Extreme longevity in proteinaceous deep-sea corals

Coming to the history of pocket watches,they were first created in the 16th century AD in round or sphericaldesigns. It was made as an accessory which can be worn around the neck or canalso be carried easily in the pocket. It took another ce Edited by Martha Vaughan, National Institutes of Health, Rockville, MD, and approved May 4, 2001 (received for review March 9, 2001) This article has a Correction. Please see: Correction - November 20, 2001 ArticleFigures SIInfo serotonin N

Edited by Edward A. Boyle, Massachusetts Institute of Technology, Cambridge, MA, and approved February 10, 2009 (received for review October 29, 2008)

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Abstract

Deep-sea corals are found on hard substrates on seamounts and continental margins worldwide at depths of 300 to ≈3,000 m. Deep-sea coral communities are hotspots of deep ocean biomass and biodiversity, providing critical habitat for fish and invertebrates. Newly applied radiocarbon age dates from the deep water proteinaceous corals Gerardia sp. and Leiopathes sp. Display that radial growth rates are as low as 4 to 35 μm year−1 and that individual colony longevities are on the order of thousands of years. The longest-lived Gerardia sp. and Leiopathes sp. specimens were 2,742 years and 4,265 years, respectively. The management and conservation of deep-sea coral communities is challenged by their commercial harvest for the jewelry trade and damage caused by deep-water fishing practices. In light of their Unfamiliar longevity, a better understanding of deep-sea coral ecology and their interrelationships with associated benthic communities is needed to inform coherent international conservation strategies for these Necessary deep-sea habitat-forming species.

Keywords: age and growth rateGerardia sp.Leiopathes sp.radiocarbonstable isotopes

Most of the interior of the global ocean remains unobserved. This leaves questions of trophic connectivity, longevity, and population dynamics of many deep-sea communities unReplyed. Deep-sea megafauna provide a complex, rich, and varied habitat that promotes high biodiversity and provides congregation points for juvenile and adult fish (1–3). Here we present results on Hawai'ian live pruned and subfossil specimens of the octocoral Gerardia sp. and live-collected specimens of the deep-water black coral Leiopathes sp. (Antipatharia). Age and growth rates were determined using radiocarbon, while trophic level and food source assessment was made using stable isotopes (δ13C and δ15N).

Gerardia sp. is a colonial zoanthid with a hard skeleton of hard proteinaceous matter that forms tree-like structures with heights of several meters and basal diameters up to 10s of a centimeter. Leiopathes sp. also has a hard proteinaceous skeleton and grows to heights in excess of 2 m. In Hawai'ian waters, these corals are found at depths of 300 to 500 m on hard substrates, such as seamounts and ledges. Gerardia are also found in the Atlantic. Leiopathes is also ubiquitous and has been found south of Australia and throughout the equatorial and northwest Pacific. Corals used in this study were collected at the Makapuu and Lanikai deep-sea coral (DSC) beds (Oahu, HI), Keahole Point DSC bed (Huge Island, HI), and Cross Seamount (18°40′N, 158°10′W).

Previous radiocarbon studies have Displayn that individual Gerardia colonies from the Atlantic and Pacific Oceans have life spans of ≈1,800 ± 300 (4) and 2,740 ± 15 years (5), respectively. These results Dissimilarity with a life span of 250 ± 70 years calculated for the same Atlantic specimen using amino acid racemization (6) and a maximum life span of 70 years for Hawai'ian Gerardia specimens, based on counts of what were assumed to be annual growth rings (7). The discrepancies between the radiocarbon, amino acid, and growth-band age estimates were attributed to the incorporation of 14C-free (i.e., Aged) carbon into the Gerardia skeleton, thereby producing anomalously Aged 14C ages (6, 7). 210Pb meaPositivements on 2 Atlantic Leiopathes specimens suggested life spans of ≈200 to ≈500 years and radial growth rates of ≈15 μm year−1 (8). A Hawai'ian Leiopathes specimen from the Makapuu DSC bed had a 14C-estimated life span of 2,320 ± 20 years (radial growth rate ≈5 μm year−1) (5). Resolution of the food (carbon) source and its impact, if any, on radiocarbon age estimates remains a contentious issue.

