ICES Journal of Marine Science, 53: 964–971. 1996
The geographic scale of synchronized fluctuation patterns in
zoobenthos populations as a key to underlying factors: climatic or
man-induced
J. J. Beukema, K. Essink, and H. Michaelis
Beukema, J. J., Essink, K., and Michaelis, H. 1996. The geographic scale of
synchronized fluctuation patterns in zoobenthos populations as a key to underlying
factors: climatic or man-induced. – ICES Journal of Marine Science, 53: 964–971.
Densities of zoobenthic species observed at different locations tend to fluctuate in
parallel even when these sites are far apart. Climatic factors can synchronize
population changes over wide geographic areas if they have a direct effect on
recruitment or mortality. Several examples indicate that severe winters represent a
major synchronizing factor among many of the zoobenthos species of tidal flats, both
by immediately enhanced mortality rates in species sensitive to low temperatures and
by enhanced recruitment in bivalve species some months later. Long-term monitoring
in three areas of the Wadden Sea (Balgzand, Groningen, and Norderney) revealed
synchronous baseline patterns in the fluctuations of several species. Examples are
shown for the polychaete Nephtys hombergii and the tellinid bivalve Macoma balthica.
Local departures from such common patterns indicate local disturbing factors.
Examples are shown on scales of about 1 km (a waste-water discharge) and several
tens of kilometres (eutrophication in the westernmost part of the Wadden Sea).
? 1996 International Council for the Exploration of the Sea
Key words: abundance fluctuations, common causes, synchronization, tidal flats,
Wadden Sea, zoobenthos.
J. J. Beukema: Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB
Den Burg, Texel, The Netherlands; K. Essink: National Institute for Coastal Marine
Management/RIKZ, PO Box 207, 9750 AE, Haren, The Netherlands; H. Michaelis:
Niedersächsisches Landesamt für O
} kologie, Forschungsstelle Küste, An der Mühle 5,
D-26548, Norderney, Germany.
Introduction
Successful management of ecosystems depends on our
ability to identify causes of undesirable changes. As
such, changes in abundance are inherent to any population within an ecosystem. The problem is to distinguish
between natural and man-induced changes. The
phenomenon of synchronized fluctuations may offer a
clue, particularly when the geographic scale of similar
fluctuation patterns is also known. Within restricted
areas, time series of abundance of many marine zoobenthos species tend to show more or less parallel
fluctuation patterns (Beukema and Essink, 1986; Essink
and Beukema, 1986). Such synchronized changes in
population density are not remarkable if the distance
between sampling sites is short relative to the dispersal
capabilities of the species. If, however, sampling
locations are so far apart that the samples cannot be
considered to be drawn from one intermingling
population, any apparent synchronization in annual
variation will point to the existence of some environ1054–3139/96/060964+08 $18.00/0
mental factor that operates over large areas and governs
the dynamics.
Environmental factors that fluctuate in phase over
wide geographical areas are often of astronomical origin, such as the 11-year cycle in sun spots or the
18.6-year cycle of lunar tides. Both cycles appear to
affect marine environmental conditions such as temperature and salinity (Gray and Christie, 1983), but other
cycles may also be involved (Fromentin and Ibanez,
1994). Weather conditions induce large and irregular
year-to-year variations in environmental parameters
which are superimposed on these cycles and long-term
trends. For the present discussion, it is relevant to note
that year-to-year variation in climatic factors stretches
also over large distances. For instance, the occurrence of
severe winters in western Europe is synchronized over an
area of >10 degrees latitude or about 2000 km extending
from the Atlantic coast of France (Formentin and
Ibanez, 1994) to the northern Baltic (Beukema et al.,
1993; cf. figure 3 of Desprez et al., 1991). In coastal
areas around the North Sea, cold winters affect densities
? 1996 International Council for the Exploration of the Sea
The geographic scale of synchronized fluctuation patterns
5°
6°
965
7°
8°E
North Sea
54°N
Wangerooge
Norderney
Rottum
Ameland
Terschelling
53°30'
N.p.zijl
n
de
ad
W
a
Se
Groningen
Texel
Germany
Netherlands
Den Helder
0
53°
20
40
60
80 km
Balgzand
10 m depth line
Sampling areas
Figure 1. The three sites of long-term studies of intertidal macrozoobenthos in the Wadden Sea.
