vol. 154, no. 4
the american naturalist
october 1999
Patterns in the Fate of Production in Plant Communities
Just Cebrian*
Boston University Marine Program, Marine Biological Laboratory,
Woods Hole, Massachusetts 02543
Submitted June 12, 1998; Accepted May 31, 1999
abstract: I examine, through an extensive compilation of published reports, the nature and variability of carbon flow (i.e., primary
production, herbivory, detrital production, decomposition, export,
and biomass and detrital storage) in a range of aquatic and terrestrial
plant communities. Communities composed of more nutritional
plants (i.e., higher nutrient concentrations) lose higher percentages
of production to herbivores, channel lower percentages as detritus,
experience faster decomposition rates, and, as a result, store smaller
carbon pools. These results suggest plant palatability as a main limiting factor of consumer metabolical and feeding rates across communities. Hence, across communities, plant nutritional quality may
be regarded as a descriptor of the importance of herbivore control
on plant biomass (“top-down” control), the rapidity of nutrient and
energy recycling, and the magnitude of carbon storage. These results
contribute to an understanding of how much and why the trophic
routes of carbon flow, and their ecological implications, vary across
plant communities. They also offer a basis to predict the effects of
widespread enhancement of plant nutritional quality due to largescale anthropogenic eutrophication on carbon balances in ecosystems.
Keywords: plant community, primary production, herbivory, decomposition, carbon storage.
The amount of CO2 fixed by primary production in plant
communities can follow diverse trophic routes (fig. 1).
Herbivores remove a fraction of production, with the rest
being accumulated as plant biomass and entering the degradable detrital compartment over the plant life span.
This compartment may also receive plant detritus imported from other communities (Nixon 1980; Twilley et
al. 1986). A fraction of plant detritus is exported off the
community by means of physical agents, such as rivers in
* Address for correspondence beginning January 1, 2000: Dauphin Island Sea
Lab, 101 Bienville Boulevard, P.O. Box 369-370, Dauphin Island, Alabama
36528; e-mail: [email protected].
Am. Nat. 1999. Vol. 154, pp. 449–468. q 1999 by The University of Chicago.
0003-0147/1999/15404-0006$03.00. All rights reserved.
terrestrial communities or currents and waves in aquatic
ones (Mann 1988; Pomeroy and Wiebe 1993). The rest of
detritus undergoes decomposition within the community,
with a small fraction of recalcitrant detritus escaping from
further degradation and entering the refractory compartment (Schlesinger 1997).
Temporal changes in the biomass and degradable detrital mass of plant communities are related to the trophic
routes of production by the following mass-balance equations:
(DB/t) = NPP 2 C 2 DP,
(1)
(DDB/t) = DP 1 I 2 D 2 E 2 RA,
(2)
where DB/t and DDB/t correspond to the increments in
plant biomass and degradable detrital mass per unit time
(g C m22 d21), respectively, and NPP, C, DP, I, D, E, and
RA stand for net primary production, consumption by
herbivores, detrital production, import, decomposition,
export, and refractory accumulation, respectively (all variables in g C m22 d21). Under steady state assumptions, B
and DB remain constant with time, and, thus, the sum of
primary production and import equals the sum of herbivory, decomposition, export, and refractory accumulation.
The assessment of the trophic routes of production in
a plant community is important because these routes are
indicative of the ecological role of the community. The
extent of the fraction of production removed by herbivores
reflects the importance of herbivores as controls of plant
biomass (Petrusewicz and Grodzinski 1975; Cebrian and
Duarte 1994). On the other hand, the absolute flux of
production consumed by herbivores (in g plant C m22
d21) set limits to the abundance of herbivores supported
by a plant community (McNaughton et al. 1989; Cyr and
Pace 1993). The amount of detritus exported off a plant
community points to the magnitude of allochthonous secondary production supported by the community because
most exported detritus are consumed within the receiving
communities (Mann 1988). In contrast, accumulation of
refractory detritus within a community represents a net
450 The American Naturalist
Figure 1: Fate of primary production in plant communities
carbon sink since refractory carbon is preserved over longterm scales (Schlesinger 1997).
A few studies have analyzed the extent and controls of
the variability in specific trophic routes of production
across diverse plant communities. Comparisons among a
broad range of aquatic and terrestrial communities show
that more productive communities support higher levels
of absolute consumption by herbivores, and consequently,
they maintain larger herbivore abundances (McNaughton
et al. 1989; Cyr and Pace 1993). Absolute consumption
increases linearly with primary production across communities (McNaughton et al. 1989; Cyr and Pace 1993).
This tendency implies that the percentage of production
removed by herbivores, which is indicative of their potential role as controls of plant biomass, is independent
of the magnitude of primary production when aquatic and
terrestrial communities are compared (Cebrian and
Duarte 1994). The fraction of production removed is associated with the biomass turnover rate (i.e., fraction of
biomass renewed per day [d21]) of the plant community,
probably because faster turning-over communities have a
greater palatability for herbivores (Cebrian and Duarte
1994; Duarte and Cebrian 1996). Plant detritus from communities with faster biomass turnover rates also seem to
undergo faster decomposition rates probably because of
their expected greater palatability for decomposers (En-
riquez et al. 1993; Cebrian and Duarte 1995). Plant communities having higher fractions of production removed
by herbivores and faster decomposition rates store smaller
biomass and detrital pools if differences in the intensity
of heterotrophic consumption override differences in the
magnitude of production (Cebrian et al. 1998). Marine
plant communities typically exposed to substantial advection by waves and currents tend to export large amounts
of detritus (Duarte and Cebrian 1996).
