Mar Biodiv (2009) 39:251–264
DOI 10.1007/s12526-009-0017-4
ORIGINAL PAPER
Habitat structure and biological characteristics of a maerl
bed off the northeastern coast of the Maltese Islands
(central Mediterranean)
Marija Sciberras & Miraine Rizzo & Jael R. Mifsud &
Katielena Camilleri & Joseph A. Borg &
Edwin Lanfranco & Patrick J. Schembri
Received: 22 April 2009 / Revised: 29 May 2009 / Accepted: 2 June 2009 / Published online: 25 June 2009
# Senckenberg, Gesellschaft für Naturforschung and Springer 2009
Abstract Forty stations within a 20 km2 Maltese maerl bed
were sampled by grab to gather data on sediment
granulometry and the percentage mass, sphericity, and
morphotype of rhodoliths. Two stations were monitored
between July 1996 and April 1998 to study temporal
variation in species diversity and abundance of the epi- and
endo-benthos. Maerl was commonest at 51–90 m depth
with 20–39% live rhodoliths in central parts of the maerl
bed, while the peripheral parts had less than 20% live
rhodoliths. The most abundant rhodolith morphotypes were
branching forms and those with a rugged surface. The
maerl bed proved to have high species diversity with 244
animal and 87 algal taxa recorded; molluscs, crustaceans,
and annelids were the dominant taxa in the endobenthos,
and bryozoans and sponges in the epibenthos. Community
composition, rhodolith morphology and sediment characteristics at the two sites were related to differences in the
hydrodynamic regime resulting from seabed topographical
heterogeneity.
Keywords Maerl . Malta . Central Mediterranean .
Coralline algae . Epibenthos . Endobenthos
Electronic supplementary material The online version of this article
(doi:10.1007/s12526-009-0017-4) contains supplementary material,
which is available to authorized users.
M. Sciberras (*) : M. Rizzo : J. R. Mifsud : K. Camilleri :
J. A. Borg : E. Lanfranco : P. J. Schembri
Department of Biology, University of Malta,
Msida MSD2080, Malta
e-mail: marija_sciberras@yahoo.com
P. J. Schembri
e-mail: patrick.j.schembri@um.edu.mt
Introduction
Maerl sediments are characterized by accumulations of
calcareous rhodophytes (mostly Corallinaceae but also
Peyssonneliaceae), that form habitats with a high species
diversity over broad geographical and depth ranges
(Barberá et al. 2003; Foster 2001; Freiwald and Henrich
1994). In European waters, these biogenic sediments occur
throughout the Mediterranean and are patchily distributed
along the Atlantic coast from Portugal to Norway, although
they are rare in the English Channel, Irish Sea, North Sea,
and Baltic Sea (BIOMAERL team 1998; De Grave et al.
2000; Hall-Spencer 1998). Light, salinity and temperature
seem to be the main environmental factors influencing the
distribution of maerl beds (Littler et al. 1991; Steller et al.
2007; Wilson et al. 2004), provided there is sufficient water
motion to prevent rhodolith burial (Marrack 1999; Wilson
et al. 2004).
Maerl beds are biodiversity ‘hot-spots’ as they enhance
biological and functional diversity of coastal sediments
(BIOMAERL Team 1998; Bordehore et al. 2003; Grall
et al. 2006; Jackson et al. 2004; Steller et al. 2003).
Rhodolith-forming algae have been described as ‘ecological
engineers’ (Jones et al. 1994; Steller et al. 2003) as they
provide a variety of ecological niches for a highly diverse
suite of species, including epibenthic, epiphytic, cryptic,
and infaunal species (Amado-Filho et al. 2007; De Grave
1999; De O Figueiredo et al. 2007; Foster et al. 2007; Grall
et al. 2006; Kamenos et al. 2004a; Peña and Bárbara 2008a,
b; Riul et al. 2009; Steller et al. 2003).
Maerl beds are threatened by numerous anthropogenicrelated exploitative activities including dredging, eutrophication, fishing, and mariculture (Ballesteros 2006; Barberá
et al. 2003; Bordehore et al. 2003; Grall and Hall-Spencer
252
2003; Hall-Spencer 1998; Hall-Spencer and Moore 2000;
Massuti et al. 1996; Riul et al. 2008). In the Maltese
Islands, the main threat to maerl beds is from bottom
trawling, although changes in the sedimentary regime due
to coastal development may pose an additional threat
(Barberá et al. 2003; Borg et al. 1999). Loss of maerl
habitat is exacerbated by the slow rate of growth of the
constituent rhodoliths (Blake and Maggs 2003; Bosence
and Wilson 2003), which is far outstripped by anthropogenic extraction and disruption. The conservation value of
these ecologically fragile systems in European waters is
recognized under EU legislation (Council Directive 92/43/
EEC, 1992) and international conventions (Convention for
the protection of the Mediterranean Sea against pollution,
1976; Bern Convention, 1996; OSPAR convention, 1998)
(Airoldi and Beck 2007; Barberá et al. 2003). A special
Action Plan for the protection of Mediterranean coralligenous and maerl assemblages has been recently adopted
within the framework of the United Nations Environment
Programme’s Mediterranean Action Plan (UNEP-MAP)
(Agnesi et al. 2009).
Maerl beds cover large areas off the Maltese Islands at
depths of ca. 40–100 m (Borg et al. 1998; Dimech et al.
2004). Two extensive maerl beds are known to date; one
located in 1993 off the rocky shoal of ‘is-Sikka l-Bajda’ off
the northeastern coast of Malta and extending northeastward off Gozo (Borg et al. 1998), and the other located in
2004 off the southeastern coast of Malta at a maximum
water depth of 85 m (Dimech et al. 2004). Although Borg
et al. (1998) provided the first scientific record of maerl in
the Maltese Islands, local fishermen have long been aware
of the presence of such beds, and commonly refer to mearl
as ramel haj (Maltese for “living sediment”) owing to the
high productivity of such beds.
For effective conservation management of maerl habitats,
in-depth studies on the distribution, biotic diversity and
community structure of maerl beds are required. The aim of
the present work was to determine the spatial extent, physical
characteristics, and taxonomic and functional diversity of the
Maltese maerl bed off the northeastern coast of the Maltese
Islands to provide a basis for future studies designed to better
understand aspects of function, diversity and productivity of
this maerl bed.
Material and methods
Characterization of the maerl bed
In April 1996, 0.1 m2 Van Veen grabs were taken
approximately 0.5 nautical miles apart along 12 transects
laid 1 nautical miles apart and located perpendicular to the
NE coast of the islands of Gozo and Malta (Fig. 1). The
Mar Biodiv (2009) 39:251–264
results of this survey revealed an extensive maerl bed at
30–100 m depth, ca. 10 nautical miles long and between 1
and 3 nautical miles wide, and covering a seabed area of
around 20 km2 (Fig. 1). Rhodoliths collected in the grab
samples were identified on the basis of gross morphology
using Giaccone (1972–1973), Hamel and Lemoine (1953),
and Preda (1908), and a selection of specimens were
checked using a combination of light microscopy and
scanning electron microscopy. Rhodoliths were classified
into six morphotypes (see Fig. 2), and the collective weight
of each morphotype was determined (± 0.1 g) for each grab
sample, and expressed as a percentage of the total sediment
weight. Rhodoliths were divided into non-nucleated rhodoliths, which are composed entirely of coralline algal tissue,
and nucleated rhodoliths, which have a non-algal core of
inorganic or biogenic origin (Foster 2001; Freiwald 1995;
Freiwald and Henrich 1994), and the percentage composition of each was determined. Rhodolith shape was
determined by measuring the longest intercept (a), the
largest axis at right angles to axis a (b), and the widest part
of the plane at right angles to both axes a and b (c), for 50
randomly picked nucleated rhodoliths and 50 non-nucleated
rhodoliths for each station. The ratios b/a and c/b were used
to read sphericity (Ψ) values from the graph given in
Krumbein (1941). Each rhodolith was assigned to one of
the following sphericity classes: ≤0.3, 0.31–0.40, 0.41–
0.50, 0.51–0.60, 0.61–0.70, 0.71–0.80, 0.81–0.90, 0.91–
1.0. Standard granulometric analysis of the non-biogenic
sediment was carried out by sieving samples through nested
test-sieves (Endecott) of mesh sizes 8 mm, 4 mm, 2 mm,
1 mm, 500 µm, 250 µm, 125 µm, and 63 µm, following the
procedure given in Buchanan and Kain (1971).
