OCEANO LOGICA ACTA, 1982, N' SP
~
-------'----------1~r----
The energetics of detritus utilisation
in coastal lagoons
De tritus
Herbivore
Phytoplanklon
Encrgy conversion
Détritus
Herbivores
Phytoplancton
Conversion de rtnc rgic:
and nearshore waters
R. C. Newell
InstÎtUlc for Marine Environmcntal Rcscarch , Prospect Place, Plymouth PLI 3DH , England.
ABSTRACf
SÎnce production by macrophytes and saltmarsh plants gre81ly exceeds direct consumption by
herbivores, the consumer community of Jagoons and estuarinc ccosystcms Î$ exposed to a food
rcsource which has eDiered the watc! colum n as plant debris.
It is shown Ihat although primary production by saltmarshes is high. the combincd production
br macro phytcs, phyto plankton and smaller algae in a Iypical kelp bed is similar to Ihat of a
saltmarsh and close to Ihat attained by phytopla nklon under nut rie nt-rich upwelling
conditions. In cach, primary production is approxima tely 1.5 % of the incident energy.
Dcspite the fact that primary production in lagoons and estuari ne ecosystems docs not appear
to be unduly higher than that attained in planktonic systems, the evidence for al leasl the
detritus-feeding consumer community associaled with macrophyte beds is that secondary
production is approximately 10 % of primary production. This is vcry similar to the production
attaincd in a typical plant-herbivorc systcm and suggests thal the dctrilivores are utilising
fragmented plant material di rectly in an analogous fashion tO herbivores. Secondary
production by thc consume r community would be anticipated to be at least an order of
magnitude lower Ihan this if lhe decomposer o rganisms re presented a pri ma ry food resource
for the consume r community of nearshorc waters.
Finally , it is shown tha t energy conversion by decomposer o rganis ms is not markedly highe r
Ihan that in food chains in other ecosystems.
The fact that the production attained by the detritivores relalive to primat)' production is vcry
similar to that ac hieved in a Iypical plant-herbivore community suggesis Ihat the consume rs
utilise plant deb ris directly as a food resource before it has been mineralised through the
decomposer food chain. Living phytoplankto n cells and lo ng- lasting paniculale debris may
thus form the dominant food resource for the consume r community o f estuaries, lagoons and
nea rshore waters. The microhele rotrophic decomposer o rganisms, however, appear to be
primarily responsible for recycling unexploitcd plant debris and Ihus sustain the primary
production near to the maximum value of 1.5 % of incident energy which is commonl y allained
in nearshore ecosystems.
Oceanof. Acta , 1982. Proceedings Inter national Symposium o n coastal
SCORlIABO/ UNESCO , Bordeaux, France, 8- 14 Scpte mbe r, 198 1, 347-355.
Rf:SUMË
lagoons.
Utilisation é nergétique du détritus dans les lagunes et les eaux côtières.
Les communautés de consommateurs dans les écosystèmes lagu naires cl estuariens dépendent
d' une ressource trophique venant essent ielle ment de débris végélaux, la production pri maire
des herbiers dé passant largement leur consommatio n directe par les herbivores. Il est montré
que bien que la production primaire des marais maritimes soit élevée, la production combinée
des macrophytes, du phytoplancton cl des microalgues dans les matelas végétaux benthiques
est similaire à celle des marais maritimes et voisine de celle des zones d'upwclling. Dans
chaque cas, la production primaire est approximativement égale à 1 % de l'énergie incidente.
En dépit du fait que la production primaire dans les lagunes n'apparaît pas êlre très supérie ure
à celle des systèmes pélagiques, on a des ra isons de pense r que, au moins pour les délritivores
associés aux matelas de maerophyles, la production secondaire est éga le à approximativement
10 % de celle de la production primaire. Ce rappan de production est très se mblable à celui
observé pour un système typique plante-herbivore. ce qui suggère que les délritivores utilisent
le matériel végétal fraction né directeme nt d'une façon identique a ux herbivores. La
production secondaire par les communau tés de consommateurs pourrait êlre inférieure au
347
R. C. NEWELL
moins d' un ordre de grandeur si les décomposeurs représentaient une source de nourriture
principale pour la communauté des consommateurs des caux côtières. Enfin on montre que la
conversion d'énergie par les organismcs décomposeurs n'est pas très supérieure à celle
observéc dal's les chaines alimentaires d'autres écosystèmes.
Le fait quc la production des détritivores, relativement à celle d'une communauté typiquc
plante-herbivore, soit très similaire suggère que les consommateurs utilisent directement les
débris végétaux comme source de nourriture avant que celle-ci ait été minéralisée par les
déeomposcurs. Les particules vivantes phYlOplanctoniques et les particules détritiques à long
temps de résidcnce constituent ainsi la ressource trophique majeure pour les communautés de
consom mateurs des lagunes ct aussi des estuaires et des caux côtières. Les décomposcurs
microhétérotrophes apparaissent cependant être les responsables principaux du recyclage des
débris végétaux non exploités ct ainsi amènent la production primaire à son taux maximum de
5 % de l'énergie incidente; taux communément atteint dans les écosystèmes côtiers.
Oceanol. Acta, 1982, Actes Symposium International sur les
SCOR/IA I10 / UNESCO. 110rdeaux, 8-14 septembre 1981. 347-355.
lagunes
côtières,
increased step in the food chain could be offset by possession of a mueh higher conversion cfficicncy than 10 % by
decomposer organisms and by their subsequent efficient
utilisation by the consumer community of the coastal
ccosystcm.
The amounts of energy which flow through this detri tal
pathway, and abovc ail, the e ncrgetics of conversion of
plant debris through the decomposer organisms arc thus
central to our underslanding of the role of primary production by coastal plants in the maintenance of the characteristically high secondary production in nca rshore communi·
tics.
