Estuarine, Coastal and Shelf Science 86 (2010) 276–282
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss
Consequences of sea water temperature anomalies on a Mediterranean
submarine cave ecosystem
Valeriano Parravicini a, *, Paolo Guidetti b, Carla Morri a, Monica Montefalcone a,
Marco Donato c, Carlo Nike Bianchi a
a
b
c
DipTeRis, Department for the Study of Territory and its Resources, University of Genoa, Corso Europa 26, I-16132 Genoa, Italy
Department of Biological and Environmental Sciences and Technologies, University of Salento, Via Provinciale Monteroni, CoNISMa, I-73100 Lecce, Italy
D’Appolonia Engineering Consulting Company, Via San Nazaro 19, I-16145 Genoa, Italy
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 16 July 2009
Accepted 9 November 2009
Available online 13 November 2009
Thermal anomalies up to 4 C above the climatological mean caused dramatic mass mortalities in
benthic ecosystems of the NW Mediterranean during the summer heat waves of 1999 and 2003.
Information on the sessile communities of the submarine cave of Bergeggi (Ligurian Sea) was taken in
1986 and 2004, i.e. before and after the two thermal events, using wire-frame photography in four
sectors of the cave ecosystem with different morphologies and environmental features. Percent cover
data of growth forms (as descriptors of the structural aspects of cave ecosystem) and feeding guilds
(functional aspects) were analysed by multivariate and univariate techniques. Differences in trophic
organisation and total biotic cover in the four sectors were significant and consistent in the two years.
Thus, food web constraints (such as water confinement and trophic depletion), that are mostly dependent on topography, underwent no major change following the thermal events. On the contrary,
structural aspects changed across time, 3-dimensional growth forms being replaced by 2-dimensional
ones, leading to a general homogenisation of the cave communities. Positive thermal anomalies are
thought to have selectively killed erect and massive organisms, their replacement by encrusting
organisms possibly representing a phase in cave recolonisation. Submarine caves are poorly resilient
ecosystems, and understanding their capacity of recovery after major disturbances is mandatory for their
management and conservation.
Ó 2009 Published by Elsevier Ltd.
Keywords:
submarine caves
mass mortality
growth forms
feeding guilds
recovery
Ligurian Sea
1. Introduction
Global warming and human activities affect community structure and functioning of marine coastal ecosystems (Stachowitsch,
2003; Harley et al., 2006; Halpern et al., 2008), but our knowledge
about pattern and consequences of their change with time
is still inadequate (Bianchi and Morri, 2003). The importance
of coastal ecosystems stems from their naturalistic, sociocultural and economic values (Costanza et al., 1998), and requires proper tools to be selected for their management and
conservation.
Uniqueness and vulnerability are important concepts for setting
conservation priorities (Hiscock et al., 2003; Hiscock and TylerWalters, 2006).
* Corresponding author.
E-mail address: [email protected] (V. Parravicini).
0272-7714/$ – see front matter Ó 2009 Published by Elsevier Ltd.
doi:10.1016/j.ecss.2009.11.004
From this perspective, submarine caves are unique and
vulnerable ecosystems (Sarà, 1976) protected by the European
Community (Habitat Directive 92/43 EEC), but few data about the
impact of environmental change on these marine ecosystems are
available, virtually all studies dealing with spatial or short term
variations (Balduzzi et al., 1989; Martı́ et al., 2004a; Bussotti et al.,
2006). Sea water warming has been shown to induce species shift
in Mediterranean cave mysids (Chevaldonné and Lejeusne, 2003).
