A Branch Campus of Texas A&M University April 12, 2010
NATURE Editor
Dear Sirs,
Enclosed and attached please find a manuscript that my co-author, Mr. Chih-Lin Wei, and I would like to submit to NATURE. It is our intention that this paper be included with the Census of Marine Life cluster of papers. The title of our paper (Biodiversity of Deep-Sea Macrofauna as a Function of Food Supply) reflects the dependence of community structure on productivity and will we believe find a wide and appreciative audience.
Last autumn we submitted a somewhat similar paper with the same title. It was returned to us without review because your editorial staff concluded that it would not have a wide enough audience. This puzzled us because we look on our discovery as confirmation of theory that has, to date, defied quantification (see for example the new book by Mike Rex and Ron Etter , 2010, Deep-Sea Biodiversity, Harvard Univ. Press). No one working in the deep ocean has been able to relate the mid-depth species maximum to food supply until now.
We inferred that our earlier ms. was returned because it considered only the Gulf of Mexico, and thus was provincial in scope. With this in mind, we expanded our analysis to include several sets of data in the western North Atlantic. By piecing several different studies together, we have been able to confirm that the same pattern exists there, thus indicating that “all” continental margins might have mid-depth species maxima (MDMs) that are a function of food supply.
We look forward to your sending our ms. out for review. Most sincerely,
Gilbert T. Rowe Regents Professor Chih-Lin Wei PhD Candidate
T
EXAS
A&M
U
NIVERSITY AT
G
ALVESTON
P. O. Box 1675 • Galveston, TX 77553-1675 • (409) 740-4847 • 409-740-5001 fax
1
Biodiversity of Deep-Sea Macrofauna as a Function of
Food Supply
Gilbert T. Rowe1 & Chih-Lin Wei2 1
Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX 77553, USA & 2Department of Oceanography, Texas A&M University, College Station, TX 77843, USA
Abstract: The mid-depth maximum (MDM) in species diversity in deep-sea macrofauna (60 species per 100 individuals (E(S100)) has been defined for the first time in terms of the
input of organic detrital particulate organic carbon (POC) (14 mg C m-2 day-1) in the northern Gulf of Mexico. Lowest mean diversities (E(S100) = 26 and 23 spp.) were
encountered at the deep (3.7 km) and shallow (0.5 km) extremes of the estimated POC input rates (2.7 and 78 mg C m-2 d-1). This pattern supports the hypothesis that diversity on the upper continental slope will increase due to a decline in competitive exclusion as the input of POC declines offshore, up to a maximum tipping point, after which diversity will decrease as food resources decline offshore. That similar correlations can be made on the NW Atlantic margin suggests that these patterns may be encountered on many continental slopes.
Variations in the numbers of co-existing species in natural communities have puzzled ecologists for more than half a century1, 2, but the suite of possible variables that might control biodiversity is large3, with explanations remaining equivocal. On seemingly monotonous muddy sea floors, it has been suggested that biodiversity is directly related to environmental stability4 and inversely related to physiological stress5. Diversity increases from physically dynamic shallow water habitats into the supposedly more tranquil deep sea6 , but this increase from shallow to deep water is reversed at
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intermediate depths on the continental slope, producing an inverse parabola with a ‘mid-depth maximum’ (MDM)7.
It has been suggested that an inverse parabola is a general reaction of diversity to productivity8, with dominance by a few species when resources are liberal, followed by a decrease in dominance as resources diminish. The increase in diversity initially may be a relaxation of competitive exclusion. On the ocean floor this increase continues offshore until it reaches a ‘tipping point’, past which the further decline in resources leads to a loss of species. To date, the relationships between the tipping point in deep-sea macrofauna and specific levels of food supply have not been described. The purpose of this note is to define, for the first time, the diversity tipping point, or MDM, for deep continental margin macrofauna in terms of specific rates of particulate organic carbon (POC) input.
