A Competitive Hierarchy Model Integrating Roles of Physiological Competence
and Competitive Ability Does Not Provide a Mechanistic Explanation for the
Zonation of Three Intertidal Fucus Species in Europe
Rolf Karez; Anthony R. O. Chapman
Oikos, Vol. 81, No. 3. (Apr., 1998), pp. 471-494.
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Tue Dec 11 12:51:02 2007
OlKOS
81: 471-494.
Copenhagen
1998
A
competitive hierarchy model integrating roles of physiological
competence and competitive ability does not provide a mechanistic
explanation for the zonation of three intertidal
Fucus
species in Europe
Rolf Karez and Anthony
R.
0.
Chapman
Karcz,
R.
and Chapman, A.
R.
0. 1998. A competitive hierarchy model integrating
roles of physiological competence and competitive ability does not provide a mecha-
nistic explanation for the zonation of three intertidal
Fucus
species in Europe.
-
Oikos 81: 371 394.
It has been clear for the last 20 yr that both competitive ability and physiological
competence on the intertidal gradient of rocky shores determine the zoned distribu-
tion of fucoid seaweeds in the North Atlantic. However to this point. there has been
no concept integrating these functions for seaweed vegetation in a single mechanistic
explanation. Keddy's competitive hierarchy model, which has not been tested in
marine systems
(i.e. not on seaweed vegetation) provides an explanation for the
zonation of plant species on environmental gradients. The model proposes that
competitive abilities of spccies on a stress or resource gradient are inversely related to
fundamental niche breadths. We tested
2
assumptions of the model to detem~ine
whether it provided
a
comprehensive explanation of zonation of 3
Fttcus
species on
the island of Helgoland in the North Sea. The
2
assumptions translate into specific
predictions for the
Fticzrs
assemblage (where
F.
srrrurus
occurs on the low shore.
F.
spiraiis
on the high shore. and
F.
t.c~siculu.sus
in between): I. competitive ranking is
F.
srrratu5
>
F.
cesiculosus
>
F. spirali.~:
2.
fundamental niche breadth rankings are the
reverse of cornpctitive ability rankings. Pairwise competition experiments were done
in the field. A highly modified substitutive design was used, in order to take into
account the shortcomings of this approach. The empirically
deri~ed competitive
hierarchy did not fit prediction 1. Transplant experiments with adults and juveniles
provided results contrary to prediction
2.
Since none of the assumptions of the model
fit. it cannot be used to provide a mechanistic explanation for the zonation
of
FU(.US
species
011
Helgoland. Unlike other inlportant models of competition, Keddy's
approach does not claim universal validity in all communities. This means that it
requires empirical testing in each species
assemblage.
and more importantly. that the
negative outcome reported here does not invalidate the concept in general.
R.
Kure:. Ahreilung Aleeresbofmrik.
Illst.
jZr ~%leereskcrrzde,Diisternhrooker Weg
20.
0-24105
Kiel, Gertr~rmnj.
(rknre~@ifi?~.~mi-h-if1.h).
A.
0.
Clinpr~ian. Depr
qf
-
R.
Biologj,, Dtrlliotrsie (Itiit.., Hulifcis.
.VS.
Canatla
5-31?
451.
One of the steepest environmental gradients for plants
marshes has mixed terrestrial and marine origins, and
occurs at the interface between land and sea. In the
for the two components. the landward and seaward
North Atlantic Ocean, in areas removed from human
ends of the gradient represent different poles of
physio-
engineering influence, salt marshes tend to dominate the
logical stress. However. on rocky shores of the North
intertidal gradient on soft sediments. The flora of
Atlantic. this level of complexity is reduced because the
Accepted 11 September 1997
Copyrtght
d
OIKOS 1998
lSSN 0030-1299
Prtnted In l~eland
-
all r~ghts reserved
vegetation consists of seaweeds with a marine origin for
which terrestrial conditions become increasingly more
stressful landwards. On this tidal gradient, there is a
very obvious zonation of algal species (Stephenson and
Stephenson 1972), and, in the boreal waters of the
North Atlantic. fucoids (division Heterokontophyta:
order Fucales) are often dominant in
terms of total
biomass. There are 6 species of fucoids in these waters,
and they have been the subject of intensive ecological
investigation (reviewed by Chapman 1995). This paper
is concerned with 3 common species of
Fzicus
L.
occur-
ring in Europe. Where there is a closed vegetation,
FZICIISserratus
L..