of several benthic species either by reducing survival
(sensitive species listed in for example Crisp, 1964;
Ziegelmeier, 1964; Beukema, 1979, 1990) or by enhancing subsequent recruitment (Möller, 1986; Beukema,
1982, 1992a). Both processes probably contribute to
the observed synchronization in fluctuation patterns in
several tidal-flat species over distances of >100 km in the
Wadden Sea (Beukema and Essink, 1986; Beukema
et al., 1993).
For several reasons, there is a lack of knowledge of
the common fluctuation patterns over large areas (Wolfe
et al., 1987). However, such information is important,
because these patterns may be considered to represent
the baseline for local deviations. Parallel patterns may
be used to define departures as to, for example, the
(positive or negative) direction, magnitude, and geographic scale. Such outlining may offer a clue to the
detection of the causal factors involved. The cause of
some local disturbance may also be identified more
convincingly if the geographic scale of the population
changes match the expected range of the disturbing
factor. In particular, (local) anthropogenic effects may
be distinguished more clearly from (large-scale) natural
causes of observed changes in abundance. To reach
these goals, simultaneous studies of fluctuation patterns
in populations of the same species at different
comparable sites are required. About 15 years ago, the
COST-(6)47 programme was initiated by the
Commission of the European Communities to start
concerted studies on marine benthos along European
coasts (Lewis, 1984). The results presented here
represent part of this programme.
Materials and methods
Long-term time series are available on macrozoobenthos
sampled at least once per year at fixed stations on tidal
flats at three locations within the Dutch and German
Wadden Sea. The locations (Fig. 1) are, from west to
east:
(1) Balgzand (near Den Helder); 15 stations within a
50 km2 area have been sampled from 1969 onwards
J. J. Beukema et al.
The distance between Balgzand and Groningen is
120 km, and between Balgzand and Norderney 180 km.
Sampling methods applied were similar and consistent.
They included sieving of sediment cores in the field
and subsequent sorting, counting, and determination of
ash-free dry weight (AFDW) in the laboratory. Data
obtained in the late-winter/early-spring period are used
for investigating effects of mortality and data from the
late summer period for investigating effects on recruitment. For bivalves, both numeric data (n m "2) and
biomass (g AFDW m "2) estimates were used to characterize density. For worms only biomass estimates were
used, because the juvenile stages are not quantitatively
retained in the 1-mm sieves used, and the variance in
numeric data is unduly influenced in this group by the
large numbers in the selection range.
Data on winter temperatures were taken from
monthly reports of the weather station De Kooy (Royal
Dutch Meteorological Institute), 1 km distance from
Balgzand.
4
(a)
°C
2
0
–2
–4
2.5
70
75
80
Year
85
90
95
75
80
Year
85
90
95
75
80
Year
85
90
95
(b)
2.0
g AFDW m–2
(for details see Beukema, 1988), covering the entire
intertidal range and a range of sediment types;
(2) Groningen Wad (near N.p.zijl=Noordpolderzijl);
five stations within 5 km2 have been sampled from
1969 onwards (for details see Essink, 1978), covering
a restricted range of intertidal levels (immersed
about 35–55% of the time) and sediment types
(5–15% silt); because two stations were seriously
affected by waste-water discharges (Essink and
Beukema, 1986), these have been treated separately
from the other three;
(3) Norderney; four stations within 1 km2 have been
sampled from 1976 onwards (for details see Dörjes
et al., 1986), covering a restricted range of intertidal
levels (immersion about 35–55% of the time) and
sediment types (<5% silt).
