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JPR Advance Access originally published online on July 10, 2009 Journal of Plankton Research 2009 31(10):1283-1297; doi:10.1093/plankt/fbp056 This Article

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Multivariate characterization of spawning and larval environments of small pelagic fishes in the Gulf of California Gerardo Aceves-Medina1,*, Ricardo Palomares-García1, Jaime Gómez-Gutiérrez1,3, Carlos J. Robinson2 and Ricardo J. Saldierna-Martínez1

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Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Av. Ipn S/N, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23096, Mexico 2 Laboratorio de Ecología de Pesquerías, Instituto de Ciencias Del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM), Apdo. Postal 70-305, Mexico D.F. 04510, Mexico 3 Australian Antarctic Division, Department of Environment and Heritage, 203 Channel Highway, Kingston, TAS 7050, Australia

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Received on September 26, 2008; accepted on June 14, 2009 What's this?

Abstract Spawning and nursery areas of Sardinops sagax (Pacific sardine) and Engraulis mordax (northern anchovy) were characterized during early winter in the Gulf of California, using near-surface horizontal

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Multivariate characterization of spawning and larval environments of small pelagic fish... Página 2 de 2

and oblique Bongo tows. The main spawning area for anchovy was located near the islands of Tiburón and Ángel de la Guarda and for sardine near both coasts on either side of the central region of the gulf. A hydroacoustic survey showed a close spatial overlap between the distribution of small pelagic fish schools, their spawning areas and areas with the highest zooplankton biomass. Distribution and abundance of eggs and distinct larval stages showed that the nursery area is considerably larger than the spawning area. Sardines and anchovies had distinct inter-specific larval drift patterns, mostly caused by differences in the spawning locations that were influenced by regionally distinct advection caused by coastal upwelling, filaments and eddies. Abundance of eggs and early larvae of both species were closely associated with higher abundance of fucoxanthin and chlorophyll a, zooplankton biomass and the small copepod Acartia clausi. Older larvae were mostly associated with abiotic environmental variables and large-sized copepods, such as Centropages furcatus and Calanus pacificus. These results suggest the importance of sequential spatial overlap of larvae with food availability as they drift in the Gulf of California. Corresponding editor: Mark J. Gibbons

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Journal of Plankton Research -- Table of Contents (October 2009, 31 [10])

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Oxford Journals Life Sciences Journal of Plankton Research Volume 31, Number 10

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Contents: Volume 31, Number 10, October 2009

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Author] HORIZONS FEATURED ARTICLE ORIGINAL ARTICLES

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HORIZONS George B. McManus and Laura A. Katz Molecular and morphological methods for identifying plankton: what makes a successful marriage? JPR Advance Access published on July 31, 2009 J. Plankton Res. 2009 31: 1119-1129; doi:10.1093/plankt/fbp061 [Abstract] [FREE Full Text] [PDF] [Request Permissions]

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FEATURED ARTICLE Robert R. Bidigare, Fei Chai, Michael R. Landry, Roger Lukas, Cecelia C. S. Hannides, Stephanie J. Christensen, David M. Karl, Lei Shi, and Yi Chao Subtropical ocean ecosystem structure changes forced by North Pacific climate variations JPR Advance Access published on July 31, 2009 J. Plankton Res. 2009 31: 1131-1139; doi:10.1093/plankt/fbp064 [Abstract] [FREE Full Text] [PDF] [Request Permissions]

ORIGINAL ARTICLES Jagadeesan Premanandh, Balakrishnan Priya, Dharmar Prabaharan, and Lakshmanan Uma Genetic heterogeneity of the marine cyanobacterium Leptolyngbya valderiana (Pseudanabaenaceae) evidenced by RAPD molecular markers and 16S rDNA sequence data JPR Advance Access published on July 8, 2009 J. Plankton Res. 2009 31: 1141-1150; doi:10.1093/plankt/fbp055 [Abstract] [Full Text] [PDF] [Request Permissions] Jacqueline Rücker, Emilienne Ingie Tingwey, Claudia Wiedner, Charles Mbunya Anu, and Brigitte Nixdorf Impact of the inoculum size on the population of Nostocales cyanobacteria in a temperate lake JPR Advance Access published on August 7, 2009 J. Plankton Res. 2009 31: 1151-1159; doi:10.1093/plankt/fbp067 [Abstract] [Full Text] [PDF] [Request Permissions] Sébastien Personnic, Isabelle Domaizon, Télesphore Sime-Ngando, and Stéphan Jacquet Seasonal variations of microbial abundances and virus- versus flagellate-induced mortality of picoplankton in three peri-alpine lakes JPR Advance Access published on July 14, 2009 J. Plankton Res. 2009 31: 1161-1177; doi:10.1093/plankt/fbp057 [Abstract] [Full Text] [PDF] [Request Permissions] Rémy D. Tadonléké, Jérôme Lazzarotto, Orlane Anneville, and Jean-Claude Druart Phytoplankton productivity increased in Lake Geneva despite phosphorus loading reduction JPR Advance Access published on July 22, 2009 J. Plankton Res. 2009 31: 1179-1194; doi:10.1093/plankt/fbp063 [Abstract] [Full Text] [PDF] [Request Permissions] Maria Lorena Longhi and Beatrix E. Beisner Environmental factors controlling the vertical distribution of phytoplankton in lakes JPR Advance Access published on July 30, 2009 J. Plankton Res. 2009 31: 1195-1207; doi:10.1093/plankt/fbp065 [Abstract] [Full Text] [PDF] [Supplementary Data] [Request Permissions] Benjamin Genovesi, Mohamed Laabir, Estelle Masseret, Yves Collos, André Vaquer, and Daniel Grzebyk


