Marine Science

ICES Journal of

Marine Science ICES Journal of Marine Science (2014), 71(2), 374– 390. doi:10.1093/icesjms/fst129

Nursery systems for Patagonian grenadier off Western Patagonia: large inner sea or narrow continental shelf?

1

Universidad de Los Lagos, imar Centre, Camino a Chinquihue Km. 6, Puerto Montt 5502764, Chile Universidad Austral de Chile, Trapananda Centre, Camino a Coyhaique Alto, Coyhaique 5950000, Chile 3 University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory, 1 Williams St., Solomons MD 20688, USA 4 Universidad de Concepcioń, Department of Oceanography, Barrio Universitario, Concepcion 4070386, Chile 5 Fisheries Studies Centre (CEPES), Pe´rez Valenzuela 1276, Providencia 7500562, Chile. 2

*Corresponding Author: tel. +56 65 322 425; fax +56 65 322 428; e-mail: [email protected] Niklitschek, E. J., Secor, D., Toledo, P., Valenzuela, X., Cubillos, L., and Zuleta, A. 2014. Nursery systems for Patagonian grenadier off Western Patagonia: large inner sea or narrow continental shelf? – ICES Journal of Marine Science, 71: 374– 390. Received 9 March 2013; accepted 1 July 2013; advance access publication 17 November 2013.

Adjacent to Chile’s long and narrow continental shelf, the Patagonian Inner Sea (PES) is among the largest and most complex estuarine systems in the world. The PES harbours high concentrations of juveniles and adults of important groundfishes, which spawn within or in near proximity to it. A dominant view is that recruitment primarily originates here rather than in adjacent coastal regions. We used otolith stable isotopes to evaluate the relative contribution of several PES and continental shelf regions to recruitment of Patagonian grenadier, one of the most abundant groundfishes in the area. Seawater chemistry confirmed that d13C and d18O differentiated these nursery and feeding regions. Estimated recruitments from PES nurseries to adult feeding regions were important (10 – 35%), but lower than dominant contributions from shelf nurseries (64 – 85%). Stable isotope differences within otoliths indicated, however, that most adults had previously used PES habitats as subadults. Adults exhibited stronger homing to feeding habitats in the PES than to shelf regions, suggestive of seasonal site fidelity or partial migration behaviours. The proximity of principal spawning areas to the bifurcation of the West Wind Drift Current may cause large interannual and decadal variations in larvae transport and the relative contribution of different shelf and PES nurseries to recruitment. Keywords: hoki, Macruronus magellanicus, mixture models, otolith microchemistry, recruitment.

Introduction Many of the same ecologically and commercially important marine species are distributed on either side of the Patagonian Plateau, suggestive of transoceanic migrations and seasonal and/or reproductive mixing. Such species include Patagonian toothfish Dissostichus eleginoides Smitt 1898 (Ashford et al., 2006, 2007), southern hake Merluccius australis Hutton, 1872 (MacKenzie and Longshaw, 1995; Quinteiro et al., 2000), blue whiting Micromesistius australis australis Norman, 1937 (Arkhipkin et al., 2009; Niklitschek et al., 2010) and Patagonian grenadier Macruronus magellanicus Lo¨nnberg, 1907 (Schuchert et al., 2010). The coastal waters around Patagonia are different in bathymetry, extent, and water quality (Figure 1). In the Atlantic Ocean an expansive continental shelf merges with a relatively continuous coastline. In contrast,

the Pacific shelf along Patagonia is narrow but harbours a reticulated system of more than 90 000 km of gulfs, sounds, channels and fjords. This Patagonian Estuarine System, ranges from the Reloncavi Sound (41830’S) to Cape Horn (54830’S) and is considered to be one of the most extensive estuarine regions in the world (Iriarte et al., 2010). The Patagonian Estuarine System (PES) harbours high concentrations of eggs, larvae and juveniles of some of the most important coastal fishes, such as southern hake and Patagonian grenadier (Balbontıń and Bernal, 1997; Bernal and Balbontıń, 2003; Lillo et al., 2004b, 2006, 2008, 2009a, 2011; Balbontıń, 2006; Bustos et al., 2007; Landaeta et al., 2011, 2012), which spawn within or in near proximity to the PES. Consistent with the essential nursery role attributed to estuaries elsewhere (Costa et al., 2002), the dominant view is that the PES, rather than the adjacent continental shelf,

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Edwin J. Niklitschek 1,2*, David H. Secor 3, Pamela Toledo1, Ximena Valenzuela 2, Luis A. Cubillos 4, and Alejandro Zuleta 5

Nursery systems for Patagonian grenadier

D’Amato and Carvalho, 2005). Nonetheless, no major spawning/ nursery habitats have been found in the Atlantic Ocean, and at least a fraction of the Northwest Atlantic stock is assumed to originate from nurseries located in the Pacific Ocean (Galleguillos et al., 1998; Giussi et al., 2004; D’Amato and Carvalho, 2005; Olavarrıá et al., 2006; Schuchert et al., 2010). Patagonian grenadier is a eurybathic species that exhibits strong affinity for Subantarctic waters (SAAW) (Cousseau, 1993). In the Southeast Pacific, the species follows the SAAW, which meets and flows above the Subsurface Equatorial Water (ESSW), both along the shelf and within the PES (Silva and Neshyba, 1979; Sievers and Silva, 2008). While early stages of Patagonian grenadier tend to remain in SAAW, subadults and adults seem to move actively between SSAW and EESW layers (Lillo et al., 2010, 2011). Upwelling events, however, may expose early stages to the hypoxic, high salinity EESW layer, which is expected to exhibit high d180 and low d13C values (Quay et al., 2003). In contrast, mixing events occurring in the PES, may expose these early stages to low salinity estuarine waters (EW), which tend to be depleted in terms of both 180 and 13C, and flow on top of the SAAW (Sievers and Silva, 2008). The submarine canyons where the main spawning aggregations congregate (Figure 1) are affected by three main oceanographic factors: (i) the West Wind Drift that approaches South America and bifurcates at a seasonally variable latitude (35 –458S) into the

Figure 1. (A) Distribution of Patagonian grenadier Macruronus magellanicus around South America (shaded area), modified from Giussi et al. (2004), continental shelf (white area), major oceanic currents and main spawning grounds for this species. (B) sampling regions and sampling stations for seawater and fish in the Southeast Pacific Ocean. Oceanic current acronyms: HC ¼ Humboldt Current, WWD-B ¼ Western Wind Drift bifurcation, CHC ¼ Cape Horn Current, ACC ¼ Antarctic Circumpolar, EFC ¼ Eastern Branch of Falkland Current, WFC ¼ Western Branch of Falkland Current, ASD ¼ Argentinian Shelf Drift. Sampling region acronyms: CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, ME ¼ Magellan Estuarine System, SPS ¼ Southern Peruvian Shelf, NMS ¼ Northern Magellan Shelf, CMS ¼ Central Magellan Shelf, SMS ¼ Southern Magellan Shelf.


