Aquatic Living Resources 16 (2003) 107Ð112 www.elsevier.com/locate/aquliv Foreword Introducing nature in fisheries research: the use of underwater acoustics for an ecosystem approach of fish population

The changes in environmental conditions require an “eco- biomass, or more directly establishing total allocated catches system approach” be adopted when considering fish popula- (TACs) based on the stock biomass. However, in many cases tions. This new approach implies the design of new concepts the contribution of fisheries acoustics remained limited. and hypotheses including knowledge on ecology, behaviour Eventually we are entering a new era, which is based upon and fisheries. Being able to observe in real time and in three two observations. dimensions the living organisms and their environment be- • It is now recognised that fisheries activity in the world comes essential. These are precisely the capabilities of un- has reached and most probably exceeded its maximum derwater acoustics, which is going to play a major role in sustainable yield (Pauly et al., 2002; Myers and Worm, aquatic ecology research. 2003). • The failures of stock management in many cases have demonstrated that the study of a fish stock indepen- 1. Introduction dently from its biology and behaviour, and more gener- ally from the ecosystem where this stock is living, usu- Based on pioneer works in the 1950s by Schaefer (1954), ally lead to erroneous conclusions on its status. Beverton and Holt (1957), Gulland (1969), Fox (1970), These two observations have oriented towards new among others, fisheries biology and its associated models of thoughts in fisheries biology, and to the conclusion that the the dynamics of populations represented a huge step forward understanding of stock dynamics would require an ecosys- in the analysis and monitoring of exploited fish populations. tem approach. These models helped to manage a number of important fisheries in the world, initially with great success. A major advantage was the ability to manage a stock on the basis of 2. Behavioural ecology in fisheries research limited data; mostly derived from the fishery itself. Implicit in these models was the concept of “stability” of the stock Such new approach implies new hypotheses, which and its insensitivity to any other parameter than the fishery. should explicitly include behavioural and other biological or Any change in the characteristics of the population was ecological parameters. Some of these hypotheses, in the expected to be due to changes in the pattern of the fishery. design of which teams of our institutes were involved, are The history of most studied fisheries has shown that these described below. assumptions are not completely valid. The adaptation of fish populations to changes in environmental conditions has the 2.1. The “meeting point” hypothesis potential to change the fundamental characteristics of the main parameters considered in conventional stock models. A Dagorn and Fréon (1999) have produced a simulation good, well-described example is the pattern of area occupa- showing that tuna fish will form a school from an originally tion by a stock with changes in abundance (Swain and Sin- dispersed population faster when the fish are attracted by a clair, 1994; Gauthiez, 1997; Fréon and Misund, 1998). floating object, than without one. This would be the basis of On the other hand, since its beginning in the 1970s, fish- the use of fish aggregating devices (FADs). Essentially, the eries acoustics has been developed in order to correct the object serves as a “meeting point” for the fish, in an ocean main biases present in indirect data such as fishing statistics. environment that otherwise lacks obvious spatial references. A well known bias is detailed by Fréon and Misund (1998) This hypothesis has an impact on the way we understand who show that, depending on the spatial strategy of a species, (and use) the aggregative behaviour of such large pelagic a decrease in the global biomass can result in a decrease or an fish. increase of the catch per unit of effort (cpue). Contrarily to fisheries data, acoustic methods provide direct abundance 2.2. The biological trap estimates (MacLennan and Simmonds, 1992). The echo- integration results were generally used for two purposes: The biological trap (Fréon and Dagorn, 2000) is basically tuning virtual population analysis (VPA) models using actual a development of the FAD argument, and is also derived from

