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2013 deGoeij Science Sponge loop

Authors:
  • NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University
DOI: 10.1126/science.1241981
, 108 (2013);342 Science
et al.Jasper M. de Goeij
Within Coral Reefs
Surviving in a Marine Desert: The Sponge Loop Retains Resources
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effects between duplicates. Although in some
cases, this interference can be exploited, for
example, by using it to repress gene expres-
sion (5,23), we propose that a more common
outcome is the minimization of this interfer-
ence in gene duplicates that persist over evo-
lutionary time. Whether such minimization is
generally accompanied by an increase in regu-
latory complexity, as seen here, remains to be
determined.
References and Notes
1. A. Force et al., Genetics 151, 15311545 (1999).
2. H. Innan, F. Kondrashov, Nat. Rev. Genet. 11,97108
(2010).
3. A. Wagner, Genome Biol. 3, reviews1012.1reviews1012.3
(2002).
4. A. Wag ner, Proc. Biol. Sci. 270,457466 (2003).
5. J. T. Bridgham, J. E. Brown, A. Rodríguez-Marí,
J. M. Catchen, J. W. Thornton, PLOS Genet. 4,e1000191
(2008).
6. F. Messenguy, E. Dubois, Gene 316,121 (2003).
7. C. Boonchird, F. Messenguy, E. Dubois, Mol. Gen. Genet.
226,154166 (1991).
8. B. B. Tuch, D. J. Galgoczy, A. D. Hernday, H. Li,
A. D. Johnson, PLOS Biol. 6, e38 (2008).
9. F. Messenguy, E. Dubois, Mol. Cell. Biol. 13,25862592
(1993).
10. A. Bender, G. F. Sprague Jr., Cell 50,681691
(1987).
11. A. E. Tsong, M. G. Miller, R. M. Raisner, A. D. Johnson,
Cell 115,389399 (2003).
12. C. R. Baker, B. B. Tuch, A. D. Johnson, Proc. Natl. Acad.
Sci. U.S.A. 108, 74937498 (2011).
13. M. J. Harms, J. W. Thornton, Curr. Opin. Struct. Biol. 20,
360366 (2010).
14. T. B. Acton, J. Mead, A. M. Steiner, A. K. Vershon,
Mol. Cell. Biol. 20,111 (2000).
15. N. Amar, F. Messenguy, M. El Bakk oury, E. D ubois ,
Mol. Cell. Biol. 20, 20872097 (2000).
16. A. Jam ai, E. Dubois, A. K . Vershon, F. Me sseng uy,
Mol. Cell. Biol. 22, 57415752 (2002).
17. J. Mead et al., Mol. Cell. Biol. 22, 46074621
(2002).
18. S. Tan, T. J. Richmond, Nature 391,660666
(1998).
19. T. E. Hayes, P. Sengupta, B. H. Cochran, Genes Dev. 2,
17131722 (1988).
20. F. Messenguy, E. Dubois, C. Boonchird, Mol. Cell. Biol.
11, 28522863 (1991).
21. G. C. Finnigan, V. Hanson-Smith, T. H. Stevens,
J. W. Thornton, Nature 481,360364 (2012).
22. M. Lynch, J. S. Conery, Science 302, 14011404
(2003).
23. M. Y. Dennis et al., Cell 149,912922 (2012).
24. Single-letter abbreviations for the amino acid
residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu;
F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met;
N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val;
W, Trp; and Y, Tyr.
Acknowledgments: We thank B. Tuch for assistance and
comments; O. Homann for assistance on experimental
techniques; and C. Nobile, C. Dalal, S. Devika, R. Bennett,
L. Mera, and T. Sorrells for comments. This work was funded
by grant RO1 GM057049 from the NIH.
