Impact of El Nin o events on pelagic fisheries inperuvianwaters

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1 Deep-Sea Research II 51 (24) Impact of El Nin o events on pelagic fisheries inperuvianwaters Miguel N iquen, Marilu Bouchon Department of Pelagic Research, Instituto del Mar del Perú, P.O. Box 22, Callao, Peru Received 2 February 23; accepted 3 May 24 Abstract Using data from stock assesment surveys on pelagic resources during El Nin o events of 1972/73, 1982/83, 1997/98, we analyze biological changes on pelagic ecosystems and pelagic fisheries during different stages of development of El Nin o phenomenon: emergence, full, final and post-nin o. Results indicate changes in spatial distribution of resources, their concentration and size structure. In anchovy (Engraulis ringens) a decrease inbiomass was observed, which was estimated at 1.2 milliontons inseptember 1998, the lowest throughout the 199s. This resource showed anasymmetric distribution towards the south of Peru. Other pelagic resources increased their biomass during or after Nin o events, primarily sardine (Sardinops sagax), jack mackerel (Trachurus murphyi), pacific mackerel (Scomber japonicus), and longnose anchovy (Anchoa nasus). At the end of the El Nin o phenomenon we found less productivity but more diversity inthe pelagic ecosystem. During the 1997/98 El Niño, the diversity index (Manual de Ecologia, 1 a Edition, Editorial Trillas, Mexico, 267pp) increased from.87 to In both the emergence stage and fully developed stages of El Nin o we found large numbers of sardine and longnose anchovy present simultaneously. Size structure of sardine, jack mackerel, and pacific mackerel showed an increase in juveniles. Anchovy during El Nin o showed a single modal group composed of adults, but the post-nin o phase indicated an increase in juveniles with an average length of 6 7 cm. In El Nin o conditions spawning among anchovy was low, but among sardine and pacific mackerel it was high. We observed, for the first time during full spawning, juvenile sardines with a total length of 18 2 cm. The anchovy spawning season during the post-nin o phase was considerably lengthened, from April to December Drastic change occurred in fisheries when monospecific fisheries, based on anchovy before El Nin o, became multispecific fisheries based on sardine, jack mackerel, pacific mackerel, longnose anchovy and other species typical of tropical and warm oceans. Landings of anchovy decreased substantially, but those of longnose anchovy, jack mackerel, pacific mackerel, and sardine increased. r 24 Elsevier Ltd. All rights reserved. 1. Introduction Corresponding author. addresses: mniquen@imarpe.gob.pe (M. N iquen), mbouchon@imarpe.gob.pe (M. Bouchon). The El Nin o phenomenon generates substantial changes in oceanographic and meteorological /$ - see front matter r 24 Elsevier Ltd. All rights reserved. doi:1.116/j.dsr