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Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France) JPR Advance Access published on August 1, 2009 J. Plankton Res. 2009 31: 1209-1224; doi:10.1093/plankt/fbp066 [Abstract] [Full Text] [PDF] [Supplementary Data] [Request Permissions] Rodrigo Brasil Choueri, Paloma Kachel Gusso-Choueri, Maria da Graça Gama Melão, Ana Teresa Lombardi, and Armando Augusto Henriques Vieira The influence of cyanobacterium exudates on copper uptake and toxicity to a tropical freshwater cladoceran JPR Advance Access published on July 14, 2009 J. Plankton Res. 2009 31: 1225-1233; doi:10.1093/plankt/fbp058 [Abstract] [Full Text] [PDF] [Request Permissions] Elena Gorokhova and Jonna Engström-Öst Toxin concentration in Nodularia spumigena is modulated by mesozooplankton grazers JPR Advance Access published on July 22, 2009 J. Plankton Res. 2009 31: 1235-1247; doi:10.1093/plankt/fbp060 [Abstract] [Full Text] [PDF] [Request Permissions] Sónia Cotrim Marques, Ulisses Miranda Azeiteiro, Filipe Martinho, Ivan Viegas, and Miguel Ângelo Pardal Evaluation of estuarine mesozooplankton dynamics at a fine temporal scale: the role of seasonal, lunar and diel cycles JPR Advance Access published on August 1, 2009 J. Plankton Res. 2009 31: 1249-1263; doi:10.1093/plankt/fbp068 [Abstract] [Full Text] [PDF] [Request Permissions] Katherine A. Cresswell, Geraint A. Tarling, Sally E. Thorpe, Michael T. Burrows, John Wiedenmann, and Marc Mangel Diel vertical migration of Antarctic krill (Euphausia superba) is flexible during advection across the Scotia Sea JPR Advance Access published on July 30, 2009 J. Plankton Res. 2009 31: 1265-1281; doi:10.1093/plankt/fbp062 [Abstract] [Full Text] [PDF] [Request Permissions] Gerardo Aceves-Medina, Ricardo Palomares-García, Jaime Gómez-Gutiérrez, Carlos J. Robinson, and Ricardo J. Saldierna-Martínez Multivariate characterization of spawning and larval environments of small pelagic fishes in the Gulf of California JPR Advance Access published on July 10, 2009 J. Plankton Res. 2009 31: 1283-1297; doi:10.1093/plankt/fbp056 [Abstract] [Full Text] [PDF] [Request Permissions] Clear

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JOURNAL OF PLANKTON RESEARCH

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Multivariate characterization of spawning and larval environments of small pelagic fishes in the Gulf of California ´ MEZ-GUTIE´RREZ1,3, CARLOS J. ROBINSON2 GERARDO ACEVES-MEDINA1*, RICARDO PALOMARES-GARCIÁ1, JAIME GO AND RICARDO J. SALDIERNA-MARTIŃEZ1 1

DEPARTAMENTO DE PLANCTON Y ECOLOGIÁ MARINA, CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS (CICIMAR), AV. IPN S/N, COL. PLAYA PALO DE SANTA 23096, MEXICO, 2LABORATORIO DE ECOLOGIÁ DE PESQUERIÁS, INSTITUTO DE CIENCIAS DEL MAR Y LIMNOLOGIÁ, UNIVERSIDAD NACIONAL ´ NOMA DE ME´XICO (UNAM), APDO. POSTAL 70-305, MEXICO D.F. 04510, MEXICO AND 3AUSTRALIAN ANTARCTIC DIVISION, DEPARTMENT OF AUTO

RITA, LA PAZ, B.C.S.

ENVIRONMENT AND HERITAGE,

203 CHANNEL HIGHWAY,

KINGSTON, TAS

7050,

AUSTRALIA

*CORRESPONDING AUTHOR: [email protected] Received September 26, 2008; accepted in principle June 10, 2009; accepted for publication June 14, 2009; published online 10 July, 2009 Corresponding editor: Mark J. Gibbons

Spawning and nursery areas of Sardinops sagax (Pacific sardine) and Engraulis mordax (northern anchovy) were characterized during early winter in the Gulf of California, using near-surface horizontal and oblique Bongo tows. The main spawning area for anchovy was located near the islands of Tiburoń and Ańgel de la Guarda and for sardine near both coasts on either side of the central region of the gulf. A hydroacoustic survey showed a close spatial overlap between the distribution of small pelagic fish schools, their spawning areas and areas with the highest zooplankton biomass. Distribution and abundance of eggs and distinct larval stages showed that the nursery area is considerably larger than the spawning area. Sardines and anchovies had distinct interspecific larval drift patterns, mostly caused by differences in the spawning locations that were influenced by regionally distinct advection caused by coastal upwelling, filaments and eddies. Abundance of eggs and early larvae of both species were closely associated with higher abundance of fucoxanthin and chlorophyll a, zooplankton biomass and the small copepod Acartia clausi. Older larvae were mostly associated with abiotic environmental variables and large-sized copepods, such as Centropages furcatus and Calanus pacificus. These results suggest the importance of sequential spatial overlap of larvae with food availability as they drift in the Gulf of California.