Supplementary Materials
www.sciencemag.org/content/342/6154/104/suppl/DC1
Materials and Methods
Figs. S1 to S4
Tables S1 to S5
References (2538)
21 May 2013; accepted 6 September 2013
10.1126/science.1240810
Surviving in a Marine Desert: The
Sponge Loop Retains Resources
Within Coral Reefs
Jasper M. de Goeij,
1
*Dick van Oevelen,
2
Mark J. A. Vermeij,
3
Ronald Osinga,
4
Jack J. Middelburg,
5
Anton F. P. M. de Goeij,
6
Wim Admiraal
1
Ever since Darwinsearlydescriptionsofcoralreefs,scientistshavedebatedhowoneofthe
worldsmostproductiveanddiverseecosystemscanthriveinthemarineequivalentofadesert.
It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced
on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to
fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna.
This sponge loopwas confirmed in aquarium and in situ food web experiments, using
13
C- and
15
N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as
coral reefs persist in oligotrophic seasthe reefsparadoxand has implications for reef
ecosystem functioning and conservation strategies.
Coral reefs thrive in oligotrophic tropical
seas, but nevertheless belong to the most
productive ecosystems on Earth (13).
Efficient retention and recycling of carbon and
nutrients causes the net production of reefs to
be close to zero, despite high gross primary pro-
duction (4). Reef primary producers such as
corals and algae release up to 50% of their
fixed carbon (5,6), of which up to 80% im-
mediately dissolves in seawater (7). This shunt
into the dissolved organic matter (DOM) pool
represents a major flow of energy and nutrients
on coral reefs (7). In the open ocean, microbes
enable the transfer of DOM to higher trophic
levels through the well-established microbial
loop (8). Studies on coral reefs have therefore
also initially focused on microbes in reef waters
and adjacent permeable sediments to understand
the fate of DOM in these systems (7,911).
However, uptake rates by bacterioplankton, in
the sense of the microbial loop, are largely in-
sufficient to explain the observed DOM removal
on Caribbean and Indo-Pacific reefs (12). It there-
fore remains unclear how the largest source of
energy and nutrients on reefs is transferred to
higher trophic levels.
Cryptic habitats, for example, the coral reefs
crevices and cavities, are identified as major
sinks of DOM on Caribbean and Indo-Pacific
reefs (12). These habitats cover up to two-thirds
of the reefsvolume,andthebiomassofcryp-
tic organisms can exceed that on the open reef
(13,14). DOM removal rates in cryptic habitats
on Caribbean reefs (12) are comparable to the
average gross primary production rates of the
entire coral reef ecosystem (2). DOM removal
rates on Indo-Pacific reefs are lower (12)but
still account for up to 46% of the average gross
reef productivity. Sponges are primarily respon-
sible for total DOM uptake and remove the
same amount of DOM from the water column in
30 min as free-living bacteria take up in 30 days
(12,15). Therefore, sponges retain organic mat-
ter within the reef community and thereby pre-
vent energy and nutrient losses to the open ocean.
Surprisingly however, sponges respire only 42%
of the carbon taken up from the surrounding
water (15,16). Assuming that the remaining 58%
is used for growth, a biomass increase of 38% of
body carbon per day (more than a doubling of
biomass every 3 days) would be expected (16). In
reality, however, the net growth rate of sponges is
near zero (15,16), implying high losses of sponge
biomass through a rapid tissue turnover.
Arapidturnoverandextensivelossofsponge
cells to the surrounding water has been shown
for the sponge Halisarca caerulea (17).The
spongesfiltercells(choanocytes)divideevery
5 to 6 hours, representing the fastest cell cycle
found in any multicellular organism to date (17).
This rapid cell production is counterbalanced by
massive shedding of old choanocytes as partic-
ulate organic matter (POM or detritus) into the
water column (17). Massive shedding of POM is
also observed in other tropical sponges (18,19).
1
Department of Aquat ic Ecology and Ecotoxicology, Instit ute for
Biodiversity and Ecosystem Dynamics, University of Amsterdam,
Post Office Box 94248, 1090 GE Amsterdam, Netherlands.