INTRODUCfION
The sign ificance of energy flow studies has becn widely
recognizcd in the ecology of terrestrial and fresh water
communities and they provide sorne insight into the ways in
which encrgy fixed by planls may bccome available to
suppo rt consumcr communities at different trop hic levels.
ln many simple food chains, for examplc, it has been
est imated thal as much as 90 % of the energy from primary
production is dissipaled in the stcp to primary consumers
(herbivores) whilst of the residual 10 % which is incorporated into the hcrbivores, a further 90 % is dissipated in the
step 10 primary carnivores leaving only 1 % o f the original
energy from primary production ineorporated into the
consumer community at the second trophic level. Although
a 10 % .. energy caseade" of this type has been generally
found to apply to simple plant-herbivore-carnivore food
chains. especially in sorne terrestrial communities and in
frcshwater planktonic systems (see Smith, 1977) , food webs
in coastal ccosystems are o ften very complicated (see also
Steele, 1974; Mills, 1975). Partly for this reason, energy
flow sludies have only becn relatively recently attempted for
coastal communiiies as a whole, and where they have been
made, obvious differences emergc from the simplc food
chain deseribed abovc.
ln almost ail cases, primary production by the macrophytcs
and saltmarsh plants which characlerizc coa~tal walcrs
grcatly exceeds consumption by herbivores. Most of the
encrgy [rom primary production thus becomes availablc to
support eonsumcr production only aftcr il has been
fragmented and processed through decompose r pathways.
ln this respect, the nearshore ecosystems are more analogous with the detritus based food chains in forest Icaf litter
than with open grassland systems although thesc, 100, may
have a significant proportion of primary production channelled through decomposer pathways. In cstuarinc systems
Teal (1962). for example, showcd that primary consumer
respiration accounted for only 7 % of nel above ground
production in a Spartina marsh in Georgia, with bacterial
respiration accounting for as much as 47 % of net production and the residual 45-46 % being potentially avai!able for
export from the saltmarsh 10 support consumer production
in the water column.
If. as has been shown abovc, thcre is likely to be a 90 %
dissipation of encrgy with cach slep in the food chain , il
follows tha! primary production in coastal zones must bc
much higher than in othcr ecosystems 10 offset the interpolation of dccomposer organisms into the food chain, or the
ratio of consumer production to primary production must bc
al Icast an order of magnitude lower than in a simple plantherbivore system. Altcrnatively, if the decomposcr organisms themselves represent a principal food rcsource for
consumer organisms (NewelL 1965 j Darncll , 1967 ; Odum.
De La Cruz. 1967), the encrgetic losses associated with an
THE STRUCrURE OF NEARSHORE COMMUNITI ES
The carbon incorporated by the eoastal plants ultimately
controls the amount of energy which is available 10 support
secondary production, and is affectcd both by the relative
areas of saltmarshes, macrophytes and phytoplankton as
weil as by water depth, light and nutricnts. There is sorne
evidcnce which suggests that primary production by the
nearshore macrophytes and by saltmarsh grasses may he
considerably grcatcr than that by phytoplankton , and thus
the consumer product ion in estuaries and lagoons may
remain high despite the additional steps in the food chain
which arc associated with the utilisation of dccomposing
plant debris. Mann (1972 ; 1973), for cxample , found that
primary production in the scaweed zone at St Margaret's
Bay, Nova Scotia, greally exceeded that in the shallow
waters of the bay ilself, even though the area occupicd by
thc phytoplankton was greater than that of the seaweed
zone. Again, Penhale and Smith (1977) showed that production by the saltmarsh grasses Sportina altemiflora and
Zostera mari/la was as mueh as 311.3 g carbon.rn- 2.yr- 1 and
335 g carbon.m - 2.yr- 1 respectivcly, cornpared with only
69.3 g c.m- 2.yr- 1 by the phytoplanklon in an estuary near
Beaufort, North Carolina_ Howevcr, in Ihis case the large
area of water eompared with that occupied by saltmarsh
plants rcsulted in the major primary production for the
estuarine ccosyslem as a whole bcing by the phytoplankton.
Primary production by a Spartina marsh is generally regarded as being amongst the highest for any plant community
and exceeds that of many lropical crops, having a production which is twice Ihat of sugar cane (sec Smith. 1977). This
is probably duc to thc combinat ion of high tempcratures.
light and nutrients ralher Ihan any intrinsic incrcase in
photosynthetic efficiency and reccnt mcasurcmenlS on phytoplankton production suggest that under favourable conditions it can bc as high as that of a Spartif/a marsh. Brown
(1980; 1981) has recently cstirnaled primary production by
phytoplankton in upwelling areas off the Cape Pcninsula,
South Africa, where nUlrients arc rarely limiling, and has
shown Ihat average net production down 10 the compensa-
34.
DETRITUS UTiLIZATION IN LAGOONS AND COASTAL WATERS
Table 1
T~ primary production and lIel production tffidmcy in Ihrtt difforent sources of primary production. Ali l'a lu('$ calcu/tlled as "'tafl amrual
prodJ4ctû)II kl.m - z x J()l. Bastd 011 Newelf ct al. (1982).