Characterization of the gross 3-D structure of the maerl bed
Three 10 cm diameter, 15 cm long cores were collected
from Sites 1 and 2 (Fig. 1) by SCUBA divers and lifted
upright to the surface. One core sample from each site was
cast with Crystic Polyester Resin 2-406 PA (Scott Bader,
U.K.) to determine the three-dimensional structure of the
rhodolith bed, the other two cores were frozen at −18°C,
sectioned into 2 cm layers, and dried at 100°C. When dry,
each sediment fraction was graded separately by dry
sieving through nested sieves as detailed above. The
percentage weight of each sediment fraction was used to
calculate the mean, mode and median (D50) particle size,
interquartile deviation (D75–D25), sorting coefficient, kurtosis, skewness and the proportion of gravel, sand and mud,
using the GRADISTAT v.4 software (Blott and Pye 2001).
Six 0.1 m2 Van Veen grab samples were also collected
from each of Sites 1 and 2 during July 1996. For each grab
sample, 50 randomly chosen rhodoliths were weighed and
measured along three perpendicular axes, and the total
Mar Biodiv (2009) 39:251–264
253
Fig. 1 Bathymetry northeast of the Maltese Islands showing the
location of the 12 transects (A–L) and a rocky shoal (Sikka l-Bajda).
Stations along each transect are labelled 1, 2 ...n, where 1 is the station
closest to the coast and n is the furthest one away (in the figure, labels
are given for Transect A only, as an example). Stations where no live
calcareous algae were collected are marked (×) while (●) indicates the
presence of live calcareous algae. Sites 1 and 2 were sampled
repeatedly between 1996 and 1998
Fig. 2 Rhodolith morphotypes: Morph A (rhodoliths with very thin
and fine branches), Morph B (laminar, smooth rhodoliths including
Peyssonnelia sp.), Morph C (spherical rhodoliths having a smooth
surface), Morph D (rhodoliths having a very rugged and rough
surface), Morph E (rhodoliths having long, medium thin branches open branching), Morph F (rhodoliths having short finger-like
branches - closed branching)
254
volume of 50 rhodoliths was obtained by water displacement in a measuring cylinder.
Sampling of biota
Three 0.1 m2 Van Veen grab samples were collected from
Sites 1 and 2 once every 3 months between July 1996 and
April 1998. The samples were sieved through 1 mm sieves,
sorted, and the algae, molluscs, crustaceans, polychaetes
and echinoderms identified to the lowest possible taxon.
Estimates of macrofaunal abundance were expressed as
number of individuals per 0.1 m2 grab, while those of
algae as wet weight (g) per 0.1 m2 grab. For algae with
sediment-binding rhizoids (e.g., Flabellia petiolata), only
the laminae were weighed, and the abundance of species
with fine ramifying filaments that entangle sediment
particles and rhodoliths (e.g., Womersleyella setacea)
was estimated using a 4-point percentage cover scale
(<25%, 25–50%, 51–75%, and >75%). Sixty rhodoliths
from two of the three grab samples collected from Sites 1
and 2 during July and October 1997 and January and April
1998 were examined to determine epifauna growing on
rhodoliths. Estimates of rhodolith epifauna abundance
were expressed as number of epiphytic individuals per
100 cm2 of rhodolith surface. For bryozoans, the whole
colony was taken to represent a single unit. Sphericity was
calculated for a sample of 125 rhodoliths to investigate if
any correlation exists between sphericity and the number
of epiphytic fauna.
Environmental conditions
Physical parameters of the water column, including water
transperancy, temperature, salinity, and total suspended
matter, were measured at Sites 1 and 2 at approximately
monthly intervals, weather permitting. A Secchi disc was
used to measure water transperancy, and a temperature–
salinity probe [Kent EIL 5005] was used to measure the
salinity and temperature at every 5 m depth interval. A
5-l sample of water was collected from 1 m depth below
the surface using a Van Dorn water sampler, and later
filtered under vacuum through a 45 μm cellulose nitrate
membrane of known weight. The filter was dried at 100°C to
determine the amount of suspended solids in the water
column, and then incinerated in a muffle furnace at 550°C to
determine the amount of organic matter.
Data analysis
The 42 stations found to contain live rhodoliths (see Fig. 1
and Appendix 1) were divided into two groups based on a
two-step Cluster analysis (Clusters 1 and 2), using
Schwarz’s Bayesian clustering criterion and percentage
Mar Biodiv (2009) 39:251–264
mass of rhodoliths and depth of station as continuous
variables. One-way analysis of variance (ANOVA) was
used to determine differences in the proportion of rhodoliths and non-biogenic sediment characteristics between the
two clusters. Rhodolith samples were composed primarily
of nucleated rhodoliths (percentage mass of nucleated vs
non-nucleated rhodoliths; 79.06 ± 27.28% vs. 20.94 ±
27.28%, n =40), hence the combined values of nonnucleated and nucleated rhodoliths were used for analysis
of rhodolith sphericity and morphotype. One-way
ANOVAs were used to determine differences between
rhodolith sphericity and water depth for 5 stations
(K1–K5) along a depth gradient and between this
attribute and sampling station position for 11 stations
(A1, B2, C4, D4, E5, F6, G7, H5, I4, J4, K3) at more or
less constant depth (60–71 m). Differences between
rhodolith morphotype (6 levels corresponding to morphs
A–F) and station clusters (Clusters 1 and 2) were
determined using two-way ANOVA.
Temporal and spatial differences in total abundance of
macrofauna were tested using two-way ANOVA. A
dominance index (dm) defined as dm=100(n/N), where n
is the number of specimens of a species and N is the total
number of individuals collected, was used to identify the
dominant species in the maerl bed faunal assemblage. The
dominance index was also calculated for macroalgae, using
wet weight values. Multivariate analysis was carried out
using PRIMER v.6 (Clarke and Warwick 2001) on fourthroot transformed abundance data for macrofauna to produce
a Bray-Curtis sample similarity matrix. The faunal assemblage composition between sampling sites and seasons was
compared using an a priori two-way crossed analysis of
similarity (ANOSIM).
To assess the functional diversity of the maerl bed,
species were grouped in the following feeding categories:
suspension feeders, deposit feeders, macrograzers, micrograzers, predators, scavengers, multifunctional feeders, and
others (comprising commensals, parasites, and one bivalve
species, Solemya togata, that feeds by direct absorption).
Species with insufficient information in the literature on
their feeding biology were assigned to the ‘unknown’
category. Those described to feed both by scavenging and
predation, and by suspension and deposit feeding were
included as separate categories: ‘predator/scavenger’ and
‘suspension/deposit feeder’, respectively. Information on
the feeding ecology of the identified species was mainly
drawn from Day (1967), Gambi et al. (1985), Graham
(1988), Hughes (1986), Kohn (1983), Marshall and Orr
(1960), Morton (1983), Nicol (1967), Pérès (1982), and
Scipione (1999). Kruskal-Wallis tests were used to test for
significant differences in percentage total abundance and
number of species within each feeding category between
Sites 1 and 2.
Mar Biodiv (2009) 39:251–264
Results
Environmental conditions
No significant differences were detected in water temperature, salinity, transperancy, total suspended matter, and
percentage suspended organic matter between Sites 1 and 2.
Mean surface water temperature was 20.96±3.91°C for Site
1 and 21.10±3.90°C for Site 2, and the mean bottom water
temperature was 18.17±1.49°C and 18.76±2.37°C for Sites
1 and 2, respectively. Surface and bottom salinity averaged
37.52±0.17 at both sites. Levels of mean total suspended
matter and suspended organic matter were 1.49±0.35 mg/L
and 32.23±17.84% at Site 1, and 1.71±0.43 mg/L and
37.99±23.27% at Site 2, respectively. Mean water transperancy averaged 23.43±3.42 m at Site 1 and 24.08±
3.82 m at Site 2.
