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Exploring the causes of spatial variation in an assemblage of benthic invertebrates from a submarine cave with sulphur springs
Journal
ELSEVIER
of Experimental Marine Biology 208 (1996) 153-168
and Ecology.
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
Exploring the causes of spatial variation in an assemblage of benthic invertebrates from a submarine cave with sulphur springs Lisandro Dpzrtimento
Benedetti-Cecchi*, di Scienie dell’Amhrertte
Laura Airoldi, Marco Abbiati, Francesco e de1 Territorio,
Cinelli
Universitri di Ptsa, Vta A Volta 6. l-56126.
Pwa,
Italy
Recetved 20 November
1995; rewed
29 Apnl 1996; accepted 24 May 1996
Abstract In this study we tested possible explanations concerning the spatial distribution of organisms in a submarme cave (Snow Hall, Grotta Azzurra Cave) influenced by sulphur-water springs. The major goals of the study were: (1) to determine wheibrr the effects on other Invertebrates due to the removal of sponges were conststent across positions in the Snow Hall: (2) to contrast the performance of two sponges and one cnidarian in different sites within the Azzurra Cave and, in the case of the cnidarian, also in other caves not affected by sulphurous activity. and (3) to examine patterns of colonisation of cleared surfaces at different distances from the entrance of the Snow Hall and at different distances from the boundary between sea and sulphur water. The removal of the massive sponge Geodia cydonium from the vault significantly increased the abundance of other invertebrates and patterns were consistent across positions; in contrast, the removal of the smaller sponge PetrosiaJiciformis from the sides of the Snow Hall had little effect. Patterns of growth of Geodia cydonium did not differ among positions, nor among replicated areas wtthin posttions, while significant differences among replicated areas withm each of the two sides of the Snow Hall occurred for Petrosia jiciformis. Patterns of mortality of the cnidarian Astroides calyculuris differed largely among areas within sites, and a trend toward a greater mortality in the inner part of the Snow Hall was evident. Early patterns of colonisation were very patchy, and neither position nor the distance from the boundary affected the abundance of recrutts in cleared plots. Several potential processes that might have determined the observed results are discussed. The need for further experiments involving comparisons between the Snow Hall and other caves not influenced by thermal springs is also stressed. Kepvords: Environmental Spatial patterns
*Corresponding
heterogeneity;
author. Tel.: ( + 39-50) 500.943,
0022.0981/96/$15.00 P/I SOO22-098
0
Submarine
fax:
caves:
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1996 Elsevier Science B.V. All rights reserved
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experiments;
It
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1. Introduction A major goal of community ecology is to explain the causes of spatial and temporal variation in the distribution and abundance of species in natural systems. Different patterns may result because of variability in the abiotic environment (Barry and Dayton. 199 1; Dunson and Travis, 199 1). in the frequency and intensity of biological interactions (Sih et al.. 1985) and patchiness in the initial supply of propagules (Connell. 1985: Gaines and Roughgarden, 1985; Lewin, 1986; Underwood and Fairweather. 1989). In particular, the interplay between physical and biological processes is likely to account for much of the variation observed in natural assemblages of species (Menge and Sutherland, 1987: Danielson, 1991; Hixon and Menge. 1991). The use of lield experiments is straightforward to address questions about cause-effects relationships and this approach has been widely used to explain patterns of species distribution in marine systems accessible to humans. such as intertidal and shallow subtidal habitats (e.g.. Dayton. 1993: Underwood and Petraitis, 1993). Marine ecologists have been attracted to submarine caves because of the occurrence of strong environmental gradients on spatial scales of a few meters (Riedl. 1966; Ott and Svoboda. 1976: Cinelli et al.. 1977). Changes in the intensity of light and in the hydrodynamic regime are easily perceived as one approaches the interior of a cave. Ecologists have correlated these and other factors (e.g.. features of the water column such as concentration and quality of suspended particulate matter), with patterns of distribution of organisms along the exterior-interior axis (Norton et al., 197 1; Gili et al.. 1986: Balduzzi et al., 1989: Zabala et al., 1989: Fichez. 1990. 1991). However, experimental work in submarine caves is logistically difficult (Benedetti-Cecchi et al., 1996). and this possibly explains the paucity of experimental investigations in these systems. The causes underlying the distribution of cave benthos are. therefore, not well understood. This research is part of a multidisciplinary study on a sublittoral cave at Capo Palinuro (Azzurra Cave), on the south-west coast of Italy (Western Mediterranean). This cave supports a rich assemblage of benthic invertebrates and is characterized by the occurrence of sulphur-water springs in its innermost part. These form a sharp oxicanoxic boundary with the warm sulphurous water above the cooler sea-water. variability in the composition, flow and temperature of the water, and differences m the intensity of light and in trophic inputs may occur at distances ranging from centimeters to tenths of meters (Airoldi and Cinelli, 1996; Southward et al.. 1996: Fitzsimons and Dando. 1996). This heterogeneity is presumed to have strong effects on the distribution of organisms and their interactions, making this cave a unique system. Patterns of distribution have been examined in detail for \ome of the most abundant species in the Snow Hall. the portion of the cave containing the thermal springs (Benedetti-Cecchi et al.. submitted). Spatial heterogeneity was observed in relation to different factors, including distance from the entrance, distance from the thermal boundary. orientation of the rocky surface\ (sides vs. vault) and also among replicated areas (a few meters apart) within each level of these variables. While some of these patterns conform to the hypothesis of a direct effect of the physical environment on the organisms. others do not. For example. the distribution of two cnidarians (Astrordrs
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1.55
calycularis and Leptosammia pruvoti) was negatively correlated with the presence of sponges (Geodia cydonium and Petrosia jiciformis), the abundances also changing from the outer to the inner part of the Snow Hall. In particular, significant statistical interactions between the type of substratum (sponges vs. other) and position were found for both cnidarians, suggesting that effects due to the presence of sponges potentially changed in relation to the distance from the entrance. The strength of these effects might have been influenced by differential recruitment, growth and/or mortality of cnidarians at outer vs. inner positions. In the present study we examine some of the hypotheses outlined above by manipulating some of the most abundant species in the Snow Hall. First we determined the consistency of the effects due to the removal of sponges on other organisms (cnidarians and serpulidea) in different parts of the Snow Hall, in order to clarify whether the presence of sponges affected the abundance and distribution of other organisms at each position. In addition we contrasted the growth of two sponges (Geodia cydonium and Petrosia$ciformis) at different distances from the thermal springs in the Snow Hall, and the mortality of one cnidarian (Astroides calycularis) transplanted either to different sites in the Azzurra Cave and to other caves not influenced by sulphur springs. These analyses should provide a measure of the degree of correlation between the performance of the target species with the thermal environment. Finally, we examined patterns of colonisation of artificially cleared plots in different parts of the Snow Hall and in relation to the distance from the boundary. This experiment tested whether spatial variability in the distribution of species could be explained in terms of different patterns of recruitment.
2. Materials
and methods
2.1. Study site This study was done from November 1993 to May 1995 in the Grotta Azzurra Cave of Capo Palinuro, on the south-west coast of Italy (Western Mediterranean). The cave consists of a double entrance with a, large cavity (named Central Hall) of about 120 000 m3 in volume and with a maximum depth of about 30 m (Alvisi et al., 1994). A smaller cavity (named Snow Hall) opens on the south side of the Central Hall. All experiments were done in the Snow Hall. A main feature of this region of Grotta Azzurra is the occurrence of hot sulphur-water springs (Stuben et al., 1996) forming an oxic-anoxic interface at about 9 m in depth, with the warm (23-24 “C) sulphurous water above the ambient, cooler (14-20 “C) sea water. The springs arise from fissures in the floor located along the east side in the interior part of the Snow Hall. Dense mats of sulphur oxidising bacteria are present on the rocky surfaces of the vault and the sides above the chemocline. In contrast, all the hard substrata below the chemocline support a rich assemblage of epifauna organisms. The most conspicuous species in these areas are sponges (particularly Geodia cydonium and Petrosia jiciformis) and cnidarians (As-
156
L Benrdetti-Crcchrrt (II. I J. E.%pMar. Bwl Ecol. 20X (1996) 15.3-168
troides calyzularis and Leptosammia pruvoti) which may cover up to 100% of the primary substratum (Benedetti-Cecchi et al., submitted). Detailed descriptions of this part of the cave have been reported elsewhere (Southward et al., 1996).
2.2. Experimental
removal of sponges
The effects due to the removal of Geodia cydorzium and Petrosin jc$ormis were investigated in two distinct experiments. The first was initiated in November 1993 and consisted in the removal of Geodia qdonium from each of two areas randomly located at each of two positions (outer vs. inner) on the vault of the Snow Hall. Areas were 8-10 m apart, while the distance among positions was of 15-20 m. In each area (4-6 m’ in size), ten sponges with a basal surface ranging from 200 and 2.50 cm’ were located. and five of them, chosen at random, were removed from the substratum with hammer and chisel. Thus, each area contained five replicates of both control (sponges present) and treatment (sponges removed) plots. These were marked at their comers with epoxy putty (Subcoat S, Veneziani) for subsequent relocation. The effects of the removal of Geodia cydonium were evaluated by comparing the percent coverage of the target species in quadrats of 100 cm’ previously occupied by the sponges in treatment plots, or placed directly over the sponges in control plots. Thus, the area of sampling was slightly smaller than the size of the treatment plots. in order to reduce edge effects. A plexiglass sheet divided into 100 squares 1 cm2 in area was used for sampling. Percent cover values were determined (by a single observer) as the number of quadrats containing each species. Only the central portion of the small squares was scored. Classical dots were not used because of low visibility. Plots were sampled on four different occasions up to May 1995. The epoxy putty provided the reference marks for positioning of the quadrat with reasonable precision in both treatment and control plots. To avoid damage to the sponges in the controls. epizoic organisms present from the beginning of the experiment were not removed. The implications of this for the interpretation of results are considered later. A second experiment involving the manipulation of Petrosiajiczformis was set up in May 1994. In this case sponges were removed from each of two areas randomly located on each of the two sides (east vs. west) of the Snow Hall, where this species is particularly abundant. The east side is very close to the springs of sulphur water, while the west one is about 20 m away. Therefore, an east-west rather than an outer-inner contrast was made with this experiment. Each area contained five experimental (sponges removed) and five control (sponges present) plots scattered at random. Areas were 5-10 m apart and 3-5 m’ in size. Plots were quadrats of 15 X 15 cm marked at their corners with epoxy-putty. Treatments were produced by removing the sponges with a knife. Care was taken not to disturb the other organisms in the quadrats. Because several species could not be detected unless Petrosia was removed. repeated sampling of controls through time was not feasible in this experiment. Therefore quadrats were sampled only at the end of the experiment. in May 1995. At that time the sponges were photographed and removed from the controls, and these were photographed again along with the treatment plots. The slides were projected over a matrix of 100 equally spaced dots and the percent coverage of the target species determined with the point-intercept technique. A surface of 100 cm2 was sampled in the middle of each plot.