No<
produclion
Input as
Iighl
x 10'
Net productio n
efficienc)'
%
0.538
36.06
1.49
Rcca1culaled
from Brown
(1980 ; 1981)
Kelp btd
(a) Ph ytoplank!on
(b) Undcrstorc)' algae
(c) Kelp + epiphytcs
TOlal
0.239
0.11 6
0.232
0.587
36.06
1.63
Salt marsh
0.343
25.08
1.37
Newcll el al. ( 1982)
Rccalculated
from Teal (1962)
Primary produccr
Average phylOplQllklotr
in upwelling afea.
x 10'
lion depth is as high as 0.5 x 1~ kJ.m- 2.yr- J of watcr
su rface. The corresponding figure for phOlosynthetically
active radiation is 36.08 x 1~ kJ. m-1.yr- 1 so that the net
production efficiency for the phytoplankton in a nutrientrieh zone is 1.49 % (Newell ef al., 1982 ; sec also Table 1), a
value which is very similar to thal recorded by Teal ( 1962)
for a Sparrina marsh. He obtllined Il radiation input figure
cquivalcnI 10 25.08 x 10' kJ. m- 1.yr- 1 and a primary production figu re of 0.343 x 1 ~ kJ .m - l.ye! whieh yields a net
production cfficiency of 1.37 %. A value of 1.4-1.5 % thus
see ms to approach the maximum convcrsion efficiency
attained by both the wetland vegetation which comprises a
major input into coastallagoons and estuaries, and by the
phytoplanla on in waters which are ric h in nutrients. Any
differences hetween the two in other areas are probably
attributable 10 the cffects of lu rbidity and nutrient limitation
in suppressing primary produclion by the phytoplankton
ratltcr titan to a funda mental diffcrcncc in the primary
productivity of coastal plants compared with phYloplankton.
As the waters become shallow, the depth through which
photosynthesis can occur beeomes less and one might e:o;pect
a reduction in total energy fi:o;ed Ihrough photosynthesis. lt
is in this zone that the maerophytes and aquat1c seagrasses
tend to replace Ihe phYlOplankton as a source of primary
production , and it is interesting to fin d Ihat in a recent sludy
o f a kelp bed the combined prima ry productio n by macrophytes and phytoplankton was similar 10 Ihat of the
phytoplanklon alone in the deeper upwelling water column
nearby (Newell et al., 1982). Table 1 shows that the
phytoplankton production in a shallow macrophyte bed of
10 m depth was 0.239 x l~ kJ.m - 2.yr- 1 compared with Ihe
value o f 0.538 x l ~ kJ .m- 1.yr- 1 in the deep water column .
Howcver the macrop hytes, comprising kclp ?luS epiphytes
contributcd an additional 0.23 x lOS kJ .m- .yr- I and the
underslOrey algae a further 0.116 x l~ kJ .m- 1.yr- 1• The
total production in a mi:o;ed shallow water corn munit y
dominated by maerophytes was Ihus appro:o;imatcly
0.587 x I~ kJ.m- 2.yr- 1 whieh rep rescnls a net production
cfficicncy of 1.63 % from Ihe incident radiation input of
36.08 x I~ k1.m- l .yr- 1 (Newell et al., 1982 ; also Table 1).
The reduelion in waler de pth , and hence in water column
through whieh primary production by the phytoplankton
could occur is thus almost balanced by Ihe contribution of
macTophytes which QCCur in the coastal stTip.
For shallow water eoastal lagoons as a whoJe , the refore , it
secms likely that the combined energy input from primary
prod uction by phytopla nkton, macrophytes and maritime
grasses which is necessary to support the consumer communit y is likely to he approximately 1.5 % of the incident
e nergy fro m radiation and represents a maximal attainable
e nergy fi:o;a tion by planls under conditions wherc nutrients
arc no n-limiting. This is equivalellt to a ncl production of
approximately 0.3-0.5 x l ~ kJ.m - 2.yr- 1 depending on lali-
Source
tude and , using the energetics of the very simple food chain
descrihed above , wc would anticirate Ihis 10 ?c capable of
supporting 0.03.0.05 x I ~ kJ .m- .yr- I of pnmary consumer production and 0.003.0.005 x 10' kJ. m- 2.yr- 1 of carnivore production.
Unfonu natcly, there are very few nearshorc communities
where production by both primary and secondary consumers have been eSlimated and where losses by tidal f1u shing
fro m the system is small. Wc have reccnlly , however, using
data mainly from Velimirov et al. (1977) and Field el al.
( 1980) , calculated the combined production of the det ril usfceding primary consu mers in a macrophyte bed and have
compared both Ihis value and the production by larger
carnivores with the net primary production in the syste m
(Newell ~t al. , 1982). The rcsults show Ihat even though the
primary consumers utilise detrital mate rial , their production
was 0,(1614 x 10' kJ.m-l.yr- 1 whilst that of the large carnivores was 0.0063 x 10' k.J .m- 1.ye l . T ltcsc values re prescnt
an ccological cfficiency of 0.064/0.587 x 100 = 10.42 % by
the primary consumers and 0.0063/0.0614 x 100 = 10.26 %
by the larger carn ivores and suggcst thal the energeties of
the shalJow waler communities may be in close agreement
wil h those of other ecosystems, deSplle the complc:o;ity of
the food webs and the fact that the primary consumers
ulilise the products of primary production through the
deuilal pathway. There is thus no cvide nce fro m this
macrophyle community that primary production is higher
than in the nearby planktonic ecosystem nor that seeondary
production by the detrilal consu mer organisms is less Ihan
o ne wo uld anticipatc for primary consumers in other
simpler food chains. 11 would be of conside rable interest to
make similar comparisons for communilies bascd on seagrass debris but the information is not, as far as 1 am aware,
available al present.
This close agreement helween production by the consumer
organisms which ulilise de trital material and that which
would he predieted for hcrbivores suggests that the eonsumers arc utilising the products of fragmenlation directly, in
an analogous way to herbivores. Alternatively, if the
detritivores arc utilising the decomposer organisms as a
source of food (Newell , 1965; Darnell , 1967 ; Odum , De La
C ruz, 1967 ; Hargrave, 1970) , the conversion efficieney of
the microbiota and its subsequent incorporation by detritivores must he sufCicient l)' high 10 account for the large
production by the primary consumers, despite the interpolation of at least one addilional step in the food chain.