2 564 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) conditions in the Pacific Ocean, with manifestations impacting the Peruvian coast (Zuta et al., 1976); this has mainly affected pelagic resources, producing alterations in their biological processes, behaviour, and gradual decrease in their populationlevels (Valdivia, 1976). One of most sensitive species to these changes is anchovy, which in the 196s reached biomass levels of 15 2 million tons, providing annual landings that exceeded 1 million tons in 197. From 1972, abundances diminished drastically due to a combination of high exploitation and anomalies caused by powerful El Nin o (Tsukayama, 1983). This situationworsened in early 198s, with the occurrence of another exceptionally strong El Nin o phenomenon in (Csirke et al., 1994). This paper describes the effects onpelagic resources of strong or exceptionally strong El Nin o events occurring during the periods , and , predominantly translated into biological alterations and vertical and latitudinal changes in distribution and concentration. These effects are of particular interest because they are related to biological processes such as their reproductive cycle and recruitment, as well as the ecosystem approach to fishery management. 2. Methods The study area is the Peruviancoast between Sand W, which is dominated by the Humboldt Peru eastern boundary current system, characterized by a complex system of surface and sub- surface currents associated with variations of coastal upwelling, and increases in southerntrade winds (Zuta and Guillen, 197). The mainpelagic species are anchovy (Engraulis ringens), sardine (Sardinops sagax), jack mackerel (Trachurus murphyi), and pacific mackerel (Scomber japonicus) (Tsukayama, 1983). For species identification Chirichigno and Velez (1998) was used. Stock assessments of the main pelagic resources were made by hydroacoustic surveys of pelagic stocks, using a SIMRAD EK 5 and EK 4 echosounder operating at 12 and 38 Khz to a depth of 25 m. Sea-surface temperature and salinity were taken from land oceanographic stations every 1 min during the operations at sea and from coastal stations at Chicama and Chimbote, provided by the Oceanographic Forecasts and Marine Hydrophysical Department of IMARPE. Biometrics and biological samplings of pelagic species were made, and species composition of catch, biological aspects, size structure, individual weight, sex and sexual maturity were recorded. The diversity was estimated using the Shannon - Wiener Index (Franco, 1985) onthe commercial catch data. 3. Results and discussion The El Nin o events reveal the following changes, summarized in Fig. 1 and described below, in the environmental conditions and stocks of the mainpelagic resources betweenthe pre-el Nin o period and the end of the event Environmental conditions One characteristic of the El Nin o events was a very marked temperature change between Paita and Chimbote (51 11S) caused by the intrusion of warm equatorial surface waters, producing extreme thermal anomalies of up to 8 1C above the average inthe phase of maximum development. However, betweencallao and Ilo ( S) variations were smaller, and anomalies reached+6 to+2 1C (Zuta et al., 1984). Each El Nin o had different features (Bjernes, 1966). The data, however, shows that in1971, 1982 and 1996, there was a period of cold weather prior to the phenomenon, which lasted until the early months of the following year (Fig. 2). The period of higher temperature observed in 1972 was quite protracted (Zuta et al., 1976), while in it was short and much more intense. By contrast, the temperature rise of was both long in duration and strong in its intensity. In all three cases, two development peaks were observed, with the second having a higher intensity (Fig. 2).

3 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) CHANGES IN ENVIRONMENTAL CONDITIONS CHANGES IN DISTRIBUTION CHANGES IN SIZE STRUCTURE CHANGES IN REPRODUCTION CHANGES IN BIOMASS Getting closer to the coast Getting deeper Migration to the South Young increasing of other pelagics Dispersion of adults Lower intensity and Change in timing on anchovy Increased activity and continuous on other pelagics Anchovy decrease Increase in other pelagics FISHERIES CHANGES Fisheries monospecific Fisheries multispecific Fig. 1. Effects of El Nin o events on pelagic resources Niño Sep71 Nov Jan72 Mar May Jul Sep Nov Jan73 Mar May Jul Sep Nov -5. Anomalies ( C) Sep81 Nov Jan82 Mar May Jul Sep Nov Jan83 Mar May Jul Sep Nov -5. Niño Niño SeP96 Nov Jan97 Mar May Jul Sep Nov Jan98 Mar May Jul Sep Nov Fig. 2. Sea-surface temperature anomalies observed at Chicama (7142 S W) before, during and after El Nin o events Changes in Latitudinal and Vertical Distribution Historical data analysis indicates displacement, from north to south and west to east, of several marine species (Chirinos de vildoso, 1976; N iquen et al., 1999; Kameya, et al., 21). Some of them, originating from Panamanian waters, were observed in the north-central region of the Peruvian coast during the 1997/98 El Nin o event (N iquen

