Variability in the growth patterns of Loxechinus aLbus ...

BULLETIN OF MARINE SCIENCE. 89(3):699–716. 2013 http://dx.doi.org/10.5343/bms.2012.1063

Variability in the growth patterns of Loxechinus albus along a bathymetric gradient associated with a fishing ground Carlos Molinet, Cecilia A Balboa, Carlos A Moreno, Manuel Diaz, Paulina Gebauer, Edwin J Niklitschek, and Nancy Barahona Abstract Here we assess the growth pattern variability of the urchin Lochechinus albus (Molina, 1782) in a fishing ground where it was distributed between 0 and 100 m depth. The bathymetric gradient was divided into four strata, and urchin samples were collected for growth estimations. Images were used to characterize the urchin population along this bathymetric gradient, and historical records for the urchin fishery at this fishing ground were examined. Four algorithms were used to model growth, and the Akaike’s Information Criteria was used to determine the best model fit. Among the four bathymetric strata, both size and age composition, and the growth patterns of L. albus differed significantly. In the shallowest stratum, urchins were smaller and younger than in the deeper strata. Urchins from 5 to 15 m depth displayed greater initial growth rates compared with urchins from 25 to 100 m depth; however, growth decelerated faster at 5–15 m depth than at deeper habitats. Based on results, we hypothesize that the growth pattern of L. albus observed in the shallowest stratum represents a case of age (size) truncation due to fishing, which requires further study.

Since the end of the 1990s, the sea urchin Loxechinus albus (Molina, 1782) has supported the greatest edible sea urchin fishery in the world (Vásquez et al. 1984, Guisado and Castilla 1987, Moreno and Vega 1988, Andrew and O’Neill 2000, Vásquez 2001, Moreno et al. 2006, 2011, Kino and Agatsuma 2007, Pérez et al. 2010). This fishery began in Chile in the 1940s, but steady growth did not occur until the mid-1970s (Moreno et al. 2006). The fishing pressure led to a crisis in 2001, which led to the establishment of a management plan that took effect in 2005 (Moreno et al. 2006). Loxechinus albus is one of the key herbivores of the coastal ecosystems off Chile (Vásquez et al. 1984, Guisado and Castilla 1987, Moreno and Vega 1988, Vásquez 2001, Kino and Agatsuma 2007, Pérez et al. 2010). Its geographic distribution spans the southern cone of South America, from Isla Lobos in Peru (06°55.5´S, 80°42.5´W) in the Pacific to the central zone of Argentina (37°35´S) and the Malvinas/Falkland Islands (51°40´S) in the Atlantic (Schuhbauer et al. 2010). In the fjords and channels of southern Chile, around 90% of the L. albus population inhabits between 0 and 20 m depth (Inostroza et al. 1983, Moreno et al. 2011), even though its bathymetric distribution has been described as from the intertidal down to 340 m depth (Larraín 1975). This extended distribution range reported for L. albus is linked to the species’ capacity to feed on drifting macroalgae (Castilla and Moreno 1982, Contreras and Castilla 1987), which reaches deep habitats via physical transport mechanisms (Vetter and Dayton 1998, 1999). Bulletin of Marine Science

© 2013 Rosenstiel School of Marine & Atmospheric Science of the University of Miami