© 2003 Éditions scientifiques et médicales Elsevier SAS and Ifremer/IRD/Inra/Cemagref. All rights reserved. doi:10.1016/S0990-7440(03)00058-5 108 Foreword / Aquatic Living Resources 16 (2003) 107–112 observations on the aggregative behaviour of tuna. Fisher- 2.5. Other hypotheses men exploit the aggregation under FADs and introduce large numbers of rafts into the fishing area to concentrate the fish Other hypotheses along the same or similar lines, incorpo- for more efficient capture. One possible secondary effect of rating behaviour or other biological aspects, have also been this technique is that the fish may stay with the rafts as they postulated. These may also have important impacts on how drift. This drift may follow a different route from the normal we view and assess fish populations. Examples include con- migration pattern of the fish. In some situations and if the cepts such as meta-populations (McQuinn, 1997), and more effect is strong enough, the tuna may be “trapped” by the generally the evolutionary concepts synthesised by Cury FADs and end up in the “wrong” place, i.e. not where their (1994) and entitled “obstinate nature”. migration would have placed them. If this area is unfavour- Such new sets of hypotheses are likely to improve dra- able (poorer food resources, etc.) there would be a risk of matically the potential results of fisheries biology research. additional mortality or reduction in recruitment. In this con- These present a strong requirement: to be able to observe the text the large number of human introduced floating objects in nature and the fish living in their environment. the ocean would be of concern. This is the main reason of the parallel evolution of fisher- ies acoustics, described in details by Fernandes et al. (2002). 2.3. Fish learning and catchability This evolution can be seen simply through the changes in the titles of the ICES symposia related to underwater acoustics, It has been demonstrated that fishes are able to “learn” the from “Fisheries Acoustics” for the first ones (Bergen, 1973, effect of a fishing gear and increase their capability to avoid it 1982; Seattle, 1987) to “Fisheries and Plankton Acoustics” (e.g. Soria et al., 1993; Pyanov, 1993). In an evolutionary (Aberdeen, 1995), and finally “Symposium on Acoustics in perspective, the fish behaviour will adapt to high levels of Fisheries and Aquatic Ecosystems” (SAFAE) in Montpellier fishing activity through selection for those fish, which are (2002). better at avoiding, capture. This would result in a decrease in catchability, proportional to the fishing effort (Fréon and Misund, 1998). This response has been documented in some 3. Improving fisheries biology using acoustic data fisheries (e.g. Brehmer and Gerlotto, 2001). In order to adapt underwater acoustics to “fisheries ecol- 2.4. The “school trap” hypothesis (Bakun, 2001) ogy”, it is necessary to evaluate precisely the advantages that it can bring to ecological research, to gather the elements of Alternate dominance of one species has been observed in techniques and methods that are directly applicable to this many mixed pelagic fisheries. This has been well docu- discipline, and to define the points that need specific research mented, for instance, for Peruvian anchovy (Engraulis for an eventual adequacy of acoustics methods and tech- rigens) versus sardine (Sardinops sagax). A fast change in niques to ecology. dominance might be facilitated by the probability of indi- In this regard, three main objectives may be defined: viduals or groups of the declining species being included in a • Taking advantage of existing past research. To evaluate school of the dominant species. The fish may then be consid- the quantity and quality of information already present ered as “trapped” in this school with the possibility of them in acoustic surveys. Since the 1970s, many countries being in, for that species, sub-optimal biological conditions. have developed acoustic survey programs on the main Such behaviour would accelerate the declining of the domi- pelagic stocks in their respective EEZs (Fernandes et al., nated stock and be responsible for the fast changes in species 2002). At this time the ecological information (micron- dominance. ekton, bottom shape and type, school type and behav-

Fig. 1. Some acoustic results on behavioural ecology of pelagic fish. (a) Peruvian landings of anchovy and sardine since 1983; (b) biomass of anchovy, sardine and horse mackerel in Peruvian waters estimated by acoustics since 1983. Foreword / Aquatic Living Resources 16 (2003) 107–112 109

iour, hydrological information, etc.) was considered as method has been designed and applied for decades by background noise and not exploited. Under a new per- Chile and Peru in the South-East Pacific Ocean (Gutier- spective, these data could be used to develop, define and rez et al., 2000). Although it will require some technical extract ecological indicators, allowing observation of improvement (principally the design of autonomous sci- decades of change in pelagic ecosystems. It is likely that entific echo sounders), it may already overcome a series some methods will be needed for transforming acoustic of drawbacks that appear in a single vessel survey; it data into ecological data. provides detailed information in the area of high produc- • Preparing the future. The set of new hypotheses will tion and abundance where fishing vessel are spending require new series of data to be collected, in a more most of their time; and it makes possible real time survey ecological and behavioural way. Being able to observe of ecological changes at all scales in a given ecosyste- in real time and in three dimensions the living organisms m.Anyway, there is a huge amount of acoustic data in the and their environment will be essential. This will require world, still unprocessed from an ecological point of new tools, such as multifrequency echo sounders (spe- view, which could already give some answers to the cies and group identification), multibeam systems (3D questions asked by the new hypotheses. We will give observation) and omnidirectional sonars (kinematics of some preliminary examples on the use, for an ecosystem schools), which are already conceived and will need a approach, of standard echo sounding survey data ini- wider use in the close future. tially collected for fish stock study. They show how a • Improving the present research. Two different kinds of stock can be observed and studied from an ecosystem improvements can be considered: technical and method- perspective inside its environment. For such demonstra- ological. We will not discuss the first one, which was tion, we used long and detailed data series. One of them developed in the SAFAE and published in the Part 1, was provided by the Instituto del Mar del Peru (IMA- technological proceedings of this symposium (ICES J. RPE), which is acknowledged here, on anchovy and Mar. Sci. 60, n¡ 3). The most promising method for sardine stocks off the Peruvian coast; the second one ecological research and monitoring is the use of acoustic comes from the Bay of Biscay (IFREMER data base), on data collected and recorded aboard fishing vessels. Such similar multispecific assemblage.

