MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 204: 27–38, 2000 Published October 5
INTRODUCTION
The structure of plant assemblages is generally
thought to be regulated by the interplay of consumers,
resources and abiotic factors. Although benthic
microalgae can have a pivotal role as primary produc-
ers in littoral communities (Daehnick et al. 1992, Pinck-
ney & Zingmarck 1993), the factors affecting microal-
gal community structure and diversity remain poorly
studied in comparison to pelagic microalgae (Hille-
brand & Sommer 1997). Herbivory on epilithic microal-
gae has been studied sporadically in the marine envi-
ronment (Castenholtz 1961, Nicotri 1977, Hunter &
Russell-Hunter 1983, Sommer 1997, 1999a). These
experiments indicated potentially predominant top-
down control and differential influence of different
types of herbivores on species composition and vertical
structure of the algae. On the other hand, recent stud-
ies have demonstrated pronounced nutrient limitation
in marine microphytobenthos and strong effects of
experimental nutrient enrichment on species composi-
tion and diversity (Sundbäck & Snoeijs 1991, Hille-
brand & Sommer 1997). The relative influence of nutri-
ent and grazing effects on these communities has not
yet been simultaneously assessed in marine environ-
ments.
© Inter-Research 2000
*Present address: Erken Laboratory, University of Uppsala,
Norr Malma 4200, 76173 Norrtälje, Sweden.
E-mail: helmut.hillebrand@ebc.uu.se
Marine microbenthic community structure
regulated by nitrogen loading and grazing
pressure
Helmut Hillebrand
*
, Boris Worm, Heike K. Lotze
Institut für Meereskunde, Abteilung Meeresbotanik, Düsternbrooker Weg 20, 24105 Kiel, Germany
ABSTRACT: Generalisations on the combined effects of consumers and resources on autotrophs in
aquatic food webs largely rely on freshwater studies. In this study, we tested these general concepts
with marine benthic microalgae, which are important components of coastal food webs. We manipu-
lated nitrogen availability and herbivore presence in a factorial field experiment in the Western Baltic
Sea. Moreover, we investigated how herbivore control varied among 3 sites and 2 seasons and tested
for trophic cascades by enhancing demersal fish density at 2 sites. Nitrogen availability and herbivore
presence had strong and antagonistic effects on microalgal biomass, species composition and diver-
sity. Herbivores significantly reduced algal biomass, whereas nutrient enrichment led to an increase
in biomass. Herbivore effects on microalgal biomass increased with increasing nitrogen availability,
indicating a functional response of herbivores to nutrient enrichment. The response of microalgae at
the species level suggested a trade-off between nutrient use and grazing resistance which appeared
to be linked to algal growth form. Compared to other growth forms, large erect species were most
responsive to both nitrogen loading and herbivory. Grazing reduced microalgal diversity at low nutri-
ent supply, but enhanced it at high nutrient supply. Herbivore effects varied considerably among dif-
ferent sites and were stronger in spring than in summer. Manipulations of fish density during sum-
mer did not have any effects on microalgal community structure. In conclusion, our results
demonstrate that herbivores and nutrients have strong and balancing effects on marine microbenthic
community structure.
KEY WORDS: Periphyton · Herbivory · Species composition · Nutrients · Diversity
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Mar Ecol Prog Ser 204: 27–38, 2000
This scarcity of studies is contrasted by the thorough
investigation of grazing effects on stream periphyton
(reviewed by Steinman 1996). According to such stud-
ies, herbivores at natural densities can strongly reduce
algal biomass (Hill & Knight 1987, Steinman et al.
1987), change the physiognomy of the community by
removing their upper layers (Lowe & Hunter 1988,
Steinman et al. 1991), and influence successional pat-
terns (Tuchman & Stevenson 1991). Simultaneous
manipulation of nutrient supply and grazing revealed
strongest effects on freshwater periphyton (Marks &
Lowe 1989, Rosemond 1993, Rosemond et al. 1993).
However, it remains unresolved if conclusions derived
from streams, which are characterised by a unique
matrix of habitat constraints (Biggs et al. 1998), can be
transferred to the marine microbenthos.
