FISHERIES OCEANOGRAPHY Fish. Oceanogr. 23:5, 436–457, 2014 Modeling the impact of climate variability on Black Sea anchovy recruitment and production CEREN GURASLAN€ *, BETTINA A. FACH INTRODUCTION AND TEMEL OGUZ Institute of Marine Sciences, Middle East Technical University, Many of the largest fisheries today in the world’s Erdemli, 33731, Mersin, Turkey oceans are based on small pelagic fish species such as anchovy and sardine. Anchovies are small saltwater forage fish belonging to the Engraulidae and Anchoa ABSTRACT families. Of those, Anchoveta or the Peruvian The connection of climate variability with anchovy anchovy (Engraulis ringens), the European pilchard spawning and recruitment in the Black Sea in partic- (Sardina pilchardus), the Japanese anchovy (Engraulis ular, and other ecosystems in general, was studied japonicus), and the European anchovy (Engraulis encra- using a two-way coupled lower trophic level and sicolus) are distinctive in the world’s catch and are har- anchovy bioenergetics model. Climate variability was vested for human consumption. The European represented by a 50-yr time series of daily tempera- anchovy supports intense fisheries in the Mediterra- ture and vertical mixing rates with stochastic varia- nean Sea (Plounevez and Champalbert, 2000) and tions. Temperature was found to be the dominant Black Sea (Chashchin, 1996; Daskalov, 2003), where factor influencing early life stages and hence popula- it constitutes the main fisheries resource. tion dynamics of Black Sea anchovy as marked by a Environmental factors are known to influence pop- high correlation of anchovy egg production and ulation dynamics of small pelagic fish species via regu- recruitment success in response to changes in temper- lation of egg survival and hence recruitment success ature. Each decrease of 2°C in summer mean temper- (Lasker, 1975; Crawford et al., 1987; Cury and Roy, atures resulted in a delay in the timing of egg 1989; Bakun, 1996; Schwartzlose et al., 1999; Takah- production of between 12 and 19 days. Water tem- ashi and Watanabe, 2004a,b; Palomera et al., 2007; peratures in the spawning season had a greater influ- Houde, 2008). Such factors may include input of nutri- ence than the number of available spawning females ents into the surface water through mixing, offshore on the intensity of egg production. Anchovy recruit- egg and larval transport, and water column stability ment was similarly influenced by temperature, with (Peterman and Bradford, 1987; Bakun and Parrish, decreased temperatures resulting in a significant delay 1991; Borja et al., 1996; Tsai et al., 1997; Cole and in the onset of peak recruitment during the fall by McGlade, 1998; Painting et al., 1998; Guisande et al., 21–38 days. Also, recruitment numbers in December 2001, 2004; Lloret et al., 2004). Changes in vertical decreased by about 20% with decreasing tempera- mixing rates of the water column have been shown to tures. The impact of temperature on production was explain 70% of the variance in the recruitment index slightly diminished by the impact of vertical mixing. of the Bay of Biscay anchovy (Borja et al., 1996). The strong linkage of climate variability with However, ambient temperature is known to be a criti- anchovy spawning and recruitment has an important cal factor affecting marine fauna, particularly the prediction potential for short-term anchovy stock reproduction biology of clupeid species (Blaxter and estimations, which may serve fisheries management Hunter, 1982; Tsuruta and Hirose, 1989; Imai et al., purposes. 1998; Funamoto et al., 2004). Anchovy is a thermo- philic species known for its higher vulnerability to Key words: anchovy bioenergetics model, anchovy temperature fluctuations as compared with other spe- recruitment, climate impact, stochastic temperature cies sharing the same trophic level such as sardine variability (Lluch-Belda et al., 1991). Cushing (1996), on the other hand, suggests that the variation in recruitment *Correspondence. e-mail: [email protected] numbers is linked to spawner availability and is there- Received 9 June 2013 fore regulated by exploitation of the existing stock. Revised version accepted 4 June 2014 However, as in the case of the Black Sea anchovy, the 436 doi:10.1111/fog.12080 © 2014 John Wiley & Sons Ltd Impact of climate on Black Sea anchovy dynamics 437 intense fishing activity during the 1980s did not lead Sea (Politikos et al., 2011), the Gulf of Lions (Pethy- to a collapse of the anchovy fishery until the alien bridge et al., 2013), the Bay of Biscay (Pecquerie et al., ctenophore (Mnemiopsis leidyi) invaded the whole sys- 2009), the coast off Peru (Xu et al., 2013) and the tem in 1989 (Oguz, 2005). Black Sea (Oguz et al., 2008a). The use of such models Anchovy has undergone significant fluctuations in gives an insight into the life cycle dynamics and shows standing stock size over the past five decades due to that human impact coupled with environmental vari- regional climate variability, intensive fishing activity, ability may initiate strong perturbations in marine eco- increased anthropogenic nutrient input from rivers, systems including the collapse of commercially and, as in the case of the Black Sea, introduction of valuable fish stocks such as anchovy in the Black Sea the alien ctenophore species Mnemiopsis leidyi (Oguz, (Oguz et al., 2008a,b). 