I N T RO D U C T I O N Sardine and anchovy are distributed throughout the upwelling systems along the west coast of continents. Wide fluctuations in population densities and distribution have prompted considerable research efforts to understand mechanisms that influence seasonal and spatial population variability (Lluch-Belda et al., 1992; Chavez et al., 2002). Recruitment success of small pelagic fish is strongly dependent on the vulnerability of their early life stages (Hjort, 1914). This continues to

stimulate extensive research efforts to understand the physical and biological processes controlling spawning, hatching success rate, larval drift and survival rates (Cury and Roy, 1989; Bakun, 1996). The spawning environment of sardines and anchovies has been characterized in several oceanic regions, primarily using sea surface temperature (SST) and concentration of chlorophyll a obtained from field surveys and/or satellite imagery (Lluch-Belda et al., 1992; Hammann et al., 1998; Sańchez-Velasco et al., 2000;

doi:10.1093/plankt/fbp056, available online at www.plankt.oxfordjournals.org # The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]


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Oozeki et al., 2007). Pacific sardine Sardinops sagax and northern anchovy Engraulis mordax found in the California Current System tend to avoid spawning in areas with strong wind-induced upwelling, a spawning strategy that avoids massive offshore transport of eggs and larvae (Parrish et al., 1981). In contrast, in the Gulf of California, spawning is apparently coupled to regions with strong upwelling because the regional current system transports larvae from the mainland coast of Mexico to near the coast of the Baja California Peninsula (Hammann et al., 1988). Eggs and larvae of the two most abundant small pelagic fish species (S. sagax and E. mordax) are distributed throughout the Gulf of California, mostly during the cooler November– May season (Hammann et al., 1988; Green-Ruiz and Hinojosa-Corona, 1997; Hammann et al., 1998). The Pacific sardine seems to have a wide spawning area in the central gulf at SST ranging between 17 and 20.88C and the northern anchovy spawns mainly near the large islands of ´ ngel de la Guarda with SSTs between Tiburoń and A 15 and 178C (Hammann et al., 1998). Temperature is a useful indicator of the spawning habitat for small pelagic fish around the world, but less studied biological variables could have a considerable effect on the successful spawning and larval recruitment processes (Lynn, 2003; Bellido et al., 2008). Lynn (Lynn, 2003) found that, in the presence of an adequate food supply, spawning can occur outside of the typical temperature range. He also demonstrated that high densities of small pelagic fish eggs were strongly associated with high zooplankton densities; that seem to be an evolved strategy that promotes improved opportunity of a food supply for subsequent larval development, and/or adult food requirements for serial spawning. Thus, the distribution of zooplankton biomass can be used to delineate the boundaries of the spawning habitat of small pelagic fish. Young pelagic fish larvae actively feed on phytoplankton, mostly dinoflagellates (Hunter, 1981) and copepods (Arthur, 1976), but this has not been investigated as an environmental factor that promotes adult selection of the time and location of spawning. We used a multifactorial analysis to characterize the spawning and nursery environments of S. sagax and E. mordax in the Gulf of California during a period of high mesoscale activity. Our objective was to record the environmental characteristics of the range of the adults, spawning areas (eggs) and nursery areas ( preflexion, flexion and postflexion larval stages) to investigate selection of interspecific habitats of spawning, and characterize larval drift of two of the most abundant small pelagic fish species in the Gulf of California.

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METHOD The oceanographic survey was made from 19 November to 4 December 2005. We recorded multiple physical (temperature, salinity, density, depth of the thermocline, stratification of the water column and concentration of dissolved oxygen) and biological variables (concentration of photosynthetic and accessory phytoplankton pigments, zooplankton biomass and abundance of the most common copepod species) to characterize the environment of small pelagic fish in their egg and larval phase. The zooplankton trawls sampled the distribution and abundance of eggs (spawning areas) and all the larval developmental stages ( preflexion, flexion and postflexion), to characterize the environment of the nursery areas throughout their larval drift. Additionally, we simultaneously made a hydroacoustic survey to detect the distribution and relative concentration of adult small pelagic fish schools during the beginning of the spawning season.

Detection of environmental variables Satellite data from the moderate resolution imaging spectroradiometer (MODIS) provided information on SST and chlorophyll a concentration for geographical analyses (3 – 26 November 2005) (http://oceancolor.gsfc. nasa.gov/cgi/browse.pl). Vertical profiles of temperature, salinity and density were measured at 23 oceanographic stations with a CTD (Mark III, General Oceanics) from the surface to 200 m or to 10 m above the seafloor in shallower waters. Along the path of the survey (Fig. 1), the near-surface water temperature was measured every 5 s from water pumped from an inlet at the ship’s bow, at a depth of 4 m, with a CTD (Microcat Seabird) and geo-referenced with a GPS (AG160, Trimble Navigation). At each station, water samples were collected with 5-L Niskin bottles at depths of 0, 5, 10, 25, 50 and 75 m. From each Niskin bottle, the dissolved oxygen concentration was measured with an YSI oxymeter and 350 mL sea water was filtered (GF/F filters, 0.7 mm) and frozen with liquid nitrogen. Phytoplankton pigments were quantified using HPLC as described by Vidussi et al. (Vidussi et al., 1996), using the pigment response factor described by Mantoura and Repeta (Mantoura and Repeta, 1997), using commercial pigment standards (International Agency for 14C stable isotope determinations) and identified through retention times and spectral characteristics. From 11 phytoplankton pigments, we selected peridinin, fucoxanthin and chlorophyll a as useful signatures or proxies for dinoflagellates, diatoms and phytoplankton biomass,

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zooplankton captured in the 333-mm mesh net, the rest of the biomass was divided into 18-aliquots with a Folsom device to identify and count the most abundant copepod species (Palomares-Garcıá et al., 1998), then abundance was standardized to individuals 1000 m23.

