BULLETIN OF MARINE SCIENCE, 65(3): 755–760, 1999
RECOVERY OF ECTEINASCIDIA TURBINATA HERMAN 1880 (ASCIDIACEA: PEROPHORIDAE) POPULATIONS AFTER DIFFERENT LEVELS OF HARVESTING ON A SUSTAINABLE BASIS
J. L. Carballo, A. Hernández-Zanuy, S. Naranjo, B. Kukurtzü and Alida García Cagide
ABSTRACT The harvesting of Ecteinascidia turbinata on a sustainable basis could be an example for the production of metabolites from marine organisms while protecting natural popu- lations. A research program was carried out in order to determine the recovery capacity of an E. turbinata population, after carrying out harvesting experiments in the Carribbean and Mediterranean Sea. In the Mediterranean, 25, 40 and 100% of the population was collected, with two collections for each group at 45 and 60 d. There was complete recov- ery of the biomass in the 25 and 40% collections after 45 d, but in the 100% collections only 62% of the biomass had recovered after 60 d. In the Caribbean, 25, 50, 75%, and later 100%, collections were carried out. After 16 d there was a recovery of the density of the population but not of the biomass. After 3 mo there was a recovery of density, biom- ass and root coverage in the 100% collection.
Natural substances obtained from marine invertebrates are currently one of the main sources of new medication against illnesses such as cancer. For a few years research has been carried out on a substance produced by the colonial tunicate Ecteinascidia turbinata Herdman, 1880, which shows activity against various types of solid tumors (Rinehart et al., 1990; Wright et al., 1990). The only current source of this compound are the natural populations of this tunicate whose biogeographical distribution extends over the tropical waters of the Caribbean and some areas of the Mediterranean (Pérès, 1958). The species E. turbinata grows mainly on mangrove roots, although there are some references to its growth over algae or the marine seagrass Thalassia testudinum (Bingham and Young, 1991). Concerning Cuba specifically, the species grows mainly on mangrove roots where there is competition for the substratum, especially with organisms such as sponges and other ascidians (Hernández-Zanuy, 1990). On the other hand, in Estany des Peix, where there is one of the largest currently known populations of the tunicate, the species has a quite different behavior, living directly on the bottom when there is an adequate sediment compositon (coarse sand), and to a lesser extent over marine seagrass and algae such as Caulerpa prolifera (Carballo et al., 1997). There are some references on the exploitation of ascidian populations as a fisheries resource, especially in semi-controlled conditions, for human consumption (Chung et al., 1989). However, there is scarce research on recovery at population level in natural popu- lations where research is directed toward possible commercial exploitation. Bingham and Young (1995) point out that prudent collection methods could permit exploitation of E. turbinata without irreversibly impacting wild populations of the species. Therefore, given the commercial importance of this biological resource as a source of a new drug, the generation of E. turbinata biomass from larvae captured in their natural habitat (Carballo
755 756 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999 et al., 1999), as well as the population´s recovery capacity following controlled collec- tions on a sustainable basis, were investigated. The recovery from the stolon is of great importance since a colony can regenerate from the stolon after damage following a reproductive period. This has adaptative importance especially in a habitat like the Estany des Peix where populations disappear completely at the end of October due to the drop in temperature to levels below the species´ tolerance (Carballo, 1999). The population remains latent until it grows again from the stolon in mid-May. In this manner, the stolon generates the first population which sexually repro- duces in the summer thus producing a new population for the coming winter. This phe- nomenon has also been observed in the mangroves along the coast of Cuba where there are sub-populations that disappear and regenerate from the stolon in a synchronous pat- tern. The main objective of our research was to study the recovery of biomass after differ- ent intensities of experimental harvesting.