represents the most important nursery area for several groundfishes in western Patagonia (Ce´spedes et al., 1996, Anonymous, 2012). As in other coastal systems (Able, 2005), this hypothesis has not been formally tested. A challenge in comparing nursery importance is overcoming the risk of spurious conclusions due to uneven sampling intensities among potential nursery habitats (Able, 2005). In the present work, we contrast recruitments from estuarine and shelf regions in western Patagonia to several feeding aggregations of adult Patagonian grenadier, an abundant member of the groundfish, exploited on an industrial scale in shelf waters. Distributed from the Southeast Pacific islands of Juan Fernandez to the Falkland (Malvinas) Islands in the Southwest Atlantic Ocean (Figure 1), its latitudinal range stretches from 29– 578S (Cape Horn), including oceanic seamounts, continental shelf and slope areas and most of the PES (Giussi et al., 2004; Ernst et al., 2005; Chong et al., 2007). The largest known spawning aggregations occur between 44 and 478S, in submarine canyons located on the Pacific shelf (Ernst et al., 2005; Rubilar et al., 2006; Lillo et al., 2009a). Nevertheless, several secondary spawning areas may exist across its distribution range as suggested by the presence of ripe adults in commercial captures located elsewhere (Ernst et al., 2005), and by the reported presence of larvae on either side of the Magellanic Strait (538S), nearby Cape Horn (558S), and farther north in coastal areas of the Atlantic Ocean (Figure 1) (Machinandiarena and Ehrlich, 1999; Bernal and Balbontıń, 2003;

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376

Material and methods In the present study, we focused on the Southeast Pacific Ocean continental shelf and the PES areas used by Patagonian grenadier along the western coast of Patagonia (Figure 1). The continental shelf was subdivided into four sampling areas, which followed recognized biogeographic regions (Lancellotti and Vasquez, 1999; Haüssermann, 2006; Spalding et al., 2007): South Peruvian (SPS), Northern Magellan (NMS), Central Magellan (CMS) and Southern Magellan (SMS). The PES was subdivided in three relatively discrete oceanographic units (Niklitschek et al., 2013): the Chiloe Inner Sea (CE), the Aysen Fjords System (AE), and the Central Magellan Fjords System (ME) (Figure 1). While commercial fisheries exist in each of the four shelf regions, the main known spawning areas are concentrated in the NMS. Highest concentrations of eggs, larvae and early juveniles, on the other hand, have been reported in the CE and AE estuarine regions. We developed a four-year effort (2008 –2012) to collect early juvenile (ages 0+ and 1+) and mature (ages .5+) Patagonian grenadier from all sampling areas (Figure 1). Sampling covered a total of 690 trips using trawl deployments from industrial and research vessels and longline and purse-seine deployments from artisanal

boats. A few juvenile samples (eight) were obtained by dissecting Southern hake stomachs. We wanted to reduce the risk of spurious patterns caused by lack of independence between individuals within year classes or within schools. Thus, to include and control for possible interannual variability in otolith composition, we selected adult samples belonging to three year classes (2003, 2004 and 2005) common to all sampling areas. This balanced design, however, was not possible for juveniles, where samples from SPS, NMS and SMS belonged to the same year class (2010) but samples from AE and CE corresponded to year classes 2008–2009 and 2011–2012, respectively. We were unable to obtain juvenile fish samples from the ME and the CMS areas. To capture interschool variability, we selected a minimum of three independent sampling deployments per area, where each deployment was separated from others by at least 18 km and/or 24 h. Sagittal otoliths from juvenile and adult Patagonian grenadier were embedded in plastic resin, and then sectioned using a lowspeed diamond saw (Secor et al., 1992). A transverse (0.2-mm thick) section was cut at both sides of the primordial area and then glued to a 2-mm thick plastic wafer such that the glue occurred only under the resin margins. Once mounted on a petrographic slide, we used a micromill to extract size- and shape-standardized prisms from the otolith core, as well as from its intermediate and marginal regions. Core, intermediate and marginal otolith prisms had nominal volumes of 0.035, 0.015 and 0.029 mm3 and were designed to represent the young-of-the-year (YOY, first 5 –7 months of life), subadult (2–4-year-old) and adult (.5-year-old) life phases, respectively. To determine the relative composition of stable isotopes, otolith prisms were first decontaminated according to the protocol described in Rooker et al. (2001). Prisms were immersed for 5 min in 1% nitric acid to remove surface contamination, and then rinsed with double-distilled water (DDIH2O) for 5 min to remove the acid. Finally, they were dried under a Class 100 laminar flowhood, weighed to the nearest 0.01 mg, and stored in clean plastic vials. All instruments were cleaned with 10% HCL, DDIH2O, and dried with ultra-clean nitrogen air between samples. For stable isotope analysis, otolith fragments were powdered and submitted to the University of Arizona Isotope Geochemistry Laboratory for analysis, following procedures detailed by Kerr et al. (2007). Stable isotopes were measured with an automated carbonate preparation device (KIEL-III) attached to a gas-ratio spectrometer (Finnigan MAT 252). Otolith samples were reacted with dehydrated phosphoric acid under vacuum at 708C. The CO2 was then analysed for concentrations of 13C and 18 O, reported as per ml relative to a standard, hereafter d13C and d18O. The standard substance for both isotopes corresponded to Vienna Pee Dee Belemnite (VPDB, international standards NBS-18 and NBS-19). Precision estimates reported by the Isotope Geochemistry Laboratory indicated coefficients of variation of 0.6% and 0.5% for d13C and d18O, respectively.

Seawater chemistry Relative concentrations of 18O in seawater and 13C in dissolved inorganic carbon (DIC) were determined in 107 seawater samples (Figure 1), collected between 1 and 250 m depth, during 11 research cruises, carried out between July and December in years 2009–2012. Water samples for d18O analysis were stored in dark bottles and refrigerated until analysis. Water samples for d13C were preserved by adding 1 ppt of sodium azide and analysed within the same timespan. Analyses were conducted by the University of California –


northern Humboldt Current and the southern Cape Horn Current (Silva and Neshyba, 1979; Gatica et al., 2009), (ii) the alongshore Chile –Peru current system that diminishes in strength south of 458S, ending at about 488S (Silva and Neshyba, 1979; Leth and Shaffer, 2001), and (iii) the Pacific Patagonia cold estuarine front, a broad zone extending along the PES that becomes strongest between 44 and 478S (Da´vila et al., 2002; Acha et al., 2004). Thus, Patagonian grenadier eggs and larvae face a combination of retentive and advective forces that are believed to transport at least a fraction of them to the adjacent PES (Figure 1). Here, Patagonian grenadier dominate the ichthyoplankton composition during the early spring (Castro and Landaeta, 2003; Landaeta and Castro, 2006), reaching larval densities that are comparable or even higher than those observed within the spawning areas (Ernst et al., 2005). Moreover, the documented presence of subadults and adults of this species in the PES (Lillo et al., 2006) suggests that at least part of the population might spawn and complete its life cycle in these waters. Several hundred kilometres north and somewhat isolated from the PES and adjunct shelf region, dense aggregations of subadults (ages 1 –3) supported a large purse-seine fishery in Central Chile (35–408S) during the 1980s and 1990s. The presence of such aggregations suggest immigration into this area early in life and supports the currently held view that a second important nursery for Patagonian grenadier occurs on the shelf, somewhere along the exposed coastline and north of the principal spawning area (Ernst et al., 2005; Cubillos et al., 2009). The main purpose of the presently described investigation was to compare regional estuarine and shelf nursery contributions of juveniles to the Patagonian grenadier stocks (fished aggregations) along the Northeast Pacific Ocean, off the west coast of Patagonia. To achieve these goals, we measured and compared the relative composition of the stable isotopes 13C and 18O in portions of otolith sections representing different life phases. Otolith composition in juvenile fish were used to produce regional baselines to discriminate natal habitats for adult samples (Thorrold et al., 1997a; Kerr et al., 2007; Rooker et al., 2008). Comparing stable isotope composition between subadult and adult portions of otoliths, we also evaluated homing and migrations among regions across these phases of life history.