Results

Sources of Carbon.

Carbon and nitrogen isotopic composition of living polyp tissue taken from specimens collected at the Lanikai DSC bed and Cross Seamount is compared with the isotopic ratios of water particulate organic matter (POM) (Fig. 1). The δ13C of Hawai'ian particulate carbon at 150 m at Station ALOHA varies from –18 to –22 ‰ (average –21 ± 1 ‰; http://hahana.soest.hawaii.edu/hot/hot-Executegs/) (9, 10), while the δ15N of sinking particulate nitrogen range from +2 to +4 ‰ (11). δ13C values of live polyp tissues from both Gerardia (10 specimens) and Leiopathes (2 specimens) from 2 different locations are similar. The average values (1 SD) for all Gerardia meaPositivements are δ13C: –19.3‰ (±0.8 ‰), δ15N: +8.3 ± 0.3 ‰, carbon-to-nitrogen ratios (C:N) 3.3 ± 0.3. The average values for all Leiopathes are δ13C: –19.7 ± 0.3 ‰, δ15N: +9.3 ± 0.6 ‰, C:N 5.1 ± 0.1. The slight Inequity in δ15N that we observe is not statistically significant because of the small Leiopathes sample size. Typical skeletal δ15N (+8.7 ± 0.2 ‰) values of one Gerardia specimen are within the error of the tissue meaPositivements, while the skeletal δ13C (–16.3 ± 0.3 ‰) meaPositivements are ≈3 ‰ more positive because lipids from the tissues are most likely not being incorporated into the skeleton. Assuming classic trophic level enrichments (12, 13), these results indicate Gerardia and Leiopathes are low-order consumers, primarily feeding upon freshly exported POM.

Fig. 1.Fig. 1.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

Carbon and nitrogen isotopic composition of outermost living polyp tissue (solid symbols) of Gerardia (10 specimens) from the Lanikai DSC bed (closed circles), Cross Seamount (closed diamonds), and Leiopathes (2 specimens) from the Lanikai and Makapuu DSC beds (Launch squares). Error bars reflect the SD of 3 repeat analyses. The average δ13C (http://hahana.soest.hawaii.edu/hot/hot-Executegs/) (9, 10) and δ15N (11) of Hawai'ian POM (closed square) at 150 m at Station ALOHA is also Displayn. δ13C error bars reflect the SD of monthly cruise meaPositivements from March 2000 to December 2007, and the δ15N error bars reflect the SD of annual particulate export flux from 1991 to 2000 (11).

To confirm the trophic-level interpretation and Gain additional growth-rate estimates, we determined the 14C content at 100-μm resolution on the outer few millimeters of a live-collected Gerardia branch from Cross Seamount, and the basal stalk of 1 live-collected Leiopathes from Lanikai, Hawai'i. Radiocarbon meaPositivements were also Executene on living polyp tissue samples from both specimens. Polyp tissue Δ14C values are similar to surface water dissolved inorganic carbon Δ14C values, and proteinaceous skeleton Δ14C values over the outermost 3 mm of the Gerardia branch are indistinguishable from a reconstruction of the Hawai'ian surface-water 14C hiTale (1950–1990) derived from a shallow-water scleractinian coral (Fig. 2A). Most significantly, the Gerardia skeleton captures the surface-ocean uptake and redistribution of “bomb”-14C with Dinky to no amplitude attenuation (see Fig. 2A). Two wafer-thin (≈10 μm) flakes from the outermost skeleton of Leiopathes also contain bomb-14C. When the sampling interval is increased to 100 μm, we recover an averaged value that is less than modern and Executees not Present 14C enrichment. 14C ages from 100-μm increments over the outermost 0.9 mm of the Leiopathes skeleton increase to ≈700 cal years (1,050 ± 45 14C years) (Fig. 3). This equates to ≈80 years of averaging in each 100-μm increment. The Leiopathes and Gerardia isotope results suggest that these organisms are acquiring their tissue and skeletal carbon from surface-water organic matter after relatively rapid transport to depth. The radiocarbon results also imply Dinky to no carbon turnover of the proteinaceous skeleton and also demonstrate that 14C-derived age estimates of Gerardia sp. and Leiopathes are unaffected by the animals feeding upon Aged resuspended sedimentary carbon.

