Patterns in Species Diversity during Succession of Coastal Dunes
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Patterns in Species Diversity during Succession of Coastal DunesAuthor(s): Maike IsermannSource: Journal of Coastal Research, 27(4):661-671. 2011.Published By: Coastal Education and Research FoundationDOI: http://dx.doi.org/10.2112/JCOASTRES-D-09-00040.1URL: http://www.bioone.org/doi/full/10.2112/JCOASTRES-D-09-00040.1
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Patterns in Species Diversity during Succession ofCoastal Dunes
Vegetation Ecology and Conservation BiologyBremen UniversityLeobener Strasse, 28359 Bremen, Germanymaike.firstname.lastname@example.org
ISERMANN, M., 2011. Patterns in species diversity during succession of coastal dunes. Journal of Coastal Research,27(4), 661671. West Palm Beach (Florida), ISSN 0749-0208.
The humped-back relationship in species diversity during succession was tested using vegetation in a coastal sand dunesystem of the German Wadden Sea island of Spiekeroog. Permanent plots were studied over 15 years along a spatialchronosequence from young grey dunes to old brown dunes. Species diversity, succession rate, and environmentalindicator value were used to evaluate multitemporal dynamics of the ecosystem. Long-term development of the dunevegetation was reflected along the chronosequence, whereas fluctuations of plant communities were analyzed by short-term changes of each permanent plot.
The study confirmed the intermediate stress theory, whereas highest species diversity was reached at the transitionzone of the environmental gradients. Total species richness showed humped-back relations along the xerosere. Hotspotsin species diversity varied with the life form group. Highest richness of herbaceous plants was reached in semidynamicyoung grey dunes, whereas highest richness of bryophytes and lichens shifted due to competition effects to the driestparts of the dune gradient in older successional stages.
Moreover, the study confirmed the biodiversity-stability theory, with highest ecosystem stability at highest diversity.More stable environments showed lower succession rates than dynamic, disturbed environments. Thus, duringsecondary succession with probably repeated disturbance, the succession rate was higher and no clear direction ofvegetation development was found in comparison to primary succession. The succession rate in a primary seriesrepresented a unimodal relation with total species richness. Thus, species-poor vegetation often dominated by onespecies, such as heathlands, as well as species-rich vegetation, showed lowest succession rates. These communitiesprobably are more stable due to a balanced species combination represented by higher evenness.
ADDITIONAL INDEX WORDS: Chronosequence, fluctuation, permanent plot, succession rate, time series, vegetationdynamics.
Coastal dunes are one of the most vulnerable landscapes in
northwest Europe and include priority habitats, considering
the European Union Habitats and Species Directive. For
example, habitats with open, short, dry grasslands at the
mainland are often threatened due to agricultural use.
Furthermore, many coastal dune habitats contain rare species
and are species rich (Doody, 2001). In general, species diversity
depends on different ecological features like plant productivity
(Rosenzweig, 1995), which is often correlated with environ-
mental factors like soil pH (Isermann, 2005) and scale
dependent (Auerbach and Shmida, 1987). Relationships among
the changes of species diversity in the course of ecological
succession are different. General models of ecological succes-
sion predict an increase of species diversity with increasing age
Vegetation succession is affected by external and internal
factors (Bakker et al., 1996). External effects, like atmo-
spherically nutrient deposition, often give rise to various
internal developments, such as soil acidification. Vegetation
composition is also affected by various internal mechanisms,
like altered competition interactions, and shows a feedback
mechanism by the vegetation itself (Bakker et al., 1996).
Vegetation development is controlled by processes, which often
differ during primary and secondary succession (Austin, 1981).
Most sand dunes are spatial sequences representing chron-
ological series (Salisbury, 1952), because the spatial series of
dune ridges from the sea inland developed one after another. In
general, these chronosequences describe the formation and
development of vegetation and environmental factors of the
dunes (Cowles, 1899; Ranwell, 1960). Mechanisms of direc-
tional changes in species composition are governed by abiotic
factors; species interactions or spread of dominant plant
species retrospectively affects abiotic conditions. Long-term
vegetation changes in dunes are especially linked with the
development of the soil (Salisbury, 1925). Strong relationships
between plant communities and soil parameters, especially the
C:N ratio and soil pH, were shown, e.g., along a dune zonation
DOI: 10.2112/JCOASTRES-D-09-00040.1 received 12 April 2009;accepted in revision 2 December 2009.
Coastal Education & Research Foundation 2011
Journal of Coastal Research 27 4 661671 West Palm Beach, Florida July 2011
in Denmark (Frederiksen et al., 2006). Mechanisms determin-
ing dune plant patterns appear at both the individual and the
community level (Feagin et al., 2005), e.g., in changes of species
abundance and species composition of the plant community.
In view of their patterns of development, dunes are
particularly suitable for the study of the relationship between
succession and zonation (Johnson, 1997; Lichter, 1998).
Successional dynamics in vegetation have mostly been eval-
uated by using permanent plots and indirectly by using
chronosequence studies of the vegetation zonation (Foster
and Tilman, 2000). Investigations of chronosequences can
expose regional-scale successional trends due to changes of
vegetation and environment (Bakker et al., 1996); permanent
plots, on the other hand, can reveal changes on a local scale.
Nevertheless, directional vegetation change in dunes can be
overlaid by seasonal fluctuations, which are determined, e.g.,
by variation in precipitation and groundwater (Van Der
Maarel, 1978, 1981), wind disturbance, and associated sand
erosion and accumulation (Martnez, Vazquez, and Sanchez,
2001). Therefore, it is a methodological challenge to distinguish
between fluctuation and succession in dune vegetation using a
The present study evaluates changes in plant diversity
during the past 15 years in dune vegetation influenced by
natural succession. The main scope of the study was to analyze
species diversity in relation to succession. Questions addressed
by this study are as follows: (1) Does species diversity of coastal
dune vegetation change in relation to succession in a humped-
back (>) manner? (2) Does the chronosequence approach reflect
the time-related vegetation development? (3) Does a relation-
ship exist between succession rate and species diversity, and
are species-rich communities more stable? and (4) Do species of
later successional stages change in cover abundance strength
compared with those from earlier stages?
