Fish larvae abundance and distribution in the central Gulf of California during strong environmental changes (1997–1998 El Niño and 1998–1999 La Niña)

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Deep-Sea Research II 51 (2004) 711–722 www.elsevier.com/locate/dsr2

Fish larvae abundance and distribution in the central Gulf of California during strong environmental changes (1997–1998 El Nin˜o and 1998–1999 La Nin˜a) Laura Sa´nchez-Velasco, Carlos Avalos-Garcı´ a, Margarita Renterı´ a-Cano, Bernardo Shirasago Centro Interdisciplinario de Ciencias Marinas, Ave. Inst. Polite´cnico Nacional s/n, CP 23000, La Paz BCS, Me´xico Received 13 September 2002; accepted 3 May 2004

Abstract The pelagic ecosystem of the Gulf of California was affected by the 1997–1998 El Nin˜o warming event and the 1998–1999 La Nin˜a cooling. Larval fish abundance and distribution were analyzed in the central Gulf during El Nin˜o (November 1997 and March 1998) and La Nin˜a (November 1998 and March 1999). Mean sea-surface temperature (SST) differed significantly between El Nin˜o and La Nin˜a ðPo0:05Þ, with variations up to 4  C. The lowest zooplankton biomass and larval abundance were recorded during El Nin˜o, when species with tropical–subtropical affinity dominated. The Bray–Curtis Dissimilarity Index defined two persisting station groups. The oceanic group, located south of Islas Angel de la Guarda and Tiburo´n, was strongly co-dominated by Benthosema panamense, Engraulis mordax, and Vinciguerria lucetia larvae in November 1997, whereas larvae of these species together with Triphoturus mexicanus, Sardinops caeruleus, and Scomber japonicus larvae co-dominated in November 1998. Abundances of these last two species were drastically reduced during El Nin˜o. Larval Diogenichthys laternatus, B. panamense, V. lucetia, and T. mexicanus co-dominated the oceanic station group in March 1998, but were less prominent in March 1999, except for V. lucetia, which co-dominated with E. mordax larvae. This situation was associated with the peak of maximum intensity of the La Nin˜a. The second station group, located in the vicinity of Big Islands, was dominated by B. panamense larvae in both Novembers and by E. mordax larvae in both Marches; in both cases this probably was more reflective of high larval abundance in the adjacent oceanic area than a preferential habitat in the Big Islands vicinity. Results suggest that the fish larvae abundance and distribution were altered in different ways by the environmental changes caused by the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a. r 2004 Elsevier Ltd. All rights reserved.

Corresponding author. Tel.: +52-612-12-2-53-44; fax: +52-

612-12-2-53-22 E-mail addresses: [email protected], net.mx (L. Sa´nchez-Velasco).

lsvelasc@prodigy.

1. Introduction In mid-1997 the strongest El Nin˜o-Southern Oscillation episode of the last century in the

0967-0645/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2004.05.021

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northeastern Pacific was recorded. This event increased sea level, salinity, and temperature, affecting primary production and the pelagic ecosystem in general (Schwing et al., 1997; Lynn et al., 1998; Hayward et al., 1999). The El Nin˜o was followed in late 1998 by a transition to a cold episode characterized by stronger than normal coastal upwelling and a decrease in sea level, resulting in a strong La Nin˜a episode with major intensity at the beginning of 1999 (Hayward et al., 1999; Schwing et al., 2000; Durazo et al., 2001). The Gulf of California is characterized by a great diversity of fish and an abundance of species of commercial and ecological importance. Coastal pelagic species like Pacific sardine Sardinops caeruleus, Northern anchovy Engraulis mordax, and Chub mackerel Scomber japonicus sustain important fisheries from late autumn to early spring (e.g., Lluch-Belda et al., 1986; CisnerosMata et al., 1997), and mesopelagic species like Vinciguerria lucetia, Benthosema panamense, and Triphoturus mexicanus are common throughout the year in varying abundance (Moser et al., 1974; De la Cruz-Agu¨ero, 1997). Spawning areas and seasons have been defined for many species (e.g., Moser et al., 1974; Green-Ruı´ z and HinojosaCorona, 1997; Hammann et al., 1998; Sa´nchezVelasco et al., 2004), but the effect of strong environmental changes, like the El Nin˜o and La Nin˜a, on fish life cycles, particularly the larval stages that are most vulnerable to the environment, have been studied relatively little. Moser et al. (1974) analyzed larval fish distributions during the 1957–1958 El Nin˜o, recording a great increase of V. lucetia larvae in the oceanic area; Green-Ruı´ z and Hinojosa-Corona (1997) determined that E. mordax eggs were concentrated in the coldest zone of the Gulf during the 1991–1992 El Nin˜o; Sa´nchez-Velasco et al. (2000) found that E. mordax larvae had more adaptability to environmental changes than S. caeruleus larvae, which tended to disappear during the 1997–1998 El Nin˜o and Avalos-Garcı´ a et al. (2003) detected a strong increase of larval B. panamense during the 1997–1998 El Nin˜o. Because of the complexity of the pelagic ecosystem, it is necessary to have a better understanding of the ichthyoplankton com-