These organisms migrate outside at night to feed, thus importing
organic matter into the oligotrophic cave ecosystem: as the
species that is gaining supremacy does not form the huge swarms
typical of the disappearing species, the energy budget of the cave
will likely be modified, with implications for the whole cave
ecosystem functioning (Bianchi, 2007). There have been no
attempts, however, to measure change in the resident, benthic
component of caves. Submarine cave benthic communities are
dominated by sessile invertebrates such as sponges, ascidians,
bryozoans, cnidarians, serpulids and brachiopods (Bianchi,
2003). Their distribution within the cave is primarily dictated by
V. Parravicini et al. / Estuarine, Coastal and Shelf Science 86 (2010) 276–282
gradients of light and water movement (Riedl, 1966; Morri and
Bianchi, 2003; Martı́ et al., 2004b). Such gradients are expressed
differently according to cave morphology. In blind-ending caves
(i.e. cul-de-sac caves) they develop regularly along the exterior–
interior axis, conforming to the classical zonation scheme, but in
tunnel-shaped caves or cavities with complex morphologies this
classical pattern may not be exhibited (Bianchi et al., 1998; Ugolini
et al., 2003).
Climate change has been shown to cause important modifications to the coastal ecosystems of the NW Mediterranean Sea
(Morri and Bianchi, 2001). During the summer heat waves of 1999
and 2003, anomalies of water temperature of up to 4 C above the
climatological mean caused mass mortalities of subtidal rocky reef
invertebrates (Cerrano et al., 2000; Pérez et al., 2000; Garrabou
et al., 2009). No information, however, has been published for
submarine caves.
The submarine cave of Bergeggi (Ligurian Sea, NW Mediterranean) was extensively studied in the 1970s and 1980s (Bianchi
et al., 1986; Sgorbini et al., 1988; Morri et al., 1994), well before
the two above-mentioned positive thermal anomalies. During
a dive in the cave in September 2003, mortality of sponges proved
obvious, with necrotic Agelas oroides (Schmidt) and Chondrosia
reniformis Nardo at the cave entrance and completely dead Petrosia ficiformis (Poiret) in the inner portions. In 2004, we decided
to re-survey a number of stations where quantitative data on the
sessile communities had been taken in 1986 in order to assess
whether significant changes, if any, had occurred after these
anomalies. The Bergeggi cave provides a unique opportunity for
this kind of study not only because of the large amount of preexisting information but also for its complex morphology, which
includes both blind-end and tunnel-shaped portions. For the first
time, therefore, the analysis of sessile communities is not conducted according to the putative major environmental gradient
along the exterior–interior axis (Bianchi et al., 1996), but in
morphological sectors with homogeneous environmental conditions. Similarly, this study provides for the first time a measure of
long-term (18 years) change within a sea cave ecosystem.
277
2. Materials and methods
2.1. Study site
The submarine cave of Bergeggi belongs to a larger karstic system
including also a wide emerged part (Fig. 1). The submerged part is
0–7 m deep and is divided into two branches, both opening under
the vault of Remo’s cavern (Fig. 2): the western branch is more
complex, being composed of a 40 m long gulley with 2 chambers
(First chamber and Lights’ chamber), a main hall and an inner lake
(Lemons’ lake) reaching the surface; the eastern branch essentially
comprised a large lake (lake from the hole). Based on a cluster
analysis of several physical–chemical variables (light intensity,
water temperature, salinity, density, current speed, pH, dissolved
oxygen, and suspended matter), Morri et al. (1994) identified 4
homogeneous sectors, related to morphology, within the submarine
cave: the chambers, the gulley, the hall, and the lakes.
The cave is included within the Marine Protected Area ‘Bergeggi
Island’ and thus should not be subjected to any major anthropogenic disturbances. Visitation by divers is negligible, as it is not
listed among the diving sites of the MPA. Although located few
kilometres downcurrent of an industrial harbour, the MPA has the
best water quality according to environmental indicators of the
European Water Framework Directive 60/2000 (Mangialajo
et al., 2007).
2.2. Choice of cave community descriptors
To evaluate change in the cave ecosystem, structural and functional aspects were preferred over taxonomic composition. Structure was depicted by growth forms, an expression of the strategy of
substratum occupation, function by feeding guilds, describing
trophic organisation (Cocito et al., 1997). The same species often
exhibits different growth forms in different situations, while normally does not change feeding guild.
Based on Jackson (1979) and Connell and Keough (1985), and
taking into account the ratio between the height (h) and the
Fig. 1. Plan view map of the Bergeggi marine cave, with indication of the four sectors investigated (C: chambers; G: gulley; H: hall; L: lakes) and position of the sampling stations in
each sector (1 and 2).