Nevertheless, no attempt to compare all the trophic
routes of production combined into thorough carbon balances across a broad range of aquatic and terrestrial plant
communities has been made. Our knowledge about how
primary production, consumption by herbivores, detrital
production, decomposition, refractory accumulation, export, and import dovetail carbon balances across a continuum of diverse aquatic and terrestrial plant communities is meager. Likewise, although controls of the
variability in some particular routes across communities
have been identified, we lack knowledge of mechanisms
responsible for differences in the entire carbon balance
among communities.
It has been suggested that plant communities with faster
biomass turnover rates have higher fractions of production
lost to herbivores and faster decomposition rates because
they should have higher plant nutrient concentrations and,
Fate of Production in Plant Communities 451
thus, enhance the metabolism and feeding rates of heterotrophs (Cebrian and Duarte 1994, 1995; Duarte and
Cebrian 1996). Nielsen et al. (1996) compare turnover
rates and nutrient concentrations for a broad range of
types of autotrophs (from microalgae to terrestrial macrophytes) under natural and experimental conditions and
conclude a strong association between higher nutrient concentrations and faster turnover rates. Therefore, communities formed by plants with faster turnover rates
should also have plants with higher nutrient concentrations. Yet, the association between plant nutrient concentrations and turnover rates across aquatic and terrestrial
communities, and its effects on the levels of consumption
by heterotrophs, remains to be tested. Moreover, greater
levels of consumption by heterotrophs in communities
with faster turnover rates could entail lower levels of accumulation of biomass and detrital mass within these communities, provided differences in consumption are greater
than differences in production. Demonstrating these hypotheses would render the association between plant
trophic quality and turnover rate as a main control of the
carbon balance in plant communities: because plant communities with faster turnover rates are more palatable to
heterotrophs, they would experience higher intensities of
consumption (i.e., larger fractions of production removed
and faster decomposition rates) and, as a result, they would
accumulate less biomass and detrital mass. That would be
so regardless of other numerous factors that could influence differences in consumption by herbivores (e.g., characteristics of the specific herbivore populations in the different plant communities compared) and in decomposition and carbon storage (e.g., temperature, humidity, sediment redox conditions) across the plant communities compared.
In this article, I examine, through an extensive compilation of published reports, differences in the trophic
routes of carbon flow (eqq. [1] and [2]) across a wide
range of aquatic and terrestrial types of plant communities
and analyze how these differences affect their ecological
role. Then I test whether communities composed of plants
with higher nutrient concentrations also have faster biomass turnover rates. I further test whether, as a result of
the association between higher plant palatability and faster
turnover rates, communities with faster turnover rates are
subject to higher levels of consumption by herbivores and
faster decomposition rates and, as a consequence, accumulate less plant biomass and detrital mass. I end by discussing the contribution of the patterns found to an understanding of how much and why carbon balances differ
across plant communities.
Methods
From over 200 published reports, I compiled an extensive
data set of plant nutrient concentration, biomass, detrital
mass, and magnitude and trophic fate (consumption by
herbivores, detrital production, export, decomposition,
and refractory accumulation) of production for the following types of plant communities: marine and freshwater
phytoplanktonic communities, marine and freshwater
benthic microalgal beds, marine macroalgal beds, freshwater macrophyte meadows, seagrass meadows, brackish
and marine marshes, grasslands, mangroves, and shrublands and forests (see data set). The data set is available
from the author upon request at http://www.mbl.edu/usr/
just/. Reports covering all the trophic routes of production
for a given community were obviously uncommon, and,
hence, the data set compiled combines reports covering
different numbers of the variables considered. Moreover,
the variables compiled only referred to the aboveground
compartment in most of the reports for aquatic or terrestrial macrophyte communities, with only a few reports
accounting for both the below- and aboveground compartments (see data set). Three initial criteria were applied
when selecting papers: first, only studies of plant communities referring to natural conditions were considered
(i.e., studies with manipulated conditions and artificial
communities were discarded); second, studies focused on
a single plant species were accepted only if that species
accounted for most biomass and production within the
community; and third, studies were considered if they covered at least 1 yr or the full growing season for seasonal
producers (which usually spans from late winter to early
fall).
Plant nutrient concentrations were reported as nitrogen
(N) and phosphorus (P) concentrations expressed as the
percentage of plant tissue dry weight (%DW). Nitrogen
and phosphorus are the two nutrients most often reported
in the literature. Plant biomass corresponds to the stock
of alive plant material (g C m22). The values compiled of
plant detrital mass (g C m22) correspond to particulate
detritus above the upper sediment layers for aquatic and
terrestrial macrophyte communities, and to dead cells for
microalgal communities. Hence, the detrital pool of plantdissolved carbon is disregarded because it was reported in
very few articles. The values of detrital mass compiled for
communities of macrophytes include both degradable and
refractory detritus, although the total pools of degradable
and refractory detritus were underestimated since only the
upper sediment or soil layers were accounted for. When
temporal changes in plant nutrient concentrations, biomass, and detrital mass through the study period were
reported, yearly average values were calculated. Net primary production is defined as the net amount of atmos-
452 The American Naturalist
pheric CO2 fixed by photosynthesis. It was expressed in g
C m22 d21 by dividing the cumulative value for the study
period by the number of days covered by the study. Plant
turnover rate corresponds to the fraction of biomass renewed per day (d21), and it was estimated as the ratio of
primary production to plant biomass when direct values
were not provided in the report.
Plant consumption by herbivores is defined as the ingestion of plant biomass by herbivores (g C m22 d21).