2
Department of Ecosystem Studies, NIOZ Royal Netherlands
Institute for Sea Research, NL-4400 AC Yerseke, Netherlands.
3
Department of Aquatic Microbiology,Institute for Biodiversity
and Ecosystem Dynamics, University of Amsterdam, Carmabi,
Piscaderabaai z/n Willemstad, Curaçao.
4
Department of Aqua-
culture and Fisheries, Wageningen University, Post OfficeBox
338, 6700 AH Wageningen, Netherlands.
5
Faculty of Geo-
sciences, Utrecht University, Budapestlaan 4, 3584 CD Utrecht,
Netherlands.
6
Faculty of Health, Medicine and Life Sciences,
Maastricht University, Post Office Box 616, 6200 MD Maastricht,
Netherlands.
*Corresponding author. E-mail: j.m.degoeij@uva.nl
4 OCTOBER 2013 VOL 342 SCIENCE www.sciencemag.org108
REPORTS
This suggests that sponges use the majority of
incorporated carbon to rejuvenate their filter sys-
tem and maintain a high cell turnover.
We hy p othe s ize he r e tha t s h ed sp o n ge ce l l s
(detritus) are subsequently ingested by particle-
feeding organisms (detritivores). Sponges thereby
make the energy and nutrients stored in the DOM
pool available to organisms at higher trophic lev-
els that would otherwise be unable to capitalize
on this resource. Because small detritivores (such
as crustaceans and polychaetes) are themselves
fed upon by larger animals higher in the food
web, sponges are at the base of a sponge loop that
ultimately recycles energy and nutrients back into
the ecosystem in a similar way as the microbial
loop does in the open ocean.
To st udy th e prop o sed D O M-s pong e-de t rit u s
feedback loop on coral reefs, we tested three key
predictions of this hypothesis: (i) sponges take up
DOM, (ii) sponges convert DOM into detritus,
and (iii) sponge-derived detritus is taken up by
detritivores. These three predictions were first
tested in flow chambers in a controlled running-
seawater aquarium setup (fig. S1) using
13
C- and
15
N-enriched DOM, extracted from the cosmo-
politan marine diatom Phaeodactylum tricornutum,
as a food web tracer (20).
All three key elements were confirmed ex-
perimentally (Fig. 1). Four common reef sponge
species showed uptake of dissolved organic car-
bon (DO
13
C) and nitrogen (DO
15
N) (Fig. 1A).
All four species subsequently produced
13
C- and
15
N-enriched detritus (Fig. 1B). The four sponge
species converted 11 to 24% of the assimilated
DO
13
Cintodetritus(PO
13
C) and 18 to 36% of
the DO
15
NintoPO
15
Nwithin3hours(Fig.1,A
and B). Control incubations showed that detritus
production without sponges was less than 4%
of the detritus production in incubations with
sponges. Detritivores subsequently fed on the
labeled sponge-derived detritus (Fig. 1C). Iso-
topically enriched detritus, collected from speci-
mens of the four tested sponge species (fig. S2)
that were repeatedly fed with
13
C- and
15
N-enriched
DOM (20), was added to six cores containing cav-
ity sediments with residing fauna and, in three out
of six cores, motile fauna were added (hermit
crabs and snails) (fig. S1). Within 6 hours, sponge
detritus was incorporated by 17 out of 28 (
13
C) and
23 out of 28 (
15
N) specimens of detritivores.
After experimental confirmation of a sponge
loop in flow chambers, the question arose wheth-
er this newly found pathway could actually be
identified in a complex coral reef environment.
