Environmental Pollution 113 (2001) 95±107
www.elsevier.com/locate/envpol
Complex interactions between autotrophs in shallow marine and
freshwater ecosystems: implications for community responses to
nutrient stress
K.E. Havens a,*, J. Hauxwell b, A.C. Tyler c, S. Thomas d, K.J. McGlathery c,
J. Cebrian e, I. Valiela b, A.D. Steinman a, Soon-Jin Hwang f
a
South Florida Water Management District, 3301 Gun Club Road, West Palm Beach, FL 33416-4680, USA
b
Boston University Marine Program, Marine Biological Laboratory, Woods Hole, MA 02543, USA
c
Department of Environmental Sciences, University of Virginia, Charlottesville, VA 22903, USA
d
IRD, Gamet c/o Cemagref 361, Rue JF Breton, 34033 Montpellier Cedex 1, France
e
Dauphin Island Sea Lab, 101 Bienville Boulevard, PO Box 369-370, Dauphin Island, AL 36528, USA
f
The Graduate School, College of Agricultural and Life Sciences, Konkuk University, Seoul 143-701, South Korea
Received 7 March 2000; accepted 8 June 2000
``Capsule'': Complex interactions between phytoplankton, attached algae, and vascular plants a€ect ecosystem responses
to nutrient stress.
Abstract
The relative biomass of autotrophs (vascular plants, macroalgae, microphytobenthos, phytoplankton) in shallow aquatic ecosystems is thought to be controlled by nutrient inputs and underwater irradiance. Widely accepted conceptual models indicate that
this is the case both in marine and freshwater systems. In this paper we examine four case studies and test whether these models
generally apply. We also identify other complex interactions among the autotrophs that may in¯uence ecosystem response to cultural eutrophication. The marine case studies focus on macroalgae and its interactions with sediments and vascular plants. The
freshwater case studies focus on interactions between phytoplankton, epiphyton, and benthic microalgae. In Waquoit Bay, MA
(estuary), controlled experiments documented that blooms of macroalgae were responsible for the loss of eelgrass beds at nutrientenriched locations. Macroalgae covered eelgrass and reduced irradiance to the extent that the plants could not maintain net growth.
In Hog Island Bay, VA (estuary), a dense lawn of macroalgae covered the bottom sediments. There was reduced sediment±water
nitrogen exchange when the algae were actively growing and high nitrogen release during algal senescence. In Lakes Brobo (West
Africa) and Okeechobee (FL), there were dramatic seasonal changes in the biomass and phosphorus content of planktonic versus
attached algae, and these changes were coupled with changes in water level and abiotic turbidity. Deeper water and/or greater
turbidity favored dominance by phytoplankton. In Lake Brobo there also was evidence that phytoplankton growth was stimulated
following a die-o€ of vascular plants. The case studies from Waquoit Bay and Lake Okeechobee support conceptual models of
succession from vascular plants to benthic algae to phytoplankton along gradients of increasing nutrients and decreasing underwater irradiance. The case studies from Hog Island Bay and Lake Brobo illustrate additional e€ects (modi®ed sediment±water
nutrient ¯uxes, allelopathy or nutrient release during plant senescence) that could play a role in ecosystem response to nutrient
stress. # 2001 Elsevier Science Ltd. All rights reserved.
Keywords: Algae; Lakes; Estuaries; Nutrient dynamics; Macroalgae; Periphyton
1. Introduction
Aquatic ecosystems around the world have been
heavily impacted by discharges of nutrients from human
* Corresponding author. Fax: +1-561-687-6442.
E-mail address: [email protected] (K.E. Havens).
activities, including point sources of urban, residential,
and industrial pollution, and non-point sources of
agricultural pollution. Carpenter et al. (2000, p. 752)
noted that cultural eutrophication (enrichment with
nutrients from human sources) is ``a widespread and
growing problem of lakes, rivers, estuaries, and coastal
oceans.'' Problems associated with excess nutrient
0269-7491/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved.
PII: S0269-7491(00)00154-8
96
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
inputs have been documented for freshwater lakes, rivers, wetlands, and the coastal marine environment
(Smith et al., 1999).
Phosphorus (P) and nitrogen (N) are the nutrients
most often limiting to autotrophs in freshwater and
marine ecosystems (Schindler, 1977; Hecky and Kilham,
1988; Vitousek and Howarth, 1991; Downing, 1997).
When lakes, rivers, or estuaries receive additional inputs
of these nutrients from anthropogenic sources, there are
generally increases in the biomass of autotrophs, and
sometimes dramatic changes in taxonomic structure
and functional groups (Valiela et al., 1997a; Smith et al.,
1999; Philippart et al., 2000). These changes can radiate
upwards through the food web, a€ecting primary
and secondary consumers (e.g. Valiela et al.; Moeller et
al., 1998). Excessive nutrient loading can also lead to
phenomena such as harmful algal blooms (Paerl, 1988;
Burkholder and Glasgow, 1997).
Many aquatic ecosystems that are impacted by nutrients are shallow, and in contrast to deep planktondominated ecosystems they are capable of supporting a
variety of autotrophs. These include: vascular plants;
algae attached to plants, sediments, rocks, and other
substrata; macroalgae; and phytoplankton. These autotrophs compete for nutrients, light, and space, and have
other complex ecological interactions that may in¯uence
how the ecosystem as a whole responds to nutrient stress.