Detrital production (g C m22 d21) corresponds to the sum
of plant mortality by senescence, metabolical exudation of
organic carbon, and plant material removed but nonconsumed by herbivores. Metabolical carbon exudation was
not measured in many of the reports compiled for aquatic
and terrestrial macrophytes, but the magnitude of plant
carbon exudation in these communities is normally small
in comparison with that of mortality by senescence (Grier
and Logan 1977; Wetzel 1984). Hence, detrital production
in communities of macrophytes should not be underestimated importantly. Plant mortality by senescence is estimated as “litterfall,” that is, senescent material shed from
the plant, for communities of macrophytes, and as cell
sedimentation and lysis rates for communities of microalgae. Direct measurements of lysis rates were provided in
few reports, with most rates thus being estimated as the
difference between primary production and the sum of
any biomass increment, consumption by herbivores, sedimentation, metabolical exudation, and horizontal advection. Values of plant consumption and detrital production
were expressed on a daily basis by dividing the cumulative
values over the study period by the number of days
covered.
Plant decomposition (g C m22 d21) is the consumption
of plant detritus by decomposers. Direct values of plant
decomposition were not provided in most of the phytoplanktonic and benthic microalgal communities compiled.
I estimated it from respiration measurements of the total
micropelagic or microbenthic communities enclosed in incubation bottles or benthic chambers, respectively, as explained by Duarte and Cebrian (1996): plant decomposition within the bottles or chambers was estimated by
subtracting the sum of phytoplankton or microphytobenthos respiration and grazing by microherbivores (i.e., those
contained in the bottle or chamber) from the total community respiration value. Phytoplankton and microphytobenthos respiration was estimated from values of gross
primary production for the same communities by assuming that respiration represents 35.4% 5 6.9% and
26.4% 5 6.4% of gross phytoplankton and microphytobenthos production, respectively. Grazing by microherbivores was supposed to be 50% 5 30% of the total grazing value (micro- and macroherbivores) obtained for the
same community. These conversion values (mean 5 SD)
were obtained by Duarte and Cebrian (1996) through a
compilation of published reports. Finally, decomposition
of sedimenting dead phytoplanktonic cells was assumed
to be 17% of the net primary production measured in the
community (Martin et al. 1987) and added to the decomposition values obtained from the bottles. The value of
17% corresponds to a mean for a vast oceanic area, and
the percentage of phytoplanktonic production decomposed during sedimentation can vary considerably among
regions (Muller and Suess 1979; Suess 1980). Nevertheless,
the use of mean values of autotrophic respiration, grazing
by microherbivores and decomposition of sedimenting
phytoplanktonic detritus should not entail a consistent
bias on the derivation of decomposition for phytoplanktonic and microphytobenthic communities. This is shown
by the comparison of the estimated carbon budgets among
the communities considered (see below). Moreover, the
error in the estimates of phytoplanktonic and microphytobenthic decomposition involved by the mean values used
is unimportant in relation to the broad range of decomposition encompassed by the aquatic and terrestrial communities compared (see results on decomposition).
When direct values of decomposition were not provided
in communities of aquatic and terrestrial macrophytes,
they were derived as
D = (DP 2 E) # (1 2 e2kDt ),
(3)
where D, DP, and E denote cumulative decomposition,
detrital production, and detrital export over the duration
of the study (i.e., g C m22 [study duration]21), Dt corresponds to the duration of the study (d), and k is the
decomposition rate (d21). Decomposition was expressed
into a daily basis (g C m22 d21) by dividing the cumulative
values by the duration of the study. Equation (3) assumes
that the pool of degradable detrital mass in the community
(fig. 1) does not change over the study period, and, hence,
it was only applied in climax communities with steady
pools of degradable detrital mass. When decomposition
rates (k, d21) were not derived directly, they were estimated
as the ratio of detrital production (g C m22 d21) to degradable detrital mass (g C m22) since the latter variable
remained unchanged over the study period (Olson 1963).
A few decomposition values in some types of communities
of macrophytes were derived by using mean values of k
for the specific types provided by Enriquez et al. (1993).
The estimates of decomposition only cover the duration
of the studies compiled (i.e., from one to a few years) and,
hence, disregard long-term decomposition of refractory
detritus.
Export corresponds to the transportation of plant detritus off the community through rivers in terrestrial communities and waves, tides, and currents in aquatic com-
Fate of Production in Plant Communities 453
munities. Export off phytoplankton communities in
enclosed lakes and open ocean was assumed to be 0 since
phytoplankton detrital carbon, albeit horizontally advected, never traversed the community boundaries. Hence,
export values for phytoplanktonic communities refer only
to coastal communities. None of the reports compiled
accounted for export of dissolved detrital material, and,
hence, these estimates correspond only to export of particulate detrital material. Export values were expressed on
a daily basis (g C m22 d21) by dividing the cumulative
values over the study period by the number of days
covered.
Refractory accumulation corresponds to the amount of
nonexported detrital production that is not decomposed
during the duration of the study (i.e., from one to some
few years). It thus represents the amount of refractory
detritus accumulated during the duration of the study but
disregards long-term accumulation once diagenetic losses
have occurred (i.e., burial). Whenever direct values were
not reported, refractory accumulation was calculated as
the difference between net primary production and the
sum of consumption by herbivores, export, and decomposition over the study period (Schlesinger 1997). Refractory accumulation was then expressed on a daily basis
(g C m22 d21) by dividing the cumulative value by the
number of days in the study. This procedure was valid
only for climax communities with steady pools of plant
biomass and degradable detrital mass.