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V. Parravicini et al. / Estuarine, Coastal and Shelf Science 86 (2010) 276–282
Fig. 2. Axonometric representation of the submarine cave of Bergeggi, viewed from
the sea, to show morphological complexity.
radius (r) of the organism, a total of 7 growth forms were identified:
runners, determinate sheets, indeterminate sheets, flattened (h < r)
mounds, hemispherical (h ¼ r) mounds, domed (h > r) mounds and
vines. Runners and sheets (either determinate or indeterminate)
are 2-dimensional, strictly adhering to the substrate, mounds and
vines are 3-dimensional, projecting to some extent into the water
column and producing higher habitat complexity. The additional
category ‘bare substrate’ was also considered.
Considering the mechanisms by which sessile invertebrates
move sea water to get their food (Riedl, 1966; Jørgensen, 1983;
Pandian and Vernberg, 1987a,b), 5 feeding guilds were defined:
passive (e.g. cnidarians) filter feeders, active ciliate (e.g. serpulids),
active ciliate with lophophore (e.g. bryozoans and brachiopods),
active pumping sponges, and active pumping ascidians.
(Se, 4 levels) as a fixed factor and stations (St, 2 levels) as a random
factor nested within sectors. The two sampling years, ‘before’ and
‘after’ the positive temperature anomalies, have been considered
formally as ‘random’, due to the lack of temporal replication within
each of the two levels of this factor. Each analysis used 9999
random permutations and each term found significant was examined, when appropriate, using pair-wise comparisons. Permutational test for multivariate dispersion (PERMDISP; Anderson, 2006)
was also used. The multivariate configuration of both GF and FG
datasets was visualised through non-metric multi-dimensional
scaling ordination (nMDS). Spatial patterns were visualised by
interpolating the 1st axis scores of individual stations, obtained by
principal coordinates (PCO) analysis (Anderson, 2003), across the
cave map. As the interaction Y St(Se) was found significant for
both the GF and the FG datasets (see Results), canonical analysis of
principal coordinates (CAP, Anderson and Willis, 2003) was also
performed on both GF and FG datasets to characterise the differences among stations and between years. Descriptors responsible
for differences among stations were investigated calculating
correlations of original variables with the first two canonical axes
(r1 and r2): the descriptors for which O(r1 þ r2) 0.5 were arbitrarily defined as the main responsible of the observed differences.
2.4.2. Univariate analyses
Three-way analysis of variance (ANOVA) was used for the main
descriptors identified by CAP. Homogeneity of variance was tested
through Levene’s test and data were transformed to log(x þ 1)
whenever necessary. Student–Newman–Keuls’s (SNK) post-hoc
test was used when appropriate.
3. Results
3.1. Multivariate patterns
2.3. Sampling
The sampling design adopted the four sectors defined by Morri
et al. (1994): chambers (C), gulley (G), hall (H) and lakes (L). Within
each sector, 2 sampling stations (1 and 2) were positioned through
random selection on a cave map, and in each station the cover of
sessile epibiota was quantified by wire-frame photography in the
summer of both 1986 and 2004. Photographs were taken using an
invertible film with a Nikonos V camera, an underwater electronic
strobe, and an extension tube mounted on a 35 mm lens. This
close-up system allowed shooting an area of 166 cm2 (Corriero
et al., 2000); a total of 5 replicates were obtained, always from
vertical surfaces, in each station. Slides were analysed under
a binocular microscope by superimposing a transparent grid
divided into 25 equal squares and quantifying cover by giving each
descriptor (i.e. growth forms and feeding guilds) a score ranking
from 0 to 4 in each square and then adding up scores for all squares
where the descriptor was present. An arbitrary value of 0.5 was
assigned to descriptors filling less than one fourth of a square
(Bianchi et al., 2004). The height of the organisms was estimated by
the length of their shade.