Conceptual models have been developed to describe
changes in the relative biomass of plants, benthic
algae, and phytoplankton as a function of nutrient
loading and underwater irradiance. The model of
Sand-Jensen and Borum (1991) predicts that in shallow
lakes and estuaries with low nutrient availability in the
water, benthic algae and vascular plants will dominate
due to their ability to sequester nutrients from the
sediments. In nutrient-enriched waters, however, phytoplankton will dominate because they rapidly sequester water column nutrients, increase in biomass, and
shade the benthic algae and plants. Valiela et al.
(1997a) expanded this model to explicitly consider
benthic macroalgal mats. They predicted that with
increased nutrient loading, macroalgae will be favored
over vascular plants because they have: (1) a lower
compensation irradiance for growth; (2) more rapid
uptake of N, which typically is the primary limiting
nutrient in estuaries (Howarth, 1988); and (3) more
rapid growth. Macroalgae are predicted to form canopies that shade, and eventually kill, vascular plants. At
the highest rates of nutrient loading, phytoplankton are
predicted to dominate because they have an even lower
compensation irradiance, nutrient uptake, and growth
rates than benthic algae.
This paper presents four case studies that independently test these models or provide information about
how other complex interactions between autotrophs can
a€ect ecosystem responses to cultural eutrophication.
2. Case study 1 Ð e€ect of macroalgal shading on
eelgrass (Zostera marina) production in a coastal estuary (Waquoit Bay, USA)
In the region of Cape Cod, MA, septic systems have
become a major source of N loading to coastal ecosystems. As noted by Valiela et al. (1997b) and others,
increased inputs of N can cause a suite of changes in
estuaries, including macroalgal blooms. Observational
evidence indicates that the thick canopies of macroalgae
that accumulate on the bottom of receiving estuaries
can shade and eventually replace seagrass beds (Duarte,
1995). A loss of eelgrass (Z. marina) has coincided, for
example, with increased rates of N loading and
increased macroalgal biomass in estuaries in New England (Short et al., 1993), including estuaries of Waquoit
Bay (Costa, 1988; Valiela et al., 1992; Lyons et al., 1995;
Short and Burdick, 1996; Fig. 1, top panel).
This case study involved controlled experiments in
two estuaries of Waquoit Bay, MA (Hauxwell et al.,
2000). These experiments were performed: (1) to assess
whether macroalgal canopies signi®cantly impact
Fig. 1. Top panel: relationship between the biomass of eelgrass (Zostera marina), the biomass and canopy height of macroalgae, and
nitrogen (N) loading rate in Waquoit Bay, MA, USA. Bottom panel:
aboveground summer (1 June±10 September) net production of Z.
marina (g dry wt. biomass m 2 summer 1) versus macroalgal canopy
height, calculated by multiplying density of shoots by growth rates of
shoots in enclosures in the low and higher N estuaries containing different canopy heights of macroalgae (meanS.E.).
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
eelgrass production and were responsible for recent
decline of eelgrass in one of the estuaries; and (2) to
determine the relative contributions of phytoplankton,
epiphyton, and macroalgae to light limitation of
eelgrass.
To evaluate how increased macroalgal biomass a€ected eelgrass production (density and growth rate of
shoots), macroalgal enclosure/exclosure experiments
were conducted during summer 1998 in two eelgrass
meadows. The ®rst site, Sage Lot Pond, featured a low
N loading rate (5 kg N ha 1 year 1) (Valiela et al.,
1997b), a pristine eelgrass population, and an approximately 2-cm macroalgal canopy. The second site, Hamblin Pond, had a higher N loading rate (30 kg N ha 1
year 1; Valiela et al., 1997b), a declining eelgrass population (90% cover loss in past decade), and an approximately 9-cm macroalgal canopy. Plastic fences (50 cm
high) were placed around the sides of 11 m plots of
eelgrass within the two meadows in late May 1998,
using SCUBA. The 2.5-cm mesh size was small enough
to include or exclude macroalgae, but large enough so
that water circulation and irradiance were not signi®cantly a€ected. In each meadow there were control
enclosures, in which the existing macroalgal canopy was
unaltered. Treatments included total macroalgae
removal, with a 0-cm canopy height maintained
throughout the experiment, and macroalgal additions,
with a 12-, 19-, or 25-cm canopy height in the low N
estuary and a 14- or 18-cm canopy height in the higher
N estuary. The treatments were selected to represent
ranges observed in natural communities subjected to
varying levels of nutrient input. Macroalgae for the
treatments were collected from the meadows in which
they were used and consisted of a mixture of Cladophora
vagabunda (®lamentous green alga) and Gracilaria tikvahiae (branched red alga). Three replicate enclosures of
each canopy height were established. Density (shoots
m 2) and growth (mg shoot 1 day 1; using a standard
marking technique; Zieman and Wetzel, 1980) measurements were made within each enclosure every 3±4
weeks from 28 May to 10 September. Summer production (g m 2 summer 1) was then calculated by multiplying plant density by growth rate for each enclosure
on each date and summing for the experimental period.
In both meadows, production of eelgrass decreased as
the macroalgal canopy height increased (Fig. 1, bottom
panel). In the low N estuary, the existing 2-cm canopy
did not signi®cantly a€ect production; results between
controls and 0-cm treatments were similar. Shoot production in the macroalgal addition treatments declined
at rates dependent on canopy height (12 cm addition had
38%, 19 cm addition had 17%, and 25 cm addition
had just 11% of the production attained in controls).