1.5
0.1
0.5
0
70
2.5
(c)
2.0
g AFDW m–2
966
1.5
0.1
0.5
0
Results
The polychaete Nephtys hombergii Sav. shows significantly higher mortality in cold winters (Beukema, 1979,
1985) and, therefore, may be considered to represent a
winter-sensitive species. Indeed, biomass values
observed in late winter on Balgzand (solid line in
Fig. 2b) were extremely low after severe winters (1979,
1985, 1986, and 1987; Fig. 2a), whereas dense populations developed during periods characterized by a succession of mild winters (1973–1975, 1988–1990). In
addition, high and low biomass values were to a large
extent synchronized in all three sampling areas (Fig. 2b).
Significant positive correlations were observed between
local biomass and winter temperature for all three data
sets (p<0.01 or 0.001, n=19–26), and Spearman rank
correlation coefficients were in the range +0.7 to +0.8.
The degree of similarity of the fluctuation patterns in
the three areas has been expressed in Spearman rank
70
Figure 2. Long-term (1969–1994) changes in (a) winter (Jan–
Mar) air temperatures ()C) in the western Wadden Sea, plotted
as deviations from the long-term average; (b) late-winter biomass (g AFDW m "2) of Nephtys hombergii at Balgzand
(average of 15 stations (—-—), Groningen (3 undisturbed
stations) (– –,– –), and Norderney (4 stations) (– –0– –); (c)
late-winter biomass (g AFDW m "2) of N. hombergii at
Groningen (2 stations that were seriously disturbed by wastewater discharges until 1974).
correlation coefficients (Table 1A). Statistical significance cannot be attached to these values, because consecutive data within the individual time series were not
mutually independent. However, the 1-year autocorrelation was relatively weak and non-significant (Table 1A)
in this short-lived species. To test whether the correspondence between the patterns in the three areas might be
The geographic scale of synchronized fluctuation patterns
967
Table 1. Spearman rank correlation coefficients (number of paired observations in parentheses) for the
relation between biomass fluctuations of (A) Nephtys hombergii and (B) Macoma balthica at the three
locations and for the 1-year autocorrelation within each series
Correlation between areas
A. Nephtys hombergii
Balgzand
Groningen
Norderney
B. Macoma balthica
Balgzand
Groningen
Norderney
Balgzand
Groningen
Norderney
Autocorrelation
–
+0.61 (25)
–
+0.78 (19)
+0.69 (18)
–
+0.4
+0.4
"0.1
–
+0.59 (22)
–
+0.74 (17)
+0.72 (17)
–
"0.4
"0.2
"0.1
due to chance, the number of simultaneous year-to-year
increases or decreases were counted. Out of the total of
56 paired cases, 44 bore the same sign (p<0.01, ÷2 test).
Similar responses to winter temperatures have probably
synchronized the abundance patterns through mortality.
Synchronization not only occurs within species
over large areas, but also between species. As an
example, Figure 3 shows the fluctuations in biomass of
N. hombergii and Lanice conchilega on the Balgzand.
The same patterns emerge, although the variations in the
latter species are much more extreme.
The tellinid bivalve Macoma balthica (L.) is one of the
most common species in the Wadden Sea and is therefore highly suitable for comparing dynamics in different
areas. Density (in numbers) during late summer fluctu-
ated in a similar way in the three sampling areas (Fig. 4).
The peaks reflect high numbers of spat particularly in
summers following cold winters (cf. Fig. 2a), viz. 1979,
8000
6000
4000
2000
0
n m–2
3000
2
(a)
75
80
85
90
95
75
80
85
90
95
75
80
85
Year
90
95
(b)
2000
g AFDW m
–2
1000
0
1500
1
(c)
1000
500
0
0
70
75
80
85
90
95
Year
Figure 3. Long-term (1969–1995) changes in late-winter
biomass (g AFDW m "2) of Nephtys hombergii (– –-– –)
and Lanice conchilega (—,—) at Balgzand (averages of 15
stations).