Characterization of the maerl bed
Live maerl-forming calcareous algae were collected from a
depth ranging between 31 m and 103 m (Appendix 1), but
occurred more commonly at a water depth of 51–90 m.
Five maerl-forming algal species were identified from the
study area; four Corallinaceae: Lithothamniom corallioides
(P.L. Crouan & H.M. Crouan) P.L. Crouan & H.M. Crouan,
Phymatolithon calcareum (Pallas) W.H. Adey & D.L.
McKibbin, Neogoniolithon brassica-florida (Harvey)
Setchell & L.R. Mason, and Mesophyllum lichenoides (J.
Ellis) M. Lemoine; and one Peyssonneliaceae: Peyssonnelia
sp. The overall mean percentage mass (± SD) of rhodoliths
was 13.44±11.58%, and reached a maximum of 39%
(Appendix 1). A significant positive correlation, albeit
weak, was found between depth of station and percentage
mass of rhodoliths (Pearson-moment correlation coefficient=
0.345; p=0.029, n=40). Two-step Cluster analysis generated
two clusters: (1) Cluster 1, composed of 13 stations (B2, D4,
E5, F6, G7, G8, H6, I7, J4, J5, J6, K4, K5), and (2) Cluster
2, composed of the remaining 27 stations. Stations in Cluster
1 had higher percentage mass of rhodoliths and percentage
content of gravel (Table 1) and a significantly higher mean
particle diameter (Md) (F=6.26, p=0.017) than stations in
Cluster 2.
Rhodolith shape varied from non-spherical to spherical;
however, for ca. 50% of the rhodoliths, sphericity ranged
between 0.6 and 0.8 (Fig. 3) indicating that rhodoliths show
a tendency towards a spherical shape. Sphericity did not
change significantly with water depth (F=0.72, p=0.58,
n=5), but differed significantly between different sampling
station locations (F=6.5, p<0.001, n=11). Rhodoliths
collected from stations located closer to ‘is-Sikka ilBajda’, particularly those from stations D4, E5, F6, and
G7 (refer to Fig. 1), were found to have higher sphericity
255
Table 1 Mean (± SD) percentage mass of the live rhodoliths (% mass
rhodoliths), water depth (m), mass of gravel (%), mass of sand (%),
mass of mud (%), mean particle diameter (phi), and sorting
coefficient, for the two station clusters generated by two-step cluster
analysis
Sample size (N)
Depth (m)
% mass rhodoliths
Gravel content (%)
Sand content (%)
Mud content (%)
Mean particle diameter (Md)
Sorting coefficient (Qd)
Cluster 1
Cluster 2
13
78.62±15.08
26.35±9.81
58.09±17.71
40.6±17.81
1.31±0.91
−0.58±0.87
1.31±0.32
27
57.56±12.22
7.22±5.76
27.84±13.46
69.80±13.66
2.36±2.54
0.11±0.75
0.94±0.56
values (0.61–0.8), than rhodoliths collected from peripheral
stations (0.41–0.6). The predominant rhodolith morphotypes were morphs D (rhodoliths having a very rugged and
rough surface), E (open branching form) and F (closed
branching form) (Fig. 4). ANOVA using data for rhodolith
percentage mass between Clusters 1 and 2 and rhodolith
morphotype indicated a significant interaction between the
two factors (Table 2). Morphotypes D and F had a higher
percentage mass in Cluster 1 stations (mean depth: 78.62±
15.08 m) compared to Cluster 2 stations (mean depth:
57.56± 12.22 m), which had approximately the same
percentage mass of morphotypes D, E, and F (Fig. 4).
3-D structure of the maerl bed
The core samples revealed a loose layer of sediment down
to about 7 cm from the surface, which was mostly
composed of rhodolith-derived calcareous sand with small
gastropod shells and other biogenic fragments, including
echinoderm spines, bivalve shells, serpulid tubes, bryozoan
tests, and foraminiferans. Interstitial sediment was poorly
sorted, more so at Site 1 than Site 2, and was primarily
composed of medium rhodolith-derived gravel (<2–>1 mm)
and medium and coarse sands (>500 µm) (Table 3).
Sediment particles smaller than 500 µm made up less than
20% of the core samples. Rhodoliths from Site 2 were
larger and heavier than rhodoliths from Site 1 (Table 4).
Characterization of biota
A total of 331 species (244 macroinvertebrates and 87
algae) were collectively recorded from Sites 1 and 2.
Species which could not be identified down to genus or
species level due to lack of taxonomic expertise were given a
higher order taxonomic rank such as family (Phyllodocidae,
Paraonidae, Sabellidae, Nereidae). Appendix 2 presents the
full list of the species identified. Molluscs (namely gastro-
256
Mar Biodiv (2009) 39:251–264
Table 2 Two-way ANOVA results for significance testing of
percentage mass of rhodoliths between station clusters generated by
two-step cluster analysis (Clusters 1 and 2) and morphotypes (Morphs
A–F)
Morphotype
Clusters (1, 2)
Morphotype x Cluster
Error
Fig. 3 Mean percentage frequency distribution of rhodoliths in
different sphericity classes. Error bars represent the 95% confidence
intervals
pods and bivalves), crustaceans, and annelids (particularly
polychaetes) were the dominant taxa in terms of number of
species in the endobenthos (45, 25, 64, and 57, respectively),
and algae, bryozoans, and sponges in the epibenthos (87, 16,
and 14, respectively). The overall number of species was
significantly higher at Site 1 than Site 2 (Table 5), owing in
part to a more diverse macroalgae species assemblage at Site
1 (Table 6). Macroinvertebrate abundance was higher at Site
2, whereas biomass of macroalgae was higher at Site 1
(Table 6). Although macroinvertebrate abundance was
significantly different across seasons (Table 5(b)), no
Fig. 4 Mean percentage mass of rhodoliths for each of the six
morphotypes and the two clusters generated by two-step cluster
analysis (black square Cluster 1, black circle Cluster 2). Error bars
represent the 95% confidence intervals
df
MS
F
P
5
1
5
228
7308.32
70.16
965.53
276.79
26.40
0.25
3.49
< 0.001
0.615
0.005
apparent seasonal pattern was observed. Nonetheless,
there were conspicuous inter-annual differences in macroinvertebrate abundance since values of this attribute were
higher for samples collected during summer 1996 (125.83±
42.54 ind. per grab) than for summer 1997 (65.33 ± 18.80
ind. per grab). A similar trend was observed for autumn
1996 (89.17±37.60 ind. per grab) and autumn 1997 (47.83±
16.92 ind. per grab), and for winter 1997 and winter 1998
(97.83±20.68 and 64±26.12 ind. per grab, respectively).
Macroinvertebrate assemblage composition differed significantly between sites and across seasons (two-way
crossed ANOSIM, Global R for site=0.653, p=0.1%;
Global R for season=0.339, p=0.1%) at the 0.05 level of
significance. Crustaceans, particularly amphipods and
decapods, were well represented at the two sites sampled;
however, they were more abundant at Site 1 (59.33%) than
at Site 2 (42.90%). Conversely, gastropod abundance was
higher at Site 2 (32.68%) than at Site 1 (11.69%), in part
because of the higher abundance of Bittium latreilli at Site 2
(see Table 7). Barleeia unifasciata and Calcinus tubularis
were not recorded from Site 1, while Nereis rava was
absent from Site 2. Species which occurred at a relatively
low abundance at Site 2 (i.e., contributed to less than 1%
of the total abundance at Site 2) but which had a higher
abundance at Site 1, included: Leptochelia savignyi,
Amphitoe ramondi, Echinocyamus pusillus and Gonilia
calligypta (Table 7). Cheirocratus sundevallii contributed
only 0.51% of the total abundance at Site 1 but 2.35% at
Site 2. Flabellia petiolata (% wet wt.=45.9%) was the
dominant macroalga among the macroalgal assemblage
recorded at the two sites sampled (Table 8). Codium bursa
was absent from Site 2 but contributed to 50.8% of the
total wet weight at Site 1, almost certainly due to its large
size and high water content. Womersleyella setacea was
present in 70.6% of the grab samples analysed and
occurred more commonly at Site 1 than at Site 2 (present
in 92.6% of grab samples at Site 1 vs. 41.7% grab samples
at Site 2).