ENERGETICS OF DETRITUS DECOMPOSITION
Our knowledge of the turnove r and microbial ulilisation o f
detrital material has, until rcccnt ly, becn mainW based on
expcriments on the kinelics of uptake of simple 4C·labc lled
substrates by mixed populations of microheterotrophs from
planktonic systems (Wright . Hobbie , 1965 ; Hobbie, 1967 ;
349
R. C. NEWELL
Hobbie, Crawford, 1969 j Gordon el al. , 1973 ; Crawford el
al., 1974). Synchronous measurements of the 1"<:0 2 (rom
respiration thcn allows calculation of .. apparent growth
yie lds" obtaincd by division of the amount of substrate
incorporated into the organism per unit time (the net
uptake) by the IOtal uptake (net uptake + respired 14C)
(Wi lliams, 1970 ; 1973). These methods suggest that sorne
orga nie substrates can bc Încorporated with a high e(ficieney
by marine microheterotrophs, but they are unlikely to apply
to the ove rail conversion of the mixed dissolved and
panieulate fract ions represented by the deeomposition of
piani debris as a whole. Indeed , they can probably only bc
applied to the 5mall labile eomponents of photoassimilated
carbon whieh i5 released by phytoplankton rathee than to
the wholc of the dissolved fraction of the debris (Andrews,
Williams, 1971 ; Ogura , 1972 ; 1975 j Wiebc, Smith . 1977;
Larsson , Hagstrôm, 1979).
An altcrnative has been 10 isolate specifie strains of bacteria
and to study Iheir cnergy yie1ds and growth on single
substrates (fo r review, sec Payne , 1970). Thc isolation of
such strains generalty results in the se lection of ralher large
bacteria comparcd with Ihose which are fo und in natural
waters, and which show both an efficient uptake and
conversion of specifie substratcs including even rclatively
complex structural polysaccharides. Unfortu nate[y, neilher
this technique nor that based on the kinetics of uptake of
simple substrates altow prediction of the ability of complcx
natura l populations o f microheterotrophs to convert the
mixture of dissolved and partieulate o rganic mattcr which is
characteristically released during the decomposition of
debris from macrophylcs, phytoplankton and seagrasscs.
Another approach , and one which we have recently used to
compare the heterotrophic fate of macroalgae (Newell el
al.. 1980 ; Lucas el al., 1981; Stuart el al., 1981 a,b j
reviewed in Linley, Ncwell, 1981 j Newelt , Lucas, 1981 ),
phytoplanklOn (Newell et al., 1981) and debris from sa[tmarsh grasses (Newell et al., 1982), is to express the
.. carbon conversion cfficiency" in tenns of the amounl of
carbon incorporaled by the mieroheterotrophic decomposer
corn munity per unit carbon used from natural plant debris.
The increase in biomass o f bacteria and protowa, and ils
carbon equivaJc nt , ean bc calculated fro m estimates of their
numbcrs by acridine orange direct counling (AODC, see
Hobbic el al. , 1977 ; Daley, 1979) and ccII dimensions using
scanning elcctron microscopy. If these cstimates arc syn·
chronised with losses of carbon from thc culture media , the
.. carbon conversion cfficiency " (mg carbon incorporated
into bactcria/mg carbon used from the subst rate) can bc
calculated. This method has the advantages that natural
debris, rather than single component substrates are avaiJa·
bic as a carbon source , and that nal ural heterogeneous
popu lations of microhctcrotrophs rather than specific bacte·
rial isolates arc used. Unli ke indirect methods of assessing
microbial biomass (see Hamilton, HOlm·Hansen, 1%7;
Holm- Hansen, 1973; Moriarty , 1975; 1977), il is also
possible to directly observe changes in the relat ive abundance of different eomponents of the microheterotrophic
community, and to follow carbon conversion not only from
a carbon source into bacteria, but from baelc ria inlO grazing
micronagellatcs and ciliates.
~ompositlon
Table 2
The prodm:tiQII of orgall~ mor~r /rom ph)'lopwnk/Qn and btlllhû;
plallls in 011 ~Sl!lary n(ar Beaufort, NOrlh Carolina. TM dota ore
upressed bOlh in semIS of gramJ ofcarbon.m-2.,vr. -1 and;n /trmJ of
lM lotal OrtO of warer in lM esruory (based on Penhak, Sm;lh,
1977).
Souree of
production
Production
g.C.m- 1.y-l Area
PhytoplanklOn
69.3
335.0
Zo5ura marina
ËpiphYlcs
Sparlina alre rnij/ora
Relative
production
g.e, m- z watcr.yr - 1
532
69.3
58.6
74.5
93
93
311.3
31
17.6
13.0
macrophyte bcds, phytoplankto n production is equal in
sign ificanee to that of the macrophytcs (sec Table 1) so that
the direct utilisation of phytoplankton or its decomposition
products by consumer organisms is likely to he of dominant
importance even in coastal lagoons which support significant production by seagrasscs and macroalgae.
The inereasc in bacterial biomass and simultaneous utilisa·
tion of carbon in mcdia containing phytoplanklon debris at
an initial concentration of 12-15 mg C. I- \ is plolted as a
function of time o f incubation at 10 oC in Figure 1 (from
Newell et al., 1981). Il can he secn that the incrcase in the
carbon equ ivalcnl of baeterial biomass is accompanîcd by a
utilisation of the carbon in the phytoplankton debris up to
approximatcly day 3. Aftcr this, nagellates and ciliatcs,
many of which are known to activcly grazc on bacteria
(Fcnchel , 1969 ; Sieburth , 1979), appeared in the incubation
media .