All the different assumptions, methods, and mean values
employed for the estimation of the trophic routes of production bring out the questions whether these estimates
are representative of the real carbon balances in the communities considered and, thus, whether they are comparable among different communities. To address these questions, I calculated the mean percentage of production
represented by consumption by herbivores, decomposition, export, and refractory accumulation for each type of
community from all the values in the data set. Biomass
and detrital mass were steady and import negligible during
the study interval in practically all the communities compiled. Therefore, if the mean percentages of production
consumed, decomposed, exported, or accumulated sum
up to about 100% for each community type, the values
in the data set should be in general representative of real
carbon balances in the communities considered. The sums
obtained were (mean 5 SE): for phytoplankton,
112.2% 5 12.6%; for benthic microalgal beds, 102.4% 5
20.1%; for macroalgal beds, 98.5% 5 27.7%; for freshwater
macrophyte meadows, 123.7% 5 23.8%; for seagrass
meadows, 112.5% 5 22.6%; for marshes, 116.2% 5
18.7%; for grasslands, 126.7% 5 17.5%; for mangroves,
90.5% 5 22.2%; and for shrublands and forests,
95.6% 5 10.6%. None of these values is significantly dif-
ferent from 100% (t-test, P 1 .05). Hence, although the
assumptions employed entail a certain bias in some of the
estimates, the values in the data set generally represent
valid carbon balances for the communities considered,
and, therefore, the differences in the trophic fate of production found across these communities are reliable.
Values reported in g plant DW were multiplied by 0.4
for conversion into g C (Wiebe 1988; Schlesinger 1997).
Values for phytoplankton reported on a volumetric basis
(i.e., g C m23 or g C m23 d21) were integrated through
the depth limits of phytoplankton distribution in the water
column and transformed into an areal basis (i.e., g C m22
or g C m22 d21). ANOVA was performed on differences
in plant nutrient concentration, plant carbon pools (biomass and detrital mass), and routes of carbon flow (herbivore consumption, detrital production, decomposition,
export, and refractory accumulation) across communities.
Differences between two specific types of communities
were analyzed with a HSD Tukey multiple comparison test
(Zar 1984). Relationship between variables were analyzed
with correlation and least-square regression techniques.
Differences among correlation coefficients were tested with
the Fischer Z statistic (Fischer 1921). The variables were
log-transformed when necessary to comply with the assumptions of the techniques used.
Results
The NPP varied significantly among the communities considered (fig. 2A; ANOVA, P ! .05). Yet, when specific pairs
of communities were compared, most pairs of communities showed similar ranges of NPP (Tukey HSD test,
P 1 .05). Only benthic microalgal beds reached smaller
values of production than most other community types
(Tukey HSD test, P ! .05). In contrast, both turnover rate
and N and P concentrations declined from microalgal
communities to communities of aquatic macrophytes to
communities of terrestrial macrophytes (fig. 2B– 2D; Tukey HSD test, P ! .05). In fact, faster turnover rates were
closely associated with higher N and P concentrations
across communities (fig. 3A, 3B; table 1), whereas primary
production was independent of N and P concentrations
and turnover rate (fig. 4A–4C; table 1). The nutrient concentrations reported for phytoplanktonic communities refer only to marine phytoplankton. Freshwater phytoplankton normally have lower concentrations (mean N range:
3.9%–5.2%; mean P range: 0.35%–0.62%; Hecky et al.
1993). The inclusion of these values would have certainly
increased the range for the phytoplankton communities,
but the differences found across communities would still
hold (fig. 2C, 2D). Moreover, because the nature of the
dependence of phytoplankton turnover rates on internal
nutrient concentrations seems similar in marine and fresh-
454 The American Naturalist
Figure 2: Box plots showing the distribution of (A) net primary production, (B) plant turnover rate, (C) plant nitrogen concentration, (D) plant
phosphorus concentration, (E) percentage of primary production consumed by herbivores, and (F) absolute consumption by herbivores across the
types of communities considered. Boxes encompass 25% and 75% quartiles, and the central line represents the median. Bars encompass the range
of values between the 25% quartile minus 1.5 times the difference between the quartiles 75% and 25% and the 75% quartile plus 1.5 times the
difference between the quartiles 75% and 25%. Circles and asterisks represent values outside these limits.
Fate of Production in Plant Communities 455
Figure 3: The relationships (A) between plant turnover rate and nitrogen concentration and (B) between plant turnover rate and phosphorus
concentration across the communities compiled. Open circle, phytoplankton; filled circle, benthic microalgae; open square, macroalgal beds; filled
diamond, freshwater macrophyte meadows; filled square, seagrass meadows; filled triangle, marshes; open triangle, grasslands; open diamond, mangroves;
and asterisk, forests. Lines represent the fitted equations.
water communities (Kilham and Hecky 1988), freshwater
phytoplankton with lower nutrient concentrations should
show proportionally slower turnover rates. Therefore, the
associations between turnover and nutrients found across
communities (fig. 3A, 3B) should not have been affected
significantly had freshwater phytoplankton been considered.
The percentage of production consumed by herbivores
was higher in microalgal communities than in communities of macrophytes (fig. 2E; Tukey HSD test, P ! .05).
The distribution of percentage of production consumed
across communities resembled the distributions of nutrient concentrations and turnover rate. Indeed, the percentage of production consumed increased with faster
turnover rates across communities (fig. 5A; table 1). In
contrast, absolute consumption did not show a significant
increase from communities of macrophytes to microalgal
communities (fig. 2F; Tukey HSD test, P 1 .05), although
it varied among communities (ANOVA, P ! .05). The distribution of absolute consumption across communities
rather resembled that of primary production. In fact, absolute consumption was associated with primary production across communities, with more productive communities channeling larger fluxes of production toward
herbivores (fig. 5B; table 1). Correspondingly, the percentage of production consumed and absolute consumption were very poorly related to primary production and
turnover rate, respectively (fig. 5C, 5D).
The percentage of production entering the detrital com-
partment was lower in microalgal communities than in
communities of macrophytes (fig. 6A; Tukey HSD test,
P ! .05). Absolute detrital production, however, was not
smaller in microalgal communities (fig. 6B; Tukey HSD
test, P 1 .05), but it displayed a distribution across communities similar to that of primary production. Accordingly, absolute detrital production and primary production
were strongly related across communities, with more productive communities transferring proportionally larger
fluxes of detrital production (fig. 7; table 1).