Therefore, the water exchange of two in situ
cryptic reef cavities (75 and 100 liters) with the
surrounding reef water was temporarily restricted
(12,20), and
13
C- and
15
N-enriched DOM was
injected into the enclosed cavity at the start of
two consecutive incubation periods of 3 hours
(fig. S3). Once we restored the water exchange
between the water column and the cavities, the
presence and fate of labeled DOM were ana-
lyzed over the subsequent 45 hours within the
main cavity compartments; that is, sponges,
sponge-derived detritus, surface sediment, bac-
terioplankton, nonsponge filter feeders, and mo-
tile fauna such as hermit crabs and snails (20).
The relative abundance of
13
Cand
15
Ninthese
compartments over time provided qualitative
Fig. 1. Fate of DOM tracer
13
C(redbars)and
15
N(blue
bars) through sponge-
driven DOM transfer in flow
chamber experiments. (A)
Uptake of tracer DOM (DO
13
C
and DO
15
N; micromoles of
tracer per millimole of sponge
CorNTSD; n=4speci-
mens) by the sponge species
Halisarca caerulea (Hc), Hal-
iclona implexiformis (Hi),
Chondrilla caribensis (Cc),
and Scopalina ruetzleri (Sr).
The uptake of DO
13
Cby
sponges is further specified
in tissue assimilation (dark
red bars) and respiration
(light red bars). (B)Produc-
tion of detritus (PO
13
Cand
PO
15
N; micromoles of tracer
per millimole of sponge C or
NTSD; n=4specimens)
by the sponges HC, HI, CC,
and SR. (C)Uptakeof
sponge-derived tracer detritus
(PO
13
CandPO
15
N; micro-
moles of tracer per millimole
of faunal C or N TSD) by
detritivores (n=28speci-
mens) picked from six cores
of reef sediment; three cores
were supplemented with hermit crabs and snails.
Fig. 2. In situ sponge-
driven transfer of tracer
DOM (red line,
13
C; blue
line,
15
N) in coral reef cav-
ities after a temporary
6-hour closure (gray shad-
ing) and the subsequent
45 hours. The mean above-
background isotope tracer incor-
poration (Dd
13
Cand Dd
15
N)
of two cavities is shown for the com-
partments (A)sponges,(B)sponge-
derived detritus, and (C)detritivores;
that is, nonsponge filter feeders (solid
line) and motile fauna (dashed line). For guidance,
the interval of peak tracer incorporation is high-
lighted for each compartment. t,time;h,hours.
www.sciencemag.org SCIENCE VOL 342 4 OCTOBER 2013 109
REPORTS
evidence in support of our proposed pathway of
sponge-driven DOM transfer (Fig. 2). After the
introduction of labeled DOM to coral cavities, the
uptake of tracer
13
Cand
15
N was first observed
in sponges (first prediction: DOM-sponge; mean
sponge Dd
13
C27permil()andDd
15
N111;
Fig. 2A) immediately after the 6-hour incubation
period. Between 12 and 24 hours after the in-
cubation, the relative isotope abundance peaked
in sponge-derived detritus (second prediction:
sponge-detritus; mean detritus Dd
13
C24and
Dd
15
N261;Fig.2B).Thesponge-derivedde-
tritus was finally transferred into motile fauna
and nonsponge filter feeders after 45 hours (third
prediction: detritushigher trophic levels; steady
increase to a detritivore Dd
13
C3to4and Dd
15
N
12 to 17;Fig.2C).The
13
C:
15
Nratioofsponge-
derived detritus was lower than the
13
C:
15
Nof
the sponges (Fig. 2, A and B), indicating that
the detritus was relatively enriched in N. The
DOM-derived Dd
13
CorDd
15
N in the surface
sediment or the bacterioplankton was generally
lower than 2, indicating limited uptake by
these compartments.
The seemingly paradoxical observation that
productive ecosystems such as coral reefs thrive
in nutrient-poor waters can only be explained
through processes ensuring efficient capture, re-
tention, and recycling of energy and nutrients.