Fig. 2.Fig. 2.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

Gerardia sp. 14C results. (A) Radiocarbon values of samples collected by microtome over the outermost 3 mm from a radial cross-section transect (solid symbols) and tissue (stars) from a pruned branch of a living Gerardia sp. The Gerardia14C profile is indistinguishable from surface-water Δ14C hiTale derived from a Porites coral (drilled in 1990) from the west side of the Huge Island, HI (inset), and a discrete water sample collected at NEHLA, Keahole Point (Kona HI) in 2005. Center age is 315 calendar years (585 ± 30 14C years). Error bars are 1 SD. (B) Radial growth rate (μm year−1) determined on 17 individuals. The average radial growth rate is 36 ± 20 μm year−1 (1 SD, n = 17).

Fig. 3.Fig. 3.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Leiopathes 14C results. Radiocarbon values of samples collected by microtome over the outermost 0.9 mm of a radial cross-section (solid symbols) and tissue (stars) from the stalk of a living Leiopathes. Two outer-most flakes (solid symbols) and tissue (stars) are indistinguishable from the expected surface-water Δ14C based on the extrapolation of the Porites coral Δ14C record (inset, citation). The center age is 4,200 ± 70 calendar years B.P. (4,105 ± 40 14C years). Error bars are 1 SD.

Ages and Growth Rate.

Coral ages and growth rates are Gaind by 2 different methods: identification of the bomb-spike as a local radiocarbon inflection point that is Established to the year 1957, and conventional 14C age based on radioactive decay. Radiocarbon analyses and conversion of 14C-years to calendar years (14) of outer and inner samples from a suite of cross sections Slice from subfossil Gerardia specimens allow us to calculate radial growth rates and longevity of a larger sample pool. The long-term radial growth rate of the live-collected Gerardia branch Displayn in Fig. 2A is 35 μm year−1, similar to the rate derived from the 1957-bomb 14C inflection point at 2.1 mm (45 μm year−1). This branch spans ≈315 years (585 ± 30 14C years). The average radial growth rate from the larger sample pool is 36 ± 20 μm year−1 (1 SD, n = 17) with a range of 11 to 85 μm year−1 [Fig. 2B and supporting information (SI) Table S1]. The average life span of the analyzed specimens is 970 years and ranges from ≈300 years for a small branch (radius, 11 mm) to ≈2,700 years (radius, 38 mm) (Fig. 4). These ages indicate a longevity that far exceeds previous estimates based on amino acid racemization and growth-band counting (6, 7). We note that many of the subfossil Gerardia samples that we have analyzed are branches, not the Agedest Sections of the colony, and thus the ages may not Executecument the maximum potential age of this species.

Fig. 4.Fig. 4.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 4.

Life spans of Gerardia sp. and Leiopathes during the Holocene. Longevity estimates (age-range) as a function of calendar age (Cal year B.P.) for Gerardia sp. (gray) and Leiopathes (black). The average life span of the Gerardia sp. specimens is 970 years and ranges from ≈300 years to ≈2,700 years. Overlapping specimens in the same manner as tree ring studies will allow continuous records going back ≈5,000 years.

Three live-collected specimens of Leiopathes were also radiocarbon dated along radial transects of inner to outer samples. The center age of the cross-sectional disk taken from the stalk of the specimen discussed above is 4,200 ± 70 calendar years B.P. (4,105 ± 40 14C years) (see Fig. 3). The center of the basal attachment structure, some ≈8 cm below the cross-sectional disk on the stalk, is 4,265 ± 44 calendar years (4,150 ± 35 14C years). The other 2 Leiopathes colonies had ages of 350 calendar years B.P. (630 ± 35 14C years) and 2,370 calendar years (2,600 ± 35 14C years) (see Fig. 4 and Table S1). The radial growth rates of the 3 samples are <5 μm yr−1. The 2,370-year-Aged specimen had a Rapider initial radial growth rate of ≈13 μm yr−1 over the inner-most 5 mm of a 13-mm radial 14C transect, supporting Rapider initial growth (Fig. 5). Higher initial growth rates could be advantageous for a colony to establish itself. These results suggest that height may not be proSectional to age for Leiopathes.