F. cesiculosi/s
L.
and
F.
spira1i.s
L.
frequently occur in consecutive, contiguous zones be-
tween the tide marks from sea to land. Seaweeds other
than fucoids and species of fucoids other than the
3
above may form zones, but these are not of concern
here. It is quite clear that the formation of zones by the
3 species under consideration is under the dual control
of varying physiological competences and competitive
interactions along the intertidal gradient (reviewed by
Chapman 1986. 1995). The gradient encompasses
changes in resources
(e.g. dissolved minerals [Schon-
beck and Norton 1979a. Hurd and Dring 19901) and
also in stresses which cannot be considered resources
(e.g. temperature, Davison et al. 1989). The
3
species of
fucoids which occur on different parts of the gradient
have different physiological competences in the face of
changing stresses landwards. Drought tolerance of the
photosynthetic machinery of
F.
serrutus
is reduced in
relation to
F. cesiculosus,
which is, in turn, reduced
below that of
F.
spiralis
(Dring and Brown 1982).
F.
spiralis
is much more tolerant of freezing than low-
shore species (Pearson and Davison 1993). This same
species has enhanced phosphorus uptake capability in
comparison with
F.
resiculosus,
which. in turn, sur-
passes
F. serratus
(Hurd and Dring 1990). Fucoids
obtain all of their phosphorus during immersion, and,
landwards, the time of immersion is diminished up to
5-fold through the portion of the gradient occupied by
the three species. In all of these cases, it is the landward
borders of the species
that are related to the limits of
physiological competences. Furthermore, at least in
special circumstances, seaward borders may be physio-
logically determined. Dring (1987) showed that, in the
turbid
waters of the Bristol Channel in England, the
lower boundary of
F. serratus
is likely determined by
inadequate light availability for photosynthesis. In the
subtidal populations of
Fucus
occurring in the Baltic
Sea, light penetration may well regulate the depth of
the downslope boundary (Kautsky et al. 1986).
There is also evidence that competition among the
Fucla
species plays a major role in the formation of
zones. Both upper and lower bounds of fucoids may be
controlled by competition. In a rather simple experi-
mental design, Hawkins and Hartnoll (1985) and
Hawkins and Harkin (1985) demonstrated that the
seaward boundaries of the 3 European
F~~cus
species
under consideration could be disrupted by removing the
canopy occupants. Hence. downslope boundaries were
influenced by competitive interaction. Upslope migra-
tions indicated that competition has a similar role in
setting upper boundaries for some species pairs. Fur-
ther cases are reviewed by Chapman (1986, 1995).
Simply identifying physiological competence and
competitive ability as determinants of zonation does
little to provide an explanatory mechanism which inte-
grates the two. However, Chapman (1995) recognized,
retroactively, that there was an appropriate integrating
model (Keddy
1989a). He attempted to apply the re-
sults of earlier experiments, not done specifically with
model assumptions in mind, to explain the zonation of
Fucus
species of eastern Canada. The experimental
results did not fit model assumptions, but the designs of
the tests used by Chapman (1995) are not considered as
appropriate here. For
example, a replacement series
design (a substitutive model) was used to test competi-
tive ability without taking into account all of the short-
comings of such a design. For this reason. we began a
study to test whether Keddy's
(1989a) model (Fig. 1)
could provide a mechanistic explanation (which inte-
grates the roles of competition and physiological com-
petence) for the phenomenon of fucoid zonation in the
intertidal zone of the island of Helgoland in the North
Sea.
According to Keddy's
(1989a) model (Fig. 1). plant
species which are zoned on an environmental gradient
may have overlapping fundamental niche breadths (i.e.
portions of the gradient in which species are able to
exist in the absence of interspecific competition). so that
all species are able to exist (physiologically) at the
benign end of the gradient. The species which occupies
space at this benign end of the gradient is the top
competitor which displaces other species to positions
higher on the gradient. The top competitor cannot
survive conditions outside its realized distribution. The
species which occurs in the zone contiguous with that
of the top competitor is the second most effective
competitor. This second-ranking species displaces all
other species (except the top competitor) to positions
higher up the gradient where it is unable to exist. These
relationships continue on down through the hierarchy
to the worst competitor which is displaced to the
highest position on the gradient where physiological
conditions are least benign. There may be a strategic
resource allocation trade-off between competitive abil-
ity and tolerance of stress at the less benign end of the
gradient, but this is not known with certainty for any
single seaweed species.