E. J. Niklitschek et al.

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Data interpretation and statistical inference To support the use of d18O and d13C as environmental proxies, we first regressed their ambient concentrations onto the corresponding temperature and salinity values measured in each water sample. To test whether these isotopes were incorporated into the otolith proportional to their concentration in the water column, we regressed d18O and d13C concentrations in otolith cores of juvenile fish onto corresponding seawater concentrations, averaged at a regional scale. For the latter purpose, we included only seawater samples from the subsurface layer, between the picnocline and 100 m deep, where Patagonian grenadier is expected to spend its first months of life (Castro and Landaeta, 2003). Statistical analyses of isotopic concentrations in seawater and otoliths were based upon univariate and multivariate versions of generalized linear mixed models, GLMM (Searle, 1987; Littel et al., 1996; Venables and Dichmont, 2004). Univariate GLMM were used to test univariate differences in isotopic concentrations among and within sampling areas, after accounting for lack of independence (as random effects) due to correlation within sampling events and cohorts using the R package “lme4” (Bates et al., 2012). Null and alternative hypotheses were compared through likelihood ratio tests (Venables and Ripley, 2002). Bivariate GLMMs (Hadfield, 2010) were used to test bivariate differences in seawater and otolith concentrations of d13C and d18O among different sampling areas and to compare different habitat grouping models for otoliths and seawater. Bivariate GLMM models were fit using the R package “MCMCglmm” (Hadfield, 2010). Model comparisons were based upon mean deviance and the number of parameters being estimated in each model using Akaike’s (1973) information criterion (AIC) for univariate models, and the Deviance Information Criterion (DIC) for multivariate ones (Hadfield, 2010). GLMM assumptions about univariate or bivariate normality were assessed graphically by comparing full model-residuals Q-Q plots against randomly generated (1000 samples) Q-Q envelopes (Venables and Ripley, 2002). Homoscedasticity and linearity were assessed graphically by plotting model residuals against their corresponding predicted values. Homoscedasticity was also evaluated by testing the significance of Pearson’s correlation between full model predicted values and the absolute value of their residuals. Null hypotheses for all analyses in the present work were rejected under a significance level (a) of 0.05.

Habitat grouping models used for the bivariate analysis of seawater and otoliths considered a null hypothesis (H0) that pooled all regions into a single group. This null hypothesis was contrasted against: (i) the full hypothesis (H1) that discriminated each sampling region, (ii) a second alternative hypothesis (H2) that pooled shelf and estuarine areas into four ecoregions: South Peruvian (SP), Northern Magellan (NM), Central Magellan (CM) and Southern Magellan (SM), and (iii) the 12 possible combinations of the following hypotheses, defined for estuarine (A) and shelf areas (B): A0: all three estuarine systems grouped into a single class; A1: discrimination into three estuarine areas (CE, AE, ME); A2: northern estuaries (CE + AE) separate from southern (ME) ones; B0: all four shelf areas grouped into a single class; B1: discrimination into four shelf areas (SPS, NMS, CMS, SMS); B2: Southern Peruvian Shelf (SPS) separate from all Magellan shelf (NMS + CMS + SMS) areas; B3: SPS and NMS separate from Central –Southern Magellan shelf areas (CMS + SMS). To estimate the most likely number of sources (nursery areas) and/or the relative contribution of these sources to the different sampling areas (mixtures) we used a series of finite distribution mixture models (Everitt and Hand, 1981; Millar, 1987) (FDMs) that considered different numbers of sources and mixtures. FDMs reconstruct the observed distribution of isotopic concentrations at a given mixture based upon the following parameters: (i) the number of sources (nursery or feeding areas); (ii) the source isotopic baselines (means and standard deviations for each source); and (iii) the proportional contribution from each source to each mixture. In this particular application, FDMs were fit through a maximum likelihood procedure that assumed a normal distribution of isotopic signatures and a multinomial distribution of model errors (Niklitschek et al., 2010). In practice, we maximized the joint likelihood of the data by estimating the parameters vector c, given the model: l(c|X) =

M N m=1 i=1

K k=1

1 1 ′ pk,m × j/2 × exp − (xi,m − mk ) Sk (xi,m − mk ) 2 2p |Sk |1/2

where, 1 ; natural-scaled mix proportion of source k at pk,m ¼ 1 + e−bk,m mixture m, bk,m ¼ logit-scaled mix proportion of source k at mixture m, mk ¼ vector of (j ¼ 2) means for source k stable isotope baseline. Sk ¼ variance-covariance matrix for source k stable isotope baseline. xi,m ¼ vector of stable isotope values observed in fish i from mixture m. Natural-scaled mix proportions (

pk,m ) were back-calculated

k,m estimates. Variances of

from the logit-scaled b pk,m were

approximated from V[bk,m ] as follows:

k,m

b V

V pk,m = 4 . bk,m 1 − e


Davis, Stable Isotope Facility, within 60 days after collection. Analyses of d18O were carried out using a Laser Water Isotope Analyser V2 (Los Gatos Research, Inc., Mountain View, CA, USA) and reported relative to the VSMOW standard. Precision reported by the laboratory was ≤0.3 ppt. Analysis of seawater d13C utilized a Surveyor HPLC coupled to a Thermo-Finnigan Delta Plus Advantage isotope ratio mass spectrometer (IRMS, Thermo Scientific, Bremen, Germany) through an LC Isolink interface. Water subsamples (2 ml) were injected directly into a liquid carrier stream, then mixed with phosphoric acid (1.7 M, degassed) and heated (to 808C), to force equilibrium between CO2 and H2CO3 to gaseous CO2. Enriched CO2 was then transferred to the helium carrier gas, dried and transferred to the IRMS. To calculate delta values of sample CO2 peaks, two laboratory standards were analysed with every 10 samples: (i) lithium carbonate dissolved in degassed deionized water, and ii) deep seawater reference material (both calibrated against NIST 8545).

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Results Seawater We found significant univariate differences in seawater d13C and d18O between sampling areas (subsurface layer), which accounted for 22% and 77% of the observed variability (residual deviance), respectively (Figure 2). Seawater d13C tended to be higher in shelf than in estuarine regions, although this difference was not always significant. Seawater d18O also tended to be higher in shelf regions, particularly in the SPS and the NMS samples, which exhibited values that were significantly higher than either estuarine region (Figure 2). The bivariate GLMM analysis also indicated significant differences between sampling regions. Here the most informative bivariate model corresponded with the full hypothesis (DIC ¼ 193.6) that considered each sampling region as a separate group. Nonetheless, the second-best alternative hypothesis, A1B2 that grouped both Magellan Shelf areas (NMS and SMS) together, exhibited a very close DIC value of 193.7. Linear regression analysis showed no evidence of significant relationships between d13C and temperature, salinity or their combination. Significant relationships were found, however, between d18O and temperature and salinity, with a significant covariance effect from sampling area. The most informative habitat-grouping hypothesis was A0B0, which only discriminated between estuaries and continental shelf habitats. The resulting regression model defined independent intercepts and salinity coefficients for estuarine and for shelf habitats, but a single temperature coefficient for both habitat types (Figure 3).

Juvenile otoliths Core sections of juvenile Patagonian grenadier otoliths exhibited d18O values that ranged between 2 0.028 and 1.88 (Figure 4). While d13C exhibited a greater range of values, between 2 3.58

Figure 2. Relative concentrations of stable isotopes of carbon (d13C) and oxygen (d18O) in seawater (picnocline-100 m) in five different sampling regions. CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, SPS ¼ South Peruvian Shelf, NMS ¼ Northern Magellan Shelf, CMS ¼ Central Magellan Shelf. Box-plot whiskers length equals 1.5 times the interquartile range. Different superscript letters indicate significant differences in mean values (Tukey’s test on GLMM model).