The study area was located on the German Wadden Sea
island of Spiekeroog (Figure 1). The area is protected as part of
the Wadden Sea National Park (intermediate protection zone).
The island can be divided in distinct areas of different age
(Figure 1). The oldest part originates from around AD 1650,
and the eastern part has developed since AD 1960 (Gerlach,
Albers, and Broedlin, 1994). Foredunes on Spiekeroog are due
to continuing sand dynamics up to 20 years old, the main yellow
dune ridges are 45 to 70 years old, the grey dunes are 70 to
170 years old, and the brown dunes are up to 270 years old
(Gerlach, Albers, and Broedlin, 1994). The study area was
composed of a dune chronosequence in the older, western part
of the island, and plot ages were estimated according to
The dry dune chronosequence, the xeroseries, is character-
ized by a typical vegetation zonation. On the beach driftline,
vegetation such as the Salsolo-Cakiletum maritimae occurs.
The xeroseries started with low embryonic dunes grown by the
Figure 1. The island Spiekeroog, the location of the permanent plots (Niedersachsisches Landesamt Fur Okologie, 1993), and the development of the dune
areas on the island (Gerlach, Albers, and Broedlin, 1994; according to Sindowski, 1970). A line represents the location of the chronosequence along which the
permanent plots were located. Plains (white) in the south are saltmarhes, in the centre reflect the village, and in the eastern part the white plains reflect
dunes in the north and salt marshes in the south. The geographic coordinates are for plot 1 (53u46933.80 N, 007u42948.40 E), plot 2 (53u46932.40 N, 007u42952.20E), plot 3 (53u46922.60 N, 007u42930.40 E), plot 4 (53u46927.20 N, 007u42934.90 E), plot 5 (53u46922.60 N; 007u42930.40 E), plot 6 (53u46920.40 N, 007u42948.70 E),plot 7 (53u46912.50 N, 007u43901.20 E), plot 8 (53u46918.70 N, 007u43901.80 E), plot 9 (53u46923.00 N, 007u42930.60 E), plot 10 (53u46907.00 N, 007u42957.50 E), andplot 11 (53u46906.60 N, 007u42956.70 E).
Journal of Coastal Research, Vol. 27, No. 4, 2011
Honckenyo-Agropyretum juncei. In the case of sand accumula-
tion, dunes rise to higher yellow dunes, typically covered by the
Elymo-Ammophiletum and characterized by sparse vegetation
and a raw soil more or less without organic matter. With lesser
sand accumulation, shrublands like the Hippophao-Sambuce-
tum establish on the landwards slopes. Increased sand
stabilization, continued leaching out of nutrients by precipita-
tion, and increased vegetation cover support the origin of soil
organic matter, so that grey dunes develop. Grey dunes in
relation to a decreasing gradient of sand accumulation and in
relation to soil development, e.g., expressed as a decreasing soil
pH, are covered by plant communities like the Phleo-Tortule-
tum ruraliformis, the Festuco-Galietum veri, and the lichen-
and bryophyte-rich Violo-Corynephoretum. These grey dune
communities often contain many rare species and occur in less
disturbed conditions more often on the islands than on the
mainland, so they are highly valuable in the sense of nature
conservation. The following brown dunes with low soil pH and
high organic matter content are characterized, on the one
hand, by short, dense grasslands like the Carex arenaria
[Koelerio-Corynephoretea] community and, on the other hand,
by heathlands, which on Spiekeroog are represented by the
Carici arenariae-Empetretum. The oldest dune parts are
grown by dune woodlands, including Betula pubescens, Pinus
silvestris, Populus tremula, Quercus robur, and since about
10 years ago, Fagus sylvatica.
Dunes are in general characterized by sand dynamic, which
supports small-scale vegetation mosaics and younger vegeta-
tion stagesespecially in grey dunes. Therefore, natural and
human-induced disturbance plays an important role. The
dunes on Spiekeroog were grazed by cattle and sheep until
about 1900; rabbits have been eradicated since 1880 (Meyer-
Deepen and Meijering, 1970), only hares and pheasants with
lower scrabbling activities occur. Many parts of the outer dunes
are stabilized by planting of marram grass; thus, higher sand
accumulation into the following dunes is more or less stopped.
Only beach and foredunes show higher sand dynamic,
particularly due to recreation activities. During the past
15 years, disturbance in the inner dunes was low, including
human impacts, e.g., due to recreation activities. Establish-
ment of the national park and general enhanced public
environmental awareness, combined with increased respon-
siveness of global change, e.g., the importance of dunes in
relation to sea-level rise, support the decline in human dune
During the last century, land use changed and in the
following dunes developed to be more fixed and without an
appreciable amount of open sandy areas (Meyer-Deepen and
Meijering, 1970). Due to changes in land use, dunes in the
North Sea area are, since the middle of the last century,
characterized by an increase in various scrub vegetation, e.g.,
native shrubs such as Crataegus monogyna, Hippophae
rhamnoides, and Ligustrum vulgare and nonnative ones like
Rosa rugosa (Isermann and Cordes, 1992; Van Der Laan,
1985). The development towards older successional stages on
Spiekeroog was already visible around 1950 (Wiemann and
Domke, 1959). Further changes of the dune vegetation were
analyzed in 1990 on the landscape scale using vegetation maps
(Isermann and Cordes, 1992), and recent changes were studied
on a smaller scale with permanent plots.