L Benedettl-Cecchr
2.3. Patterns calycularis
rt al. I J. Exp. Mur
Biol.
of growth of sponges and transplant
Ecol. 208 (1996)
experiment
153-168
157
of Astroides
The sponges that served as controls in the previous experiments were also used to test the null hypothesis of no differences in patterns of growth among positions (for Geodiu cydonium) and among sides (for Petrosiajiciformis) in the Snow Hall. The three major axes of the former species were measured with a ruler in November 1993 and in May 1995, and growth was expressed in terms of changes in volume. In contrast, growth for the second species was expressed in terms of changes in coverage from May 1994 to May 1995, with estimates obtained from photographs. An additional experiment was set up in October 1994 to test the null hypothesis of no differences in the mortality of Astroides calycularis transplanted to different positions of the Azzurra Cave and to other 2 caves without sulphur water. Clumps of 15-40 polyps were collected at the entrance of the Azzurra Cave with hammer and chisel and transported to the laboratory where they were maintained in aquaria until relocation (within 24 h). Therefore, all clumps were treated similarly in terms of transportation and exposure to air. Sets of three replicate clumps were transplanted to each of three areas chosen at random in each of the following sites: (1) site of collection, (2) outer part of the Snow Hall, (3) inner part of the Snow Hall, (4) inner part of Trombetta Cave, and (5) inner part of Cattedrale Cave. Clumps were re-attached to the substratum with epoxy-putty. This species provided a convenient material for this kind of experiment because of the presence of a carbonate skeleton that could be detached and reattached to the rock without any apparent damage to the polyps (see Section 3). Clumps were retrieved in May 1995 and mortality (the percentage of corallites without the polyp) was recorded for each clump. Transplant experiments of other species were not attempted because of logistical problems. 2.3. Colonisation
experiment
This experiment was begun in February 1994 to investigate patterns of species recruitment and colonisation in relation to position in the Snow Hall and distance from the boundary between sea and sulphur water. Plots were squares of 400 cm2 cleared of resident organisms with hammer and chisel and marked at their corners with epoxyputty. Sets of three replicate plots located at random within areas of about 2 m2 were marked at two distances from the boundary: (1) at the upper level of distribution of macrobenthic organisms (20-30 cm below the chemocline) and (2) about 1.5 m below the boundary, in the sea-water layer. Two random areas were replicated for each distance at each of two positions in the Snow Hall: outer and inner positions. The percent coverage of species was determined by sampling an area of 100 cm’ in each plot in the same way as described for the first experiment (see Section 2.2). Sampling was repeated on three different occasions until May 1995. 2.5. Analysis
of data
Three-way mixed model ANOVAs were used to test for the effects of the removal of sponges on the percent coverage of the target species. In these analyses position (the
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sides in the case of Petrosiu ficiformis) was fixed while areas were random and nested within position (sides). Treatment (fixed) was orthogonal to both areas and position (sides). Two-way nested ANOVAs were used to compare patterns of growth of sponges, with position (sides) fixed and areas random as the nested factor. The same model was used to analyze patterns of mortality of Astroides calpxhris, with sites fixed as the nesting variable and areas random. Finally. for analyses of data on patterns of species colonisation. position and distance from the boundary were considered as fixed orthogonal factors, and areas such as the random variable were nested within each combination of position by distance. Analyses were repeated at single dates. The Cochran’s test was used to verify the assumption of homogeneity of variances, and appropriate transformations were applied to the data when necessary (Winer. 1971; Underwood, 1981).
3. Results Removal of Geodicl cydoniurtz influenced the abundance of three species of cnidarians and tubiculous polychaetes in the Snow Hall (Fig. 1). Only the last date of sampling was analyzed, because variances could not be stabilised early in the experiment. Significant effects of the treatment were found in all cases (Table 1). Given the direction of these effects, the tests for Astroides calycularis and Leptosatmniu pru\,oti must be regarded as slightly conservative as some polyps of both species were present in control plots from
IO
IO
A A. calycdans
8
B: c 1
1nomata
a
61
T
6
20
16I
D Serpulids T
12 8 4 0
N&993
Fig
I
Effects due to the removul
Hall ilt different
of C‘rod~~ c~vdor~rwn on cmdanan\
dlbtanceh from the entrance.
from two rephcatr
areas m each postIon
Data
rare mean
May’94
oci94
and polychaetes
percent coverqr
Ma995
on the wult
( + ISE) of
of the Snow
ten rephcates pooled
I
2 32
I
2 I
df
F
0.036 0.640 0.036 0 304 0914
P
date (May 1995) were analysed.
5.3 48.400” 0.5 4.250 26.5 22 500 I 600 1.9 0.850 01 9.40 None C = 0.30 P > 0.05
MS
calwtlnris
* Tested agamst the pooled term [Areas(P) + Restdual].
Only data from the last samplmg
Postt1on = P Areas(P) = A Treatment = T TXP TXA Restdual Transformatton Cochran’s test
Source of vartatton
Asrrordes
Species
F
28 0.017 13 0.006 18.6 0.010 0.003 5.4 01 0001 0 005 Angular c = 0.33 P > 0.05
MS
C~r~~oplt~lliu ~mwnata
0.237 0.282 0.049 0.145 0.897
P
F
0.049 21.0 0.002 0.3 0.263 59 6 00 0.000 0.6 0.004 0.007 Angular C = 0.36 P > 0.05
MS
Leptosclt?lnrrupruvoti
0.044 0.732 0.016 0.948 0.556
P
4410 0.0 51.2 7.2 0.5
F
0.025 2 16.225 30.625 1.225 8.075 None C = 0.36 P > 0.05
I 1.025
MS
Serpulidea
0.002 0.997 0.019 0.115 0.598
P
Table 1 Results of analyses of vartance on the effects of the removal of Groditr c.vdornrtrn from dtfferent postttons m the Snow Hall and m different areas at each positton, on cmdartans and aerpuhdea
I 2 co
$
3
$
2
2 h a ? k
$
@
s
a
t7 2
$
i3
160
L. Benedettl-Cecchi
et cd I J. E.rp. Mar. Bwl
Ecol
-70x (1996) I_?-168
the beginning of the experiment (Fig. 1A, C). With the exception of Cat-yophyllia inornata. the analyses also revealed significant differences among positions: Astrordes calwularis was more abundant at outer positions, while the opposite occurred for both Leptosammia pruvoti and polychaetes (Fig. 1). No significant interactions among position and treatment were found. even after the power of these tests was increased by pooling procedures (Winer, 197 1). In contrast to the above results, the removal of Petrosia jciforttzis had little effects on the assemblage of benthic invertebrates on the sides of the Snow Hall (Fig. 3). A negative effect due to the removal of thus sponge was found only for Didemtzum candidum (F,,, = 135.5. P = 0.0073). the abundance of this asctdian being also variable among areas (F2,7Z = 3.6, P = 0.037). The cnidarian Polycyathus muellerae showed different patterns of distribution along the two sides of the Snow Hall, being more abundant on the west side far from the suiphur springs (F, 1 = 961 .O. P = 0.001). No other clear pattern emerged from this experiment for the other species investigated (Fig. 2). Patterns of growth of Geodia qdotziutn were consistent among positions and among areas within positions (Fig. 3A. Table 2). Shrinkage was observed in two cases in the outer part of the Snow Hall. Merging of two adjacent sponges also occurred in this position, but only the target one was measured by the end of the study (merging was not completed and the two sponges could be distinguished easily). In contrast, highly significant differences among areas were found for Petrosia fic~f&mis on the east side close to the sulphur sprmg (Fig. 3B. Table 3). Because some of the transplanted clumps of Astroides calww1ari.s could not be relocated by the end of the experiment, only two replicates per area were used in both statistical analyses and graphical presentation. No polyps died in clumps relocated into the site of collection (Fig. 4). indicating that the transplanting procedure did not
0
A tenacmr
P muellerae L. pruvotr
Serpuhdea D candrdum
F1.g. 7. Effects due to the removal of Prtmrc~frcrf~rmrs on benthlc mvertebrates on the side\ of the Snow Hall at dlfferent distances from the sulphur sprmps. Data are from May 1995 (after I2 months from the removal of sponge\) and represent mean percent coverage ( + ISE) of ten repkate\ pooled from two rephcate ared.\ on each ude.
L. Benedetti-Cecchi
Q -
et al
06
3
z>
1
I J Exp. Mar.