We conducted two basic types of FDM analyses, an “unknown source” analysis, whose vector c contained (m + 5) × k elements that included the isotopic baselines (mk and Sk) characterizing each source, and the logit-scaled proportional contributions from each of the k sources to each of the m mixtures bk,m. The second type corresponded to a “fixed-source” analysis whose baseline parameters (yi,j and Sk) were estimated previously and independently from the mixture model. Thus, in fixed-source models the vector c only contained the m × k estimates of bk,m. As the likelihood of a mixture model increases with the number of mixtures and sources being tested, we conducted a systematic model selection procedure based upon the original (smaller is better) formulation of Akaike (1973)’s information criterion. A fixed-source FDM was used to infer the proportional contribution from each nursery area to the sampled adult aggregations. Here, we compared the isotopic composition observed in the otolith cores of adults with nursery region baselines derived from otolith cores of juveniles. Because the juvenile fish used to derive these nursery region baselines were 6 –22 months old, there was a time lag between otolith core formation and fish capture. To assess the probable degree of mixing among nursery regions during this time, we carried out an unknown-source FDM analysis of the isotopic composition of otolith core sections of juveniles. Besides estimating the crossed contribution (mixing) among nursery areas, this analysis yielded alternative estimates about the likely number of nursery regions (sources) and their corresponding baseline parameters. To evaluate regional fidelity and movements among feeding regions between subadult and adult phases, we used a fixed-source FDM approach that compared milled subadult portions of otoliths from adults with feeding region baselines. These baselines were developed using the most recently formed portion of the same otoliths, which was assumed to contain the isotopic imprint from the feeding region where the adult fish was captured.



379

Figure 4. Relative concentrations of stable isotopes of carbon (d13C) and oxygen (d18O) in core sections representing the first months of life of juvenile Patagonian grenadier Macruronus magellanicus (ages 0+ and 1+) from five different sampling areas. CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, SPS ¼ South Peruvian Shelf, NMS ¼ Northern Magellan Shelf, CMS ¼ Central Magellan Shelf. Box-plot whiskers length equals 1.5 times the interquartile range. Different superscript letters indicate significant differences in mean values (Tukey’s test on GLMM model).

and 0.16, both isotopes were significantly different between sampling areas (GLMM, p , 0.0001). Pairwise comparisons indicated that d13C values in CE and the SMS, were significantly lower than those observed in AE and in the SPS, with intermediate values found in the NMS (Figure 4). Mean d18O values observed in AE were significantly lower than those observed in all continental shelf regions (SPS, NMS, SMS). The highest mean d18O values

were observed in the SPS, although this difference was significant only when compared to estuarine regions (Figure 4). The bivariate GLMM analysis of juvenile otolith composition also indicated significant differences in mean d13C and d18O between sampling areas. The three best-known Patagonian grenadier nursery areas (CE, AE and SPS) tended to exhibit larger differences from each other than the NMS and SMS compositions, which


Figure 3. Observed (circles) and predicted (lines) values of d18O against salinity and temperature in seawater samples collected along the Southeast Pacific Coast (39– 518S), between 2009 and 2012. Predicted values correspond to the most informative regression model, which discriminated between estuarine (open circles) and continental shelf (closed circles) samples. Left panel shows salinity effects, given temperature averages by habitat-type. Right panel shows temperature effects, given salinity averages by habitat-type.

380

instead, between mean d18O values in otolith cores and congruent seawater samples (Pearson’s r ¼ 0.99, p , 0.01, Figure 6). Mean disequilibrium between otolith and seawater values also showed contrasting results between carbon and oxygen, with differences of 21.21 and +1.44 for d13C and d18O, respectively.

Adult otoliths Overall, univariate d18O and d13C levels and their bivariate distributions in core sections from adults were similar to equivalent core sections observed in juvenile specimens (Figure 7). Otolith d13C and d18O observed in adult fish tended, however, to increase in portions representing older phases, which exhibited significantly higher mean concentrations than the core section (Figure 7). Within each life phase, univariate differences found between sampling regions changed with the life phase assayed (YOY, subadult, adult). Thus, while neither d13C nor d18O differences between sampling regions were significant in otolith cores, we did observe significant

Figure 5. Bivariate diagram of d13C and d18O in otolith core sections representing the first months of life of juvenile Patagonian grenadier Macruronus magellanicus (ages 0+ and 1+) collected from five sampling regions. CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, SPS ¼ Southern Peruvian Shelf, NMS ¼ Northern Magellan Shelf, SMS ¼ Southern Magellan Shelf. Left panel shows 68-percentile ellipses estimated for individual or grouped sampling regions. Right panel shows 68-percentile ellipses corresponding to the four hypothetical sources identified by a four-sources finite distribution mixture model.

Table 1. Loge-scaled likelihood (LL) and Deviance Information Criterion (DIC) for alternative GLMM bivariate models used to explain d13C and d18O variability in otolith cores from juvenile Patagonian grenadier Macruronus magellanicus (ages 0+ and 1+). Grouping hypotheses A1B2: estuarine regions discriminated as separate categories (CE and AE); SPS separate from Magellan shelf regions (NMS + SMS) A1B1: all estuarine and shelf regions discriminated as separate categories (full model) A1B0: all estuarine systems discriminated as separate categories; all shelf regions grouped into a single class A0B0: all estuarine systems grouped into a single class; all shelf regions grouped into a second class A0B2: all estuarine systems grouped into a single class; Magellan shelf regions grouped into a single class separate from SPS

Number of groups 4

LL 2242.4

DIC 521.1

5 3

2242.1 2242.1

521.2 522.0

2

2241.7

522.5

3

2242.5

523.2

CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, SPS ¼ Southern Pacific Shelf, NMS ¼ Northern Magellan Shelf, SMS ¼ Southern Magellan Shelf. Only results from the five most informative hypotheses are shown, selected and ranked according to their DIC values.


were similar to each other and overlapped with CE and SPS samples (Figure 5). The most informative GLMM model, A1B2 (DIC ¼ 521.1), discriminated the two sampled estuarine regions (CE and AE) and the SPS as three separate groups, while pooling the Magellan shelf regions (NMS and SMS) into a single category (Table 1). This combination (A1B2), however, was not much different from the full model (DIC ¼ 521.2), which distinguished each sampling region as a separate group (Table 1). Estimated baselines for the A1B1 hypothesis showed highly variable values for d13C/ d18O covariances (Table 2), equivalent to correlations between 0.03 and 0.4. We did not find evidence of a significant correlation between GLMM-adjusted mean d13C values in otolith cores of juvenile fish and seawater in the corresponding sampling regions (Pearson’s r ¼ 2 0.07, p . 0.9, Figure 6). While the largest disequilibrium between otolith and seawater was observed in the CE region (21.75), the AE region exhibited both the lowest seawater d13C and the highest otolith d13C. A positive relationship was found,


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Nursery systems for Patagonian grenadier Table 2. Otolith isotope composition baselines estimated for nursery and adult feeding regions of Patagonian grenadier Macruronus magellanicus. Estimated chemical fingerprint Mean (Variance) d13C

d18O

22.21 (0.272) 20.99 (0.269) 21.94 (0.221) 21.25 (0.243)

0.94 (0.08) 0.61 (0.099) 1.27 (0.070) 1.39 (0.093)

20.03 (0.247) 20.15 (0.286) 20.72 (0.140) 0.46 (0.188) 20.32 (0.681) 21.22 (0.163)

2.42 (0.124) 1.71 (0.046) 2.25 (0.034) 2.70 (0.024) 2.59 (0.046) 2.50 (0.069)

Covariance (d13C, d18O) 0.0064 0.0016 0.0313 0.0814 0.093 0.053 0.032 0.008 0.087 20.001

Nursery baselines based upon otolith cores from juvenile fish (ages 0+ and 1+). Feeding region baselines estimated from marginal sections of otoliths from adults. Sampling regions grouped according to the most informative hypotheses corresponding to juvenile (Table 1) and adult (Table 3) fish. CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, ME ¼ Magellan Estuarine System, SPS ¼ Southern Peruvian Shelf, NMS ¼ Northern Magellan Shelf, CMS ¼ Central Magellan Shelf, SMS ¼ Southern Magellan Shelf.