Along a transect from (young) grey to (old) brown dunes, 11
permanent plots (Figure 1), placed in typical plant commu-
nities, were established in 1990. In comparison to strictly
random sampling design (Frederiksen et al., 2006), the
permanent plots were established in typical plant commu-
nities, initially with plots containing only one plant community
instead of a possible mixture of different communities in one
plot. Moreover, this sampling design was used because a long-
term development was of primary interest instead of a short-
term competition approach between two plant species. Along
the chronosequence, vegetation changes with indirect and
direct methods were compared. Moreover, vegetation changes
were compared on large and small spatial scales, as well as
considered on different temporal scales, and time-intensive
vegetation mapping (Isermann and Cordes, 1992) and perma-
nent plots were combined.
Permanent plots were recorded to detect long-time vegeta-
tion changes. Because of sand mobility, it was not possible to set
up plots in dunes more seawards. Plots, 1 m2 in size, were
marked with a wooden peg at each corner. Lost plots were
reestablished at the most probable same place in relation to
global positioning system (GPS) data and photos of the plot
location in the dune landscape. Changes in species composition
were studied in most cases every fifth year from 1990 to 2005;
in total, 34 releves were analyzed (Appendix). Fieldwork was
carried out in late summer (July/August). This variation has no
effects on the results of this study, especially not for short-lived
species, because of the rather long period of the study.
Vegetation releves were carried out, and the percentage of
cover of each vegetation layer (shrubs and trees, herbs and
grasses, and bryophytes and lichens) was estimated. Plant
species cover was recorded using the Barkman-Doing-Segal
scale (Barkman, Doing, and Segal, 1964). The data were
converted into average percentages of the cover range.
Ellenberg indicator values (Ellenberg et al., 1991) were used
to compare environmental conditions in different vegetation
Statistical analyses were, if not otherwise mentioned, carried
out with the program Minitab (Anonymous, 1998). To distin-
guish different vegetation groups according to the zonation, all
releves were classified using a two-way indicator species
analysis (TWINSPAN), running PC-ORD software with cut
levels 0, 2, 5, 10, and 20 (Mccune and Mefford, 1999).
All raw data of the 34 observations were used to analyze
changes in vegetation (cover and species diversity of different
vegetation layers) and in environmental conditions (cover-
weighted Ellenberg indicator values) along the chronose-
quence. A choice of diversity indices was used to compare the
resulting differences between the indices. The chronosequence
of different plant communities was expressed as numbers of the
vegetation groups mentioned in Appendix. Regression analysis
Species Diversity Patterns during Coastal Dune Succession 663
Journal of Coastal Research, Vol. 27, No. 4, 2011
was used, and the significance of the quadratic model in
relation to the linear one was tested by forwards and
backwards stepwise regression.
The variation in species diversity was measured as number
of species in total and for each vegetation layer separately.
Differences in total species richness between the earliest and
the latest observation were shown graphically in biplots.
To estimate changes of vegetation and environment in
relation to the development from one community to another,
differences in environmental factors, vegetation cover, and
species diversity between distinguished vegetation groups
were assessed with one-way analysis of variance.
The change in cover abundance values of different species in
plots between the first and the last observation years was
estimated (data not shown), and species with a clear response
($5% total cover change) are marked in bold (Appendix).
General changes of the species composition in time were
assessed by detrended correspondence analysis (DCA) running
CANOCO software (Ter Braak and Smilauer, 2002) with its
default options. Species with only one occurrence were omitted.
Ordination analysis was chosen because the variation during
time was expected to be continuous and because the method is
useful to examine relationships over time in different stands
(Austin, 1977). To analyze the direction of change in vegetation
composition, a DCA ordination diagram was used. In the
sample plot, subsequent years were connected by arrows to
indicate the direction in changes of species composition.
To analyze the direction of vegetation changes, Spearman
rank correlation, running SPSS 12, between plot scores of the
ordination axis and both environmental and vegetational factors
were used. Environmental factors were represented by mean
Ellenberg indicator values; vegetational factors were repre-
sented by the number of species and cover of each vegetation
layer, as well as species-diversity indices. Furthermore, dune
ages were correlated with the DCA ordination scores.
To measure the change of floristic composition between the
survey dates, Euclidean distance was used (Myster and
Pickett, 1994; Olff and Bakker, 1991). It was calculated for
each plot based on the relative abundances of the species used
in the DCA analysis described earlier. The overall rate of
succession (net rate) was calculated as the Euclidean distance
between the first and the last years of observation. The 5-year
rate of succession was calculated as the average Euclidean
distance between successive investigation years. To evaluate
relations between succession rate and species diversity,
relationships between Euclidian distance and number of
species, as well as diversity indices, were analyzed.
NOMENCLATURE: Wisskirchen and Haeupler (1998)
for vascular plants, Koperski et al. (2000) for bryophytes, and
Wirth (1995) for lichens; plant communities according to
Schaminee, Stortelder, and Westhoff, (1995).
The TWINSPAN classification resulted in four main vegeta-
tion groups, based on floristic similarities (Appendix). Group 1
(G1) represented earlier succession stages of grey dunes (Phleo-
Tortuletum ruraliformis, Festuco-Galietum veri), mostly char-
acterized by higher sand dynamic. Group 2 corresponded to
lichen- and bryophyte-rich plant communities of the old, fixed
grey dunes (Violo-Corynephoretum). The Violo-Corynephore-
tum group was divided into four subgroups: a typical one (G2a),
a group rich in the neophyte Campylopus introflexus (G2b, C.
introflexus [Koelerio-Corynephoretea] community), a lichen-
rich one (G2c), and a group rich in Dicranum scoparium (G2d).
