effects of increased mortality on gorgonian corals (cnidaria, octocorallia): different demographic...
TRANSCRIPT
COELENTERATE BIOLOGY Review Paper
Effects of increased mortality on gorgonian corals(Cnidaria, Octocorallia): different demographic featuresmay lead affected populations to unexpected recoveryand new equilibrium points
G. Santangelo • R. Cupido • S. Cocito •
L. Bramanti • C. Priori • F. Erra • M. Iannelli
Received: 15 July 2014 / Revised: 17 February 2015 / Accepted: 1 March 2015
� European Union 2015
Abstract Over the last years, several marine popula-
tions suffered a drastic mortality increase of different
origins; assessing the changes occurring in the demo-
graphic structure of such populations will allow
evaluating their future trends and their ultimate fate.
The aim of our research was to assess main demo-
graphic descriptors and related dynamics in popula-
tions of the Mediterranean gorgonians Paramuricea
clavata and Corallium rubrum (the ‘‘precious red
coral’’) both subject to increased mortality, by life-
history tables and Leslie-Lewis transition matrices.
Gorgonian populations have been generally been
considered to have low recruitment and low dynamics.
Here, we test whether these features change when
mortality rises and if such populations can reach new
equilibria? Our findings show large differences be-
tween the two species examined, with lower recruit-
ment and adult colony density, shorter life-span but
over-abundant reproductive output in P. clavata.
Recruitment density dependence was found in crowd-
ed populations of both species, albeit with different
trends. Populations of both species tend to recover
even after drastic mortality increase and P. clavata
reaches a new equilibrium at lower densities than at
pristine values, and this in a few years time. The
findings in this review could shed some light on the
poorly understood dynamics occurring in deep-water
dwelling, affected populations of long-lived and slow-
growing gorgonian corals.
Keywords Octocorals � Mass mortality �Demography � Population dynamics � Mediterranean
SeaGuest editors: Yehuda Benayahu, Oren Levy & Tamar Lotan /
Coelenterate Biology: Advanced Studies on Cnidaria and
Ctenophora
G. Santangelo (&) � C. Priori � F. Erra
Department of Biology, Conservation and Demography
on Long-Lived Species Research Group, University of
Pisa, Via Volta 6, 56126 Pisa, Italy
e-mail: [email protected]
R. Cupido � S. Cocito
ENEA Marine Environment Research Centre,
PO Box 224, 19100 La Spezia, Italy
L. Bramanti
CNRS UMR8222, LECOB, Observatorie Oceanologique
Univ. Marie Curie, 18 Avenue du Fontaule,
66650 Banjuls-sur-Mer, France
C. Priori
OGS, National Institute of Oceanography and
Experimental Geophysics, Borgo Grotta Gigante 42/C,
34010 Sgonico, TS, Italy
M. Iannelli
Department of Mathematics, University of Trento, Via
Sommarive 14, 38123 Povo, Trento, Italy
123
Hydrobiologia
DOI 10.1007/s10750-015-2241-1
Introduction
Recent changes in marine communities toward sim-
pler structures with lower abundance and biomass of
long-lived species may have dramatic consequences
on marine ecosystems (Knowlton & Jackson, 2008;
Rossi, 2013). The complexity and plasticity of life
histories can protect populations from drastic envi-
ronmental changes and can foster their persistence.
Demographic studies on long-lived, slow-growing,
deep-dwelling species require dedicated long-term
research, which can provide precious insights in the
complex dynamics of their populations, and thereby
help plan rational measures for their conservation and
management (Caswell, 2001; Santangelo & Bramanti,
2006; Doughty et al., 2014).
Gorgonian corals are long-lived, slow-growing
species, whose lifespan can surpass a full century
(Roark et al., 2006; Priori et al., 2013). Healthy
colonies can form dense canopies resembling minia-
ture terrestrial forests (Rossi, 2013). Gorgonians are
among the main components of the Mediterranean
coralligenous species assemblages, one of the world’s
richest in terms of biodiversity (Ballesteros, 2006 and
references therein).
As gorgonians are habitat-forming species, their
survival is strictly intertwined with that of the whole
marine community. By efficiently intercepting seston
via their three-dimensional fans, they transfer energy
from the less stable, high-turnover planktonic system
to the more stable benthic one, thus playing a
particularly important role in the Mediterranean,
where hermatypic hexacorals are less common than
in tropical seas (Gili & Coma, 1998).
Currently, gorgonian populations are subject to
various sources of mortality linked to direct or indirect
human disturbances acting synergistically or additive-
ly (e.g., bottom trawling, line and net fishing,
eutrophication, global warming, and ocean acidifica-
tion; Garrabou et al., 2001; Tsounis et al., 2012;
Bramanti et al., 2013; Rossi, 2013). Moreover, some
species have high economic value, and hence their
populations have been and still are intensively
exploited (e.g., Goffredo & Lasker, 2008; Tsounis
et al., 2010, Lasker, 2013). Whatever the causes,
profound changes in the structure of gorgonian
populations have increased the need to carry out
dedicated research to acquire extensive, sound data on
their life-history and demographic features, with the
ultimate aim of formulating dynamic models of their
population trends to guide effective conservation and
management efforts.
Repeated anomalous mortality events, co-occurring
with anomalous temperature increases, have recently
affected benthic suspension feeders of the circalittoral
rocky shores of the northwestern Mediterranean, with
particularly damaging effects on the gorgonians living
there (Cerrano et al., 2000, Bramanti et al., 2005;
Coma et al., 2009; Garrabou et al., 2009; Crisci et al.,
2011). A sound understanding of gorgonian popula-
tion structure and dynamics before and after such
anomalous mortality events can shed much light on the
responses of stricken marine populations and commu-
nities to Global Climate Change, and provide precious
tools for assessing both the present status and future
trends of the impacted populations (Santangelo et al.,
2007; Bramanti et al., 2009; Cupido et al., 2009).
When examined in detail over sufficiently long-
time periods, gorgonians reveal large differences in
their life histories and life cycles. This is particularly
evident when their reproductive features are com-
pared. Unfortunately, the lack of standardized sam-
pling methods and the consequent scarcity of
comparable data make it difficult to affect such
comparisons (Santangelo & Bramanti, 2010).
Different life histories may produce different
population dynamics, and hence gorgonians may
exhibit species-specific responses to anomalous mor-
tality events. Herein we present a review of our
longstanding research on the demographic features of
two temperate gorgonian corals found throughout the
Mediterranean on its mesophotic rocky bottoms:
Paramuricea clavata (Risso, 1828) and Corallium
rubrum (L 1758). P. clavata is one of the largest
gorgonians in the Mediterranean and forms dense
canopies on vertical and sub-vertical cliffs, while C.
rubrum is a highly valuable species endemic to the
Mediterranean and neighboring Atlantic, whose
populations have historically been subjected to intense
exploitation for over two thousand years (Santangelo
& Abbiati, 2001; Tsounis et al., 2010 and references
therein). As these two species exhibit large differences
in their reproductive parameters, they may provide
valuable insight into the highly variable mortality rates
to which gorgonian corals are subjected.
Gorgonian populations have been generally con-
sidered to be provided of low recruitment and low
Hydrobiologia
123
dynamics but these features could drastically change
under increased mortality rates. Aim of our researches
was to explore future scenarios of marine populations
subject to drastic mortality increase of different origin
by means of projections of their population structure
over time based on their main demographic features by
means of algebraic transition matrices.
Life at the edge of the summer thermocline: a case
study on the recovery of a temperate gorgonian
population stricken by anomalous mortality events
Paramuricea clavata (Risso, 1826) is a highly repro-
ductive, external brooder with discrete (time-limited)
reproduction in late spring. One large colony may
produce hundreds of thousands oocytes, and the
colonies living in a single square meter may produce
hundreds of thousands or even millions of oocytes
m-2 (Table 1) The species has one of the highest
reproductive outputs among studied gorgonians (Beir-
ing & Lasker, 2000; Torrents & Garrabou, 2011). Its
life span can exceed 50 years (Coma et al., 1995;
Cupido et al., 2012). In contrast to some other
gorgonians (Lasker et al., 1998), sexual reproduction
is dominant in its life-cycle.