The essence of Keddy's
(1989a) model can be found
in its
3
assumptions: 1. "[Ilt is assumed that the species
in the community have inclusive niches: i.e. the gradient
is a gradient of resource quantity. with all species
having best performance (size; growth rate and
repro-
- -
-
Fig.
1.
Two models explaining
a)
species distribution along
field observation
=
realized niches
resource gradients. a) Upper
graph: physiological response
curves of
4
species realized in
the field. Removal of
neighbours may lead to the
pattern explained by niche
differentiation (lower left) or
by the competitive hierarchy
hypothesis (lower right).
b)
Fundamental and realized
niches of the models on the
same resource gradient.
\
competitive hierarchy
Modified after Keddy (1989a).
niche
b)
niche differentiation
competitive hierarchy
fundamental niches fundamental niches
realized niches
realized niches
ductive output) at the same end of the gradient."
2.
"[Tlhe species vary in competitive ability in a pre-
dictable manner and [...I competitive ability is an inher-
ent characteristic of a species. perhaps having
something to do with rates of resource acquisition and
capacity to interfere with neighbours."
3.
"[Clompeti-
tive abilities are negatively correlated with fundamental
niche width, perhaps because of an inherent trade-off
between ability for interference competition and ability
to tolerate low resource levels.".
The model assumptions indicate explicitly that the
gradient is a resource gradient, but Keddy (1989a: p.
73) made it clear that it is also applicable to an environ-
mental gradient. Keddy's model may be tested in a
straightforward manner: zoned species along a gradient
should show transitive ranks in their competitive abili-
ties and. in reverse order, in the widths of their funda-
mental niches. According to the second of Keddy's
assumptions these ranks should be consistent among
different environmental conditions (environments).
Keddy and his co-workers provided much evidence for
the competitive hierarchy hypothesis from their own
work. In most cases. the surveyed gradient was parallel
to the shoreline of Canadian lakes. Gradients mediated
by wave exposure exist between sheltered bays with rich
organic content, high soil nutrient levels (=low stress
sensu Grime
1974), high plant biomass and low distur-
bance, and exposed sites with infertile soils of coarser
grain structure, low plant biomass, with high levels of
stress and disturbance (Keddy 1984, Wilson and Keddy
1985, 1986a, b). It should be noted that this gradient is
a very complex one. However, even on gradients of, for
example, only one mineral nutrient, interactions with
other factors (ion balances) may produce complex gra-
dients (Austin and Austin 1980).
In his studies with lakeshore plant communities,
Keddy (1984) found no evidence that niche differentia-
tion (Fig. l) led to species' coexistence. He found that
most species had highest biomasses at the same (high
fertility) end of the gradient (Wilson and Keddy 1985),
that the competitive abilities of species from the high
fertility end were highest (Wilson and Keddy 1986'0)
and that diffuse competition was greatest there (Wilson
and Keddy 1986a). In the following years, Keddy found
that plant biomass (and height) is a trait that often
explains competitive dominance (Gaudet and Keddy
1988, Keddy
1989b). He came to the conviction that in
plant communities consistent hierarchies of competitive
ability prevail (Keddy and Shipley 1989, Shipley 1993.
Shipley and Keddy 1994) rather than intransitive net-
works as known from, for example, bryozoan assem-
blages (e.g. Buss and Jackson 1979. Karlson and
Jackson 1981. Russ 1982). For hierarchies to develop.
competitive interactions have to be asymmetric (Keddy
and
Shipley 1989. Shipley and Keddy 1994). Keddy et
al. (1994) partly confirmed that hierarchies of competi-
tive effects (sensu
Goldberg 1990) were mostly consis-
tent between different environments. although in single
species pairs there were some reversals. Recently,
Keddy recommended looking for general patterns of
plant traits rather than compiling more and
more single
species pairs observations (Keddy 1992). and he co-
operated in an intercontinental experiment designed to
test the assumption that competitive intensity increases
with habitat productivity. Only partial supporting evi-
dence could be found (Reader et al. 1994).
The assumptions of Keddy's
(1989a) model may be
used to formulate testable hypotheses: 1. The competi-
tive ranking of the 3
Fucus
species on Helgoland is:
F.
