This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and

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2 Fisheries Research 99 (2009) 7 16 Contents lists available at ScienceDirect Fisheries Research journal homepage: Historical analysis of Cuban commercial fishing effort and the effects of management interventions on important reef fishes from Rodolfo Claro a, Yvonne Sadovy de Mitcheson b,, Kenyon C. Lindeman c, Alida R. García-Cagide a a Instituto de Oceanología, Cuba b University of Hong Kong, Hong Kong and Society for the Conservation of Reef Fish Aggregations, Hong Kong c Florida Institute of Technology, United States article info abstract Article history: Received 29 September 2008 Received in revised form 10 April 2009 Accepted 14 April 2009 Keywords: Spawning aggregation Reef fish Snappers Groupers Management Cuba Long-term fishery datasets can provide valuable insights into fishing histories, and represent a baseline against which to examine current status and plan for future management. For coral reef-associated fisheries, however, such datasets are extremely rare. We analyse a unique 45-year set of landings data on six reef fishes of commercial importance in Cuba s coastal fisheries, together with information on management interventions, and examine the likely implications of over-fishing and management on the long-term condition of one grouper (Serranidae) and five snapper (Lutjanidae) species. The data clearly demonstrate differential responses to fishing and management according to the biology of the different species examined. In particular, those species that aggregate most predictably, and at a small number of spawning sites, are more prone to uncontrolled fishing and in need of effective management. The increase in the number and severity of management measures over the last 20 years reflects attempts to address declines in the fishery following its development prior to the 1980s. The data suggest short-lived successes, and challenges to successful management from changing socio-economic circumstances and environmental impacts. The importance of considering, in addition to landings information, social and economic factors, management history, the biology of targeted species and the implications of environmental factors in relation to resource use, trends, and management is clearly illustrated in this study. Managers should strive to document species-specific data over the long-term and aim for robust and adaptive fishery management that constantly adjusts to the range of factors that affect fishing activity, exploited species, and responses to management Elsevier B.V. All rights reserved. 1. Introduction Within the tropics, our understanding of the history of coastal fisheries and the impacts of management interventions is seriously undermined by an almost complete absence of the type of long-term species-specific data available for many temperate fisheries. One of the very few exceptions is the detailed multi-decadal database on the coastal fishery of Cuba, a government-owned and managed fishing industry. Because of natural variability in fish populations over time and how this might interact with management actions, especially in the case of multi-species fisheries, long-term fishery data are particularly for providing important insights into the actual or probable effects of management and other biotic and abiotic factors on landings. The lessons learned from such information provide valuable guidance for future action that can be framed in more precautionary and practical terms than is possible in the absence of such a fishery history. The coastal fishery of Cuba repre- Corresponding author. Tel.: ; fax: address: yjsadovy@hku.hk (Y.S.d. Mitcheson). sents a unique long-term record of a tropical, multi-species, fishery that promises to teach much about the interplay between fishery management and other social factors, and the biology of key exploited species. Traditionally, the catches of reef-associated finfishes in Cuba have shown strong seasonal trends, mainly associated with the reproductive periods of the most economically important species, among them snappers (Lutjanidae) and groupers (Serranidae). This seasonality in catch trends is determined by the increased vulnerability of aggregating species to fishing during the reproductive period and the resulting focus of fishing activity on spawning individuals which yield a large proportion of annual catches of such species (Baisre, 1985, 2000, 2004; Claro et al., 2001). Since the responses of aggregating species to fishing vary according to the biology of different targeted species, an understanding of the impacts of fishing and the consequences of management can only be understood by species-specific analyses in the context of the coastal fishery and its management history as a whole. The history of the coastal, reef-associated, fishery of Cuba is one of increasing and decreasing fishing pressure and variable management effectiveness that ultimately led to substantial declines /$ see front matter 2009 Elsevier B.V. All rights reserved. doi: /j.fishres