Biol
Ecol. 208 (1996)
153-168
161
A: G. cydonium
04
3 .s 2 02 ii L= 3
3
0.0
Inner
Outer
Close
FX
oo-
1
Fig 3. Patterns of growth of sponges m the Snow Hall. (A): Ratios of final vs mmal volumes (natural loganthms) of Geodia cydonium over a period of 18 months at dtfferent dtstances from the entrance of the Snow Hall and in two rephcate areas for each distance. Data are mean values ( + ISE) of five sponges. (B): Rattos of final vs. mlttal percent coverages (natural loganthms) of Prtrosia ficrformrs over 12 months on sides located at two distances (close vs. far) from the sulphur springs and in two rephcate areas for each stde. Data are mean values ( + ISE) of five sponges.
Table 2 Analysts of vanance on spattal vanabdity of growth of Geodta cydomum (from November and Petrosm ficiformrs (from May 1994 and May 1995) m the Snow Hall Source of variatton
df
MS
F
1993 to May 1995)
P
Geodra c~dorzrutn
Posmon Areas(Posmon) Restdual Transformation Cochran’s test
I 2 16
0.1049
1.3 0 0784 1.4 0 0580 Ln C = 0.57, P > 0.05
0.367 0 287
0.0086 0.2 0.0389 19.0 0.0020 Ln c = 0.49, P > 0.05
0.685 0.000
Petrosra jictformrs
Stdes Areas(Stdes) Residual Transformatron Cochran’s tent The natural
logarithms
1 2 16
of the ratto between
final and mttial stzes were used as data entrtes in the analyses.
CONT
SHO
SHI
Ftg. 4. Mortahty of Amwdr~ ~~~/~rdtrr~~ tran\planted to different we\ ot the Auurra Cave and to web not mfluenced by thermal actlwty There were three replute area\ for each \lte and two clumps (30-50 polyps each) per area Data are mean percentage values ( + I SE) CONT. we of collectton (control ). SHO. outer part of the Snow Hall: SHI, mner part of the Snou Hall, TR Trombetta cave. CA, Cnttedrale cace
96-
01
May’94
12 El
May’95
T
c L pmm
May’94 40
Oct’94
0294
May’95
May’94 12,
” 40
E. Eudendnum sp
Oct’94
May’95
Oct’94
May’95
Oct’94
May’95
D A;lfurea
May’94 F Polychaetes
30
0
May’94
Oct’94
May’95
May’94
Ftg 5 Pattern\ ot coIomwt1on of benthlc In\ertebratr\ In plot\ cleaed at two distances from the boundary between sea and wlphur hater at both outer and tnner powons tn the Snow Hall. Data are mean percent coverage ( + ISE) of
1994
0.140 0.007 0.011 0.024 0 004 Angular c = 0.48 P > 0.05
1 I 1 4 16
May 1995 Postnon = P Dtatance = D PxD Areas(P X D) Restdual Transformatton Cochran’s test
0011 0 059 0.034 0.025 0.003
MS
Angular C = 0.42 P > 0.05
I64
I
I 1
df
Transformation Cochran’s test
Positton = P Dtstance = D PXD AreaatP X D) Restdual
Mq
Source of vartatton
Ca~~oph.vllicr itmwrta
Spectes
5.6 0.3 0.4 56
0.4 2.3 1.4 8.5
F
Table 3 Results of analyses of vartance on patterns of recolomaatton at different dtstances from the boundary
0.076 0.612 0 543 0.005
055 1 0.202 0.310 0.000
P
I .6 0.2 0.0 3.6
F
45.375 77.042 77.042 39542 lO.S83 None C=O.l9 P>O.O5
11 1.9 1.9 3.7
None c = 0.48 P > 0.05
6 000 0.667 0.167 3.750 1.042
MS
0.344 0.235 0.235 0 025
0 215 0 695 0.843 0.028
P
0. I 27.1 4.3 0.4
F
sp.
0.0 0.167 1.8 2281 500 0.1 150.000 33.1 1271.250 38.147 None c=o42 P>O.O5
None C = 0.38 P > 0.05
2.04 1 737.042 I 17.042 27.208 67.792
MS
Eudedrium
0.991 0.251 0.749 0.000
0.798 0.006 0.107 0.805
P
2.2 0.6 0.9 4.9
F
> 0.05
2.3 3.9 0.1 9.9
P>O.O5
0.07 1 0.123 0.000 0.032 0003 Angular C = 0.23 P
155.042 45.375 63.375 II ,625 14 542 None c=o37
MS
Serpulidea
0.208 0.119 0.917 0.000
0.215 0.471 0.400 0.009
P
at outer and inner poamonn tn the Snow Hall, in dtfferent areas at each posttton and
Leptosammia prurotr
of eptfauna orgamsms
2
tu 8 = g 3
R E
0 E-
9
; & 3 3 .‘1
R
2 :: s 2
!2 : R ”
164
L. Benedettr-Crcchi
et NI I J. Exp
Mar
Bml
Ecol
208 (1996)
1.5.7-168
introduce artifacts, at least within the range of environmental conditions provided by the control site. The most obvious pattern was the high variability in mortality among areas within sites other than the control (F,,,.,, = 5.1, P = 0.0025). A trend toward a greater mortality in the interior part of the Snow Hall was also evident (Fig. 4). although variability between sites was not significant (F,,,,, = 3.4. P = 0.053). There were large differences in patterns of colonisation of invertebrates among areas within each combination of position by distance from the boundary (Fig. 5). Only two sampling occasions were analyzed (the first and the last date), in order to limit the number of tests on the same hypotheses. Significant differences among areas were found for all the organisms, while a significant effect due to the distance from the boundary was observed only for Eudendriwtz sp. (Table 3). Hydroids were more abundant far from the boundary but this pattern was statistically relevant only in May 1994 (Table 3). The yellow sponge Aplpillu sulft~rea, hydroids and polychaetes showed marked fluctuations in abundance through time, while temporal trends were more consistent for cnidarians (Fig. 5).
4. Discussion The experimental evidence provided by the present study indicates that: (1) the removal of Geodia c_vdoniwrz significantly increased the abundance of other invertebrates, while Petrosia jkifi)rtnis had a positive effect only on D. candidurn; (2) patterns of growth of Geodia cydonium did not differ among positions nor among areas within positions. while significant differences among areas occurred for Petrosia ,jcijortnts; (3) mortality of Astroides calycularis differed largely among areas within sites located in different parts of the Azzurra Cave, and in other caves not influenced by thermal activity. A trend toward a greater mortality in the inner part of the Snow Hall was also evident; (4) early patterns of colonisation of species were very patchy and were not affected by distance from the boundary. 4.1. Interactions
hetrveett sponge.\ and other it~~~er~ehrute.c
Competitive interactions in assemblages of sessile invertebrates have been reported (Jackson. 1977; Buss and Jackson, 1979: Sebens. 1982). The most frequent mechanisms underlying these interactions involve overgrowth (Connell, 1961; SarB, 1970; Buss, 1980) and allelopathy (Jackson and Buss, 1975). In contrast, the effects of Geodia qdotliuttz in the Snow Hall probably were a consequence of preemption of the substratum. A single Geodia cydoniutn could monopolize areas of substratum up to 1000 cm7 and only some tubiculous polychaetes were found below these sponges. In contrast, epizoism was observed for cnidarians and hydroids. but Grodia cydoniutn provided a substratum of low quality for the former organisms. The effects due to the removal of these sponges on hydroids were not reported here; this because hydroids were present on the sponges from the beginning of the experiment and remained more abundant in control plots throughout the study. Thus, results were confounded by initial differences among experimental units. The occurrence of hydroids on Geodia cydoniwn might also
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have confounded the results for cnidarians. The greater abundance of these organisms in treatment plots might have been a consequence of the lack (or lower abundance) of hydroids in plots where the sponges had been removed. Although this question was not addressed formally in the present study, the absence of correlation between the abundance of cnidarians and hydroids in control plots provided indirect evidence for the lack of important interactions among these organisms. While Geodia cydonium is a massive form, tightly connected to the substratum and protruding in the water column up to 60-70 centimeters, Petrosia jkformis is a flat, branched sponge, fixed to the substratum with only some portions of its body. The differences in size and morphology among Geodia cydonium and Petrosia jiciformis might explain the different outcomes of their removal. The experimental results and direct observations indicated that manipulation of Petrosia ficiformis had limited effects because several species of invertebrates persisted among their branches and in the microhabitats between the sponges and the substratum. The relationships among size and/or shape and competitive ability has been pointed out by several authors (Connell, 1961; Dayton, 1971; Sebens, 1982; Wootton, 1993). The general pattern emerging from these studies is the superior competitive ability of the larger organisms. The results of the present study provide further evidence for the relationship between the morphology of an organism and its effects on other species. The effects (or the lack of effects) due to the removal of sponges were consistent across the spatial scales investigated in this study. Although initial tests on interactions between treatment and position (or side in the case of PetrosiaJiciformis), had only 2 df, pooling procedures (Winer, 197 1) were always applicable, increasing the power of these tests. Therefore, while the significance of position suggested the existence of environmental differences between the outer and the inner parts of the Snow Hall, the lack of significant statistical interactions suggested that the consequences due to the removal of sponges were independent of the features of the environment. 4.2. Peflormance
of sponges and cnidarians
The sulphur-water springs provided an additional source of variability for organisms in the Snow Hall. Hypotheses were made relating the distribution and richness of species in this habitat with the authocthonous contribution to trophic inputs due to bacterial production (Southward et al., 1996; Airoldi and Cinelli, submitted). The potential role of other non-trophic effects (either negative due to the presence of toxic compounds or positive due to increased content of silicates or other rare elements) was also recognized (Benedetti-Cecchi et al., submitted). The results of the present study revealed no consistent patterns of growth of sponges living at different positions with respect to the entrance of the Snow Hall and on sides located at different distances from the sulphur springs. The large variability among areas observed for Petrosia jiciformis on the east side only, might well be a consequence of the fact that the springs were close to that side. However, it was not possible to identify a single direction (whether positive or negative) for the effects due to the thermal activity, because of probable interactions with other factors. In fact, the two areas within each side were at two different distances from the entrance of the Snow Hall (as a consequence of randomizing along a side). and
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this might have influenced the ultimate effects of the sulphur water on patterns of growth of Petrosia jiciformis. Similarly. mortality of Astroides calycularis was very patchy in space, either in the Snow Hall and in other caves not influenced by the sulphur springs. Although the causes of this mortality were not identified. results suggested that spatial heterogeneity over small scales is a general feature of submarine caves at this location. and not only a property of the Snow Hall. According to the considerations above, it seems unlikely that further insights on the effects of the thermal environment on the distribution and richness of species in the Snow Hall can be gathered by examining gradients within this habitat. The results reported here do not neglect that the Snow Hall may be a unique cave environment because of the presence of sulphur springs and bacterial trophic inputs (e.g., Southward et al., 1996). Rather, they suggest that a test for this hypothesis must include comparisons between the Snow Hall (possibly including other similar habitats) with caves not influenced by thermal activity.