Figure 4. Long-term changes in numerical densities (n m "2) of
the bivalve Macoma balthica observed in late summer at (a)
Norderney (average of 4 stations), (b) Groningen (5 stations),
and (c) Balgzand (15 stations).
J. J. Beukema et al.
20
(a)
Gronigen
Norderney
15
10
5
0
–2
1985, 1986, and 1987. Spearman rank correlations
between summer densities and mean temperatures during the foregoing winter (coefficients ranging from "0.7
to "0.5) were significantly negative in all three areas
(p<0.05 or 0.01; n=17–22). The degree of similarity
between the three series according to an evaluation of
the Spearman rank correlations was high (Table 1B),
with all p<0.01. Auto-correlation was low in all series
(Table 1B), probably because summer densities consist
mainly of recently settled spat and these numbers are not
related to number of adults. The results clearly suggest
that similar responses to winter temperatures have synchronized the abundance patterns through recruitment
processes.
Fluctuations in macrozoobenthos at different locations in the Wadden Sea are not always synchronized. A
notable departure has been observed in N. hombergii at
the two Groningen stations affected by discharges of
wastewater (Fig. 2c), particularly during the initial years
1969–1973 (Essink, 1978; Essink and Beukema, 1986).
In contrast to the other Groningen stations and the
other Wadden Sea areas (Fig. 2b), abundance remained
low during the mild-winter period of the mid-1970s.
Only from 1978 onwards, when the amounts of wastewater discharge had become negligible, did the general
pattern manifest itself at these two stations. The deviation from the general pattern allows the effect of the
discharge to be outlined in space as well as in time: only
a few km2 were affected at the population level and these
effects have not been irreversible. Other evidence
reported in Essink (1978), including extra mortality in
other species, corroborates this conclusion. Essink and
Beukema (1986) give a similar example for the worm
Eteone longa, which shows an aberrant pattern during
the first half of the 1970s at the station nearest to the
waste outlet.
Another example of lack of synchronization in part of
the Wadden Sea is shown in Figure 5. Late winter
biomass values of M. balthica followed very similar
patterns in Groningen and Norderney (Fig. 5a), whereas
an opposite trend is observed at Balgzand between 1981
and 1988 (Fig. 5b). The anomaly at Balgzand appears to
have been caused primarily by increased growth rates
during the late 1970s and early 1980s (Beukema and
Cadée, 1986, 1991). Such increases in growth have not
been observed in the easterly areas and growth rates on
the Groningen flats tended even to decline (De Pree,
1992). Growth rates in M. balthica are positively correlated to concentrations of chlorophyll (De Pree, 1992)
and particularly to concentrations of pelagic diatoms
(Beukema and Cadée, 1991). Chlorophyll concentrations and primary production increased during the
1980s in the western parts of the Dutch Wadden Sea (see
Bot and Colijn, 1996) as a consequence of the increased
nutrient discharges of the river Rhine (particularly via
Lake IJssel). These effects have not been observed in the
70
gm
968
75
80
75
80
85
90
95
85
90
95
7
(b)
6
5
4
3
2
1
0
70
Year
Figure 5. Long-term changes in late-winter biomass (g AFDW
m "2) of the bivalve Macoma balthica at (a) Groningen
(– –,– –) (means of 3 stations, 1969–1994; 1981 value by
interpolation) and Norderney (– –0– –) (4 stations, 1976–
1994), and (b) Balgzand (15 stations, 1969–1994).
easterly areas (De Jonge and Essink, 1991; De Jonge and
Van Raaphorst, 1995). Thus, the aberrant pattern
observed on Balgzand appears to be related to local
eutrophication.
The size of the area affected by eutrophication can be
assessed more precisely from a number of other longterm data series. At a tidal flat near the island of
Ameland, about 80 km east of Balgzand, M. balthica
biomass followed the Groningen/Norderney pattern,
with maximum values in the early 1980s (Laufer, 1992).