This study was conducted in the northern Gulf of Mexico (GoM) (Fig 1), extending from Florida in the east along parallel latitudes west almost to the Texas border with Mexico, at depths of 200 m out to 3,700 m on the Sigsbee Abyssal Plain9, 10. The sampling employed a 0.2 m-2 GOMEX box corer at 51 locations, for a total of 271 samples, covering 46 m-2 of sea floor. A total of 957 putative species were identified, from which the expected number of species per 100 individuals (E(S100))4, 11 was calculated at each site. E(Sn) is the ‘within habitat’ or α diversity, as opposed to species richness or total number of species (γ diversity).
Delivery of particulate organic carbon (POC) to the sea floor at each site (Fig 1) was estimated from bi-weekly composite averages of the standing stock of sea-surface chlorophyll and net primary production12 using an exponential decay equation13. The
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primary production in the east quadrant is double that in the NW GoM, which directly affects detrital carbon input to the seafloor12.
The expected number of species per 100 individuals, E(S100) has been plotted as a function of the log10 of the POC flux at each site (Fig 2). The POC flux ranged from a low of 2.7 mg C m-2 day-1 on the Sigsbee Abyssal Plain (S1 through S4) up to 77.7 mg C m-2 day-1 within the head of the Mississippi Canyon (MT1), with corresponding E(Sn) values of about 20 species per 100 individuals at each end of the distribution. The tipping point where d(E(Sn))/d(POC flux) = 0 had a value of approximately 14 mg C m-2 day-1, supporting 60 species per 100 individuals.
A comparison of the east vs. the west side of the northern GoM basin margin (Fig 3) illustrates that the west side tipping point was slightly lower (12.8 vs 14 mg C m-2 day-1), with slightly fewer species (Fig 3).
This analysis supports the idea that α diversity is suppressed when resources are high, it attains a maximum at some intermediate level of resource availability, but then declines when resources become limiting. The actual causative relationships between POC input and the inferred competition among the resident species remain complex. The lowest diversity at the shallow extreme was produced by dominance of the ampeliscid amphipod Ampelisca mississippiana within the head of the Mississippi Canyon14. As this species’ dominance diminished offshore, the evenness increased, along with expected numbers of species per 100 individuals.
The density of animals on the sea floor was a direct, log/normal function of POC input (Fig 4). The 20 or so species supported by the POC flux coexisted among several hundred individuals per square meter on the abyssal plain, with 2 to 4 mg C m-2 day-1 POC available, versus about 6,000 individuals per square meter on the upper continental
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slope, with substantial POC available (50 to 80 mg C m-2 day-1). The POC available varied by more than a factor of 10. The tipping point, at ca. 13 to 14 mg C m-2 day-1, supported densities of approximately 3,000 ind. m-2.
It has been suggested that the Gulf of Mexico may have suffered a geologically recent extinction event, based on the distribution of isopod crustaceans15. The more comprehensive taxonomic coverage by Wei et al.10 provides little additional information to refute this suggestion15. Thus, the decline in species past the tipping point depth may be a function of the basin’s history, and not a lack of food.
Several investigations along the western North Atlantic margin also have distinct MDM7, 16. We have plotted their E(Sn) value as function of estimated POC input to the sea floor (SI Appendix 1) and constructed regressions similar to the
northern GoM (Fig 5). The tipping points for this assemblage of curves ranged from 8.5 to 16.9 mg C m-2d-1, with expected species for the groups ranging from a low of 10 for the Cumacea up to about 50 for the entire macrofauna. Remarkably, the POC ranges were about the same in all the studies. The tipping points however were substantially deeper in the Atlantic (1.4 vs. 2 km) due, we believe, to the higher primary production rate in NW Atlantic. This relationship needs to be extended to other continental margins to confirm these findings.
1 Hutchinson, G. E. Homage to Santa Rosalia or Why Are There So Many Kinds of Animals? Am. Nat. 93, 145 (1959).
2 Whittaker, R. H. Evolution of species diversity in land communities. in
Evolutionary Biology Vol. 10 (eds M.K. Hecht, W.C. Steere, & B. Wallace) 250-268 (Plenum, New York, 1977).
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4 Sanders, H. L. Marine benthic diversity: a comparative study. Am. Nat. 102, 243 (1968).