4.3. Understanding the causes of spatial twiation: vs. patterns in the mature assemblage
initial difSerences in colonisation
The results of this study reveal large differences in the colonisation of species on a scale of few meters (among areas), a pattern consistent with the distribution of species in the mature assemblage (Benedetti-Cecchi et al.. submitted). Differential colonization might have occurred because of spatial variability in the supply of larvae, and/or because of differential early post-settlement mortality. Both processes have been reported as important determinants of spatial variation in marine benthic assemblages (Underwood and Denley, 1984; Connell, 1985). In the Snow Hall, the heterogeneous supply of larvae to areas of substratum might have resulted as a consequence of eddies in the circulation of the water. The hydrodynamic regime in submarine caves is affected by the degree of isolation from the open sea. which. in turn, is a consequence of the geomorphology of the caves. In the Snow Hall. patterns of circulation might have been further complicated by the outflowing of warm water from the springs. Differentiated early post-settlement mortality might also have occurred as a consequence of spatial variability in the distribution of suitable microsites for the larvae. With the exception of Eudendrium sp.. there were no differences in initial colonisation of species between distances from the boundary. This contrasts with patterns observed in the mature assemblage. where the abundance of several species decreased close to the suggesting that much of these sulphur-water (Benedetti-Cecchi et al.. submitted). patterns were not a consequence of initial differences in colonisation. but were determined at later stages of maturation. In contrast. both early and late effects might have been important in determining the lower abundance of Astroides calycularis in the interior part of the Snow Hall, another clear pattern emerging from previous studies (Benedetti-Cecchi et al., submitted). As shown in Fig. 1, early patterns of colonisation of this cnidarian in treatment plots diverged soon after the removal of Geodia qdonium, while the results of the transplant experiment indicated that the interior of the Snow Hall was not a suitable site for adults.
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Acknowledgments This study was funded in part by the EC under MAST programme contract MAS2CT93-0058. We thank Prof. A.J. Southward for critical comments on the manuscript.
References Airoldt, L. and F. Cmelli, 1996. Variability of fluxes of particulate material m a submarine cave wnh chemohthoautotrophic Inputs of organic carbon. Mar. Ecol. Prog. Ser., Vol. 139, pp. 205-217 Atroldi, L. and F. Cinelli, submitted. Sources and btochemtcal composition of suspended parttculate material m a submanne cave with aulphur water springs. Mar. Biol. Alvtsi, M.. F. Barbien, R. Brum. F. Cinelh. P. Colantom, G.F. Grandi and P. Maltoni, 1994. La Grotta Azzurra di Capo Palinuro (Salerno). Mm. 1st. It. Spel. 2nd ser., Vol 6, pp. 51-56. Balduzzi, A.. C.N. Bianchi, F. Boero. R. Cattaneo Vtetti, M. Pansini and M. Sara, 1989. The suspension-feeder communities of a mediterranean sea cave. Scierzt. Mar., Vol. 53, pp. 387-395. Barry, J.P and P.K. Dayton, 1991. Phystcal heterogeneity, and the orgamzatton of manne commumttes. In. Ecolog~al hetrrogenetty, edited by J. Kolasa and S.T.A. Pickett, Springer-Verlag, New York, USA, pp. 269-320. Benedetti-Cecchi. L.. L. Airoldi, M. Abbiati and F. Cmelh. 1996. Estimatmg the abundance of benthtc invertebrates: a comparison of procedures and vanabdity between observers. Mar. Ecol. Prog. Ser., Vol. 138. pp. 93-101. Benedettt-Cecchi, L., L. Airoldt. M. Abbtati and F. Cinelh, submnted. Spatial vanabihty in the distnbution of sponges and cmdanans m a sublittoral marine cave with sulphur water springs.. J. Mar. Biol. Ass U.K Buss, L.W., 1980. Compettttve mtransitivity and size-frequency distributions of Interacting populations. Proc Natl. Acad Sci. U.S.A., Vol. 77, pp 5355-5359 Buss, L.W. and J.B.C. Jackson, 1979. Competttive networks: nontransmve competitive relationshtps in cryptic coral reef environments Am. Nat., Vol. 113. pp. 223-234. Cinelh, F., E. Frest, L. Mazzella, M. Pansini, R. Pronzato and A. Svoboda, 1977. Dtstribution of benthtc phyto- and zoocoenoses along a hght gradient m a superficial marine cave. In, Biology of henthrc organwns. edtted by B.F. Keegan, P. 6’ CCtdtgh and P.J.S. Boaden, Pergamon Press. Oxford, pp. l73- I83 Connell. J.H.. 1961. The Influence of mterspecific competttion and other factors on the distnbutton of the barnacle Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. Connell. J.H , 1985. The consequences of variation m mmal settlement vs. post-settlement mortality m rocky mterttdal commumttes. J Exp. Mar. Biol. Ecol., Vol. 93, pp. I l-45. Danielson, B.J.. 1991. Communittes m a landscape: the Influence of habitat heterogenetty on the mteracttons between spectes. Am. Nat.. Vol. 138, pp. 1105-I 120. Dayton, P.K., 1971. Competition, dtsturbance. and commumty organization: the provision and subsequent utihzation of space m a rocky Intertidal community Ecol. Monoyr., Vol. 41, pp. 351-389. Dayton, P.K., 1992. Commumty landscape: scale and stab&y in hard bottom marme commumttes. In, Aquatic Ecology. Scale. Pattern and Process. edited by P.S. Giller, A.G Hddrew and D.G. Raffaelli, Blackwell, Oxford, UK, pp 289-332 Dunson, W.A. and J. Travis, 1991 The role of abiottc factors in community orgamzation. Am. Nat., Vol. 138, pp. 1067-1091. Ftchez, R., 1990. Decrease m allochthonous organic Inputs m dark submarine caves, connectton wtth lowermg m benthic community richness. Hydrobiologia, Vol. 207, pp. 61-69. Fichez, R.. 1991 Suspended particulate orgamc matter m a Mediterranean submarine cave. Mar Biol , Vol 108, pp 167-174. Fitzsimons. M. and PR. Dando, 1996. Chemtcal charactenstics of the water mass of the Grotta Azzurra (S. Italy): a submanne cave fed by hydrothermal springs. In, Omc-anoxic inferfaces as productwe sites, edited by PR. Dando, MAST Contract CT93-0058, Final Report, Vol. I.