Based on the response in shoot density to the lowest 12
cm addition (40 shoots lost m 2 month 1), we conclude
that a meadow similar to the one in the low N estuary
97
(peak 400 shoots m 2) would lose its aboveground biomass in less than a year if it were impacted by a nutrientrelated macroalgal bloom of similar canopy height.
Eelgrass production in the 9-cm control enclosures of
the higher N estuary was only 6% of that observed
in the 2-cm control enclosures of the low N estuary (Fig.
1, bottom panel). No control enclosures in the higher N
estuary had any shoots remaining by the middle of
summer. Upon removal of the existing macroalgal
canopy, however, there was a dramatic increase in eelgrass production. Density and growth rates of shoots
increased, resulting in production rates approximately
®ve times those in the 9-cm controls. These results indicate that a signi®cant fraction of eelgrass loss in this
estuary is due to the presence of the 9-cm macroalgal
canopy.
To estimate the potential contribution of various
autotrophs to light limitation of eelgrass we carried out
the following analysis. We ®rst determined light
attenuation by the water column of both estuaries.
Of the remaining light reaching the benthos, we estimated the amounts that could be attenuated the observed
epiphytes and macroalgae, and ®nally light available for
eelgrass photosynthesis (Fig. 2). The empirical relationship between biomass and light penetration was provided in Peckol and Rivers (1996) for macroalgae and in
Twilley et al. (1985) for epiphytes. We carried out this
analysis both for established shoots, whose leaves are
coated with epiphytes and only a portion of the photosynthetically active material is shaded by macroalgae,
and for newly recruiting shoots, whose leaves are not
yet colonized by epiphyton but whose photosynthetic
biomass is completely buried by macroalgae.
Results of this synthesis show that attenuation of light
in the water column and shading by epiphytes is of
greater importance for established shoots, but that
shading due to existing macroalgal canopies is more
important for new shoots. These results also provide
evidence that light limitation may be the mechanism by
which eelgrass declines in the higher N estuary. Established shoots may at times receive saturating levels of
light (100 mmol photons m 2 s 1; Dennison and
Alberte, 1982); however, newly recruiting shoots may
receive light intensities below compensation levels (10
mmol photons m 2 s 1; Dennison and Alberte, 1982).
In summary, there is an approximate 9±12 cm critical
macroalgal canopy height at which eelgrass begins to
decline in Cape Cod, MA. Increased standing stocks of
phytoplankton and/or shading as a result of increased
epiphyte loads on eelgrass leaves may also occur as a
result of nutrient loading to these estuaries (Short et al.,
1993; Taylor et al., 1995; Valiela et al., 1997a). In addition to shading, we do not rule out suppressive biochemical factors that may be associated with macroalgal
canopies, including low oxygen, high sul®de levels, and
high concentrations of ammonium within the canopy
98
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
Fig. 2. Mean summer light intensity (mmol m 2 s 1) at the water surface (corrected for surface re¯ectance, Peckol and Rivers, 1996), and estimated
light intensity reaching eelgrass (Zostera marina) leaves of established shoots (after interception of light due to the water column and summer
standing stocks of epiphytes and macroalgae) and newly recruiting shoots (after interception due to the water column and summer standing stocks
of macroalgae) in two estuaries of Waquoit Bay subject to di€erent nitrogen loading rates. Range of water column attenuation for established shoots
represents light reaching the tips of the tallest leaves or the base of the shoot for each estuary. Epiphyte and macroalgal shading were assumed to
occur simultaneously and were based on percentages of incoming light after phytoplankton attenuation. Hence, these processes are not hierarchical
for epiphytes and macroalgae.
near eelgrass roots. High sul®de levels may inhibit
enzymatic functions, ATP production, or nutrient
uptake (Goodman et al., 1995) in eelgrass, and high
concentrations of ammonium may be directly toxic to
eelgrass (van Katwijk et al., 1997). Understanding the
interactions among autotrophs in estuaries is important
for management e€orts in these environments. It will
be particularly important to determine the threshold
N-loading value at which the shift from eelgrass to a
macroalgal-dominated habitat occurs.
3. Case study 2 Ð the in¯uence of macroalgae on
dissolved organic N ¯uxes in a shallow coastal lagoon
(Hog Island Bay, USA)
The high surface area-to-water volume ratio of coastal
lagoons may increase the importance of sediment±water
column interactions (Nowicki and Nixon, 1985; SandJensen and Borum, 1991). Macroalgae can a€ect N
¯uxes from the sediments to the water column by intercepting regenerated N (Valiela et al., 1992; Bierzychudek et al., 1993; McGlathery et al., 1997) and may
thereby limit phytoplankton growth (Thybo-Christesen
et al., 1993). The algae can intercept both dissolved
inorganic N (DIN) and dissolved organic N (DON).
DON makes up a large fraction of the total N in marine
systems (Sharp, 1983), and a substantial portion of
atmospheric N deposition may be organic (Paerl et al.,
1990; Cornell and Jickells, 1995; Paerl, 1995; Seitzinger
and Sanders, 1999). Macroalgae are capable of utilizing
some forms of DON (Hanisak, 1983) as well as DIN,
and therefore play an important role as a DIN and
DON sink during rapid growth and as a DON source
during senescence.
The location of this case study was Hog Island Bay, a
shallow back-barrier lagoon and part of the Virginia
Coast Reserve Long Term Ecological Research project.