Our research has focused on the demographic
features of a population living just below the summer
thermocline at La Spezia (Ligurian Sea, Italy; Fig. 1).
During late summer 1999 and 2003, this population
was stricken by abnormal temperature increases due to
the sinking of the summer thermocline below its usual
depth in the NW Mediterranean, an event accompa-
nied by heavy mass mortality (Cerrano et al., 2000;
Garrabou et al., 2009). As this population has been
followed since 1998 (before the mass mortality), it has
been possible to compare its ‘pristine’ and post-
mortality status, observe the population trends over a
12 years period and make simulations of future trends.
As episodic mass mortality may have prolonged
effects on P. clavata populations (Mistri & Ceccherelli,
1994; Linares et al., 2005; Heute-Stauffer et al., 2011),
our studies focused on the demographic structure and
dynamics of the impacted population. To this end, we
have examined (1) population structure in terms of size
classes based on the mean annual colony growth rate;
(2) size at first reproduction, fertility, and fecundity of
polyps and colonies of the different classes; (3)
recruitment density and reproductive output of the
impacted population. Moreover, we have compared
these findings with the available pre-mortality data on
this population, as well as with those previously
recorded on other P. clavata populations. Finally, the
collected data have enabled simulations of population
trends over time (Bramanti et al., 2009; Santangelo
et al., 2012a). The following provides a brief summary
description of the methods adopted in these studies; a
more detailed description can be found in previous
papers (Cupido et al., 2008, 2009, 2012).
Study site, sampling, and demographic analysis
The field studies were carried out during the period
1998–2012 on a P. clavata population living at the
western edge of the Gulf of La Spezia (Ligurian Sea,
Italy, 44�010N, 09�500E; Fig. 1), off the western cliffs
of Tinetto Islet. This area is characterized by high
turbidity due to the terrestrial runoff from the neigh-
boring Magra River plume and the sewage from the
city of La Spezia. This small, geographically isolated
population dwells on a vertical cliff just below the
Table 1 Paramuricea clavata and Corallium rubrum main demographic features
Species Corallium rubrum Paramuricea clavata
Shallow Deep 1998 2004 2010
Reproductive features Internal brooder External brooder
Adult density (col./m2) 0.2–3 9 103 0.28–2 9 102 35.7 7.9 18.2
Polyp fecundity (oocytes/polyp) 0.93 0.87 // // 13-28
Size (height)/age at first rep. 1–2 cm
3–7 years
// // 8.5 cm
*3 years
Pop. repr. output (oocytes/m2) 3.8 9 104 // 2 9 106 // 1.45 9 105
Recruit density (rec./m2) 0.56–6 9 102 // 0.86 0.57 3.86
Hydrobiologia
123
upper bathymetric limit of the summer thermocline
(between 17 and 25 m depth). Because the studied
population was small in size and was impacted quite
heavily, the research has been based as much as
possible on non-destructive sampling and measure-
ment techniques (photographs and direct colony
measurements taken in the field on fixed and random
plots). Only when absolutely necessary (i.e., for sexual
analyses), small apical branch segments were collect-
ed. The mean annual growth rate (in height) was
measured on a sample of labeled colonies (n = 243)
over 3 years. It was thus possible to group the colonies
on the basis of their height in) classes defined
according to the mean annual growth measured in
the studied population (henceforth called annual size/
age classes; Santangelo et al., 2007; Priori et al., 2013;
Bramanti et al., 2014). Annual recruitment included
all new colonies found on the fixed plots in May, just
before spawning.
Reliable, accurate determination of colony sex (a
non-trivial task in P. clavata) is essential in order to be
able to estimate population sex ratio, fertility, fecun-
dity, and reproductive output of female colonies. Such
determination was performed on freshly collected tips
from colonies of different sizes (n = 205) in May, just
before spawning. The tips were dissected and exam-
ined under the stereo and optical microscope and
confirmed by histological analysis performed
following procedures described in Cupido et al.
(2012). In order to examine the spatial distribution
pattern of the sexes (i.e., sex segregation), mature
colonies were numbered using a plastic label and
mapped on a plastic sheet. Sex segregation was tested
via a Chi square test on the frequency occurrence of
same-sex nearest neighbors (Pielou, 1962; Cupido
et al., 2012).
According to Bramanti et al. (2014) determination
of colony growth rate allows for temporal resolution of
demographic models by estimating the most probable
age of the colonies in each size class and supplying a
time step for reiterating the population size-structure
models in simulations. The demographic model for-
mulated to simulate population trends was based on a
modified Leslie-Lewis transition matrix (Caswell,
2001) according to the fate of individual colonies
recorded in the field on fixed plots over the three-year
period 2007–2010. In other words, each year any
given colony can (1) survive and progress to the next,
larger class (in bold), (2) remain in the same class (no
growth), and (3) skip to other larger classes, or in a few
cases, regress to a smaller class (losing some apical
branches), or die. The matrix diagonal reports the
proportion of colonies remaining in the same class in a
single time step (Table 2).
As these populations tend to oscillate between a
small number of larger colonies and a high number of
Fig. 1 Map of the
populations studied
Hydrobiologia
123
smaller colonies (Linares et al., 2007; Tsounis et al.,
2010), the density of polyps (overall number of polyps
per 1 m2), depending on both colony size and colony
density, was included in the control function of
population growth (Bramanti et al., 2009).
Structure and dynamics of the stricken P. clavata
population
In 1998, the pre-mortality population exhibited a
density of 35.7 colonies/m2. The anomalous events
occurring over the period 1999–2003 reduced colony
density to 7.9 colonies/m2, corresponding to a 78.3%
mortality (Table 2). In the subsequent years
(2004–2006), density remained at similarly low values
and the dominant class in the surviving population
shifted toward smaller sizes (Figs. 2, 3). In more
recent years (2007–2010) the population exhibited
positive growth rates (k[ 1) and colony density
increased up to about half the pristine, pre-mortality
values (Fig. 2a).
In the years just after the anomalous mortality events
(2004–2006) recruitment fell, but in the following
period (2007–2010), it increased to five times the pre-
mortality values (Fig. 2c). When compared with other
literature reports, pre-mortality recruitment and adult
colony densities were consistent with those reported for
other, undisturbed P. clavata populations (Gori et al.,
2007; Linares et al., 2007). A two-fold increase in
recruitment density following a mass mortality event
was found by Cerrano et al. (2005).
Based on the mean annual colony growth rate
measured over 3 years (3 ± 0.7 cm year-1), the
population was divided into size/age classes distin-
guished by a 3 cm difference in height. All the size/
age structures found in the different years showed
monotonic, regularly decreasing patterns, in which
recruits (the first age class) were the dominant class.
The proportion of larger colonies increased in 2009
and 2010 (Fig. 4).
The population was completely gonochoric and sex
ratio was balanced (not diverging significantly form a
1:1 ratio). The spatial distribution of colony sex
diverged significantly from that expected in a random
distribution (0.5 probability of finding a same-sex
nearest-neighbor), revealing that some segregation by
sex could likely occur in the population on a small
spatial scale (Cupido et al., 2012). The size of female
colonies at first maturity was 8.5 cm, corresponding to
an age of about 3 years; at this size only 20% of
colonies were mature, though this percentage reaches
100% in the colonies of the larger size classes (over
31.5 cm and 11 years). In larger colonies the number
of polyps increased exponentially with size (Fig. 5a).
As polyp fecundity is high and increases with colony
size (up to 20 mature oocytes per polyp), the overall
fecundity also increased exponentially with colony
size, reaching 250.000 oocytes per colony (Fig. 5b).