2005). Observations imply that not only human- To understand the extent of the impact of climate- related activities but also environmental variations induced drivers on anchovy fecundity the present study may play a critical role in controlling anchovy produc- analyzes the way an anchovy population responds to tion. There is evidence of a strong relationship environmental variability in the form of changing between regional climatic variations such as those water temperature and water column mixing. We influenced by the North Atlantic Oscillation (NAO) investigate whether high frequency fluctuations in tem- and anchovy stock fluctuations in the Black Sea (Nier- perature decrease fecundity rates, as well as the recruit- mann et al., 1999; Oguz, 2005; Oguz et al., 2006; Oguz ment rates of anchovy and if so, to what extent. Of and Gilbert, 2007) and other areas such as in the Med- particular interest is to determine the times of the year iterranean, where anchovy oscillations have been when anchovy are particularly vulnerable to tempera- related to climatic variations (Grbec et al., 2002; ture changes (such as the spawning season) and how Katara et al., 2011), and recently the Western Medi- strongly this influences the entire population. In addi- terranean Oscillation index (Martin et al., 2012). tion, we investigate how effective increased mixing European anchovy abundance in the North Sea rates that may occur simultaneously with lower temper- has fluctuated greatly in the past (Aurich, 1953) and atures, are in enhancing nutrient flux to increase periods of high abundance seem to coincide with anchovy survival and possibly counteract temperature warm phases of the Atlantic Multidecadal Oscillation effects. These questions are elaborated using a one- (AMO) indicating the high impact of climate vari- dimensional coupled model of the lower trophic level ability on anchovy dynamics (Petitgas et al., 2012). that is two-way coupled with an anchovy population In the Pacific, the Japanese anchovy (E. japonicus) dynamics model. Here, two-way coupling means that also has shown multi-decadal fluctuations, as opposed the lower trophic level influences anchovy population to sardine population dynamics, which are related to dynamics and vice versa. Although this theoretical interdecadal North Pacific ocean/climate variability study on how a recruitment system reacts to stochastic (Yasuda et al., 1999; Yatsu et al., 2005). Such regime climate variability is designed for the Black Sea, its shifts have been observed not only in the North Paci- results may also be applicable to other systems. fic (Takasuka et al., 2008) but also in the California Below, we first describe the model setup, followed Current and Humboldt Current systems and a rela- by a presentation of model findings. We describe the tionship with climatic regime shifts has been sug- seasonal variations of anchovy survival and recruit- gested (Lluch-Belda et al., 1989; Kawasaki, 1991; ment in response to three different scenarios over 1 yr. Chavez et al., 2003). We then examine interannual variability and the rela- It has been shown that decadal scale climate vari- tionship between anchovy reproduction, recruitment ability of either natural or human origin can trigger and spawner numbers under varying environmental regime transitions that may not only harm a resource conditions. The model results are discussed and sum- but also have eventual economic effects (Steele, marized in the Discussion and Conclusions sections. 1998). Additionally, within a period of favorable envi- ronmental conditions, the fishing stress, although very MATERIALS AND METHODS heavy, may sustain a high catch; whereas under adverse environmental conditions, the same level of Model description fishery may lead to a stock collapse (Hofmann and The anchovy bioenergetics and lower trophic level Powell, 1998; Oguz, 2005). models are two-way coupled (details may also be found Bioenergetics models of anchovy have been applied in Oguz et al., 2008a). This modeling system has previ- to different regions such as Chesapeake Bay (Wang ously been tested and validated for the Black Sea et al., 1997; Rose et al., 1999), the northern Aegean (Oguz et al., 2008a,b). The one-dimensional (1-D) © 2014 John Wiley & Sons Ltd, Fish. Oceanogr., 23:5, 436–457. 438 C. Guraslan€ et al. ecosystem model of the lower trophic level represents the details of which can be found in Table 1. With the euphotic zone, assumed to be 50 m deep, with two this model setup, model anchovy experience positive layers: a surface mixed layer with daily variations and weight growth from the beginning of summer to winter a subthermocline layer. A third layer below the eupho- (from June to January) as a result of availability of fod- tic zone provides nutrients to the euphotic zone via der zooplankton, which is triggered by increased pri- mixing.