munity response to these kinds of recurrent episodes. The aim of this study is to identify changes in larval fish abundances and distributions that occurred in the central Gulf of California in late autumn and early spring during the 1997–1998 El Nin˜o and the 1998–1999 La Nin˜a.

2. Materials and methods Two well-defined climatic periods characterize the Gulf of California. Strong northwesterly winds cause strong upwelling along the eastern shore from late autumn to early spring, and southerly winds produce upwelling along the western shore in summer. The vicinity of Islas Angel de la Guarda and Tiburo´n is vertically mixed throughout the year as a result of the interaction of strong tides and abrupt changes in topography (Roden and Groves, 1959; Bada´n-Dango´n et al., 1985; Gutie´rrez et al., 2004). Four oceanographic cruises aboard the R=V ‘‘BIP XI’’ (CRIP-Guaymas, SEMARNAP) were made during El Nin˜o in November 1997 and March 1998 and during La Nin˜a in November 1998 and March 1999 (Table 1). All cruises covered the area from the northern tip of Islas Angel de la Guarda ð30 NÞ to the central Gulf of California ð26 NÞ. Four daily SST images derived from AVHRR (Advanced Very High Resolution Radiometer) channels 4 and 5 were obtained from the satellite NOAA-12, representative of each cruise (Table 1). These images were processed using the ERMAPPER image-processing system. The temperature at each station was obtained with a Neil Brown Mark III CTD (Conductivity Temperature Depth Profiler). Zooplankton hauls were made using bongo nets with a mouth diameter of 60 cm and mesh sizes of 505 and 333 mm. Hauls were oblique, from near the bottom to the surface, or from 200-m depth to the surface when the bottom depth was greater than 200 m. The water volume filtered was calculated using calibrated flowmeters placed in the mouth of each net. Samples were fixed with 5% formalin buffered with sodium borate. Zooplankton biomass, estimated by displacement volume (Kramer et al.,

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713

Table 1 General information of the cruises made in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o (*) and 1998–1999 La Nin˜a (**) Cruise date

Number of stations

Average water temperature ð CÞ

Date of AVHRR images

30 November– 8 December 1997* 20–26 November 1998** 24 March–5 April 1998* 17–24 March 1999**

12

24

2-December-97

19 18 21

21 21 18

26-November-98 19-March-98 17-March-99

1972), was standardized to ml=1000 m3 . Fish larvae were removed from the samples and identified mainly using Moser (1996). Larval abundance was standardized to number under 10 m2 of sea surface. Because of heterogeneous variances, the nonparametric Kruskall-Wallis test (Zar, 1984) was used to assess the statistical significance of interannual differences in sea-surface temperature (SST) and zooplankton biomass between both Novembers and both Marches. Similarities among stations were based on taxa with a frequency of occurrence X5% in each period. To reduce the weight of the most abundant species, the standardized data were fourth-root transformed. Groups of stations were defined using the Bray–Curtis Dissimilarity Index, a technique that is sufficiently robust for marine data because it is not affected by multiple absences and gives more weight to abundant species than to rare ones (Bray and Curtis, 1957; Field et al., 1982). Dendrograms were made by the flexible agglomerative clustering method (Sokal and Sneath, 1963). The Olmestead– Tukey test, which takes in account the frequency and abundance of each species, was used to determine the characteristic species of each station group (Sokal and Rohlf, 1979).