The majority of the population reproductive output
Table 2 Transition matrix for the Paramuricea clavata Spezia population
Size class 1 2 3 4 5 6 7 8 9 10 [10 Surv
1 0.18 0.38 0.10 0 0 0 0 0 0 0 0 0.66
2 0 0.21 0.38 0.19 0 0 0 0 0 0 0 0.78
3 0 0 0.27 0.40 0.16 0 0 0 0 0 0 0.83
4 0 0 0 0.24 0.40 0.24 0 0 0 0 0 0.88
5 0 0 0 0.11 0.37 0.31 0.09 0 0 0 0 0.88
6 0 0 0 0 0.12 0.38 0.32 0.11 0 0 0 0.93
7 0 0 0 0 0 0.09 0.41 0.28 0.14 0 0 0.93
8 0 0 0 0 0 0 0 0.49 0.43 0 0 0.92
9 0 0 0 0 0 0 0 0.22 0.49 0.25 0 0.96
10 0 0 0 0 0 0 0 0 0 0.67 0.25 0.92
[10 0 0 0 0 0 0 0 0 0 0 0.72 0.72
The matrix presents: percentage colonies that rise by one class each year (in bold), percentage colonies that rise by a number of
classes each year (they grow more), percentage of colonies remaining in the same size class (in the diagonal) and the few colonies
that loose apices and regress to a smaller class
Hydrobiologia
123
(77%) is produced by classes 6–10 (21.6% of the
overall population), while classes 11–14, composed of
larger but few colonies (1.4%) accounted for 18.8% of
the reproductive output. In contrast, colonies in
classes \ 6 accounted for only 3.8% of the population
reproductive output, despite their larger numbers
(77%), as they were smaller, less fecund and less
fertile (Cupido et al., 2012).
The main reproductive features of the P. clavata
population are summarized in Table 1. After the two
anomalous mortality events the estimated population
reproductive output decreased to 7.25% (from
2,000,000 to 145,000 oocytes m-2; Table 1) due to
reductions in both colony density and size. It is
worthwhile recalling that at the same time recruitment
increased about fivefold.
Fig. 2 Trends of colony density (a), polyp density (b), and
recruitment density (c) in the Paramuricea clavata population
of La Spezia (Italy) from 1998 to 2010
Fig. 3 Size structure of the Paramuricea clavata population of
La Spezia (Italy) from 1998 to 2007. (Modified from Cupido
et al. 2008)
Hydrobiologia
123
All the survival values recorded in the fixed plots on
the labeled colonies over the period 2007–2010 are
reported in the algebraic transition matrix shown in
Table 2. A matrix of transition probabilities was
developed for each of the 3 years and the three
averaged to produce the matrix in Table 2. This matrix
was used to conduct simulations of population trends
over time (Fig. 6). The simulated population exhibited
damped oscillations at first and then stabilized after
several cycles at a polyp density that was about 1/4 the
pristine, pre-mortality value measured in the popula-
tion (which is never reached again).
Demography of the highly valuable Mediterranean
red coral C. rubrum (L. 1758): an exemplary case
study of an overexploited gorgonian
The highly valuable Mediterranean red coral C.
rubrum has been harvested for over 2,000 years, and
several populations have been overexploited (e.g.,
Santangelo et al., 1993; Cicogna & Cattaneo, 1993).
The brilliant color of its red and easily worked axial
skeleton makes this long-lived, slow-growing, internal
brooder gorgonian one of the world’s most eco-
nomically desirable marine species, which has thus
been intensively harvested and traded throughout
history (Liverino, 1983; Cicogna & Cattaneo, 1993
and references therein).
Exhibiting an extensive bathymetric (Costantini
et al., 2010) and geographic distribution (Carpine &
Grasshoff, 1975), red coral is a component of the deep
circalittoral rocky bottom and semi-dark cave com-
munities (Ballesteros, 2006). Recent research has
furthered our knowledge of red coral populations
Fig. 4 Population size/age structure of the Paramuricea
clavata population of La Spezia (Italy) from 1998 to 2010
Fig. 5 Exponential correlation between number of polyps and
colony annual size/age class (a) and between the number of
oocytes and colony annual size/age class in the same population
(b). Modified from Cupido et al. 2012
Hydrobiologia
123
living at shallower depths (between 10 and 50 m depth,
within SCUBA diving limits; Tsounis et al., 2010 and
references therein), and some of the main demographic
and reproductive features of these populations have
been determined. The overall picture emerging from
these studies reveals that C. rubrum produces gono-
choric populations with discrete (time-limited) repro-
duction in summer, low polyp fecundity (Santangelo
et al., 2003, Tsounis et al., 2006, Torrents & Garrabou,
2011), high colony, and high recruitment densities
(200–3,000 colonies and 50–600 recruits m-2; Bra-
manti et al., 2005, Santangelo et al., 2012b, Bramanti
et al., 2014) in comparison with other gorgonians (e.g.,
Torrents & Garrabou, 2011; Doughty et al., 2014).
Moreover red coral exhibits a slow colony growth rate
(0.24–0.36 mm year-1 of colony basal diameter;
Garrabou & Harmelin, 2002; Marschal et al., 2004;
Torrents et al., 2005; Gallmetzer et al., 2010; Bramanti
et al., 2014), a long-life span (Garrabou & Harmelin,
2002), small size and early age at first reproduction
(Santangelo et al., 2003; Gallmetzer et al., 2010), and
high genetic differentiation on a small spatial scale
(Costantini et al., 2007; Ledoux et al., 2010).
The shallower populations of C. rubrum have been
intensively harvested in the past and some are still
subjected to overexploitation, even though the eco-
nomic value of such colonies is limited (Bramanti
et al., 2014). Harvesting has likely altered their size
structure, and the modern populations are made up of
mainly small, crowded colonies (e.g., Tsounis et al.,
2007). Some of these populations have also been
affected by the 1999 mortality event (Garrabou et al.,
2001; Bramanti et al., 2005). Recently, the General
Fisheries Commission for the Mediterranean (GFCM)
has promoted a ban on the fishing of these populations,
as well as a minimum legally harvestable size (colony
basal diameter of 7 mm; GFCM, 2011).
As mentioned, our knowledge of these populations
has increased considerably in recent years, whereas
information on the deeper populations (those living
below 50 m depth) still remains rather limited (Rossi
et al., 2008; Angiolillo et al., 2009). These popula-
tions, which have become the main target for current
harvesting, are mainly composed of larger, sparse
colonies, though most of their main demographic
features (e.g., population density, size and age struc-
ture, mortality, fertility, fecundity, larval output, and
recruitment) are still poorly understood (Rossi et al.,
2008; Santangelo & Bramanti, 2010). Only very
recently have dedicated research studies been pro-
moted to gather further demographic and genetic data
on these populations (Angiolillo et al., 2009; Pedoni
et al., 2009; Costantini et al., 2011; Priori et al., 2013).
The following provides a brief summary description
of the sampling and other methods adopted in the
studies.
Study sites, sampling, and demographic analyses
The findings reported here are based on sampling
carried out over the period 1993–2012 in the north-
western Mediterranean: Calafuria and Elba Island
(Tuscan Archipelago, Livorno, Italy), Portofino
(Genoa, Italy), Medes Islands and Cap de Creus
(Catalonia, Spain; Fig. 1). They regard for the most
part populations living in the shallower portion of the
species distribution range, as only recently have data
been collected on a deep population dwelling in the
Tyrrhenian Sea (Elba Island—Tuscan Archipelago,
Fig. 1), between 60 and 120 m depth (Priori et al.,
Fig. 6 Simulation of P.
clavata population trends.
After some damped
oscillation, the population is
near stabilizing at a polyp
density about 1/3 that in the
pre-mortality populations
Hydrobiologia
123
2013). The most recent new data on deep-dwelling
populations comes from collections via remotely
operated vehicle recordings (Rossi et al., 2008;
Angiolillo et al., 2009; Priori et al., 2013; Angiolillo
et al. submitted). All other samples were collected by
SCUBA divers down to 50 m and by mixed gas and
rebreather divers below this depth.