Temporal variation in epiphytic species abundance
within and between sites was almost negligible; however,
species abundance was higher at Site 1 than at Site 2
(Table 9), primarily due to higher density of Annectocyma
Mar Biodiv (2009) 39:251–264
257
samples
Sitescoefficient,
1 and 2. Values
are given
in micrometers,
Table 33 Mean,
Mean,modal
modaland
and
median
median
(D50(D
) particle
diameter
diameter
(µm), (µm),
interquartile
range collected
(D75–D25from
), sorting
skewness,
kurtosis,
percentage
50) particle
–Deach
coefficient,
skewness,
values
within
the2.brackets
are given
in phiin micrometers, values within the
gravel,
interquartile
sand, range
and mud
(D75for
2 cm layer
in the core
sampleskurtosis,
collected from
Sites
1 and
Values are
25), sorting
percentage
brackets
aregravel,
in phi sand, and mud for each 2 cm layer in the core
Site 1
0–2 cm
2–4 cm
4–6 cm
6–8 cm
8–10 cm
10–12 cm
12–14 cm
Site 2
0–2 cm
2–4 cm
4–6 cm
6–8 cm
8–10 cm
10–12 cm
12–14 cm
Mean
Mode
Median
(D50)
IQR
(D75–D25)
Sorting
coefficient
Skewness
Kurtosis
% Gravel
% Sand
% Mud
Sediment
Textural group
1,721.5
(−0.78)
1,133.8
(−0.18)
989.6
(0.02)
1,073.9
(−0.10)
1,158.1
(−0.21)
1,042.8
(−0.06)
891.5
(0.17)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,585.5
(−0.67)
1,164.8
(−0.22)
1,020.4
(−0.03)
1,035.1
(−0.05)
1,276.1
(−0.35)
1,155.9
(−0.21)
965.2
(0.05)
2,992.6
(2.31)
1,718.6
(2.04)
1,348.0
(1.87)
1,897.1
(2.35)
2,148.1
(2.34)
1,608.1
(2.05)
1,220.2
(1.81)
2.63 (1.40)
−0.25
0.60
40.8
58.8
0.4
Sandy gravel
2.94 (1.56)
−0.03
1.03
27.8
71.4
0.8
Gravelly sand
2.91 (1.54)
−0.01
1.15
21.7
77.3
1.0
Gravelly sand
3.25 (1.70)
0.04
0.96
28.1
71.0
0.9
Gravelly sand
3.17 (1.66)
−0.13
0.94
33.5
65.3
1.2
Sandy gravel
3.06 (1.62)
−0.14
1.07
26.2
72.8
1.0
Gravelly sand
2.60 (1.38)
−0.12
1.04
17.9
81.7
0.4
Gravelly sand
1,924.5
(−0.95)
1,257.2
(−0.33)
1,080.3
(−0.11)
848.8
(2.47)
912.8
(0.13)
1,172.0
(−0.23)
987.5
(0.02)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,500.0
(−0.5)
1,753.8
(−0.81)
1,291.9
(−0.37)
1,141.0
(−0.19)
893.2
(0.16)
1,004.2
(−0.01)
1,259.2
(−0.33)
1,098.5
(−0.14)
2,365.5
(1.67)
1,122.2
(1.28)
1,070.8
(1.38)
1121. 7
(1.72)
1,023.4
(1.50)
1,215.6
(1.46)
1,166.0
(1.60)
2.30 (1.20)
−0.20
0.84
43.1
56.8
0.1
Sandy gravel
2.09 (1.06)
−0.09
1.16
21.9
77.8
0.3
Gravelly sand
2.06 (1.05)
−0.12
1.10
16.5
83.0
0.5
Gravelly sand
2.47 (1.31)
−0.07
1.06
15.7
83.4
0.9
Gravelly sand
2.23 (1.16)
−0.19
1.09
12.2
87.2
0.6
Gravelly sand
2.19 (1.13)
−0.17
1.06
22.2
77.5
0.3
Gravelly sand
2.29 (1.19)
−0.18
1.02
17.4
82.3
0.4
Gravely sand
sp. at Site 1 (3.47±2.45 ind. per 100 cm2 at Site 1 vs. 0.05±
0.06 ind. per 100 cm2 at Site 2), and of Mollia patellaria at
Site 2 (0.06±0.16 ind. per 100 cm2 at Site 1 vs. 2.29±1.73
ind. per 100 cm2 at Site 2). Abundance was significantly
Table 4 Maximum length, weight and volume of rhodoliths from six
grab samples collected from Sites 1 and 2 during July 1996. Mean
length, mean weight, and mean volume per rhodolith were calculated
from measurements made for 50 randomly chosen rhodoliths from
each of the 6 grab samples collected from Sites 1 and 2 (i.e., n=300)
Length (mm)
Weight (g)
Volume (cm3)
Maximum
Mean ± SD
Maximum
Mean ± SD
Maximum
Mean ± SD
Site 1
Site 2
39.5
14.12±4.62
16.6
0.33±0.60
7.7
0.16 ( / )
48.60
15.71±6.12
39
1.01±2.01
23
0.49 ( / )
Table 5 Two-way ANOVA results for (a) number of species (S) and
(b) total abundance of species between sites and among sampling
seasons. Encrusting animal forms including bryozoans, sponges and
hydroids were excluded from analysis of number of species, while
encrusting animal forms and algae were excluded from analysis of
abundance
df
MS
(a) Number of species (S)
Site
1
697.69
Season
7
159.83
Site x season
7
78.59
Error
32
72.85
(b) Total abundance (individuals per grab)
Site
1
2,929.69
Season
7
4,900.28
Site x season
7
440.07
Error
32
660.54
F
p value
9.58
2.19
1.08
0.004
0.061
0.399
4.44
7.42
0.67
0.043
< 0.001
0.70
258
Mar Biodiv (2009) 39:251–264
Table 6 Mean values (± SD) of (a) number of species, (b) abundance,
and (c) wet weight for biota recorded from the two sites. Number of
species and abundance excludes encrusting animal forms (Bryozoa,
Porifera, hydroids). Wet weight values do not include all the recorded
algal species (see Material and methods)
Site 1
(a) Number of species
Macroinvertebrates 23.33±9.59
Macroalgae
14.63±5.67
Biota
37.96±8.56
(b) Abundance (individuals per grab)
Macroinvertebrates 65.79±34.12
(c) Wet weight (g per grab)
Macroalgae
15.71±16.46
Site 2
Overall
21.83±8.42
8.5±4.67
30.33±10.03
22.58±8.96
11.56±6.00
34.15±10.00
81.42±37.15
73.60±36.16
7.00±4.70
11.36±12.76
correlated with rhodolith size, surface area and sphericity
(Pearson product-moment correlation coefficient for size:
r=0.47, p<0.01; for surface area: r=0.60, p<0.01; for
sphericity: r = 0.20, p < 0.05) and differed also with
rhodolith shape. Whereas abundance of epiphytic fauna
was highest for laminar rhodoliths (% abundance of
individuals on morph B=34, morph C=13, morph F=9),
epifaunal species richness was higher on closely branched
rhodoliths (number of species on morph B=35, morph C=
29, morph F=41).
Trophic group analysis
Predators were the dominant trophic group in terms of
species richness (24.1%), but deposit feeders were by far
the most abundant trophic group in terms of number of
individuals (42.4%) (Table 10). Multifunctional feeders
were represented by only 12 species, but contributed to
16.8% of the total abundance. Conversely, grazers (microand macrograzers) constituted 14.4% of the non-epiphytic
species diversity, but only 8.2% of the total abundance
(Table 10). The most abundant predatory species were
Lysidice ninetta and Eunice vittata, which contributed to
52.2% of the predators at Site 1 and 70.5% at Site 2.