Figure 6. Relative concentrations of stable isotopes of carbon (d13C) and oxygen (d18O) in otolith core sections of juvenile Patagonian grenadier Macruronus magellanicus (ages 0+ and 1+) and in seawater dissolved inorganic carbon (July – December), at corresponding sampling areas. CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, SPS ¼ South Peruvian Shelf, NMS ¼ Northern Magellan Shelf. Circles correspond to GLMM-adjusted means, error bars represent standard errors. compositional differences between sampling regions in otolith sections representing both subadult and adult life phases (Figure 8). Bivariate distributions of d13C and d18O also showed greater segregation among sampling regions for subadult and adult phases than for the YOY phase sampled from the same adult otolith (Figure 8). The GLMM bivariate analyses of otolith cores (YOY phase) indicated that the most informative grouping hypothesis was H2, which pooled estuarine and shelf sampling regions into four ecoregions: Southern Peruvian, Northern Magellan, Central Magellan and Southern Magellan. Nonetheless, the difference

between H2 (DIC ¼ 944.7) and the null hypothesis H0 (no group separation, AIC ¼ 945.1) was relatively small (Table 3). In contrast to the YOY phase, the null hypothesis (H0) was the least informative one for both subadult (DIC ¼ 639.3) and adult (DIC ¼ 626.3) portions of adult otoliths. The most informative hypothesis was A1B3 for subadult (DIC ¼ 616.7) and adult phases (DIC ¼ 604.2), which considered all sampling regions separated, but pooled together the central and southern Magellanic shelf regions (Table 3). Baselines determined for the six feeding regions defined by this hypothesis showed d13C values that decreased southward and were


Source (Nursery area) Nursery regions CE AE NMS/SMS SPS Adult feeding regions CE AE ME SPS NMS CMS + SMS

382


enriched in estuarine areas when compared with shelf areas of similar latitude (Table 2). A similar decreasing southward trend was observed for d18O values, but here estuarine areas were depleted in comparison with neighbouring shelf areas.

95% that corresponded to the SPS and NMS contributions to the AE region (Table 4).

Early mixing of juveniles

Given the nursery region baselines derived from juvenile otolith cores (Table 2), we estimated that the SPS was the most important and dominant nursery region for adults collected across all feeding regions, with predicted contributions ranging between 51 and 82% (Table 5, Figure 9). Much lower contributions were predicted, for the SMS and for the two estuarine regions (CE and AE). Although contributions by feeding region showed some nominal variability, the most informative FDM corresponded to the one based upon the null hypothesis (H0) that grouped all sampling regions into a single mixture (AIC ¼ 1328.5). The predicted contributions from the four nursery regions to this homogeneous mixture were 76, 13, 9 and 3% from the SPS, AE, CE and NMS regions, respectively (Table 5). Thus, the total contribution from continental shelf nursery regions (79%) exceeded by far the total contribution from estuarine regions (22%). The uncertainty (standard errors) in regional contribution estimates ranged between 3 and 22% (Table 5).

The unknown-source FDM analysis of otolith cores from juvenile fish selected a four-source model as the most informative hypothesis. Although this FDM was determined strictly from the covariance structure in the isotopic data, without reference to sampling regions, it matched and corroborated the number of nursery regions determined by the GLMM bivariate model (hypothesis A1B2). Moreover, the bivariate distribution of the FDM hypothetical sources resembled the baselines derived directly from the data by the GLMM model (Figure 5). As hypothetical FDM distributions were contained within observed bivariate distributions (Figure 5), we were able to relate sources I, II and IV to sampling regions CE, AE and SPS, respectively. However, because no significant differences were observed in isotopic compositions between otolith cores from NMS and SMS, we failed to relate source III to either of these two regions directly. Nonetheless, we related source III to NMS as a working hypothesis considering that the main spawning aggregations occur at NMS, and that mean seawater temperature and salinity at NMS were closer to those expected from the d18O values attributed to source III (analysis not shown). FDM results indicated very low mixing rates for juveniles collected in estuarine regions CE and AE, where 83 and 90% of the samples were estimated to have a local origin (Table 4, Figure 9). Much higher mixing rates were predicted for the shelf regions. Here 29 –40% interchange was estimated to occur between SPS and NMS. The most important contributions to the SMS region were attributed to the NMS (44%) and the CE (34%) regions (Table 4, Figure 9). The uncertainty in these contribution estimates, as indexed by their standard errors, ranged between 4 and 17% in most cases, with the exception of two unreliable estimates above

Predicted contribution of nursery regions to adult feeding aggregations

Predicted contribution of subadult feeding regions to adult feeding aggregations The fixed-source mixture analysis of the subadult phase indicated highly variable degrees of regional fidelity within feeding regions between subadult and adult phases (Table 6). Uncertainty in these contribution estimates showed also higher variability than estimated contributions from nursery areas, with standard errors ranging between ,0.1 and 26% (Table 6). Most adults sampled in the three estuarine regions (CE, AE and ME) and in the SPS were predicted to have used the same region as subadults, with the highest fidelity (93%) estimated for the CE region. In contrast, only 10% of the adults captured in the NMS were estimated to have used this area as a principal feeding area earlier in life. These


Figure 7. Relative concentrations of stable isotopes of carbon (d13C) and oxygen (d18O) in otolith sections representing juvenile (ages ,1), subadult (ages 3– 4) and adult (ages .5) phases in juvenile (grey boxes) and adult (white boxes) specimens of Patagonian grenadier Macruronus magellanicus. Data from all sampling areas pooled for graphical purposes. Box-plot whiskers length equals 1.5 times the interquartile range.


383


Figure 8. Bivariate diagram of d13C and d18O in otolith sections representing juvenile, subadult and adult life-phases of adult Patagonian grenadier Macruronus magellanicus captured in seven sampling areas: CE ¼ Chiloe Estuarine System; AE ¼ Aysen Estuarine System; SPS ¼ Southern Peruvian Shelf; NMS ¼ Northern Magellan Shelf; CMS ¼ Central Magellan Shelf; SMS ¼ Southern Magellan Shelf. Different symbols or colours indicate different groups corresponding to the most informative GLMM hypothesis.

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NMS adults were predicted to have used, instead, feeding regions located mainly in the Aysen (32%) and Magellan (30%) estuarine regions (AE and ME). The Magellan Estuarine System was also predicted to represent the most important subadult feeding region for the adults sampled in the CMS and the SMS (Figure 9).