Hydroacoustic survey to detect schools of adult small pelagic fish

Fig. 1. Location of the oceanographic stations (circles) and the hydroacoustic survey track (line) in the Gulf of California in November 2005.

respectively (Bustillos-Guzmań et al., 1995). Vertical density gradients were calculated to estimate the stability of the water column (SWC) (Peterson et al., 1988): SWC ¼ Ddt =Dz; where Dd2t is the density (kg m23) difference between surface and maximum sampling depth and Dz is the difference between surface and maximum sampling depth expressed in meters.

Eggs and larvae distribution and abundance We used standard oblique 333- and 505-mm mesh Bongo net trawls to collect zooplankton samples to a maximum depth of 220 m (Smith and Richardson, 1979). To collect neustonic zooplankton, near-surface trawls were made for 10 min with a 505-mm mesh cylinder–conical net trawled at 7 km h21. Each net was equipped with a digital flow meter (General Oceanics). Samples collected with the 333-mm mesh net were preserved with 4% formalin buffered with sodium borate and samples collected with the 505-mm mesh net were preserved with 96% ethanol. The zooplankton biomass (mL 1000 m23) was estimated using the displaced volume method (Beers, 1976). Sardinops sagax and E. mordax eggs and larvae were identified, sorted and counted to estimate their abundance (Moser, 1996). We identified the preflexion, flexion and postflexion stages and estimated their stage-specific abundances (individuals 10 m22). Once the fish eggs and larvae were sorted from

Echo-detection of the schools of small pelagic fish was carried out along the transects of the gulf, using a split beam echo-sounder (EY-60, Simrad) at 120 kHz with a nominal beam-width of 78; pulse duration was set at 0.1 ms. and ping rate was set at 3 pings s21. The transducer was located in the ship’s hull at a depth of 4 m. Acoustic data were collected continuously during day and night from 6 to 200 m depth, but for small pelagic fish schools the data set was analyzed only for the layer between 10 to 50 m depth. Where the depth was ,50 m, soundings were taken to 5 m above the sea floor. Ship speed during the survey was, on average, 18 km h21. Hydroacoustic data were processed and analyzed over 100 pings, corresponding to an elementary sampling distance unit of 166 m. To discriminate schools of pelagic fish from other acoustic objects in the echo-integration analysis, the minimum backscattering volume (Sv) (MacLennan et al., 2002) was set at –55 dB and the maximum at –20 dB, similar to the range of Sv values obtained for small pelagic fish adults (Robinson et al., 2007). At specific locations, where the echo-sounder detected dense scattering layers, we used two methods to identify the organisms responsible for the signals in situ: (i) Isaacs-Kidd mid-water net (mouth 2 2 m2) trawls and (ii) a total 31 h of observations at 61 sites with a video camera (Multi SeaCam 1060, Deep Sea Power & Light) (data not shown).

Data reduction Standardized abundance (x) of ichthyoplankton and copepod species were transformed to log (x þ 1). Abiotic (SST, mean temperature of the mixed layer, SWC and near-surface oxygen concentration) and biological environmental conditions (chlorophyll a, fucoxanthin, peridinin, and abundance of numerically dominant copepod species) were used to perform canonical correspondence analysis (CCA) with PC-ORD v.4 software (McCune and Mefford, 1999). The standard error was calculated (sX ¼ s/n 1/2) for each environmental variable and transformed with (x – X)/sX; where x is the variable value and X is the average value of this particular variable. The CCA is an efficient multivariate statistical technique to test whether

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the distribution and abundance of species are related to environmental variables measured in the field (McCune et al., 2002). We did a separate CCA for Bongo and neustonic samples because they had significant quantitative differences in abundance, relative composition and biomass of zooplankton species.

R E S U LT S Environmental conditions The warmest near-surface water (4 m depth) occurred south of the study area (26.58N) and the coldest area along the mainland coast between Puerto Lobos (308N) and south Guaymas bay (27.58N) (Fig. 2a). The MODIS SST of 23 November 2005 (Fig. 2b), and the 4-m measurements, showed two plumes of cold water originating south of Isla Tiburon. These two plumes had high concentrations of chlorophyll a (MODIS image of 26 November 2005; Fig. 3b). Vertical profiles of temperature and density, measured along three transects oriented perpendicular to the coast, showed upwelling of cold, high-density water (Figs 2c and d) with low concentrations of dissolved oxygen along the coast from south of Guaymas to south of Isla Tiburoń (Fig. 3a). The thermocline was considerably shallower along the mainland coast than along the peninsula. Eddies appear clearly in temperature (Fig. 2b) and chlorophyll a satellite imagery (Fig. 3b). Integrated measurements of water column chlorophyll a ranged between 8.4 and 113 g m22 (Fig. 4a). High concentrations of fucoxanthin (.40 g m22) occurred north and south of Isla Tiburoń and west of Guaymas (Fig. 4b), which indicates the dominance of diatoms corresponding to high concentrations of chlorophyll a from satellite imagery. Concentrations of peridinin were low (,2 g m22), which corresponds to concentrations of dinoflagellates, except for relatively high concentrations north and south of Isla Tiburoń and along the southeastern coast of the gulf (Fig. 4c). The higher zooplankton biomass detected along the continental coast (north and south of Isla Tiburoń) and close Bahıá La Paz associated with the upwelling areas where high photosynthetic pigment concentrations were detected (Fig. 3c).