.
a<:."·'If"'"
•"
\
\
O'~ !
." " ...
'"
O' YI
. ...
, :';.
\., •.<.....
.....,.
•
i
0'0 <>
•
.
~.--,---:--,
0'"
."
!.é...-,,_._,.
•
Figurc
The ;/luease in Ihe carbon equil'alem of bac/niai biomass and /M
s;mullaneou5 II lilisalion of caroon in seawO/n containing ph)'Io,
planklon debris from a variery of sources al 011 in;Iial conctnlraliolr
of JZ.J5 mg.! 1 and incubalid al urc Jor up 10 5 da )'s (from New~1I
CI al. , /98/).
or pb}1oplankton
Production by the phyloplankton may , as shown on p.349,
approach that of Spartilla and macrophytes, but even where
turbidity and nutrÎents arc limiting, the area of water
compared with that of marsh grasses eommonly fesults in
production by phytoplankton bcing o f major significance in
estuarine and lagoon systems. Table 2 shows the relative
values for production in the enc10scd estuarine system
studied by Penhalc and Smith ( 1977) at Beaufort , North
Carolina. It can bc seen that the area of water in which
phytoplankton production occurs was as much as 532 km 2
compared with only 93 km ~ for the 'ZoS!era marina zone and
31 kmz fOf the Sparrina allemi/lora community. Even in
Partly for this reason , the utilisation of carbon from the
dctrital sou rce rails cxponcntially even though only a smaU
proponion of the carbon had becn uscd by day 3. The
dcdine may also bc associaled with the rapid initial utilisa·
tion of the labile componcnts of the dissolved fraction of the
detrital source, Icaving more rcfractory componenlS to bc
ut ilised by attached bactcria (sec Newcll et al. , 1981).
350
DETRITUS UTILIZATION IN LAGOONS AND COASTAL WATERS
.- 0 _
l
i"
f'
~
0'
~""-
1
1
~
1'"
..
_
:!
OO
$KELE100E"'-" •
{
1
'
,
,
•
CARBON USED (mg!""')
~~
T 020
l
r
".
ta.
•
..;
r"
a
, •
,
• CAAIIOH
USED (mgl""!
•
from which the mean value fo r the slop;: (b) is
0.09872 ± 0.0267 S.D. The bacterial carbon conversion efficie ncy established in the initial phases of decomposition of
phYlOplankton dcbris is thus 9. 87 ± 2.7 %.
This value reprcsents the ccII yield expressed in carbon for
the fre e-living bacteria utilising the more labile components
of the detrital sou rce. Unfortunatc ly, bccause grazing
Protoroa appcar in the later phases o f incubat ion, it has
been possible to calculale the ceU yields for auached
bacteria bascd on the more refractory partieulatc components of detritus in only a few instances (sec NeweU , Lucas,
1981 ; Stuart el al., 198 1).
T he bacteria themsclvcs arc in equilibriu m with the flagellates and ciliates whieh reach a combined biomass of 10-12 %
of thal of the bacteria. From Figure 3, for example, it ean be
secn that the equation for the regression for flagellate
biomass as a funetion of bacterial biomass has a slopc of
0.0924 which implies that only 9.24 % of the bacterial
biomass is incorporated into the next tropbie level. The
energy flow thro ugh the init ial stages o f the decomposer
food chain thus represents a classical ., energy cascade "
with as much as 90 % cnergy dissipation at each trophic
level. The evidencc thus suggests that natural populations of
microbial decomposcr organisms convcrt plant debris wilh
an efficiency which is similar 10 Ihat in other food chains. Il
must thercfore be inferred that the amount of e nergy
available 10 consumer organisms by direct utilisation of
dccomposcr miero-organisms is very smalt compared with
Ihat potentially available from direct ut ilisation of the
phytoplankton itself. Very similar inferences can be made
from our studies on the encrgetics o f decomposition of
maerophyle and saltmarsh grass debris.
' ) 0'0
1'"
.
•
1
,
,
,
•I:~:
.
1
• c~ do(mgll)
CAR8CIf'I useo (~î
Figure 2
1'~ tnu:/erwl carbon incorpora/km plo/led as a [unc/ion of carbon
u.red [rom incuba/ion ~dw cOn/aining phy/opùmk/on debris [rom a
"ark/y of sources (from Netr."tli ct al.. 1981).
ln the initial phases it is possible to plot the bactcrial carbon
fixation d irectly as a functÎOn of detrital carbon used as is
shown in Figure 2. The cquations for the rcgrcssions for
these and other expcrirnents are surnmarized in Table 3
DecomposJllon or macro phytes
A very similar succession of bacte ria fo1Jowed by micronageUates and ciliates accurs in incubation media containing
debris from the kelps LaminarÎ(l pallidll and Eck/onia
maxima. In Ihis ease, however, we have ~tudied the
decomposition of dissolved and partîculate fractions separately and have found that the partieulate component has both
a slower dceomposition rate and a lower conversion efficiency 10 bacteria Ihan the dissolved components. The laller
comprises a rapidly-utilisabJe primary photosynthate, Dmannitol (NeweUet al. , 1980 ; Lucas et al., 1981) as weil as
hexose sugars, and complex polysaccharides of large molecular weighl such as alginates and laminarins. The relative
rates of decomposition o f the particulate and principal
carbohydrates of the dissolved fraction arc shown in
Table 3
Eql.arwtl.f of II~ regressionJ for bacrerwl carbon syn/l~si1td ( Y,
mg./-I) and carbon urilistd ( X. mg./- I ) /rom phy/OplankfQn debris
incuba/ed at JO oC in .reawater.