Bittium latreilli was dominant amongst the deposit feeders,
with a greater contribution at Site 2 (45.1%) than at Site 1
(21.0%). The deposit feeder Leptochelia savignyi (19.9%)
was replaced by its trophic equivalent Barleeia unifasciata
(18.5%) at Site 2. Suspension feeders were represented by
28 species with a dominance of Pteromeris minuta,
Turritella turbona and Argyrotheca cuneata, however, this
trophic group contributed to just 5.5% of the total
(% ab.
(includingcontribution
Bivalvia - B,
G, Crustacea
- C,
Table 77 Species
Species that
thatcontributed
contributedtotoatatleast
least
80%
80%
of of
thethe
totaltotal
animal
animal
abundance.
Thetaxa)
% abundance
of Gastropoda
species to the- total
abundance
at
Polychaeta
- P, -Echinodermata
andCrustacea
Sipuncula- -C,
S) Polychaeta
is given - P,
each site (%The
abundance.
abundance)
% abundance
and to contribution
their respective
of species
taxa (%toab.thetaxa)
total(including
Bivalvia
B, Gastropoda- E
- G,
abundance at each
site Sipuncula
(% abundance)
Echinodermata
- E and
- S) is and
givento their respective taxa
Site 1
% Abundance
% ab. taxa.
Site 2
% Abundance
% ab. taxa.
Bittium latreilli (G)
Cestopagurus timidus (C)
Leptochelia savignyi (C)
Lysianassa costae (C)
Amphitoe ramondi (C)
Galathea intermedia (C)
Maera grossimana (C)
Echinocyamus pusillus (E)
Lysidice ninetta (P)
11.69
11.36
11.10
7.88
7.37
7.29
5.93
5.51
5.08
64.49
16.77
16.40
11.64
10.89
10.76
8.76
65.66
21.72
Bittium latreilli (G)
Cestopagurus timidus (C)
Barleeia unifasciata (G)
Lysidice ninetta (P)
Eunice vittata (P)
Lysianassa costae (C)
Ceradocus semiserratus (C)
Maera grossimana (C)
Calcinus tubularis (C)
23.16
14.09
9.52
9.07
5.33
4.31
4.06
4.00
3.55
56.68
28.28
23.29
50.18
29.47
8.66
8.15
8.03
50.18
Eunice vittata (P)
Nereis rava (P)
Gonilia calliglypta (B)
Ceradocus semiserratus (C)
Anapagurus breviaculeatus (C)
Genocidaris maculata (E)
Pteromeris minuta (B)
Socarnes filicornis (C)
Athanas nitescens (C)
Aspidosiphon (A.) muelleri (S)
Cheirocratus sundevallii (C)
4.92
3.47
3.14
2.80
2.63
2.46
2.12
1.27
1.19
0.85
0.51
22.47
15.36
23.72
4.13
3.88
29.29
16.03
1.88
1.75
90.90
0.75
Galathea intermedia (C)
Athanas nitescens (C)
Aspidosiphon (A.) muelleri (S)
Cheirocratus sundevallii (C)
Genocidaris maculata (E)
Anapagus breviaculeatus (C)
Pteromeris minuta (B)
Socarnes filicornis (C)
Echinocyamus pusillus (E)
Gonilia calliglypta (B)
Amphitoe ramondi (C)
3.05
2.79
2.73
2.35
2.35
2.16
1.84
1.65
0.89
0.76
0.51
28.28
5.61
100
4.71
67.27
4.33
36.25
3.31
25.45
15
1.02
Barleeia unifasciata (G)
Calcinus tubularis (C)
0
0
0
0
Leptochelia savignyi (C)
Nereis rava (P)
0.38
0
0.76
0
Mar Biodiv (2009) 39:251–264
Table 8 Percentage wet weight
of algal species with a contribution greater than or equal to
0.1% of the total wet weight
259
Site 1
% Wet weight
Site 2
% Wet weight
Codium bursa
Flabellia petiolata
Cystoseira corniculata
Vidalia volubilis
Rytiphloea tinctoria
Gracilaria dura
Dictyota dichotoma
Halimeda tuna
Laurencia sp.
Cystoseira sp.
Osmundea pelagosae
50.79
34.18
10.18
2.69
0.78
0.22
0.20
0.20
0.19
0.11
0.10
Flabellia petiolata
Cystoseira corniculata
Dictyota dichotoma
Cystoseira sp.
Vidalia volubilis
Osmundea pelagosae
Gracilaria dura
72.34
10.60
10.36
5.58
0.41
0.21
0.12
sampling stations indicates the presence of moderate water
movement which winnows away the finer particles from the
surface layers of the sediment or prevents their deposition.
Storm-induced bottom currents are an important source of
bottom disturbance for rhodolith movement (Bosellini and
Ginsburg 1971; Di Geronimo and Giaccone 1994; Harris et
al. 1996), and although storms (defined as gale force 10 on
the Beaufort scale) are seldom experienced in the Maltese
Islands, gusts exceeding 34 knots may occur periodically,
mostly between October and March. Although water
currents along the NE coast of Malta are relatively weak,
only reaching a maximum speed of 0.3 ms−1 and a mean
speed of 0.13 ms−1 (measured 6.3 m above the seabed in
water 35 m deep off the northeastern coast of Malta) (Drago
1995), currents may interact with local topographic features
to produce complex flows, for example near headlands
(Geyer and Signell 1990; Wolanski and Hamner 1988),
bays, boulders (Cusson and Bourget 1997; Guichard and
Bourget 1998), and reefs (Black and Moran 1991; Wolanski
and Hamner 1988). The observed coarser nature of the nonbiogenic sediment for stations closer to ‘is-Sikka l-Bajda’
shoal (Cluster 1 stations, Site 2) suggest that these may be
under the influence of a different hydrodynamic regime
than those further away (Cluster 2 stations, Site 1),
potentially offering more favorable conditions for rhodolith
growth as higher percentage mass of live rhodoliths were
abundance. Cestopagurus timidus was the dominant multifunctional feeder, contributing to 68.4% and 57.8% to this
trophic group at Sites 1 and 2, respectively. Dexamine
spinosa and Mitrella scripta were the major macrograzers,
whereas Echinocyamus pusillus and Genocidaris maculata
were the dominant micrograzers.
Discussion
Characterization of the maerl bed
Throughout 1996–1998, the water above the maerl bed had
low amounts of suspended matter (maximum recorded
value=2.92 mg l−1) and consequently was very transparent
(maximum recorded Secchi depth=31.9 m). The high
degree of light penetration can therefore explain the
common occurrence of live coralline algae at a water depth
of 51–90 m, which far exceeds most other maerl beds in the
NE Atlantic that typically occur from low in the intertidal to
a depth of ca. 30 m (Birkett et al. 1998). The higher
occurrence of nucleated rhodoliths suggests in situ settlement and development of propagules, rather than development elsewhere (e.g., in a ‘rhodolith factory’; Freiwald
1995) and transport of broken pieces to the maerl bed. The
overall coarse nature of the non-biogenic sediment at the
Table 9 Total number of
species and mean abundance
(± SD) (individuals per 100 cm2
of rhodolith surface) for each of
the six epiphytic faunal taxa
recorded growing on rhodoliths
Bryozoa
Porifera
Annelida
Foraminifera
Cnidaria
Mollusca
Number of species
Abundance (individuals per 100 cm2 of rhodolith surface)
Site 1
Site 2
Site 1
Site 2
13
12
7
2
2
1
15
14
9
2
2
1
13.97±4.9
3.64±2.40
16.23±8.92
6.60±2.59
2.68±1.08
0.37±0.42
6.91±1.68
2.94±1.47
5.44±4.09
0.71±0.42
0.45±0.27
0.10±0.24
260
Table 10 Raw values and percentage number of individuals in
each trophic group. Data
includes animal species collected from both sites
Mar Biodiv (2009) 39:251–264
Trophic Group
Deposit feeders
Macrograzers
Micrograzers
Multifunctional feeders
Predators
Scavengers
Suspension feeders
Suspension/deposit feeders
Predator/scavenger
Others
Unknown
recorded at stations in the vicinity of the shoal (% mass of
rhodoliths at Cluster 1 stations=26.35±9.81%, Cluster 2
stations=7.22±5.76%, Site 1=5.82%, Site 2=18.35%).
