Red coral: conservation and management of an over-exploited Mediterranean species

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 253–259 (2001)

DOI: 10.1002/aqc.451

Red coral: conser�ation and management of ano�er-exploited Mediterranean species

GIOVANNI SANTANGELOa,* and MARCO ABBIATIb,c,1

a Dipartimento di Etologia, Ecologia, E�oluzione, Pisa, Italyb Centro Interdipartimentale di Ricerca per le Scienze Ambientali, Ra�enna, Italy

c Dipartimento di Biologia E�oluzionistica Sperimentale, Uni�ersita di Bologna, Bologna, Italy

ABSTRACT

1. Corallium rubrum is a precious circum-Mediterranean octocoral, which occurs on rocky reefsbetween 10 and over 250 m in depth.

2. This species has been harvested for a long time and most commercial populations have beenover-exploited. The Mediterranean overall yield was reduced by 66% over the last 15 years.

3. Two type populations may be identified: (a) dense shallow-water populations consisting ofsmall, slow-growing, short-lived colonies and (b) deep-dwelling populations, composed of large,sparse, long-lived colonies. The former populations have little economic value, but should ensurea reproductive stock for the species.

4. While the structure and demography of shallow-water populations have been studied, thedemographic parameters of deep-dwelling populations are largely unknown.

5. Recent genetic studies quantified levels of genetic divergence among coastal populations.Estimated numbers of migrants among populations suggested that the planulae of C. rubrum haveshort-range dispersal. Geographic distances greater than 100 km can be considered as the thresholdfor genetic divergence between populations.

6. Development of a regime for the sustainable exploitation of this species requires a betterknowledge of population dynamics, life-history traits and quantitative genetics, especiallyconcerning commercial populations.Copyright © 2001 John Wiley & Sons, Ltd.

KEY WORDS: conservation strategies; Corallium rubrum ; harvesting data; population dynamics; populationgenetics

INTRODUCTION

Red coral (Corallium rubrum L 1758) is a species endemic in the Mediterranean Sea and neighbouringAtlantic coasts, where it occurs on rocky reefs between 10 and 250 m in depth (Laborel and Vacelet, 1961;Zibrowius et al., 1984). The species is harvested in both Western and Eastern Mediterranean countries,with major commercial stocks located in the Western Mediterranean. Red coral is one of the distinctive

* Correspondence to: Giovanni Santangelo, Dipartimento di Etologia, Ecologia, Evoluzione, Via Volta 6, I-56126 Pisa, Italy.E-mail: [email protected] E-mail: [email protected]

Copyright © 2001 John Wiley & Sons, Ltd. Received 20 August 2000Accepted 22 November 2000

G. SANTANGELO AND M. ABBIATI254

components of the Mediterranean ‘coralligenous’ biogenic reefs (Gili and Coma, 1998) and of thesemi-dark cave species assemblages (Laborel and Vacelet, 1961). According to Weinberg (1979),temperatures higher than 20–21°C, together with high light intensities, limit the upper distribution of thisoctocoral.

Two types of red coral populations may be identified. Shallow-water populations occur on vertical cliffsand in caves at a depth range between 10 and 60 m and consist at present of crowded small, slow-growing,short-lived colonies which are often heavily affected by boring sponges (Corriero et al., 1997; Cicogna etal., 1999). Deeper than 60 m, red coral occurs mainly on rocky outcrops. These deep-dwelling populationsconsist of large, sparse, long-lived colonies (Santangelo et al., 1999). Nowadays, only the latterpopulations have commercial value. The main bulk of available knowledge refers to the more accessiblecoastal populations of this species. These are ecologically interesting, because of their high reproductionrates that ensure a stock of breeders for the species. Only limited knowledge is available for the deeperdwelling commercial populations.

Red coral has been harvested since ancient times and commercial, deep-dwelling populations have beenwidely over-exploited (Cicogna et al., 1999). In the recent past the international community has shownrenewed interest for this resource, and some efforts have been made to increase the knowledge ofpopulation biology and dynamics of this precious species (GFCM, 1984, 1989). The goals of this paperare to analyse red coral fishing trends over the last decade, to summarize the actual knowledge on thebiology of the species and, based on this knowledge, to suggest preliminary criteria for red coralsustainable exploitation.

FISHING

Data on red coral harvesting examined in the present work were obtained from FAO (1998) FisheryStatistics. These data are usually provided by wholesales of the coral-processing sector and thereforerepresent estimates, rather than precise fishing records. Likely they are an under-estimation of the overallMediterranean yield and, although not completely reliable, they are the only data available.

Red coral fishing trends in the Western Mediterranean during the period 1981–1991 have beenpreviously examined (Santangelo et al., 1993). During that period, the Western Mediterranean yield(accounting for most of the overall Mediterranean harvesting) underwent a 50% reduction. Here weexamine the overall Mediterranean fishing trend of red coral in the period 1987–1996. Data revealed areduction of more than 40% of the overall harvesting during this period (Figure 1). Sharp variations inthe yield are strictly related to the availability of the resource. Exhaustion of commercial banks ordiscoveries of new exploitable areas are followed by a drop or a peak in the yield, respectively.

FAO (1998) Official Fishery Statistics provides data for the following countries: Italy, France, Spain,Greece, Croatia, Albania, Tunisia, Morocco and Algeria. Two major patterns of the resource exploitationemerged. For the sake of simplicity, hereafter we shall refer to the first five of the above-mentionedcountries as ‘Type I countries’, while the last four are referred to as ‘Type II countries’. A decreasing trendover time is evident for ‘Type I countries’ (Figure 1). Irregular fluctuations of the yield over time areevident for ‘Type II countries’ (Figure 1) even if some reduction of the yield (11700 kg in 1987 versus 9275in 1996) is observed. The yield curve for the ‘Type II countries’ is characterized by two peaks: one in 1988and the other in 1991. The first peak is mainly due to an increase of harvesting in Morocco (8400 kg in1988 versus 6200 in 1987), the second peak is due to the rapid increase of Algerian harvesting (12000 in1991 versus 4244 kg in 1990). Both countries experienced a sharp fall in yield after these peaks. While in1991 North African countries accounted for more than 50% of the overall Mediterranean yield, in 1996they accounted for 32% only.

Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 253–259 (2001)

RED CORAL CONSERVATION 255

Figure 1. Temporal variations of: (1) overall Mediterranean red coral yield; (2) Type I country yield (Italy, France, Spain, Greece,Croatia); (3) Type II country yield (Albania, Tunisia, Morocco, Algeria).

LIFE HISTORY AND DEMOGRAPHY

In recent years the main demographic parameters of red coral shallow-water populations have beendescribed (Abbiati et al., 1991; Cicogna and Cattaneo-Vietti, 1993) and a preliminary model forpopulation dynamics was developed (Abbiati et al., 1992). Some efforts were also made to describe theage structure of deep-dwelling populations (Garcia-Rodriguez and Masso, 1986; Santangelo et al., 1999).

Data on age structure and demographic parameter here discussed have been gathered from populationsliving along the Western Italian coast, as described in Abbiati et al. (1992) and Santangelo et al. (1999).The age of the colonies was determined on the basis of ‘growth rings’ analysis, according to the proceduredescribed in Santangelo (1991). Data on a deep-dwelling population were gathered form colonies collectedby professional fishermen (Santangelo et al., 1999).

Red coral is a gonocoric, brooder species, which broods semi-pelagic, lecitotrophic larvae (planulae).The ‘planulation’ period ranges between July and August and in September juveniles (recruits) may beobserved. A close, positive relationship was found between density of recruits and adults. This suggests aphilopatric behaviour of planulae and consequently that recruitment occurs mainly locally. Recruitdensities in the coastal population studied showed an average value of 33 individuals dm−2, whichaccounted for more than 50% of the overall number of colonies in the population. As it may be observed



in the ‘life table’ (Table 1), there is heavy mortality of recruits during the first year. A drop in colonyabundance is also evident at the 4th year age class, which can be probably attributed to collection oflarger colonies by recreational divers (Abbiati et al., 1992). The life table reports: age; number and densityof colonies in each age class, survival probability and birth (reproduction) coefficients of the colonies ineach age class. These data allow calculation of larval production by single age class and provide anestimate of the total number of planulae produced by the studied population.

Ten age classes were identified in the population, and a 10-year life span was thereby estimated. On thebasis of these data, an exponential curve (with negative exponent) was fitted to represent the age–sizedistribution of the colonies (Abbiati et al., 1992; Santangelo et al., 1999). As similar curves were calculatedfrom samples taken at different times, between 1991 and 1996, the population may be considered in a‘steady state’ during the period examined.

Morphometric data obtained from a deep-dwelling, commercial population (Santangelo et al., 1999)indicate a growth rate in colony diameter notably greater than that measured in coastal populationsstudied (1.57 mm year−1 versus 0.93 mm year−1, respectively). The high growth rate measured in thiscommercial population is comparable to that measured by Garcia-Rodriguez and Masso (1986) oncommercial colonies from the Gerona coast (1.32 mm year−1). No knowledge is available, at present, onreproduction, recruitment, mortality rates of deep-dwelling, commercial populations.

POPULATION GENETICS

The genetic structure of red coral populations has been investigated by means of allozymeselectrophoresis. Samples, consisting of about 100 red coral colonies, were collected by scuba diving alongthe Western Mediterranean coasts (Abbiati et al., 1993, 1995, 1999). Each colony, issued from a singleplanula larva, was considered as an individual. Allele frequencies were calculated and statistical analysesof electrophoretic data were performed. Levels of genetic divergence among population were assessedusing Nei’s genetic identity (I) and distance (D) indices.

Table 1. Frequency distribution of Corallium rubrum colonies

Xi+1/XiN biXiiYears biXi

(colonies 48.26 dm−2) (colonies dm−2)

0 01 1591 32.96(0–1) 0.490 02 777 16.1(1–2) 0.41

000.406.593183(2–3)142 17 892(3–4) 4 126 2.61 0.21

55902150.500.54265(4–5)2990.300.27 3887136(5–6)395 1580(6–7) 7 4 0.08

(7–8) 8 4 0.08 500 20001840(8–9) 9 3 0.06 614

0.02110(9–10) 738738

Total 33 52759.31

Age class (i ); number of colonies for each age class (Xi); survival coefficients (Xi+1); birth coefficients(bi) and number of planulae produced by each age class (bi, Xi). The first three age classes do notreproduce.



Mediterranean populations of C. rubrum showed significant levels of genetic differentiation. Nei’sdistances between populations were comparable to those reported for other cnidarians, the geneticsubdivisions of which have been attributed to short-range larval dispersal (Ayre and Dufty, 1994;Hellberg, 1995). A peculiar relationship between genetic differentiation and geographic distance wasobserved (Figure 2). Within a distance range of 102–105 m, genetic divergence is low and stable, andpopulations can be considered panmictic. A sharp increase of Nei’s D values and genetic structuringof the species in subpopulations is observed over 105 m (Abbiati et al., 1999). A more detailedanalysis of the genetic structure of red coral populations across the range 105–106 m is needed toprovide more insight into the occurrence of a distance threshold for population differentiation in thisspecies.

Genetic data could provide two major contributions to the conservation strategies of C. rubrum.The first is the evidence that larval dispersal of red coral is limited, considering the geographicdistribution of the species. Direct tracking of the larvae of red coral is difficult, compared withtropical scleractinians, due to the depth at which this species lives and to the non-synchronousspawning. Several authors have suggested contrasting hypotheses on the range of dispersal abilities ofthe planulae (Weinberg, 1979 and references therein). However, genetic data provide indirectestimation of the dispersal ability of red coral planulae, which ensure effective gene exchange betweenpopulations within a distance of about 100 km. It is unlikely that individual planulae can disperseover distance of 100 km, but within this range planulae can cross gaps between habitats suitable tosettlement. The underlying population structure of this species may conform to the one-dimensionalstepping stone model (Kimura and Weiss, 1964), the coastline being the dimension. This information,besides being a contribution to the knowledge of the biology of the species, has important implicationsfor the management and provides an explanation for the extremely low rates of recovery ofover-exploited banks reported by Cattaneo-Vietti et al. (in Cicogna et al., 1999).

The second relevant contribution is that genetic data clearly show that Mediterranean red coralcannot be considered as a single genetically homogeneous population. Preservation of genetic variationand maintenance of population structure are desirable goals for red coral management. To this aim,management of this resource should be defined at a regional scale. It is important that eachpopulation is harvested separately in order to avoid over-exploitation, which might lead to commercialextinction of individual banks.

Figure 2. Relationship between values of genetic distance, according to Nei (D), and geographic distance between pairs ofMediterranean populations analysed (modified after Abbiati et al., 1999, reproduced by permission of M Abbiati, S Novelli, JG

Harmalen and G Santagelo).



CONCLUSION

Mediterranean red coral fishing data in the period 1987–1996 reveal a trend of heavy reduction in totalharvest. During this period, in fact, overall yield in Italy, France, Spain, Greece and Croatia fell by aboutone half. Overall harvesting data for Albania, Tunisia, Morocco and Algeria, in comparison, showirregular fluctuations over the period, suggesting that these countries followed a ‘boom and burst’harvesting strategy, the consequences of which are now painfully evident. Despite the downward trend intotal harvest, red coral cannot be considered an endangered species because of the large number ofshallow water populations that remain only moderately exploited. A new approach in the managementand the development of conservation strategies for the species is needed. Application of the precautionaryprinciple for red coral conservation requires a protection of coastal populations in order to ensure areproductive stock for the species. A sound knowledge of demographic parameters and ecology ofcommercial red coral populations is also essential. Several types of rotating harvesting have beenproposed for the species (Caddy, 1993). In this approach the critical parameter is the spatial scale of therotation. Red coral populations are mainly self-seeders and recolonization of over-exploited areas is a veryslow process. Genetic studies showed that larval dispersal of red coral is limited: about 100 km can beconsidered the effective dispersal range for this species. The theoretical background necessary for thesustainable exploitation of red coral requires a sound knowledge of population dynamics, life-historytraits and quantitative genetics. Managing a complex of genetically distinct populations involvesdifficulties at the national and international levels, however, this is the only conservation approach thatcan be applied to genetically structured species (Ryman and Utter, 1987). All Mediterranean countriesneed to set up a common policy for red coral conservation by defining harvesting rules concerningminimum colony size, maximum yield per area and harvesting seasons.

ACKNOWLEDGEMENTS

The authors thank the numerous collaborators that contributed to the research on red coral ecology. We are alsograteful to R. Cattaneo-Vietti, J.G. Harmelin and L. Airoldi for reviewing the manuscript. This study was partiallysupported by a grant from the Italian Ministry of Agricultural Policies and by ‘60%’ grants from the Italian Ministryof University and of Scientific and Technological Research, and from the Italian National Council for Researches(CNR), Project 03642 5774.

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Red coral: conservation and management of an over-exploited Mediterranean species

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