Discussion The idea that fish populations depend upon a dominant nursery habitat and follow a single migration pattern has been implicit in classical fisheries ecology (Harden Jones, 1968). Although not

Grouping hypotheses YOY H2: shelf and estuarine regions pooled into four ecoregions (SP, NM, CM, SM) A0B0: all estuarine systems grouped into a single class; all shelf regions pooled into another single class H0: all sampling regions grouped into a single class (null hypothesis) Subadult A1B3: all estuarine regions, SPS and NMS as separate groups. CMS and SMS pooled into a single class H1: all sampling regions separate A1B2: all estuarine regions and SPS as separate groups. All Magellan shelf regions grouped into a single class Adult A1B3: all estuarine regions, SPS and NMS as separate groups. CMS and SMS pooled into a single class H1: all sampling regions separate A1B2: all estuarine regions and SPS as separate groups. All Magellan shelf regions grouped into a single class

Number of groups

LL

DIC

4

2447.1

944.7

2

2448.2

945.1

1

2448.8

945.8

6

2276.3

616.7

7 5

2276.9 2276.9

618.7 618.7

6

2270.3

604.2

7 5

2270.5 2271.2

605.3 607.8

Ecoregion acronyms: SP ¼ Southern Pacific, NM ¼ Northern Magellan, CM ¼ Central Magellan, SM ¼ Southern Magellan. Only results from the three most informative hypotheses corresponding to each phase are shown. Hypotheses selected and ordered according to their DIC values.

Table 4. Predicted contributions of hypothetical nursery areas to juvenile mixtures of Patagonian grenadier Macruronus magellanicus in the Southeast Pacific Ocean. Mean (SE) Mixture Chiloe Estuaries (CE) Aysen Estuaries (AE) Southern Peruvian Shelf (SPS) Northern Magellan Shelf (NMS) Southern Magellan Shelf (SMS)

Source I (AE) 0.07 (0.109) 0.83 (0.077) 0.03 (0.042) 0.08 (0.047) 0.05 (0.059)

Source II (CE) 0.9 (0.082) 0.11 (0.154) 0.03 (0.053) 0.19 (0.107) 0.34 (0.136)

Source III (SPS) 0.00 (na) 0.03 (0.944) 0.64 (0.091) 0.34 (0.071) 0.17 (0.077)

Source IV (NMS) 0.03 (0.137) 0.03 (0.960) 0.29 (0.114) 0.40 (0.137) 0.44 (0.167)

Number of sources, baseline parameters and contributions estimated using an unknown-source finite distribution mixture model. Standard errors (in parentheses) not available (na) when predicted values are exactly 0 or 1.


Table 3. Loge-scaled likelihood (LL) and Deviance Information Criterion (DIC) for alternative GLMM bivariate models used to explain d13C and d18O variability in otolith portions representing young-of the-year, subadult and adult phases of adult Patagonian grenadier Macruronus magellanicus.

always tested, this dominant nursery role has been frequently attributed to estuaries for many coastal species in Patagonia and elsewhere (Beck et al., 2001; Able, 2005). Here we formally contrasted relevant hypotheses about the number, location and relative importance of the main nursery habitats of Patagonian grenadier in the Southeast Pacific Ocean. We found evidence that at least four discrete nursery areas are sustaining stocks along the Chilean coast. The contribution to Patagonian grenadier recruitment estimated for estuarine regions was smaller than the contribution estimated for shelf regions, particularly for the SPS. Indeed, 62 –82% of the adults sampled in estuarine regions were predicted to have a shelf origin. This heavy reliance of the stock upon recruits from the SPS, as well as its mixed but homogeneous origin across different feeding regions, were unexpected but important results given past uncertainty about the structure and spatial dynamics of this stock (Cubillos et al., 2009). Our results support the idea that Patagonian grenadier does not depend directly on estuarine regions to complete its life cycle, but uses them as part of a “portfolio” of nurseries and feeding regions. The facultative use of multiple nursery habitats may correspond to an adaptive strategy that spreads risk and increases population resilience to adverse environmental conditions, which has been suggested to be relevant in other marine fishes (Attrill and Power, 2002; Secor et al., 2009; Kerr et al., 2010). This strategy may be also a common feature of populations inhabiting the very extensive and complex western Patagonian coast, where climatic and oceanographic oscillations can easily disrupt dominant advection trajectories of eggs and larvae (Norcross and Shaw, 1984), and reorder stability and productivity at specific shelf and estuarine habitats (Iriarte et al., 2010). While the two southernmost estuarine and shelf regions, ME and SMS, showed no evidence of being nursery habitats, juveniles sampled in the SMS were predicted to have originated elsewhere. These results were unexpected given previous reports that documented the presence of Patagonian grenadier larvae in both regions (Balbontıń and Bernal, 1997; Machinandiarena and Ehrlich, 1999; Bernal and Balbontıń, 2003). Our results, however, could be biased because we did not have juvenile ME samples available to compute specific nursery baselines for this particular region. Although this lack of juveniles in our ME samples may be explained by insufficient sampling effort (the lowest amongst all regions), it is also indicative of low abundances of YOY and yearlings in this region. We speculate that these low abundances could be related to dominant poleward and eastward advection by the Cape Horn and the Antarctic Circumpolar currents (Figure 1), which might

385


Table 5. Predicted contribution of nursery regions to feeding aggregations of Patagonian grenadier Macruronus magellanicus in the Southeast Pacific area. Predicted source contribution (nursery area) Adults mixture AE 0.04 (0.052) 0.14 (0.115) 0.04 (0.072) 0.04 (0.052) 0.15 (0.127) 0.01 (0.036) 0.12 (0.099) 0.09 (0.030)

Chiloe Estuarine System (CE) Aysen Estuarine System (AE) Magellan Estuarine System (ME) South Peruvian Shelf (SPS) Northern Magellan Shelf (NMS) Central Magellan Shelf (CMS) Southern Magellan Shelf (SMS) Pooled (null hypothesis)

CE 0.25 (0.102) 0.17 (0.094) 0.06 (0.042) 0.22 (0.110) 0.20 (0.097) 0.25 (0.097) 0.02 (0.045) 0.13 (0.038)

NMS/SMS 0.07 (0.073) 0.08 (0.112) 0.08 (0.097) 0.03 (0.046) 0.13 (0.146) 0.10 (0.108) 0.10 (0.092) 0.03 (0.030)

SPS 0.65 (0.136) 0.62 (0.186) 0.82 (0.128) 0.72 (0.130) 0.51 (0.216) 0.65 (0.149) 0.75 (0.143) 0.75 (0.062)

Predictions (and standard errors, in parentheses) obtained from a fixed-source finite distribution mixture model that compared d13C and d18O compositions in otolith cores of adults to baselines derived from isotopic compositions observed in otolith cores of juvenile fish.