Within the context of a broader study of grazer-
macrophyte-nutrient interactions (Lotze 1998, Worm et
al. 1999, 2000a, Lotze et al. 2000), we investigated the
effect of grazing and nutrient enrichment on benthic
microalgae in a factorial field experiment. We tested
the following hypotheses: (1) Herbivores and nitrogen
availability antagonistically control the biomass of
epilithic microalgae, (2) Herbivores and nitrogen exert
selective control by preferentially removing or favour-
ing certain species or growth types, (3) The grazing
effect differs on small temporal and spatial scales, and
(4) The impact of herbivores on microphytobenthos is
influenced by fish predation on herbivores (trophic
cascade).
We conducted 3 field experiments to test these hy-
potheses. For Hypotheses 1 and 2, nutrient supply and
grazer presence were experimentally manipulated at 1
site (nutrient × grazing experiment). For Hypothesis 3,
grazer presence was manipulated at 3 similar sites
(spring grazing experiment). For Hypothesis 4, fish
density was experimentally increased (summer graz-
ing experiment). Combining all experimental results
for 1 site allowed us to analyse the temporal shifts in
grazing effects (Hypothesis 3).
METHODS
Study site. The main study site was located at
Maasholm, a sheltered broadening of the Schlei
Fjord, Western Baltic Sea (54° 41’ N, 10° 00’ E). The
Schlei Fjord is a tideless, inshore water-system of
glacial origin. Salinity ranges from 12 to 18 PSU in
summer and 14 to 20 PSU in winter. Water tempera-
ture ranges from –1 to 2°C in winter and 16 to 25°C
in summer. Nutrient concentrations at Maasholm
reach up to 160 µmol l
–1
nitrate, 12 µmol l
–1
ammo-
nium and 2 µmol l
–1
phosphate from January to
March (Schramm et al. 1996). From mid-May to mid-
August, ammonium and nitrate are largely depleted
and typically remain close to the detection limit (0.0
to 0.3 µmol l
–1
), whereas soluble reactive phosphate
remains between 0.1 and 0.6 µmol l
–1
. The site is
dominated by sandy substrata, with abundant rocks
and boulders that sustain a community of epilithic
macro- and microalgae, dominated by the large
brown alga Fucus vesiculosus. Crustacean and gas-
tropod grazers are abundant (Table 1), larger herbi-
vores (urchins, limpets, fish) are absent because of
the reduced salinity level of the Baltic Sea.
Nutrient × grazing experiment. We tested the effects
of nutrient enrichment and grazing on biomass and
species composition of benthic microalgae in a factor-
ial field experiment in May 1998, since benthic
microalgae in the Baltic Sea reach their seasonal max-
imum biomass during spring. All experiments were
conducted in the shallow subtidal zone at 0.6 to 0.8 m
water depth.
The presence of gastropod and crustacean grazers
was manipulated with exclusion cages (25 × 25 ×
25 cm), covered with a clear 1 mm polyethylene mesh
28
Experiment Grazer species Mean (SE)
Site
Nutrient × grazing
Maasholm Littorina saxatilis 4031 (408)
Littorina littorea 0 (0)
Hydrobia ulvae 200 (45)
Idotea spp. 25 (11)
Gammarus spp. 0 (0)
Other 10 (5)
Spring grazing
Maasholm Littorina saxatilis 1104 (370)
Littorina littorea 41 (17)
Idotea spp. 444 (96)
Gammarus spp. 124 (25)
Wackerballig Littorina saxatilis 0 (0)
Littorina littorea 235 (43)
Idotea spp. 115 (56)
Gammarus spp. 56 (31)
Geltinger Noor Littorina saxatilis 325 (119)
Littorina littorea 10 (4)
Idotea spp. 35 (10)
Gammarus spp. 13 (7)
Summer grazing
Maasholm Littorina saxatilis 63 (24)
Hydrobia ulvae 312 (57)
Idotea spp. 13 (9)
Geltinger Noor No data
Table 1. Background data on grazer densities (individuals m
–2
)
in field experiments. Grazer densities were evaluated within
control plots (nutrient × grazing experiment and summer
grazing experiment, n = 16) or by using 25 × 25 cm frames
(spring grazing experiment, n = 10). Idotea spp. are I. baltica
and I. chelipes; Gammarus spp. are G. locusta, G. salinus
and G. zaddachi