Decomposition rates were faster in microalgal communities than in communities of macrophytes (fig. 6C;
Tukey HSD test, P ! .05). Across communities, decomposition rates were associated with biomass turnover rates,
with communities with faster turnover rates having also
faster decomposition rates (fig. 8A; table 1). Conversely,
absolute decomposition did not show an increase from
macrophytic to microalgal communities (fig. 6D; Tukey
HSD test, P 1 .05). Absolute decomposition was closely
associated with primary production across communities,
with more productive communities showing higher values
of absolute decomposition (fig. 8B; table 1). Accordingly,
decomposition rates and absolute decomposition were independent of primary production and turnover rates, respectively (fig. 8C, 8D; table 1).
Refractory accumulation, both in absolute terms and as
percentage of primary production, was smaller in microand macroalgal communities than in the rest of communities (fig. 6E, 6F; Tukey HSD test, P ! .05). Across
456 The American Naturalist
Table 1: Relationships fitted across plant communities
Dependent
variable
Independent
variable
PTR
N
PTR
P
PTR
NPP
NPP
PPC
NPP
N
P
PTR
PPC
C
NPP
NPP
C
DP
PTR
NPP
k
PTR
k
D
NPP
NPP
D
RA
PTR
PTR
RA
B
NPP
PPC
B
PTR
B
NPP
DM
k
DM
PTR
DM
DM
NPP
DP
Relationship
n
R2
F-ratio
P
log PTR = 22.6
(5.1) 1 1.9 (5.1)
log N
log PTR = 21.2
(5.1) 1 1.3 (5.1)
log P
)
)
)
log PPC = 1.9 (5.1) 1
.4 (5.04) log PTR
)
log C = 2.9 (5.1) 1
.8 (5.06) log NPP
)
log DP = 2.2
(5.03)11.1(5.03)
log NPP
log k = 2.8 (5.2)1.7
(5.1) log PTR
)
log D = 2.4 (5.02) 1
1.1 (5.04) log NPP
)
log RA = 2.7 (5.3) 2
3.4 (5.4) elog PTR
)
log B = 3.3 (5.2) 2
1.6 (5.1) log PPC
log B = 2.3 (5.1) 2
1.0 (5.03) log PTR
log B = 2.1 (5.1) 1
1.1 (5.1) log NPP
log DM = 2.1 (5.2) 2
.9 (5.1) log k
log DM = .3 (5.2) 2
.7 (5.1) log PTR
)
)
91
.78
321.2
!.00001
73
.63
124.2
!.00001
369
91
73
125
0
0
0
.50
.4
.4
1.2
122.6
.52
.55
.28
!.00001
135
135
.10
.53
9.0
153.7
!.00001
125
156
.17
.88
27.0
1161.9
!.00001
!.00001
59
.54
69.1
!.00001
59
215
0
.79
1.1
806.2
!.00001
126
98
.02
.52
115
125
.28
.49
45.1
118.3
!.00001
!.00001
369
.75
1130.2
!.00001
369
.27
138.7
!.00001
52
.7
119.8
!.00001
54
.56
68.5
!.00001
54
53
.12
.11
8.4
7.3
.005
.009
3.6
.79*
.003
.30
.06
!.00001
Note: PTR, plant turnover rate; N, plant nitrogen concentration; P, plant phosphorus concentration; NPP,
net primary production; PPC, percentage of primary production consumed by herbivores; C, absolute consumption by herbivores; DP, plant detrital production; k, decomposition rate; D, absolute decomposition;
RA, accumulation of refractory plant detritus; B, plant biomass; DM, plant detrital mass. Asterisk signifies
x2 statistic.
communities, absolute refractory accumulation was better
related to turnover rate than to primary production (figs.
9A, 9B; table 1; Z-test, H0: equality between correlation
coefficients, P ! .05). Export, expressed both in absolute
terms and as percentage of primary production, varied
widely among communities (fig. 10A, 10B) and tended to
be largest in macroalgal beds (Tukey HSD test, P ! .05).
Plant biomass increased from microalgal communities
to communities of aquatic macrophytes to communities
of terrestrial macrophytes (fig. 10C; Tukey HSD test,
P ! .05). This distribution counters the distributions of
turnover and percentage of production consumed across
communities. Accordingly, communities with faster turnover rates and higher percentages of production consumed
store smaller pools of biomass (fig. 11A, 11B; table 1). In
contrast, biomass is only weakly related to primary pro-
Fate of Production in Plant Communities 457
Figure 4: The relationships (A) between net primary production and nitrogen concentration, (B) between net primary production and phosphorus
concentration, and (C) between turnover rate and primary production across the communities compiled. Symbols as in figure 3.
duction across communities (table 1; Z-test, H0: equality
between correlation coefficients, P ! .05).
Similarly, plant detrital mass seems to increase from
microalgal communities to communities of aquatic macrophytes to communities of terrestrial macrophytes (fig.
10D; ANOVA, P ! .05). Across communities, plant detrital
mass is associated with turnover and decomposition rates,
with a tendency for communities with faster turnover and
decomposition rates to store smaller pools of detrital mass
(fig. 12A, 12B; table 1). Conversely, detrital mass is very
poorly related to primary production and detrital production (table 1). Estimates of detrital mass included only
leaf detritus in some of the forests and shrublands compiled (see data set). Therefore, I used the values of production, turnover rate, decomposition rate, and detrital
production for the foliar compartments in those communities when deriving the relationships between detrital
mass and primary production, biomass turnover rates, decomposition rates, and detrital production for all
communities.