3 8 R. Claro et al. / Fisheries Research 99 (2009) 7 16 in most key commercial species. Until 1955, commercial catches of fishes and invertebrates on the Cuban coastal platform did not exceed 10,000 tonnes annually, but, by the 1970s several species were over-fished, despite the introduction of management measures (Baisre, 1985; Baisre and Páez, 1981; Claro et al., 2001). Up until the 1960s, catches increased to 21,000 tonnes (18,000 tonnes from national waters, the remainder from the Gulf of Mexico) and demand for fish was relatively low with a focus on high quality species and larger sizes of fish (Baisre, 2004). Subsequently, demand for seafood increased due to shortages in other food products as a result of trade embargoes, resulting in the introduction of large-scale fishing gears, such as bottom trawls, long set nets and small-meshed fish traps. Until the mid 1960s the coastal fisheries in Cuba were considered under-exploited, but an increase in fishing effort, fueled by the introduction of motorized boats and large-scale fishing gears and a relaxation of fishing regulations led to over-fishing of several species by the 1970s. Particularly affected were the lane snapper (Lutjanus synagris) in the main fishing area for this species, the Gulf of Batabano, mullets (Mugilidae) in the coastal lagoons of the southeast, the Nassau grouper (Epinephelus striatus) in almost all areas, the queen conch (Strombus gigas) in several regions, and shrimp in Ensenada of the Broa and the southeast region (Claro et al., 2001). To address over-fishing an administrative process was initiated in the 1980s to reduce commercial fishing effort on the most intensively exploited resources, although overall fishing pressure was not reduced until To reduce commercial fishing effort in the 1980s, some of the effort was redirected towards hitherto under-fished resources, generally of smaller value and quality, such as stingrays, mojarras, porgies, Atlantic thread herring (Opisthonema oglinum), blackedge cusk-eel (Lepophidium brevibarbe), clams, swimming crabs and others (Baisre, 2000; Claro et al., 2001). Regulations were introduced to protect some fish populations, including closures, limits to fishing effort and quotas, and these are likely to have favoured the persistence of the spawning aggregations of the most important species (snappers). Although overall fishing effort decreased in terms of number of fishing boats and fishing gears, the organization and efficiency of the fishery increased due to several factors: (1) catch reception points were established at sea, close to fishing grounds, to reduce navigation time (and fuel), so that fishermen could spend more time fishing; (2) administrative measures were established to encourage fishermen to work 20 days every month (some fishermen do not work if they have sufficient money); and (3) economic incentives were available for boats to develop annual catch plans. While the combined effects of these and other changes in the coastal fishery stabilized overall catch during the 1980s, species had evidently reached maximum sustainable yield (Baisre, unpublished; Baisre, 1985; Baisre and Páez, 1981). By the early 1990s, despite an overall reduction in commercial fishing effort due to an economic crisis that reduced fishing, recovery in landings failed to occur. In the second half of the 1990s both commercial and subsistence fishing increased and only by the end of the 1990s was fishing effort reduced with the creation of the National Organization for Fishing Inspection. Subsistence fishing includes both poaching and licensed recreational, or sport, fishing. Snappers and the Nassau grouper are traditionally considered to be major finfish resources in Cuba but many of these species have declined over the last 4 decades. The existence of extensive seagrass beds (feeding areas) close to reefs, and mangroves (refuge areas) are favourable conditions for supporting large populations of mutton (Lutjanus analis), lane, L. synagris, cubera (Lutjanus cyanopterus) grey (L. griseus) and yellowtail snappers (Ocyurus chrysurus). The Nassau grouper was an important fishery resource until the 1970s and inhabited coral reefs along the insular shelf. The fishery of snappers and groupers in Cuba typically concentrated on seasonal spawning aggregations. In addition to fishing activities, habitat degradation has occurred in many near-shore areas over the last two decades (Claro et al., 2006). The objectives of this paper are (1) to describe the history and changes in catches over 45 years in the commercial Cuban fishery, with a focus on five species of snapper and a single species of grouper, the Nassau grouper, (2) to analyse the various factors that have likely influenced landings over the same time period, inclusive of fishery management, social conditions, fishing practices and ecological characteristics of the six species in (1) above, and (3) to evaluate the probable implications of the concentration of fishing effort on fish spawning aggregations, with a view to improving the management of aggregating species. 2. Methods Total coastal finfish landings for six targeted aggregating species and overall fishing effort in the Cuban fishery were compiled from a range of sources. Total finfish catch since 1955, and monthly catches from the Cuban shelf between 1962 and 2005 for each of five snapper species and for the Nassau grouper, were obtained from monthly and annual fisheries statistical reports elaborated by the Directorate of Fisheries Statistics of the Ministry of Cuba and available at regional fisheries agencies of the Ministry. Average monthly catches for sequential five-year periods were estimated for each species and data recorded by region. From the 1960s onwards, the Cuban shelf was divided into four fishing regions for reporting purposes; southeast, southwest, northwest and northeast. Data on total annual fishing effort (boat-days fishing) were also obtained. Due to the multi-species character of the fisheries, it was not possible to estimate fishing effort at the species level. However, total fishing effort in the finfish fishery overall was available from 1980 to 2005, and likely affected all species similarly. For most species studied, commercial catches were recorded at the species