MATERIAL AND METHODS
The study was carried out in the Estany des Peix (Formentera Island, Spain) in the Mediterranean Sea, and at Punta del Este (Isla de la Juventud, Cuba) in the Caribbean. The Estany des Peix is a shallow lagoon with a maximum depth of 4 to 5 m with a northwest opening to sea. Its bottom is mainly soft with an algae community consisting mostly of the species C. prolifera. Punta del Este is a mangrove zone (Rhizophora mangle L.) located on Juventud Island (Cuba), separated from the latter´s southeast shoreline by approximately 80 m. This margin is diversely formed, characterized by open channels which sometimes close off at one end. Due to the differing behaviors of the populations of E. turbinata in the Mediterranean and the Caribbean, two different strategies were established for their study. To determine significant differences between the treatments, a one-way ANOVA was used following a log transformation of the data. The significance of the differences between the treatments was tested using the Tukey test. To determine the ability of E. turbinata to recover after different levels of harvesting in the Mediterranean, 16 plots of 9 m2 each were measured out on the bottom of the lagoon where there was a homogeneous density of E. turbinata, thus ensuring that starting conditions would be as similar as possible. Three experimental groups were set up: a 25% collection, a 40% collection and a 100% collection (c-25%, c-40% and c-100%, respectively), with two collections at 45 and 60 d. The life history of E. turbinata in the Mediterranean ecosystem did not allow continuing the experi- ment over a longer period. Even though only two replicates were taken for each treatment, the study area was large enough (288 m2) to obtain representative results. In the Caribbean the experiment was carried out on populations living on the roots of the red mangrove. Six stations were selected with a length of 10 m each, and three experimental groups were established: c-25%, c-50% and c- 75% with two replicates each. The six stations were periodically checked until the population´s recovery appeared complete. Later, another collection, c-100%, was carried out with four replicates that were periodically checked. Three months later the entire biomass was collected to estimate the population´s capacity for regeneration. Recovery success was measured at the end of the experi- ment by comparing the biomass (g m−2) of the experimental plots with the biomass at the two control stations where no collections were made (Mediterranean), and also by comparing the den- sity (colonies per meter of mangrove perimeter) and linear coverage (length of roots covered by E. turbinata) before and after the experiment (Caribbean). In all the experiments care was taken to not damage stolons, and the colonies were not trimmed. CARBALLO ET AL.: RECOVERING STUDY IN ECTEINASCIDIA TURBINATA 757
Figure 1. Mediterranean Sea: a comparison of the biomass at the experiment parcels and the control stations at 45 and 60 d following the collections.
RESULTS
MEDITERRANEAN.—At the end of the 45 d and 60 d experiments the analysis of variance showed that there were no significant differences between the c-25%, c-40% and control plots, indicating a recovery of the biomass (P < 0.05) (Fig. 1). However, in c-100% at 45 d and 60 d, the biomass had not recovered, and only 62% of the biomass in the control plots had recovered in 60 d. In accordance to this, there were significant differences be- tween the plots where 100% of the biomass had been collected and the parcels that served as a control for each of the time periods (P < 0.05; F = 18.8 for 45 d, F = 26.3 for 60 d). Likewise, there were significant differences between the plots where the entire biomass had been collected and remaining plots. The use of control plots, as in the experiments in the Mediterranean, however, helped to monitor the natural evolution of the population density, and effectiveness is observed in the “population recovery” experiment, when a drastic reduction in the density of E. turbinata populations was recorded. For this reason, Figure 1 shows that the average density at 60 d (g m−2) in both control and experimental plots was lower than at 45 d, due to natural changes in the E. turbinata population. CARIBBEAN.—The analysis of variance indicated that there were no significant differ- ences in the initial and final (after 16 d) densities of the colonies (colonies per meter of mangrove perimeter). When biomass is not measured, population production was esti- mated as the length of the root coverage since there was the same density of colonies as at the beginning of the treatment, although some were of a much smaller size and therefore of a lesser biomass and productivity. According to these results it appears that the length of root coverage had not completely recovered 16 d after the collection (Fig. 2). However, the analysis of variance indicates that there were no significant differences among the 758 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999
Figure 2. Caribbean: length of mangrove root coverage (left axis), and density (right axis), 16 and 90 d, respectively, after the collection.
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treatments for this parameter, probably because we had fewer replicates and therefore the test was less sensitive (Nieves, pers. comm.). On the other hand, in the c-100% experi- ment (Fig. 2), there was a general recovery in the number of total colonies and the density of colonies per meter of mangrove perimeter (Table 1). In contrast to the previous experi- ment, there were significant differences between the length of root coverage (P < 0.05, F = 7.1), and the initial and final biomass (P < 0.05, F = 7.8).