N, both inorganic and organic, enters the lagoon from
agricultural run-o€, groundwater, and atmospheric
deposition. Within Hog Island Bay, algal and bacterial
uptake, remineralization, nitri®cation, and denitri®cation transform N inputs. Total dissolved N (TDN) ranges from 10 to 35 mM, and from 55 to 95% of TDN is
made up by DON. Macroalgae and benthic microalgae
are the dominant primary producers with Ulva sp., G.
tikvahiae, and Cladophora sp. being the most abundant
taxa; phytoplankton production is low throughout the
year and seagrasses have been locally extinct since
the 1930s. Shallow mid-lagoon shoals (<1 m), which
are the result of remnant oyster reefs, have higher
macroalgal biomass than shallow areas bordering the
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
mainland or the barrier islands. Substantial macroalgal
mats develop at speci®c locations in the mid-lagoon,
with the peak biomass occurring in June±July. At certain sites with high biomass (>400 g dry wt. m 2), the
macroalgal populations crash following the peak in
biomass, probably as a result of high temperatures and
self-shading within the algal mat.
The purpose of the study was to determine the
importance of DON in Hog Island Bay N cycling, and
to show the role that macroalgae play in DON dynamics. Sediment±water column DON, urea, and DIN
¯uxes were measured seasonally from October 1997 to
August 1998, in the presence and absence of Ulva sp.
during light±dark incubations of sediment cores collected from a shallow shoal area (Shoal 1) of Hog Island
Bay. In July of 1998 ¯uxes were also measured in cores
from an additional site (Shoal 2) where a massive algal
bloom (patches up to 650 g dry wt. m 2) had recently
crashed. While substantial macroalgal biomass was
measured at Shoal 1 (up to 180 g dry wt. m 2), no crash
was observed.
The sediment was a source of DON at all times of
the year. At Shoal 1, DON e‚ux was highest during the
summer and fall, and lowest in the spring (Fig. 3). The
sediments at all times of year took up DIN, and the rate
of uptake was proportional to the initial water-column
concentration. The sediment also took up urea in the
summer and fall, in contrast to sediments in other parts
of Hog Island Bay, which always were sources of urea
(Tyler et al., 2000). The release of compounds having a
low carbon (C):N ratio from coastal sediments has been
shown in other studies (Lomstein et al., 1989; Burdige
and Zheng, 1998), and the lack of e‚ux may represent a
99
di€erence in the infaunal community. In July 1998, the
release of DON and DIN from the decomposing algae
within Shoal 2 sediments was one to two orders of
magnitude higher than at Shoal 1 (Fig. 3).
Macroalgae were a net sink for DIN and urea, but a
net source for other DON compounds. Uptake/release
rates were 2.11.1, 0.70.3, and 3.40.6 mm g dry
weight m 2 for DON, urea, and DIN, respectively.
The DIN uptake represents only uptake in the light
and probably underestimates actual rates, because the
macroalgae were capable of bringing DIN concentrations to zero within a few hours. Urea uptake occurred
primarily in the dark, while the release of other DON
compounds occurred in the light more than in the dark,
indicating `leakage' during active photosynthesis.
Retention of nutrients in macroalgal biomass is temporary and N is released as DON during active growth,
and as DON, NH+
4 , and particulate organic nitrogen
upon senescence and decomposition. Ulva, like phytoplankton (Bronk et al., 1994), appears to `leak' DON
into the water during active growth, and over relatively
short time scales (hours) may act as a conduit whereby
DIN (and urea) is taken up, transformed, and subsequently released into the water column as DON. DON
release by photosynthesizing macroalgae ranges from
70 to 850 mmol m 2 of sediment surface during blooms,
and is likely to fuel heterotrophic metabolism in
the water column. Macroalgae also can a€ect sediment±
water column N ¯uxes by intercepting N that is released
from the sediment (Valiela et al., 1992; Bierzychudek et
al., 1993; McGlathery et al., 1997) and may thereby
limit phytoplankton growth (Thybo-Christesen et al.,
1993). This may be important at some times of the year
Fig. 3. Seasonal sediment±water column ¯uxes of dissolved organic (DON) and inorganic nitrogen (DIN) at the mid-lagoon Shoal 1 site in Hog
Island Bay. Shoal 2 ¯uxes are shown for July 1998 only. Positive values indicate ¯uxes out of the sediment.
100
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
in Hog Island Bay; however, it appears that in the midlagoon, the downward di€usion of DIN is a more
important process that may be limited by macroalgae
resting on the sediment surface.
Macroalgae decompose rapidly, especially compared
to vascular plant detritus, and the labile fractions disappear within days to weeks (Buchsbaum et al., 1991;
Enriquez et al., 1993). Given the biomass of macroalgae
measured at Shoal 2 in July 1998 we would predict
that the bloom would disappear in roughly 7±10 days.
Macroalgal-dominated systems, like Hog Island Bay,
are subject to periodic inputs of large quantities of labile
organic matter when algae die and decompose. There
was a release of signi®cant quantities of DIN and DON
following the crash of macroalgal blooms at certain
locations in Hog Island Bay during the summer of 1998.
At this time there was a subsequent temporary increase
in phytoplankton biomass. The macroalgal die-o€ also
resulted in accelerated nutrient cycling (Buchsbaum et
al., 1991; Duarte, 1995) and a sudden increase in oxygen
demand (Valiela et al., 1992; Duarte; Varioli et al.,
1995). Both during and after the bloom, there were
major die-o€s of the benthic invertebrate populations,
including several species of crabs and worms, due to
bottom anoxia. However, these large macroalgal mats
are patchily distributed within the lagoon, and the massive pulses of N may only have localized e€ects.