2.4. Data management
2.4.1. Multivariate analyses
Two multivariate datasets were obtained, the first using growth
forms (GF) as descriptors, the second feeding guilds (FG). All data
were log(x þ 1) transformed and used to produce two Bray–Curtis
similarity matrices. A permutational multivariate analysis of variance (PERMANOVA; Anderson, 2001) was then applied considering
sampling years (Y, 2 levels) as a random factor, topographic sectors
The sessile communities within the studied cave, both in terms
of growth forms and feeding guilds, displayed significant variability
between stations that were not consistent between the two study
years, as shown by the significant interactions Y St(Se) (Table 1).
Significant differences among sectors were found only for FG,
suggesting that the morphological and environmental features that
distinguish the four sectors affect the trophic organisation of the
communities rather than their dimensional structure. Pair-wise
comparisons revealed significant differences between lakes and
hall (P ¼ 0.034) and between gulley and lakes (P ¼ 0.047). The
Table 1
Results of PERMANOVA performed on growth forms and feeding guilds datasets.
Y: years; Se: sectors; St: stations. Bold characters indicate significant values.
Source
df
SS
MS
Growth forms
Y
Se
St(Se)
Y Se
Y St(Se)
Residuals
1
3
4
3
4
64
1578.2
19 548
8774.3
4527.8
3121.9
13 470
1578.2
6515.9
2193.6
1509.3
780.5
210.5
2.0
1.9
2.8
1.9
3.7
0.1951
0.1619
0.0501
0.1260
0.0002
79
51 020
1
3
4
3
4
64
1339
19 860
3754.5
2399.9
4171.2
6310.3
1339
6620.2
938.6
799.9
1042.8
98.6
1.29
4.4
0.9
0.8
10.6
0.3196
0.0233
0.5499
0.6293
0.0001
79
37 835
Total
Feeding guilds
Y
Se
St(Se)
Y Se
Y St(Se)
Residuals
Total
F
P
V. Parravicini et al. / Estuarine, Coastal and Shelf Science 86 (2010) 276–282
Y Se interaction was not significant for FG, thus highlighting that
differences among sectors were consistent across time.
In the case of GF, multivariate dispersion was lower in 2004 than
in 1986 (PERMDISP P ¼ 0.043), while no differences between the
two years were recorded with FG (P ¼ 0.94). Sectors were better
distinguished with FG than with GF, and such a pattern was
consistent in both years (Fig. 3). Stations in 2004 were closer to
each other than in 1986; as a result, the spatial pattern within the
cave looked more homogeneous in 2004 than in 1986 (Fig. 4).
The main descriptors responsible for the observed differences,
being highly correlated with the canonical axes of CAP, were
runners, determinate sheets, indeterminate sheets, flattened
mounds, vines, bare substrate, in the case of GF; and active ciliate,
active ciliate with lophophore, active pumping sponge, active
pumping ascidians, in the case of FG.
279
1986
3.2. Univariate patterns
Runners were the only growth form indicating that differences
among sectors were not consistent across time (Y Se, df ¼ 3,
F ¼ 19.96, P < 0.01). Their cover increased from 1986 to 2004 in the
chambers, and decreased in the gulley and in the hall.
Determinate sheets (df ¼ 3, F ¼ 11.16, P ¼ 0.039) and vines
(df ¼ 3, F ¼ 9.58, P < 0.048) showed significant differences among
sectors, the former exhibiting lower cover in the lakes than in the
chambers, the latter abounding in the gulley but being absent in the
lakes (SNK test, P < 0.05). Cover of determinate sheets also changed
significantly between the two years (df ¼ 1, F ¼ 33.78, P ¼ 0.015),
being higher in 2004 than in 1986 (SNK test, P < 0.05).