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1985. Larval settlement rate. a leadmg determmant of structure m an Games, SD and .I. Roughgarden. ecologtcal commumty of the marine Intertidal zone. Proc Natl. Acud. Ser. U.S.A . Vol. 82, pp. 37077371 I GIII, J M., T. Rtera and M. Zabala, 1986. Physical and biological gradients tn a submanne cave on the Western Mediterranean coast (north-east Spain). Mar Bml., Vol. 90. pp. 391-297 Htxon. M.A. and B.A. Menge. 1991. Species dtverstty prey refuges modtfy the mteractwe effects of predatton and competitton. T/reov Populut. Biol , Vol. 39. pp. 178-200. Jackson, J.B C., 1977. Competmon on marme hard substrata, the adaptive ~igmticance of sohtary and colomal atrategie\. Am Nat.. Vol. I I I, pp. 743-76X. Jackson, J B C. and L.W. Buss, 1975. Allelopathy and rpattal competttton among coral reef Invertebrates. Proc. Nut/. Acud. SLI. I/S.A..Vol. 72. pp. 5160-5163 Lewm, R., 1986 Supply-side ecology. Scwrce, Vol. 234, pp 25527. Menge. B.A. and J P. Sutherland, 1987 Commumty regulatton vanatton m disturbance, competttton. and predatton m relation to envtronmental stress and recrmtment Am. Nat., Vol. 130. pp. 730-757. Norton. T.A.. F.J. Eblmg and J.A Kttchmg, 1971. Light and the dtstnbutton of orgamsms m a sea cave. In. 4th European Murinr BwlogxuI Swposum. edited by D J. Cnsp, Cambndge Umv Press. London, pp. 409-432. Ott, A and A. Svoboda, 1976. Sea caves as model systems for energy flow atudie\ m pnmary hard bottom communities P.S.Z.N I Mame Ecology, Vol 40. pp. 4777485 Riedl, R.. 1966. B&ogre der Meereshohlen. Paul Parey, Hamburg. 636 pp. Sara, M , 1970. Competition and cooperatton m sponge populations. In. The hrolo,gy of the Porifua. edtted by W.C. Fry, Academic Press, London, pp. 273-284 Sebena. K.P.. 1982. Competttton for space. growth rate. reproducttve output, and escape m stze. Awr. Nat, Vol. 120, pp. l89- 197 Sth, A.. P.H Crowley, M A. McPeek. J.W Petranka and K Strohmeter, 1985. Predatton, competmon and prey commumties a revtew of tield experiments Awm Rrv ELO/ Syu, Vol. 16. pp. 269-31 I. Southward, A J.. M.C. Kenmcutt, J Alcala-Herrera. M Abbtatt, L. Atroldt. F. Cmelh, C.N Btanchi. C. Morn and E.C. Southward, 1996. On the biology of wbmarme caves wtth sulphur spnngs: appratsal of “C/“C rattos as a guide to trophtc relattons J. Mu. Bm/ Ass. U.K.. Vol. 76, pp. 765-285 Stuben. D ,G Wmckler. R Bayer, S. Braun. P Sedwtck, P Colantom, 1996 Shallow submanne geothermal sttes m caves of Capo Pahnuro (Italy). In. O.w-wmxrc ~rrferj&e~ (IAproducrrvr .srter. edited by P.R Dando, MAST Contract CT93-0058, Final Report. Vol II Underwood, A.J.. 1981 Techmques of analyst\ of variance m expertmental manne btology and ecology OcecmoRr. Mar. Bml Annu Rev , Vol. 19. pp. 513-605 Underwood. A.J and E.J. Denley. 1984 Paradtgma. explanations and generahzattons m models for the structure of mterttdal communities on rocky shores. In. Ecolog~al communitre.\ conceptual mues ad the ev~drnce. edtted by D R Strong, D. Simberloff. LG. Abele and A.B. Thistle, Prmceton Umversity Monograph, Prmceton Umv. Press. pp. I5 I - 180. Underwood, A.J. and P.G. Fairweather, 1989. Supply-\ide ecology and benthtc marme assemblages. Trend., Ecol. Ewl.. Vol 4. pp. 16-20. Underwood, A.J. and P.S. Petram\. 1993. Structure of mtertidal assemblages m dtfferent locations: how can local processes be compared” In, Sprcre., direr\-rty wz ecolo,q:rccrlcommunrtres, edtted by R Rtcklefs and D. Schluter. Umv Chtcago Press. pp 3X-51. Wmer, B.J., 197 I Statrstmzl princrples m e~~perrmentul desr,gvw. McGraw-HtII Kogakusha, Tokyo, second edmon, 907 pp. Wootton, J.T., 1993. SiLe-dependent competition. effects on the dynamtcs V’I the end pomt of mussel bed succession. Ecoloyv. Vol. 74, pp. 195-206. Zabala. M., T. Rtera, J M. Gth. M. Barange. A. Lobo and J Petiuelas, IYXY.Water flow. trophtc depletion. and benthtc macrofauna impoverishment m a wbmarme cave from the western Mediterranean. PSZ N I M~trmr Ecolo,qy. Vol. IO. pp 271-287
ELSEVIER
of Experimental Marine Biology 208 (1996) 153-168
and Ecology.
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY
Exploring the causes of spatial variation in an assemblage of benthic invertebrates from a submarine cave with sulphur springs Lisandro Dpzrtimento
Benedetti-Cecchi*, di Scienie dell’Amhrertte
Laura Airoldi, Marco Abbiati, Francesco e de1 Territorio,
Cinelli
Universitri di Ptsa, Vta A Volta 6. l-56126.
Pwa,
Italy
Recetved 20 November
1995; rewed
29 Apnl 1996; accepted 24 May 1996
Abstract In this study we tested possible explanations concerning the spatial distribution of organisms in a submarme cave (Snow Hall, Grotta Azzurra Cave) influenced by sulphur-water springs. The major goals of the study were: (1) to determine wheibrr the effects on other Invertebrates due to the removal of sponges were conststent across positions in the Snow Hall: (2) to contrast the performance of two sponges and one cnidarian in different sites within the Azzurra Cave and, in the case of the cnidarian, also in other caves not affected by sulphurous activity. and (3) to examine patterns of colonisation of cleared surfaces at different distances from the entrance of the Snow Hall and at different distances from the boundary between sea and sulphur water. The removal of the massive sponge Geodia cydonium from the vault significantly increased the abundance of other invertebrates and patterns were consistent across positions; in contrast, the removal of the smaller sponge PetrosiaJiciformis from the sides of the Snow Hall had little effect. Patterns of growth of Geodia cydonium did not differ among positions, nor among replicated areas wtthin posttions, while significant differences among replicated areas withm each of the two sides of the Snow Hall occurred for Petrosia jiciformis. Patterns of mortality of the cnidarian Astroides calyculuris differed largely among areas within sites, and a trend toward a greater mortality in the inner part of the Snow Hall was evident. Early patterns of colonisation were very patchy, and neither position nor the distance from the boundary affected the abundance of recrutts in cleared plots. Several potential processes that might have determined the observed results are discussed. The need for further experiments involving comparisons between the Snow Hall and other caves not influenced by thermal springs is also stressed. Kepvords: Environmental Spatial patterns
*Corresponding
heterogeneity;
author. Tel.: ( + 39-50) 500.943,
0022.0981/96/$15.00 P/I SOO22-098
0
Submarine
fax:
caves:
Field
Invertebrates;
( + 39-50) 49-694; e-mall. [email protected]
1996 Elsevier Science B.V. All rights reserved
1(96)02650-O
experiments;
It
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1. Introduction A major goal of community ecology is to explain the causes of spatial and temporal variation in the distribution and abundance of species in natural systems. Different patterns may result because of variability in the abiotic environment (Barry and Dayton. 199 1; Dunson and Travis, 199 1). in the frequency and intensity of biological interactions (Sih et al.. 1985) and patchiness in the initial supply of propagules (Connell. 1985: Gaines and Roughgarden, 1985; Lewin, 1986; Underwood and Fairweather. 1989). In particular, the interplay between physical and biological processes is likely to account for much of the variation observed in natural assemblages of species (Menge and Sutherland, 1987: Danielson, 1991; Hixon and Menge. 1991). The use of lield experiments is straightforward to address questions about cause-effects relationships and this approach has been widely used to explain patterns of species distribution in marine systems accessible to humans. such as intertidal and shallow subtidal habitats (e.g.. Dayton. 1993: Underwood and Petraitis, 1993). Marine ecologists have been attracted to submarine caves because of the occurrence of strong environmental gradients on spatial scales of a few meters (Riedl. 1966; Ott and Svoboda. 1976: Cinelli et al.. 1977). Changes in the intensity of light and in the hydrodynamic regime are easily perceived as one approaches the interior of a cave. Ecologists have correlated these and other factors (e.g.. features of the water column such as concentration and quality of suspended particulate matter), with patterns of distribution of organisms along the exterior-interior axis (Norton et al., 197 1; Gili et al.. 1986: Balduzzi et al., 1989: Zabala et al., 1989: Fichez. 1990. 1991). However, experimental work in submarine caves is logistically difficult (Benedetti-Cecchi et al., 1996). and this possibly explains the paucity of experimental investigations in these systems. The causes underlying the distribution of cave benthos are. therefore, not well understood. This research is part of a multidisciplinary study on a sublittoral cave at Capo Palinuro (Azzurra Cave), on the south-west coast of Italy (Western Mediterranean). This cave supports a rich assemblage of benthic invertebrates and is characterized by the occurrence of sulphur-water springs in its innermost part. These form a sharp oxicanoxic boundary with the warm sulphurous water above the cooler sea-water. variability in the composition, flow and temperature of the water, and differences m the intensity of light and in trophic inputs may occur at distances ranging from centimeters to tenths of meters (Airoldi and Cinelli, 1996; Southward et al.. 1996: Fitzsimons and Dando. 1996). This heterogeneity is presumed to have strong effects on the distribution of organisms and their interactions, making this cave a unique system. Patterns of distribution have been examined in detail for \ome of the most abundant species in the Snow Hall. the portion of the cave containing the thermal springs (Benedetti-Cecchi et al.. submitted). Spatial heterogeneity was observed in relation to different factors, including distance from the entrance, distance from the thermal boundary. orientation of the rocky surface\ (sides vs. vault) and also among replicated areas (a few meters apart) within each level of these variables. While some of these patterns conform to the hypothesis of a direct effect of the physical environment on the organisms. others do not. For example. the distribution of two cnidarians (Astrordrs
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calycularis and Leptosammia pruvoti) was negatively correlated with the presence of sponges (Geodia cydonium and Petrosia jiciformis), the abundances also changing from the outer to the inner part of the Snow Hall. In particular, significant statistical interactions between the type of substratum (sponges vs. other) and position were found for both cnidarians, suggesting that effects due to the presence of sponges potentially changed in relation to the distance from the entrance. The strength of these effects might have been influenced by differential recruitment, growth and/or mortality of cnidarians at outer vs. inner positions. In the present study we examine some of the hypotheses outlined above by manipulating some of the most abundant species in the Snow Hall. First we determined the consistency of the effects due to the removal of sponges on other organisms (cnidarians and serpulidea) in different parts of the Snow Hall, in order to clarify whether the presence of sponges affected the abundance and distribution of other organisms at each position. In addition we contrasted the growth of two sponges (Geodia cydonium and Petrosia$ciformis) at different distances from the thermal springs in the Snow Hall, and the mortality of one cnidarian (Astroides calycularis) transplanted either to different sites in the Azzurra Cave and to other caves not influenced by sulphur springs. These analyses should provide a measure of the degree of correlation between the performance of the target species with the thermal environment. Finally, we examined patterns of colonisation of artificially cleared plots in different parts of the Snow Hall and in relation to the distance from the boundary. This experiment tested whether spatial variability in the distribution of species could be explained in terms of different patterns of recruitment.