In summary this study provided compelling evidence
that the macroalgal community in¯uences the N budget
of the Hog Island Bay ecosystem. Similar results have
been obtained in studies dealing with phytoplankton in
near-shore marine environments (e.g. Philippart et al.,
2000).
4. Case study 3 Ð variations in biomass distribution
among benthic and pelagic producers in a tropical
reservoir (Lake Brobo, West Africa)
(beginning of the rainy season, July 1997; middle dry
season, March 1998; after a short ¯ood event, June
1998; and end of the rainy season, September 1998).
Biomass per unit area or volume was extrapolated to
whole-lake amounts (tons of C) based on measured
areas of cover (plants and attached algae) and lake
volume (phytoplankton).
In July 1997, vascular plants (P. octandrus) were the
most abundant autotrophs (3.5 of a total of 6.4 metric
tons C). Phytoplankton and epipelon accounted for 1.2
and 1.6 tons C, respectively, while epiphyton and epixylon each accounted for less than 0.03 tons C (Fig. 4).
At this time, water levels were sucient to permit a
relatively extensive growth of plants.
In the subsequent months water levels rapidly
declined and vascular plants were progressively stranded on the lakeshore until a total die-o€ had occurred
by March. The failure of plants to colonize deeper
regions of the lake during this drought year is thought
to be due to the rapid decline in lake water level. P.
octandrus has a poor ability to expand laterally, a feature that is common to other tropical macrophytes
(Talling and Lemoalle, 1998).
After the die-o€ of vascular plants, the concentration
of phytoplankton chlorophyll a increased from 18 to
>45 mg l 1. However, epipelon continued to account
for a greater portion of total autotrophic biomass (2.2
tons C) than phytoplankton (1.4 tons C). Only in June
1998, when a short ¯ood pulse resulted in sediment
resuspension and a more rapid development of phytoplankton than benthic algae, was this pattern changed
(epipelon 0.8 tons C; phytoplankton 1.0 tons C).
At least two possible explanations exist for the large
increase in phytoplankton after vascular plant die-o€.
First, it may be the case that the plants were suppressing the growth of phytoplankton by releasing allelopathic chemicals into the water. Previous studies (e.g.
Hootsmans and Blindow, 1994) have documented the
Freshwater lakes can be highly dynamic from the
standpoint of relative biomass of various autotrophs.
This variability, in turn, can in¯uence how the ecosystem responds to increased inputs of limiting nutrients.
The ®rst freshwater case study was conducted at Lake
Brobo, West Africa. This small (area=85 ha) reservoir
is eutrophic (phytoplankton chlorophyll a=10±20 mg
l 1) and shallow (mean depth=2.9 m), and it experiences yearly ¯uctuations in depth of up to 1.5 m. Secchi
transparencies vary from below 0.5 to near 2.0 m.
Five di€erent autotrophic compartments were examined: phytoplankton; epixylon (algae attached to ¯ooded trees); epiphyton (algae attached to vascular
plants); the host plant (Potamogeton octandrus); and
epipelon (micro-algae on the sediment surface). The
biomass was measured on four sampling dates that were
chosen according to the main hydrological events
Fig. 4. The biomass of three autotroph groups, vascular plants (hatched bars), epipelon (grey bars), and phytoplankton (black bars), in
Lake Brobo, West Africa, and corresponding changes in lake water
level (line).
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
production of allelopathic compounds by Potamogeton
pectinatus, as well as inhibitory e€ects of those
compounds on phytoplankton and other algae. This
explanation is consistent with the fact that there was very
little epiphyton growing on the plants in Lake Brobo. A
second explanation is that when dying plants release
soluble nutrients into the water (Kadlec, 1986) this fuels
the development of phytoplankton biomass (Schoenberg
and Oliver, 1988). There were not signi®cant increases in
soluble nutrients observed at the time of plant die-o€
(Thomas et al., 2000), but this may simply re¯ect the fact
that phytoplankton took up the nutrients as rapidly as
they became available. These alternative explanations
(and others, including changes in zooplankton grazing
pressure) only can be resolved by experimental research.
5. Case study 4 Ð P uptake by periphyton and
plankton in a shallow subtropical lake (Lake Okeechobee, USA)
As indicated in the previous case study and in a
number of published reports (e.g. Sand-Jensen and
Borum, 1991; Zimba, 1995; Lowe, 1996; Steinman et al.,
1997), shallow lakes can sometimes support a high biomass of epiphyton and epipelon. Where this occurs, the
lake's P cycle is likely to include a close coupling
between the attached algae and plankton (Wetzel,
1996). A number of studies have shown that co-occurring
freshwater attached algae and phytoplankton are limited by the same nutrient, which often is P (Barnese
and Schelske, 1994; Blumenshine et al., 1997). It has
been suggested that by removing P from the water column, epiphyton can suppress phytoplankton biomass
(Confer, 1974; Hansson, 1990; Sand-Jensen and Borum;
Kufel and Ozimek, 1994). Conversely, high densities
of phytoplankton sometimes can reduce light penetration so attached algae cannot achieve net growth
(Takamura et al., 1990). Given this knowledge, one
would expect that many studies have been done to
quantify inorganic and organic P cycling between
plankton and attached algae in shallow lakes. Remarkably, this is not the case.