Different intensities of water motion have been shown to
influence rhodolith shape, branching pattern and sphericity
(Bosellini and Ginsburg 1971; Prager and Ginsburg 1989;
Steneck 1986; Steller and Foster 1995). Closely branched
rhodoliths (morph F) were more common at stations closer
to the shoal, while open branched rhodoliths (morph E)
had a higher percentage mass at stations further away from
the shoal (Fig. 4), similarly indicating an increased bottom
instability due to higher energy environment in the vicinity
of the shoal. Our results are in good agreement with
observations by Di Geronimo and Giaccone (1994) and
Steneck (1986), which suggest that spherical, denselybranched rhodoliths are typical of high water movement
regimes, while open-branched rhodoliths are found in
more stable environments. The scarcity of laminar forms
such as morph B may be accounted for by the fact that
laminar forms generally form under relatively calm
conditions, on sediments that have a substantial high
mud content. As the whole study area is poor in muddy
sediments (< 2%), laminar morphotypes are not expected
to be abundant.
3-D structure of the maerl bed
Live rhodoliths formed ca. 2 cm stratum overlying a
moderately to poorly sorted, gravelly sand. The underlying
sediment layer comprised of an upper layer of ca. 7 cm of
loosely packed dead rhodolith thalli with some coarse sand
and a lower layer of hard-packed rhodolith debris and
medium to fine sand. The loosely packed upper layer of
dead rhodolith thalli suggests a good circulation of nutrients
and oxygen, which coupled with the heterogeneous
structure of rhodoliths, increases the number of niches
Number of species
Number of individuals
Raw
Percentage
Raw
Percentage
44
16
12
12
47
6
28
11
3
7
8
22.56
8.21
6.15
6.15
24.10
3.08
14.36
5.64
1.54
3.59
4.10
1465
96
186
580
547
214
191
126
12
21
20
42.37
2.78
5.38
16.77
15.82
6.19
5.52
3.64
0.35
0.61
0.58
available for benthic organisms that utilize the vertical
dimension of the maerl bed (Hall-Spencer 1998; Keegan
1974). Burial of rhodoliths below the porous upper layer
may be due to considerable water movement or bioturbation. Deposit feeders such as Leptochelia savingyi,
Amphitoe ramondi, Galathea intermedia, Maera grossimana, and Nereis rava that were recorded during this
study, may contribute to rhodolith mixing in the surface
sediment while feeding on other benthic organisms.
Bottom-foraging fish such as Mullus surmuletus and
Pagellus erythrinus (known to occur in large populations
on the maerl ground studied) and large deep-burrowing
animals (such as large irregular echinoids whose fragments were recovered from Maltese maerl samples) are
also expected to contribute to bioturbation (e.g., Fischer et
al. 1987a, b); however, this could not be confirmed during
the present study given that the sampling protocol used
was appropriate for collecting macroinvertebrates but not
the megafauna and fishes.
Associated biota
The maerl bed biotic assemblage was equally rich in algae
and fauna typical of both hard and soft substrata.
Rhodoliths, therefore, appear to extend the distribution of
species requiring hard substrata for attachment, that would
otherwise be absent from soft substrata. The faunal
assemblage included (1) burrowing and interstitial forms
that utilize the sediment underlying the rhodoliths and the
interstices between the rhodolith thalli (polychaetes, irregular echinoids, bivalves and amphipods); (2) sessile
epifaunal organisms that utilise the rhodoliths and the
stabilised upper layer of sediment (tube-dwelling polychaetes and crustaceans, byssate bivalves, ascidians,
sponges and bryozoans); and (3) vagile epifauna (decapods
and gastropods).
Mar Biodiv (2009) 39:251–264
Estimates of species richness and abundance are sampledesign dependent, and thus comparisons of species diversity between studies is difficult. Nonetheless, as has been
recorded in studies of tropical and temperate rhodolith beds
(e.g., Bordehore et al. 2003, Foster et al. 2007; Grall et al.
2006; Hinojosa-Arango and Riosmena-Rodríguez 2004;
Steller et al. 2003), our results show that annelids,
crustaceans, and molluscs are the dominant faunal groups
both in terms of abundance and species richness. Within
the rhodolith-associating Crustacea, the amphipods were
the most species-rich and abundant group, followed by the
decapods (Table 7). De Grave (1999) documented 48
species of amphipods, which were found to constitute
95.4% of the total abundance of the crustacean assemblage
collected from the maerl beds at Mannin Bay, Ireland. On
the other hand, Barberá et al. (1999) stated that amphipods
represented only 4.6% of the maerl fauna in Alicante
(Spain), and these maerl beds were dominated by polychaetes and gastropods. Echinoderms did not constitute a
dominant group among the macroinvertebrates collected in
the present study (Table 7); however, a recent video survey
of the Maltese maerl beds showed the crinoid Antedon
mediterranea, the echinoids Centrostephanus longispinus
and Stylocidaris affinis, and the asteroids Echinaster
sepositus and Astropecten sp. to be common megaepifaunal species (unpublished data).
The majority of animal species recorded from the maerl
bed also occur in other infralittoral and circalittoral habitats
(De Grave 1999; Pérès 1967). For example, some 42% of
the bivalves, 49% of the gastropods, and 44% of the
decapod species recorded in the present study have also
been recorded by Howege (1998) and Borg and Schembri
(2000) from seagrass (Posidonia oceanica) meadows.
Similarly, gravel-associated species such as the decapods
Liocarcinus zariqueiyi and Parthenope expansa, the ascidian Rhopalaea neapolitana, and the echinoid Echinocyamus pusillus were also recorded from this maerl bed. This
suggests that maerl-associated biota do not depend on the
live rhodoliths per se but on the rhodolith-derived sediment
and on the complex architecture arising from the gross
morphology of the rhodoliths and their interlinking
(De Grave et al. 2000; Pérès 1967; Rowe et al. 1990).
Flabellia petiolata and the non-indigenous filamentous
rhodophyte Womersleyella setacea, were observed to
grow profusely on rhodoliths, binding the rhodoliths into
a ‘pseudohard’ surface. Although this stabilized surface
layer provides an additional substratum for settlement of
foliose macroalgae on rhodoliths, it may deprive settlement and attachment of interstitial species, reduce the
amount of photosynthetically active radiation reaching the
photosynthetic tissues of the rhodolith-forming algae, and
prevent rhodoliths from turning—a requirement for their
survival.
261
Many studies have consistently verified the importance
of rhodoliths to the associated species (review in AmadoFilho et al. 2007; De O Figueiredo et al. 2007; Foster et al.
2007; Steller et al. 2003). Our observations suggest that
rhodolith surface area and shape play a role in maintaining
a diversity of rhodolith-associated epiphytic fauna; a higher
number of epiphytic animal species were recorded on
closely branched rhodoliths (morph F), which offer a higher
structural complexity and a larger number of microhabitats
for epiphytic fauna than spherical (morph C) rhodoliths.
The observed spatial heterogeneity in species composition
may be attributable to topographical heterogeneity, which has
been shown to influence the assemblage structure by
modifying the local hydrodynamic regime (Eckman 1983),
food availability (Abelson and Loya 1995), rhodolith
morphology (Bosence 1976; Steller and Foster 1995),
predation intensity (Menge et al. 1985), competition (Menge
1976), larval dispersal, and recruitment (Archambault and
Bourget 1999). For example, the higher abundance of
amphipods at Site 1 could be related to the higher abundance
of fleshy macroalgae at Site 1, which provide amphipods
with a source of detritus (BIOMAERL Team 1999) and
protection from predators. Codium bursa represented 50% of
the total algal wet weight at Site 1, but was absent from Site
2 (Table 8). This species is a very slow growing alga
(Vidondo and Duarte 1995) with weak attachment, and is
easily dislodged by water movement, hence its absence from
Site 2 might further suggest a higher degree of bottom
instability at this site. Furthermore, the abundance of
epiphytic biota was markedly higher at Site 1 than Site 2
(Table 9), similarly indicative of increased sediment
movement at Site 2, which prevents attachment and
growth of epiphytic biota due to abrasion. Bottom
trawling does not appear to contribute to substantial
physical disturbance at the maerl bed studied (Borg et al.