Copepod abundance Copepod-relative abundance, including only species with values .1%, is shown in Table I. Using an exploratory CCA, only Acartia clausi, Centropages furcatus and Calanus pacificus, had significant statistical correlation values (20.6 , r . 0.6, P , 0.01). Thus, we included

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only these three copepod species in further multivariate statistical analyses. The neritic copepod A. clausi was widely distributed along the gulf, with higher concentrations along the mainland coast between Isla Tiburoń and Bahıá Guaymas (Fig. 4d). The highest C. furcatus concentrations were detected along the west side of the central part of the gulf and near Topolobampo (Fig. 4e). The highest concentrations of C. pacificus occurred in the central part of the gulf, reaching from Guaymas on the mainland to Bahıá Concepcioń on the peninsula side (Fig. 4f ).

Ichthyoplankton abundance The most abundant small pelagic fish larvae collected with Bongo nets were E. mordax (505-mm mesh ¼ 79%; 333-mm mesh ¼ 68%) and S. sagax (505-mm mesh ¼ 20.7%; 333-mm mesh ¼ 32%). Round herring (Etrumeus teres) were present in low densities (505-mm mesh ¼ 0.3%; 333-mm mesh ¼ absent). A considerably different composition of larvae was collected in near surface trawls, where S. sagax represented 92% and E. mordax represented the remaining 8% (Table II). Eggs were consistently present in the following proportions, regardless of the plankton net used: S. sagax (.86%) and E. mordax (,14%) (Table II). Distribution of E. mordax eggs (Bongo and surface trawls) indicated that the main spawning during November 2005 occurred mostly along the northeast coast near Isla Tiburoń, but also around the coast of Isla Ańgel de la Guarda (Fig. 5). Also, the 505-mm mesh bongo net showed a spawning area near Guaymas. Engraulis mordax preflexion larvae had a wider distribution than eggs, likely related to currents along both coasts concentrating mainly near Punta Trinidad (278450 N and 1128300 W) along the peninsular coast, north of the big islands and near Guaymas (Fig. 6). Flexion stage larvae (from Bongo nets) had a wide distribution north of the big islands, but in the central part of the gulf they were distributed mainly along the peninsular coast. Flexion stage larvae, collected with the neuston net, were abundant along the continental coast of the central region of the gulf. Postflexion stage larvae were found in low densities mainly north of the big islands, but also near Bahıá Concepcioń, and north of Guaymas (Fig. 6). Spawning areas of S. sagax, indicated by the concentration of sardine eggs, were located mainly near Guaymas and north of Bahıá Concepcioń. Some spawning areas were detected north of Isla Tiburoń (Fig. 5). Preflexion and flexion stage larvae were concentrated north of the big islands and had a wider distribution than eggs, indicating a dynamic drift

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Fig. 2. (a) In situ continuous measurement of temperature at depth of 4 m; (b) Aqua/MODIS SST satellite imagery (23 November 2005); (c) vertical temperature distribution and (d) vertical density distribution along transects 3, 4 and 5 in the Gulf of California during November 2005.

(Fig. 7). In the central region of the gulf, preflexion and flexion stages had a more oceanic and southern distribution than sardine eggs. Postflexion stage larvae collected with bongo nets had a smaller distribution

area, mainly located around the big islands, but postflexion stage collected from surface tows were more abundant near Isla Carmen off the peninsular coast (Fig. 7).

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Fig. 3. (a) Percentage of oxygen saturation; (b) Aqua/MODIS satellite imagery of chlorophyll a on 26 November and (c) total zooplankton biomass in the Gulf of California during November 2005.

Hydroacoustics The scattering volume (Sv) recorded along transects is shown in Fig. 8. During the day, dense schools of fish were detected in deep waters within the depth range of detection (10– 50 m). During the night, the scatterers were distributed in dispersed shoals and detected near the surface. Although adult sardines and anchovies certainly avoid the Isaacs-Kidd midwater net (none were collected); underwater video analysis showed that Pacific sardines and northern anchovies were present in regions where Sv was high (Fig. 8). Most of the schools were located in the region of the big islands and south of Isla Tiburon, where they overlapped with E. mordax eggs, while moderate densities of small pelagic fishes were found near Santa Rosalıá, associated with a high density of S. sagax eggs (Fig. 8).

Data analyses Canonical correspondence analysis from the bongo net samples explained 45.2% of the cumulative variance along the three main axes (Table III). Axis 1 (explained variance ¼ 20.5%) detected an intraspecific ontogenetic segregation (egg to larvae postflexion stage) of E. mordax and S. sagax, probably caused by abundance differences among developmental stages, but most likely caused by drifting larvae, as seen in the negligible overlap of distribution patterns among distinct life stages (Fig. 9a). Axis 1 had a high correlation with several food sources, such as concentration of fucoxanthin (r ¼ 20.823) and chlorophyll a (r ¼ 20.728), abundance of the copepod A. clausi (r ¼ 20.670) and zooplankton biomass (r ¼ 20.56) shown in Table IV. Axis 2 explained 14.2%

of the total variance (Table III), with species segregation of E. mordax (upper side) and S. sagax (lower side) of the dispersion diagram (Fig. 9a). Axis 2 was also highly associated with SWC (SWC ¼ 20.637) and abundance of the copepod C. furcatus (r ¼ 0.739) shown in Table IV. The explained variance of Axis 3 was 10.4%, which showed a gradient driven by the abundance of the larger larvae ( postflexion stage) of both fish species (Fig. 8b, Table III). This axis was also associated with the abundance of the copepod C. pacificus (r ¼ 20.648) shown in Table IV. In general, dispersion diagrams show that eggs and young larvae were more correlated with food sources and older larvae were more correlated with SWC and larger copepods such as C. pacificus (Fig. 9a and b). Canonical correspondence analysis of neustonic samples indicated that eggs and larvae of anchovy and sardine had distinct geographical distributions (Fig. 10). However, intraspecific, ontogenetic segregation of fish larvae was not as clear as in the CCA using Bongo net samples (Fig. 10). Axis 1 explained 29.4% of the total variance (Table III), which was highly correlated with the distribution and abundance of the early stages of S. sagax. Fucoxanthin concentration (r ¼ 0.97), average temperature of the mixed layer (r ¼ 0.93) and concentration of chlorophyll a (r ¼ 0.88) had the highest correlations with Axis 1 (Table IV). Axis 2 explained 19.1% of the total variance (Table III). Eggs and postflexion larvae of E. mordax showed intraspecific segregation of the larval stages (Fig. 10), which was associated with gradients of concentration of dissolved oxygen (r ¼ 0.73) and SWC (r ¼ 0.61) (Table IV). No significant correlations were detected among environmental variables and fish abundance in Axis 3 (Table IV).

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Fig. 4. Integrated concentration from the water column (in g m22) of: (a) chlorophyll a as a proxy for bulk of phytoplankton; (b) fucoxanthin as a proxy for diatoms; (c) peridinin as a proxy for dinoflagellates. Distribution and abundance (individuals 1000 m23) of three copepods: (d) Acartia clausi; (e) Centropages furcatus and (f ) Calanus pacificus in the Gulf of California during November 2005.

DISCUSSION Seasonal patterns in the Gulf of California have been characterized by a 4-month warm period (July through October) and a 5-month cool period (December through April), with 1 – 2-month transition periods between them (Soto-Mardones et al., 1999). Peak

spawning of sardine and anchovy occurs during the cool season (Hammann et al., 1988; Green-Ruiz and Hinojosa-Corona, 1997) when primary productivity is enhanced by strong tidal mixing around the big islands (especially through the Canal de Ballenas) and the wind-driven coastal upwelling along the mainland coast

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Table I: Total abundance, mean abundance for the positive stations and relative abundance (%) of the most abundant copepod species found in the Gulf of California during November 2005 collected with 23 bongo oblique trawls with net mesh of 333 mm

Copepod species Pseudocalanus elongatus Rincalanus nasutus Acartia clausi Centropages furcatus Subeucalanus mucrunatus Calanus pacificus Other copepod species Total copepods

Total abundance org..1000 m23

Positive stations

Mean abundance + SD) org..1000 m23 (+

Relative abundance (%)

1 445 766 1 127 266 369 755 288 096 91 352 84 741 5 531 851 8 938 827

4 14 19 22 3 19

361 441 (+324 644) 80 519 (+92 217) 19 460 (+61 581) 13 095 (+14 486) 30 450 (+42 161) 4460 (+11 855)

16 13 4 3 1 1 62 100

Table II: Total abundance (org..m22), relative abundance (%), number of positive stations and mean abundance for the positive stations of egg and fish larvae of S. sagax, E. mordax and E. teres collected in the Gulf of California during November 2005 with 23 bongo oblique trawls with net mesh of 505 mm (B505) and 333 mm (B333) and surface net trawls (SN) Fish eggs Species Sardinops sagax Total abundance Relative abundance No. positive stations Mean abundance Standard deviation (+) Engraulis mordax Total abundance Relative abundance No. positive stations Mean abundance Standard deviation (+) Etrumeus teres Total abundance No. positive stations

Fish larvae

B505

B333

SN

163 85 5 33 48.2

11 999 99 6 1996 4852.4

215 92 2 108 31.8

522 20 11 48.7 69.7

4959 32 12 413 1172.8

125 92 10 40.7 12.5

28 15 4 6.8 6.9

170 1 6 28.4 38.2

18 8 6 3 4.9

2064 79 16 129 179.2

10 506 68 19 552.9 684.7

11 8 10 1.1 1.3

0 0

0 0

0 0

26 1

(Hidalgo-Gonza´lez and Alvarez-Borrego, 2004). However, our ichthyoplankton data showed that spawning events of these two species occurred in November, considered to be a warm-to-cold transition period. Colder water was located south of Isla Tiburon, where advection of surface layers was directed towards the middle gulf. The cold filaments and jets usually interact with wind-driven coastal upwelling and cyclonic eddies in the central part of the gulf (Pegau et al., 2002). During the cool season, strong vertical mixing and continuous flow of nutrient-rich water favor the numerical dominance of diatoms in the central gulf (Thunell et al., 1994; Gaxiola-Castro et al., 1999; Garcıá-Pa´manes and Lara-Lara, 2001). We found that fucoxanthin had the high concentrations of carotenoid that closely co-varied with the concentration of chlorophyll a. Thus, diatoms are likely responsible for the most significant