Y = a+bX.
,
50'=
Equation of
b
r~
rtgression
N
P
7
7
7
7
5
0.001
0.001
0.01
0.001
0.005
>
Thalasswsira
Scrippsitfla
Skeletonema
Chae/Oceros
fsochrysis
-
0.0609
0.0174
0.0410
0.0250
0.0065
0. 1348
0. 1199
0.0825
0.0804
0.0760
0.9598
0.9402
0.8687
0.9471
0.9589
,-
; .,
CHAETOCEROS
l,
>-
' \"
/
1
/~~
;.i: /' . r:
Figure 3
~
The bwmass of bacteria and he/erorrophie. flagella ItS plotltd as a func /wn ofincubation ti~ ar J(l'C in
~dia conraining phytop/ankton debris [rom a
varitty of sources. Nolt tOOr the gruling flagellalts
apptar [rom day 4 onwards and are associared wirh
a dec/int in bacrerwl biomass. The re/ario fUhip
be/Ween n!(IXimunI jülgellare biomass and marimum
bacrerial biomass shows lhur r~ prorOIoa achieve a
bwmass of 9.24 % of /OOr of the bacteria (from
Netr."ell ct al.. 1981).
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351
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" C' .~I ~ l DRY ....... . . ! ~.I·.,
R. C. NEWElL
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lA MINAAIA
o,a,u~~
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,. 0 M ,
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FL~GELl~TfS
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,.
INCUBATION
•
Figure 4
'0
I N CUB A TIO N
The rare of milislllWl1 of Ihe primory pholosynrJwle D-monnirof,
sugar.f and famillari11$. and lM particulme compotrents of kelp debris
incuballd in seawa/er al lU'C. Vall/es Iwve bun expressed as
. glJJ(ose equil'alel1ls '. TIœ 50 % ufilisDtiol1 /ÏrTU!S of D·ma11fjilol al/d
sugars + lamirwri11$ are indicaled by arrows (from Newel/, LIICOS,
/981).
TI M E
!DAYS)
Figure 6
The biomass ofbacltria and 8razing Pr%zoa (microjWgelfules and
cilioles) as a fimclwn of film' in sea ....arer inc/lbared al J{re wilh
7.2 g.I-1 drkd mucilage from Ihe kelp Laminaria pallida (/rom
U nley. Ne ....ell, 1981).
p. 349), over 99 % wi ll bc mi neralized by the baele ria a nd
approximately 10 % of Ihe baete rial pré'y density (Linlcy et
al. , 1981). Figure 6 shows that following the addition o f
7.2 g. I-1 d ried mucilage from Laminaria paUida, Ihe baclerial biomass increased to almost 100 mg.I- 1 and was followed by an increasc in flagellates a nd dliates whose combined biomass reached app roximately 10 mg.I- 1 ( Linley el al.,
1981). The bacterial prey density mcanwhile declined shar·
ply a nd was fo tlowed by a decl ine in the protozoa.
There is thus very liule differe nce in the hete rotrophic fa te
of macrophyte debris and thal from phytoplankton , cither
in the ste p from plant debris to bacteria or bacteria 10
protozoa , which in caeh case is approximately 10 %. The
ovcrall turnover lime fo r both types of de bris is also likely to
bc similar. In phytoplanklon , for e]Cample, the dissolved
o rganic compone nt comprises a mean of 34 % of the total
cll rbon in the dehris ami hlls a .'i0 % utilisation time of o nly
37 h whcreas the partieulate eomponcnt comprises 66 % and
has a 50 % utilisat ion time of as much as 277 h. In kclps, the
dissolved compement comprises bctween 23 and 35 % of the
carbon fixed (Jo hnston el al., 1977; Hatchcr el al., 1977;
Ncwcll et al., 1980) and has a turnover time o f approximatcly 48 h whereas the more complex ca rbohydrates and
structural components have a turnover time of approxirnately 340 h (Newell , Lucas, 1981).
Jt is thus possible to say tha t of the 1.5 % of incident energy
which is fixed by pnmary production o f the algae, and which
rep resents approximately 0.35·0.58 x 1~ kJ.m- 2.yr. - t (sec
Figure 4. Il Is appare nt tha t D-mannitol has a 50 % utilisation IÎme of o nl y 48 h at 10 oC whe reas the time for sugars is
144 h and that for the paniculate frac tion is more than
340 h.
Despite the d iffercn t rates of utilisat ion of the components
of o rganic debris, and the fa ct that conve rsion of the
dissolved components is mo re e fficient than that of the morc
rcfractory particulatc compone nts (St uart el al., 1981 a),
estima tion of t he utilisation of organk carbon a nd synchronous incrcase in bactcria l biomass shows that an overall
carbon conve rs ion cfficiency of approximately 10 % into
bacteria commonl y occurs in media containing ke lp debris
incubatcd with scawate r fro m the kclp bcd. Figure 5 shows,
for example, that sorne of the dissolvcd frac tion i5 released
frcely into the water column where it is convened wit h an
cfficicncy of 1.'i % whilst a sim ilar proportion is associated
with fragmentatio n products and is convened with a highe r
efficie ncy of 33 %. The pankulate matle r, whkh comprises
as much as 70 % of the plant dcbris is, howevcr, conve n cd
with an cffieieney of only 5.5 % ( Lucas el al., 1981 ; Ncwell,
Lucas, 1981). Out of an estimated annual carbon production
of 1172 g. carbon.m - 2.yr. -l , by the k,elp, bacterial carbon
production is thus 129.5 g carbon.m- 2.yr. - 1 (equivalcnt to
259 g dry mass; sec Luria. 1960) or 11.05 % of the primary
production by the kclp.