Table 6. Predicted contribution of subadult feeding areas to adult mixtures of Patagonian grenadier Macruronus magellanicus identified in the Southeast Pacific Ocean. subadult feeding area Adult mixture (sampling area) CE AE ME SPS NMS CMS + SMS

CE 0.93 (0.047) 0.40 (0.132) 0.15 (0.054) 0.10 (0.065) 0.00 (na) 0.05 (0.056)

AE 0.07 (0.112) 0.53 (0.185) 0.19 (0.000) 0.33 (0.145) 0.32 (0.182) 0.12 (0.059)

ME 0.00 (na) 0.07 (0.116) 0.62 (0.098) 0.03 (0.037) 0.30 (0.133) 0.49 (0.010)

SPS 0.00 (0.121) 0.00 (0.255) 0.00 (0.112) 0.54 (0.163) 0.18 (0.37) 0.00 (0.010)

NMS 0.00 (na) 0.00 (na) 0.00 (na) 0.00 (na) 0.10 (0.26) 0.07 (0.046)

CMS 1 SMS 0.00 (na) 0.00 (na) 0.04 (0.000) 0.00 (na) 0.10 (0.135) 0.27 (0.013)

Predictions obtained from a finite distribution mixture model based upon 6-sources (Table 3). CE ¼ Chiloe Estuarine System, AE ¼ Aysen Estuarine System, ME ¼ Magellan Estuarine System, SPS ¼ Southern Peruvian Shelf, NMS ¼ Northern Magellan Shelf, CMS ¼ Central Magellan Shelf, SMS ¼ Southern Magellan Shelf. Standard errors (in parentheses) not available (na) when predicted values are exactly 0 or 1.

flush eggs and larvae away from the Magellanic estuaries and shelf into the Atlantic Ocean. Because some adult feeding areas, such as the SMS or the Argentine Shelf, are separated from the main spawning area (NW

Patagonian canyons) by 1400 km or more (Figure 1), it seems unlikely that all adults return to spawn here, at least on an annual basis. Although some contingents may skip spawning, as found in hoki Macruronus novaezelandiae (Livingston et al., 1997), the


Figure 9. Connectivity diagrams showing: (A) estimated mixing among nursery regions (left panel), (B) estimated contribution of nursery areas to adult feeding aggregations (middle panel), and (C) estimated contribution of subadult feeding regions to adult feeding regions. Line widths are proportional to estimated contributions. Only contributions .10% are shown. Numbers contained in circular arrows indicate percentage of local origin. Dashed lines indicate direction of the flow is uncertain.

386

unexplained variability has been reported in the relative contribution of these two sources to otolith carbon (Elsdon et al., 2010). Thus, a number of studies report that variability in d13C of ingested prey (Radtke et al., 1996; Elsdon et al., 2010), and changes in metabolic rates (Kalish, 1991b; Gauldie et al., 1994; Dufour et al., 2008) have highly significant effects upon otolith d13C in several species. Hence, we speculate that the large d13C depletion and the lack of correlation we found between otolith and seawater DIC values, was probably related to rather large contributions of organic sources to otolith carbon in Patagonian grenadier juveniles. Because small differences in routine metabolism are expected among sampling regions, most of these observed variability in otolith d13C would be related to differences in the isotopic composition of preys consumed by juvenile fish in different regions. Because otolith core sections represented several months of life, all d13C effects produced by short-term variations in habitat DIC, prey composition or metabolism were integrated into single responses for each juvenile fish. A similar situation occurred with water DIC data, which exhibited large variability (Figure 6), but was represented by a single seasonal average per region. While most juveniles had been of local origin, we had no information about their movements within each nursery region, whose microbasins may exhibit large differences in water masses and allochthonous carbon sources (Sievers and Silva, 2008; Silva et al., 2011). It is also possible that large intra-seasonal variability in DIC and dietary d13C values had resulted from short-term phytoplankton blooms and food-web shifts that characterize the SPS and PES regions (Vargas et al., 2007; Montero et al., 2007, 2011; Gonza´lez et al., 2010, 2011). These large increases in primary production overlap with seasonal changes in the absolute and relative contribution of allochthonous carbon, which tends to be low in d13C and may fuel up to 50% of the secondary production in the PES (Vargas et al., 2011). Across the distant regions investigated, Patagonian grenadier exhibited both homing and mixing across life-history phases. Rapid dispersal from nursery areas, within the first two years of life, and large mixing rates between shelf and estuarine regions were predicted (Figure 9A). After this initial period, recruits from the SPS dispersed and became the dominant group in all feeding areas (Figure 9B). Large proportions of adults were found to remain in the same feeding areas they used as subadults, particularly in estuarine regions where the fidelity rates reached 53 –93% (Figure 9C). Whether this high-fidelity pattern resulted from homing or resident behaviours remains uncertain because the milling technique we used did not provide the temporal resolution required to identify short-term or recent migrations. The estimated contributions from subadult to adult regions exhibited the most variable uncertainty estimates among all the mixture models we fit. Uncertainty (standard errors) in all these models depends upon the shape of the likelihood profile, which was sensitive and provided larger, and sometimes unreliable, estimates when small baseline differences between sources were combined with a small or null representation of these sources in a given mixture. The SPS is a very productive habitat (Peterson et al., 1988; Thiel et al., 2007) that has been shown to play an important nursery role for several fishes (Cubillos et al., 2001; Vargas and Castro, 2001; Landaeta and Castro, 2002; Landaeta et al., 2008). While its high productivity would favour higher growth and survival rates of early juveniles than other areas, its larger contribution to Patagonian grenadier recruitment can be also related to the advective forces (Silva and Neshyba, 1977; Strub et al., 1998; Leth and Shaffer, 2001) that might transport a larger proportion of


presence of larvae near the Magellanic Strait suggests spawning in the SMS region. Nonetheless, our results show its relative contribution to recruitment seems low for the SE Pacific stock and remains unknown for the SW Atlantic stock. Moreover, a few anomalously high d18O values (.2) observed in otolith cores from CMS and SMS adults (Figure 8) are indicative of some contribution from a fifth nursery region located in either cold areas of the Southeast Pacific or in the d18O-enriched waters of the Southwest Atlantic (Niklitschek et al., 2010). While these locations match expectations from dominant advective forces discussed above, additional sampling efforts are needed to further investigate the reproductive role of the ME, SMS and Southwest Atlantic regions, and the actual connectivity between the Southeast Pacific and Southwest Atlantic stocks. The significant differences we found in seawater d18O and d13C among sampling regions support their use as tracers of habitat-use patterns for coastal fishes along Western Patagonia. Particularly for those whose spatial and bathymetric distribution limits the use of direct tagging or tracking methods. Both estuarine and shelf water samples showed the expected enrichment of d18O with increasing salinity and decreasing temperature. The regression slope observed for salinity in estuarine samples (0.26) was similar to slope values observed in other temperate estuaries (Fairbanks, 1982; Scheurle and Hebbeln, 2003). In shelf water samples, the d18O –salinity relationship was driven by high salinity and d18O-enriched water masses, such as the EESW, exhibiting a steeper slope of 0.48, similar to the value of 0.50 calculated for subtropical oceanic waters by Xu et al. (2012). Water d13C was not significantly related to salinity or temperature, although an overall trend towards a positive relationship was observed between d13C and salinity, following theoretical and empirical expectations (Fry, 2002). This relationship was probably masked by d13C responses to ecosystem differences in productivity, carbon cycling and allochthonous carbon sources between regions (Peterson and Fry, 1987). Our results supported the assumption that otoliths incorporate d18O in direct proportion to d18O in seawater. Thus, otolith cores of juveniles collected in estuarine habitats (CE and AE) showed lower (albeit not always significant) d18O levels than those collected in d18O-enriched shelf habitats. As expected, d18O was found inversely and significantly correlated with temperature in both seawater and otoliths (Kalish, 1991a, 1991b; O’Neil and Kim, 1997; Thorrold et al., 1997b; Campana, 1999; Høie et al., 2003). Thus, we predicted d18O to be enriched in otolith cores from juveniles captured at higher latitudes (SMS region) where subsurface water temperature is 3 –48C cooler than in the SPS and NMS regions. The mean d18O observed in juveniles from the SMS region (1.27) was, however, much lower than the expected value of 1.88 (computed by us, after Kim and O’Neil, 1977) and was not significantly different from the NMS region (1.25). Although this similarity in d18O values supports the hypothesis that SMS yearlings were mainly of NMS origin, it could be also reflecting a shift in the relationship between d18O, temperature and salinity in the SMS region. Such a shift could be related to the absence of the high salinity, d18O-enriched ESSW layer in the SMS water column. Variability in otolith d13C is hard to interpret because otolith 13 d C is not in full equilibrium with seawater d13C (Kalish, 1991b; Schwarcz et al., 1998). While available studies indicate otolith carbon is obtained from both water DIC and metabolism (Radtke et al., 1996; Elsdon et al., 2010), a dominant contribution of 70 – 100% is commonly accepted for DIC sources (Kalish, 1991b; Schwarcz et al., 1998; Høie et al., 2003). However, a large and still


387


Acknowledgements The Fisheries Studies Centre (CEPES) provided samples, as well as collaboration in field activities. The Instituto de Fomento Pesquero (IFOP) facilitated sampling activities aboard several research cruises. The Instituto de Investigacioń Pesquera (INPESCA) provided seawater and otolith samples from the SPS region.

