which is thought to achieve that physiological capacity largely as a result of gigantothermy (Paladino et al ., 1990) and other advanced heat retention mechanisms (Davenport et al ., 2009; Greer et al ., 1973) in spite of a low metabolism consistent with ectothermic reptiles (Wallace & Jones, 2008).…”

Section: Discussionmentioning

confidence: 99%

An enigmatic pelagic fish with internalized red muscle: A future regional endotherm or forever an ectotherm?

Arostegui

Shero

Frank

et al. 2023

Journal of Fish Biology

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Ectothermy and endothermy in extant fishes are defined by distinct integrated suites of characters. Although only ⁓0.1% of fishes are known to have endothermic capacity, recent discoveries suggest that there may still be uncommon pelagic fish species with yet to be discovered endothermic traits. Among the most rarely encountered marine fishes, the louvar Luvarus imperialis is a remarkable example of adaptive evolution as the only extant pelagic species in the order Acanthuriformes (including surgeonfishes, tangs, unicornfishes and Moorish idol). Magnetic resonance imaging and gross necropsy did not yield evidence of cranial or visceral endothermy but revealed a central‐posterior distribution of myotomal red muscle that is a mixture of the character states typifying ectotherms (lateral‐posterior) and red muscle endotherms (central‐anterior). Dissection of a specimen confirmed, and an osteological proxy supported, that L. imperialis has not evolved the vascular rete that is vital to retaining heat in the red muscle. The combination of presumably relying on caudal propulsion while exhibiting internal red muscle without associated retia is unique to L. imperialis among all extant fishes, raising the macroevolutionary question of whether this species – in geologic timescales – will remain an ectotherm or evolve red muscle endothermy.

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“…As such, studies often use literature data on δ 13 C EAA fingerprints from natural and cultured primary producer collections to characterize resource utilization patterns of consumers across a wide range of systems. This approach relies on the assumption that normalized δ 13 C EAA fingerprints are robust to changing environmental conditions (e.g., Arthur et al 2014; MacDonald et al 2019; Phillips et al 2020). One of the only studies to rigorously test this concept was Larsen et al (2015), who found that normalizing δ 13 C AA values to their mean in a marine diatom species ( Thalassiosira weissflogii ) cultured across a range of light, salinity, temperature, and pH conditions significantly reduced δ 13 C AA variance.…”

Section: Discussionmentioning

confidence: 99%

Amino acid carbon isotope fingerprints are unique among eukaryotic microalgal taxonomic groups

Stahl

Rynearson

McMahon

2023

Limnology & Oceanography

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Eukaryotic microalgae play critical roles in the structure and function of marine food webs. The contribution of microalgae to food webs can be tracked using compound-specific isotope analysis of amino acids (CSIA-AA). Previous CSIA-AA studies have defined eukaryotic microalgae as a single functional group in food web mixing models, despite their vast taxonomic and ecological diversity. Using controlled cultures, this work characterizes the amino acid δ 13 C (δ 13 C AA ) fingerprints-a multivariate metric of amino acid carbon isotope values-of four major groups of eukaryotic microalgae: diatoms, dinoflagellates, raphidophytes, and prasinophytes. We found excellent separation of essential amino acid δ 13 C (δ 13 C EAA ) fingerprints among four microalgal groups (mean posterior probability reclassification of 99.2 AE 2.9%). We also quantified temperature effects, a primary driver of microalgal bulk carbon isotope variability, on the fidelity of δ 13 C AA fingerprints. A 10 C range in temperature conditions did not have significant impacts on variance in δ 13 C AA values or the diagnostic microalgal δ 13 C EAA fingerprints. These δ 13 C EAA fingerprints were used to identify primary producers at the base of food webs supporting consumers in two contrasting systems: (1) penguins feeding in a diatom-based food web and (2) mixotrophic corals receiving amino acids directly from autotrophic endosymbiotic dinoflagellates and indirectly from water column diatoms, prasinophytes, and cyanobacteria, likely via heterotrophic feeding on zooplankton. The increased taxonomic specificity of CSIA-AA fingerprints developed here will greatly improve future efforts to reconstruct the contribution of diverse eukaryotic microalgae to the sources and cycling of organic matter in food web dynamics and biogeochemical cycling studies.

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Bulk tissue and amino acid stable isotope analyses reveal global ontogenetic patterns in ocean sunfish trophic ecology and habitat use

Abstract: C. (2020). Bulk tissue and amino acid stable isotope analyses reveal global ontogenetic patterns in ocean sunfish trophic ecology and habitat use. Marine Ecology Progress Series, 633, 127-140.

Cited by 19 publications

References 73 publications

Intraspecific variation and energy channel coupling within a Chilean kelp forest

Intraspecific variation and energy channel coupling within a Chilean kelp forest

An enigmatic pelagic fish with internalized red muscle: A future regional endotherm or forever an ectotherm?

Amino acid carbon isotope fingerprints are unique among eukaryotic microalgal taxonomic groups

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