This case study made quantitative estimates of the
P standing stocks and uptake of dissolved inorganic P
(PO4) and dissolved organic P (DOP) by co-occurring
natural phytoplankton, epiphyton, and epipelon in
shallow (<3 m), subtropical Lake Okeechobee, FL,
USA (Hwang et al., 1998; Havens et al., 2000).
The pelagic region of Lake Okeechobee (1400 km2)
is turbid and eutrophic due to high nutrient inputs from
non-point agricultural sources (Havens et al., 1996).
The near-shore zone supports a dense community of
submerged plants and periphyton when water levels
are relatively low (Phlips et al., 1993; Zimba, 1995;
Steinman et al., 1997), but it is phytoplankton domi-
101
nated when water levels are high. There also is a large
(400 km2) littoral zone of emergent plants along the
western shore of the lake. The interior part of the littoral zone is nutrient poor (Hwang et al., 1998), because
it is hydrologically uncoupled from the open-water zone
and its primary source of nutrients is rainfall.
This study considered P uptake by phytoplankton and
attached algae at one littoral site and two near-shore
sites. The emergent plant Eleocharis cellulosa (spike
rush) dominated the littoral site while the near-shore
sites were dominated by Scirpus californicus (giant bulrush). The plants provided a similar amount of surface
area for epiphyton colonization at the three sites.
The sites were sampled during seven, 2-week periods,
every 2 months between November 1995 and November
1996. Environmental conditions, including temperature
and irradiance pro®les, turbidity, and total P concentrations, were determined at each site. Triplicate
samples of plankton, epiphyton, and epipelon were collected and their P content determined on a volumetric
or areal basis. Phytoplankton and attached algal uptake
of PO4 and DOP were measured under near-ambient
conditions in custom-made incubation chambers in the
laboratory. Standard radio-tracer methods were used,
with carrier-free 32P-PO4 or 50 -[l32P]ATP serving as the
P sources. Methods are described in detail in Hwang et
al. (1998). All data regarding P standing stocks and ¯ux
rates were converted to a `whole community' level, with
units of mgP m 2 or mgP m 2 h 1 so that comparisons
could be made between locations and dates with di€erent water column depths.
At the near-shore sites, most of the community P
occurred in the water column, while at the marsh site,
over 75% of the P consistently occurred in the attached
periphyton community (epiphyton and epipelon combined). There was a positive curvilinear relationship
between the percent of community P in periphyton versus irradiance (Fig. 5, top panel), and a negative curvilinear relationship between percent periphyton P and
water column PO4 (Fig. 5, bottom panel). The relationship with irradiance is consistent with the predictions
stemming from the model of Sand-Jensen and Borum
(1991), and it indicates that with greater underwater
irradiance the role of periphyton increases not only in
terms of biomass, but also as a contributor to P
dynamics.
Uptake of PO4 and DOP by the plankton/periphyton
community did not vary signi®cantly among sites but it
did vary by season. In particular, when just the nearshore sites were considered, PO4 and DOP uptake rates
in November 1995±May 1996 (when irradiance was low)
were signi®cantly lower than those measured in July and
September 1996 (when irradiance was higher). Communities at locations and seasons with low water column
PO4 retained a much greater portion of the P that was
taken up than communities in PO4 replete conditions.
102
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
6. Synthesis
Fig. 5. Relationship between the relative contribution of periphyton
to total producer phosphorus storage versus irradiance at mid-depth
(top panel) and dissolved inorganic P (PO4) availability (bottom
panel) in Lake Okeechobee, Florida, USA.
The P-de®cient communities also made greater relative
use of DOP versus PO4 than the P-replete communities.
Taken together, these results indicate a use of alternative P sources and a tight recycling of sequestered P
when that element is scarce.
This study documents great variation in the nature
and degree of P cycling among plankton and periphyton
in a shallow lake/wetland ecosystem, and provides support for a conceptual model whereby P dynamics are
a€ected by irradiance. At near-shore sites that were
subjected to dramatic ¯uctuations in underwater irradiance, community P uptake was either: (1) strongly
suppressed, coincident with higher turbidity and lower
irradiance; or (2) very active, when irradiances are
increased. This seasonality brought about reciprocal
changes in the concentration of PO4 in the water column. At a protected site in the littoral wetland, with
high irradiance year-round, the community consistently
displayed active P uptake and low water column PO4.
Although we did not explicitly consider whether competition for P occurs between plankton and periphyton,
it appears that this might be the case, especially in the Pde®cient, high irradiance littoral wetland, where uptake
of PO4 and DOP by both plankton and periphyton was
high.
The dynamics of primary producer communities illustrated by the four case studies can be placed into a
broader context using a conceptual model (Fig. 6). For
simplicity, not all pathways are shown and consumers
are not included in the model. The case studies of Hog
Island Bay and Lake Okeechobee provided examples of
nutrient uptake from the water or sediments by phytoplankton, epiphyton, and benthic algae (arrows 1).
These autotrophs, along with vascular plants, also can
release soluble nutrients into the water column (arrows
2), especially during senescence. When they die, all of
the autotrophs contribute particulate organic nutrients
to the sediment pool (arrows 3). These nutrients may
be mineralized by microbial activity (arrow 4), and
there also are exchanges of dissolved nutrients between
sediment pore-water and particles, governed by chemical equilibria and a suite of other physical and chemical
processes (arrow 5; Hieltjes and Lijklema, 1980; Olila
and Reddy, 1997). As documented in the case study of
Waquoit Bay, macroalgae (and plankton) can inhibit
the growth of vascular plants by shading (arrow 6).