Discussion
These results allow a synthetic view of the fate of production in plant communities. With the exception of
458 The American Naturalist
Figure 5: The relationships (A) between percentage of net primary production consumed by herbivores and plant turnover rate, (B) between absolute
consumption by herbivores and net primary production, (C) between percentage of net primary production consumed by herbivores and net primary
production, and (D) between absolute consumption by herbivores and plant turnover rate across the communities compiled. Lines represent the
equations fitted. Symbols as in figure 3.
microalgal communities, most production in all the communities considered is channeled as detrital production
(fig. 6A). That generalizes the predominance of the detrital
pathway in the trophic transfer of primary production to
heterotrophs, in agreement with previous results in different communities (Schlesinger 1977; Thayer et al. 1984;
Mann 1988; Cebrian and Duarte 1998). In general, most
detrital production is decomposed within the community,
with only modest fractions being exported even in communities typically exposed to substantial horizontal advection (fig. 10B). Macroalgal beds represent the only ex-
ception to this pattern, which, on the average, export about
50% of their production. This is because macroalgal beds
often inhabit rocky shores exposed to intense wave scouring (Mann 1972; Marsden 1991). In general, only a small
fraction of production is accumulated as refractory detritus
within the community (fig. 6F), although this fraction may
be sizable in grasslands, shrublands, and forests (Smith
and Clymo 1984).
In spite of these generalities, my results reveal important
qualitative and quantitative differences in the fate of production among plant communities. These differences are
Fate of Production in Plant Communities 459
Figure 6: Box plots showing the distribution of (A) percentage of primary production channelled as detritus, (B) plant detrital production, (C)
decomposition rates, (D) absolute decomposition, (E) accumulation of refractory detritus, and (F) percentage of primary production accumulated
as refractory detritus across the types of communities considered. Boxes encompass the 25% and 75% quartiles, and the central line represents the
median. Bars encompass the range of values between the 25% quartile minus 1.5 times the difference between the quartiles 75% and 25% and the
75% quartile plus 1.5 times the difference between the quartiles 75% and 25%. Circles and asterisks represent values outside these limits.
460 The American Naturalist
Figure 7: Relationship between plant detrital production and net primary
production across the communities compiled. Line represent the equation
fitted. Symbols as in figure 3.
related to differences either in the magnitude of production or in the quality of production for consumers (i.e.,
N and P concentrations in plant tissues). Across plant
communities, the quality of plant tissues for consumers is
closely associated with plant turnover rate, but it is independent of the magnitude of production (figs. 3 and 4;
table 1). I identify a tendency for plant communities with
a higher quality for consumers (i.e., faster plant nutrient
concentrations and turnover rates) to lose a higher percentage of production to herbivores (fig. 5A). This tendency supports the hypothesis that the metabolism and
feeding rates of herbivores are limited by the nutrient concentrations of their diets (Mattson 1980; Sterner and Hessen 1994; Hartley and Jones 1997; Sterner et al. 1997):
plant tissues with higher nutrient concentrations enhance
herbivore metabolism and feeding rates and, as a consequence, communities composed of plants with higher N
and P concentrations have a higher percentage of production removed by herbivores. Greater percentages of
production consumed in communities with more palatable
plants should not be due to larger herbivore abundances.
This is because across aquatic and terrestrial communities
primary production is related to herbivore abundance
(McNaughton et al. 1989; Cyr and Pace 1993), but independent of plant nutrient concentration (fig. 4A, 4B),
and therefore plant nutrient concentration and herbivore
abundance should be unrelated across communities.
The tendency for communities composed of plants with
higher nutrient concentrations to lose higher percentages
of production to herbivores implies that these communities channel smaller percentages of production as detritus (fig. 6A). Across communities, the importance of herbivory as a trophic route of primary production increases
with plant palatability, as it has been previously hypothesized (Sterner et al. 1997). Moreover, this tendency supports the notion that across the range of communities
compared, herbivores do not increase their feeding rates
over plants with lower nutrient concentrations as a means
of compensating for lower nutritional qualities. This
mechanism has been hypothesized as implausible in an
evolutionary sense because higher feeding rates on less
nutritional, slower turning-over plants would eventually
lead to plant depletion (Sterner and Hessen 1994). Yet,
enhanced feeding rates as a herbivore response to lower
nutritional quality have been found during transient periods within some particular plant communities (Williams
et al. 1994; Lindroth et al. 1995; Hughes and Bazzaz 1997).
The dependence of the intensity of herbivory (i.e., fraction of production consumed) on plant nutritional quality
across communities overrides the effect of communityspecific herbivore characteristics. For instance, some of the
communities compared host mainly migratory herbivores,
whereas others have only resident herbivores. This migratory-resident duality may introduce considerable variability in the intensity of herbivory among communities
(Nienhuis and Groenendijk 1986; Portig et al. 1994). In
addition, some communities shelter mainly invertebrate
herbivores (e.g., most submerged communities), whereas
others host vertebrate homeotherm herbivores. These two
types of herbivores have different metabolical needs, and
these differences may cause substantial variability in the
intensity of herbivory across communities (Crawley 1983;
Begon et al. 1990). Moreover, the intensity of predation
on herbivores also varies among communities, which may
entail different cascade effects on the intensity of herbivory
in different communities (Heck and Valentine 1995;
Hartley and Jones 1997). Finally, differences in herbivore
stoichiometry among communities may also be responsible for differences in herbivory. Although communities
of more nutritional plants should have herbivores with
higher nutrient contents, the range of nutrient concentrations in herbivore tissues may vary notably within a
given community (Sterner and Hessen 1994). Because herbivores with higher nutrient concentrations also have
higher nutritional demands, variations in the range of herbivore stoichiometry among communities could also generate differences in the intensity of herbivory. All these
factors could perhaps explain the 11 order-of-magnitude
variability observed in herbivory intensity among communities with similar turnover rates (fig. 5A).