5 Rhoads, D. C. Organism-sediment relations on the muddy sea floor. Oceanogr. Mar. Biol. Annu. Rev. 12, 263-300 (1974).
6 Hessler, R. R. & Sanders, L. H. Faunal diversity in the deep-sea. Deep Sea Res. 14, 65-78 (1967).
7 Rex, M. A. Community structure in the deep-Sea benthos. Annu. Rev. Ecol. Syst. 12, 331-353 (1981).
8 Rosenzweig, M. L. & Abramsky, Z. How are diversity and productivity related? in Species Diversity in Ecological Communities: Historical and Geographical Perspectives (eds Robert E. Ricklefs & Dolph Schluter) 52–65 (University of Chicago, Chicago, 1993).
9 Rowe, G. T. & Kennicutt, M. C. (eds.) The Deep Gulf of Mexico Benthos Program. Deep Sea Res. II 55, 2535-2711 (2008).
10 Wei, C.-L. et al. Bathymetric zonation of deep-sea macrofauna in relation to export of surface phytoplankton production. Marine Ecology Progress Series 399, 1-14, doi:10.3354/meps08388 (2010)..
11 Hurlbert, S. H. The nonconcept of species diversity: A critique and alternative parameters. Ecology 52, 577-586 (1971).
12 Biggs, D. C., Hu, C. & Müller-Karger, F. E. Remotely sensed sea-surface
chlorophyll and POC flux at Deep Gulf of Mexico Benthos sampling stations. Deep Sea Res. II 55, 2555-2562 (2008).
13 Pace, M. L., Knauer, G. A., Karl, D. M. & Martin, J. H. Primary production, new production and vertical flux in the eastern Pacific Ocean. Nature 325, 803-804 (1987).
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14 Soliman, Y. S. & Rowe, G. T. Secondary production of Ampelisca mississippiana Soliman and Wicksten 2007 (Amphipoda, Crustacea) in the head of the Mississippi Canyon, northern Gulf of Mexico. Deep Sea Res. II 55, 2692-2698 (2008).
15 Wilson, G. D. F. Local and regional species diversity of benthic Isopoda (Crustacea) in the deep Gulf of Mexico. Deep Sea Res. II 55, 2634-2649 (2008).
16 Maciolek, N. J. & Smith, W. K. Benthic species diversity along a depth gradient: Boston Harbor to Lydonia Canyon. Deep Sea Research Part II: Topical Studies in Oceanography 56, 1763-1774, doi:DOI: 10.1016/j.dsr2.2009.05.031 (2009). Supplementary Information is link to the online version of the paper at www.nature.com/nature. A figure summarizing the main result of this paper is available in Supplementary Information appendix 2 Fig.1
Acknowledgements This work was supported by Minerals Management Service Contract 30991, of the Dept. of the Interior of the United States.
Author Contributions GTR designed the study. GTR and C-LW collected data and performed analysis. GTR and C-LW wrote the paper and contributed to M.S. analysis.
Author Information Correspondence and requests for materials should be addressed to Gilbert.T. Rowe. (roweg@tamug.edu).
Figure 1. Box core sampling locations. The abyssal plain sites (S1 to S5) were sampled in summer 2002. The other slope sites were sampled in summer 2000 and partially re-visited in summer 2001. Map is modified from Wei et al.10.
Figure 2. Expected number of species4, 11 from 100 randomly selected individuals as a function of POC flux12. The x axis is in log10 scale. The blue line shows the quadratic regression model. The dotted lines indicate the 95% confidence interval. The x and y values (in brackets) depict the POC flux and E(S100) of the upper extremes of the model,
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along with the values at the “tipping point” where dy/dlog10(x)=0. All regression equations are in SI Appendix 3.
Figure 3. Data from Fig 2, but displayed as a comparison between the east and west halves of the GoM basin, with E(S100) as a function of POC flux12. The x axis is in log10 scale. The blue and black colors indicate the samples and the fitted models for east and west, respectively. The x, y values (in brackets) at the apex depict the POC flux and E(S100) of the “tipping point” from the two models’ predictions.
Figure 4. Macrofauna density as a function of POC flux. The macrofauna density are “macrofauna sensu strictu” (excluding nematodes, copepods, and ostacodes).
