Fish larvae in Bahía Sebastián Vizcaíno and the adjacent oceanic region , Baja California , México

The taxonomic composition of the fish larvae assemblage of Bahía Sebastián Vizcaíno and the adjacent oceanic region is presented based on oblique zooplankton hauls made during 12 oceanographic surveys between fall 1997 and fall 2000. In total, 186 taxa representing 71 families were collected. Myctophidae, Phosichthyidae, and Engraulidae were the most abundant during winter and Myctophidae, Merlucciidae, and Bathylagidae during spring. In summer and fall Phosichthyidae and Myctophidae were the most abundant. During 1999 and 2000, seasonal variability was identified in the area by the fish larvae composition, defining winter and fall as a low diversity period and spring and summer as a high diversity period. Interannual variability was detected with an El Niño event, with higher larval abundances of tropical and subtropical taxa, and a La Niña event, with high abundances of larvae of Engraulis mordax. Introduction Bahía Sebastián Vizcaíno (BSV) is on the Pacific coast of México in the middle of the Baja California Peninsula (Figure 1). It has been selected by the Mexican Government as a Priority Marine Area because of its high richness in plant and animal species. The study area is in a transitional zone under the influence of the California Current (Tsuchiya 1982), where the biota of three major water masses converge (Central Pacific Water Mass, Eastern Tropical Pacific Water Mass, and Subarctic Water Mass). Although the physical and biological dynamics of BSV and its oceanic vicinity have been described by several authors (Wyllie 1961; Bakun and Nelson 1977; Husby and Nelson 1982; Amador– Buenrostro et al. 1995), BSV-specific ichthyofaunal studies are scarce and only one work listed a total of 59 species, 50 genera, and 36 families (De la Cruz–Agüero et al. 1996). Several studies of fish larvae include BSV as a small area in the vast California Current region where most of the work is focused on commercially important species (Ahlstrom 1965; Loeb et al. 1983; Moser et al. 1987; 1993; 1994). Some studies have been made to characterize the composition and species abundance of ichthyoplankton of California and the Baja California Peninsula (Moser and Smith 1993; Funes–Rodríguez et al. 1995; 1998a; 1998b; 2000; 2002; 2006). Fish larvae assemblages reflect the oceanographic complexity of the California Current Region with subarctic–transitional, eastern tropical, and central water mass components, which are affected by the seasonal and interanual variability modifying their composition and boundaries (Moser et al. 1987; Moser and Smith 1993). Off the west coast of Baja California seasonal variations in species distribution and abundance have been related to changes in flow within the California Current System (Funes–Rodríguez et al. 2002). Even though there are a considerable number of ichthyoplankton studies along the Pacific coast of California and Baja California, fish larval dynamics in BSV and its oceanic vicinity have been scarcely studied. Our goal is to analyze the changes in the structure of the larval assemblages associated with the seasonal and interannual variability that occurred in the area during the sampling period. Materials and methods The study area is between 26°43’ and 29°04’ N, and 114°29’ and 115°58’ W (Figure 1). It is an extensive shelf area of approximately 36,000 km over the Pacific Plate and consists of a wide platform and an ocean floor of igneous rock. Mudflats, coastal dunes, and three lagoons (Manuela, Guerrero Negro, and Ojo de Liebre) are Check List 2007: 3(3) ISSN: 1809-127X


Introduction
Bahía Sebastián Vizcaíno (BSV) is on the Pacific coast of México in the middle of the Baja California Peninsula (Figure 1).It has been selected by the Mexican Government as a Priority Marine Area because of its high richness in plant and animal species.The study area is in a transitional zone under the influence of the California Current (Tsuchiya 1982), where the biota of three major water masses converge (Central Pacific Water Mass, Eastern Tropical Pacific Water Mass, and Subarctic Water Mass).
Although the physical and biological dynamics of BSV and its oceanic vicinity have been described by several authors (Wyllie 1961;Bakun and Nelson 1977;Husby and Nelson 1982;Amador-Buenrostro et al. 1995), BSV-specific ichthyofaunal studies are scarce and only one work listed a total of 59 species, 50 genera, and 36 families (De la Cruz-Agüero et al. 1996).Several studies of fish larvae include BSV as a small area in the vast California Current region where most of the work is focused on commercially important species (Ahlstrom 1965;Loeb et al. 1983;Moser et al. 1987;1993;1994).Some studies have been made to characterize the composition and species abundance of ichthyoplankton of California and the Baja California Peninsula (Moser and Smith 1993;Funes-Rodríguez et al. 1995;1998a;1998b;2000;2002;2006).Fish larvae assemblages reflect the oceanographic complexity of the California Current Region with subarctic-transitional, eastern tropical, and central water mass components, which are affected by the seasonal and interanual variability modifying their composition and boundaries (Moser et al. 1987;Moser and Smith 1993).Off the west coast of Baja California seasonal variations in species distribution and abundance have been related to changes in flow within the California Current System (Funes- Rodríguez et al. 2002).
Even though there are a considerable number of ichthyoplankton studies along the Pacific coast of California and Baja California, fish larval dynamics in BSV and its oceanic vicinity have been scarcely studied.Our goal is to analyze the changes in the structure of the larval assemblages associated with the seasonal and interannual variability that occurred in the area during the sampling period.

Materials and methods
The study area is between 26°43' and 29°04' N, and 114°29' and 115°58' W (Figure 1).It is an extensive shelf area of approximately 36,000 km 2 over the Pacific Plate and consists of a wide platform and an ocean floor of igneous rock.Mudflats, coastal dunes, and three lagoons (Manuela, Guerrero Negro, and Ojo de Liebre) are there.Two channels, Kellet Channel (14.8 km wide and 40 to 45 m deep) and Dewey Channel (7.4 km wide and 25 to 30 m deep) are open to the ocean in the southeast of the bay.Three islands are present, forming the Isla Cedros complex: Cedros, Natividad, and San Benito (Arriaga-Cabrera et al. 1998).The mean annual temperature is 18 to 20 ˚C, rainfall is minimal during winter, and no sources of freshwater empty into the bay (Wyllie 1961).(summer), and October 2000 (fall).A basic plan of 22 stations (an average of 20), both coastal and oceanic, were sampled in the area during this study.Zooplankton collections were made according to Smith and Richardson (1977) using standard CalCOFI procedures (Kramer et al. 1972).Bongo nets with 0.61-m mouth diameter, 3-m length, and 505-µm mesh with a flow-meter installed in each mouth were used to collect pairs of samples.Only one sample of each pair was used in this study.At each station the sea surface temperature (SST) and sea surface salinity (SSS) were recorded with a Seabird CTD.
The zooplankton biomass was measured with the displaced wet-volume method (Beers 1976).The total ichthyoplankton was sorted out and counted.Fish larvae were preserved in 4 % Formalin buffered with sodium borate and identified to the lowest taxonomic level possible using mainly Moser (1996).The number of larvae was standardized to 10 m 2 of sea surface (Smith and Richardson 1977).Adult habitat and zoogeographic affinity information of the identified taxa were obtained from Eschmeyer et al. (1983) and Froese and Pauly (2000).Voucher specimens of all species were cataloged and deposited in the Ichthyoplankton Collection at CICIMAR-IPN.Community diversity (H') and equitability (J) were estimated with Shannon's Index (Shannon and Weaver 1949).

Results
Mean SST values were lowest in winter and spring and highest in summer and fall (Figure 2a).Fall 1997 had the highest SST values (mean 24.9 ºC) and was remarkably higher than fall 1998, 1999, and 2000 (mean SST 19.6, 19.8, and 20.3 ºC, respectively) (mean SST 19.6, 19.8, and 20.3 ºC, respectively).During winter 1998, the mean SST (19.2 ºC) was remarkably higher than in winter 1999 and 2000 (15.7 and 16.5 ºC, respectively).Summer 1998 had the highest mean SST value for this season (21.1 ºC compared to 18.7 and 18.6 ºC in summer 1999 and 2000).Spring 1999 had the lowest SST (mean 14.7 ºC), whereas spring 2000 had a mean SST of 16.0 ºC.
The highest SSS values were measured during fall 1997 and winter 1998 (Figure 2a), whereas the mean SSS values were more uniform in the other seasons (between 33.6 and 33.8) (Figure 2a).
The annual mean zooplankton volume was lower during fall, except for fall 1997 where values were high for this season, followed by higher than normal values for winter in 1998.Spring 1999 and 2000 had the highest values for each year (Figure 2b).Higher larval abundances coupled with higher numbers of taxa were found during fall 1997 and winter and summer 1998 (Figure 2c).Lower larval abundances were measured during 1999, but the number of taxa was similar between seasons during 1999 and 2000.The highest larval abundance was found during summer 1998 (17,840 larvae/10 m 2 sea surface) and the largest number of taxa was measured during fall 1997 (Figure 2c).The lowest larval abundance and a comparatively low number of taxa were collected during fall 2000 (Figure 2c).Fish larvae belonging to 186 taxa of 71 families were identified (Table 1).Of these, two were identified to the family level, 26 to the genus level, and 158 to the species level.Larvae identified to the family and-or genus level were distinguished with the notation "type" followed by a number to denote types.These larvae could not be identified to the species level because of the lack of larval descriptions or damage to the larvae.
Diversity (H') values were particularly high during spring and summer 1999 and 2000, contrasting with the low H' values obtained during summer 1998, which resemble the low H' values of winter 1998 and 2000 (Figure 2d).Fall H' values were similar during 1998-2000, but higher in 1997 (Figure 2d).The lowest equitability (J) values were obtained during fall 1997 and 1998 and winter 1998, whereas during the rest of the sampling period J values were similar (Figure 2d).
During winter five taxa comprised at least 80 % of the total larval abundance in 1998 with Vinciguerria lucetia being the most abundant species, 11 taxa comprised ≥ 80 % of the abundance during 1999 with Diogenichthys laternatus as the most abundant, and four taxa in 2000 represented ≥ 80% of the abundance with larvae of the coastal pelagic species Engraulis mordax being the most abundant (Table 1).Eleven and nine taxa contributed with ≥ 80 % of the abundance in spring 1999 and 2000 respectively, with Merluccius productus (1999) and Sardinops sagax (2000) as the most abundant species (Table 1).Two species accounted for ≥ 80 % of the larval abundance during summer 1998 with V. lucetia being the most abundant species as it was in summer 1999, when 12 species accounted for ≥ 80 % of the abundance (Table 1).In summer 2000 five species accounted for ≥ 80% of the abundance and Triphoturus mexicanus was the most abundant species (Table 1).In fall V. lucetia was the most abundant species, except for fall 2000 when T. mexicanus was the most abundant one (Table 1).Eighty percent of the total larval abundance during fall was composed of seven, five, eight, and six species during 1997, 1998, 1999, and 2000, respectively (Table 1).Table 1.Taxonomic composition of fish larvae collected between September 1997 and October 2000 in Bahía Sebastián Vizcaíno and the adjacent oceanic region.Abundance is given in larvae/10 m 2 of sea surface.Abundance of taxa that cumulatively contributed with 80 % or more of total abundance by cruise are underlined.1998 1999 2000 1999 2000 1998 1999 2000 1997 1998 1999 2000 Ophichthidae  1998 1999 2000 1999 2000 1998 1999 2000 1997 1998 1999  Larvae of commercially important species were among the most abundant during all seasons along with the mesopelagic species, V. lucetia, several myctophids, and demersal taxa such as Sebastes (Table 1).Except for summer 1998, larvae of S. sagax were among the most abundant species year round (Table 1).Larvae of E. mordax, present in all seasons, were most abundant during winter and spring (Table 1).Scomber japonicus larvae were among the 10 most abundant taxa during winter 1998, spring 1999 and 2000, and during summer 1999 and 2000 (Table 1).
Larvae of mesopelagic (> 20 % of all taxa) and demersal (usually > 10 % of all taxa) dwelling adults were well represented during all seasons (Figures 3a and b), whereas coastal pelagic and epipelagic taxa each accounted for less than 10% of the total taxa (Figures 3c and d), and had larger intra-and interannual variability compared with the mesopelagic and demersal taxa.
In general, mesopelagic taxa were the most abundant, with cumulative larval abundances between 50% and 90% of the total in all seasons, except for winter 2000 when most of the abundance was represented by larvae of a few coastal pelagic taxa (Figure 3b).The highest larval abundances of mesopelagic taxa were in the oceanic region off BSV year round (Figure 4).Demersal taxa larvae usually were more abundant during fall (Figure 3a), with the highest abundances related to the slope zone in BSV and south of Punta Eugenia (Figure 4).The larvae of coastal pelagic taxa were concentrated around Punta Eugenia during winter and summer, whereas in spring they were more widely distributed including in the oceanic region (Figure 4).The lowest abundances of these larvae were found during fall, also related to Punta Eugenia (Figures 3c and 4).Epipelagic taxa had low abundances in all sampling periods and were widely distributed in the sampling area (Figures 3d and 4).
The larval abundances of tropical and subarctictransitional water taxa were higher than those of subtropical taxa, usually ≥ 20 % and ≥ 40 %, vs. < 20 % of the total abundance (Figure 5).Among these groups, tropical taxa were the least well represented with no more than 15 % of the total taxa (Fig 5a), whereas subarctic-transitional and subtropical taxa accounted for about 40-80 % and about 20-55 % of the total taxa (Figure 5b and c).

Discussion
Bahía Sebastian Vizcaíno is an area of high faunistic diversity in the California Current System.This is reflected in the elevated number of fish larvae taxa found during the study period.
BSV and the adjacent oceanic region represent 32% of the IMECOCAL sampling area -from Ensenada, BC (~31º N) to the Gulf of Ulloa (~25º N), and from 20 nm to 60-80 nm offshore.
Approximately 70 % of the total larvae taxa collected in all the sampling area of IMECOCAL (Spanish acronym for Mexican Investigations of the California Current) are present in BSV.
The large number of fish taxa found in the BSV area is consistent with that found by other authors, who agree that the Pacific Coast of the Baja California Peninsula has characteristics that allow mixing of Eastern Tropical, Central North Pacific, Subarctic, and Transitional taxa, all associated with the California Current (Hubbs 1960;Ahlstrom 1972;Loeb 1980;Moser et al. 1987 Myctophidae and Phosichthyidae have high larval abundance as previously seen in diverse oceanic regions (Ahlstrom 1969;1972;Loeb 1979;Moser et al. 1993;1994;Aguilar-Ibarra and Vicencio-Aguilar 1994;Rodríguez 2000;Funes-Rodríguez et al. 2006).The presence of larvae of mesopelagic species in the area together with larvae of coastal pelagic and demersal species can be explained by both the inclusion of sampling stations outside the bay and the large interaction with oceanic waters.The only geographic characteristic that limits both regions is the Isla Cedros complex.
El Niño conditions were identified in the southern portion of the California Current during summer 1997 through summer 1998 (Lynn et al. 1998;Durazo and Baumgartner 2002).A transition to cooler conditions began in fall 1998 and persisted through 2000 as La Niña conditions weakened (Hayward et al. 1999;Durazo et al. 2001;Durazo and Baumgartner 2002).Fall 1997 had the highest number of taxa, but only one species accounted for 50 % of the total larval abundance, which resulted in low equitability.During winter and summer 1998, a warm period with low fish-larvae H' can be identified.Equitability during winter 1998 was low and only the larvae of two species contributed with more than 50 % of the total abundance.Summer 1998 had the highest larval abundances in all the sampling periods, but the lowest H' for the summers.Most of the larvae taxa had similar low abundances, whereas only the larvae of V. lucetia represented more than 50% of the abundance.This period was affected by an El Niño and no seasonal pattern can be identified.The only constant is the preponderance of V. lucetia larvae, which had been recorded previously by Moser et al. (1987).
The years 1999 and 2000 were similar.Many of the fish larvae were resident taxa of subarctictransitional affinities.Tropical and subtropical taxa were more represented in the larval composition during summer and fall, but still tended to be less abundant than subarctictransitional taxa.The assemblage as a whole during these two years showed a consistent seasonal pattern: high H' in spring and summer, when most of the fish taxa had their highest reproductive activity, and lower H' during fall and winter.This contrasts somewhat with that reported by Avendaño-Ibarra et al. (2004)  During El Niño 1958Niño -59 and 1982Niño -1983, a large abundance of fish larvae of tropical taxa was measured along the Pacific coast of the Baja California Peninsula (Funes- Rodríguez et al. 1995;1998a) and this was related to the influence of warm waters during these two events.In the present study the influence of El Niño was evident during fall 1997 with larval abundances more than twice higher when compared with fall 1998, more than four times higher when compared with fall 1999, and eleven times higher when compared with fall 2000.During fall 1997 taxa recorded were from 1.7 to 2.2 times greater than that in fall 1998-2000.Winter and summer 1998 also contrasted with other winter and summer seasons in larval abundances.Winter 1998 had triple the abundance of 1999 and 2000 and summer 1998 was two to three times higher than the abundance of summer 1999 and 2000.Larvae of tropical and subtropical taxa were the most abundant during El Niño and subarctic-transitional species were the most abundant in 1999 and 2000.
During winter 1998 larvae of tropical taxa accounted for more than 40 % of the total larvae and during winter 1999, after the El Niño, larval abundances of tropical taxa were slightly below 40 % of the total.These two winters contrast strongly with winter 2000, when La Niña conditions weakened and tropical larvae were < 10 % of total larval abundance.