Group 3 reflected later succession stages with communities
dominated by sedges and grasses (C. arenaria [Koelerio-
Corynephoretea] and Deschampsia flexuosa [Nardetea/Cal-
luno-Ulicetea] communities). Group 4 (Carici arenariae-Empe-
tretum) consisted of heathlands on brown dunes and repre-
sented a dominance of dwarf shrubs with Calluna vulgaris
(G4a) and with Empetrum nigrum (G4b).
The classified vegetation groups revealed a strong zonation
from young grey dunes (G1) to brown dunes (G3 and G4). A
significant increase occurred in dune age (Table 1); thus, the
zonation of the vegetation (Appendix) reflected the dune
Along the chronosequence and the succession series, respec-
tively, Ellenberg indicator values of pH and N declined linear
Table 1. Relationships between classified vegetation groups and dune
age, indicator values, vegetation cover, number of species, and diversity
indices were estimated by regression analysis. Shown are best-fitting linear
or quadratic regressions, tested stepwise backwards and forwards. Slope of
the linear relation, form of quadratic relation (< or >), coefficient of
determination (R2adj.), and probability (p) are given. Number of
observations was n 5 34.
Linear Regression Quadratic Regression
Slope R2adj. p Form R2adj. p
Dune age (years) +23.52 0.65 ,0.001Indicator value
pH (R indicator) 20.30 0.45 ,0.001
Light (L indicator) > 0.74 ,0.001
Moisture (F indicator) < 0.53 ,0.001
indicator) > 0.49 ,0.001
Nitrogen (N indicator) 20.10 0.13 0.021
Total 7.89 0.17 0.009
Grasses > 0.15 0.033
Bryophytes > 0.44 ,0.001
Lichens > 0.12 0.057
Total 22.33 0.63 ,0.001
Shrubs and trees < 0.26 0.004
Grasses 20.38 0.49 ,0.001
Herbs 21.56 0.49 ,0.001
Bryophytes > 0.18 0.018
Lichens > 0.42 ,0.001
Jaccard index 20.01 0.51 ,0.001
Shannon index 20.10 0.21 0.003
Euclidean distance 1.81 0.13 0.021
Srensen index 20.02 0.38 ,0.001
Journal of Coastal Research, Vol. 27, No. 4, 2011
(Table 1). Indicator values of light and temperature showed
humbed-back relations, and moisture showed U-shaped rela-
tions. Moisture reached lowest and light and temperature
highest values in the lichen-rich Corynephorus sward (G2c).
Thus, the Corynephorus sward was characterized by the
lightest, warmest, and driest conditions of the xerosere.
The cover abundance of each vegetation layer differed along
the xerosere. The total vegetation cover generally increased
linearly from grey to brown dunes (Table 1), which is in line
with a decrease in bar ground reflecting the decline in sand
dynamic. No linear or quadratic relation occurred considering
the cover of shrubs and trees, as well as the cover of herbs.
Cover of shrubs and trees was only remarkable in the brown
dunes, and cover of herbs was only remarkable in the younger
succession stages, such as Phleo-Tortuletum ruraliformis,
Festuco-Galietum veri, and typical Violo-Corynephoretum.
The cover of grasses, bryophytes, and lichens (slightly) showed
humped-back relations along the succession series, with high-
est values in the Corynephorus swards (Table 1).
Species diversity varied among species groups along the
succession series. The number of trees and shrubs showed a U-
shaped relation and was higher in the young grey dunes, e.g.,
with communities of the Festuco-Galietum veri, as well as in
the heathlands. Moreover, the number of grasses decreased.
The number of bryophytes and especially of lichens showed
similarly their cover abundance; humped-back relationships,
with a higher number of species in the old grey dunes. Like the
total number of species, diversity indices (Shannon, Jaccard,
and Srensen) declined; Euclidean distance increased along
the succession series (Table 1). The Jaccard and Srensen
indices showed clearer results than the Shannon index and
During the 15 years of observation, succession was restricted
to a relatively low community level, mainly from one subgroup
to the next older subgroup (Appendix). Vegetation development
was represented by changes from the Festuco-Galietum veri
(G1) to the Violo-Corynephoretum (G2a), which reflects a
significant decrease in the number of herbaceous species
(Table 2). Moreover, soil moisture and pH conditions declined
during succession. Mainly developments came from younger to
older succession stages within the Violo-Corynephoretum
(G2ab, bc, and cd), whereas between the typical subgroup
(2a) and the lichen- and bryophyte-rich one (2b) a significant
increase occurred in the cover of bryophytes, a decrease
occurred in the Jaccard index, and in most cases a decrease
occurred in soil pH (Table 2). Only in one case did stronger
development occur from Violo-Corynephoretum (G2) to brown
dune grasslands (G3). This development was connected with a
decrease in light availability and an increase in N conditions.
Remarkably, no clear successional change was found in the
brown dunes with grassland and heathland communities
According to the ordination diagram (Figure 2), the lines
indicate that plots of different investigation years were mostly
situated along the third ordination axis. The dune age was
negative correlated with the first three axes (Table 3); there-
fore, the oldest dunes were situated at the bottom of the
diagram. The ordination axes were characterized by different
environmental and vegetational changes (Table 3). Along the
second and third axes the indicator values for light and pH
increased and the value for moisture decreased, and along the
third axis temperature showed a slightly increasing trend.
Furthermore, along the second and third axes, the number of
geophytes and hemicryptophytes increased and that of woody
chamaephytes decreased. Moreover, an increase occurred
along the first and second axes in the number of therophytes.
Species diversity (Shannon index and evenness) increased
and dominance (Simpson index) decreased along all axes.
Hence, at the lower-left part of the diagram species-poor
vegetation types are situated, and at the upper-right part of the
diagram are species-richer plots.