B505

B333

SN

0 0

0 0

changes of phytoplankton distribution and biomass, and comprise the largest component of primary production during the warm-to-cool transition period. Areas of maximum abundance of adult small pelagic fishes and spawning activity of sardine and anchovy were located in the central region of the gulf. However, the highest densities of sardine eggs were restricted to upwelling cool water (,188C at depth of 4 m) south of Isla Tiburon, overlapping the areas with the highest zooplankton biomass, while the center of spawning of sardine was near the upwelling area near Bahıá de Guaymas and the peninsula’s central east coast, with cool water (18– 218C at depth of 4 m). We found negligible geographical overlap between the highest densities of sardine and anchovy eggs and each larval developmental stage. Preflexion larvae were collected near the main spawning area and older stages

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Fig. 5. Distribution and abundance (eggs 10 m22) of anchovy Engraulis mordax and sardine Sardinops sagax eggs collected with oblique bongo trawls of 333- and 505-mm mesh and surface trawls in the Gulf of California during November 2005.

were more widely distributed, particularly throughout the central gulf, but with considerably lower densities than the eggs. The pattern of considerably lower abundance as larvae of both species develop was consistent throughout the survey area, but most pronounced for sardine. This was attributed to high mortality of young

larvae, but also with greater avoidance of nets by older fish larvae (Smith, 1985). In any case, ontogenetic segregation suggests that an area with greater abundance of older larvae, rather than an area of high egg density, is the best indicator of the most favorable nursery areas (Smith, 1985; Moser and Pommeranz, 1999).

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Fig. 6. Distribution and abundance (individuals 10 m22) of E. mordax larvae collected with oblique 333- and 500-mm mesh bongo trawls and surface tows in the Gulf of California during November 2005.

Since spawning and nursery habitats were spatially uncoupled, current speed and direction should disperse the eggs and larvae from the spawning grounds to different regions surviving in enough numbers only in adequate nursery areas (Castro et al., 2000; Sańchez-Velasco et al., 2004). During the warm –cold transition period (November), the spawning areas of both species were mostly located along the eastern side of the gulf and the nursery areas were along the western side of the gulf. Temperature and chlorophyll a satellite imagery together with information on the distribution and abundance of eggs indicated that spawning areas of

both species were coupled with westward transport of cold water plumes that are hydrodynamically connected to eddies that promote marked gradients in environmental conditions during egg and larval drift. Thus, active circulation provides a favorable combination of factors that retain eggs and larvae in the highly productive central region between the big islands and Isla del Carmen (Hammann et al., 1998). The habitat of older sardine larvae was frontal areas with active mesoscale eddies and high availability of copepod prey, mostly C. furcatus and C. pacificus, while in near-shore upwelling areas, where chlorophyll a, A. clausi

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Fig. 7. Distribution and abundance (individuals 10 m22) of S. sagax larvae collected with oblique 333- and 500-mm mesh bongo trawls and surface trawls in the Gulf of California during November 2005.

and zooplankton biomass was highest, only sardine eggs were consistently observed. Highly dynamic regions, such as the upwelling zones in the Gulf of California, were used as feeding and spawning areas by adults. In these areas, a frontal effect becomes apparent with an accumulation of biomass (Raid, 1989). Although phytoplankton and zooplankton biomass is usually higher in frontal areas (Go´mez-Gutie´rrez et al., 2007; Robinson et al., 2007), peak abundance of sardine flexion and postflexion larvae occurred in transitional waters linked to low zooplankton biomass regions, but characterized by the highest densities of two copepod species and greater

water column stability. Uehara et al. (Uehara et al., 2005) reported that sardine larvae in areas with upwelling have low growth rates associated with lower feeding rates, supposedly caused by excessive turbulence and disruption of the thermocline (McClatchie et al., 2007). The anchovy is an opportunistic species that rapidly occupies the niche vacated by other small pelagic fish species, particularly sardines (Chavez et al., 2002). In the big island region, ichthyoplankton collected in previous studies was dominated by anchovy during both transition periods, sardine in the cool season (Green-Ruiz and Hinojosa-Corona, 1997) and the thread herring

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Fig. 8. Distribution and abundance of adult small pelagic fish expressed in scattering volume (Sv) inferred from the hydroacoustic survey in the Gulf of California in November 2005.

Table III: Axis eigenvalues and explained variance (%) from the canonical correspondence analysis calculated using the oblique and surface trawls for the period November 2005 Oblique trawls

Eigenvalue Explained variance (%) Accumulated variance (%)

Surface trawls

Axis 1

Axis 2

Axis 3

Axis 1

Axis 2

Axis 3

0.323 20.5

0.224 14.2

0.164 10.4

0.831 29.4

0.540 19.1

0.289 10.2

20.5

34.8

45.2

29.4

48.4

58.7

(Opisthonema spp.) in the warm season (Avalos-Garcıá et al., 2003). However, we found that sardine was more abundant than anchovy during the warm– cold transition leading us to propose the hypothesis that anchovy larvae are present in the gulf only when concentrations of sardine larvae in shelf waters are low. Another scenario is that each species occupies a different position in the water column and was not properly sampled. However, this is unlikely because integrated Bongo net zooplankton samples should have relatively similar species abundances if they do not have interspecific geographical differences in the spawning and nursery areas. Although abundance of sardine eggs and larvae were high in surface trawls, anchovy larvae were more frequent and abundant in the oblique bongo trawls. This agrees with previous observations that sardine larvae distribute mostly in the mixed layer (above the thermocline) and sardine eggs are released in denser aggregations close to the surface, where young larvae seasonally inhabit this neustonic environment (Schwartzlose et al., 1999).

Fig. 9. Canonical correspondence analysis dispersion diagram of the abundance data of egg, preflexion ( pf ), flexion (fl) and postflexion ( po) larval stages of E. mordax (Em) and S. sagax (Ss) collected with 333and 505-mm mesh bongo nets of: (a) Axis 1 vs. Axis 2; (b) Axis 1 vs. Axis 3. SWC, stability of the water column.

Multivariate analyses indicated that many environmental variables play a considerable role in spawning and nursery locations. We found that spawning is not restricted to colder upwelling areas (,188C SST) along the mainland coast, but at least in November 2005 there was more activity in the central gulf (18 – 218C SST). The distribution of eggs suggests that spawning occurred where pronounced gradients related to mesoscale anticyclonic eddies were present and the distribution patterns of sardine and anchovy eggs and preflexion stage larvae were retained in the central gulf. Egg and larval stage segregation was detected with the CCA; the distribution maps of each developmental stage suggest drift from the mainland coast (main anchovy spawning areas) towards the peninsular coast (highest abundance of preflexion and flexion larvae).

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Table IV: Correlation values for environmental variables of canonical correspondence analysis for oblique and superficial trawls during November 2005 Oblique trawls Variable

Axis 1

Chlorophyll a Fucoxanthin Peridinin Centropages furcatus Acartia clausi Calanus pacificus SWC TML O2 ZB SST

2 0.728 0.171 20.251 0.878 0.447 0.031 20.823 0.823 20.007 20.159 0.967 0.210 0.008 20.604 0.604 0.228 20.158 0.458 0.456 0.435 20.226 0.739 20.018 NA NA NA 20.670 0.670 20.042

Axis 2

Surface trawls Axis 3

Axis 1

0.146 0.238 NA 0.413 20.648 0.648 NA

Axis 2

NA NA

Axis 3

NA NA

0.360 20.637 0.637 0.290 20.512 0.512 20.606 0.606 0.493 0.452 0.370 0.132 20.932 0.932 0.128 20.064 0.288 0.458 20.283 0.361 0.725 20.003 20.560 0.560 0.354 20.611 0.611 NA NA NA 20.920 0.920 0.082 20.033

Bold numbers are the highest correlation values for each axis. SWC, stability of the water column; TML, temperature average of the mixed layer; O2, dissolved oxygen in surface; ZB, zooplankton biomass; SST, sea surface temperature; NA, no data available.

Fig. 10. Canonical correspondence analysis dispersion diagram of the abundance of egg (eg), preflexion ( pf ), flexion (fl) and postflexion ( po) larval stages of E. mordax (Em) and S. sagax (Ss) collected with surface trawls. SWC, stability of the water column; TML, average temperature of the mixed layer; O2, dissolved oxygen concentration at the surface; SST, sea surface temperature.

Linking spawning areas to cold jet filaments and eddies (observed from satellite imaginary) suggest that young larvae drifting towards warmer areas have increased growth rates and a shorter planktonic larval phase. This transport also moves larvae to areas with greater water column stability and food availability, which enhances successful capture of prey (Lasker, 1981). Further, larval

drift seems to be mainly driven by cyclonic and anticyclonic eddies that move larvae from the eastern side of the gulf to the western side, but at the same time, disperse larvae over large areas where they survive and are detectable in favorable habitats, in this case the northern and central areas of the Gulf of California. Several studies have shown the temporal and geographical association between the highest zooplankton biomass and the small pelagic fish spawning areas in a number of ecosystems such as southern Australia (Ward et al., 2006), Mediterranean Sea (Maynou et al., 2008) and the California Current region (Lynn, 2003). Our conclusions are consistent with McClatchie et al. (McClatchie et al., 2007) observations that sardine larvae (S. sagax) at South Australia were absent or in low numbers in regions with active upwelling events, but they were abundant in regions with high density of potential prey and high water column stability. These observations support the hypothesis of the stable ocean (Lasker, 1981), which suggest that survival and recruitment of early larvae depends on suitable size and concentration of food associated with a stable water column. However, survival of early larvae seems to be conditioned by a combination of physical and biological characteristics, and evidence for the correlation between water column stability and larval abundance is limited (McClatchie et al., 2007) and also does not always agree with the theoretical framework (Cury and Roy, 1989). Our results support the hypothesis that small pelagic fish spawning areas are more strongly correlated with high zooplankton biomass than with physical environmental variables (Lynn, 2003; Bellido et al., 2008). On the basis of spatial segregation of larval stages, including the oldest larvae not located in the areas with the highest phytoplankton and zooplankton biomass, we conclude that the overlap of spawning areas with high zooplankton biomass is not related to sufficient supplies of good quality food for oldest larvae, but with good quality and quantity of food for adults during spawning. Sardine and anchovy larvae had different interspecific drift patterns, mostly caused by differences their spawning areas, which was influenced by regionally distinct advection caused by coastal upwelling, filaments and eddies.

AC K N OW L E D G E M E N T S We thank Francisco E. Hernandez-Sandoval for his valuable technical assistance with the HPLC analysis, the crew of the R/V El Puma, graduate students and staff from ICMyL-UNAM, UABCS and CICIMAR for

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their cooperation during field work. Editorial suggestions were provided by Ira Fogel.

FUNDING G.A.M., J.G.G. and C.J.R. were supported by SNI fellowships and G.A.M., J.G.G., R.S.M. and P.G.R. were supported by COFAA-IPN and EDI-IPN grants. This project was partially funded with grants from Centro Interdisciplinario de Ciencias Marinas-IPN, CONACYT 2004-144 and 2005-117, CONABIO, and Instituto de Ciencias del Mar y Limnologıá from the Universidad Nacional Autońoma de Me´xico.

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