annual variations. The warmest period was during the November El Nin˜o cruise and the coldest during the March La Nin˜a cruise (Fig. 1). The mean SST was higher during El Nin˜o (24  C in November and 21  C in March) than during La Nin˜a ð21  C in November and 18  C in March), with significant difference between events for the same month ðPo0:05Þ. The SST distribution showed a northwest–southeast gradient with the vicinity of Islas Angel de la Guarda and Tiburo´n (Island zone) colder than the rest of the study area in all cases. The 22  C isotherm, in the Canal Ballenas during the El Nin˜o November, moved south of the study area to around 27 N during the La Nin˜a November. The 18  C isotherm, in the Canal Ballenas during the El Nin˜o March, was at approximately 28 N during the La Nin˜a March (Fig. 2). The mean zooplankton biomass was significantly lower during El Nin˜o (180 ml=1000 m3 in November and 410 ml=1000 m3 in March) than during La Nin˜a (1550 ml=1000 m3 in November and 1370 ml=1000 m3 in March). The highest biomass typically was located in the island zone in both Novembers and south of the islands in both Marches (Fig. 3). 3.2. Fish larvae abundance and distribution

3. Results 3.1. Sea-surface temperature and zooplankton biomass Daily SST images, showing a synoptic view of the Gulf of California, reflected important inter-

A total of 1203 larvae of 65 species were collected during the November El Nin˜o cruise, and 3982 larvae included in 32 species were collected during the November La Nin˜a cruise (Table 2). B. panamense (Tropical affinity), with 58% of the total larvae, E. mordax (Temperate) (19%), and V. lucetia (Tropical) (6%) were the

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Fig. 1. Daily sea-surface AVHRR temperature images obtained from the satellite NOAA-12 in the central region of the Gulf of California during November and March El Nin˜o 1997–1998 and La Nin˜a 1998–1999.

most abundant species during El Nin˜o, whereas B. panamense (35%), Engraulidae Type-1 (34%), and E. mordax (11%) were the most abundant during La Nin˜a. A total of 921 larvae included in 21 species were obtained during the March El Nin˜o cruise and 1798 larvae of 14 species during the March La Nin˜a cruise (Table 2). B. panamense (65%), E. mordax (10%), and D. laternatus (Tropical) (7%) were the most abundant species during El Nin˜o, whereas E. mordax (70%) and V. lucetia (11%) were the most abundant during La Nin˜a. The Bray–Curtis Dissimilarity Index defined two groups of sampling stations with relatively stable geographic locations during all four cruises: The Oceanic and Big Island Groups. A third group, Coastal Stations, shifted its geographic location from cruise to cruise (Fig. 4). The Oceanic Group, located south of the Islas Angel de la Guarda and Tiburo´n, had a higher larval abundance and number of species than the Big Island Group in all cases. The Oceanic group was characterized by B. panamense, E. mordax, and V. lucetia larvae during both November cruises, and larval S. caeruleus, T. mexicanus,

and S. japonicus also were prominent during the November La Nin˜a cruise. Larval D. laternatus, B. panamense, V. lucetia, and T. mexicanus characterized the Oceanic Group stations during the March El Nin˜o cruise, and V. lucetia and E. mordax larvae characterized the Oceanic area during the March La Nin˜a cruise (Table 3). The Big Island Group, located in the vicinity of Islas Angel de la Guarda and Tiburo´n, was strongly co-dominated by B. panamense and E. mordax larvae during the November El Nin˜o cruise, and by B. panamense larvae during the November La Nin˜a cruise; whereas E. mordax larvae dominated during both Marches (Table 3). Because of the variations in location and species composition of the coastal stations clustered by the drendrograms in each cruise, these were not considered as biological groups persisting over time.