Funding This research was funded by the Chilean Fund for Scientific and Technological Development (FONDECYT No. 1111006). Research equipment was contributed by INNOVA-Chile (Grant

No. 06FC01P-40). The Fisheries Studies Centre (CEPES) supported the involvement of XV.

References Able, K. W. 2005. A re-examination of fish estuarine dependence: evidence for connectivity between estuarine and ocean habitats. Estuarine, Coastal and Shelf Science, 64: 5 –17. Acha, E. M., Mianzan, H. W., Guerrero, R. A., Favero, M., and Bava, J. 2004. Marine fronts at the continental shelves of austral South America: physical and ecological processes. Journal of Marine Systems, 44: 83 – 105. Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. In Second International Symposium on Information Theory, pp. 267– 281. Ed. by B. N. Petrov, and F. Caski. Akademiai Kiado, Budapest. Anonymous. 2012. Cuota global anual de captura para las unidades de pesquerıá de merluza de cola (Macruronus magellanicus), anõ 2013. Informe Tećnico (R. Pesq.) No. 205-2012. Subsecretarıá de Pesca y Acuicultura, Govierno de Chile, Valparaı´so, Chile. (In Spanish) Arkhipkin, A. I., Schuchert, P. C., and Danyushevsky, L. 2009. Otolith chemistry reveals fine population structure and close affinity to the Pacific and Atlantic oceanic spawning grounds in the migratory southern blue whiting (Micromesistius australis australis). Fisheries Research, 96: 188– 194. Ashford, J. R., Arkhipkin, A. I., and Jones, C. M. 2006. Can the chemistry of otolith nuclei determine population structure of Patagonian toothfish Dissostichus eleginoides? Journal of Fish Biology, 69: 708– 721. Ashford, J. R., Arkhipkin, A. I., and Jones, C. M. 2007. Otolith chemistry reflects frontal systems in the Antarctic Circumpolar Current. Marine Ecology Progress Series, 351: 249– 260. Attrill, M. J., and Power, M. 2002. Climatic influence on a marine fish assemblage. Nature, 417: 275– 278. Balbontıń, F. 2006. Ictioplancton de los canales y fiordos australes. In Avances en el Conocimiento Oceanogra´fico de las Aguas Interiores Chilenas, Puerto Montt a Cabo de Hornos, pp. 115 – 120. Ed. by N. Silva and S. Palma. Comite´ Oceanogra´fico Nacional, Pontificia Universidad Cato´lica de Valparaı´so, Valparaı´so, Chile. (In Spanish) Balbontıń, F., and Bernal, R. 1997. Distribucioń y abundancia del ictioplancton en la zona austral de Chile. Ciencia y Tecnologia Alimentaria del Mar, 20: 155 – 164. Bates, D., Maechler, M., and Bolker, B. 2012. lme4: Linear mixed-effects models using S4 classes. R package version 2.15.1. http://cran.rproject.org/web/packages/lme4/index.html (last accessed 30 May 2013). Beck, M. W., Able, K. W., Childers, D. L., Eggleston, D. B., Gillanders, B. M., Halpern, B., Hays, C. G., et al. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience, 51: 633 –641. Bernal, R., and Balbontıń, F. 2003. Distribucioń y abundancia de larvas de peces desde el Estrecho de Magallanes hasta el Cabo de Hornos, Chile. Ciencia y Tecnologıá del Mar, 26: 91– 99. Bustos, C. A., Balbontıń, F., and Landaeta, M. F. 2007. Spawning of the southern hake Merluccius australis (Pisces: Merlucciidae) in Chilean fjords. Fisheries Research, 83: 23 – 32. Campana, S. E. 1999. Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series, 188: 263– 297. Castro, L., and Landaeta, M. 2003. Variaciones diarias en la distribucioń vertical de estadios tempranos de peces, con especial referencia a merluza de cola Macruronus magellanicus, en la zona de los canales, XI regioń. In Resumenes Seminario-taller de los resultados del Programa CIMAR 9 Fiordos. Comite´ Oceanogra´fico Nacional, Valparaı´so, Chile. (In Spanish) Ce´spedes, R., Adasme, L., Reyes, H., Braun, M., Figueroa, E., Valenzuela, V., Ojeda, V., et al. 1996. Identificacioń de a´reas de reclutamiento de merluza del sur en la zona sur-austral. Informe Final Proyecto


Patagonian grenadier eggs and larvae into the SPS than into alternative nursery areas. Despite its (albeit seasonally) high productivity (Gonza´lez et al., 2011), the PES was found to be a secondary nursery area for Patagonian grenadier. However, the three PESs still contributed 22% of all sampled adults and represented the most important subadult feeding region for the stock (Figure 9). The value of the PES estuarine regions for later life-stages was also reflected by high fidelity rates that ranged between 53 and 93% of adults remaining or returning to the same PES regions they used as subadults. The main spawning areas of Patagonian grenadier and other ground species, such as Southern hake, occur in a highly dynamic system located just east of the West Wind Drift (WWD) bifurcation, within the area of influence of the Pacific Patagonia cold estuarine front (Figure 1). The location of the spawning aggregations tend to be stable from year to year (Lillo et al., 1997, 2002, 2003, 2004a, 2005a, 2005b, 2009b, 2010), but large (and not fully investigated) variability exist in both the latitudinal position of the WWD split (Gatica et al., 2009) and the magnitude and direction of the local current systems (Leth and Shaffer, 2001). Numerical simulations (Leth and Shaffer, 2001) suggest that late winter and spring dynamics would favour initial retention followed by a moderate northward and eastward transport of eggs and larvae. Thus, most larvae would be advected either into the coastal Humboldt Current or into the SPS nursery region (Figure 1). Although this average pattern is consistent with the dominant nursery role we attributed to the SPS region, stochastic, cyclic or climate-induced changes in local circulation could produce abrupt changes in transport mechanisms and, thus, in the relative contribution of different habitats to recruitment (Attrill and Power, 2002; Able, 2005). Identifying and understanding the relevance of the essential habitats that support the Patagonian grenadier and other fish populations along the Patagonian coast is an enormous task of scientific interest and relevance for management and conservation. We are just starting to understand fundamental population structure and migration patterns across this very unique configuration of habitats, which includes one of the largest estuarine systems in the world, two continental shelves (South America and Antarctica) and three oceans (Pacific, Atlantic and Southern). From a political point of view, many of these stocks are currently regulated by three or more national and international entities (Chile, Argentina, CCMLAR, UK). The strong environmental gradients and the vast distances that separate nursery, feeding and spawning areas of Patagonian grenadier and other groundfishes in this area highlights their potential to develop adaptive responses to climate variability, but also the risk that current large-scale exploitation by multiple fleets may disrupt the complex spatial dynamics required to sustain their stocks.

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