The tendency toward higher intensities of herbivory
with higher plant palatability across communities suggests
Fate of Production in Plant Communities 461
Figure 8: The relationships (A) between decomposition rate and plant turnover rate, (B) between absolute decomposition and net primary production,
(C) between decomposition rate and net primary production, and (D) between absolute decomposition and plant turnover rate across the communities
compiled. Lines represent the equations fitted. Symbols as in figure 3.
that herbivores should exert a greater control of plant
biomass in communities with more palatable plants. Accordingly, herbivores have been shown to limit plant
biomass in communities with fast turnover rates (Lampert
et al. 1986; McNaughton et al. 1988; Jing and Coley 1990),
whereas they seem unimportant in communities with slow
turnover rates (Bray 1964; Petrusewicz and Grodzinski
1975; Cebrian et al. 1996). My results suggest that, at least
in part, communities with more palatable plants store
smaller pools of biomass as a result of the higher intensities
of herbivory supported: communities with faster turnover
rates store smaller pools of biomass partially because they
reach relatively similar values of production (fig. 4C) but
lose higher percentages to herbivores (fig. 5A). This hypothesis is supported by the tendencies toward lower
biomasses with faster turnover rates and larger intensities
of herbivory across communities (fig. 11A, 11B).
Yet communities with faster turnover rates also have
higher plant mortality rates (Odum 1971; Phillips and
Gentry 1994), which can also contribute to the decline in
plant biomass observed with faster turnover rates across
communities. I used techniques of path analysis to differentiate the direct connection between faster turnover
and decreasing biomass from the connection mediated
462 The American Naturalist
Figure 9: The relationships (A) between accumulation of refractory plant detritus and turnover rate and (B) between accumulation of refractory
plant detritus and net primary production across the communities compiled. Lines represent the equations fitted. Symbols as in figure 3.
through increasing herbivory. These techniques allowed
the categorization of variance in plant biomass across communities into the fraction directly explained by turnover,
the fraction directly explained by herbivory, and the fraction explained by the interaction of both herbivory and
turnover (Williams et al. 1990). The variance in plant
biomass among communities explained by turnover is significantly reduced, albeit still significant (P ! .01), when
the interaction with herbivory is eliminated (from R 2 =
.69 to R 2 = .44). This suggests that the reduction in biomass with higher palatability (i.e., faster turnover) across
communities is a partial effect of increasing herbivory.
Furthermore, I used a randomization test (Pendleton et
al. 1983) to test for spurious effects on the relationship
between decreasing biomass and increasing turnover due
to the presence of a biomass term in both variables (turnover rate was estimated as the quotient between production and biomass in many communities). The result demonstrates that the relationship obtained is different from
that expected solely from the effect of a common term in
both variables (H0: spurious slope = observed slope, P !
.001).
Detritus from communities composed of more nutritional plants undergo faster decomposition (fig. 8A). This
indicates that plant communities that turn over their
biomass compartment faster also turn over their degradable detrital compartment faster. This implies that communities with faster biomass turnover rates have higher
nutrient recycling rates, as expected to meet their faster
rates of nutrient uptake (i.e., higher nutrient demand;
Chapin et al. 1986, 1987). This trend has been hypothesized recently (Sterner et al. 1997), and these results further
support it. Accordingly, fast and efficient nutrient recycling
generally plays a pivotal role in the maintenance of communities with fast biomass turnover rates and high nutrient demands (Crossland et al. 1991; Legendre and Rassoulzadegan 1995), whereas communities with slower
biomass turnover rates normally exhibit slow recycling
rates and low nutrient demands (Enriquez et al. 1993).
The tendency toward faster decomposition rates with
higher plant nutrient concentrations across communities
is consistent with the idea that the metabolism and feeding
rates of decomposers are limited by the nutrient concentrations in plant detritus (Enriquez et al. 1993). This limitation has been shown experimentally for a number of
types of autotrophs (Swift et al. 1979; Goldman et al. 1987;
Enriquez et al. 1993), and here it is suggested to exist across
a broad range of plant communities. The tendency toward
faster decomposition rates with higher plant nutrient concentrations overrides the effects on decomposition of different abiotic factors in the communities compared, such
as temperature (Edwards 1975; Van Cleve et al. 1981),
moisture (Wildung et al. 1977; Santos et al. 1984), and
sediment redox conditions (Schlesinger 1977; Post et al.
1982). These factors could probably explain much of the
residual variability in the tendency established.
Moreover, these results indicate that communities with
more palatable detritus store smaller detrital pools as a
consequence of the faster decomposition rates supported
(fig. 12A): communities with faster biomass turnover rates
Fate of Production in Plant Communities 463
Figure 10: Box plots showing the distribution of (A) export, (B) percentage of primary production exported, (C) plant biomass, and (D) detrital
mass across the types of community considered. Boxes encompass the 25% and 75% quartiles, the central line represents the median, and bars
encompass the range of values between the 25% quartile minus 1.5 times the difference between the quartiles 75% and 25% and the 75% quartile
plus 1.5 times the difference between the quartiles 75% and 25%. Circles and asterisks represents values outside these limits.
store smaller pools of detrital mass (fig. 12B) because they
reach relatively similar values of production and detrital
production (fig. 4C) but have faster decomposition rates
(fig. 8A). Another corollary of these tendencies is that
communities composed of more palatable plants show
lower levels of refractory accumulation (fig. 9A). Refractory accumulation corresponds to the amount of primary
production nonconsumed by herbivores that is neither
exported nor decomposed over the study period. Because
both the percentage of production consumed and decomposition rates increase nonlinearly with turnover rate
across communities (figs. 5A and 8A, respectively) while
being poorly related to primary production (figs. 5C and
8C), the decrease in refractory accumulation with faster
turnover rates is exponential (fig. 9A). These results indicate that communities composed of more palatable
plants are smaller carbon sinks because they experience
higher intensities of consumption by heterotrophs, as it
has been recently suggested (Cebrian et al. 1998).