4 566 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) et al., 1999; Bouchonet al., 21). This displacement can be viewed as the shift of a system with its integral species, as the thermal anomaly intensified (Fig. 3). This is how fish, such as tunas, billfishes, pacific mackerel, and jack mackerel, appeared in 88 W 84 W 82 W 8 W 78 W 76 W 74 W 72 W Bregmaceros Tuna LONG NOSE GUAYAQUIL Skipjack tuna Pacific round herring APRIL 1997 Lamp fishes Slender thread herring 4 S PACIFIC MACKEREL BEGINING NIÑO Bill fishes Shrimps Dolphin fishes Euphilax Paita JACK SARDINE MACKEREL 6 S South pacific hake Pimentel Gurn ards Chicama 8 S 1 S 12 S 14 S 16 S 18 S 4 S 6 S 8 S 1 S 12 S 14 S 16 S 18 S 88 W 88 W 88 W Paita Chimbote GUAYAQUIL Shrimps Euphilax Pacific round herring Pimentel Slender thread herring Tuna Chicama Skipjack tuna Bregmaceros Billfishes LONG NOSE Chimbote PACIFIC MACKEREL SARDINE JACK MACKEREL Callao Callao Pisco Pisco San Juan 84 W 82 W 8 W 78 W 76 W 74 W 72 W 84 W 82 W 8 W 78 W 76 W 74 W 72 W Lamp fishes South pacifichake Gurnards APRIL -MAY 1998 LATE NIÑO San Juan 84 W 82 W 8 W 78 W 76 W 74 W 72 W Fig. 3. Species migrationby the of El Niño event along the Peruvian coast. Ilo Ilo 4 S 6 S 8 S 1 S 12 S 14 S 16 S 18 S 4 S 6 S 8 S 1 S 12 S 14 S 16 S 18 S Peruvian waters, followed by longnose anchovy (Anchoa nasus), strand machete (Opisthonema libertate), skipjack (Katsuwonus pelamis), an d finally mictophidae (Diogenichthys laternatus). The fish beard of corn(bregmaceros bathymaster) has beendetected (a species of restricted distribution) usually found off Panama Gulf (Chirichigno and Velez, 1998), together with ayamarca (Cetengraulis mysticetus), mackerel scad (Decapterus afuerae), pacific cutlassfish (Trichiurus nitens), and crabs (Euphilax sp). Meanwhile, resident Peruvianspecies like anchovy became patchier and asymmetrically distributed towards the southern Peruvian coast, instead of being widely distributed over the whole Peruviancoast as was usually the case. Sardine shoals also were displaced from the north-central to the south-central area. Incidence of warm conditions in the northcentral region in the primary stages of El Nino events determines anchovy movement, first towards the coast, and mostly within 3 Km of inshore waters. These movements result in high concentrations, making this species very vulnerable to fishing. Almost immediately, the highest concentrations begin moving south of Chimbote (91S) and deeper schools of anchovy also have been detected in the north-central region, located betweendepths of 2 and 8 m, whenthe El Niño was fully developed. This behaviour resulted ina change in fishing strategy, with the largest catches made at night when fish moved closer to the surface. With regard to sardine, the largest concentrations began to move, from a normal distribution off Paita (51S), towards Pimentel and Chicama (71 81S), simultaneously approaching the coast. Inthe most notable case they reached Ilo (171S) in the south, with higher concentrations off Chimbote (91S), close to the coast, as was the case during El Nin o event (Fig. 4). A similar pattern was found during the El Nin o event of (Zuzunaga, 1985) These interannual migrations depend on the magnitude of environmental changes. For example, insummer 1998 (the highest peak of El Nin o), most of the anchovy biomass was detected south of 131S (Fig. 4) and the bulk of the catches occurred between161 and 181S. while

5 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) Anchovy Sardine APR IL OCTOBER 1997 APRIL1998 Percent (%) APRIL1997 OCTOBER 1997 APRIL 1998 SARDINE 3 SARDINE SARDINE APRIL OCTOBER 1997 APRIL Fig. 4. Changes in distribution and size structure of anchovy and sardine during April 1997 June insummer 2 (cold conditions), the catches were spread out over Peruviancoast, with the highest value off northern Peru (Fig. 5). A complementary aspect of distribution and availability of anchovy is shown by the observation of sea birds, which left islands in the north of Peru inapril 1997, migrating mainly to the central and southern areas (IMARPE, 1997) Changes in Size Structure During the , and El Nin o events, adult anchovy prevailed and young fish were generally few or absent (Figs. 4 and 6), which impact recovery and population growth. However, at the beginning of the post-nin o phase, this behaviour varied notably with a strong Catch(%) Catch(%) SUMMER South Latitude SUMMER SouthLatitude Anchovy catch SST Fig. 5. Latitudinal changes of anchovy catch relative to seasurface temperature (SST). SST ( C) SST ( C)