level. For cubera and grey snappers, catches were registered together until 1982 and later separately, but species identification is not considered to be reliable (RC personal observation), i.e., small fishes (<40 cm) were typically treated as grey snapper, medium or large fishes as cubera snapper. Therefore, data were combined for these two species and treated as the grey-cubera fishery. Supplementary information was collected from fishers, fish biologists and the published literature to identify possible biases in the data and to describe biological characteristics of the species, including spawning season, spawning and nursery habitats and other environmental factors. Over 30 interviews of fishing boat captains and crew were conducted in western and northern Cuba between 1994 and 1996, and in In addition to the fishery data and anecdotal information, published and grey literature were summarized to construct an overall history of the fishery for each of the six species, inclusive of management interventions. Approximate locations of exploited spawning aggregation sites of the study species are shown in Fig Results Fishing activity consists of both commercial and subsistence fishing sectors. While these two sectors vary over time in terms of their relative importance and in the reliability of associated catch data, commercial fishing accounts for the majority of the landings and for the most reliable landings information. It is important to briefly consider the different fishery sectors for possible biases in the database examined in this study. Until the mid 1990s, both fishery landings and fishing effort data were considered to be reliable indicators of commercial fishing activity because the only autho-

4 Fig. 1. Approximate locations of exploited spawning aggregation sites for five snappers and the Nassau grouper on the Cuban shelf, showing the species that aggregate at each one, and the peak months of spawning for each species (modified from Claro and Lindeman, 2003). R. Claro et al. / Fisheries Research 99 (2009)

5 10 R. Claro et al. / Fisheries Research 99 (2009) 7 16 Fig. 2. Total finfish catches from the Cuban shelf between 1959 and 2005, total finfish effort (boat-fishing days) and catch per unit effort (CPUE measured as catch/boat-fishing days) since rized entity in the country allowed to buy commercial catches from fishers were government enterprises of the Ministry of the Fisheries Industry, and most landings were commercial. In the mid 1990s, subsistence fishing increased due to an economic crisis. This introduced uncertainty regarding the reliability of catch and effort information because subsistence catch was sold on the black market or used for family consumption and is typically not reflected in government landings. As an indication of the relative importance of subsistence versus commercial landings, anecdotal and sport license information suggest that sport fishing in the Archipelago Sabana-Camagüey is about 1800 tonnes yearly (Claro et al., 2004) and illegal fishing may reach approximately 500 tonnes. This compares with the much higher total commercial finfish catch over the same period in the same zone at about 6000 tonnes. In other fishing zones, the subsistence fishery is not as important because fishing grounds are less accessible to subsistence fishers. Hence, the commercial fishery is not only the most important by weight, it is also that which is most reliably recorded. Examining the coastal finfish fishery as a whole, the total catches (Fig. 2) show the typical phases of a fishery that is moving from an under- to an over-fished phase, as described by Caddy (1984); under-utilization before 1960, and fast growth from 1961 to 1975 followed by marked declines in species of key commercial importance, as determined in the present study (Nassau grouper, lane snapper, grey/cubera snapper, mullets). This situation provoked the introduction of management measures from the 1980s onwards (Table 1). Simultaneously, the organization and efficiency of the commercial fishery increased during the same decade. From 1994 to 2000, fishing effort decreased, evidently favouring an increase in catch per unit effort (CPUE). Overall catches and CPUE declined after 2000 (Fig. 2). Review of commercial landings between 1978 and 1995 for species other than those addressed in the current study reveals very different trends, although there is not the same level of species-specific detail as for the six focal species of this study. Among other reef fishes, notable declines occurred in mullet (several species), fluctuating landings or less marked declines were noted for grunts (Haemulidae) and jacks (Carangidae), while increases were recorded for mojarras (Gerreidae) (Claro et al., 2001). (Fig. 3A). Most catches of Nassau grouper (35 50% of the national capture of the species) were historically taken in the Archipelago Sabana-Camagüey (north-central area, Fig. 1; Claro et al., 2001). Although up until 1969 an important proportion of this catch was obtained from the Bahamas shelf, the distribution of fishing effort in the different countries was not known because landings information was not distinguished by fishing area across countries. Particularly notable was the sharp decline in Cuban national catches after Fig. 2 shows a remarkable drop in the national catches 3.1. E. striatus (Nassau grouper) Fishing pressure on the Nassau grouper increased notably after 1959, reaching 1700 tonnes in 1963, after which time landings declined despite the increase in fishing pressure on the Cuban shelf Fig. 3. Annual catches of Nassau grouper, Epinephelus striatus, in Cuba (A) and average monthly catches by five-year periods (B).

6 R. Claro et al. / Fisheries Research 99 (2009) Table 1 Some fishery regulations established or planned by the Cuban Ministry of Fisheries relevant to studied fish stocks and/or their spawning aggregations. Resolution/year Regulation Species affected by the regulation 1980s Many miscellaneous regulations addressed particular species or regions and were often Multiple species introduced for short periods of time and by particular Fishing Associations, e.g. seasonal spawning closures, gear bans, fishing effort control, etc. No. 561/1996 Established minimum legal sizes for commercial fishes. For lane snapper 120g=18cmFL, 92 finfish and invertebrate species for grey snapper 170g=22cm,forcuberasnapper 460g=31cm,formutton snapper 230g=24cm,foryellowtail snapper 140g=20cmandforNassau grouper 570g=32cm. No. 519/1996 Established bag limits for recreational fishing: All six studied species, as well as other - 15 kg/trip in areas of high economic importance for commercial fishing - 30 kg/trip in areas of low economic importance species No. 74/1997 Established regulations to increase selectivity of several fishing gears: minimum size mesh All six studied species as well as other species of 30 mm for some parts of traps and trawls, obligatory use of selective fishing devices to avoid the catch of juveniles and small fishes; banned the use of solid gears that destroy corals during trawling; set of rules for the use of set nets (net length, height and width, mesh size, cannot close the channels, etc.); limited licences for the use of set nets during spawning aggregations. No. 31/1999 Banned commercial fishing in 24 tourist diving points near Cienfuegos Bay. All six studied species as well as other species No. 83/1999 Limited the fishery of lane snapper during spawning migrations, from April 22 to June 4: only nine set nets are licensed, located in specific sites. Established the obligatory use of bycatch reduction devices attached to set nets, to avoid the capture of lane snapper less than 18 cm FL The capture of fishes could only be done inside this selection device, not inside the set nets. The possession of any fishing trawls on board of any fishing boat was banned during this period. No. 45/2000, 165/2001, Similar regulation to No. 83/1999 was repeated each year to control the fishery of lane 141/2002, 60/2003 snapper during spawning migrations in the Gulf of Batabanó. For each year a limited period of fishing and limited number of set nets (fluctuating from 4 to 9) was established, according to fish population assessments. 58/2004 Total prohibition on all kinds of set nets over the whole Cuban shelf during the period from April 1, to August 31 (spawning season of most snappers). 96/2004 Banned all kinds of fishing in a polygon of about 160 km 2 close to the spawning aggregation site of lane snapper in the eastern part of the Gulf of Batabano, during the following 10 days periods: April 28 to May 7, May 28 to June 6 and from June 26 to July 5 (from waxing crescent quarter to full moon each month). Outside the polygon the fishery was permitted with trawls, traps and seine nets, for a limited number of boats. Similar regulations were repeated for 2005 and 2006, and it was announced that this regulation would be permanent. 354/2001 A total prohibition on any kind of competition event using spear-guns. Limits the authorization of recreational spear-gun fishing to Saturdays, Sundays and National Holidays, except in July August (peak months of vacations). This kind of fishing is allowed only in authorized areas and quantities defined in the resolution 519/96 (above). Since 2002 the total number of recreational licences was limited to 3500 for the whole country. The price of annual licences was doubled. Lane snapper spawning aggregations in southwest Cuba. All snappers and other spawning aggregations Lane snapper in the Gulf of Batabano Mutton, cubera, dog and grey snappers, Nassau grouper, and many other medium and large species. No. 459/96 Marine Reserve Caleta de Avalo. Mutton snapper, cubera snapper, Nassau No. 560/96 Marine Reserve Pta. Francés, grouper and some other species No. 215/98 Marine Reserve Cabo Cruz. Coral reef Barrier No. 167/01 Marine Reserve Cayo La Leña Jaimanita, Península Guanahacabibes 247/2003 Marine Reserve Norte de Matanzas These MPAs include spawning aggregation sites or migration routes for several species. At least nine other spawning aggregation sites are included in the new MPA proposal (submitted to the goverment and pending approval) partly due to the closure of the fishery in this region (Claro et al., 2001). At the south-central part of the Cuban Archipelago, important catches were also obtained from spawning aggregations at Puntalón de Cayo Guano and Banco de Jagua (east of the Gulf of Batabano) (Fig. 1). The marked seasonality of Nassau grouper catches, mainly from December to February the peak reproductive months was clearly shown in the monthly landings data (Fig. 3B). More than 50% of the total annual catch was taken during this three-month period. Traditionally, spawning aggregations of this species were subjected to an intense fishery in Cuba, carried out by baited traps set at m at the shelf break. Due to declining fish yields over time and the resulting reduction in profitability of fishing on aggregations, fishing effort on the spawning aggregations declined. The peak catches noted after 1980 occurred mainly during spawning migrations when the vulnerability of fishes to fishing gears such as set nets was high. Nevertheless, there persisted an important recreational fishery, using both hook and line and spear-gun, on the spawning aggregation sites in the northern Cuban Archipelago (Fig. 1). The size of this fishery is unknown due to lack of statistical information and divers have not surveyed spawning aggregation sites to assess the numbers of fish assembling to spawn. The main aggregation sites in southern Cuba (Puntalón de C. Guano and Banco de Jagua) are no longer regularly fished due to the difficult accessibility of these sites. Overall, relatively few viable spawning aggregations are thought to persist in Cuba today L. analis (mutton snapper) Traditionally, the mutton snapper, taken by trawls, traps, hand and bottom lines, was one of the top fishery target species in Cuba, and was subjected to a high level of fishing effort by both commercial and recreational fishers. In spite of intense fishing effort on this species, catches were maintained at between 900 and 1000 tonnes annually until the 1990s (Fig. 4A). The main fishing area was the Archipelago Sabana-Camagüey, which yielded approximately 50% of the national annual catch until Later, the catches in this area declined gradually, apparently the result of excessive fishing effort. However, in other shelf areas, catches remained relatively stable until the early 1990s (Claro et al., 2001) when a drastic reduction in

7 12 R. Claro et al. / Fisheries Research 99 (2009) 7 16 Fig. 4. Annual catches of mutton snapper, Lutjanus analis, in Cuba (A) and average monthly catches by five-year periods (B). Fig. 5. Annual catches of lane snapper, Lutjanus synagris, in Cuba (A) and average monthly catches by five-year periods (B). landings occurred in all regions. Several factors likely contributed to this overall trend: a sharp reduction in commercial fishing effort occurred due to a national economic crisis that resulted in shortages of fuel, materials and spare parts for boats and fishing gears. In addition, an intense subsistence fishery developed, mainly in the Archipelago Sabana-Camagüey. Although this fishery affected almost all demersal and shore-pelagic species the mutton snapper reportedly received greater fishing pressure due to high demand for the species. The highest catches of mutton snapper were obtained during the reproductive period, which extended from April to August, and at spawning aggregations; between May and June 35 40% of the national annual catch was taken (Fig. 4B). During this period the highest proportion of adult fish was captured, with juveniles (<45 cm FL) prevailing in catches during other months of the year (Pozo, 1979; Claro, 1981a; Claro et al., 2001; Claro and Lindeman, 2008). Aggregations were fished with hook and line at the shelf break, but also with set nets and trawling during spawning migrations. Since 2004 a new regulation banned the use of set nets over the entire Cuban shelf (Table 1). Recreational fishermen also fished directly on spawning aggregations but there are no data on the intensity of this fishery. In most years, a moderate increment in catches was observed in October, known by fishermen as arribazones (fish shoals); these differ from spawning aggregations, because the fish are not mature, and seem to be associated with feeding migrations (Claro, 1981a) L. synagris (lane snapper) Lane snapper was the most important fishery species in Cuba and has been severely over-fished. Catches grew quickly in the 1960s due to the widespread introduction of bottom trawls and the large numbers of traps, and because of the intense exploitation of groups of fish during their migration towards spawning aggregation areas at the shelf break. From 1960 to 1969, lane snapper was fished mainly using trawl nets, but, starting in 1968, large set nets were introduced. Being highly efficient and productive, this gear blocked the migration of lane snapper schools moving towards the edge of the platform. Other measures also led to higher fishing pressure on this species after 1965, including reception of the catch in fishing areas by large transporter ships. Due to the combined use of trawls and set nets, catches surpassed 4200 tonnes in 1969 and stayed at more than 3000 tonnes up until 1977 (Fig. 5A), when catastrophic over-fishing of the species was identified (Claro et al., 2001). The main catches of lane snapper were obtained in the Gulf of Batabano, where from 1969 to 1975 more than 60% of the annual lane snapper catch was taken (Claro et al., 2001). The most spectacular reproductive aggregations known in Cuba were found in the eastern region of the Gulf of Batabano. These groupings were observed only in shallow waters in the north-central half of the Gulf and increased in number of fish as they advanced towards the shelf break at the Gulf of Cazones. In shallow waters, close to the shelf break, the fish schools remained during the day, and at dusk they

8 R. Claro et al. / Fisheries Research 99 (2009) moved towards deeper waters, where mating and spawning of one portion of the school took place. Immediately after spawning, fish returned to nearby shallow waters where they remained until the following day, repeating the process over 4 5 days (García Cagide et al., 2001; Claro and Lindeman, 2008). The temporary nature of lane snapper schools at the spawning site may be an adaptation to escape predators such as sharks, great barracuda, and groupers at the shelf break (Claro, 1982). Lane snapper spawning aggregations were also intensively fished in the Archipelago Sabana-Camagüey and Archipelago Jardines de la Reina (Fig. 1). In all known cases, the schools were fished in shallow waters mainly with trawl nets. In the Archipelago Sabana-Camagüey, catches were highly variable, probably the result of intensive fishing effort. Approximately 60 70% of the annual catch of lane snapper was obtained during days of fishing during the month of peak reproductive activity, generally coinciding with the period preceding full moon. The reproductive peak usually occurred in May in the Gulf of Batabano and the northwest shelf, and in June in the south and northeast zones of the Cuban platform (Claro and Lindeman, 2003). The concentration of fishing effort on the spawning aggregations was likely a major factor in the dramatic collapse of the lane snapper fishery in the Gulf of Batabanó during the 1970s (Fig. 5B). A less marked decline was noted in northeast and southeast areas of Cuba (Claro et al., 2001). Various protective measures were introduced to halt the declines in this species but were not successful. After 1978, lane snapper fishing in the Gulf of Batabano was banned during the reproductive period (three months), and for the remaining (nonspawning) months an annual limited quota was introduced. From 1987, a permanent closure was established in shallow waters adjacent to the spawning site where the schools generally concentrated when not spawning. These protective measures were extended for more than 15 years without evident recovery. After 1995, limited recovery was observed in the Gulf of Batabanó and fishing of the spawning aggregations was authorized for a limited number of boats and set nets; this may explain the increase in catches in the period Over the next three years further reductions in catches occurred and a regulation prohibiting the deployment of set nets over the entire Cuban platform was introduced in L. cyanopterus + L. griseus (cubera snapper + grey snapper) Since fishery statistics in Cuba do not reliably distinguish between captures of cubera and grey snapper, we combined the landings data of these two species for analysis. Their fishery grew quickly after 1960, peaking