In this area, total biomass hardly increased during the
1978–1991 period. However, at a tidal flat south of the
island of Terschelling, only 40–50 km north-east of
Balgzand, total biomass roughly doubled between
1977 and 1987 and the pattern of M. balthica biomass
resembled more closely the one observed at Balgzand,
with a maximum in 1987 (Tydeman, 1992). Thus the
area affected by enrichment extended over a distance
between 50 and 80 km. Apparently, the enriched area
in the western half of the Dutch Wadden Sea is
The geographic scale of synchronized fluctuation patterns
969
Table 2. Published records of synchronized fluctuations of population size (§10 yr) in marine benthic
animals at sites which were varying distances apart
Distance
(km)
Period
(y)
Area
Species
0.5
0.5
0.5
1
1–2
1–2
1–2
3–6
1–5
1–5
5
10
2–25
20–60
60
0.1–100
10–100
10–100
150
60–180
60–180
2300
10
10
20
17
10
14
11
17
20
20
15
15
25
10–20
19
8–12
25
25
7–15
16–24
19–26
11
California
Norderney
Balgzand
Groningen
Dollard
Wadden Sea
Wadden Sea
Balgzand
Balgzand
Balgzand
Orkney
Brittany
L.I. Sound
Wadden Sea
Wadden Sea
N. Yorkshire
German Bight
German Bight
Skagerak
Wadden Sea
Wadden Sea
Bothnia
G. gemma
C. edule
A. tenuis
3 spec.*
5 spec.**
2 spec.***
9 spec.****
H. filiformis
N. hombergii
S. armiger
B. sarsi
A. alba
A. forbesi
S. plana
M. balthica
S. balanoides
A. fabula
S. bombyx
5 spec.*****
C. edule
N. hombergii
P. affinis
Reference+fig. no.
Nichols and Thompson, 1985: 2
Ducrotoy et al., 1991: 2a
Beukema, 1990: 5
Essink and Beukema, 1986: 2, 3, 4
Essink et al., 1987: 6, 14, 16, 19, 21
Laufer, 1992: 6, 7
Tydeman, 1992: 8, 10, 11, 12
Beukema and Essink, 1986: 2
Beukema, 1989: 3c
Beukema, 1989: 4a
Atkins and Jones, 1991: 3
Dauvin et al., 1993: 3
Loosanoff, 1964: 6
Essink et al., 1991: 2
This paper: 5a
Kendall et al., 1985: 1, 2
Ziegelmeier, 1978: 329
Ziegelmeier, 1978: 330
Lundälv and Christie, 1986: 2a, 4
Beukema et al., 1993: 8
This paper: 2b
Andersin et al., 1978: 4
*M. balthica, E. longa, N. hombergii.
**N. diversicolor, M. balthica, M. arenaria, S. plana, C. volutator.
***C. edule, M. balthica.
****A. marina, E. longa, H. spec., N. hombergii, N. diversicolor, S. armiger, M. balthica, M. arenaria,
C. edule.
*****C. intestinalis, E. esculentus, A. rubens, A. mentule, S. penicillus.
directly affected by fresh water (originating from the
river Rhine) discharged through the sluices from Lake
IJssel.
Discussion
Within restricted areas, parallel fluctuations in zoobenthos abundance at nearby stations are quite common. For example, nearly half (47%) of the more than
1000 time series (25 species at 15 sites) compared within
the Balgzand area (50 km2) showed high similarity
(Beukema and Essink, 1986). For the three undisturbed
stations within the Groningen area (4 km2), the proportion was also around 50% (Essink and Beukema,
1986). When comparing Balgzand and Groningen
(120 km apart), the proportion was only 15%, indicating that patterns become more dissimilar over larger
distances (Beukema and Essink, 1986).