Lavaniegos and Jiménez-Pérez ( 2006) found a similar pattern in the copepod community structure of the southern portion of the California Current.They found that the species richness of copepods was higher during El Niño than during La Niña, observing an incursion of tropical epipelagic species, but during La Niña endemic transitionalzone species had a higher occurrence in the study area.Funes- Rodríguez et al. (2006) also found that during El Niño 1982-84 a larval group of tropical species was useful in distinguishing the event, whereas assemblages of larvae of temperate taxa characterized 'normal years' along the Pacific coast of Baja California Sur.
Because the larvae of mesopelagic taxa were among the most abundant and represented 20-40 % of the total taxa during all seasons, H' variations between seasons were low.In all seasons mesopelagic larvae were the most represented and also among the 10 most abundant taxa, and V. lucetia was consistent in all seasons.
Winter 2000 was an exception to the predominance of mesopelagic taxa, when the coastal-pelagic species E. mordax accounted for nearly 2/3 of the total larvae.
Several commercial species spawn around the BSV area.The coastal-pelagic S. sagax is one of the most important and its populations are known to be affected by long-term climatic changes like El Niño and La Niña (Chavez et al. 2003;Lluch-Belda et al. 2003).During this study, larval S. sagax, a transitional species that spawns in the area year round with its highest abundance during summer (Moser et al. 1993;1994) were collected in all seasons except for fall 1997, coinciding with the highest SST recorded.Only during 1998, again coinciding with a high SST annual average, larvae of this species were not among the most abundant taxa.Larval E. mordax were among the most abundant during winter, in agreement with Smith and Eppley (1982), who observed the highest abundances of E. mordax larvae in the California Current in winter and spring correlated with an increase of primary production and with minimal abundances recorded during El Niño.
Larvae of M. productus, a subarctic-transitional species that spawns during winter and spring (Moser et al. 1993), were absent during winter 1998 and 1999 but abundant during spring 1999 and 2000.Results for these three commercial species are partially in agreement with those of Moser et al. (1987) and Funes- Rodríguez et al. (2002), who showed that once the warming events ended larval S. sagax and M. productus remained less abundant, but larval E. mordax increased.The exception in this study was that S. sagax larvae were the most abundant species during 1999 and 2000.
There are no records of Opisthonema spp.larvae being collected in the study area (Moser et al. 1993;1994).The Opisthonema spawning season off the southern Baja California Peninsula is July-December, with highest larval abundance during summer (Moser 1996).Several postflexion larvae were collected in BSV in fall 1997 and preflexion larvae were collected in summer 1998.During an El Niño the northward-flowing countercurrent along the Baja California coast probably plays an important role in the limiting of the spawning habitat of the adults and in transporting larvae of warm water taxa to the north (e.g.Moser et al. 1987;Moser et al. 2001).Thus, the unusual presence of early larvae of Opisthonema spp. in BSV may imply local spawning, which would indicate northward movement of the adults during the warm conditions, whereas the presence of more developed larvae could indicate advection of them by the currents.
In conclusion, the large number of larval fish taxa found during this study is consistent with an interpretation of the high productivity of BSV and its adjacent oceanic region.In terms of hydrographic anomalies, larval diversity, equitability, and taxa composition, the 1997-98 El Niño seems to have been more notable than the 1998-2000 La Niña and was represented by a high proportion of tropical and subtropical taxa that contributed the highest larval abundances.Effects of the La Niña could have been partially dampened by the dominance of subarctictransitional species year round in the area, but these effects were apparent in the greater than usual larval abundances of opportunistic species like E. mordax.
During 1999 and 2000, the seasonal variability was evident in the high larval fish diversity during spring and summer and low diversity during fall and winter, despite the interannual variability recorded during La Niña 1999.During El Niño 1997-1998 no clear seasonal pattern could be found in the larval fish assemblage.

Figure 1 .
Figure 1.Study area and sampling stations in Bahía Sebastián Vizcaíno and the adjacent oceanic region.

Figure 4 .
Figure 4. Fish larvae distributions by taxa habitat affinity in Bahía Sebastián Vizcaíno and the adjacent oceanic region, averaged by season from September 1997 to October 2000.

Table 2 .
Most abundant fish larvae families recorded during the sampling period in Bahía Sebastián Vizcaíno and adjacent oceanic region.Values are given in percentage of abundance for each sampling season.