The number of species, as well as the cover of both grasses
and lichens, increased, especially along axis 3 (Table 3). Hence,
in dominant vegetation units, especially of the brown dunes (E.
nigrum heath, plot 11), Hieracium pilosella dune (plot 2), C.
arenaria grassland (plot 7), and C. introflexus turf (plot 5),
grasses, sedges, and lichens increased; related to the plot
position, these changed from lower parts to the top right of the
diagram. The Deschampsia grassland (plot 8) tended slightly
to a cyclic development (Figure 2). The grey dune (plot 3),
affected by secondary succession due to slope erosion, showed
various development directions and had a high Euclidean
distance (Table 4). Plots of both Corynephorus swards (plots 4
and 6) and the CallunaEmpetrum heath (plot 9) changed from
upper parts to the bottom left of the ordination diagram
Table 2. Differences of vegetation parameters and environmental factors
between those plant communities that developed from one to another
vegetation group. No detectable differences in the change were found
between group 2b and group 2c. Presented are the mean (Mn) 6 standarddeviation (SD). Vegetation groups are G1 (Phleo-Tortuletum ruraliformis
and Festuco-Galietum veri); G2 (Violo-Corynephoretum) with G2a
(typicum), G2b (Campylopus introflexus rich), and G2d (Dicranum
scoparium rich); and G3 (Carex arenaria [Koelerio-Corynephoretea] and
Deschampsia flexuosa [Nardetea/Calluno-Ulicetea] communities).
Mn SD Mn SD F p
(F indictor) 3.98 0.18 2.77 1.01 7.76 0.032
pH (R indicator) 4.62 0.47 3.37 0.72 9.23 0.023
Herbs (n) 14.40 2.61 5.00 6.93 8.07 0.030
Dune age (years) 640.00 0 713.30 63.51 7.50 0.034
(%) 15.00 22.54 85.70 17.53 22.10 0.005
Jaccard index 0.95 0.05 0.88 0.01 8.21 0.035
pH (R indicator) 3.40 0.72 2.20 0.29 9.41 0.028
pH (R indicator) 2.60 0.18 2.20 0.29 6.24 0.047
Cover total (%) 119.50 5.79 101.10 6.01 19.44 0.005
Light (L indicator) 7.60 0.57 6.30 0.42 15.46 0.006
indicator) 1.80 0.18 2.70 0.38 19.14 0.003
Cover total (%) 110.10 6.01 142.58 18.61 17.92 0.004
F 5 F-value of the ANOVA, ration of within- and between group variance,
p 5 probability.
Species Diversity Patterns during Coastal Dune Succession 665
Journal of Coastal Research, Vol. 27, No. 4, 2011
(Figure 2); they developed to species-poorer and less diverse
communities. The opposite development of the Calluna
Empetrum heath (plot 9) was in line with a decrease in the
indicator values of light, temperature, and pH and an increase
in moisture, reflecting the increase in woody chamaephytes
characterizing the heath.
Species-specific Cover Changes
Some general trends of several species showed marked
(.5%) cover abundance changes between the first and the last
observation years (Appendix). In the young grey dune vegeta-
tion was a decrease in Tortula ruralis, a typical moss for
pioneer vegetation and an increase in bryophytes of later
succession stages like D. scoparium and Hypnum lacunosum,
as well as an increase of Agrostis tenuis. Lichen-rich grey dune
vegetation was often characterized by a decline in Coryne-
phorus canescens, Rumex acetosella, and sometimes tube-
shaped Cladonias (e.g., Cl. anomea and Cl. chlorophaea).
Moreover, this lichen-rich vegetation showed an increase in C.
arenaria but even more in the neophytic moss C. introflexus; in
one case, an increase was found in the relatively foliose
Cladonia foliacea that probably grew on the Campylopus turf.
The grasslands of the old dunes, the C. arenaria and the D.
flexuosadominated plots, showed a reverse development of C.
arenaria and D. flexuosa, respectively. Furthermore, species of
older succession stages (Hypnum ericetorum and Cladonia
arbuscula) increased. The brown dune heathlands represented
an increase in D. scoparium and both H. ericetorum and
Pleurozium schreberi. Moreover, the CallunaEmpetrum heath-
land showed an increase in cover of E. nigrum and C. vulgaris
and hence a vegetation change towards older succession stages.
Changes in Species Richness
Changes in species richness varied in relation to succession.
Comparison of the number of species in the first and the last
observations, and additional regression analyses between
species richness and observation year (data not shown because
they are not significant), showed successional trends, as well as
The number of herbaceous species (Figure 3b) decreased in
the Phleo-Tortuletum ruraliformis (plot 1), typical for the
young grey dunes. In comparison, the number of bryophytes
and lichens showed more variation. The number of bryophytes
and lichens (Figure 3c) decreased between 1990 and 2005 in
the Corynephorus grey dunes (plots 4 and 6). In contrast, the
number of herbaceous species fluctuated, probably because of
the occurrence of annual and other short-lived species.
Bryophyte and lichen richness increased at both sites with
secondary succession (plots 3 and 5), e.g., due to the increase of
C. introflexus. However, at dominant Campylopus stands (plot
5) strong fluctuations occurred, probably due to bryophytes
and lichens growing temporarily in small gaps or on Campy-
lopus turfs. This resulted in a decline (plots 4 and 6) and an
increase (plot 3) in the total number of species (Figure 3a). The
dense D. flexuosa grassland (plot 8) was characterized by a
decrease in bryophytes and lichens, as well as strong
fluctuations of herbaceous species richness, probably due to
reduced space and changed environmental conditions between
the Deschampsia tussocks in comparison to the open Coryne-
phorus swards. The brown dunes showed a clear increase in
bryophytes and lichens (plots 911), which are typical in
heathlands with the enhanced moisture contents. The number
of other herbaceous species fluctuated a little, probably
because only few spaces between the heathlands allowed the
establishment of further species.