1999), probably because fishing, being illegal within 3
nautical miles off the Maltese coast, only occurs sporadically. It is thus likely that the observed spatial differences
in species assemblage composition are due to higher
physical disturbance at Site 2, owing to its vicinity to ‘isSikka l-Bajda’ shoal, as is suggested from sediment
granulometry and rhodolith structural characteristics.
Trophic group analysis
The relatively low contribution of grazers (micro- and
macrograzers) to the total abundance (Table 10) suggests
that most of the primary production present in the area is
not consumed in situ by herbivores but rather enters the
food web via the detrital pathway. Deposit feeders were
indeed the most species-diverse after predators, as well as
the most abundant group. The coexistence of a noticeably
large number of deposit feeding species can be attributed to
262
the heterogeneity of the maerl bed, and might suggest niche
partitioning of the deposit feeding resource axis. Rowe
et al. (1990) have also recorded deposit feeders to be
dominant on Irish maerl beds. On the other hand, De Grave
(1999) and Grall and Glémarec (1997) found a prevalence
of predators, followed by scavengers and then deposit
feeders, on maerl beds in Brittany and Ireland (Mannin
Bay), respectively. The relatively high number of predatory
species on the maerl bed can explain the coexistence of a
large number of prey species in the same trophic group,
since predators may maintain the level of their prey below
the threshold level of competitive exclusion (Grall and
Glémarec 1997).
Mar Biodiv (2009) 39:251–264
Acknowledgments Part of this research was undertaken in the
framework of the BIOMAERL project with support from the
European Commission’s Marine Science and Technology Programme
(MAST III) under contract MAS3-CT95-0020. Maltese participation
in the BIOMAERL project was made possible through grants from the
University of Malta , the Malta Council for Science and Technology,
and the Ministry of Education of the Government of Malta, for which
we are grateful. We thank Prof P.G.Moore (University Marine
Biological Station, Millport and coordinator of the BIOMAERL
project) and Dr J. Hall-Spencer (University of Plymouth) for their
help and interest. We are also grateful to two anonymous referees
whose comments on an earlier draft of this paper greatly improved it.
The work described in this paper was carried out in full conformity
with the laws of Malta. The authors declare that they have no conflict
of interest.
References
Conclusion
Maerl beds have long been recognized as habitats that
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in this respect. Although few of the species found in maerl
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species assemblage within the maerl biotope that makes it
unique. The present study shows maerl beds present along
the NE coast of the Maltese Islands to be ‘biodiversity
hotspots’, in terms of macroalgae, infauna and macroepifaunal species. The potential importance of maerl as a
habitat for the juvenile stages of demersal and pelagic
species and the high secondary production they support is
recognised by local fishers, who risk punitive action by
fishing illegally over these beds. Despite their important
roles as productive marine ecosystems that support a high
biodiversity (Kamenos et al. 2004b; Martin et al. 2007), and
notwithstanding their status as a non-renewable resource,
rhodoliths have been threatened by several types of human
activity, including large-scale commercial extraction, alteration of water quality by discharges, and use of heavy
demersal fishing gear, the effects of which might be
irreversible over timescales relevant to humans. Maerl beds
are now receiving local and international protection and
some maerl-forming species such as Lithothamnion corallioides and Phymatolithon calcareum are both included in
Annex V of the EC ‘Habitats Directive’ 1992. It is widely
recognised that to manage specific habitats and species
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biology and ecology, and their sensitivity to natural and
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the knowledge of the physical, structural, taxonomical and
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NE coast of the Maltese Islands, which is a necessity for
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Appendix 1 The depth (m) and geographic position (longitude and latitude are given in degº
min’ sec’’) of the stations where live rhodoliths were present are given. The percentage mass
of the live rhodoliths at each station is also given, except for stations G4 and H3 where only a
very small amount of live rhodoliths and no non-biogenic sediment were collected
Station code
Depth (m)
A1
67
Geographical
% mass
Position
rhodoliths
36 02.45N
3.63
14 20.59E
A2
75
36 02.86N
1.45
14 20.94E
B1
51
36 01.38N
11.45
14 21.93E
B2
66
36 01.87N
25.88
14 22.26E
B3
74
36 02.23N
13.81
14 22.69E
C1
31
36 00.61N
0.07
14 22.70E
C2
36 01.04N
38
1.18
14 23.09E
C3
57
36 01.41N
7.54
14 23.50E
C4
70
36 01.87N
14.97
14 23.72E
D3
53
36 00.99N
14 24.57E
1
12.19
D4
36 01.35N
67
20.18
14 24.95E
E3
44
36 00.40N
5.23
14 25.31E
E4
36 00.78N
58
1.19
14 25.62E
E5
70
36 01.28N
35.79
14 26.02E
F4
46
36 00.09N
18.35
14 25.84E
F6
61
36 00.83N
35.8
14 26.51E
G4
51
35 58.69N
-
14 25.95E
G5
54
35 59.00N
2.83
14 26.28E
G7
66
36 00.30N
38.84
14 26.98E
G8
75
36 00.70N
32.73
14 27.43E
H2
53
35 58.85N
5.82
14 26.61E
H3
55
35 59.24N
14 26.90E
2
-
H4
35 59.72N
55
14.79
14 27.29E
H5
60
36 00.11N
6.51
14 27.61E
H6
36 00.48N
87
18.56
14 28.07E
I1
49
35 58.13N
2.01
14 26.78E
I2
47
35 58.51N
2.08
14 27.17E
I3
54
35 58.96N
10.88
14 27.52E
I4
62
35 59.29N
18.41
14 27.86E
I5
65
35 59.71N
0.03
14 28.22E
I6
75
36 00.10N
0.02
14 28.60E
I7
102
36 00.27N
8.68
14 28.76E
J3
60
35 58.55N
5.46
14 28.61E
J4
66
35 58.92N
14 29.02E
3
28.84
J5
35 59.32N
72
27.98
14 29.32E
J6
97
35 59.69N
22.74
14 29.70E
K1
35 57.08N
46
10.48
14 29.19E
K2
56
35 57.49N
4.36
14 29.49E
K3
71
35 57.93N
11.63
14 29.80E
K4
90
35 58.31N
36.07
14 30.09E
K5
103
35 58.76N
10.44
14 30.52E
L1
83
35 56.62N
14 30.86E
4
8.62
Appendix 2 Classified species list of the species collected using grab sampling during the seasonal sampling
at Sites 1 and 2 between July 1996 and April 1998
Algae
Gastropoda
Bivalvia
?Aglaothamnion sp.
Alvania beani
Aequipecten opercularis
?Aglaozonia sp.
Alvania discors
Astarte fusca
Aphanocapsa litoralis
Ascobulla fragilis
Chlamys flexuosa
?Aphanocapsa sp.
Barleeia unifasciata
Ctena decussata
Audouinella saviana
Bittium jadertinum
Digitaria digitaria
Audouinella cf. virgatula
Bittium latreillii
Diplodonta apicalis
Bolbocoleon piliferum
Caecum trachea
Glans trapezia
Botryocladia microphysa
Calyptraea chinensis
Glycymeris glycymeris
cf. Callithamnion sp.
Cerithiopsis fayalensis
Gonilia calliglypta
Calothrix sp.