Such tight recycling mechanisms involve micro-
bial processing of coral- and algal-derived DOM
in the water column and permeable reef sands
(7,11). Here we show that, in addition to the
transfer of DOM via bacteria to fauna (8), sponges
transform the majority of DOM into particulate
detritus, a pathway that has hitherto not been
recognized (Fig. 3). The underlying mechanisms
of DOM uptake and rapid cell turnover in sponges
are not yet fully understood. Sponges form close
associations with microorganisms, forming so-
called holobionts, and both sponge cells and mi-
crobes can assimilate DOM (16), although their
relative contributions remain largely unknown.
The sponge loop nevertheless greatly enhances
our growing understanding of the efficiency that
typifies coral reefs, thus supporting reef life, in-
creasing biodiversity (21,22,)andmaintaining
high productivity. Sponges not only recycle the
energy retained in DOM but also provide reef
fauna with a source of nutrients (such as N),
thereby fertilizing the coral reef ecosystem. The
efficient and fast uptake, retention, and release
(23)ofnutrientswithintheoriginallyoligotrophic
ecosystem by sponges may also catalyze nutrient-
induced shifts in the coral-algal-microbe com-
munity after eutrophication, often associated
with coral reef degradation (24,25). Top-down
controlled shifts from coral- to sponge-dominated
reefs have been predicted (26)andrecordedin
the Caribbean (27,28), but still sponges are rarely
considered in analyses of alternative stable states
on coral reefs. Other oligotrophic ecosystems where
sponges are abundant, such as deep-sea cold-water
coral reefs and temperate Mediterranean reefs,
may also sustain the functioning of a sponge loop.
Deep-sea sponges contribute substantially to the
respiration of cold-water reef communities (29)
and produce large amounts of detritus (30). Medi-
terranean reefs are dominated by (cryptic) sponges,
of which several abundant species are found to
take up DOM (31). Although this study shows
the presence of the sponge loop mainly qualita-
tively, DOM turnover by sponges (15)approaches
the daily gross primary production of the entire
reef ecosystem (2,4), suggesting that this ener-
getic pathway is of great ecological importance
(Fig. 3). Recognition of the key role of sponges in
coral reefs has, consequently, implications for
studies on ecosystem services and conservation
strategies in ecosystems where sponges are a
ubiquitous component.
References and Notes
1. H. T. Odum, E. P. Odum, Ecol. Monogr. 25,291320
(1955).
2. B. G. Hatcher, Trends Ecol. Evol. 5,149155 (1990).
3. M. J. Atkinson, J. L. Falter, in Biogeochemistry of Marine
Systems, K. D. Black, G. B. Shimmield, Eds. (Blackwell
Publishing, Oxford, 2003), pp. 4064.
4. C. Crossland, B. Hatcher, S. Smith, Coral Reefs 10,5564
(1991).
5. Y. Tanaka, T. Miyajima, I. Koike, T. Hayashibara,
H. Ogawa, Bull. Mar. Sci. 82,237245 (2008).
6. A. F. Haas et al., J. Exp. Mar. Biol. Ecol. 389,5360
(2010).
7. C. Wild et al., Nature 428,6670 (2004).
8. F. Azam et al., Mar. Ecol. Prog. Ser. 10,257263
(1983).
9. Z. Dubinsky, I. Berman-Frank, Aquat. Sci. 63,417
(2001).
10. C. E. Nelson, A. L. Alldredge, E. A. McCliment,
L. A. Amaral-Zettler, C. A. Carlson, ISME J. 5,13741387
(2011).
11. A. F. Haas et al., PLOS ONE 6, e27973 (2011).
12. J. M. de Goeij, F. C. van Duyl, Limnol. Oceanogr. 52,
26082617 (2007).
13. C. Richter, M. Wunsch, M. Rasheed, I. Kötter,
M. I. Badran, Nature 413,726730 (2001).
14. S. Scheffers, G. Nieuwland, R. Bak, F. van Duyl,
Coral Reefs 23,413422 (2004).