Similarly, the biomass of flage l1ates and eiliatcs is always
BACTERW,. CARBON
( ~C.m·· <lI~et>y·· 1
.
... :·-.,. m-. ran
;' r"§~B
protozoa and returned to sup pon funher primary production within 12 days at JO oC, and probably cven faster al
highcr tempcratures such as occur in shallow watcr cstuaries
and lagoons during the sum mcr momhs. Approximalely
10 % of the primary product io n br the mac rophytes, reprcse nti ng 0.035-0.058 x I ~ kJ.m- .yr. - t could bc initially
incorporatcd into baeteria , but of Ihis material 90 % would
bc dissipated wilhin a fcw day by the grazing microflagellales and ciliates which a rc associated wit h the bacteria. lt is
thus likcty (hat, as a potential food resource for larger
consume r organisms, bacterial production from both phytoplankton and macrophyte debris could provide considerably
less than JO % of Ihe primary production in the habitat.
~
.... ..
El.,., - ....
'"
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..........
.,. .\0'
...
_.
~ §]
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.
" " .",
. ... .. . .
.,............. Q P Occ~.U ~ .·1
Figure 5
Decomposition of sallmarsh plant d"br is
Schrmalic diagram shov";ng lite dissofl'ed and parliculale curbon
released as a proportion of an/wal carbon prodllclion by Ihe kelp
Laminaria pallida, The com'ersio" effidenCf of frte dissoh·rd
organie malla. dissoll'ed organic nUliler associated wilh Ihe par/icl/'
late ·fracliol', and the portiCI/laie componem is shawn. logelher wilh
lite baC/erial carbon production based 011 primary produClioti by lhe
ke/p. nIe bacleria are Ihemsell"f!S ;,/Corporoted wilh un efficiency of
approximalel)' 10 % by Ihe Pro/Ozoa (based on Nrwell, LI/cas,
We have recently established the carbon conversion effieîcney of the microheterotrophic commu nity whic h is associated with the deeomposition o f Ihe saltmarsh grasses
Spartina alœrniflora and hmcus roemerianus (Ncwell et al.,
in press). ln this case Ihe malerial comprises only 1.5 % of
total carbon fixed as dissolved substances ( Penhalc, Smith,
1977), most of the detrital carbon ente ring the estuarine and
coastal lagoon ecosyslems as fine paniculate mauer. Odum
1981).
352
DETRITUS UTtLtZATtON IN LAGOONS AND COASTAL WATERS
consumption by herbivores, the commu nities of lagoons and
cstuarine ecosystems may bc partly dependent o n a food
rcsourcc which has entered the waler column as debris. 1
al50 suggested that if the consumers were utilisi ng first or
second Slage deco mposer organisms as a food re5Ourcc ,
production by the plants must bc sufficicntl y high to
compensate for the energetic loss through the deco mposer
food chain. or that secondary production in coastal communilies must bc at least an o rde r of magnitude lower than in
othe r ecosystems. Alternativcly, the deco mposer organisms
might have a radically higher conversion efficieney than the
lO % which applies to othe r food chains, and thus compensate for the encrgetie !osses associated with the interpola·
tion of an additional step in the food chain.
Although primary production by saltmarshes is known to be
high (sec p. 34~ and Tea l, 1962) our informatio n for
phytoplankto n production in upwclling areas and for the
mixed communily of phytoplanklon, macrophytes and
unde rstorey algae in kelp bcds suggests Ihat the sum of
pri mary production in ail these areas is like ly to bc
approximale ly 1.5 % of the incident e nergy. This varies
somewhat wit h latitude but prima ry production is likely to
bc bctween 0.35 and 0.58 x lOS kJ .m- 2.yr- 1 in both saltmarsh·estuari nc communilies. coastal lagoons domi nated
by mixed macrophyte and phytoplankto n communities and
in upwelling areas. In other words. despite the high primary
productivity of saltma rshes, there is little reason to suppose
that th is greatly exceeds that attai nable in other warm
nutrient-rich ecosystcms and it is certainly not suffieicnt ly
high to offset the likely energet ic losses ineurred if the
consumer organisms were to utilise decomposer organisms
as a food resource.
Since primary production is nOI markedly highcr than in
other ccosySle ms, the second alternative is that production
by the detritus eating consumer organisms is at least an
order of magnitude lower than in othcr ecosystems bccause
o f the encrgy losses incurred through t.he deeo mposer food
chain. The evidence for al least the detritus- feeding consuIllet" communily associaled wilh macrophylc bed5 i.5 thal il i.5
10.42 % of primary production and that production by the
larger ca rnivo res is o nly 1.07 % of the primary production
and 10.26 % o f prima ry consumers. Prod uction would he
ant icipated to bc at least an order of magnitude lower tha n
this if the decomposcr organisms themselvcs reprcsented a
prima ry food resource for the consume r community of
nears hore waters.
Finally, it could bc 5upposed that if the dccompose r
o rganisms had a very high conversion efficiency of detrital
mnterial into microheterotrophic biomass, and if the consu·
mer orga nisms could ab50rb these organisms cffecti vely,
this might offset the e nergetic losses associated wilh the
interpolation of decomposcr organisms into the food chain
to consumers. The evidence for all major sources of plant
debris, including phytoplankton. maerophytes and saltmarsh grasses suggests, however. that energy con ... ersion
through the decomposer food chain i5 ve ry similar 10 that in
othe r trophic sysle ms with Il 90 % ene rgy loss at eaeh
succcssive step. O f the 0.35·0. 58 x lOS kJ .m - 2.yr- 1 incorpo·
ratcd into plant production, thercfore, ovcr 90 % wo uld bc
lost in the step to bacteria and a furthe r 9 % in the step to
protozoa.