Indeterminate sheets (df ¼ 4, F ¼ 7.29, P < 0.0001), flattened
mounds (df ¼ 4, F ¼ 8.83, P < 0.0001) and vines (df ¼ 4, F ¼ 3.11,
P ¼ 0.021) also showed a significant interaction Y St(Se). Indeterminate sheets’ cover was higher in 2004 than in 1986 in all
sampling stations, whereas the opposite was true for flattened
mounds’ cover: they nearly disappeared, in particular, from station
a
2D stress: 0.08
86H1
04C1
86C1
86G1 04G2
86C2 04C2
04G1
04H2
86L1
86H2
04H1
86G2
86L2
04L2
86H2
04H1
04G
1 86H1
04C1
04G2 86C2
86C1
04C2 86G1
86G2
04H2
04L1
-10
-5
0
5
10
PCO1 scores
15
20
25
Fig. 4. Contour maps of the scores obtained by the 1st axis of the PCO analysis on
growth forms dataset for the two years investigated. PCO1 explained 63.7% of the total
variation.
H1. Vines’ cover was similar in the two years except in station G2,
where it showed higher in 2004.
For bare substrate, both the interaction Y St(Se) and the
difference among sectors were significant (ANOVA, df ¼ 4, F ¼ 29.5,
P < 0.0001 and df ¼ 3, F ¼ 19.4, P ¼ 0.018, respectively). Higher
values of this descriptor were found in the lakes, followed by the
chambers, gulley and hall, in the order (Fig. 5): all these differences
were significant (SNK test, all P < 0.05).
All the FG selected by CAP showed a significant interaction
Y St(Se): active ciliate (ANOVA, df ¼ 4, F ¼ 9.45, P < 0.0001), active
ciliate with lophophore (df ¼ 4, F ¼ 13.48, P < 0.0001), active
pumping sponge (df ¼ 4, F ¼ 9.65, P < 0.0001) and active pumping
ascidians (df ¼ 4, F ¼ 9.85, P < 0.0001). Cover of active pumping
sponges was higher in 2004 than in 1986 (SNK test, all P < 0.05) in
all sectors except in the hall (Fig. 6).
4. Discussion
04L1
b
2004
2D stress: 0.07
86L1
86L2
04L2
Fig. 3. Non-metric multi-dimensional scaling ordination plots of station centroids
in 1986 and 2004 obtained from growth forms (a) and feeding guilds (b) datasets.
C: chambers; G: gulley; H: hall; L: lakes.
This study provided for the first time information about two
little-explored issues: (1) spatial variation in a cave with complex
morphology, and (2) change across a decadal scale period in cave
ecosystem structure and function, here described through growth
forms and feeding guilds in sessile communities.
The adoption of a sampling design based on sectors differing in
morphology and environmental conditions proved more effective
in highlighting the spatial pattern of sessile communities than the
more traditional exterior–interior gradient analysis (Cinelli et al.,
1977; Gili et al., 1986; Balduzzi et al., 1989). In the submarine cave of
Bergeggi, sessile communities differed among sectors especially for
their trophic organisation and for the amount of total biotic cover:
size and morphology of the individual sectors have a primary
influence on water confinement, and hence trophic depletion
(Bianchi et al., 1998). In the case of growth forms, differences
among sectors were blurred by the comparatively high variability
within sectors: although this may be at least partly due to the
small size of our sampling unit (Parravicini et al., 2009), fine scale
variability has been detected also in studies adopting larger
280
V. Parravicini et al. / Estuarine, Coastal and Shelf Science 86 (2010) 276–282
DETERMINATE SHEETS
Cover (%)
RUNNERS
30
6
20
4
10
2
0
0
Cover (%)
INDETERMINATE SHEETS
100
20
80
16
60
12
40
8
20
4
0
0
FLATTENED MOUNDS
Cover (%)
VINES
BARE SUBSTRATE
60
100
40
80
30
60
20
40
10
20
0
C1 C2
Chambers
G1 G2
H1 H2
Gulley
Hall
L1
L2
0
Lakes
C1 C2
Chambers
G1 G2
H1 H2
Gulley
Hall
L1 L2
Lakes
Fig. 5. Percent cover (mean þ SE; n ¼ 5) of the growth forms (including bare substrate) that showed the highest correlations with the first two CAP axes, to illustrate differences
among stations between 1986 (white bars) and 2004 (grey bars). Note different scales on Y axis.
sampling units (Gili et al., 1986; Benedetti-Cecchi et al., 1996;
Bussotti et al., 2006).