Furthermore, as suggested in Lake Brobo, vascular
plants might inhibit phytoplankton and epiphyton by
producing allelopathic chemicals (arrows 7).
This complex set of physical, chemical, and biological
interactions makes it considerably more challenging
to predict responses of shallow aquatic ecosystems to
nutrient stress than deeper systems where phytoplankton are the only autotrophs and where benthic±
pelagic coupling is of relatively low importance. Nevertheless, some general conclusions can be drawn from the
literature and the case studies presented as examples
here.
Sand-Jensen and Borum (1991, p. 154) concluded
``competition for light is probably the most important
factor for the balance among photoautotrophic communities.'' Those authors and Valiela et al. (1997a)
noted that reduced light availability generally is linked
with increased nutrient loading, because increased
nutrient availability stimulates the growth of certain
autotrophs (phytoplankton and macroalgal mats) that
reduce the amount of light reaching vascular plants. The
results from Waquoit Bay and Lake Okeechobee support this model. In the Bay, experimental nutrient
enrichment led to increased growth of macroalgae, and
declines in vascular plants due to extreme shading. In
the Lake, turbid nutrient-rich water resulted in a
reduced biomass and P content of epiphyton and epipelon, and only phytoplankton (in the mixed water column) experienced irradiances that supported net
growth. Although it was not observed here, high phytoplankton biomass itself can lead to reductions in light
availability and further declines in vascular plants and
attached algae. This phenomenon has been well docu-
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
103
Fig. 6. Major ecological interactions between macroalgae, phytoplankton, vascular plants, epiphyton, and benthic algae in shallow aquatic ecosystems. The numbered arrows are identi®ed in the text. Solid arrows indicate pathways of nutrient transfer. Other processes are indicated with dashed
arrows or lines. Not all pathways are shown and the model does not include consumers, which also can a€ect ecosystem nutrient dynamics.
mented in estuarine (e.g. MacIntyre and Cullen, 1996)
and lake systems (Sche€er et al., 1994).
Enhanced nutrient inputs tend to favor algae (phytoplankton and attached algae) over vascular plants
because algae obtain nutrients primarily from the water
column (Madden and Kemp, 1996). They have more
rapid rates of nutrient uptake and growth, and they also
have a lower compensation irradiance (1±10 mm photons
m 2 s 1 for algae, compared to 10±100 mm photons m 2
s 1 for vascular plants; Duarte, 1995; Valiela et al.,
1997a).
Phytoplankton become dominant when the water is
either too deep or too turbid to support submerged
vascular plants and attached algae, or when the rates of
nutrient loading are extremely high and residence time
of the water is long (Sand-Jensen and Borum, 1991;
MacIntyre and Cullen 1996; Valiela et al., 1997b). Phytoplankton blooms may be short-lived phenomena that
occur in response to seasonal in¯uxes of nutrients or
optimal environmental conditions (Paerl, 1988; Havens
et al., 1998). This is the situation observed in Lake
Brobo, where phytoplankton biomass rapidly increased
during a drought year when vascular plants died o€. In
some cases, phytoplankton blooms occur year-round
(e.g. Berger, 1989). Dense blooms of phytoplankton can
have dramatic e€ects on the other components of the
ecosystem and humans who utilize the water resource.
The algal taxa most often responsible for blooms
include species that can produce harmful toxins. In
freshwater systems, cyanobacterial toxins are the greatest concern (Paerl, 1988), while in estuaries toxic dino¯agellates are most problematic (Burkholder and
Glasgow, 1997). There also are impacts related simply
to their high biomass and eventual senescence of phytoplankton blooms. In eutrophic lakes with dense
blooms of cyanobacteria, there have been `summer
kills' of entire ®sh communities linked with sudden collapses of the blooms during one or two cloudy days
(Barica, 1978). During senescence of blooms, toxic substances such as ammonia can reach high concentrations,
killing ®sh and macro-invertebrates (e.g. Jones, 1987).
Macroalgae become dominant in nutrient-impacted
estuaries that have a shallow water column, relatively
short residence time, and a moderate to high rate of
nutrient loading (Valiela et al., 1997a). Blooms of macroalgae have dramatically di€erent impacts than phytoplankton. They most often are produced by ®lamentous
chlorophytes, and this group generally does not produce
104
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
toxins (Hay and Fenical, 1988). However, as Valiela et
al. noted, macroalgal blooms exert a variety of direct
and indirect ecosystem e€ects. Sand-Jensen and Borum
(1991) noted that light attenuation in a few centimeters
of dense periphyton exceed that occurring in an overlying meter of water. This e€ect was clearly illustrated
by the case study in Waquoit Bay.
When vascular plants decline, organisms that use
them as habitat also are a€ected. The loss of eelgrass
beds in coastal estuaries has been documented to alter
the abundance and composition of benthic fauna
(Valiela et al., 1992), including the loss of commercially
valuable winter ¯ounder (Heck et al., 1989), white hake
(Heck et al.), Atlantic cod (Gotceitas et al., 1997),
American lobster (Barshaw and Bryant-Rich, 1988),
and scallops (Eckman, 1987; Bricelj et al., 1991) that
utilize eelgrass habitat during early stages of their life
history.