Fig. 2. Abundance of anchovy and sardine in the Bay of Biscay as observed during acoustic surveys in 2000 and 2001 from IFREMER acoustic surveys. Symbol size is proportional to scrutinised Sa values for each species. 110 Foreword / Aquatic Living Resources 16 (2003) 107–112

Fig. 3. Echograms in the Bay of Biscay showing the assemblage of anchovy with another pelagic species (anchovy with horse mackerel, sardine, sprat).

Three cases are given: where a kind of “synchrony” of abundance of sardine • Temporal change of stock biomass. Some of the hypoth- and anchovy appears in the fishing data (Fig. 1a). Sar- eses presented above have been drawn from long term dine and anchovy seem “incompatible”, and collapse catch data series, where some simultaneity of the popu- alternately according to climatic conditions. When ob- lation changes has been seen. This is the case in Peru, serving the actual biomass values (Fig. 1b), the syn- Foreword / Aquatic Living Resources 16 (2003) 107–112 111

chrony does not present the same “absolute” character as Another point is that it seems extremely important and seen with fishing data. It is confirmed that there are urgent to develop research to confirm or discard the behav- “SardineÐno anchovy” and “AnchovyÐno sardine” peri- ioural hypotheses. In many cases, they were drawn without ods, but the synchrony is only observed on rather long support of real in situ observations: the limited value of time scale and does not obviously need any behavioural fisheries data for behavioural observation may bias strongly hypothesis to exist: changes in the climatic condition the conclusion that one can draw from them. For instance, we (Chavez et al., 2003) are sufficient. Moreover, sardine showed that in Peru the “school trap”, which seemed agree- and anchovy are able to coexist during rather long peri- able when observing the catch statistics of anchovy and ods of “intermediate conditions” (e.g. Fig. 1b). sardine, is unlikely to have any effect on these stocks. • Spatial distribution, competition and coexistence. The But the ecosystem approach, including behavioural ecol- hypothesis of exclusion of a population from an area ogy, is indispensable. As acoustics is one of the very few occupied by another one is not always demonstrated methods able to provide real time in situ 3D observation data when the actual ecosystem is studied. For instance we on living organisms and their ecosystem, it will be the re- observed in the Bay of Biscay that sardine and anchovy sponsibility of fisheries acousticians to develop tools to pro- were present in two well differentiated areas in 2000, vide information on the fish living in their environment. The while they overlapped in 2001 (Fig. 2). The objective of “Ecology Acoustics” is born. this paper is not to study the determinism of such phe- nomena, but we may note that the water masses were quite differently distributed in these 2 years. The same References observation was done in Peru. Although they usually do not share the same area, when anchovy and sardine in Bakun, A., 2001. ‘School-mix feedback’: a different way to think about low Peru are coexisting in a single place, their abundances frequency variability in large mobile fish populations. Progr. Oceanogr. are positively correlated (Gutierrez, personal communi- 49, 485Ð511. Beverton, R.J.H., Holt, S.J., 1957. On the Dynamic of Exploited Fish cation). As in the case of time series, there is a Populations. Chapman & Hall. “Sardine-no anchovy” and “Anchovy-no sardine” area Brehmer, P., Gerlotto, F., 2001. Comparative analysis of swimming behav- pattern, but this remains a general drawing, which is iour in different populations of Sardinella aurita:influence of environ- likely more complex and more related to combinations ment and exploitation; effect on catchability. ICES CM 2001/Q:04. and compromises of tropisms and taxis than to a simple Chavez, F.P., Ryan, J., Lluch-Cota, S.E., Niquen, M., 2003. From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science competition/exclusion between two species. 299, 217Ð221. • Occupation of space in three dimensions. Fish is occu- Cury, P., 1994. Obstinate nature: an ecology of individuals. Thoughts on pying a space in three dimensions, and in most of the reproductive behaviour and biodiversity. Can. J. Fish. Aquat. Sci. 51, fisheries data, the vertical one is practically ignored, 1664Ð1673. although it may be the most important for the species. Dagorn, L., Fréon, P., 1999. Tropical tuna associated with floating objects: a This vertical dimension can allow the life of exclusive simulation study of the meeting point hypothesis. Can. J. Fish. Aquat. Sci. 56, 984Ð993. species in a single (horizontal) area but still remaining Fernandes, P.G., Gerlotto, F., Holliday, D.V., Nakken, O., Simmonds, E.J., completely separated. Very often such evidence is not 2002. Acoustic application in fisheries science: the ICES contribution. visible from fishery data, which cannot clearly describe ICES Mar. Sci. Symp. 215, 473Ð492. this vertical dimension. In most of the cases, a vertical Fox, W.W., 1970. An exponential surplus yield model for optimizing stratification of the species occurs. Moreover, the spatial exploited fish populations. Trans. Am. Fish. Soc. 99, 80Ð88. Fréon, P., Misund, O.A., 1998. Dynamics of Pelagic Fish Distribution and organisation of pelagic fish may be affected by the Behaviour—Effects on Fisheries and Stock Assessment. Blackwell Sci- presence of other species (Fig. 3): in the case of the Bay ence, Oxford, UK. of Biscay, for instance, the shape and dimension of Fréon, P., Dagorn, L., 2000. Review of fish associative behaviour: toward a schools are strongly dependent on the other species generalisation of the meeting point hypothesis. Rev. Fish Biol. Fish. 10, sharing the space: the anchovy schools formed when a 183Ð207. Gauthiez, F., 1997. Spatial structures of demersal fish populations. Charac- predator such as horse mackerel is present, are different terization, biometric developments and fisheries science. Thèse Dr Uni- from those organised when the species share the same versité Claude Bernard, Lyon, France. trophic level (sardine, sprat) (Massé, 1996). Gulland, J.A., 1969. Manual of methods for fish stock assessment Pt. 1. Fish Population Analysis. FAO Manuals Fish. Sci. 4, FRS/M4. Gutierrez, M., Ñiquen,, M., Teraldilla, S., Herrera, N., 2000. Las opera- 4. Conclusion ciones EUREKA: una aproximación de la abundancia de anchoveta en el periodo 1982Ð1999. Bol. IMARPE 19, 83Ð102. As these few examples show, a large part of the hypoth- MacLennan, D., Simmonds, J., 1992. Fisheries Acoustics. Chapman & Hall, eses that we listed, and more generally the ecosystem ap- London. proach of fish stocks, can be explored using acoustic data. Massé, J., 1996. Acoustics observation in the Bay of Biscay: schooling, vertical distribution, species assemblages and behaviour. Scient. Mar. 60 One interesting point is that standard fisheries acoustics is (Suppl. 2), 227Ð234. already able to answer many questions: it is clear that acous- McQuinn, I.H., 1997. Metapopulations and the Atlantic herring. Rev. Fish tic data have been dramatically underexploited so far. Biol. Fish. 7, 297Ð329. 112 Foreword / Aquatic Living Resources 16 (2003) 107–112