So far I have discussed the dependence of intensity of
herbivory and decomposition rates on plant palatability
across communities. Absolute consumption by herbivores,
however, is very poorly related to plant palatability across
communities (fig. 5D). Instead, differences in absolute
464 The American Naturalist
Figure 11: The relationships (A) between plant biomass and the percentage of net primary production consumed by herbivores and (B) between
plant biomass and turnover rate across the communities compiled. Lines represent the equations fitted. Symbols as in figure 3.
consumption across communities are better related to differences in absolute production (fig. 5B), in agreement
with results of other across-systems comparisons (McNaugton et al. 1989; Cyr and Pace 1993). The association
between absolute consumption and production across
communities is a mathematical consequence of the ranges
of the variables compared: absolute consumption is the
product between primary production and the percentage
consumed by herbivores and, because primary production
and the percentage consumed vary by four and three orders of magnitude across the communities compared, respectively (fig. 5C), differences in absolute consumption
across communities are better correlated to primary production than to the percentage consumed. As a consequence, when a broad range of communities is compared,
more productive communities tend to transfer greater
fluxes of production to herbivores (fig. 5B). McNaugton
et al. (1989) and Cyr and Pace (1993) also show that higher
absolute consumptions in more productive communities
are conducive to larger herbivore abundances. Therefore,
differences in herbivore biomass across communities seem
to be associated with differences in the magnitude of production rather than with the quality (i.e., nutrient concentration in plant tissues) of that production. These tendencies, if confirmed, would indicate that, across
communities, increases in herbivore biomass due to larger
absolute consumptions override any possible increases due
to enhanced growth rates resulting from more palatable
diets. Higher predation rates on herbivores feeding on
more palatable plants could perhaps partially explain these
hypothesized trends. Similarly, absolute decomposition is
closely related to production across communities (fig. 8B),
and it is independent of plant palatability (fig. 8D). Again,
the reason depends on the relative range of the variables
compared across communities. At the time scales covered
by the studies compiled (i.e., from one to some few years),
the variability in production across communities is greater
than the variability in the percentage decomposed, and
because decomposition is the product of production and
percentage decomposed, its variability across communities
is dictated by variability in production.
Differences in export, both as absolute magnitude and
as percentage of production, across communities are independent of differences in plant palatability and are only
weakly related to differences in production (least square
regression of log export versus log production: R 2 = .23,
P ! .05). Differences in export across communities may
be related to differences in the intensity of horizontal advection through the community. This is supported by the
fact that communities with higher export rates are typically
exposed to substantial horizontal advection through waves,
currents or tides, such macroalgal beds, seagrass meadows,
and land-ocean fringing communities such as marshes and
mangroves (fig. 10A, 10B). Communities with high export
rates have the potential to support large levels of secondary
production in adjacent communities (Nixon 1980; Twilley
et al. 1986; Duarte and Cebrian 1996). Moreover, high
export rates must imply substantial nutrient losses for the
exporting communities since virtually all of the exported
detritus are consumed and recycled elsewhere (Hedges and
Fate of Production in Plant Communities 465
Figure 12: The relationships (A) between plant detrital mass and decomposition rate and (B) between plant detrital mass and turnover rate across
the communities compiled. Lines represent the equations fitted. Symbols as in figure 3.
Parker 1976; Smith and MacKenzie 1987). Hence, communities with high export rates must have high rates of
nutrient import from adjacent communities to offset nutrient losses and maintain primary production. This argument suggests important implications for the interplay
between “new” (i.e., fueled by allochthonous nutrients)
and recycled production in plant communities: communities with higher percentages of production exported
should have greater fractions of their production fueled
by imported nutrients (i.e., higher factions of new
production).
In summary, plant nutritional quality for consumers
and primary production are independent predictors of the
nature and magnitude of the trophic routes of carbon flow
in plant communities. Communities composed of more
palatable plants lose higher percentages of production to
herbivores, channel lower percentages as detritus, and experience faster decomposition rates. I present evidence that
communities with more palatable plants store smaller carbon pools as a result of the higher intensities of herbivory
and faster decomposition rates supported, but more experimental work is needed to confirm this hypothesis.
These results may have important implications for broadscale carbon and nutrient balances because widespread
anthropogenic eutrophication may enhance the nutritional
quality of plant communities in large areas (Duarte 1995;
Borum and Sand-Jensen 1996; Wedin and Tilman 1996).
Absolute consumption and decomposition, however, are
not associated with plant nutritional quality but with pri-
mary production across communities. The patterns in the
nature and controls of the trophic fate of production reported here encompass contrasting communities ranging
from unicellular autotrophs to structurally complex macrophytes. When the range of communities compared is
reduced, factors other than plant nutritional quality and
magnitude of production may be most important at explaining differences in the trophic fate of production.
Hence, the dependence of the patterns reported on the
range of communities encompassed needs investigation.
Acknowledgments
Research was supported by a postdoctoral fellowship from
the Culture Ministry of the Spanish government. I thank
M. Cole, M. Griffin, C. Jones, K. Kroeger, E. Stieve, E.
Watson, and M. Williams for enlightening discussions on
the ideas presented. M. Williams also provided valuable
statistical help. I also thank R. Sterner and two anonymous
referees for helpful comments on the manuscript. I am
deeply indebted to the staff of the Marine Biological Laboratory/Woods Hole Oceanographic Institution Library
for providing help with the literature research.
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