Cerithiopsis tubercularis
Gouldia minima
Ceramium tenerrimum
Cerithium lividulum
Limatula subauriculata
Chondria tenuissima
Chauvetia turritellata
Lissopecten hyalinus
Chroodactylon ornatum
Clathromangelia quadrillum
Modiolus adriaticus
Cladophora patentiramea
Colubraria reticulata
Neolepton sulcatulum
Codium bursa
Cosmotriphora pseudocanarica
Nucula nitidosa
?Cordylecladia sp.
Crassopleura incrassata
Palliolum incomparabile
Crouania attenuata
Crepidula unguiformis
Pseudochama gryphina
Cryptonemia sp.
Dermomurex scalaroides
Pteromeris minuta
Cryptonemia tuniformis
Fusinus rudis
Solemya togata
Cystoseira corniculata
Gibbula fanulum
Striarca lacteal
Cystoseira cf. dubia
Haedropleura secalina
Tellina balaustina
Cystoseira sp.
Haminoea hydatis
Tellina pygmaea
Cystoseira spinosa
Jujubinus exasperatus
Thracia convexa
Dasya corallicola
Jujubinus ?montagui/tumidulus
Thracia distorta
Dasya corymbifera
Jujubinus striatus
Venericardia antiquata
Dasya punicea
Melanella polita
Dasya rigidula
Metaxia metaxae
Polyplacophora
Dictyota dichotoma
Mitrella scripta
Acanthochitona fascicularis
Dictyota ?linearis/mediterranea
Mitrolumna olivoidea
Callochiton septemvalvis
Dictyota sp.
Monophorus cf. perversus
Leptochiton africanus
Ectocarpus sp.
Muricopsis cristata
Lithophyllum sp.
Nanobalcis nana
Crustacea
Flabellia petiolata
Natica dillwynii
Alpheus sp.
Gelidiella sp.
Ocinebrina aciculata
Achaeus cranchii
1
Algae
Gastropoda
Crustacea
Gelidium sp.
Odostomia conoidea
Ampelisca sp.
Gigartina teedei
Opisthobranchia sp.
Amphitoe ramondi
Gracilaria dura
Phalium granulatum
?Anapagurus breviaculeatus
Gracilaria sp.
Rissoina bruguieri
?Apherusa bispinosa
Halimeda tuna
Turritella turbona
Apseudes talpa
Halopithys incurva
Vermetidae sp.
Athanas nitescens
Halopithys pinastroides
Vexillum ebenus
Calcinus tubularis
Halopteris filicina
Vexillum savignyi
Ceradocus orchestiipes
Halopteris scoparia
Vitreolina philippi
Ceradocus semiserratus
Hydrolithon sp. 1
Volvarina mitrella
Cestopagurus timidus
Hydrolithon sp. 2
Williamia gussonii
Cheirocratus sundevalli
Cirolanidae sp. 1
Hypoglossum hypoglossoides
Jania adhaerens
Annelida
Cirolanidae sp. 2
Jania rubens
Amage adspersa
Copepoda sp.
?Laurencia minuta
Aponuphis fauveli
Cyathura carinata
Laurencia obtusa
Branchiomma vesiculosum
Dexamine spinosa
Laurencia cf paniculata
Capitella capitata
Ebalia edwardsii
Laurencia sp. 1
Capitomastus minimus
Eurydice truncata
Laurencia sp. 2
Cirratulus filiformis
Eurynome aspera
Leathesia sp.
Chone acustica
Eusirus longipes
Lyngbya sp.
Eunice vittata
Galathea intermedia
Meredithia microphylla
Eusyllis lamelligera
Gammarella fucicola
Microdictyon tenuius
Fabricia sp.
Gnathia vorax
Osmundea pelagosae
Filograna sp.
Gourretia minor
Peyssonnelia sp.
Glycera convoluta
Harpinia antennaria
Peyssonneliaceae sp.
Glycera sp.
Hippolyte sp.
Phaeophila dendroides
Harmothoe longisetis
Hippomedon oculatus
Polysiphonia elongata
Harmothoe sp.
Hippomedon sp.
Polysiphonia mottei
Hyalinoecia grubii
Hyale camptonyx
Polysiphonia cf. ornata
Jasmineira sp.
Inachus ?thoracicus/aguiarii
Polysiphonia ruchingeri
Josephella sp. 1
Iphimedia minuta
Polysiphonia setacea
Josephella sp. 2
Joeropsis brevicornis
Polysiphonia cf. setigera
Lumbrineris gracilis
Lembos viguieri
Polysiphonia sp. 1
Lumbrineris impatiens
?Leptocheirus bispinosus
Polysiphonia sp. 2
Lumbrineris sp. 1
Leptocheirus pectinatus
Polysiphonia spinosa
Lumbrineris sp. 2
Leptocheirus sp.
2
Algae
Annelida
Crustacea
Polysiphonia cf. urceolata
Lysidice ninetta
Leptochelia savignyi
Rhizoclonium kochianum
Marphysa fallax
?Leucothoe incisa
Rivularia polyotis
Myxicola infundibulum
?Leucothoe spinicarpa
Rytiphlaea tinctoria
Nematonereis unicornis
Liljeborgia dellavallei
Scytosiphon cf. lomentaria
Nereidae sp.
Liocarcinus corrugatus
?Seirospora sp.
Nereiphylla paretti
Liocarcinus maculatus
Spatoglossum solierii
Nereis rava
Liocarcinus sp.
Sphacelaria cirrosa
Nereis sp.
Liocarcinus zariquieyi
Sphacelaria sp.
Notomastus profundus
Lysianassa costae
Spyridia filamentosa
Oridia armandi
Lysianassa longicornis
Stilophora rhizodes
Paraonidae sp.
Maera grossimana
Streblocladia collabens
Pelogenia arenosa
Metaphoxus fultoni
Ulothrix subflaccida
Phyllochaetopterus socialis
Mysidacea sp. 1
Valonia utricularis
Phyllodocidae sp.
Nebalia bipes
Vidalia volubilis
Pista cristata
Ostracoda sp. 1
Zanardinia sp.
Placostegus sp.
Pagurus excavatus
Zonaria tournefortii
Platynereis dumerilii
Pagurus sp.
Platynereis sp.
Palicus caronii
Echinodermata
Pomatoceros sp.
Parthenope massena
Antedon mediterranea
Sabellidae sp.
Pereionotus testudo
Echinocyamus pusillus
Scalibregma inflatum
Pisa cf. armata
Genocidaris maculata
Schistomeringos rudolphii
Processa sp.
Luidia ciliaris
Serpula sp. 1
Socarnes filicornis
Neolampas rostellata
Serpula sp. 2
Thoralus cranchii
Ophiuroid sp.
Spiophanes kroyeri
Upogebia cf. mediterranea
Stylocidaris affinis
Spirorbis sp.
Urothoe elegans
Syllis amica
Sipunculida
Syllis prolifera
Porifera
Aspidosiphon muelleri
Syllis sp. 1
Spg. 1
Sipunculus nudus
Syllis sp. 2
Spg. 2
Syllis sp. 3
Spg. 3
Brachiopoda
Tharyx sp.
Spg. 4
Argyrotheca cuneata
Thelepus cf cincinnatus
Spg. 5
Vermiliopsis sp.
Spg. 6
Cephalochordata
Spg. 7
Branchiostoma lanceolatum
Spg. 8
3
Ascidia - Urochordata
Bryozoa
Porifera
Ascidia sp.
Aetea sp.
Spg. 9
Red ascidian sp.
Ascophoran cheilostome sp. 1
Spg. 10
Rhopalaea neapolitana
Celleporina sp.
Spg. 11
Chorizopora brongniartii
Spg. 12
Sarcodina
Cyclostome sp. 2
Spg. 13
Cibicides sp.
Entalophoroecia sp.
Spg. 14
Miniacina miniacea
?Filicrisia sp.
Lichenoporid cyclostome sp. 1
Microporella pseudomarsupiata
Cnidaria
Mollia patellaria
Actinaria sp.
?Plagioecia sp.
Hydroid sp.
Reptadeonella violacea
Nausithoidae sp.
Rhynchozoon sp.
Schizomavella rudis
Tubulipora sp.
4
Edwin lanfranco