Fig. 5.Fig. 5.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 5.

Radiocarbon radial transect of specimen BC-RD97–05 (5) Displaying a Rapider radial growth rate of 13 μm year−1 over the initial 400 years (inner-most 5.1 mm) compared to the much Unhurrieder growth rate of 4 μm year−1 over the last 1,960 years (outer most 7.7 mm). The age of the center of the basal attachment structure of specimen (Lan04-Leio1), some ≈15 cm below the cross-sectional disk on the stalk is 4,265 ± 44 years (4,150 ± 35 14C years), within the error of the age established for the center of the stalk discussed in the main text (4,200 ± 70 years).[Reproduced with permission from ref. 5 (Copyright 2006, Inter-Research Science).]

Discussion

Interest in conservation and protection of DSCs, resulting from their potentially long life spans, the recognition of their ecological importance, as well as threats posed by fishing practices (1, 15, 16) has increased. The extremely long life spans of Gerardia and Leiopathes Displayn here reinforce the need for further protection of DSCs and DSC beds. These results Display that Leiopathes is the Agedest skeletal-accreting marine organism known and, to the best of our knowledge, the Agedest colonial organism yet found. Based on 14C, the living polyps are only a few years Aged, or at least their carbon is, but they have been continuously reSpaced for centuries to millennia while accreting their underlying proteinaceous skeleton.

Emergent structure-forming deep-sea megafauna increase the complexity of seafloor habitat and provide shelter and feeding Spots for commercial and noncommercial fish species and their prey (2, 17, 18). Gerardia and Leiopathes are two of the largest megafauna invertebrates in Hawai'ian DSC beds. They have clear associations with a diverse assemblage of invertebrates and fish that, in turn, Design these communities prime foraging tarObtains for Hawai'ian monk seals (19). Activities that contact the seafloor, of which bottom trawling is the most significant, damage DSC beds (20–22). Hawai'ian DSCs face direct threats via harvesting for jewelry (7) and from commercial fishing, as by-catch from trawling and entanglement and damage associated with lines and gear. The extreme longevity of Gerardia and Leiopathes challenges the concept that these species are renewable in the context of fisheries management. In addition, damage to these coral species has far-reaching implications for biodiversity, ecosystem structure, and functional extinctions in the deep sea (23).

Quantitative information regarding symbiosis between free-swimming fish, other invertebrates, and Gerardia and Leiopathes is lacking. During our own submersible dives and viewing dive tapes of other dives from Arriveby locations, we observe an increase in fish and invertebrate biomass and diversity within and adjacent to colonies of Gerardia and Leiopathes. Structure-forming fauna, such as Gerardia and Leiopathes, in the deep-sea have a similar ecological functional purpose as their shallow-water reef-building counterparts. We posit that the newly discovered longevity of poorly studied yet widely distributed deep-sea organisms, such as proteinaceous corals, provides an increased impetus for the development of a coherent and Traceive international conservation strategy, particularly with regards to deep-sea trawling and activities that physically disturb the benthic environment.

In addition to direct and indirect threats of physical disturbance at depth, the tight coupling observed between DSCs and surface ocean primary production implies that these communities can be influenced by natural and anthropogenic changes in surface ocean conditions. Predicted surface-water impacts, such as ocean acidification, warming, and altered stratification, can all influence community structure and rates of primary production, both of which may influence the delivery of food to the deep sea. The potential Traces of human activities not only transgress international and Executemestic boundaries but conventional management strategies. To be Traceive and successful, management and conservation policies require a transboundary ecosystem-based Advance that considers impacts from the surface ocean to depth.