The succession rate of the species composition was repre-
sented by the Euclidean distance (Table 4) between the first and
the last years of observation. Plots dominated by one species,
like the H. pilosella community (plot 2), the C. introflexus turf
(plot 5), and the E. nigrum heath (plot 10), showed only few
changes in their species composition and had a low overall rate
of succession (Table 4). According to the mean rate of succes-
sion, moreover, the D. flexuosa grassland (plot 8) and both plots
of the lichen-rich C. canescens swards (plots 3 and 6) showed a
lower 5-year rate of succession than species-richer communities.
The Euclidean distance showed a slight but not significant
trend to a humped-back relation with the total number of
species (Figure 4a); low succession rates were observed in
species-poor communities, as well as in species-rich ones.
Furthermore, a slight and significant humped-back relation
was found between the overall succession rate and the
Figure 2. Ordination diagram using detrended correspondence analysis
of all 34 releves, x 5 axis 1, y 5 axis 2 (eigenvalue: total 5.588, axis 1 5
0.903, axis 2 5 0.636, axis 3 5 0.219, and axis 4 5 0.182; lengths of
gradient: axis 1 5 6.709, axis 2 5 4.143, axis 3 5 2.748, and axis 4 5 3.397).
The lines indicate the changes in species composition of the permanent
plots (no. plot/year). Symbols reflect the vegetation groups (Table 1): black
dots 5 G1 (young grey dunes); black diamond 5 G2 (bryophyte- and lichen-
rich old grey dunes); grey dots 5 G3 (dune grasslands); and grey diamond
5 G4 (brown dune heathlands).
Journal of Coastal Research, Vol. 27, No. 4, 2011
evenness (Figure 4b). The overall succession rate at first
increased with increasing evenness and then showed a
reduction and a runout at the higher values of evenness.
The dunes of the island of Spiekeroog are one example in
which environmental conditions changed with the vegetation
during succession. Nutrient content, expressed as indicator
value N, and soil pH declined along the chronosequence. Thus,
soils of young grey dunes were characterized by higher soil pH
and higher nutrient content. Along the chronosequence, light
and temperature showed a humped-back relation and moisture
a U-shaped one. Therefore, the Corynephorus sward of the old
grey dunes was composed of light, very dry, nutrient-poor
stands with a low soil pH. Finally, the brown dunes with
grasslands and heathlands included less dry soils with a very
Table 3. Spearman rank correlation between Ellenberg indicator values (cover weighted); detrended correspondence analysis ordination axes 1, 2, and 3;
correlation between percentages of life forms (cover weighted); and cover abundance and species richness of life form groups with each ordination axis.
Moreover, the correlation between the ordination axes and some diversity indices and the correlation with the dune age are shown. Spearman rank coefficient
(rS) and probability (p) are given.
Axis 1 Axis 2 Axis 3
rS p rS p rS p
Ellenberg indicator value
Light (L indicator) 0.444 0.008 0.654 0.001
Temperature (T indicator) 0.309 0.071
Moisture (F indicator) 20.568 0.001 20.838 0.001
pH (R indicator) 0.503 0.002 0.425 0.011
Dune age (years) 20.425 0.012 20.613 0.000 20.482 0.004
Life form (%)
Chamaephytes, woody 20.573 0.001 20.706 0.001
Hemicryptophytes 0.433 0.009 0.681 0.001
Geophytes 0.561 0.001 0.475 0.004
Therophytes 0.309 0.071 0.508 0.002
Cover abundance (%)
Total cover 0.522 0.001
Shrubs and trees 20.526 0.001 20.711 0.001
Grasses 0.355 0.036 0.500 0.002 0.427 0.011
Herbs 0.496 0.002
Grasses and herbs 0.360 0.034 0.499 0.002
Lichens 0.489 0.003 0.765 0.001
Bryophytes and lichens 0.407 0.015
Total 0.511 0.002 0.831 0.001 0.669 0.001
Shrubs and trees 20.400 0.017 20.623 0.001
Grasses 0.414 0.014 0.695 0.001 0.466 0.005
Herbs 0.547 0.001 0.310 0.070
Grasses and herbs 0.288 0.094 0.677 0.001 0.454 0.006
Bryophytes 0.456 0.006
Lichens 0.494 0.003 0.791 0.001
Bryophytes and lichens 0.287 0.095 0.453 0.006 0.665 0.001
Shannon index 0.808 0.001 0.762 0.001 0.526 0.001
Simpson index 0.769 0.001 0.610 0.001 0.447 0.008
Evenness 0.731 0.001 0.423 0.013 0.299 0.086
Euclidean distance 20.417 0.014 20.575 0.001
Srensen index 20.362 0.036
Jaccard index 0.407 0.017 0.460 0.006
Table 4. Overall succession rate measured as total Euclidean distance between the first and the last years of observation, and 5-year succession rate
measured as mean Euclidean distance of all observation years. Given are also the vegetation groups (Appendix) reflecting the youngest and the oldest
successional stages of each plot.