The age of colonies was determined by the thin
section organic matrix staining dating method set out
by Marschal et al. (2004), based on toluidine-blue
staining of the organic matrix concentric growth rings
which are annually deposited in the colonies’ axial
calcareous skeleton (Fig. 7). This dating method has
been successively applied to several red coral popula-
tions (Torrents et al., 2005; Gallmetzer et al., 2010;
Priori et al., 2013; Bramanti et al., 2014). Further
details on these procedures have been reported in
previous papers (Priori et al., 2013; Bramanti et al.,
2014).
Due to SCUBA diving depth and time limits, the
methods adopted enable studying (annual) recruit-
ment only in the shallowest part of the species
bathymetric distribution range (between 20 and 50 m
depth). Recruitment studies have been designed
through the use of square (10 9 10 cm) marble
settlement plates (Bramanti et al., 2005, 2007; San-
tangelo et al., 2012b). More recently, recruitment has
also been determined via macro-mode photographic
sampling (recruit diameter measure on average
0.6 mm), and examination of the photos at high
magnification (Bramanti et al., 2014).
The reproductive output of the entire population, as
well as the corresponding output values for colonies of
different classes was calculated based on the fertility
and fecundity values. A detailed description of the
procedures followed has been reported previously
(Santangelo et al., 2003; Santangelo et al., 2007; Priori
et al., 2013; Bramanti et al., 2014). All the data on
population size/age structure, survival, and reproduc-
tion have been included in static life tables (time
specific life table, according to Ricklefs & Miller,
1999). In such life tables, under steady-state condi-
tions (a population in which the different classes are
constantly proportional over time; according to
Caswell, 2001), the ratio between the numbers of
colonies in two consecutive classes provides a mea-
sure of survival and mortality (Santangelo et al.,
2007). Table 3 shows a complete life table for a
shallow red coral population (Calafuria Italy).
Simulations were carried out using a discrete
dynamic model based on a Leslie-Lewis algebraic
transition Matrix (Ebert, 1999; Caswell, 2001) which
includes the reproduction and mortality values mea-
sured in the population. The density dependence of
recruitment, positive for low and negative for higher
densities, actually measured in the studied population,
was also included in the model (Santangelo et al.,
2007; Bramanti et al., 2009). Detailed descriptions of
the model and simulations have been reported in the
papers cited above.
Demography of C. rubrum
Colony growth rate (in basal diameter mm/year)
yielded a good fit with the power curve with positive
exponent reported in Fig. 8a. According to previous
findings (Cicogna & Cattaneo-Vietti, 1993; Bramanti
et al., 2005, 2007, 2014), colony basal diameter
growth is 2–3 times faster during the first four years of
colony life and then falls with age (Fig. 8a). This
reduction of basal diameter growth is confirmed by the
finding of a constant growth of the circular crown area
of colony sections and of a decreasing average annual
growth with age increase (Fig. 8b, c; Priori et al.,
2013; Bramanti et al., 2014). The average colony
growth rate of the shallow populations at Portofino and
Cap De Creus was 0.24 mm year-1 (Bramanti et al.,
Fig. 7 Thin section of a red coral colony base prepared by the
organic matrix staining dating method. The count of this colony
annual growth rings yields an age of about 29 years
Hydrobiologia
123
2014). A slightly higher growth rate (by about 8%) has
been found in the deeper population of Elba Island
(0.26 mm year-1; Priori et al., 2013), in which the
maximum age of colonies, estimated on the basis of
their diameter, is over a full century (Priori et al.,
2013). Unfortunately, due to the asymptotic trend of
the relation between average colony growth and age,
the ability to predict colony age on the basis of their
averaged basal diameter is considerably reduced for
larger colonies (Doughty et al., 2014). The minimum
legally harvestable size (7 mm colony basal diameter),
established by the FAO GFCM (2011), corresponds to
a colony age ranging from 30 to 35 years (Priori et al.,
2013; Bramanti et al., 2014).
Recruitment density, which also varied between
years and on a small spatial scale, exhibited consis-
tently high values in the few shallow populations in
which was studied (Table 1). Moreover, tenfold
differences have been found between different geo-
graphic locations (Bramanti et al. 2005, 2007; San-
tangelo et al., 2012b; Bramanti et al., 2014).
In all shallow populations for which a large number
of samples of all the different size classes (including
recruits) could be examined via methods that were
non-selective for larger colonies (Santangelo & Bra-
manti, 2010), recruits were the dominant class, and the
frequency distribution of size-age classes exhibited a
monotonic, regularly decreasing trend (Santangelo
et al., 2007; Bramanti et al., 2014). These findings
suggest these populations could be in a steady state.
Such colony size distribution may exhibit different
patterns in the cases for which sampling was selective
for larger colonies, either in small samples or samples
collected in areas marginal to the main populations
and therefore irregularly colonized by red coral
(Santangelo & Bramanti, 2010; Priori et al., 2013;
Doughty et al., 2014).
Corallium rubrum is a ‘‘planulator’’ and all popula-
tions studied were gonochoric at both the colony and
polyp level. The minimum size at first reproduction is
quite small (1.8 mm in basal diameter), corresponding
to an age of about 3 years, and the sex ratio was
balanced (not significantly divergent from a 1:1 ratio)
(Priori et al., 2013; Bramanti et al., 2014). Due to the
sterility of some polyp of female colonies, the average
fecundity of these polyps is below one oocyte per
polyp in shallow and deep populations (0.93–0.87
oocytes per polyp, Table 1; Santangelo et al., 2003;
Priori et al., 2013). Overall, red coral fecundity is
considerably lower than that measured in other
octocorals (Torrents & Garrabou, 2011).
Larval production depends on the size/age of the
colony; while the smallest reproductive colonies
produce 24 planulae on average, the older, larger
colonies can produce up to 6,500–7,000 planulae
(Priori et al., 2013). This clearly indicates that there
are probably large differences in larval output between
populations with different size and age structures.
Table 3 Life table of the shallow Calafuria population (Livorno, Italy)
Class Colonies Survival Fertility Planulae per
polyp produced
Sex ratio No. of polyps Planulae per
capita produced
Planulae produced
by each class
1 822.00 0.89 0.00 0.87 0.58 0.00 0.00 0.00
2 731.00 0.63 0.00 0.87 0.58 6.20 0.00 0.00
3 463.00 0.70 0.36 0.87 0.58 15.91 0.15 1338.86
4 323.00 0.52 0.64 0.87 0.58 31.06 10.03 3240.58
5 167.00 0.44 0.82 0.87 0.58 52.18 21.59 3605.88
6 73.00 0.29 0.97 0.87 0.58 79.72 39.02 2848.47
7 21.00 0.57 0.98 0.87 0.58 114.06 56.41 1184.57
8 12.00 0.33 0.99 0.87 0.58 155.58 3.26 932.65
9 4.00 0.75 1.00 0.87 0.58 204.24 103.23 412.91
10 3.00 1.00 1.00 0.87 0.58 261.33 131.87 395.61
11 3.00 0.33 1.00 0.87 0.58 326.14 164.57 493.71
12 1.00 1.00 1.00 0.87 0.58 399.23 201.46 201.46
13 1.00 – 1.00 0.87 0.58 480.87 242.65 242.65
Modified from Santangelo et al. (2007)
Hydrobiologia
123
Lastly, about 76% of the colonies examined at
Portofino and Cap de Creus and 93% of those
examined at Elba Island were fertile (Priori et al.,
2013; Bramanti et al., 2014).
Size/age-dependent abundance, survival, and re-
productive data for the shallow red coral population of
Calafuria are reported in Table 3. The majority of
reproductive output (85%) comes from colonies in
classes 3–7. Several simulations have been carried out
based on these data (Santangelo et al., 2007; Bramanti
et al., 2009). The simulations reported in Fig. 9 deal
with four different scenarios. In the first the population
is subjected to a single anomalous mortality event
(such as that recorded locally in 1999); the population
possess the ability to recover in a few years (Fig. 9a).