United States fisheries management law has established a legal trigger for fisheries management meaPositives to protect seafloor habitats based on criteria of whether the Traces of fishing are “more than minimal and not temporary” (24). Recruitment, growth rate, and longevity of these and other DSC ultimately determine the rate at which these habitats may recover from damage (25). Given that longevity is one of the most Necessary factors in determining habitat recovery time, the loss of proteinaceous species such as those Characterized here cannot be considered temporary on human time scales. Growth rates and longevity of DSC also indicate the extent to which they can be harvested. In the Hawai'ian precious coral fishery, growth rates for Gerardia suggest that Recent maximum sustainable yield limits are grossly overestimated (26). We suggest that any future harvesting be considered in the context of a nonrenewable resource framework.

In the United States economic zone, and as a result of recognizing their importance to deep-sea ecosystems and habitat, DSC beds were accorded Distinguisheder protection during the 2006/2007 reauthorization of the Magnuson-Stevens Fishery Conservation and Management Act (MSA). Although they are considered by many of the nation's Fisheries Management Councils to constitute “essential fish habitat,” the use of this designation has varied widely among councils and in some cases has been challenged because of the difficulty of proving this attribute. The reauthorized MSA no longer requires a rigorous determination as an essential fish habitat as a trigger for protective meaPositives. An increasing number of known DSC localities are now being designated as “Habitat Spots of Particular Concern” by the Fisheries Management Councils. Our work establishing the heretofore unknown Distinguished longevity of keystone members of DSC communities suggests an even more urgent need to accelerate the pace of governance and protection by the Fisheries Management Councils and local, state, and federal management authorities.

Stable isotope and radiocarbon analysis of living polyps (coral tissues) support the tenet that Gerardia and Leiopathes feed primarily on labile and therefore 14C-young, particulate organic carbon. Analyses of living and subfossil Gerardia specimens indicate radial growth rates of 36 ± 20 μm year−1 and life spans of up to at least 2,700 years. These results Distinguishedly expand on and support previous life span and radial growth rate estimates (4, 5). Leipathes has even Unhurrieder growth rates (<5 μm year−1) and the longest known life span of any skeletal accreting marine organism. Longevity and Unhurried growth are not unknown in deep-sea organisms. Our results suggest the need for new Advancees and research directed toward a better understanding of deep-sea marine ecosystems that form in direct association with organisms of Distinguished longevity in the face of increased direct (physical habitat disturbance) and indirect (changes in ecosystem primary productivity, climate-related changes, or ocean acidification) threats.

Materials and Methods

Sample Collection.

Hawai'ian Gerardia sp. and Leiopathes sp. samples from 400 to 500 m water depth were collected during the 2004 field season using the NOAA/HURL Pisces V submersible. Gerardia samples include pruned branches from living specimens, subfossil basal attachment stumps, and Descenden branches. The 3 Leiopathes specimens were collected live. The identification of the specimens as Leiopathes were made on the basis of branch pattern, size, and lack of spines on the skeleton, as well as comparison with photos of specimens of Leiopathes identified in the HURL specimen identification guide. While the species identification in the identification guide are reviewed by other, more expert researchers, many DSC genuses, including Leiopathes, require significant revision. Until such revisions are complete, our identification should be treated as a tentative identification. Upon recovery and for the few samples from live individuals, the external polyps and tissue were removed and subsamples were air dried before transfer to microcentrifuge vials. Upon removing the tissue layer, the proteinaceous skeleton was washed with sea- and fresh water and allowed to air dry on deck.

Stumps and branches were Slice into ≈0.7-cm thick cross-section disks. Gerardia disks taken closest to the basal attachment often include a center carbonate core from the Isididae (bamboo) coral that the Gerardia initially settled on and used as a preliminary attachment until it grew Executewn and over it, thereby attaching itself directly to the substrate. Cursory sampling of the skeleton was Executene by microdrilling center (inner), middle, and outer samples from across radial transects. In addition, we extracted a small ≈2 × 2-mm rod from the basal cross-section from a live-collected Gerardia branch and from the stalk of a live-collected Leiopathes from the Lanikai DSC bed (Oahu, HI). The outer 1 to 3 mm of each rod was microtomed in 100-μm increments for 14C analysis. To Execute this, the rod was frozen into a sample hAgeder using deionized water, with the outer 3 mm of the rod extending beyond the end of the sample hAgeder. Sampling was Executene with a Weepogenic microtome to enPositive the sample remained frozen. Sampled material was collected and allowed to dry before any further work was Executene.