4. Discussion The interannual variations of SST recorded in this study by in situ and satellite data are an

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32

NOVEMBER EL NIÑO

31 30 29

NOVEMBER LA NIÑA 20

23

18

19

22

28

22

21

24

27

715

26

25

25 24

N

PACIFIC OCEAN

23

31 30 29 28 27

MARCH LA NIÑA

MARCH EL NIÑO

32

15

19 18

14

18

17 16

20

21

19

26

20

25 24 23 117 116 115 114 113 112 111 110 109 108 107

117 116 115 114 113 112 111 110 109 108 107

W Fig. 2. Distribution of SST in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a.

indicator of the influences of the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a in the Gulf of California causing a strong transition from heating to cooling conditions over a short time, as recorded in the eastern North Pacific (Lynn et al., 1998; Hayward et al., 1999; Schwing et al., 2000). This transition was reflected in the Gulf of California by changes in zooplankton biomass and in larval fish abundances and distributions. The decrease of zooplankton biomass and larval fish abundance and the increase in the number of species of fish larvae with tropical–subtropical affinity during the El Nin˜o cruises, and the increases of zooplankton biomass and larval fish abundance with dominance of larvae of transitional-temperate affinity in the La Nin˜a cruises are consistent with the changes observed for other zooplankton groups in the Gulf of California

during the 1982–1983 El Nin˜o and 1985 La Nin˜a (Jime´nez-Pe´rez and Lara-Lara, 1988; LavaniegosEspejo et al., 1989; Lavaniegos-Espejo and LaraLara, 1990). At that time, the zooplankton biomass levels were lower during El Nin˜o than during La Nin˜a conditions and the number of copepod and euphausiid species with tropical–subtropical affinity increased during the warming event. The co-dominance of the larvae of mesopelagic B. panamense and V. lucetia of tropical affinity and coastal pelagic E. mordax of temperate affinity in the Oceanic Group during November of both El Nin˜o and La Nin˜a showed that these species were relatively insensitive to the changes generated by both events in the pelagic ecosystem of the Gulf; changes indicated by the variation in the range of SST recorded in the oceanic area with values

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716

32 31

NOVEMBER EL NIÑO

30

NOVEMBER LA NIÑA

ml/1000 m3

29

1 to 100 101 to 500 501 to 1000 > 1000

28 27 26 25 24

N

PACIFIC OCEAN

23

32 31

MARCH EL NIÑO

MARCH LA NIÑA

30 29 28 27 26 25 24 23 117 116 115 114 113 112 111 110 109 108 107

117 116 115 114 113 112 111 110 109 108 107

W Fig. 3. Distribution of zooplankton biomass in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a.

between 23 and 26  C during the El Nin˜o and between 18 and 22  C during the La Nin˜a. However these three species were less abundant and occurred less frequently during the November La Nin˜a cruise, when larvae of the coastal pelagic species S. caeruleus and S. japonicus became more abundant, consistent with their usual late autumn to early spring peak (Moser et al., 1974). The greatest concentrations of eggs and larvae of these two species have been recorded between 17 and 22  C SST (Esqueda-Esca´rcega, 1995; Hammann et al., 1998). This SST range prevailing in the oceanic area during the November La Nin˜a was an indicator of favorable conditions for their spawning, in contrast to the seawater warming recorded during the November El Nin˜o, when the larvae of S. caeruleus and S. japonicus were practically absent. The larval co-dominance of the five species

during the November La Nin˜a cruise in comparison to the results of Moser et al. (1974) recorded in December 1956, a period considered under the influence of a La Nin˜a, showed that V. lucetia, B. panamense, and S. caeruleus larvae were codominant in both cold autumns, but T. mexicanus larvae were the most abundant in December 1956 and the family Engraulidae and S. japonicus larvae were scarce. The co-dominance of the tropical mesopelagic species D. laternatus, V. lucetia, B. panamense, and T. mexicanus in the Oceanic Group during the March El Nin˜o cruise contrasted strongly with their decreases during the March La Nin˜a cruise, except for V. lucetia larvae, which together with E. mordax larvae strongly co-dominated in the Oceanic area during the latter cruise. Moser et al. (1974) recorded high abundance and frequency of

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Table 2 List of species identified in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a Species