Plot number 1 2 3 4 5 6 7 8 9 10 11
Successional stage 1 12a 2ab 2bc 2bd 2cd 2d3 3 4a 4ab 4b
Euclidean distance (total) 40.1 25.0 70.1 96.7 15.5 53.8 51.2 44.9 58.3 4.1 53.3
Euclidean distance (mean) 55.6 33.9 39.6 55.0 49.1 31.2 51.2 32.7 57.9 33.0 53.3
Species Diversity Patterns during Coastal Dune Succession 667
Journal of Coastal Research, Vol. 27, No. 4, 2011
low soil pH. These changes of environmental conditions along a
dune zonation were typical for the dune xerosere and are
known from various other regions, such as the Swina Gate
Barrier in Poland (abuz and Grunewald, 2007). In general,
the interplay of different processes like accumulating sand at
the first dune ridges, leaching out of nutrients, increasing
vegetation cover, and accumulating organic matter in the
landwards following dunes resulted in different plant commu-
nities along the chronosequence (Carter, 1993; Salisbury,
1925). With ongoing succession in dunes, climatic aspects
became increasingly important. The humped-shaped tempera-
ture gradient along the studied chronosequence reflects the
warmer conditions on southern slopes with lichen- and
bryophyte-rich Corynephorus swards and the colder conditions
on the northern slopes containing Empetrum heath. Dry
valleys of the grey dunes were often grown by C. arenaria or
D. flexuosadominated grasslands; moreover, south slopes or
flat areas were grown by the dominant neophytic moss C.
introflexus, especially on disturbed sites with following
A typical change of the vegetation structure occurs along the
xerosere: The young grey dunes are characterized by mostly
short grasses and herbs; on the grey dunes, bryophytes and
especially lichens play an important role; and on the brown
dunes, trees and especially dwarf shrubs become important
cover abundances. These pattern and processes of dune
succession on Spiekeroog are comparable on a global scale
because the vegetation structure is similar (Doing, 1985).
In general, the chronosequence showed an initial increase in
species richness from the species-poor yellow dunes to the
young grey dunes after surface stabilization, followed by a
Figure 3. Biplots of the number of species in the first and last years of
observation, which indicate increase and decrease in species richness
between both years. (a) Total number of species, (b) herbaceous species, (c)
bryophytes and lichens. (Spearman rank rS correlation across all 5 years:
bryophytes and lichens, as well as total number of species in plots 4 and 6,
and herbaceous species in plot 1: rS 5 21.000, p , 0.001).
Figure 4. (a) Relationships between overall succession rates measured as
total Euclidian distance between the first and the last years of observation,
and species richness shown as the mean total number of species of each
plot over the years (R2adj. 5 0.10, p 5 0.266). (b) The relationship with the
average evenness over the years (R2adj. 5 0.41, p 5 0.048). Numbers
represent permanent plot numbers.
Journal of Coastal Research, Vol. 27, No. 4, 2011
relatively constant level or a decrease during later parts of
succession (Morrison and Yarranton, 1973). Average of total
species richness increased in a humped-back manner, e.g., in
dunes of the German Baltic Coast (Isermann, 2005). In this
permanent plot study, only a linear decline was found in total
species richness because the succession only started with the
grey dunes, which had the highest number of species. The
yellow dunes could not be taken into account in the permanent
plot study due to sand mobility. Similar to other dune studies,
highest values of species diversity occurred in young grey
dunes, where disturbance in the sense of sand accumulation
and erosion reached intermediate levels. Although yellow
dunes are missing, the study confirmed the intermediate stress
theory, whereas highest species richness is reached at inter-
mediate levels of environmental and disturbance gradients.
Similar to our results, much lower species richness than in
the young grey dunes is known from other regions in pioneer
communities, such as yellow dunes with Ammophila arenaria,
as well as from old grey dunes with grasslands dominated by C.
arenaria (Bogaert and Lemeur, 1995). On Spiekeroog, from the
young grey dunes inland, total species richness declines with
dune age, which was also shown for coastal Lake Michigan
sand dunes in the United States (Lichter, 1998). In comparison
to the assumed humped-back relation of total species richness,
species diversity, as well as cover abundance of bryophytes and
lichens, showed a humped-back relation along the chronose-
quence. The highest species diversity of bryophytes and lichens
in the old grey dunes reflects the enhanced competition of
bryophytes and lichens in comparison to herbs and grasses on
these dry and acid soils. Thus, species diversity of different life
forms varies in relation to the dune type and along the
chronosequence. The diversity within different functional
types reflects the variation of environmental conditions
(Garca-Mora, Gallego-Fernandez, and Garca-Novo, 2000).
The succession series of the dunes on Spiekeroog confirms
differences in species diversity relationships regarding both
primary and secondary succession. Regarding secondary suc-
cession, species richness increased after slope erosion in the first
5 years in the Corynephorus sward, but the increase was
reduced in the following years and total species richness did not
reach the original number of species. The vegetation changed to
a C. introflexusdominated turf of bryophytes. Thus, the species
composition changed and the primary succession was deflected,
whereas the secondary succession was a progressive one in
which the cover abundance of C. introflexus increased strongly.
The increase of C. introflexus generally results in species poor
communities, such as dry calcareous grasslands (Van Der Laan,
1985). Thus, the presented dune study approves the general
decline in species richness of secondary successions after an
initial species increase. Similarly, these relationships were
shown in secondary succession on exposed lake sediments
(Odland and Del Moral, 2002), on coastal dunes in Canada
(Morrison and Yarranton, 1973), and in eastern Denmark
In dunes, sand dynamics (accumulation as well as erosion)
creates periodic vegetation disturbances and is one of the most
significant factors affecting vegetation and succession (Junger-
ius et al., 1995). On Spiekeroog, the rate of successional change
following disturbance, e.g., by erosion of dune slopes, is fast in
comparison to the whole dune series, but this could explained
by the primary character of these sites within a secondary
succession series. Unstable environments are often character-
ized by strong year-to-year variation in environmental and
vegetation conditions (Vestergaard, 2006), as well as in a faster
species turnover (Martnez, Vazquez, and Sanchez, 2001).