DISCUSSION
A study of mangrove roots in the Florida Keys (Bingham and Young, 1995) showed large temporal variability in an E. turbinata population, due to predation and/or natural change, although they lived at least 3 yrs. In Puerto Rico, Morgan (1979) reported that a colony grows exponentially through budding and duplicates its size every 6 d for a period of 50 d, reaching sexual maturity at the end. The old zooids die off immediately and the remaining tissues die after 120 d, leaving behind a network of stolons from which subse- quent generations of zooids originate. These mature after 20 d and die after 50 d. This CARBALLO ET AL.: RECOVERING STUDY IN ECTEINASCIDIA TURBINATA 759 regression and regeneration process continues until the colony is invaded by a competitor or destroyed by a predator. We observed that the colonies which do not reach sexual maturity remain stable for a longer period of time in terms of biomass, or area occupied on the root than those which do mature. Therefore, the minimum time recorded by us to determine recovery of the biomass after a harvest, appears to match Morgan’s period of 50 d. The recovery of an entire population of E. turbinata seems adequate after collecting 25% to 40% of the total biomass, whereas it is slower when 100% of the biomass is collected. Thus the optimum rate of harvesting, at least in the Mediterranean ecosystem, should be between 25 and 40% of the population, with a waiting period of at least 45 d before a second harvest if there is no damage to the stolon during harvesting. This pro- cess, however, may have difficulties if applied in Cuba due to the heavy competition for the free space on the mangrove roots by other organisms such as sponges or ascidians of the genus Ecteinascidia. Although competition for the substratum is the subject of an- other study and is not reflected in our results, the poor results obtained in the c-100% experiments (replicate 4) in Cuba were due to the presence of competitors, especially sponges, that occupied the space available after eliminating E. turbinata biomass from the mangrove roots. However, in the mangroves the recovery is also quick if caution is taken to leave the stolon intact as well as part of the population, as observed in the first experiment. When the entire biomass is removed, even if the stolon is untouched, the empty space is rapidly taken over by other ascidian species or by sponges, which do not permit a complete recovery of the biomass even 3 mo after the collection. However, to obtain a faster recovery of the population it would be advisable to leave part of it behind since a re-emergence of healthy zooids from the basal stolons seems possible. The asexual reproduction of E. turbinata seems to guarantee an extremely high degree of genetic relatedness in local populations. Jackson (1986) suggests that high levels of genetic relat- edness within clonal populations are not an accidental consequence of short-distance dispersal, but the result of natural selection for the retention of young near parents. A study on the larval ecology of E. turbinata in Formentera indicated that the majority of the larvae remained close to their parent colonies (Carballo, 1999). Therefore, the larvae of neighboring colonies take over the empty space, thus reestablishing the population. Nevertheless, the recovery of a population of E. turbinata can occur in two different ways, either from the stolon or by the recruitment of larvae. In the experiment carried out in the mangroves of Cuba where 100% of the biomass was collected, harvesting was done by carefully leaving the greatest part of the stolon intact on the mangrove root to allow for the recovery of the initial population from the stolons. However, the experiment could not be isolated completely from the rest of the population in its natural surroundings, and although the larvae have a limited displacement capacity, the results could depend to a certain degree on the density of the population and its reproductive state.
ACKNOWLEDGMENTS
We wish to thank F. de la Calle and Jesús, the boat captain, for their help at different stages of our work in Formentera Island. We also thank Macario, Alina, and the entire crew of the KAMARACO, as well as the personnel at the metereological radar station on Isla de la Juventud, for their help in the mangroves of Punta del Este. Thanks to A. Velasco for assistance with the translation of this article. 760 BULLETIN OF MARINE SCIENCE, VOL. 65, NO. 3, 1999
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DATE SUBMITED: October 7, 1998. DATE ACCEPTED: May 7, 1999.
ADDRESSES: (J.L.C.) Instituto de Ciencias del Mar y Limnología, UNAM—Estación Mazatlán, Apartado Postal 811, Mazatlán 82000, Mexico. E-mail: