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© Daniel Cryan 2015 The Galapagos Sailfin Grouper: A Case Study in the Importance of Reproductive Biology in Fisheries Management Daniel Cryan Bill Durham Darwin, Evolution, and Galapagos 10/9/15 Cryan 2 Introduction The Galapagos Archipelago is world renowned for its unique collection of endemic coastal and terrestrial life. Here, one can find iconic species such as the Galapagos giant tortoise, the marine iguana, the flightless cormorant, and of course Darwin’s finches. Many visitors to the islands are unaware, however, that the waters surrounding the Islands are also home to their own diverse and fascinating collection of marine life. Here, a confluence of major currents unites species from the cool southern provinces of Chile and Argentina, with warm-water species from the west coast of Central America, as well as with tropical species from the Indo-Pacific. These waters are also home to an impressive number of endemic marine fishes, including the distinctive Galapagos sailfin grouper, or as it is locally known, the bacalao (Constant, 1992). The Galapagos sailfin grouper is an apex predator in the rocky reef ecosystems of the Galapagos Marine Reserve, and has supported a significant fishery in the islands since the early 1920’s. In recent years, however, fishermen have reported smaller and smaller catches of bacalao, in terms of both size and overall abundance. In this paper I postulate that the declines in the grouper population are largely the result of detrimental fishing practices that fail to account for (or even exploit) the unique reproductive biology of the sailfin grouper. I begin with a discussion of protogynous hermaphroditism in groupers, its role in reproduction, and the fisheries implications of targeting large males. I then examine the longevity and slow-maturation of the Galapagos grouper, and the potential consequence of targeting immature fish. Lastly, I discuss the role of spawning aggregations in grouper reproduction, and the importance of protecting key spawning sites from fisheries exploitation. Finally, I make a series of recommendations, based on my three hypotheses, on what conservation measures should be implemented to ensure the future of the Galapagos sailfin grouper. Cryan 3 Biological and Socioeconomic Background The bacalao or Mycteroperca olfax is a member of the subfamily Epinephelinae, a diverse group of fishes found worldwide, known colloquially as “groupers.” Taxonomists have recently reevaluated the phylogenetic lineage of this group of fishes, placing groupers alongside soapfishes and fairy basslets in the larger family Epinephelidae, separating them from the closely related anthias and sea basses, which now form their own family Serranidae. There are 16 genera and 163 species of groupers found worldwide, with 10 species and 6 genera found in the Galapagos Marine Reserve (Craig, 2007). Of these 10, the bacalao is the largest and most ecologically important grouper found in the Islands, growing to over 120 cm (4 ft.) long. Like most groupers, the Galapagos grouper has a large robust body with a wide truncate caudal fin. Its head and mouth are both large, and it is a fairly slow, deliberate swimmer. The sailfin grouper gets its name from its distinct dorsal fin, in which the second and third spines are elongated, giving it a signature sail-like curve. Most individuals are grayish brown to olive green in color, and often have light spotting and vertical markings along their sides, (though a small portion of the population, known locally as the bacalao rey or “king grouper,” are a bright yellowish gold color over their entire bodies) (Deloach, 2003). In most places, groupers are among the top predators in their ecosystem, and the Galapagos is no exception. Like its relatives worldwide, the Galapagos grouper feeds on a variety of crustaceans and small reef fish, and is only susceptible (as an adult) to species such as sharks or larger groupers. One study found that sailfin grouper fed mainly on the pacific creolefish (Paranthius coronus), another smaller grouper found throughout the islands. Like other large groupers, the bacalao is an ambush predator, spending most of its time cruising near the bottom, hiding near the mouths of caves and under ledges, waiting to strike out at Cryan 4 unsuspecting fish. Juveniles are often found in shallow mangrove forests and sandy lagoons, while adults tend to live in deeper waters around rocky reefs, drop offs, underwater lava ridges, and other vertical structures (Grove, 1997). Unlike many other groupers worldwide, who have grown wary of humans due to overfishing, the Galapagos grouper is still fairly gregarious (a trait common in species throughout the islands) and will sometimes approach divers or snorkelers with curiosity (Craig, 2011). An adult Galapagos grouper comes out from an underwater cave. © Daniel Cryan 2015 In the 1920’s, the first commercial fishery for Galapagos grouper began in the Archipelago. It was established by a group of Norwegian settlers who caught, dried, and salted the fish, so that they could be exported to mainland Ecuador. Many fish were used as the main ingredient in the traditional Ecuadorian dish Fanesca, a popular Easter stew. (Although this fact may seem trivial or irrelevant now, it will prove important later on when discussing the decline of the bacalao). This fishery not only marked the beginning of the exploitation of bacalao, it also heralded the beginning of the finfish fishery as a whole in the Galapagos (Lacquet, 2007). Over the next several years, more and more fishermen traveled to the relatively untouched waters of the islands to tap into the seemingly endless supply of fish. This growth coincided with the globalization of the Islands as a whole. Over the second half of the 20th Century, the number of tourists and residents in the islands increased exponentially, placing heightened pressures on the Cryan 5 Islands’ marine life. During the 1990’s, at the peak of the sea cucumber fishery, there was a record high of nearly 1200 registered Galapagos fishermen (Castrejón, 2013). Though bacalao is best known for its use in Fanesca, it is also delicious baked with a side of limes. © Daniel Cryan 2015 During this period of unprecedented growth, however, fishermen and researchers began to notice a change in the composition and size of the fishermen’s catch. In a reconstruction of the total catch from 1950 to 2010, Schiller et al. found that the composition of the catch had changed significantly over time. Serranids (the family containing the bacalao, as well as other groupers and sea basses) had once comprised more than two thirds of the total catch, but now they only accounted for about a quarter of the total, and had been replaced by species such as tunas and mullets (Schiller, 2013). Another study from Burbano et al. looked at the reported “best day’s catch” of Galapagos grouper amongst different age groups of fishermen. They found that older Cryan 6 fishermen used to catch significantly more Galapagos grouper than the younger generations, and that the fish caught a few decades ago were also larger (Burbano, 2014). These studies, along with the general absence of bacalao in fishermen’s catches nowadays, indicate that this species has experienced some level of decline over the past few decades. Determining the precise cause of this decline will be crucial for reversing this trend and ensuring the long term viability of this species. Reconstructed Galapagos fish catch from 1950 to 2010. © Schiller 2013. My Hypotheses When postulating reasons for the decline of a given species of food fish, it’s often dangerous to oversimplify the situation and assume that fishermen are simply catching too many fish. This fails to account for the nuances of the situation, and will inevitably lead to ineffective Cryan 7 or impractical conservation measures. A more practical approach is to examine the life history of a given species, and evaluate how fishing effort may influence a species’ ability to survive and reproduce. In the case of the Galapagos grouper, I propose that the majority of the decline over the past few decades can be directly attributed to fishing practices that work against the grouper’s unique reproductive biology. Specifically, fisherman have traditionally harvested large males, creating a skewed sex ratio. Nowadays, they target juveniles, before they have the ability to reproduce. And lastly, they often target grouper spawning aggregations, which once again threatens the population’s long-term viability. It is common practice for fishermen to target the largest fish possible. Larger fish equate to higher profits at market, and so it is in the best interest of a fishermen to catch the largest fish possible. As a result, in places where overfishing occurs, it is usually the largest fish that are the first to go, as long term survival becomes increasingly difficult. The Galapagos grouper is no exception to this rule. Fishermen are now catching increasingly smaller fish, as large individuals become extremely rare (Burbano, 2014). For many species this is just an unfortunate result of overfishing, and not a problem in and of itself, but for the Galapagos grouper, this lack of large individuals is especially problematic. This is because the bacalao, like many other groupers, is a protogynous hermaphrodite. A protogynous hermaphrodite is an organism that begins its life as a female, but later in life transitions to male, once it has reached a certain size (Bhandari, 2006). The evolutionary advantage of such an adaptation is that large healthy males are favored by natural selection and that there is a low likelihood of closely related species interbreeding, because at any given life stage they are all the same gender (Ghiselin, 1969). In 1993, Coello and Grimm conducted a study of the life history of Galapagos grouper, by examining the age, size, and sex of fish caught by Galapagos fishermen. They found a highly Cryan 8 skewed sex ratio of 48 females for every 1 male in the local population. Due to the nature of protogynous hermaphroditism, it’s not uncommon to see skewed sex ratios in the wild, even amongst healthy populations. Yet this ratio was still higher than those seen in any other related species of groupers (Coello, 1993). And in 2015, a study by Usseglio et al. found that the ratio was now even higher, reaching 67 females for every 1 male. The same study found that it took over 15 years for half of all groupers to become male, and that the average size of sex change was 83.7 cm. With so few large males in the population, it becomes increasingly difficult for the sailfin grouper to spawn successfully. This is problematic because without reproduction the population cannot replenish itself, and will continue to dwindle until no fish remain. Protecting large males will be essential in the conservation of the Galapagos grouper (Usseglio, 2015). Sex Distribution of Galapagos Grouper. © Usseglio et al. 2015 Cryan 9 Ironically, the historic targeting of large males leads directly to the next major problem facing the Galapagos grouper, which is the targeting of immature juveniles. When fishermen no longer have large fish to catch (because these fish are very rare) their only option is to either target other species (which can be seen in the expansion of the Galapagos fishery towards species like tuna and mullets) or to target smaller individuals (Schiller, 2013). This can prove problematic if fishermen begin to target immature juveniles, who are not yet able to reproduce. And unfortunately for the bacalao, thanks to their unique reproductive biology, this is exactly what has begun to occur. Size Distribution of Galapagos Grouper. © Usseglio et al. 2015 Cryan 10 In their 2015 study, Usseglio et al. examined grouper growth rates and age of maturation by correlating total body length, gonad development, and otolith ring formation. An otolith, commonly known as a “fish ear bone,” is a calcium carbonate structure located in the heads of bony fish. Every year another ring of carbonate is deposited, providing an accurate metric for a wild fish’s age. The researchers found that, like many other large groupers, the bacalao grew relatively slowly and had a high longevity. In addition, they found that the average age of maturation for the groupers was 7.8 years old, with an average size of 61.1 cm. This meant that, of all the fish caught by the fishermen, 73% were juveniles, and only 27% were mature. This high abundance of juveniles is an especially alarming result, considering these individuals are not yet able to reproduce and propagate the species. Ensuring that juvenile sailfin grouper are able to mature and reproduce, before they are subject to fisheries pressure, should be a top priority for conservation of this species (Usseglio, 2015). Finally, as if the situation weren’t hard enough for the Galapagos grouper, evidence suggests that fishermen are targeting them in the very act of reproduction. And once again, it is the sailfin grouper’s unique reproductive biology that makes it so vulnerable. Large groupers typically reproduce in what are known as “spawning aggregations.” During one of these aggregations, several mature fish meet up at select locations in groups that can range from 20-30 to tens of thousands, depending on the species. Researchers believe that changes in the lunar cycle trigger these migrations to the spawning locations, as spawning always occurs on roughly the same day in the lunar cycle each year. During the late afternoon and early evening, the mature fish will all swim together and release their gametes in one spectacular mass-fertilization. (Sala, 2001). It was unknown for many years whether or not the bacalao engages in spawning aggregations, simply because little research had been done on the species, however, in 2015 Cryan 11 Salinas-de-León et al. observed the first sailfin grouper spawning aggregations off Darwin and Wolf Islands, confirming that this behavior does in fact exist in this species (Salinas‐de‐León, 2015). This is worrying, considering that elsewhere in the world fishermen often target spawning aggregations, due to the relatively high abundance of fish found there. And because they target fish in the very act of reproduction, many large adults are removed from the population, preventing any future breeding, and endangering the future of the species as a whole. In the Caribbean, the Nassau grouper (Epinephalus striatus) has suffered severe regional declines, which are largely the result of fishermen targeting their spawning aggregations. But are fishermen in the Galapagos doing the same? The circumstantial evidence certainly seems to suggest so. The sailfin grouper spawning season occurs from October to March, during a period of high marine productivity in the Galapagos. The fishing season for this species also historically occurred during the same period, though nowadays they are fished year round in an attempt to compensate for the decline. And this period also occurs right before the Christian religious holiday of Easter, during which Fanesca, the traditional dish made from bacalao, is served throughout all of Ecuador. What this suggests, is that fishermen have historically targeted bacalao during this period due to their high spawning abundance which conveniently occurred right before Easter. Additionally, all four spawning sites discovered by Salinas-de-León et al. are within the legal fishing areas of the Galapagos Marine Reserve, so any fishermen who wanted to target these aggregations would be completely within their legal rights to do so. Consequently, protecting these important spawning sites is crucial for ensuring the survival of this species (Salinas‐de‐León, 2015). Cryan 12 Conservation Recommendations Though the situation for the Galapagos grouper may seem dismal (having three major threats to its reproductive viability), the bright side is that identifying these threats allows researchers and policymakers to make specific and concrete recommendations for the protection of this species. Currently, there are no specific regulations in the Galapagos governing the fishery of the bacalao. If we are to protect this species, this must change immediately. The first step is to introduce a temporary maximum size limit of 83.7 cm (the average age of maturation for males). This will ensure that large males are protected, at least until the population has begun to rebound, at which time the maximum limit could be readjusted or removed. The next step would be to implement a minimum size limit of 61.1 cm, to protect juvenile fish that have not yet matured and reproduced. Minimum size limits are standard practice in fisheries management, and so this limit should remain relatively permanent, with room for adjustment, as is necessary. In order to protect grouper in the actual act of spawning, all identified spawning areas should be set aside as no-take zones, and researchers should continue to search for new spawning areas, which should also be protected (Castrejón, 2013). Also, a fishing closure during peak spawning months (October to March) should also be implemented, at least until the population has begun to rebound. Another novel idea to help the grouper population would be to set up a grouper hatchery and aquaculture center in the islands, to help supplement the wild population while it is recovering. Such a venture would also provide employment to local fishermen, and help alleviate the economic losses caused by the new fisheries regulations. Conclusion The Galapagos sailfin grouper is truly a remarkable species. It is a top predator in the local marine ecosystem, a unique endemic species of the Galapagos Archipelago, a popular sight Cryan 13 amongst divers and snorkelers, and perhaps most importantly, a culturally and economically important fish for the islands. This fish holds the unique distinction of supporting the very first fishery in the Galapagos, one that would eventually grow and expand into other fisheries that would change and define the identity of these Islands. In this sense, the Galapagos grouper is important to these Islands, not only practically in terms of its ecosystem importance, but symbolically to the Islands as a whole. And although this species is facing a multifaceted decline, the situation is not hopeless. Now that we have identified the major threats facing this species (fishermen targeting males, targeting juveniles, and targeting spawning aggregations) we can take the steps necessary to protect the grouper. And in general, it is worth remembering, that conservation is not just for the species being conserved, it’s for us too. This is especially true for fish, because if the fish disappears, so does the fishery, and thus the fishermen’s livelihood. So as we move forward let us remember that it is not only the bacalao’s future that is at stake, but ours as a well. A Galapagos grouper adorns this mural outside the Puerto Ayora Fish Market. © Daniel Cryan 2015 Cryan 14 “It is not only the bacalao’s future at stake, but ours as well.” © Daniel Cryan Works Cited Bhandari, Ramji Kumar, Mohammad Ashraful Alam, Kiyoshi Soyano, and Masaru Nakamura. "Induction of female-to-male sex change in the honeycomb grouper (Epinephelus merra) by 11-ketotestosterone treatments." Zoological science 23, no. 1 (2006): 65-69. Burbano, Diana V., Carlos F. Mena, Paulina Guarderas, Luis Vinueza, and Günther Reck. "Shifting Baselines in the Galapagos White Fin Fishery, Using Fisher’s Anecdotes to Reassess Fisheries Management: The Case of the Galapagos Grouper." In The Galapagos Marine Reserve, pp. 227-246. Springer International Publishing, 2014. Castrejón, Mauricio, and Anthony Charles. "Improving fisheries co-management through ecosystem-based spatial management: the Galapagos Marine Reserve." Marine Policy 38 (2013): 235-245. Cryan 15 Craig, Matthew T., Y. J. Sadovy de Mitcheson, and Phillip C. Heemstra. "Groupers of the World." Published by NISC, Grahamstown, South Africa, 402p (2011). Craig, Matthew T., and Philip A. Hastings. "A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini." Ichthyological Research 54, no. 1 (2007): 1-17. Coello, Segundo, and A. S. Grimm. "The reproductive biology of Mycteroperca olfax (Jenyns) (Pisces Serranidae): protoginy and breeding season." Rev. Cien. Mar. Limn 3 (1993): 115-128. Constant, Píerre. "Marine life of the Galapagos." (1992). DeLoach, Ned. Reef fish identification: Galápagos. New World Publications Incorporated, 2003. Ghiselin, Michael T. "The evolution of hermaphroditism among animals." Quarterly Review of Biology (1969): 189-208. Grove, Jack Stein, and Robert J. Lavenberg. The fishes of the Galápagos islands. Stanford University Press, 1997. Lacquet, Jennifer L. “Marine Extraction in Galapagos,” Shifting Baselines (blog), Science Blogs, May 8, 2007, http://scienceblogs.com/shiftingbaselines/2007/05/08/fishing-in-galapagos/. Sala, Enric, Enric Ballesteros, and Richard M. Starr. "Rapid decline of Nassau grouper spawning aggregations in Belize: fishery management and conservation needs." Fisheries 26, no. 10 (2001): 23-30. Salinas‐de‐León, P., E. Rastoin, and D. Acuña‐Marrero. "First record of a spawning aggregation for the tropical eastern Pacific endemic grouper Mycteroperca olfax in the Galapagos Marine Reserve." Journal of fish biology (2015). Cryan 16 Schiller, Laurenne, Juan José Alava, Jack Grove, Günther Reck, and Daniel Pauly. "A reconstruction of fisheries catches for the Galapagos Islands 1950-2010 Schiller et al 2013." (2013). Usseglio, Paolo, Alan M. Friedlander, Edward E. DeMartini, Anna Schuhbauer, and Pelayo Salinas de Léon. Age, growth and reproduction of the Galapagos sailfin grouper Mycteroperca olfax (Jenyns, 1840): an overdue and needed comprehensive baseline. No. e1429. PeerJ PrePrints, 2015.