in the late 1970s, with highest fishing effort directed principally towards the grey snapper (Fig. 6A). After 1982, a marked reduction of this resource took place while fishing effort remained constant. After 1990, social and economic factors resulted in large shifts up and down in fishing effort and some recovery for the species may have occurred after The two snappers are similar in morphology and their spawning aggregations occurred over the same general time period; most catches came from spawning aggregations. Cubera snappers were taken predominantly from its spawning aggregations with hook and line, while grey snappers were taken mainly (85 90%) by trawls, set nets and traps during spawning migrations in shallow waters (Claro, 1983b). The landings of both species showed marked seasonal trends with very high catches during the two-month reproductive period when they aggregated to spawn (July August; Fig. 6B). Catches for these species also increased in October, probably associated with feeding migrations of non-reproductive fish (Claro, 1983b). Although both species reproduced at similar places and months of the year, they exhibited different reproductive strategies. Cubera Fig. 6. Annual catches of cubera and grey snappers, Lutjanus griseus, and L. cyanopterus, in Cuba (A) and average monthly catches by five-year periods (B). snapper spawned during and after the full moon (Claro and Lindeman, 2003), while grey snapper spawned just prior to the new moon (Domeier et al., 1996). Aggregated grey snapper were captured mainly in the channels and straits between the islands that skirt the Cuban platform close to the shelf break. Most fishes captured had ripe gonads, as determined by high gonado-somatic index (a measure that examines gonad weight relative to body weight; gonads increase in size in the spawning season) and the presence of hydrated oocytes (the oocyte stage that occurs very shortly before egg release at spawning) (Claro, 1983a), and their densities in areas close to the shelf edge increased sharply during these months. Aggregations of the grey snapper remained in shallow waters during the day, moved towards the adjacent shelf break in the evening to spawn, and returned immediately after spawning to nearby reefs and seagrass beds. This process repeated itself for individual fish 4 5 times during 8 10 days in one lunar phase and, in the following month other individuals underwent similar cycles (Claro, 1983a; Claro and Lindeman, 2008). Large aggregations are not known for grey snapper which probably forms smaller groups for spawning. Large groups of cubera snapper are also captured during their spawning migrations in the straits among the keys, close to spawning sites. Contrary to the grey snapper, however, cubera snapper remained at the shelf break for several days, where its aggregations are seen together with those of L. jocu, dog snapper (García Cagide et al., 2001; Heyman et al., 2001, 2005; Claro and

9 14 R. Claro et al. / Fisheries Research 99 (2009) 7 16 la Reina; Fig. 1) contributed 35 40% of the national catch of yellowtail snapper, and the Gulf of Batabano 25 35% of the national catch. Other catches came from shelf areas of northern Cuba. Insufficient information precludes a more detailed analysis of the changes in catch volumes and patterns observed over time for this species. The reproductive period of yellowtail snapper in Cuba extended from March to October and spawning aggregations were less well defined, either spatially or temporally, compared to the other species included in the present study. The spawning peak in the Gulf of Batabano was observed during May and June, while in the northwest region of Cuba it occurred in April and May (Claro, 1983c). Although specific spawning aggregation sites were not recorded, there were clear increases in density of yellowtail snapper at multiple locations of the reef close to the edge of the platform during the respective reproductive periods, compared to non-reproductive periods, and most landings were greatest when fish were ripe (Fig. 7B). During the reproductive season, most individuals had swollen abdomens, many had hydrated oocytes, and there was an increase in the gonado-somatic index (Claro, 1983c). 4. Discussion Fig. 7. Annual catches of yellowtail snapper, Ocyurus chrysurus, in Cuba (A) and average monthly catches by five-year periods (B). Lindeman, 2003). In these places, the species is fished intensively with hook and line by commercial fishermen O. chrysurus (yellowtail snapper) Up until annual catches of yellowtail snapper catch did not exceed 500 tonnes but subsequently catches increased as fishing pressure grew. Initially a large proportion of fish taken were big specimens because most fishing was carried out with hook and line at the shelf break, where big fish were more abundant. With the introduction of bottom trawls (in shallow waters) and the increase in trap number in the early 1960s, catches increased notably (Fig. 7A) with small size fish prevailing (Claro, 1983d; Carrillo de Albornoz and Ramiro, 1988; Claro et al., 2004). The use of these large fishing gears resulted in the abandonment of hook and line fishing and was probably a major factor in the decline in size of yellowtail taken in catches. After 1969, the fishery underwent substantial changes, apparently due to the adoption of management actions that indirectly affected the yellowtail fishery. Although these actions were not specifically directed towards the yellowtail snapper, its target species, such as lane, mutton and grey snappers, partly share the same habitat. After 1987 yellowtail snapper catches declined, partly because of high mortality of juveniles taken in trawl fisheries for this species (Bustamante et al., 1982; Claro et al., 2004). The south-central area of Cuba (Archipelago Jardines de The fishery database of Cuba is unique among coral reef fisheries, both in terms of the long-term nature of the dataset as well as in its relative reliability and monthly detail for several key commercially important species. As such, it is valuable for evaluating details of landings trends, hypothesizing on the major causes of changes observed over time, and for developing options for management. The data clearly show that, over the last 4 5 decades, there were marked and often striking changes in the fishery of several important commercial fish species over the coastal platform of Cuba, with overall trends differing between species according to their biology and fishery vulnerability. While it is not possible to establish cause and effect for