Although two points in time represent a rather weak resolution
for a time series, some inferences can be made if change in time is
considered instead of spatial variation. The differences among
sectors found for the trophic organisation were consistent in the
two years examined, thus suggesting that it remained stable over
time. In other words, it is likely that the invariant environmental
constraints due to cave morphology and size do not allow for
change in the ecosystem functioning of the cave, whose food web
remains entirely dependent on the input from outside (Ott and
Svoboda, 1976). On the contrary, a general trend of change was
evident with growth forms. Cover of 2-dimensional forms, such as
sheets, was higher in 2004 than in 1986, while the reverse was
Cover (%)
ACTIVE CILIATE
ACTIVE CILIATE WITH LOPHOPHORE
60
60
40
40
20
20
0
0
Cover (%)
ACTIVE PUMPING SPONGES
ACTIVE PUMPING ASCIDIANS
80
18
60
16
12
40
8
20
4
0
C1 C2
Chambers
G1 G2
H1 H2
Gulley
Hall
L1
L2
Lakes
0
C1 C2
G1 G2
H1 H2
Chambers
Gulley
Hall
L1 L2
Lakes
Fig. 6. Percent cover (mean þ SE; n ¼ 5) of the feeding guilds that showed the highest correlations with the first two CAP axes, to illustrate differences among stations between
1986 (white bars) and 2004 (grey bars). Note different scales on Y axis.
V. Parravicini et al. / Estuarine, Coastal and Shelf Science 86 (2010) 276–282
true for 3-dimensional forms: mounds almost disappeared from
the cave. As bare substrate did not increase between 1986 and
2004, this implies that 3-dimensional forms were replaced by
2-dimensional ones (having however the same feeding strategy).
This resulted in the structural homogenisation of the cave
community, as illustrated by the lower multivariate dispersion in
2004. The mortalities caused by the thermal events of 1999 and
2003 hit especially massive sponges: Petrosia ficiformis, which was
found dead during the field observations of 2003, used to be the
most abundant 3-dimensional species within the Bergeggi cave in
the 1970s and 1980s (see for instance Fig. 1 of Plate I in Bianchi
et al., 1986). Encrusting sponges were less affected or, alternatively,
recovered faster; no signs of mortality of encrusting forms were
evident in September 2003. The stochasticity of cave assemblages
(Balduzzi et al., 1989) should have implied a rather random
recolonisation after the mortality events, as suggested by the high
variability within sectors seen in both growth forms and feeding
guilds.
Changing structural traits (growth forms) while maintaining
unaltered functional ones (feeding guilds) after a major environmental stress may represent a form of compensatory dynamics
(Naeem, 1998; Fischer et al., 2001). Mortalities induced by the high
summer temperatures of 1999 and 2003 have led to a non-random
organisms’ loss (Gross and Cardinale, 2005). Subsequent recolonisation led to the replacement of erect and massive organisms by
encrusting ones, possibly the expression of an early successional
phase in which competition for the substrate is unimportant.
Clearly, long-term studies will be needed to see whether the
vertical growth of sessile organisms in undisturbed conditions will
drive the cave back to its former status. Submarine caves are
thought to be poorly resilient ecosystems (Harmelin, 1980;
Lejeusne and Chevaldonné, 2006): understanding their capacity of
recovery after disturbances is mandatory for their management
and conservation.
Acknowledgements
T. Pérez (Marseilles) participated in the dive of September 2003
and drew our attention to sponge mortality. Research on the
submarine cave of Bergeggi was initiated in 1974 by the GRBM
Cerianthus (Genova); field activities in 1986 were carried out in the
frame of the environmental studies promoted by the municipality
of Vado Ligure, those in 2004 thanks to a collaboration between
DipTeRis and the ‘‘Bergeggi Island’’ MPA. The present work is done
under the aegis of the project ‘The impacts of biological invasions
and climate change on the biodiversity of the Mediterranean Sea’
(Italy–Israel co-operation) funded by the Italian Ministry of the
Environment.
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