Myrophis vafer Bathycongrus macrurus Heteroconger Type 1 Etrumeus teres Harengula thrissina Opisthonema sp. Sardinops caeruleus Anchoa sp. Engraulis mordax Engraulidae Type 1 Leuroglossus stilbius Gonostomatidae Vinciguerria lucetia Stomias atriventer Synodus lucioceps Synodus Type 1 Synodus Type 2 Diaphus pacificus Triphoturus mexicanus Benthosema panamense Diogenichthys laternatus Bregmaceros bathymaster Bregmacerotidae Type 1 Caelorinchus scaphopsis Physiculus rastrelliger Physiculus Type 1 Merluccius productus Cherublema emmelas Lepophidium stigmatistium Ophidion scrippsae Lophiodes spilurus Lophiodes Type 1 Hemiramphus saltator Sebastes constellatus Sebastes Type 1 Pontinus sp. Pontinus Type 1 Scorpaena guttata Prionotus ruscarius Triglidae Type 1 Diplectrum Type 1 Paralabrax Type 1 Paralabrax Type 2 Serranus sp. Serranus Type 1 Serranidae Type 1 Hemanthias signifer Pronotogrammus multifasciatus

November El Nin˜o

November La Nin˜a

X

%F

11 20 7

8 17 8

5 7 38 11 1652

8 17 17 17 58

490

75

49 8 3 18 127 5052 57 164 8 24

33 8 8 17 42 100 25 42 8 8

9

8

6

8

16 19 4

8 17 8

8 115 7 10 24

8 25 8 8 8

5 7 5 6 5

8 8 8 8 8

6 10

8 8

March El Nin˜o

X

%F

89

11

497

37

1099 3460

95 42

5 248

11 53

51

26

356 3574

74 100

27

42

24 86 32

26 32 21

22

16

121 8

32 16

13

16

46

16

22 35

16 37

March La Nin˜a

X

%F

X

%F

445

35

647 5919

14 100

35

6

306

48

250 24

24 12

926 23

19 10

270 2861 294 59

41 59 35 18

16 306 134

10 10 43

6 24

6 12

26

24

30

14

15

10

22

14

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Table 2 (continued ) Species

Apogon atricaudus Trachurus symmetricus Eucinostomus gracilis Haemulidae Type 1 Haemulidae Type 2 Sciaenidae Type 1 Sciaenidae Type 2 Ephippidae Type 1 Pomacentridae Type 1 Opistognathus sp. Howella Type 1 Mugil cephalus Mugil Type 1 Halichoeres dispilus Halichoeres semicinctus Labrisomidae Type 1 Hypsoblennius gentilis Ophioblennius steindachneri Coryphopterus sp. Gobulus crescentalis Lythrypnus dalli Gobiidae Type 1 Gobiidae Type 2 Gobiidae Type 3 Gobiidae Type 4 Scomber japonicus Cubiceps pauciradiatus Psenes sio Citharichthys fragilis Citharichthys Type 1 Citharichthys Type 2 Etropus crossotus Etropus Type 1 Syacium ovale Paralichthyidae Type 1 Achirus mazatlanus Symphurus atricaudus Symphurus atramentatus Symphurus oligomerus Symphurus williamsi Symphurus Type 1 No. of species Mean abundance

November El Nin˜o

November La Nin˜a

X

%F

24

8

11 67 8 5 3 16 8

8 17 8 8 8 8 8

25 23

25 33

7 16

%F

5

11

40

26

March La Nin˜a

X

%F

8

6

3

6

11

6

X

%F

7

10

8 17

8

8

65 93 5 4 7 17 6 30

33 42 8 8 8 17 8 33

110

17

39 8

17 8

5

8

22 57 26 89

17 8 8 8

65 735

X

March El Nin˜o

11

11

62

21

13

12

92

47

20

6

87

10

8 19 5

11 26 11

12 25

6 24

65

10

30

21

2 3

6 6

8 43

11 21 12

6

32 32 535

42 21 245

14 405

%F, percentage of occurrence and X, mean abundance within each cruise. Abundance is expressed as number of larvae per 10 m2 . Type, species not described in the literature.

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Fig. 4. Dendrograms of sampling station groups defined by the Bray–Curtis Dissimilarly Index and the flexible agglomerative clustering method, and their locations in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a.