In the case study of Hog Island Bay, macroalgae also
in¯uenced the transfer of nutrients between the sediments and water column. Valiela et al. (1997a) noted
that in systems polluted by excessive levels of nutrients,
macroalgae take up `new' nutrients from the water and
`old' nutrients that are regenerated in the sediments
during microbial decomposition. The result is an
uncoupling of the biogeochemical cycling between the
sediments and the water column (Thybo-Christesen et
al., 1993; McGlathery et al., 1997) which may suppress
phytoplankton growth. However, low light can reduce
nutrient uptake and cause release of nutrients to the
water column (McGlathery et al.). Self-shading and
increased temperature can cause a seasonal collapse of
the mat and release huge amounts of nutrients into the
water column, as in Hog Island Bay during the summer
of 1998. This can result in short-lived phytoplankton
blooms (Sfriso et al., 1992; Valiela et al., 1992). Because
macroalgae can sequester large amounts of nutrients,
water quality (in terms of nutrient concentrations and
transparency) in macroalgal-dominated systems will
tend to be considerably better than in deeper, phytoplankton-dominated systems with the same rate of
external nutrient inputs (Valiela et al., 1997a).
The e€ects of macroalgal blooms may be very longlived relative to phytoplankton blooms. Valiela et
al. (1997a, p. 1106) noted that seaweed blooms ``may
remain in an environment for years to decades'', and
gave as an example a bloom of Cladophora in an Australian estuary that persisted for 12 years. Valiela et al.
(1992) reported that the Cladophora and Gracilaria
blooms in Waquoit Bay have been present for more
than 20 years. The highly eutrophic lagoon of Venice
(Italy) has been dominated most of the time by blooms
of Ulva, with only periodic dominance by phytoplankton (Sfriso et al., 1992). Valiela et al. (1997a)
noted that nutrient enrichment has been implicated in
the start of virtually every macroalgal bloom.
7. Conclusion
According to published models (Sand-Jensen and
Borum, 1991; Duarte, 1995; Valiela et al., 1997a),
increased loading of nutrients to freshwater and marine
ecosystems can bring about a transition from vascular
plant to algal dominance. Microalgae (phytoplankton
and attached algae) have higher nutrient uptake rates
than macroalgae, which in turn have higher rates than
freshwater and marine angiosperms. With increased
growth of phytoplankton and macroalgae there is a
reduction in light penetration and this causes a decline
of angiosperms. At the highest rates of nutrient loading,
phytoplankton biomass becomes so high that no other
autotrophs can maintain net growth. The results from
the four case studies presented here provide support for
this model. When macroalgal mats were experimentally
increased in Waquoit Bay, there were dramatic declines
in eelgrass production. When P concentrations
increased in Lake Okeechobee, there was increased
phytoplankton, reduced underwater irradiance, and
reduced periphyton. The results also indicated other
complex interactions that might in¯uence how a particular ecosystem responds to nutrient stress. In Hog
Island Bay, dense macroalgal lawns substantially
reduced the export of N from sediments to the water
column during the growing season, and this could
negatively in¯uence phytoplankton. In Lake Brobo,
angiosperms may have produced allelopathic chemicals
that suppressed phytoplankton production. Hence,
phytoplankton only increased in biomass after a major
plant die-o€. Alternatively, the dying plants may have
released nutrients that stimulated phytoplankton
growth.
One factor not explicitly considered here is the role of
grazing by herbivores in e€ecting the responses of autotrophs to nutrient enrichment. Complex trophic interactions in freshwater ecosystems are becoming increasingly
understood since the publication of seminal research in
the late 1980s (Carpenter et al., 1985, 1987). However,
our understanding of such interactions in marine ecosystems is less well developed. Worm et al. (2000, p. 339)
recently emphasized the important role of grazers in
coastal ecosystems, noting that they can ``bu€er moderate eutrophication e€ects''. A number of other recent
studies have documented interactive e€ects between grazers, nutrients, and benthic algal production. An understanding of these complex interactions clearly is
important to successful eutrophication management.
Acknowledgments
The Hog Island Bay research was supported by
The Virginia Coast Reserve LTER Project and an
additional award to Karen McGlathery (National
K.E. Havens et al. / Environmental Pollution 113 (2001) 95±107
Science Foundation award numbers DEB-9411974 and
DEB-9805928, respectively). The research on Waquoit
Bay was supported by a National Estuarine Research
Reserve Graduate Research Fellowship from the
National Oceanic and Atmospheric Administration
(award number NA77OR0228) and a United States
Environmental Protection Agency STAR Fellowship
for Graduate Environmental Study (U-915335-01-0)
awarded to Jennifer Hauxwell. The Quebec-Labrador
Foundation Atlantic Center and Environment's Sounds
Conservancy Program also provided supporting funds.
David Giehtbrock and Gabrielle Tomasky provided
technical assistance in the project. The South Florida
Water Management District and the Center for Environmental Studies, Florida Atlantic University, supported the research on Lake Okeechobee. Therese East,
Andrew Rodusky, and Bruce Sharfstein provided technical assistance. The research on Lake Brobo was
supported by the Institut de Recherche pour le Development as part of the program Petits-Barrages. The
authors are grateful to Peter Doering, Susan Gray, R.
Thomas James, Val Smith, and one anonymous
reviewer for providing comments on an earlier draft of
the paper.
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