2. Materials
and methods
2.1. Study site This study was done from November 1993 to May 1995 in the Grotta Azzurra Cave of Capo Palinuro, on the south-west coast of Italy (Western Mediterranean). The cave consists of a double entrance with a, large cavity (named Central Hall) of about 120 000 m3 in volume and with a maximum depth of about 30 m (Alvisi et al., 1994). A smaller cavity (named Snow Hall) opens on the south side of the Central Hall. All experiments were done in the Snow Hall. A main feature of this region of Grotta Azzurra is the occurrence of hot sulphur-water springs (Stuben et al., 1996) forming an oxic-anoxic interface at about 9 m in depth, with the warm (23-24 “C) sulphurous water above the ambient, cooler (14-20 “C) sea water. The springs arise from fissures in the floor located along the east side in the interior part of the Snow Hall. Dense mats of sulphur oxidising bacteria are present on the rocky surfaces of the vault and the sides above the chemocline. In contrast, all the hard substrata below the chemocline support a rich assemblage of epifauna organisms. The most conspicuous species in these areas are sponges (particularly Geodia cydonium and Petrosia jiciformis) and cnidarians (As-
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troides calyzularis and Leptosammia pruvoti) which may cover up to 100% of the primary substratum (Benedetti-Cecchi et al., submitted). Detailed descriptions of this part of the cave have been reported elsewhere (Southward et al., 1996).
2.2. Experimental
removal of sponges
The effects due to the removal of Geodia cydorzium and Petrosin jc$ormis were investigated in two distinct experiments. The first was initiated in November 1993 and consisted in the removal of Geodia qdonium from each of two areas randomly located at each of two positions (outer vs. inner) on the vault of the Snow Hall. Areas were 8-10 m apart, while the distance among positions was of 15-20 m. In each area (4-6 m’ in size), ten sponges with a basal surface ranging from 200 and 2.50 cm’ were located. and five of them, chosen at random, were removed from the substratum with hammer and chisel. Thus, each area contained five replicates of both control (sponges present) and treatment (sponges removed) plots. These were marked at their comers with epoxy putty (Subcoat S, Veneziani) for subsequent relocation. The effects of the removal of Geodia cydonium were evaluated by comparing the percent coverage of the target species in quadrats of 100 cm’ previously occupied by the sponges in treatment plots, or placed directly over the sponges in control plots. Thus, the area of sampling was slightly smaller than the size of the treatment plots. in order to reduce edge effects. A plexiglass sheet divided into 100 squares 1 cm2 in area was used for sampling. Percent cover values were determined (by a single observer) as the number of quadrats containing each species. Only the central portion of the small squares was scored. Classical dots were not used because of low visibility. Plots were sampled on four different occasions up to May 1995. The epoxy putty provided the reference marks for positioning of the quadrat with reasonable precision in both treatment and control plots. To avoid damage to the sponges in the controls. epizoic organisms present from the beginning of the experiment were not removed. The implications of this for the interpretation of results are considered later. A second experiment involving the manipulation of Petrosiajiczformis was set up in May 1994. In this case sponges were removed from each of two areas randomly located on each of the two sides (east vs. west) of the Snow Hall, where this species is particularly abundant. The east side is very close to the springs of sulphur water, while the west one is about 20 m away. Therefore, an east-west rather than an outer-inner contrast was made with this experiment. Each area contained five experimental (sponges removed) and five control (sponges present) plots scattered at random. Areas were 5-10 m apart and 3-5 m’ in size. Plots were quadrats of 15 X 15 cm marked at their corners with epoxy-putty. Treatments were produced by removing the sponges with a knife. Care was taken not to disturb the other organisms in the quadrats. Because several species could not be detected unless Petrosia was removed. repeated sampling of controls through time was not feasible in this experiment. Therefore quadrats were sampled only at the end of the experiment. in May 1995. At that time the sponges were photographed and removed from the controls, and these were photographed again along with the treatment plots. The slides were projected over a matrix of 100 equally spaced dots and the percent coverage of the target species determined with the point-intercept technique. A surface of 100 cm2 was sampled in the middle of each plot.
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of Astroides
The sponges that served as controls in the previous experiments were also used to test the null hypothesis of no differences in patterns of growth among positions (for Geodiu cydonium) and among sides (for Petrosiajiciformis) in the Snow Hall. The three major axes of the former species were measured with a ruler in November 1993 and in May 1995, and growth was expressed in terms of changes in volume. In contrast, growth for the second species was expressed in terms of changes in coverage from May 1994 to May 1995, with estimates obtained from photographs. An additional experiment was set up in October 1994 to test the null hypothesis of no differences in the mortality of Astroides calycularis transplanted to different positions of the Azzurra Cave and to other 2 caves without sulphur water. Clumps of 15-40 polyps were collected at the entrance of the Azzurra Cave with hammer and chisel and transported to the laboratory where they were maintained in aquaria until relocation (within 24 h). Therefore, all clumps were treated similarly in terms of transportation and exposure to air. Sets of three replicate clumps were transplanted to each of three areas chosen at random in each of the following sites: (1) site of collection, (2) outer part of the Snow Hall, (3) inner part of the Snow Hall, (4) inner part of Trombetta Cave, and (5) inner part of Cattedrale Cave. Clumps were re-attached to the substratum with epoxy-putty. This species provided a convenient material for this kind of experiment because of the presence of a carbonate skeleton that could be detached and reattached to the rock without any apparent damage to the polyps (see Section 3). Clumps were retrieved in May 1995 and mortality (the percentage of corallites without the polyp) was recorded for each clump. Transplant experiments of other species were not attempted because of logistical problems. 2.3. Colonisation
experiment
This experiment was begun in February 1994 to investigate patterns of species recruitment and colonisation in relation to position in the Snow Hall and distance from the boundary between sea and sulphur water. Plots were squares of 400 cm2 cleared of resident organisms with hammer and chisel and marked at their corners with epoxyputty. Sets of three replicate plots located at random within areas of about 2 m2 were marked at two distances from the boundary: (1) at the upper level of distribution of macrobenthic organisms (20-30 cm below the chemocline) and (2) about 1.5 m below the boundary, in the sea-water layer. Two random areas were replicated for each distance at each of two positions in the Snow Hall: outer and inner positions. The percent coverage of species was determined by sampling an area of 100 cm’ in each plot in the same way as described for the first experiment (see Section 2.2). Sampling was repeated on three different occasions until May 1995. 2.5. Analysis
of data
Three-way mixed model ANOVAs were used to test for the effects of the removal of sponges on the percent coverage of the target species. In these analyses position (the
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sides in the case of Petrosiu ficiformis) was fixed while areas were random and nested within position (sides). Treatment (fixed) was orthogonal to both areas and position (sides). Two-way nested ANOVAs were used to compare patterns of growth of sponges, with position (sides) fixed and areas random as the nested factor. The same model was used to analyze patterns of mortality of Astroides calpxhris, with sites fixed as the nesting variable and areas random. Finally. for analyses of data on patterns of species colonisation. position and distance from the boundary were considered as fixed orthogonal factors, and areas such as the random variable were nested within each combination of position by distance. Analyses were repeated at single dates. The Cochran’s test was used to verify the assumption of homogeneity of variances, and appropriate transformations were applied to the data when necessary (Winer. 1971; Underwood, 1981).
3. Results Removal of Geodicl cydoniurtz influenced the abundance of three species of cnidarians and tubiculous polychaetes in the Snow Hall (Fig. 1). Only the last date of sampling was analyzed, because variances could not be stabilised early in the experiment. Significant effects of the treatment were found in all cases (Table 1). Given the direction of these effects, the tests for Astroides calycularis and Leptosatmniu pru\,oti must be regarded as slightly conservative as some polyps of both species were present in control plots from
IO
IO
A A. calycdans
8
B: c 1
1nomata
a
61
T
6
20
16I
D Serpulids T
12 8 4 0
N&993
Fig
I
Effects due to the removul
Hall ilt different
of C‘rod~~ c~vdor~rwn on cmdanan\
dlbtanceh from the entrance.
from two rephcatr
areas m each postIon
Data
rare mean
May’94
oci94
and polychaetes
percent coverqr
Ma995
on the wult
( + ISE) of
of the Snow
ten rephcates pooled
I
2 32
I
2 I
df
F
0.036 0.640 0.036 0 304 0914
P
date (May 1995) were analysed.
5.3 48.400” 0.5 4.250 26.5 22 500 I 600 1.9 0.850 01 9.40 None C = 0.30 P > 0.05
MS
calwtlnris
* Tested agamst the pooled term [Areas(P) + Restdual].