Figure 5. Species diversity as a function of POC flux in the North Atlantic (See Fig 2 in SI Appendix 2 for station locations). The x axis is in log10 scale. Diversity, E(S50), of gastropod, polychaeta, and cumacea are from Gay Head-Bermuda transect6, 7. Diversity, E(S100), of macrofauna are from the Georges Bank and western North Atlantic16. Export POC flux was calculated using the average of monthly net primary production from January 1998 to December 2007 (Detail descriptions in SI Appendix 1).
1
Biodiversity of Deep-Sea Macrofauna as a Function of
Food Supply: Supplementary Information
Gilbert T. Rowe1 & Chih-Lin Wei2 1
Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX 77553, USA & 2Department of Oceanography, Texas A&M University, College Station, TX 77843, USA
SI-1. Supplementary Methods:
Benthic macrofauna was sampled in northern Gulf of Mexico from the shelf break of Texas-Louisiana to the Sigsbee Abyssal Plain9. A total of 51 locations from depths 200 to 3700 m (Fig. 1) were sampled in summers of 2000 to 2002 with a 0.2-m2 GOMEX box corer17. At least 5 cores were deployed at each station and overall 271 cores were taken, which equalled over 46 m2 of seafloor sampled. The top 15 cm of sediments were sieved through a 300 micrometer mesh to separate macrofauna animals from the fine mud and sand fraction. The retained material was fixed in 10% buffered formalin diluted with filtered seawater. Samples were stained with 5% Rose Bengal for at least 24 hours, and then rinsed with
freshwater. The stained samples were sorted into major taxonomic groups and transferred to 70% ethyl alcohol for permanent preservation and species identification. Animal density was estimated based on Macrofauna Sensu Stricto (excluding large size meiofauna such as nematodes, copepods, and ostracodes). A total of 957 putative species (27 % named species and 73% undescribed species) from 6 major
macrofauna taxa (amphipods, aplacophorans, bivalves, cumaceans, isopods, and polychaetes) were identified.
Local species diversity (α diversity) was estimated using Sanders-Hurlbert expected number of species4, 11 to give an absolute measure of species richness at a normalized sample size. The diversity index is given by
∑
= ⎥⎦ ⎤ ⎢ ⎣ ⎡ ⎟⎟ ⎠ ⎞ ⎜⎜ ⎝ ⎛ ⎟⎟ ⎠ ⎞ ⎜⎜ ⎝ ⎛ − − = S i i n n N n N N S E 1 1 ) (2
where E(Sn) is the expected number of species in a sample of n individuals randomly selected from an assemblage containing N individuals and S species; Ni is the number of individuals in the ith species.
High resolution SeaWiFS ocean-color data (pixel size = ~1 km2) were obtained from January 1998 to December 2002. Depth-integrated net primary production (NPP) at 51 sampling sites (catchment = 5-by-5 pixels per site) was estimated from biweekly composite averages of surface chlorophyll
concentration (SST), photosynthetic available irradiance (PAR), and sea surface temperature (SST) using a Vertical General Production Model (VGPM)12, 18. Delivery of particulate organic carbon (POC) to the seafloor was estimated from NPP using an exponential decay model [flux (Z) = 3.523 NPP Z-0.734 where Z is the sample depth]12, 13. Detailed methods and the ocean-color data of the Gulf of Mexico sampling sites can be found in Biggs et al.12.
Contemporaneous ocean-color images are not available for the North Atlantic benthic data6, 7, 16; therefore, export POC flux was calculated using the averages of monthly NPP composites from January 1998 to December 2007 (pixel size = ~9km, catchment = 3-by-3 pixels per site) based on the VPGM model18. The standard VPGM product was downloaded from the Ocean Productivity web page, Oregon State University19.
Expected number of species was calculated using PRIMVER 6 version 6.1.1220. Analyses and graphics were conducted using R version 2.9.121. Bathymetric maps of the Gulf of Mexico22 and the western North Atlantic23 were constructed using ESRI®ArcMapTM 9.2.