The study also confirmed that the development of disturbed
areas, in particular on small scales, require time-series data
gathered from particular sites and cannot be estimated from a
static survey using a chronosequence (Foster and Tilman,
During primary succession, cover abundance of pioneer and
persistent species showed a reversed development; the coloniz-
ing succession stage contains many pioneer and few persistent
species. By the way, similar to the development on exposed lake
sediments (Odland and Del Moral, 2002); not only bryophytes
and lichens but also sedges and grasses with clonal growth, like
C. arenaria or Festuca rubra, play an important role, especially
in secondary dune succession (Isermann and Krisch, 1995).
Moreover, during primary succession at earlier succession
stages, like the young grey dunes, therophytes are more
important than in older succession stages (Olff, Huisman,
and Van Tooren, 1993). The intermediate stages of succession
have medium numbers of pioneers and persistent ones; in the
later stages, many persistent species occur and few pioneers
remain (Morrison and Yarranton, 1974). Hence, in the old grey
dunes hemicryptophytes and geophytes and in the old brown
dunes woody chamaephytes and phanerophytes are more
abundant (Olff, Huisman, and Van Tooren, 1993). Due to the
changing spectrum of competition strategies, species richness
of vegetation is highest in the transition period, represented,
e.g., by young grey dunes. At the beginning of primary
successions, environmental conditions are generally uniform
over relatively large areas (Morrison and Yarranton, 1974),
and the vegetation, e.g., yellow dunes dominated by A.
arenaria, often is homogenous. In landscape types like coastal
dune series with well-developed environmental gradients,
species-rich vegetation will occur in the middle part of existing
gradients (Van Der Maarel, 1978). In coastal dunes, e.g.,
species richness was highest at intermediate levels of soil pH
(Isermann, 2005). Moreover, species-rich vegetation is related
to environmental heterogeneity (Morrison and Yarranton,
1974); e.g., the transition succession period of the dunes with
intermediate soil pH levels showed also the highest standard
deviation of soil pH (Isermann, 2005).
Species-poor communities of grey and brown dunes, domi-
nated by only a few species, probably have low succession rates
because they showed a metastable stage, resembling older
dunes. Moreover, in the case of high numbers of species, the
succession stages rate was low. These species-rich communities
probably are due to their high diversity that is more or less
stable. Both cases could be explained according to evenness:
communities with a balanced distribution of species showed the
lowest succession rates.
Species-rich vegetation of the young grey dunes on Spieker-
oog showed only few changes in species composition during the
Species Diversity Patterns during Coastal Dune Succession 669
Journal of Coastal Research, Vol. 27, No. 4, 2011
study period. In general, during primary succession, commu-
nities with higher species richness showed less temporal total
variation (Tilman and Downing, 1994). Thus, more diverse
communities are more stable, because stability in ecosystems
has to be considered as a dynamic process. Moreover, species-
poor heathlands with E. nigrum showed only few changes in
species composition, probably because heathlands are one of
the old succession stages in the dune xerosere. Thus, the dune
xerosere reflects that vegetation changes are lower in old
succession stages than in earlier stages, because the rate of
succession change in later stages generally declines over time
(Foster and Tilman, 2000). Thus, the study is in line with the
biodiversity-stability theory, with highest ecosystem stability
at highest diversity.
Similar relationships between vegetation zones and distinct
successional trends are known from salt marshes, where
succession trends were mostly restricted to a particular
altitudinal zone of the salt marsh (Roozen and Westhoff,
1985). Vegetation changes from one to another succession stage
of the salt marsh are shown to be rare, because these processes
need much longer times to develop (Roozen and Westhoff,
In coastal dunes of Spiekeroog, changes in plant species
composition, species diversity, and succession rate had clear
differences during the development from younger to older
succession stages, as well as during primary and secondary
succession. Differences in plant communities were more visible
along the chronosequence, reflecting long-term changes during
succession. In addition, fluctuations and stepwise, short-term
development of plant communities could be shown by the
vegetation development of each permanent plot. Therefore, the
study shows the need for multitemporal approaches to
distinguish between short-term fluctuation and long-term
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Vegetation groups (14) are distinguished by two-way
indicator species analysis (TWINSPAN) classification. Young
grey dunes (group 2) are divided into four subgroups (2ad),
and group 4 is split into subgroups 4a and 4b. Moreover, the
corresponding plot numbers and their plant communities are
represented. Species with a total change in percentage of
cover abundance between 1990 and 2005 larger than at least
5% of the total are in bold. Furthermore, the vegetation
groups distinguished by TWINSPAN analyses were shown
and differentiated by vertical lines.
Moreover, following species occur in the given periods:
Centaurium pulchellum (0.5), Eryngium maritimum (0.1),
and Tortula ruralis (5.0) in plot 1 1990; Holcus lanatus (0.5),
Taraxacum laevigatum (agg. 0.5), and Viola tricolour (0.1) in
plot 1 2000; Cerastium semidecandrum (0.5) in plot 2 1990;
Erigeron acris (0.1) and Peltigera canina (2.0) in plot 2 1995;
Arabidopsis thaliana (0.3), Brachythecium albicans (4.0),
Brachythecium rutabulum (1.0), Rosa rubiginosa (0.3), Rubus
caesius (1.0), Trifolium arvense (0.3), Vicia lathyroides (0.3),
and Rhytidiadelphus triquetrus (1.0) in plot 2 2000; Lepidocea
reptans (0.3) in plot 4 1990; Cladonia rangiferina (0.1) in plot
4 2004; Plantago coronopus (0.5) in plot 5 1990; Cladonia
ciliata (0.5) and Hypogymnia physodes (0.5) in plot 5 2000;
Cladonia mitis (1.0) in plot 8 2005; Quercus robur (0.1) and
Sorbus aucuparia (0.1) in plot 9 1990; Scleropodium purum
(1.0) in plot 9 2005; and R. caesius (1.0) in plot 11 2005.
Species Diversity Patterns during Coastal Dune Succession 671
Journal of Coastal Research, Vol. 27, No. 4, 2011