In the second simulation the population is still
recovering after similar multiple mortality events
occurring at four-year intervals (Fig. 9b). In the third
simulation the population is driven to extinction in
about 60 years by periodic mortality events at three-
year intervals. In the fourth simulation (Fig. 9d), a
60% reduction in harvesting of larger colonies that
allows the population to achieve saturation in about
30 years (Santangelo et al., 2007; Bramanti et al.,
2009).
Discussion
The La Spezia population of P. clavata has been
impacted twice by anomalous mortality events (the
highest mortality ever reported for this species) that
coincided with the thermal anomalies in the NW
Mediterranean in late summer 1999 and 2003. This
mortality dramatically reduced its density and chan-
ged its size/age structure, with a disproportionate
effect on larger colonies (Cerrano et al., 2005: Cupido
et al., 2009), and hence a shift toward smaller sizes.
The frequency distribution of size classes based on
average annual colony growth revealed a pattern of
regularly decreasing abundance with increasing size/
age. Throughout all the years examined, the first
age/size class (recruits) was the dominant one (Fig. 4).
Both adult and recruit densities remained at low values
during the first 3 years after the mortality events, while
b Fig. 8 a Relation between colony growth (averaged basal
diameter) and age fitted to a power curve with positive exponent;
b constant grow of the circular crown area of red coral colonies;
(Modified from Bramanti et al. 2014). c Relation between
colony age and average growth fitted by a power curve with
negative exponent (Modified from Priori et al. 2013)
Hydrobiologia
123
in subsequent 4 years such density values rose to about
� and five times the pristine values, respectively. It is
important to note that this recovery started only after
dead colonies, still encountered 3 years after the mass
mortality, detached from the cliff harboring the
population. Such a finding suggests that not only the
density of live large colonies, but also that of dead
ones, is likely to have a negative effect on population
recovery (Cupido et al., 2009, 2012).
The overall population sex ratio was balanced,
though the spatial distribution of sexes showed some
significant segregation (colonies of different sex are
not randomly distributed). Although the mechanisms
underlying the spatial segregation of sexes is un-
known, this finding, if confirmed, seems quite relevant
and may likely reveal the cause of the frequent
anomalous, unbalanced sex ratios found by other
researchers in gorgonian populations: if the distribu-
tion is segregated by sex, limited sampling, in terms of
space and/or number, could lead to misleading find-
ings of unbalanced sex ratios (Cerrano et al., 2005;
Gori et al., 2011).
The minimum size at first reproduction corresponds
to an early age of sexual maturity (about 3 years).
However, only 20% of colonies were ripe at this size,
and the percentage of fertile colonies only reaches
100% in the older, larger colonies. As both number of
female polyps and fecundity increased with colony
size (Fig. 5a, b), the colony reproductive output
increases exponentially with size. Early onset of
reproduction and high fecundity are basic features of
successful colonizer octocorals (Benayahu & Loya,
1985). All these findings indicate that extremely wide
differences in reproductive output could occur be-
tween populations with different size/age structures, as
well as between populations affected or unaffected by
mass mortality events that drastically and dispropor-
tionally reduced the number and density of the larger
colonies. Seven years after the mass mortality event,
the estimated population reproductive output was only
7.3% that of the pre-mortality population (Cupido
et al., 2012), and about 20% of that determined in other
undamaged stable populations (Coma et al., 1995),
and this came mainly from colonies in the medium-
size classes. However, the population has been recov-
ering since the catastrophic mortality by increasing
both its colony and recruitment densities, albeit with a
sharp fall in its reproductive output.
The impacted population exhibited unexpectedly
rapid dynamics, despite the fact that gorgonians have
Fig. 9 Simulations of population density trends over time
based on abundance, survival, and reproduction coefficients of a
red coral population living in the shallower part of the species
bathymetric range (Calafuria population, NW Mediterranean,
Italy); a after a single mortality event the population recovers in
about 15 years; b after periodically repeated anomalous
mortality events at 4-year intervals the population still recovers.
c A population affected by multiple anomalous mortality events
at 3-year intervals is driven to extinction in about 60 years; d if
harvesting (mortality) is reduced by 60%, the population reaches
saturation in about 30 years. (Modified from Santangelo et al.
2007)
Hydrobiologia
123
generally been considered species exhibiting slow
dynamics (Gotelli, 1988; Lasker, 1991; Linares et al.,
2007). This population has nonetheless showed a
relatively fast recovery rate with positive growth in
recent years. Recruitment density, five times higher
than the pre-mortality values and three times higher
than that measured in other, undisturbed populations
(Linares et al., 2007), seem to have sustained this
remarkably high recovery capacity (Cupido et al.,
2009, 2012). However, the population is still far from
its original size/age structure, has attained only half its
pristine density, and has likely stabilized around these
lower values (Table 1). Simulations, carried out using
a transition matrix based on the observed survival of
colonies in subsequent years, also suggest that the
population after deep, dumping oscillations will
remain stable at lower densities also in the future as
well, and will probably reach a new, equilibrium state
at lower density values. A study of the growth trends in
this population extended into the future should enable
determining whether this equilibrium between mor-
tality and recruitment rates will be stable, or if new
dynamics, also provoked by new mass mortality
events, could lead this population to more profound,
undamped oscillations.
On the basis of the studies reported in the previous
chapter, some main features of C. rubrum populations
can be drawn. All the colonies collected from the
different populations and examined by thin section
organic matrix staining dating revealed a slow annual
basal diameter growth rate (0.24–0.26 mm year-1; on
average) and that diameter growth rates fall as colony
age increases (Priori et al., 2013; Bramanti et al.,
2014). The further finding of a constant yearly increase
in the surface of the circular crown area is consistent
with a decrease in diameter growth with colony age.
Due to the asymptotic trend of the relation between
size and age, estimation of the ages of older, larger
colonies ([1 century) has a higher inherent degree of
uncertainty (Doughty et al., 2014). The minimum
legally harvestable size (7 mm GFCM, 2011) is
reached in about 30–35 years. This age estimate
furnishes a timeframe for planning controlled ex-
ploitation (e.g., rotating harvesting plans; Caddy,
1989) by enabling an assessment of the minimum
allowable time interval between two subsequent
harvestings. In this regard, it is worthwhile recalling
that wholesale eradication of colonies has been found
to slow the recovery process, while harvesting that
selectively leaves, smaller colonies and the bases of
larger ones in the field could foster faster recovery of
the harvested populations.
Red coral colonies have a small size and an early
age at first reproduction, thus the small-sized, but
reproductive colonies, which are dominant in crowd-
ed, shallow populations, produce the majority of the
larval output that guarantees population survival. Such
features may have fostered the survival of the over-
harvested populations in the shallower part of the
species distribution range (Santangelo & Abbiati,
2001; Santangelo et al., 2003; Tsounis et al., 2006;
Gallmetzer et al., 2010). The recruitment values found
in these studies are the highest reported for gorgoni-
ans—20–50 times higher than that measured in P.
clavata populations (Linares et al., 2007; Cupido et al.,
2012) and even 100–1,000 times higher than the
lowest recruitment densities reported in other gor-
gonians (e.g., Grigg, 1988; Lasker et al., 1998;
Doughty et al., 2014). Unfortunately, it has not (until
recently) been possible to obtain measures of the
recruitment rates in the sparse, deep-dwelling popula-
tions of red coral.
Contrary to recruitment, the fecundity of red coral
polyps is among the lowest reported for gorgonians
(Torrents & Garrabou, 2011): as some polyps are
sterile, each polyp of a female colony produces on
average less than one mature oocyte (Santangelo et al.,
2003; Priori et al., 2013; Bramanti et al., 2014). The
reproductive output per square meter, calculated in a
crowded, shallow-water population (Santangelo et al.,
2007) was about 38,000 mature oocytes, 20–50 times
less than that measured in P. clavata populations
(720,000–2,000,000 mature oocytes m-2; Coma et al.,
1995; Cupido et al., 2012).