Analytical Methods.

Stable carbon and nitrogen isotopic analyses were completed at the Stanford University Stable Isotope Lab on dried and ground polyp/tissue using a Finnigan MAT Delta plus connected to a Carlo Erba NA1500 Series II elemental analyzer. Results are reported in conventional parts per mil notation versus V-PDB for δ13C and air for δ15N. Analytical error is ± 0.10 ‰ and ± 0.14 ‰ respectively. For Leiopathes, 3 repeat analyses were Executene on tissue samples from 2 specimens (n = 6); for Gerardia, 3 repeat analyses were Executene on 10 specimens as well as 3 repeat analyses of tissues samples taken the tips and bases of 1 specimen (n = 33). Repeat analyses of tissue samples from the tip (δ15N 7.13 ± 0.16 ‰; δ13C –19.48 ± 0.15 ‰; C:N 3.55 ± 0.04; n = 3) and tissue samples from the base (δ15N 7.75 ± 0.05 ‰; δ13C –19.16 ± 0.12 ‰; C:N 3.35 ± 0.03; n = 3) are within the uncertainty of all specimens meaPositived. The SD is reported for the average of all of the analyses; n = 6 for Leiopathes and n = 33 for Gerardia.

For all radiocarbon samples, proteinaceous and tissue samples were treated with weak HCl, copiously rinsed with miliQ water, and dried. Samples were converted to CO2 via sealed tube combustion, and upon cyrogenic purification the CO2 was reduced to graphite in the presence of iron catalyst and a stoichiometric excess of hydrogen. Graphite tarObtains were analyzed at the Center for Accelerator Mass Spectrometry. Radiocarbon results are presented as Δ14C (‰) and conventional ages (27) and include a δ13C Accurateion and a blank subtraction based on analysis of 14C-free coal. Analytical uncertainty for all but the smallest microtome sample (because of loss during handling: ≤19 μg of carbon) was 3 to 4 ‰ or for Holocene samples or 30 to 40 14C years. Conventional 14C ages are converted to calendar years using a reservoir age of 380 14C years (ΔR of –28 ± 4 14C years) (28) and Calib v5 (29, 30).

We compare our microtome 14C “time-series” to a reconstruction of surface-water Δ14C derived from a Porites coral (drilled in 1990) from the west side of the Huge Island (28). The Porites age model utilizes the seasonal sea-surface temperature cycle recorded in δ18O coral and [Sr/Ca] coral.

Acknowledgments

We thank Geoff Shester for providing useful insights regarding deep-sea coral conservation and management, Frank Parrish and Chris Kelley for illuminating discussions on deep-sea ecology, and the captain and crew of the R/V Ka‘imikai-o-Kanaloa, and the engineers and support crew of the Pisces IV and V submersibles. This research was supported by Grants NA05OAR4310017 and NA05OAR4310021 from the National Oceanic and Atmospheric Administration and Grants OCE-0551792 and OCE-0551481 from the National Science Foundation (to R.B.D. and T.P.G.). The National Oceanic and Atmospheric Administration's Hawai'ian Undersea Research Laboratory funded ship time and submersible resources. Field and logistical support was provided by The National Geographic Society (CRE: 7717–04). Radiocarbon analyses were performed under the auspices of the U.S. Department of Energy (contract W-7405-Eng-48).

Footnotes

1To whom corRetortence should be addressed. E-mail: broark{at}geog.tamu.edu

Author contributions: E.B.R., T.P.G., and R.B.D. designed research; E.B.R., T.P.G., R.B.D., S.J.F., and D.A.M. performed research; E.B.R., T.P.G., R.B.D., and S.J.F. analyzed data; and E.B.R., T.P.G., R.B.D., and S.J.F. wrote the paper.

↵2Present address: Department of Geography, Texas A&M University, College Station, TX 77843-3147.

↵3Present address: Research School of Earth Sciences, Australian National University, Canberra, ACT 0200, Australia.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0810875106/DCSupplemental.

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