.!! "
i
"
•
•
"
"
"
"
"
Figure 7
The sutttssum of boettrio, fW~/Ùltts and ci/iotts il1 Hawottr
conraining JJ.J mg.1 1 drkd SpartÎna Itaf pot'l'{Jtr itu:ubattd IIf JU'C
for up 10 28 days (from Nt...,tlf c t al.. in prtss).
and De La Cru z ( 1967) found Ihat as much as 42 % o f
Sparrina debris and 65 % o f Junew liHer enclosed in bags on
a saltmarsh re mained ahe r 300 days. This yields a daily loss
o f only 0. 19 % in Spartina and 0. 12 % in June/l! in long-term
expe rime nts, so that evidentl y the mate rial is likely to
remain as dctritus for a lo nge r time tha n debris from either
phytoplankton 'ur macrophytes.
Ini tial colonizatio n of powdered debris fo llows the characteriSlie succession of baeteria, followed by flagcllates and
ciliates tha t we have noted for otller sources of debris
(Fig. 7) und is accornpanicd by a utilisution of orgnnic
carbon. Figure 8 shows that the carbon loss associated with
Ihe inerease in bacteria in media enriched with Spartina
deb ris results in an overall carbon conversion efficiency of
approximately 13 % by the baetcria . The comparable figu re
for hmeus debris is 6. 1 % although in this case a higher
conversion efficiency is obta ined du ring the log phase of
bacterial growth a ft er the initial establishment of baeteria
on the debris (Newe ll el al. , in press). The ave rage value for
bacle rial earbon conversion bascd on the twO spccies of
saltmarsh grass is thus 9.5 % 50 Ihat it sce rns that as in the
C,jM; of algae debris. baetcrial production based on saltmarsch piani debris is likcJy to bc approximale ly lO % of the
primary productio n b)' the saltmarsh. Again . sioce the
maximal biomass 0 prOlozoa in the mcdia was only 6-8.5 %
o Ihe bilcterial biomass. the ovcrall incorporation into
prolozoa al the ~ cond trophic Ic ...e l is Icss Iha n 1 % o f thc
primar)' produclion.
DISCUSS ION
At the outset
pointcd out that since production by
macrophytcs and saltmars h plants greatly exceeds direct
"r-.--~-,------,-,
SPARI ....
Figure 8
The carbol/ los$ ossociO/ed ....ilh Ihe iI/utaH of bocttria in
mtdio roll/Oil/;'lg JJ.J mg./- I dmd Spartina k of po ....dtr
incuboltd al JU'C. TIw bocltriol carbon incor(JOro(ion JX'
III/il corboll IIStd is olso .showl/ olld indkolt:1 011 QI,trolllU'l
corbolt comusiolt efficilmcy of 1].2 'li, allllOl/gh 0 highu
COllVtrsiOl1 is ochitl'td dl/rillg ,Ile log phost of boe/triol
gfOwlh ufitr IIIt Îlliliale.stab(ishmtnl pluut (from Newefl ct
al.• in prtSI).
\
_.\ . -
.-
• • C ...... L
1
,
•
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~
•
353
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•
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.....
.. . ",. "" •
/'
R. C. NEWEll
The trophic stru ct ure of nea uho re and e stuarine : lagoon
ecos)'stc ms Ihus appca rs 10 bc bascd o n a fairly prcdictable
e ne rget ie basis despite the diffe re nt plant communities
whie h contribute to primary production. Becausc o f the
high ene rge tic losses which occu r through the microhe tcro-tro phic deeomposcr o rganisms. these are very unlik e ly to
re presenl a significanl tro phie rcsource for the consumer
eommunit y whosc productio n is co mparable with that of
prima!)' consume rs in a he rbi vo re communit)'. This suggests
that the consume rs ut ilise pIa ni debris directl)' as a food
resource befo re it has bee n m ine ra lised Ihro ugh Ihe decom ·
poser food chain . and that lo ng-lasting partic ulate de bris as
well as living ph)'to pta nkt o n cells may form the domi na ni
food resou rce fo r the consu me r community of estuaries,
lagoo ns and nearsho re wate rs.
This concl usio n suppo rts obse rvatio ns by Ca mme n ~f al.
(1978; also Camme n , 1980) on the deposit-fe ed ing pol)'c haete N~reis SIlCCÎ"~Q and b)' Stuart e t al. (1981 b) o n the
bivalve A fdaco mya aler which suggest that th e carbon
requirc mc nls of Ihesc invc rt e brates could no t be met fro m
t he bacteria avai lab le in t he food a nd that both o f
o rganis ms may de ri ve as much as 50 % o f theÎ r ca rbon
req uire me nls b)' di rect ut ilisatio n o f d etrital malc ria l. The
mic roh cterotroph ic decomposc r o rga nisms arc , however . o f
do minant importa nce in ree)'cling unex ploitcd plant d ebris
including fa cca l mate ri al (Stu art el al. , 198 1 b ). and thus
susta ining the p rimary prod uctio n near to th e maximum
valu e of 1. 5 % o f incide nt ene rg)'.
Atknowledgements
This ..... ork was carried out du ri ng te nure of a Se nior
Research Fc llowship o f the Ro)'al Socie ty of Lo ndon. 1 a m
grat e ful fo r p rov ision o f financia l su pport fro m Ihis sourcc
a nd fo r the ex tensive colla boralio n with m)' collea gues,
cspceiall)' Pc. J . G. Field , Dr. M. J. Lucas, Ms E. A. S .
Linle y a nd Ms. V. Stua rt in the o ri ginal rescarch which i~
s)' nlhesized in Ihis review.
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