3
SI-2. Supplementary Figure(s) and Legend(s)
SI-2 Fig.1. Unimodal diversity-productivity model in relation to animal density and sampling depths. The diagram follows a conceptual model of Rex and
Etter24 with the empirical curve fits and scales from Fig. 2 and 4. The top x-axis
is approximate depth corresponding to the labels on the bottom POC axis. At the deepest part of Gulf of Mexico (GoM) basin (~3.8 km), the extreme low
4
particulate organic carbon (POC) inputs (<3 mg C m-2 day-1) can only support
several hundred animals m-2 and 20 or so species per 100 individuals, due to
the low population density being more prone to extinction from stochastic
events24. The ascending limb of the diversity-productivity curve (black) shows
the accumulation of species as population growth (blue curve) and food supplies (POC flux) increase. The curve approaches a tipping point where
population density is approximately 3500 individuals m-2 and d[E(S100)]/d(POC
flux) = 0 at POC flux = 14 mg C m-2 day-1. The tipping points of organic carbon
inputs are consistently between 10 to 20 mg C m-2 day-1 for the GoM and the
western North Atlantic macrofauna (Fig. 5), despite the varying of the mid-depth
diversity maximum (MDM) ( approximately 2000 m for the N. Atlantic6, 7, 16). An
inverse relationship between the descending limb and the population density has been attributed to competitive exclusion due to high population density at
the higher extreme of POC inputs3, 7, 24, in our case, the head of the Mississippi
Canyon. Regression equations are: Diversity, E(S100), as a function of POC flux, Y = -28.5 + 155.8 log10 X – 68 log10 X2, R2 = 0.61, F2, 48 = 37.72, P < 0.001;
Animal density as a function of POC flux, Y = -1997.8 + 4750.8 log10 X, R2 =
5
SI-2 Fig.2. Sampling locations in the Gulf of Mexico (red) and western North
6
SI-2 Fig.3. SeaWiFs satellite-based net primary production (NPP) from the
photosynthetic carbon fixation in the surface ocean. The western North Atlantic
sites6, 7, 16 used monthly composite averages of NPP from January 1998 to
December 200719. The northern Gulf of Mexico data are average of
biweekly-composite NPP from January 1998 to December 200212 during the benthic
sampling9, 10. The two highest NPP values were near the head of the
7
SI-2 Fig.4. Estimated organic carbon input to the seafloor communities on the
continental slope of the western North Atlantic and northern Gulf of Mexico. The POC input was calculated from net primary production (NPP) (SI-2 Fig.3) based
8
SI-2 Fig.5. Relationship of macrofaunal diversity, E(S100), to SeaWiFS
satellite-based net primary production (NPP) in the northern Gulf of Mexico12. The x axis
is in log10 scale. The unimodal model predicts that the tipping point of diversity in the northern Gulf of Mexico is comparable to that in the western North Atlantic (SI-2 Fig.6) at intermediate level of NPP between approximately 650 to
750 mg C m-2 day-1. Regression equation: Y = -1726.8 + 1243.7 log10 X - 216.3
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SI-2 Fig.6. Relationships between macrofaunal diversity to SeaWiFS
satellite-based net primary production (NPP) in the North Atlantic. Diversity, E(S50), of gastropods, polychaetes, and cumaceans are from the Gay Head-Bermuda
transect of the western North Atlantic6, 7 and diversity, E(S100), of the whole
macrofauna community is from the Georges Bank and western North Atlantic16.
The regression models predict that the maximum macrofaunal diversity occurs
when the surface primary production is approximately 700 mg C m-2 day-1;
however, the relationship for polychaetes is not statistically significant.
10
R2 = 0.58, F2,19 = 12.92, P<0.001; Polychaeta, Y = -1.7 + 4.9E-02 X - 3.1E-05
X2, R2 = 0.2, F2,18 = 2.19, P = 0.14; Cumacea, Y = -1.9E+01+ 9E-02 X - 6.9E-05
X2, R2 = 0.47, F2,12 = 5.28, P = 0.02; Macrofauna, y= 1.1E+01 + 1.2E-01 X -
9.5E-05 X2, R2 = 0.54, F2,19 =11, P < 0.001.