6 568 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) Percent (%) APRIL JUNE increase in young and juvenile fish (IMARPE, 1998), coming from spawnings starting at the end of the El Nin o event and disappearance of adults, which were probably concentrated near the coast and therefore undetectable by echosounders and not catchable by purse seiners. Sardine changed from predominantly adults to mostly young fish during the El Nin o event (Fig. 4). In general, an increase in the abundance of juvenile sardine has been observed during El Nin o events (Fig. 7), with mainly individuals between 1 and 2 y of age, which were detected throughout the whole El Nin o period. The presence of warm conditions has favoured this stock increase. It is important to highlight the fact that large numbers of young fish were observed among Longitud total (cm) The red line indicates size at first maturity Fig. 6. Anchovy Size structure during El Nin o events. sardine, longnose anchovy, pacific mackerel, and also hake (Merluccius gayi), lumptail searobin (Prionotus stephanophrys) and Vinciguerria spp, all of which were favoured by the strength of the 1997/98 El Nin o. This has beendetected in different phases of El Nin o, especially at the middle of the event in September 1997 (Fig. 8). This situationindicates a recovery inthe stocks of the mainpelagic species, because at the end of El Nin o event, a new species composition is observed, as a result of the entrance of other pelagic species, different to anchovy, which mainly have a juvenile size structure, and whose development depends on the environmental conditions. If the conditions are warm, the change will be long lasting, and if the environment is cold, other pelagics will tend to disappear, originating a rapid return of anchovy.

7 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) SEPTEMBER Percent (%) APRIL JUNE Longitud total (cm) The red line indicates size at first maturity Fig. 7. Size structure Sardine during El Nin o events. In case of longnose anchovy, fish beard of corn (Bregmaceros bathymaster) and sea-catfish (Galeichthys peruvianus), where adults prevail the stocks grew during the whole El Nin o event, in which these adults had almost completed a full life cycle during 18 months of oceanographic anomalies Changes in the Reproductive Process During the El Nin o, the anchovy reproductive cycle was disrupted and spawning diminished in intensity (Perea et al., 1998), while the opposite happened to the pacific mackerel and sardine: spawning increased in intensity at the beginning of El Nin o, and during El Nin o they approximated the historical average (Fig. 9). Furthermore, spawning juvenile sardine and pacific mackerel were detected during the final period of El Nin o. Sexually mature sardines are predominantly cm in length, but at this time significant numbers of sexually mature sardines with lengths of 18 2 cm were observed, which suggests that El Nin o conditions favoured the reproductionof this species. This is probably related to better environmental conditions for sardine, allowing these juveniles to develop their full reproductive potential. It is worth mentioning that the current range of sardine sizes corresponds to that found in sardine off California, where it is known that 5% is sexually mature at a length of 19 cm. Macewicz (1996) and Parrish et al. (1989) mention that California sardine and Peru Chile sardine probably have a common origin and constitute only one species. This evidence of early spawning of sardine would indicate that sardines on the Peruvian coast during El Nin o years behave ina similar way to the Californian sardines, during normal years. It is unknown if this evidence has temporary or permanent character in other years. It should be kept in mind that this was the first opportunity to sample juvenile sizes insitu inthe appropriate prespawing or spawning season, which allowed for

8 57 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) Before El Niño During El Niño Anchovy Anchovy Sardine Sardine Jack Mackerel Jack Mackerel Pacific Mackerel Pacific Mackerel Longnose anchovy Longnose anchovy Merluza hake Merluza hake Lumptailsearobin Lumptailsearobin Sea cat fish Sea cat fish Vinciguerria Vinciguerria Fish beard of corn Fish beard of corn After El Niño Anchovy Sardine Jack Mackerel Pacific Mackerel Longnose anchovy Merluza hake Lumptailsearobin Sea cat fish Vinciguerria Fish beard of corn % Young % Adults Fig. 8. Proportion of young marine species before, during and after the El Niño event. EL NIÑO Gonadosomatic Index (IG) SARDINE PACIFIC MACKEREL LONGNOSE Jan-97 Mar May Jul Sep Nov Jan-98 Mar May Jul Sep Nov Month IG Historical IG average Fig. 9. Gonadosomatic index (IG) of pelagic resources during El Nin o