Long-term monitoring studies executed simultaneously at different sites often reveal synchronized
fluctuation patterns. The example of synchronization
of abundance fluctuations of N. hombergii and L.
conchilega over a large Wadden Sea area in response to
mortality induced by cold winters is not a unique
observation. Similar patterns have been observed in
other winter-sensitive species. Among the 29 macrozoobenthic species monitored during the last 25 years on
Balgzand (Beukema, 1989), no less than 12 show
enhanced mortality and reduced abundance after cold
winters (Beukema, 1990). Some of these species are
restricted to special habitats and therefore occur in only
one or two of the sampling areas. However, three belong
to common and often numerous species in the Wadden
Sea, viz. N. hombergii, L. conchilega and Cerastoderma
edule (cf. Beukema et al., 1993). The dynamics of these
species may, therefore, be used to make a general
assessment of possible departures in a local benthic
fauna from the common Wadden Sea pattern.
The positive influence of cold winters on subsequent
recruitment observed in M. balthica is not unusual in
bivalves in coastal areas (Beukema, 1982). In the
Wadden Sea, extraordinarily high spat fall has also been
observed in 1979 and 1987 for Cerastoderma, Mytilus,
and Mya.
A search of the literature revealed synchronized
patterns to be particularly numerous for adjacent
(<10 km) sampling stations (Table 2). Nevertheless,
970
J. J. Beukema et al.
highly similar patterns also occur at distances of well
over 100 km. Examples are the study by Lundälv and
Christie (1986) on various species in subtidal rockyshore areas in Norway and Sweden, the study by
Andersin et al. (1978) on Pontoporeia affinis in the
Gulf of Bothnia between Sweden and Finland, and the
present study.
Since extreme meteorological conditions such as
severe winters are often synchronized over distances of
the order of 1000 km, one may wonder why synchronized fluctuation patterns in abundance are not encountered more often over much larger areas. Winters that
were severe in the Wadden Sea were also extraordinarily
cold in France (cf. Desprez et al., 1991). Nevertheless,
fluctuation patterns in M. balthica (Desprez et al., 1991),
Scrobicularia plana (Essink et al., 1991), and C. edule
(Ducrotoy et al., 1991) differed between the Wadden Sea
and France. In all these cases, the winter-induced synchronization appears to be limited to the Wadden Sea,
suggesting that absolute temperatures are more important than relative temperatures. Temperatures experienced during an unusually cold winter in France are
similar to average winter temperatures in the Wadden
Sea. This may explain why synchronization is limited to
the more northern parts of the distribution area.
Examples of local departures from common fluctuation patterns, such as presented here for N. hombergii
and M. balthica, have been published previously.
Rosenberg (1976) has shown the effect of distance from
a former pulp mill discharge on Thyasira and Polyphysia
populations. Beukema (1995) indicates that relative biomass values of some species were affected by lugworm
dredging in 1 out of 15 sampling stations. Barnett and
Watson (1986) attribute different fluctuation patterns in
Tellina tenuis at two nearby stations to effects of heated
effluents on one of them.
In addition to M. balthica, several other benthic
species on Balgzand appear to have responded positively
to the increased food availability. No less than 11 out of
29 zoobenthic species monitored showed significantly
higher abundance in the 1980s than in the 1970s and, as
a consequence, total zoobenthic biomass doubled during
this period (Beukema, 1989, 1992b).
Clearly, departures from common fluctuation patterns
can be useful in identifying the underlying causes. The
more restricted deviant patterns are geographically, the
more certain we may be about the connection with a
local source of disturbance. However, even when large
areas are involved, geographic delimitation offers a clue
as to the cause of the deviant patterns and would
strengthen the evidence that a particular source of
disturbance has indeed been the agent. As shown above,
the geographic scale of any disturbance can only be
assessed if populations are monitored at a sufficiently
dense network of stations. Therefore, we need monitoring programmes that are both large-scale and long-term.
The COST (6)47 programme was a good start and it
is very unfortunate that so few sampling programmes
have been maintained consistently, because of lack of
long-term commitment of research institutes.
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