Only data from the last samplmg
Postt1on = P Areas(P) = A Treatment = T TXP TXA Restdual Transformatton Cochran’s test
Source of vartatton
Asrrordes
Species
F
28 0.017 13 0.006 18.6 0.010 0.003 5.4 01 0001 0 005 Angular c = 0.33 P > 0.05
MS
C~r~~oplt~lliu ~mwnata
0.237 0.282 0.049 0.145 0.897
P
F
0.049 21.0 0.002 0.3 0.263 59 6 00 0.000 0.6 0.004 0.007 Angular C = 0.36 P > 0.05
MS
Leptosclt?lnrrupruvoti
0.044 0.732 0.016 0.948 0.556
P
4410 0.0 51.2 7.2 0.5
F
0.025 2 16.225 30.625 1.225 8.075 None C = 0.36 P > 0.05
I 1.025
MS
Serpulidea
0.002 0.997 0.019 0.115 0.598
P
Table 1 Results of analyses of vartance on the effects of the removal of Groditr c.vdornrtrn from dtfferent postttons m the Snow Hall and m different areas at each positton, on cmdartans and aerpuhdea
I 2 co
$
3
$
2
2 h a ? k
$
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s
a
t7 2
$
i3
160
L. Benedettl-Cecchi
et cd I J. E.rp. Mar. Bwl
Ecol
-70x (1996) I_?-168
the beginning of the experiment (Fig. 1A, C). With the exception of Cat-yophyllia inornata. the analyses also revealed significant differences among positions: Astrordes calwularis was more abundant at outer positions, while the opposite occurred for both Leptosammia pruvoti and polychaetes (Fig. 1). No significant interactions among position and treatment were found. even after the power of these tests was increased by pooling procedures (Winer, 197 1). In contrast to the above results, the removal of Petrosia jciforttzis had little effects on the assemblage of benthic invertebrates on the sides of the Snow Hall (Fig. 3). A negative effect due to the removal of thus sponge was found only for Didemtzum candidum (F,,, = 135.5. P = 0.0073). the abundance of this asctdian being also variable among areas (F2,7Z = 3.6, P = 0.037). The cnidarian Polycyathus muellerae showed different patterns of distribution along the two sides of the Snow Hall, being more abundant on the west side far from the suiphur springs (F, 1 = 961 .O. P = 0.001). No other clear pattern emerged from this experiment for the other species investigated (Fig. 2). Patterns of growth of Geodia qdotziutn were consistent among positions and among areas within positions (Fig. 3A. Table 2). Shrinkage was observed in two cases in the outer part of the Snow Hall. Merging of two adjacent sponges also occurred in this position, but only the target one was measured by the end of the study (merging was not completed and the two sponges could be distinguished easily). In contrast, highly significant differences among areas were found for Petrosia fic~f&mis on the east side close to the sulphur sprmg (Fig. 3B. Table 3). Because some of the transplanted clumps of Astroides calww1ari.s could not be relocated by the end of the experiment, only two replicates per area were used in both statistical analyses and graphical presentation. No polyps died in clumps relocated into the site of collection (Fig. 4). indicating that the transplanting procedure did not
0
A tenacmr
P muellerae L. pruvotr
Serpuhdea D candrdum
F1.g. 7. Effects due to the removal of Prtmrc~frcrf~rmrs on benthlc mvertebrates on the side\ of the Snow Hall at dlfferent distances from the sulphur sprmps. Data are from May 1995 (after I2 months from the removal of sponge\) and represent mean percent coverage ( + ISE) of ten repkate\ pooled from two rephcate ared.\ on each ude.
L. Benedetti-Cecchi
Q -
et al
06
3
z>
1
I J Exp. Mar.
Biol
Ecol. 208 (1996)
153-168
161
A: G. cydonium
04
3 .s 2 02 ii L= 3
3
0.0
Inner
Outer
Close
FX
oo-
1
Fig 3. Patterns of growth of sponges m the Snow Hall. (A): Ratios of final vs mmal volumes (natural loganthms) of Geodia cydonium over a period of 18 months at dtfferent dtstances from the entrance of the Snow Hall and in two rephcate areas for each distance. Data are mean values ( + ISE) of five sponges. (B): Rattos of final vs. mlttal percent coverages (natural loganthms) of Prtrosia ficrformrs over 12 months on sides located at two distances (close vs. far) from the sulphur springs and in two rephcate areas for each stde. Data are mean values ( + ISE) of five sponges.
Table 2 Analysts of vanance on spattal vanabdity of growth of Geodta cydomum (from November and Petrosm ficiformrs (from May 1994 and May 1995) m the Snow Hall Source of variatton
df
MS
F
1993 to May 1995)
P
Geodra c~dorzrutn
Posmon Areas(Posmon) Restdual Transformation Cochran’s test
I 2 16
0.1049
1.3 0 0784 1.4 0 0580 Ln C = 0.57, P > 0.05
0.367 0 287
0.0086 0.2 0.0389 19.0 0.0020 Ln c = 0.49, P > 0.05
0.685 0.000
Petrosra jictformrs
Stdes Areas(Stdes) Residual Transformatron Cochran’s tent The natural
logarithms
1 2 16
of the ratto between
final and mttial stzes were used as data entrtes in the analyses.
CONT
SHO
SHI
Ftg. 4. Mortahty of Amwdr~ ~~~/~rdtrr~~ tran\planted to different we\ ot the Auurra Cave and to web not mfluenced by thermal actlwty There were three replute area\ for each \lte and two clumps (30-50 polyps each) per area Data are mean percentage values ( + I SE) CONT. we of collectton (control ). SHO. outer part of the Snow Hall: SHI, mner part of the Snou Hall, TR Trombetta cave. CA, Cnttedrale cace
96-
01
May’94
12 El
May’95
T
c L pmm
May’94 40
Oct’94
0294
May’95
May’94 12,
” 40
E. Eudendnum sp
Oct’94
May’95
Oct’94
May’95
Oct’94
May’95
D A;lfurea
May’94 F Polychaetes
30
0
May’94
Oct’94
May’95
May’94
Ftg 5 Pattern\ ot coIomwt1on of benthlc In\ertebratr\ In plot\ cleaed at two distances from the boundary between sea and wlphur hater at both outer and tnner powons tn the Snow Hall. Data are mean percent coverage ( + ISE) of
1994
0.140 0.007 0.011 0.024 0 004 Angular c = 0.48 P > 0.05
1 I 1 4 16
May 1995 Postnon = P Dtatance = D PxD Areas(P X D) Restdual Transformatton Cochran’s test
0011 0 059 0.034 0.025 0.003
MS
Angular C = 0.42 P > 0.05
I64
I
I 1
df
Transformation Cochran’s test
Positton = P Dtstance = D PXD AreaatP X D) Restdual
Mq
Source of vartatton
Ca~~oph.vllicr itmwrta
Spectes
5.6 0.3 0.4 56
0.4 2.3 1.4 8.5
F
Table 3 Results of analyses of vartance on patterns of recolomaatton at different dtstances from the boundary
0.076 0.612 0 543 0.005
055 1 0.202 0.310 0.000
P
I .6 0.2 0.0 3.6
F
45.375 77.042 77.042 39542 lO.S83 None C=O.l9 P>O.O5
11 1.9 1.9 3.7
None c = 0.48 P > 0.05
6 000 0.667 0.167 3.750 1.042
MS
0.344 0.235 0.235 0 025
0 215 0 695 0.843 0.028
P
0. I 27.1 4.3 0.4
F
sp.
0.0 0.167 1.8 2281 500 0.1 150.000 33.1 1271.250 38.147 None c=o42 P>O.O5
None C = 0.38 P > 0.05
2.04 1 737.042 I 17.042 27.208 67.792
MS
Eudedrium
0.991 0.251 0.749 0.000
0.798 0.006 0.107 0.805
P
2.2 0.6 0.9 4.9
F
> 0.05
2.3 3.9 0.1 9.9
P>O.O5
0.07 1 0.123 0.000 0.032 0003 Angular C = 0.23 P
155.042 45.375 63.375 II ,625 14 542 None c=o37
MS
Serpulidea
0.208 0.119 0.917 0.000
0.215 0.471 0.400 0.009
P
at outer and inner poamonn tn the Snow Hall, in dtfferent areas at each posttton and
Leptosammia prurotr
of eptfauna orgamsms
2
tu 8 = g 3
R E
0 E-
9
; & 3 3 .‘1
R
2 :: s 2
!2 : R ”
164
L. Benedettr-Crcchi
et NI I J. Exp
Mar
Bml
Ecol
208 (1996)
1.5.7-168
introduce artifacts, at least within the range of environmental conditions provided by the control site. The most obvious pattern was the high variability in mortality among areas within sites other than the control (F,,,.,, = 5.1, P = 0.0025). A trend toward a greater mortality in the interior part of the Snow Hall was also evident (Fig. 4). although variability between sites was not significant (F,,,,, = 3.4. P = 0.053). There were large differences in patterns of colonisation of invertebrates among areas within each combination of position by distance from the boundary (Fig. 5). Only two sampling occasions were analyzed (the first and the last date), in order to limit the number of tests on the same hypotheses. Significant differences among areas were found for all the organisms, while a significant effect due to the distance from the boundary was observed only for Eudendriwtz sp. (Table 3). Hydroids were more abundant far from the boundary but this pattern was statistically relevant only in May 1994 (Table 3). The yellow sponge Aplpillu sulft~rea, hydroids and polychaetes showed marked fluctuations in abundance through time, while temporal trends were more consistent for cnidarians (Fig. 5).