SI-2 Fig.7. Classification of estimated seafloor organic carbon input in the
northern Gulf of Mexico. The figure legend follows Fig. 1. The POC flux was
calculated using mean monthly NPP from January 1998 to December 200212.
The POC input was only mapped for the continental slope (POC < 80 mg C m-2
day-1). The highest POC class (dark blue) occurred near the shelf break at
depth of approximately 200 m (white line). Near the head of the Mississippi Canyon (MT1), the high POC input area has moved below the 200-m isobath into the deepwater due to the high surface phytoplankton production (SI-2 Fig.
11
center of the Sigsbee Abyssal Plain and the Florida Abyssal Plain (S4). The carbon cycling at these sites, based on sediment community oxygen
consumption25, agree remarkably well with the extremes portrayed here. The
three bright-color POC classes (red, green, and yellow) correspond to the highest diversity classes in SI-2 Fig.8 where E(S100) = 55 to 60.
SI-2 Fig.8. Predicted macrofauna diversity, E(S100), as a function of export POC
flux based on the regression model in Fig. 2. The figure legend follows Fig. 1. The red class shows the distribution of tipping points where E(S100) = 59 to 60 in the diversity-productivity relationship (Fig. 2). The wide distribution of tipping points (red class) in the northeast GoM near the De Soto Canyon indicates a potential diversity hot spot. High summer productivity associated with
anticyclonic and cyclonic eddies over the slope near the shelf have been
12
area also corresponds to a northeast mid-slope macrofaunal zone with a distinct
species composition10.
SI-3. Supplementary Equation(s):
Fig. 2. Regression equations is: Y = -28.5 + 155.8 log10 X - 68 log10 X2, R2 = 0.61, F2, 48 = 37.72, P <
0.001
Fig. 3. Regression equations are: Western Gulf of Mexico, Y = -36.8 + 174 log10 X -78.6 log10 X 2
, R2 = 0.58, F2,22 = 15.47, P < 0.001; Eastern Gulf of Mexico, Y = -28.5 + 158.6 log10 X - 69.1 log10 X
2
, R2 = 0.66, F2,23 = 22.31, P < 0.001
Fig. 4. Regression equations is: Y = - 1997.8 + 4750.8 log10 X, R2 = 0.88, F1,48 = 339.4, P < 0.001
Fig. 5. Regression equations are: Gastropoda, Y = -4.6 + 33.6 log10 X - 14.5 log10 X2, R2 = 0.49, F2,19 =
8.95, P < 0.01; Polychaeta, Y = 0.3 + 31.8 log10 X - 13 log10 X 2
, R2 = 0.43, F2,18 = 6.84, P < 0.01;
Cumacea, Y = 1.8 + 18 log10 X - 9.7 log10 X 2
, R2 = 0.59, F2,12 = 8.64, P <0.01; Macrofauna, Y = 6 + 70.5
log10 X - 29.5 log10 X 2
, R2 = 0.8, F2,19 = 37.47, P < 0.001.
SI-5. Supplementary Notes
Additional acknowledgements:
We thank Michael Rex, Nancy Maciolek, and Woollcott Smith for raw data from their publications. For macrofauan species identification, we thank G. Fain Hubbard and Yuning Wang (polychaetes), George D. F. Wilson (isopods), John M. Foster and Yousria Soliman (amphpods), Roe Davenport, Mary K. Wicksten and Min Chen (bivalves), Iorgu Petrescu (cumaceans), and Amélie H. Scheltema (aplacorphorans). We also thank Archie Ammons, Clifton Nunnally, Lindsey Loughry, Matt Ziegler, and Xiaojia Chen, Min Chen, Yuning Wang, and Yousria Soliman for sample sorting. We thank Captain Dana Dyer and the men and women onboard R/V Gyre for their assistance. This research was funded by the US Department of Interior, Minerals Management Service, Contract No
1435-01-99-CT-13
30991. This paper is a contribution of the Continental Margin Ecosystems (COMARGE) component of the Census of Marine Life (CoML) supportd by the Sloan Foundation.
Additional references
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