.serratu.r
>
F.
resiculosus
>
F. .spirali.s:
2. The fundamen-
tal niche breadth rankings are:
F. .serratus
<
F,
ce.riculo-
.sus
<
F. .spiralis.
Competitive ranks were tested in a highly modified
replacement series design deployed in field experiments.
Fundamental niche breadths were tested in transplant
experiments in the absence of "alien" competitors.
Materials and methods
Description of the study site
The study was done on the sandstone north-east shore
of the island of Helgoland in the North Sea (54'1
1'N.
7"53'E). This shore is known locally as the "Nordost-
Felswatt". and will be referred to hereafter as the
"NE-Intertidal". From a high cliff close to shore, a flat
rocky terrace extends
seawards horizontally
>
300 m
from mean high water to mean low water, with a
difference in vertical level of 2.4 m (Janke 1990). Thus,
the mean angle of gradient is less than 0.5". Along the
whole stretch.
the NE-Intertidal is sheltered from west-
erly storms by a seawall ("N-Mole").
A pattern of grooves in the bedrock distorts the
normal zonation, leading to two tidal gradients: a large
scale gradient along the land-sea axis and a small scale
gradient. right-angled to the former. Only zonation
patterns of the most conspicuous macroalgae along the
large scale gradient will be considered here.
On the lower shore, there is a dense canopy of
Fuci~s
serratus
(leaf area index
>>
I)
which becomes more scat-
tered with a lower cover landwards. Dense patches of
Myti1~t.s edulis L.
populate the tops of the sandstone
slabs.
F.
r~esic~~1osu.s
alone or together with
F. serratus
builds patches of sparse canopies. In the uppermost
zone of the main NE-Intertidal. plateaux of rocks more
recently fallen from the cliff are often populated by a
dense mixed canopy. mostly of
F. aesiculosus
and
F.
spiralis
and, in a few cases,
F. serratus.
The area
surrounding these boulders is populated from ca March
to September by dense stands of green ephemeral algae.
mainly
Enteromorpha
Link in Nees species (Janke
1986).
F.
spiralis
forms a distinct zone on large concrete
blocks of the eastward extents of the NE-Intertidal. The
typical zonation pattern of
Fucus
spp. (landwards
F.
.serrutus-F. ~~esiculosus-F. .spiralis),
conspicuous on
most of Helgoland's seawalls. and the main subject of
this study, is not clearly discernible in the main
NE-
Intertidal.
The grazer guild consists mainly of
Littorina
L.
spp.
and small crustaceans, while limpets, a major structur-
ing force on e.g. many British coasts (Southward and
Southward 1978. Hawkins 1981). are absent from the
Helgoland intertidal.
More comprehensive descriptions of the distribution
of Helgoland's intertidal species are given by
Markham
and Munda (1980), Janke (1986) and some of the
studies summarized by Harms (1993).
Competition
Crnsztses of tlutural
Fucus
gernzling dmsit), in the
Helgolarzd intrrtidc~l zone
Censuses in the Helgoland intertidal zone of subjec-
tively "dense" stands of
Fucus
spp. were done in or-
der to estimate appropriate experimental densities. In
July 1993. numbers were assigned to 20 patches of
Fzrcus
germlings distributed across the fucoid belt.
Seven of them were chosen
randomly and algae from
5 small areas (5
x
5 cm. coordinates with random
number tables) of each were scraped from the rock
and brought to the laboratory. Densities of samples
and size class frequency distributions from subsamples
were estimated. Patches of
Fucus spiralis
juveniles (1-
2 cm length) occurred at densities up to 70 000
shoots m'. Since the experimental size of fucoids was
to be 1.0-1.5 cm, this density was considered to be
the approximate natural (maximum) density, although
only
F. spira1i.s
seems to establish such dense stands
of juveniles (pers. obs. and see Schonbeck and Nor-
ton
1979b: but see Creed et al.
1996 for similar data
on
F, .serrntus).
Replacet7zent series esprrinzent
For experimental examination of competition. the re-
placement series design (de Wit 1960) was used. Here,
the original design was extended by using 3 replacement
series with 3 total densities. Densities of low
=
10 000.
medium
=
50 000 and high
=
100 000 shootslm"ere
chosen for the experiment so that the highest field
density for fucoid germlings of the experimental size