The simulations revealed that the local shallow red
coral population studied (Calafuria Italy) possesses a
considerable capacity to recover from anomalous
mortality events. Nonetheless, any increase in the
frequency of such events (every 3 years) could drive
the population to extinction in about 60 years.
Conclusions
Although several demographic studies have been
conducted on gorgonian coral demography (e.g.,
Grigg, 1977, 1988; Babcock, 1991; Gotelli, 1991;
Lasker, 1991; Chadwick-Furman et al., 2000, Goffredo
Hydrobiologia
123
& Chadwick-Furman, 2003; Linares & Doak, 2010), in
only a few cases has the power of demographic models
to provide projections been fully explored to aid in the
formulation of adequate management and conserva-
tion measures (Bramanti et al., 2014). Current knowl-
edge of the basic demographic features of gorgonian
corals living on deep circalittoral bottoms is rather
limited, as demographic studies on these populations
require precisely targeted, long-lasting (and therefore
costly) research studies (e.g., Doughty et al., 2014).
Such study is nevertheless essential to supply the basic
data for formulating dynamic models in order to
project population trends over time, and thereby guide
the necessary conservation (Caswell, 2001). Determi-
nations of colony age and recruitment, as well as
colony and population reproductive output, are basic
steps in the study of population dynamics. However, to
date only a meager body of literature on marine
benthos deals with descriptors able to link the age
structure of a population with its reproduction in a
unique demographic model (Edmunds and Elahi,
2007; Santangelo et al., 2007; Bramanti et al., 2009;
Edmunds, 2010; Bramanti et al. 2014).
The two temperate gorgonians, whose basic life-
history features are outlined in this review, seem to
represent an example of the adoption of highly
different demographic strategies. Such diverging
strategies are based on values of reproductive output,
recruitment, and colony density which differ by one or
two orders of magnitude and follow’reverse’ trends:
high recruitment densities and low reproductive
output in C. rubrum,—while low recruitment and
high reproductive output in P. clavata. In both cases,
the demographic analysis has revealed some major but
hidden aspects of their dynamics. Even though single
colony samples of these two species may reveal
irregular size class distributions with multiple peaks,
suggesting discontinuous recruitment occurring at a
small spatial scale (Santangelo et al., 2012b; Doughy
et al., 2014), the overall size/age structures of the
populations of both species revealed monotonic,
regularly decreasing patterns, in which recruits are
the dominant class and the proportion of larger/older
class colonies decreases. Such a pattern is consistent
with the hypothesis of populations in a steady state
(with a constant proportion of the number/survival of
the colonies in the different size classes). This finding
has enabled building a static life-history table for a
population of the highly valuable gorgonian C. rubrum
living in the shallow portion of the species bathymetric
range. Based on the frequency of colonies in the
different size/age classes, and the fecundity, fertility
and survival rates, the table was then utilized to
conduct simulations of population trends over time.
These simulations revealed that the red coral popula-
tion possesses a considerable capacity to recover,
albeit slowly, after repeated anomalous mortality
events (Santangelo et al., 2007; Bramanti et al., 2009).
The case study of the non-commercially harvested
gorgonian P. clavata reveals a rather different history.
This population was also subjected to dramatic mass
mortality events that, however, affected larger/older
colonies disproportionally and thereby shifted the
population frequency distribution toward the smaller
sizes. The availability of exhaustive pre- and post-
mortality data on density, recruitment, and size/age
structure over 12 years has allowed us to follow the
population recovery after the anomalous mortality
events. On these bases, it has been possible to
determine the mechanisms underlying this population
recovery from the mass mortality event: recruitment
reached a level five times and colony density 50% that
of the pre-mortality values. This, despite a population
reproductive output that had been reduced by about
93%. The population was divided into size/age classes
according to the colony mean annual growth rate and a
transition matrix constructed based on the actual
survival rate of the colonies in fixed plots over
consecutive years. The population may, some years
after the anomalous mortality events, have reached a
new equilibrium at density values about half the pre-
mortality figures and that it may remain at these lower
values in the future as well. Such findings are
consistent with an overly abundant population repro-
ductive output of this species that, even if reduced
drastically by mass mortality, has nonetheless provid-
ed a number of oocytes sufficient to foster increased
recruitment. These findings are also consistent with
strict density-dependent control of recruitment exerted
mainly by larger colonies in crowded, stable P. clavata
populations that have not been affected by anomalous
mortality events. When this negative, density-depen-
dent control of recruitment is removed by an anoma-
lous increase in mortality, the population starts
recovery rapidly.
Acknowledgments We would like to thank J.M. Gili, S.
Rossi, G. Tsounis, I. Vielmini, the Italian Research group on
Hydrobiologia
123
Red Coral, the researchers and technicians of ISPRA, ENEA
S.Teresa (La Spezia), the Portofino and Cap de Creus MPA
authorities, the Astrea R/V crew, T. Garcia, R. Rinaldi and A.
Ferrucci for their invaluable and friendly help in collecting
deep-dwelling red coral colonies. Our appreciation also goes to
A. Cafazzo for his help in revising the English text. These
studies have been funded by the Italy–Spain UNIPI-CISC
exchange research project, by the Italian PRIN project
2009-2011, the Italian project on Deep-dwelling red coral
populations, MedSea and the COREM European Projects.
L. Bramanti’s work has been funded by a Marie Curie Intra
European fellowship.
References
Angiolillo, M., S. Canese, E. Salvati, M. Giusti, A. Cardinali, M.
Bo & S. Greco, 2009. Presence of Corallium rubrum
assemblages below 50 m along the Calabrian coasts. In
Pergent-Martini, C. & Brichet (eds) UNEP-MAP-RAC/
SPA, 2009. Proceedings of the 1st Symposium on Con-
servation of the Coralligenous Bio-concretions (Tabarka,
January 2009). RAC/SPA publ., Tunis.
Babcock, R. C., 1991. Comparative demography of three spe-
cies of scleractinian corals using age- and size-dependent
classifications. Ecological Monographs 61: 225–244.
Ballesteros, E., 2006. Mediterranean Coralligenous assem-
blages: a synthesis of present knowledge. Oceanography
and Marine Biology: An Annual Review 44: 123–195.
Beiring, E. A. & H. R. Lasker, 2000. Egg production by colonies
of a gorgonian coral. Marine Ecology Progress Series 196:
169–177.
Benayahu, Y. & Y. Loya, 1985. Settlement and recruitment of a
soft coral: why is Xenia macrospiculata a successful
colonizer? Bulletin of Marine Science 36: 177–188.
Bramanti, L., G. Magagnini, L. DeMaio & G. Santangelo, 2005.
Recruitment, early survival and growth of the Mediter-
ranean Red Coral Corallium rubrum 1758, a four-year
study. Journal of Experimental Marine Biology and Ecol-
ogy 314: 69–78.
Bramanti, L., S. Rossi, G. Tsounis, J. M. Gili & G. Santangelo,
2007. Settlement and early survival of red coral on settle-
ment plates: some clues for demography and restoration.
Hydrobiologia 580: 219–224.
Bramanti, L., M. Iannelli & G. Santangelo, 2009. Mathematical
modelling for conservation and management of gorgonian
corals: young and olds, could they coexist? Ecological
Modelling 220: 2851–2856.
Bramanti, L., J. Movilla, M. Guron, E. Calvo, A. Gori, C.
Dominguez-Carrio, J. Grinyo, A. Lopez-Sanz, A. Marti-
nez-Quintana, C. Pelejero, P. Ziveri & S. Rossi, 2013.
Detrimental effects of ocean acidification on the eco-
nomically important Mediterranean red coral (Corallium
rubrum). Global Change Biology 19: 1897–1908.