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It is reasonable to expect differences in individual growth rates for urchins in deeper strata associated with energetic limitations related to lower food availability (Ebert et al. 1999, Wing et al. 2003, Schuhbauer et al. 2010). In addition, but to a lesser extent, changes in temperature, salinity, and dissolved oxygen over a bathymetric gradient also may have metabolic effects on sea urchins (Siikavuopio et al. 2007, 2008, Schuhbauer et al. 2010). Along with the trophic, metabolic, and reproductive factors that determine bathymetric differences in L. albus individual growth patterns, it is reasonable to expect fishing effects as suggested by Schuhbauer et al. (2010). These effects can lead to density-dependent and trophic consequences observed in benthic species (e.g., Orensanz 1986), and compensatory growth as observed in fishes (e.g., Ali et al. 2003). Evolutionary responses induced by the selective pressure of the fishery have been observed in other species, such as Atlantic cod, Gadus morhua, Linnaeus, 1758 (Swain et al. 2007), and white seabream, Diplodus sargus (Valenciennes, 1830) (Pérez-Ruzafa et al. 2006). The fit of growth models in areas where larger individuals have been selectively removed by fishing results in truncated size and age structures, and can cause erroneous estimates and interpretations of growth curves, with management consequences for the fishery (Götz et al. 2008, Hsieh et al. 2010). In addition to the range of factors that may affect the growth patterns of urchins, comparison of these patterns based on available literature is complicated by the diversity of models used to analyze observed growth in different populations and depth strata of interest (Grosjean 2001). Among the three published studies of L. albus growth, Gebauer and Moreno (1995) applied the von Bertalanffy model, Schuhbauer et al. (2010) selected the von Bertalanffy model, and Flores et al. (2010) selected the Tanaka model among three other models. Studies by Gebauer and Moreno (1995; 39°26´01˝S, 73°12´57˝W, intertidal) and Schuhbauer et al. (2010; 52°03´06˝S, 59°44´15˝W, 0–15 m depth) were carried out on urchins from unfished areas, while Flores et al. (2010; between 44°00´S and 44°30´S, 9 yrs were not observed in 5–15 m, where around 90% of the individuals were between 4 and 7 yrs (Fig. 3E). In 25–45 m, a broader range of size classes was observed, with individuals between 2 and 12 yrs old (Fig. 3F), while strata 50–70 and 75–100 m contained mostly size classes between 5 and 14 yrs, with very few individuals 9 yrs of age and >75 mm TD, which contrasts with the size distribution recorded in the 1990s. Furthermore, the variation in CPUE from 1986 to 2011, and the reduced number of fishing trips made to this fishing ground despite its close proximity to Quellón (5 nmi), suggests strong fishing pressure, which is consistent with that reported by Moreno et al. (2011). The most intensive fishing of L. albus to the south of Chiloé (i.e., surrounding the study area) began in the mid-1970s (Moreno et al. 2006). Since 2005, this area has produced 3000 and 4500 t of landings, and smaller average urchin sizes compared with other areas (Molinet et al. 2009, Moreno et al. 2011). It is therefore reasonable to assume that this area of easy access has experienced selective removal of urchins. This selection may have affected the size-age relationship,

molinet et al.: Growth of Loxechinus albus along a bathymetric gradient

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Figure 7. Size composition determined for the fishing ground associated with the urchin study site, obtained from benthic monitoring conducted by the Instituto de Fomento Pesquero (IFOP). White bars, no depth recorded; light gray, 15 ind m−2) within a marine reserve grew much slower than those outside the reserve, suggesting a densitydependent effect. While linear growth is not probable from a biological perspective (von Bertalanffy 1938, Pauly 1981, Schnute 1981), it could be useful for adjusting highly truncated size structure data to the size of maximum individual growth, but explicitly assuming that there is age-size truncation. In light of the available information, a plausible hypothesis is that the model fit to the urchin growth data from 5 to 15 m depth is an extreme case of age (size) truncation due to fishing, which has been reported for other fisheries (Hsieh et al. 2010). The urchin growth patterns reported by Flores et al. (2010) represent moderate age truncation, given that their study area is less accessible to fishers (10–20 hrs transit from Quellón). Finally, the growth pattern of urchins at 25–45 m depth is consistent with observations by Gebauer and Moreno (1995) and Schuhbauer et al. (2010) in areas without fishing, and corresponds to populations without age (size) truncation (i.e., a “natural” growth pattern for L. albus in this study area). Selective removal of larger individuals by fishing has been reported by others, who also describe genetic effects on populations (Swain et al. 2007, Hutchings and Fraser 2008). These effects can result in the persistence of smaller individuals per age class despite good conditions for growth, and can lead to subsequent projections of catch decline (Swain et al. 2007). The evolutionary consequences of such effects can be difficult to reverse (Hsieh et al. 2010). Our results show that the fit of growth models based on information from disturbed populations, either due to fishing or other natural events, have the potential to lead to the erroneous interpretation of results, particularly in spatially structured and commercially exploited populations, where precautionary measure must be taken to avoid detrimental decision making (e.g., Orensanz et al. 2004). An effective measure for mitigating the effects of disturbances, such as fishing, is the implementation of marine reserve areas (e.g., Clark 1996, Behrens and Lafferty 2004, Parnell et al. 2005, Lau et al. 2011). The halting of the selective effects of fishing enables the study of the life history of exploited species under more “natural” conditions. Such populations also allow the testing of the hypotheses regarding age truncation in exploited populations (e.g., Swain et al. 2007, Hsieh et al. 2010).


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Acknowledgments This project was funded by the FONDECYT 1100931 grant. We thank the crew of L/M Jairo and its captain J Cuevas for their support during the sampling campaigns. We thank R Roa-Ureta and A Parma who kindly proposed a number of changes to the manuscript. Finally we thank four anonymous reviewers who helped to improve this work.

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