each study species, some clear trends from the data, and through comparisons between species, emerged that allow for an in-depth, albeit qualitative, evaluation of Cuba s fisheries. The following discussion considers a range of factors in relation to the trends in the six study fish species, inclusive of fishing effort, management interventions and economic shifts, environmental and biological factors, and draws several key conclusions of fishery significance. In all studied species there were clear signs of over-fishing, especially among those that aggregate to spawn with high predictability, despite a range of management interventions since the 1980s to combat over-fishing. While some of the management measures appear to have resulted in positive outcomes for the fishery in the short-term, enforcement was evidently variable in effectiveness and the fishery overall declined. As a result, there was a steady increase in the number and variety of management measures introduced and considered to address the problem of over-fishing over several decades. Two factors were strongly implicated as contributors to over-fishing; excessive and largely uncontrolled fishing effort in terms of both number of vessels and scale and types of fishing gears, and intense fishing focused on spawning aggregations and accounting for a large proportion of annual catches for all species. The study species are the only ones in the fishery exploited at, or close to, spawning aggregations, although mullets, which also have declined markedly, are taken during spawning aggregation and migrations in some areas. In addition, environmental changes may have contributed to the trends noted in these reef fish fisheries. For example, the degradation of coral reefs as result of coral bleaching and algal overgrowth during several ENSO events, may have negatively affected aspects of the life cycle of these reefassociated species (Alcolado, 2004; Claro et al., 2006). In the case

10 R. Claro et al. / Fisheries Research 99 (2009) of the mullets, fished largely in estuaries and coastal lagoons, river modifications may also have affected their abundance. The differences in responses to similar overall fishing pressures experienced by the six study species, which vary biologically in several respects, allow for interesting comparisons. Of all study species, the Nassau grouper and lane snapper exhibited the most marked declines, almost certainly related to the heavy concentration of fishing effort on their spawning aggregations and lack of effective species-specific regulations. Both fisheries were subjected to heavy subsistence use in addition to the commercial fishery. For Nassau grouper, there was an almost complete absence of speciesspecific protective management, with the exception of a minimum legal size that is too small for the species (32 cm TL). Moreover, relative to other study species the Nassau grouper has the shortest reproductive season, is highly vulnerable to traps and hook and line, and there are few spawning sites (Claro and Lindeman, 2003). In addition, this species is long-lived with late maturation, making it particularly vulnerable to over-fishing and in need of appropriate management action (Claro et al., 1990; Sadovy and Eklund, 1999; Sala et al., 2001; Sadovy de Mitcheson et al., 2008). For the lane snapper, its collapse in the Gulf of Babatano in the 1970s was likely the result of several non-sustainable fishing actions: intensive fishing throughout the year and high fishing effort with highly effective fishing gear (set nets and bottom trawls) during spawning migrations. Given the various management interventions introduced in the 1980s for this important commercial species, its relatively short life cycle, fast growth rate and early maturation (Claro, 1981b, 1982; Claro and Lindeman, 2008) some recovery was expected. While a slow increase in catches over 15 years was noted, and increasingly strict fishing regulations introduced (limited fishing effort, a quota and a minimum legal size), reintroduction of intense fishing activity during the spawning season was probably the major factor that again reduced the population. Although fishing regulations were enforced, they may not have provided sufficient protection; for example, in some years catches were permitted during spawning seasons or quotas were too high. Over the last decade, lane snapper stocks continued to decline despite additional regulations (Table 1). Habitat degradation may also have influenced this species through hyper-salinization of inner lagoons, damage to Thalassia beds from hurricanes, and changes in water circulation in coastal areas (Claro and Lindeman, 2008). Although mutton snapper catches exhibited clear declines, these were less marked than for the Nassau grouper and lane snapper. The mutton snapper was not found in large concentrated aggregations but rather in gatherings close to the shelf break over a short period of time. It is noteworthy that fishing on spawning aggregations was not as intense for the mutton snapper as for the Nassau grouper and lane snapper largely due to differences in reproductive behaviour. Mutton snapper did not congregate in shallow waters and were only fished by hook and line, which does not have the same negative impact as trawls or set nets. Another factor that might influence the maintenance of high landings in the mutton snapper is the relatively high number of spawning sites compared to other species studied (Fig. 1). Moreover, the existence of extensive seagrass beds (feeding areas), close to the reefs and mangroves (refuge areas) creates favourable conditions for the persistence of an abundant population for mutton snapper in Cuba (Claro and Lindeman, 2008). Grey snapper have similar reproductive behaviour to the lane snapper, are intermediate in their biological characteristics between the lane and mutton snappers and exhibited declines in landings. They have a longer life span and later sexual maturation than lane snapper, and the converse compared to the mutton snapper (Claro, 1981a, 1983b). Management measures affecting the grey snapper have largely been driven by changes occurring in the economically more valuable lane snapper stocks. However, due to the absence of large and highly concentrated spawning aggregations, grey snappers are less vulnerable to intense fishing during their spawning season. This species is in need of protective regulations, especially during the reproductive season. Reproductive behaviours and other biological attributes of cubera snapper resemble those of the mutton