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Table 3 Characteristic species of the station groups obtained by the Olmestead–Tukey test in the central region of the Gulf of California in November and March during the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a Species

November El Nin˜o

November La Nin˜a

Big islands X Engraulis mordax Benthosema panamense Vinciguerria lucetia Triphoturus mexicanus Sardinops caeruleus Scomber japonicus

Oceanic %F

71 330

No. Stations No. Species

75 100

Big islands

X

%F

273 689 82

80 100 100

4 13

No. Stations No. Species

%F

355

5 23

100

X

%F

69 136 20 29 29 10

100 100 67 92 33 67

4 21

March El Nin˜o Engraulis mordax Benthosema panamense Vinciguerria lucetia Triphoturus mexicanus Diogenichthys laternatus

X

Oceanic

12 29

March La Nin˜a

87

100

246 77 42 44 45

5 4

100

84 67 100 84 6 8

5 5

356

100

305

100

3 9

%F, percentage of occurrence; X, mean abundance within each group (number of larvae per 10 m2 ).

occurrence for all mesopelagic species in April 1956 and April 1957, but in different proportions probably reflecting the influence of the 1957–1958 El Nin˜o. Larval B. panamense were scarce in April of those years, contrasting strongly with their dominance during March in this study, under the influence of the 1997–1998 El Nin˜o. The low larval abundance and frequency of occurrence of mesopelagic species during the March La Nin˜a cruise is an unusual condition that coincides with the peak intensity of the La Nin˜a event in the North Pacific (Schwing et al., 2000; Durazo et al., 2001). This peak intensity was indicated in the oceanic area of the Gulf by the low SST in March 1999 (from 16 to 19  C) compared to March 1988 (from 19 to 21  C). In addition, Lavı´ n et al. (2002), who analyzed the temperature anomalies in the Gulf of California by using satellite images from 1984 to 2000, recorded the strongest negative anomalies in

1999. It is possible that the mesopelagic species, at least during spring 1999, migrated to the south of the Gulf looking for better temperatures for spawning. The low larval abundance and number of species at the Big Island Group stations resulted from the harsh environment prevailing in this area, where year-round continuous vertical mixing occurs, generated by the interaction of strong tides and abrupt topographic changes (AlvarezBorrego and Lara-Lara, 1991; Sa´nchez-Velasco et al., 2002; Navarro et al., 2004; Gutie´rrez et al., 2004). The dominance of B. panamense and E. mordax larvae in this zone may be more an extension of their high abundance and frequency of occurrence in the adjacent Oceanic area than a preferential habitat in the Big Islands vicinity, except during the March El Nin˜o cruise when E. mordax larvae were concentrated there. The

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variations in distribution and abundance of E. mordax larvae in this study are difficult to explain, but high concentrations of eggs and larvae of this species have been recorded in the vicinity of the Big Island zone during El Nin˜o episodes (e.g. Green-Ruı´ z and Hinojosa-Corona, 1997; Sa´nchezVelasco et al., 2000), suggesting an important relationship between the coldest SST of the Gulf and the spawning of the species under the influence of the warmest events. Even though the coastal station groups were not considered as a biological group in this study, Avalos-Garcı´ a et al. (2003), who analyzed the larval fish assemblages in the central Gulf of California during summer 1997–1998, defined a coastal assemblage over the continental shelf of the eastern edge of the Gulf, characterized by coastal demersal species with maximum spawning at this time. Our results showed interannual changes in the abundance and distribution of fish larvae, mainly in the oceanic area of the central Gulf of California, which are associated with changes in the spawning of the species responding in different ways to the 1997–1998 El Nin˜o and 1998–1999 La Nin˜a effects.

Acknowledgements The authors express their thanks to Instituto Polite´cnico Nacional (IPN) and CONACyT for supporting this study through project CGEPI 20010817 and CONACyT 34071-T and to SEMARNAP CRIP-Guaymas for its collaboration on board the V/R BIP XI, especially to Dr. Miguel Cisneros-Mata. L.S.V. thanks SNI-CONACyT and COFAA-IPN for their financial help. C.A.G. and M.R.C. thank CONACyT and CGPI-IPN for the scholarships. Thanks to Dra. Alma Rosa Padilla for her technical support and to Dr. Ellis Glazier for editing the English-language text. References Alvarez-Borrego, S., Lara-Lara, J.R., 1991. The physical environment and primary productivity of the Gulf of California. In: Simoneit, B.R.T., Dauplin, J.P. (Eds.), Gulf

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