4. Discussion The experimental evidence provided by the present study indicates that: (1) the removal of Geodia c_vdoniwrz significantly increased the abundance of other invertebrates, while Petrosia jkifi)rtnis had a positive effect only on D. candidurn; (2) patterns of growth of Geodia cydonium did not differ among positions nor among areas within positions. while significant differences among areas occurred for Petrosia ,jcijortnts; (3) mortality of Astroides calycularis differed largely among areas within sites located in different parts of the Azzurra Cave, and in other caves not influenced by thermal activity. A trend toward a greater mortality in the inner part of the Snow Hall was also evident; (4) early patterns of colonisation of species were very patchy and were not affected by distance from the boundary. 4.1. Interactions
hetrveett sponge.\ and other it~~~er~ehrute.c
Competitive interactions in assemblages of sessile invertebrates have been reported (Jackson. 1977; Buss and Jackson, 1979: Sebens. 1982). The most frequent mechanisms underlying these interactions involve overgrowth (Connell, 1961; SarB, 1970; Buss, 1980) and allelopathy (Jackson and Buss, 1975). In contrast, the effects of Geodia qdotliuttz in the Snow Hall probably were a consequence of preemption of the substratum. A single Geodia cydoniutn could monopolize areas of substratum up to 1000 cm7 and only some tubiculous polychaetes were found below these sponges. In contrast, epizoism was observed for cnidarians and hydroids. but Grodia cydoniutn provided a substratum of low quality for the former organisms. The effects due to the removal of these sponges on hydroids were not reported here; this because hydroids were present on the sponges from the beginning of the experiment and remained more abundant in control plots throughout the study. Thus, results were confounded by initial differences among experimental units. The occurrence of hydroids on Geodia cydoniwn might also
L. Benedetti-Cecchi et al. 1 J Exp. Mar. Biol. Ecol. 208 (1996) 153-168
165
have confounded the results for cnidarians. The greater abundance of these organisms in treatment plots might have been a consequence of the lack (or lower abundance) of hydroids in plots where the sponges had been removed. Although this question was not addressed formally in the present study, the absence of correlation between the abundance of cnidarians and hydroids in control plots provided indirect evidence for the lack of important interactions among these organisms. While Geodia cydonium is a massive form, tightly connected to the substratum and protruding in the water column up to 60-70 centimeters, Petrosia jkformis is a flat, branched sponge, fixed to the substratum with only some portions of its body. The differences in size and morphology among Geodia cydonium and Petrosia jiciformis might explain the different outcomes of their removal. The experimental results and direct observations indicated that manipulation of Petrosia ficiformis had limited effects because several species of invertebrates persisted among their branches and in the microhabitats between the sponges and the substratum. The relationships among size and/or shape and competitive ability has been pointed out by several authors (Connell, 1961; Dayton, 1971; Sebens, 1982; Wootton, 1993). The general pattern emerging from these studies is the superior competitive ability of the larger organisms. The results of the present study provide further evidence for the relationship between the morphology of an organism and its effects on other species. The effects (or the lack of effects) due to the removal of sponges were consistent across the spatial scales investigated in this study. Although initial tests on interactions between treatment and position (or side in the case of PetrosiaJiciformis), had only 2 df, pooling procedures (Winer, 197 1) were always applicable, increasing the power of these tests. Therefore, while the significance of position suggested the existence of environmental differences between the outer and the inner parts of the Snow Hall, the lack of significant statistical interactions suggested that the consequences due to the removal of sponges were independent of the features of the environment. 4.2. Peflormance
of sponges and cnidarians
The sulphur-water springs provided an additional source of variability for organisms in the Snow Hall. Hypotheses were made relating the distribution and richness of species in this habitat with the authocthonous contribution to trophic inputs due to bacterial production (Southward et al., 1996; Airoldi and Cinelli, submitted). The potential role of other non-trophic effects (either negative due to the presence of toxic compounds or positive due to increased content of silicates or other rare elements) was also recognized (Benedetti-Cecchi et al., submitted). The results of the present study revealed no consistent patterns of growth of sponges living at different positions with respect to the entrance of the Snow Hall and on sides located at different distances from the sulphur springs. The large variability among areas observed for Petrosia jiciformis on the east side only, might well be a consequence of the fact that the springs were close to that side. However, it was not possible to identify a single direction (whether positive or negative) for the effects due to the thermal activity, because of probable interactions with other factors. In fact, the two areas within each side were at two different distances from the entrance of the Snow Hall (as a consequence of randomizing along a side). and
166
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-708 (1996)
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this might have influenced the ultimate effects of the sulphur water on patterns of growth of Petrosia jiciformis. Similarly. mortality of Astroides calycularis was very patchy in space, either in the Snow Hall and in other caves not influenced by the sulphur springs. Although the causes of this mortality were not identified. results suggested that spatial heterogeneity over small scales is a general feature of submarine caves at this location. and not only a property of the Snow Hall. According to the considerations above, it seems unlikely that further insights on the effects of the thermal environment on the distribution and richness of species in the Snow Hall can be gathered by examining gradients within this habitat. The results reported here do not neglect that the Snow Hall may be a unique cave environment because of the presence of sulphur springs and bacterial trophic inputs (e.g., Southward et al., 1996). Rather, they suggest that a test for this hypothesis must include comparisons between the Snow Hall (possibly including other similar habitats) with caves not influenced by thermal activity.
4.3. Understanding the causes of spatial twiation: vs. patterns in the mature assemblage
initial difSerences in colonisation
The results of this study reveal large differences in the colonisation of species on a scale of few meters (among areas), a pattern consistent with the distribution of species in the mature assemblage (Benedetti-Cecchi et al.. submitted). Differential colonization might have occurred because of spatial variability in the supply of larvae, and/or because of differential early post-settlement mortality. Both processes have been reported as important determinants of spatial variation in marine benthic assemblages (Underwood and Denley, 1984; Connell, 1985). In the Snow Hall, the heterogeneous supply of larvae to areas of substratum might have resulted as a consequence of eddies in the circulation of the water. The hydrodynamic regime in submarine caves is affected by the degree of isolation from the open sea. which. in turn, is a consequence of the geomorphology of the caves. In the Snow Hall. patterns of circulation might have been further complicated by the outflowing of warm water from the springs. Differentiated early post-settlement mortality might also have occurred as a consequence of spatial variability in the distribution of suitable microsites for the larvae. With the exception of Eudendrium sp.. there were no differences in initial colonisation of species between distances from the boundary. This contrasts with patterns observed in the mature assemblage. where the abundance of several species decreased close to the suggesting that much of these sulphur-water (Benedetti-Cecchi et al.. submitted). patterns were not a consequence of initial differences in colonisation. but were determined at later stages of maturation. In contrast. both early and late effects might have been important in determining the lower abundance of Astroides calycularis in the interior part of the Snow Hall, another clear pattern emerging from previous studies (Benedetti-Cecchi et al., submitted). As shown in Fig. 1, early patterns of colonisation of this cnidarian in treatment plots diverged soon after the removal of Geodia qdonium, while the results of the transplant experiment indicated that the interior of the Snow Hall was not a suitable site for adults.
L. Benedetti-Cecchr
et al. I J. Exp. Mar. Biol Ecol. 208 (1996) 153-168
167
Acknowledgments This study was funded in part by the EC under MAST programme contract MAS2CT93-0058. We thank Prof. A.J. Southward for critical comments on the manuscript.
References Airoldt, L. and F. Cmelli, 1996. Variability of fluxes of particulate material m a submarine cave wnh chemohthoautotrophic Inputs of organic carbon. Mar. Ecol. Prog. Ser., Vol. 139, pp. 205-217 Atroldi, L. and F. Cinelli, submitted. Sources and btochemtcal composition of suspended parttculate material m a submanne cave with aulphur water springs. Mar. Biol. Alvtsi, M.. F. Barbien, R. Brum. F. Cinelh. P. Colantom, G.F. Grandi and P. Maltoni, 1994. La Grotta Azzurra di Capo Palinuro (Salerno). Mm. 1st. It. Spel. 2nd ser., Vol 6, pp. 51-56. Balduzzi, A.. C.N. Bianchi, F. Boero. R. Cattaneo Vtetti, M. Pansini and M. Sara, 1989. The suspension-feeder communities of a mediterranean sea cave. Scierzt. Mar., Vol. 53, pp. 387-395. Barry, J.P and P.K. Dayton, 1991. Phystcal heterogeneity, and the orgamzatton of manne commumttes. In. Ecolog~al hetrrogenetty, edited by J. Kolasa and S.T.A. Pickett, Springer-Verlag, New York, USA, pp. 269-320. Benedetti-Cecchi. L.. L. Airoldi, M. Abbiati and F. Cmelh. 1996. Estimatmg the abundance of benthtc invertebrates: a comparison of procedures and vanabdity between observers. Mar. Ecol. Prog. Ser., Vol. 138. pp. 93-101. Benedettt-Cecchi, L., L. Airoldt. M. Abbtati and F. Cinelh, submnted. Spatial vanabihty in the distnbution of sponges and cmdanans m a sublittoral marine cave with sulphur water springs.. J. Mar. Biol. Ass U.K Buss, L.W., 1980. Compettttve mtransitivity and size-frequency distributions of Interacting populations. Proc Natl. Acad Sci. U.S.A., Vol. 77, pp 5355-5359 Buss, L.W. and J.B.C. Jackson, 1979. Competttive networks: nontransmve competitive relationshtps in cryptic coral reef environments Am. Nat., Vol. 113. pp. 223-234. Cinelh, F., E. Frest, L. Mazzella, M. Pansini, R. Pronzato and A. Svoboda, 1977. Dtstribution of benthtc phyto- and zoocoenoses along a hght gradient m a superficial marine cave. In, Biology of henthrc organwns. edtted by B.F. Keegan, P. 6’ CCtdtgh and P.J.S. Boaden, Pergamon Press. Oxford, pp. l73- I83 Connell. J.H.. 1961. The Influence of mterspecific competttion and other factors on the distnbutton of the barnacle Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. Connell. J.H , 1985. The consequences of variation m mmal settlement vs. post-settlement mortality m rocky mterttdal commumttes. J Exp. Mar. Biol. Ecol., Vol. 93, pp. I l-45. Danielson, B.J.. 1991. Communittes m a landscape: the Influence of habitat heterogenetty on the mteracttons between spectes. Am. Nat.. Vol. 138, pp. 1105-I 120. Dayton, P.K., 1971. Competition, dtsturbance. and commumty organization: the provision and subsequent utihzation of space m a rocky Intertidal community Ecol. Monoyr., Vol. 41, pp. 351-389. Dayton, P.K., 1992. Commumty landscape: scale and stab&y in hard bottom marme commumttes. In, Aquatic Ecology. Scale. Pattern and Process. edited by P.S. Giller, A.G Hddrew and D.G. Raffaelli, Blackwell, Oxford, UK, pp 289-332 Dunson, W.A. and J. Travis, 1991 The role of abiottc factors in community orgamzation. Am. Nat., Vol. 138, pp. 1067-1091. Ftchez, R., 1990. Decrease m allochthonous organic Inputs m dark submarine caves, connectton wtth lowermg m benthic community richness. Hydrobiologia, Vol. 207, pp. 61-69. Fichez, R.. 1991 Suspended particulate orgamc matter m a Mediterranean submarine cave. Mar Biol , Vol 108, pp 167-174. Fitzsimons. M. and PR. Dando, 1996. Chemtcal charactenstics of the water mass of the Grotta Azzurra (S. Italy): a submanne cave fed by hydrothermal springs. In, Omc-anoxic inferfaces as productwe sites, edited by PR. Dando, MAST Contract CT93-0058, Final Report, Vol. I.
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