15. J. M. de Goeij, H. van den Berg, M. M. van Oostveen,
E. H. G. Epping, F. C. Van Duyl, Mar. Ecol. Prog. Ser.
357,139151 (2008).
16. J. M. de Goeij, L. Moodley, M. Houtekamer, N. M. Carballeira,
F. C. van Duyl, Limnol. Oceanogr. 53, 13761386
(2008).
17. J. M. de Goeij et al., J. Exp. Biol. 212, 38923900
(2009).
18. H. M. Reiswig, Biol. Bull. 141,568591 (1971).
19. G. Yahel, J. Sharp, D. Marie, C. Hase, A. Genin, Limnol.
Oceanogr. 48,141149 (2003).
20. Materials and methods are available as supplementary
materials on Science Online.
21. M. Slattery, D. J. Gochfield,C. G. Easson, L. R. K. ODonahue,
Mar. Ecol. Prog. Ser. 476,7186 (2013).
22. B. W. Bowen, L. A. Rocha, R. J. Toonen, S. A. Karl;
the ToBo Laboratory, Trends Ecol. Evol. 28,359366
(2013).
23. M. W. Southwell, J. B. Weisz, C. S. Martens, N. Lindquist,
Limnol. Oceanogr. 53,986996 (2008).
24. T. P. Hughes et al., Curr. Biol. 17,360365 (2007).
25. S. A. Sandin et al.,PLOS One. 3, e1548 (2008).
26. M. González-Rivero, L. Yakob, P. J. Mumby, Ecol. Modell.
222, 18471853 (2011).
27. A. V. Norström, M. Nystrom, J. Lokrantz, C. Folke,
Mar. Ecol. Prog. Ser. 376,295306 (2009).
28. S. E. McMurray, T. P. Henkel, J. R. Pawlik, Ecology 91,
560570 (2010).
29. D. van Oevelen et al., Limnol. Oceanogr. 54,18291844
(2009).
30. U. Witte, T. Brattegard, G. Graf, B. Springer, Mar. Ecol.
Prog. Ser. 154,241252 (1997).
31. M. Ribes et al., Environ. Microbiol. 14, 12241239
(2012).
Acknowledgments: J.M.d.G. and D.v.O. contributed equally
to this work. We thank D. M. de Bakker, C .G. W. Whalen, and
B. E. Alexander for their technical assistance in the field
and lab; C. E. Mueller, and P. van Rijswijk for preparation of
the DOM substrate, lab assistance, and isotope analysis; and
E. R. Hunting for discussion. This work was supported
financially by the Innovational Research Incentives Scheme
of the Netherlands Organization for Scientific Research
(NWO-VENI; 863.10.009, granted to J.M.d.G.) and the
Schure-Beijerinck-Popping fund. J.M.d.G. and R.O. are also
affiliated with Porifarma BV Poelbos 3, 6718 HT Ede,
Netherlands. The authors declare no conflicts of interest.
A detailed description of all materials and methods and
additional data are available as supplementary materials.
All authors discussed the experimental data and jointly
wrote the manuscript. The data are deposited in DRYAD,
accession no. http://doi.org/10.5061/dryad.4gb17.
Supplementary Materials
www.sciencemag.org/content/342/6154/108/suppl/DC1
Materials and Methods
Figs. S1 to S3
References (3239)
17 June 2013; accepted 6 September 2013
10.1126/science.1241981
Fig. 3. A simplified scheme of dominant pathways (millimoles of C m
2
day
1
)oforganiccarbon
transfer on coral reefs in the pelagic (blue), benthic reef (green), and sediment (yellow) eco-
system compartments. The proposed sponge loop (red arrow) is shown in addition to the classical mi-
crobial loop. GPP, gross primary production. *(2),(5,6), (7), (12), §(11,12(11); see (20)fordetails.
4 OCTOBER 2013 VOL 342 SCIENCE www.sciencemag.org
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