9 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) Millions Tons Millions Tons Millions Tons April April 1998 April1997 October1997 April1998 Anchovy Sardine Jackmackerel Mackerel Fig. 1. Pelagic biomass before, during and after El Niño events. the correctionof a lack of samples inthese sizes at spawning time. Another interpretation of the observed size distributionis a reductioninsardine growth rate, influenced by poor feeding conditions, which would be reflected by the presence of small, but older thanexpected sardines. The intensity and reproductive activity of other pelagic resources such as pacific mackerel and longnose anchovy were increased (Fig. 9) Changes in Biomass of Pelagic Resources During an El Nin o event, a remarkable decrease in anchovy biomass and increase in the biomass of other pelagic species has beenobserved (Figs. 1 and 11). However, the magnitude of impact depends on the intensity of El Nin o events and the species compositionduring the period before the development of the phenomenon. In , at the beginning of the El Nin o, anchovy Anchovy Biomass Millionstons 1 Post-Niño ElNiño E-97 M M J S N E-98 M M J S N Anchovy dominance was almost total, decreasing drastically throughout the course of the event. At the end of the event increases in stock as of sardine, jack mackerel and mackerel were noticeable. With regard to the El Nin o, other pelagic resources dominated the period before the event, and represented 95% of total biomass by the end of it. The El Nin o was anintermediate case betweenthe two previous ones, where anchovy biomass was relatively important before the event and decreased dramatically during its development (N iquenand Gutierrez, 1998), while the biomass of other pelagic species, which was substantial before the event, increased or tended to remainstable throughtout. Inthree analyzed cases, a decrease infish productivity is general, mainly due to a decrease inthe biomass of anchovy. The El Niño event could be seen as an exception in that the total biomass increased during the last year, but this increase, in fact, was due to the increase in jack mackerel (as a migratory resource) abundance (53% of the total). During the last El Nin o event ( ) a decrease in anchovy biomass was observed during the mature phase of the phenomenon, which only started to show weak signs of recovery at the end of 1998, while the biomass of other pelagic species increased during the first half of the El Nin o event and decreased during the second half of it and during the post-nin o phase (Fig. 11) Changes in Pelagic Fisheries Other Pelagic As a consequence of stock variations in the main pelagic resources, of three El Nin o events analysed, the Peruviananchovy fishery was seriously Biom. Other Pelagic Millionstons Fig. 11. Anchovy biomass and other pelagic during El Nin o

10 572 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) affected and was forced to diversify its catches, towards other pelagic resources (Fig. 12) such as sardine, jack mackerel, pacific mackerel and longnose anchovy. It also took advantage of the availability of unusual species such as round sardine, ayamarca, strand machete, golden fish and others. From 199 until the beginning of the El Nin o events, we observed an increase in anchovy catches due to good spawning and a trend towards cold conditions. This was observed in purse-seine landings, where anchovy was the principal component during the summer of 1994 and the fall of 1997, making up 9% of total catch on the north and central Peruvian coast ( S). Inthe winter of 1997, a decrease in anchovy catch from purse-seine fleets was observed, while the catches Anchovy Landings Millionstons El Niño E-97 M M J S N E-98 M M J S N Anchovy Post - Niño Other Pelagic Landing Other Pelagic Thousandstons Fig. 12. Anchov and other pelagic landings during El Niño inother pelagic species remained relatively stable before large fluctuations increasing during the post-nin o period (Fig. 11). As a result, the proportion of the different species in the landing varied considerably over this period, with an abrupt change in the first quarter of 1998, when the anchovy fishery was closed (Fig. 13). The relationship between SST of Chimbote (91S) and Shannon Wiener Index during January 1997 and September 1998 (Fig. 14), showed a direct relationship until April Then, while SST decreased, Shanon Wiener index remained high. Inthis case other factors have a bearing on the diversity index, elevated salinity being a likely Diversity Index (H') J97 M M J S N J98 M M J S H' SST ( C) Fig. 14. Relationship between Shannon Wiener index (H )and sea-surface temperature (SST) off northern-central Peru, during the El Niño SST ( C) 1..8 Proportion S = Summer F = Fall W = Winter Sp = Spring S94 F W Sp S95 F W Sp S96 F W Sp S97 F W Sp S98 F W Sp Anchovy Sardine Jack& Pacific Mackerel Other species Fig. 13. Changes in the seasonal species composition in purse-seiner landings off north-central Peru,

11 M. Ñiquen, M. Bouchon / Deep-Sea Research II 51 (24) principal factor (Moronet al., 1998). Nonetheless, one must keep in mind that this diversity index was computed from commercial fishery data and therefore is likely to be underestimated and distorted by fishery strategies and fishery regulations such as the closure of the fishery for anchovy. 4. Conclusions Observations carried out during El Nino events reveal the following changes in the stocks of the mainpelagic resources (Fig. 1): 1. Environmental changes: During El Nin o events, very marked increases in sea-surface temperature take place, especially betweenpaita and Chimbote (51 11 S), with thermal anomalies of up to 8 1C above average during stages of maximum development. 2. Changes in distribution: anchovies, instead of being widely distributed over the whole Peruvian continental shelf, became more coastal, within3 Km, more patchy, and asymmetrically distributed towards the southernperuvian coast, instead of being widely distributed over the whole Peruviancoast, while sardine shoals were displaced from north-central to southcentral area. Both species displayed a trend to deepento below 2 m. 3. Changes in size structure: Anchovy size structure showed a predominance of adults, with a low incidence of juveniles. Only in the post-nin o phase, the number of young and juvenile anchovy increases notably. Sardine changed from mostly adult to mostly young fish. 4. Changes in the reproductive process: Reproductive process of anchovy are affected in its intensity and disrupted during maximum El Nino intensity, awaiting better environmental conditions to recover. Meanwhile, reproductive activity of other pelagic resources such as sardine, pacific mackerel and longnose anchovy increased, and this became evident during the beginning of El Nin o period, indicating that El Nin o events had caused quick renovation of these stocks. 5. Changes in biomass structure of pelagic resources: From anchovy dominance, to a prevalence of other pelagic types such as sardine (except during the event), jack mackerel, pacific mackerel, longnose anchovy, vinciguerria, lumptail searobin, pacific cutlassfishes and mictophydae. 6. Changes in landings: From a monospecific fishery to a multispecı fic fishery, with an increased percentage of other pelagic resources and a reduced percentage of anchovy. Finally, impacts of El Nin o events on pelagic resources reflect a clear spatial tendency toward a more southerly displacement and a temporal sequence in the changes of the biological processes (reproduction, recruitment, abundance). Moreover, we canidentify some response patterns of such changes, whose knowledge is very important for the improvement of pelagic fisheries management. Acknowledgements We appreciate the kindness and collaboration of Dr. Pierre Freonand we are grateful with people of Pelagic Resource Department of IMARPE. Special thanks to the anonymous reviewers of this paper because of their suggestions. References Bjernes, J., Survey of El Nin o inits relation Tropical to Pacific meteorology. Bulletinof I ATCC 12 (2), Bouchon, M., Cahuin, S., N iquen, M., 21. Fluctuations of pelagics ichthtofauna in the North Central Region of the Peruvian COAST from 1994 to In: Tarazona, J., Arntz, W.E., Castillo de Maruenda, E. (Eds.), El Niño en América Latina, impactos Biolo gicos y Sociales. Consejo de Ciencia y Tecnología, Lima-Perú, pp Chirichigno, N., Velez, J., Clave para identificar los peces marinos del Perú. Publicación Especial. Inf. Inst. Mar Perú, 496. Chirinos de Vildoso, A., Aspectos biolo gicos del Feno meno El Nin o Parte I: Distribucio nde la Fauna. In: Proceedings of the Workshop El Nin o. Guayaquil, Ecuador, 4 12 December FAO Fishing Information 185, Csirke, J., Guevara, R., Cardenas, G., Niquen, M., Chipollini, A., Situationof resources anchovy (Engraulis ringens)

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