Bramanti, L., I. Vielmini, S. Rossi, G. Tsounis, M. Iannelli, R.
Cattaneo-Vietti, C. Priori & G. Santangelo, 2014. Demo-
graphic parameters of two populations of red coral (Co-
rallium rubrum L. 1758) in the North Western
Mediterranean. Marine Biology 161: 1015–1026.
Caddy, J. F., 1989. Background concepts for a rotating har-
vesting strategy with particular reference to the Mediter-
ranean red coral Corallium rubrum. Marine Fishery
Review 55: 10–18.
Carpine, C. & M. Grasshoff, 1975. Les gorgonaires de la
Mediterranee. Bulletin de l’Institut Oceanographique
Monaco 71: 1–140.
Caswell, H., 2001. Matrix population models: construction,
analysis and interpretation, 2nd ed. Sinauer Associates,
Sunderland, MA.
Cicogna, F. & R. Cattaneo-Vietti, 1993. Red coral in the
Mediterranean Sea, art, history and science. Ministero
Risorse Agricole, Alimentari e Forestali, Rome.
Cerrano, C., G. Bavestrello, C. N. Bianchi, R. Cattaneo-Vietti,
S. Bava, C. Morganti, C. Morri, P. Picco, G. Sara, S.
Schiapparelli, A. Siccardi & F. Sponga, 2000. A catas-
trophic mass mortality episode of gorgonians and other
organisms in the Ligurian Sea, summer 1999. Ecology
Letters 3: 284–293.
Cerrano, C., A. Arillo, F. Azzini, B. Calcinai, et al., 2005.
Gorgonian population recovery after a mass mortality
event. Aquatic Conservation: Marine and Freshwater
Ecosystems 15: 147–157.
Chadwick-Furman, N. E., S. Goffredo & Y. Loya, 2000. Growth
and population dynamic model of the reef coral Fungia
granulosa Kluzinger, 1879 at Eilat, northern Red Sea.
Journal of Experimental Marine Biology and Ecology 149:
199–218.
Coma, R., M. Ribes, M. Zabala & J. M. Gili, 1995. Reproduction
and cycle of gonadal development in the Mediterranean
gorgonian Paramuricea clavata. Marine Ecology Progress
Series 117: 173–183.
Coma, R., M. Ribes, E. Serrano, E. Jimenez, J. Salat & J. Pas-
cualc, 2009. Global warming-enhanced stratification and
mass mortality events in the Mediterranean. Proceedings of
the National Academy of Sciences USA 106: 6176–6181.
Costantini, F., C. Fauvelot & M. Abbiati, 2007. Fine-scale ge-
netic structuring in Corallium rubrum: evidence of in-
breeding and limited effects of larval dispersal. Marine
Ecology Progress Series 340: 100–119.
Costantini, F., M. Taviani, A. Remia, E. Pintus, P. J. Schembrini
& M. Abbiati, 2010. Deep-water Corallium rubrum L.(1758) from the Mediterranean Sea: preliminary genetic
characterization. Marine Ecology 31: 261–269.
Costantini, F., S. Rossi, E. Pintus, C. Cerrano, J. M. Gili & M.
Abbiati, 2011. Low connectivity and declining genetic
variability along a depth gradient in Corallium rubrum
populations. Coral Reefs 30: 991–1003.
Crisci, C., N. Bensoussan, J. C. Romano & J. Garrabou, 2011.
Temperature anomalies and mortality events in marine
communities: insights on factors behind differential mor-
tality impacts in the NW Mediterranean. Plos ONE 6:
e23814.
Cupido, R., S. Cocito, S. Sgorbini, A. Bordone & G. Santangelo,
2008. Response of a gorgonian (Paramuricea clavata)
population to mortality events: recovery or loss? Aquatic
Conservation: Marine and Freshwater Ecosystems 18:
984–992.
Cupido, R., S. Cocito, M. Barsanti, S. Sgorbini, A. Peirano & G.
Santangelo, 2009. Unexpected long-term population
Hydrobiologia
123
dynamics in a canopy-forming gorgonian following mass
mortality. Marine Ecology Progress Series 394: 195–200.
Cupido, R., S. Cocito, V. Manno, S. Ferrando, A. Peirano, M.
Iannelli, L. Bramanti & G. Santangelo, 2012. Sexual
structure of a highly reproductive, recovering gorgonian
population: quantifying reproductive output. Marine
Ecology Progress Series 469: 25–36.
Doughty, C. L., A. M. Quattrini & E. E. Cordes, 2014. Insights
into the population dynamics of the deep-sea coral genus
Paramuricea in the Gulf of Mexico. Deep Sea Research II
99: 71–82.
Ebert, T. A., 1999. Plant and animal populations. Methods in
demography. Academic Press, S. Diego, CA.
Edmunds, P. J., 2010. The population biology of Porites as-
treoides and Diploria strigosa on a shallow Caribbean reef.
Marine Ecology Progress Series 418: 87e104.
Edmunds, P. J. & R. Elahi, 2007. The demographics of a 15-year
decline in cover of the caribbean reef coral Montastraea
annularis. Ecological Monographs 77: 3–18.
Gallmetzer, I., A. Haselmair & B. Velimirov, 2010. Slow
growth and early sexual maturity: bane and boon for the red
coral Corallium rubrum. Estuarine, Coastal and Shelf
Science 90: 1–10.
Garrabou, J. & J. G. Harmelin, 2002. A 20-year study on life-
history traits of a harvested long-lived temperate coral in
NW Mediterranean: insights into conservation and man-
agement needs. Journal of Animal Ecology 71: 966–978.
Garrabou, J., T. Perez, S. Santoretto & J. G. Harmelin, 2001.
Mass mortality event in red coral Corallium rubrum
populations in the Provence region (France, NW Mediter-
ranean). Marine Ecology Progress Series 217: 263–272.
Garrabou, J., R. Coma, N. Bensoussan, P. Chevaldonne, et al.,
2009. Mass mortality in NW Mediterranean rocky benthic
communities: effects of the 2003 heat wave. Global
Change Biology 15: 1090–1103.
GFCM (General Fisheries Commission for the Mediterranean
Scientific Advisory Committee SAC), 2011. Report of the
transversal workshop on red coral Ajaccio (Corsica),
France, 5–7 October 2011.
Gili, J. M. & R. Coma, 1998. Benthic suspension feeders in
marine food webs. Trends in Ecology and Evolution 13:
297–337.
Goffredo, S. & H. R. Lasker, 2008. An adaptive management
approach to an octocoral fishery based on the Beverton–
Holt model. Coral Reefs 27: 751–761.
Goffredo, S. & N. E. Chadwick-Furman, 2003. Comparative
demography of mushroom corals (Scleractinia: Fungiidae)
at Eilat, northern Red Sea. Marine Biology 142: 411–418.
Gori, A., C. Linares, S. Rossi, R. Coma & J. M. Gili, 2007.
Spatial variability in the reproductive cycle of the gor-
gonians Paramuricea clavata and Eunicella singularis
(Anthozoa, Octocorallia) in the Western Mediterranean
Sea. Marine Biology 151: 1571–1584.
Gori, A., S. Rossi, E. Berganzo, J. L. Pretus, M. R. T. Dale & J.
M. Gili, 2011. Spatial distribution patterns of the gor-
gonians Eunicella singularis, Paramuricea clavata and
Leptogorgia sarmentosa (Cape of Creus, Northwestern
Mediterranean Sea). Marine Biology 158: 143–158.
Gotelli, N. J., 1988. Determinants of recruitment, juvenile
growth and spatial distribution of a shallow water gor-
gonian. Ecology 69: 157–166.
Gotelli, N. J., 1991. Demographic models for Leptogorgia vir-
gulata, a shallow-water gorgonian. Ecology 72: 457–467.
Grigg, R. W., 1977. Demography of population dynamics of two
gorgonian corals. Ecology 58: 278–290.