Myers, R.A., Worm, B., 2003. Rapid worldwide depletion of predatory fish Swain, D.P., Sinclair, A.F., 1994. Fish distribution and catchability: what is communities. Nature 423, 280Ð283. the appropriate measure of distribution? Can. J. Fish. Aquat. Sci. 51, Pauly, D., Christensen, V., Guenette, S., Pitcher, T.J., Sumaila, U.R., 1046Ð1054. Walters, C.J., Watson, R., Zeller, D., 2002. Towards sustainability in world fisheries. Nature 418, 689Ð695. Jacques Massé * Pyanov, A.I., 1993. Fish learning in response to trawl fishing. In: Olsen, S., Ifremer, Laboratoire d’Écologie halieutique, Wardle, C.S., Hollingworth, C.E. (Eds.), Fish Behaviour in Relation to rue de l’Ile d’Yeu, BP 21105, Fishing Operations. ICES Mar. Sci. Symp., 196, pp. 12Ð16. 44311 Nantes cedex 3, France Schaefer, M.B., 1954. Some aspects of the dynamics of populations impor- tant to the management of the commercial marine fisheries. IATTC Bull E-mail address: [email protected] 1, 26Ð56. François Gerlotto Soria, M., Gerlotto, F., Fréon, P., 1993. Study of learning capabilities of tropical clupeoids using an artificial stimulus. In: Olsen, S., Wardle, C.S., IRD, Roman Diaz 264, Santiago, Chile Hollingworth, C.E. (Eds.), Fish Behaviour in Relation to Fishing Opera- tions. ICES Mar. Sci. Symp., 196, pp. 17Ð20. * Corresponding author. Aquat. Living Resour. 16 (2003) 549 www.elsevier.com/locate/aquliv

Erratum> Acoustics in Fisheries and Aquatic Ecology. Part 2

The Foreword to a special issue of Aquatic Living Re- sources, vol. 16, issue 3, “Acoustics in Fisheries and Aquatic Ecology. Part 2” on pages 107–112, was printed with its last set of figures in black and white due to a printing error. Theses figures should have been in color. The correct figures to this article, “Foreword. Introducing nature in fisheries research: the use of underwater acoustics for an ecosystem approach of fish population” by J. Massé and F. Gerlotto, are printed below (Fig. 3).

Fig. 3. Echograms in the Bay of Biscay showing the assemblage of anchovy with another pelagic species (anchovy with horse mackerel, sardine, sprat).

> doi of original article 10.1016/S0990-7440(03)00058-5.

doi:10.1016/j.aquliv.2003.10.001