snapper, but their natural population levels are relatively smaller, possibly due to more specialized habitat requirements (Starck, 1970; Lindeman and DeMaria, 2005). For the cubera snapper, there is little focused fishing effort other than during short periods when spawning migrations form and at the spawning sites, and the species is not as intensively fished as other snappers. Protective measures clearly are needed, however, particularly on spawning aggregations. Of all the species studied yellowtail snapper forms the least concentrated and predictable spawning aggregations but nonetheless has undergone declines in catches. The species is intensively fished during the spawning season and no protective measures were established except for a minimum legal size that is arguably too small (Claro et al., 2004). The yellowtail snapper is fished together with lane and grey snappers, all them coincident in time and space during their respective spawning periods. Yellowtail snapper, however, seem to be less vulnerable to fishing because their aggregations are not highly concentrated, which may explain the less pronounced decline in catches over the last few decades in comparison with other snappers. On the other hand, the fishery mainly extracts small size adults since larger adults prefer deeper waters, where trawling is not possible. This means that an important part of the population may continue to spawn in less accessible deeper waters. Another negative impact on yellowtail snapper is the high proportion of juvenile fishes taken by trawls and traps. For example, in the Archipelago Sabana-Camagüey 85.8% of all yellowtail snapper in trawl catches, and 40.5% taken in traps, are juveniles (Claro et al., 2004). There is evidence that other, anthropogenically driven environmental factors may have contributed to declines in snapper and Nassau grouper populations in Cuba. These include reduction of seagrass areas in some regions, such as the inner waters of the Archipelago Sabana-Camagüey (Alcolado et al., 1999), increases in coral bleaching and diseases associated with increases in water temperatures during ENSO events (Claro et al., 2006). Other factors may include damage to coastal marine habitats from various causes, such as pollution and other kinds of habitat degradation that have increased in recent years (Martínez, Montalvo, Miravet, Lugioyo, Loza and Pérez, unpublished report 2004; Claro, 2007). Considering all six study species, the greatest overall depletions occurred in those species that are most intensively exploited during their spawning aggregations. In this respect is noteworthy that marked declines have also been observed in mullet species, which are often targeted on or moving to spawning aggregations. This is in contrast to other groups of fishes such as jacks, mojarras and grunts that are not knowingly targeted in association with aggregations. In the Nassau grouper and lane snapper, spawning aggregations appear to be particularly distinctive with animals predictably concentrated in large numbers and readily accessible to fishermen in well-known months. Even though the mutton snapper is also a highly aggregative species and is heavily exploited, the use of selective and small-scale fishing gears at the spawning sites and the large number of spawning sites relative to Nassau grouper and lane snapper, appear to allow for persistence of the fishery even under high fishing pressure. Likewise, species such as the grey and yellowtail snappers seem to be less affected by heavy exploitation during the spawning season, although there are clear signs of stock declines in both species. The overall resilience, or response, of different species to fishing ultimately depends on the intensity and nature of fishing activity, vulnerability to fishing and other biological features, such as

11 16 R. Claro et al. / Fisheries Research 99 (2009) 7 16 reproductive behaviour, longevity, and maturation size, as well as environmental factors and management effectiveness (Ault et al., 1998). Although the development of a sustainable fishery needs to take such factors into account, it is clear from a comparison across the six species that one measure likely to benefit all species would be the successful implementation of species-specific conservation management. For some species this needs to focus on spawning times and/or sites during the spawning season. The Ministry of the Fisheries Industry is working towards the total elimination of all kinds of bottom trawls on the Cuban shelf. 5. Conclusion The long-term species-specific database and related management and social information available in Cuba provide a rare and extremely valuable opportunity for understanding fishing history and for identifying and evaluating management options. Management is so reactive in many countries that data from past management interventions are often never gathered, much less analysed, and, remarkably, the possible effects on the fishery often not considered. Many problems with scientific prediction as well as problems among agency fisher relations arise because of the absence of follow-up analyses of how management interventions impact various processes over time. In many countries, even if fishery data are collected and available for analysis they often involve lumping of species or give no, or little, indication of effort or social changes that could have affected landings. The Cuban dataset provides an important lesson on the value of detailed species-specific information and illustrates clearly the importance of sustained management and precautionary approaches. It also demonstrates how the biology of exploited species, particularly species that exhibit differences in their spawning behaviour in relation to their vulnerability to exploitation, can influence their responses to fishing practices. Acknowledgements We are most grateful to the many fishers who assisted us. From the Ministry of the Fisheries Industry of Cuba, we thank the Provincial Fisheries Associations, the Directorate of Coastal Fisheries and Servando Valle (Centre of Fisheries Research). Funding for this work was provided by the Society for the Conservation of Reef Fish Aggregations, which is partly supported by the Packard Foundation. Additional funding was provided by a Doherty Fellowship at the Department of Marine and Environmental Systems, FIT. References Alcolado, P.M., García, E.E., Espinosa, N. (Eds.), Protecting biodiversity and establishing sustainable development in the Sabana-Camagüey Ecosystem. 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