Grigg, R. W., 1988. Recruitment limitation of a deep benthic
hard-bottom octocoral population in the Hawaiian Islands.
Marine Ecology Progress Series 48: 121–126.
Huete-Stauffer, C., I. Vielmini, M. Palma, A. Navone, P. Pan-
zalis, L. Vezzulli & C. Cerrano, 2011. Paramuricea cla-
vata (Anthozoa, Octocorallia) loss in the Marine Protected
Area of Tavolara (Sardina, Italy) due to a mass mortality
event. Marine Ecology 32: 107–116.
Knowlton, N. & J. B. C. Jackson, 2008. Shifting baselines, local
impacts, and global change on coral reefs. Plos Biology
6(e54): 215e220.
Lasker, H. R., 1991. Population growth of a gorgonian coral:
equilibrium and non-equilibrium sensitivity to changes in
life history variables. Oecologia 86: 503–509.
Lasker, H. R., 2013. Recruitment and resilience of a harvested
Carribean octocoral. Plos ONE 8(9): e74587.
Lasker, H. R., K. Kim & M. A. Cofforth, 1998. Production,
settlement and survival of plexaurid gorgonian recruits.
Marine Ecology Progress Series 162: 111–123.
Ledoux, J. B., J. Garrabou, O. Bianchimani, P. Drap, J. P. Feral
& D. Aurelle, 2010. Fine-scale genetic structure and in-
ferences on population biology in the threatened Mediter-
ranean red coral, Corallium rubrum. Molecular Ecology
19: 4204–4216.
Linares, C. & D. F. Doak, 2010. Forecasting the combined ef-
fects of disparate disturbances on the persistence of long-
lived gorgonians: a case study of Paramuricea clavata.
Marine Ecology Progress Series 402: 59–68.
Linares, C., L. Coma, D. Diaz, M. Zabala, B. Hereu & L.
Dantart, 2005. Immediate and delayed effects of a mass
mortality event on gorgonian population dynamics and
benthic community structure in the NW Mediterranean
Sea. Marine Ecology Progress Series 305: 127–137.
Linares, C., D. Doak, R. Coma, D. Diaz & M. Zabala, 2007.
Life history and viability of a long-lived marine inver-
tebrate: the octocoral Paramuricea clavata. Ecology 88:
918–928.
Liverino, B., 1983. Il corallo. Li CausiEsperienza e ricordi di un
corallario. Li Causi, Bologna.
Marschal, C., J. Garrabou, J. G. Harmelin & M. Pichon, 2004. A
new method for measuring growth and age in the precious
Mediterranean red coral Corallium rubrum (L). Coral
Reefs 23: 423–432.
Mistri, M. & V. U. Ceccherelli, 1994. Growth and secondary
production of the Mediterranean gorgonian Paramuricea
clavata. Marine Ecology Progress Series 103: 291–296.
Pedoni, C., M. C. Follesa, R. Cannas, G. Matta, P. Pesci, & A.
Cau, 2009. Preliminary data on red coral (Corallium
rubrum) population of Sardinian Sea (Western Mediter-
ranean). In Pergent-Martini C. & M. Brichet (eds) UNEP-
MAP-RAC/SPA, 2009. Proceedings of the 1st Symposium
on Conservation of the Coralligenous Bio-concretions
(Tabarka, January 2009). RAC/SPA publ., Tunis.
Pielou, E. C., 1962. The use of plant to neighbor distances for
detection of competition. Journal of Ecology 50: 357–367.
Priori, C., V. Mastascusa, F. Erra, M. Angiolillo, S. Canese & G.
Santangelo, 2013. Demography of deep-dwelling red coral
Hydrobiologia
123
populations. Age and reproductive structure assessment.
Estuarine Coastal and Shelf Science 118: 43–49.
Roark, E. B., T. P. Guilderson, R. B. Dumbar & B. L. Ingram,
2006. Radiocarbon-based ages and growth rates of
Hawaiian deep-sea corals. Marine Ecology Progress Series
327: 1–14.
Ricklefts, R. E. & G. L. Miller, 1999. Ecology, 4th ed. Freeman
and Co., New York.
Rossi, S., G. Tsounis, C. Orejas, T. Padron, J. M. Gili, L. Bra-
manti, N. Teixido & J. Gutt, 2008. Survey of deep-dwelling
red coral (Corallium rubrum) populations at Cap de Creus
(NW Mediterranean). Marine Biology 154: 533–545.
Rossi, S., 2013. The destruction of the ‘‘animal forests’’ in the
ocean: toward an over-simplification of benthic ecosys-
tems. Ocean and Coastal Management 84: 77–85.
Santangelo, G. & M. Abbiati, 2001. Red coral: conservation and
management of an overexploited Mediterranean species.
Aquatic Conservation: Marine and Freshwater Ecosystems
11: 253–259.
Santangelo, G. & L. Bramanti, 2006. Ecology through time: an
overview. Biology Forum 99: 395–424.
Santangelo, G. & L. Bramanti, 2010. Quantifying the decline in
Corallium rubrum populations. Marine Ecology Progress
Series 418: 295–297.
Santangelo, G., M. Abbiati, G. Giannini & F. Cicogna, 1993.
Red coral fishing trends in the Western Mediterranean Sea.
Scientia Marina 57: 139–143.
Santangelo, G., E. Carletti, E. Maggi & L. Bramanti, 2003.
Reproduction and population sexual structure of the over-
exploited Mediterranean red coral Corallium rubrum.
Marine Ecology Progress Series 248: 99–108.
Santangelo, G., L. Bramanti & M. Iannelli, 2007. Population
dynamics and conservation biology of the over-exploited
Mediterranean Red coral. Journal of Theoretical Biology
244: 416–423.
Santangelo, G., R. Cupido, S. Cocito, G. Tsounis, L. Bramanti &
M. Iannelli, 2012a. Demography of long-lived octocorals;
survival and local extinction. Proceedings of the 12th Coral
Reef Symposium Cairns 8–12 July 2012.
Santangelo, G., L. Bramanti, S. Rossi, G. Tsounis, I. Vielmini,
C. Lott & J. M. Gili, 2012b. Patterns of variation in re-
cruitment and post-recruitment processes of the Mediter-
ranean precious gorgonian coral Corallium rubrum.
Journal of Experimental Marine Biology and Ecology 411:
7–13.
Torrents, O. & J. Garrabou, 2011. Fecundity of red coral Co-
rallium rubrum (L) populations inhabiting in contrasting
environmental conditions in the NW Mediterranean.
Marine Biology 158: 1019–1028.
Torrents, O., J. Garrabou, C. Marschal & J. G. Harmelin, 2005.
Age and size at first reproduction in the commercially ex-
ploited red coral Corallium rubrum (L.) in the Marseilles
area (France, NW Mediterranean). Biological Conserva-
tion 121: 391–397.
Tsounis, G., S. Rossi, M. Aranguren, J. M. Gili & W. Arntz,
2006. Effects of spatial variability and colony size on the
reproductive output and gonadal development cycle of the
Mediterranean red coral (Corallium rubrum L.). Marine
Biology 148: 513–527.
Tsounis, G., S. Rossi, J. M. Gili & W. Arntz, 2007. Red coral
fishery at the Costa Brava (NW Mediterranean): case study
for an over harvested precious coral. Ecosystems 10:
975–986.
Tsounis, G., S. Rossi, R. Grigg, G. Santangelo, L. Bramanti & J.
M. Gili, 2010. The exploitation and conservation of pre-
cious corals. Oceanography & Marine Biology: An Annual
Review 48: 161–212.
Tsounis, G., L. Martınez, N. Viladrich, L. Bramanti, A. Martı-
nez, J. M. Gili & S. Rossi, 2012. Effects of human impact
on the reproductive effort and allocation of energy reserves
in the Mediterranean octocoral Paramuricea clavata.
Marine Ecology Progress Series 449: 161–172.
Hydrobiologia
123