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ICES Journal of Marine Science ICES Journal of Marine Science (2014), 71(8), 2281– 2292. doi:10.1093/icesjms/fst242 Contribution to the Special Issue: ‘Commemorating 100 years since Hjort’s 1914 treatise on fluctuations in the great fisheries of northern Europe’ Food for Thought Active opportunist species as potential diagnostic markers for comparative tracking of complex marine ecosystem responses to global trends Andrew Bakun* Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA *Corresponding author: tel: +1 305 967 4711; fax: +1 305 421 4600; e-mail: [email protected] Bakun, A. Active opportunist species as potential diagnostic markers for comparative tracking of complex marine ecosystem responses to global trends. – ICES Journal of Marine Science, 71: 2281 – 2292. Received 9 December 2013; accepted 26 December 2013; advance access publication 7 February 2014 . As it becomes ever clearer that on longer time scales marine ecosystems function as non-linear “complex adaptive systems”, potential consequences of global change become obscured within a maze of multiple possibilities. This essay attempts to route one pathway to a potentially more robust conceptual synthesis, employing the globally important example of anchovies and sardines as a model. Expressly, the anchovy emerges as an efficient specialist of neritic origin. In contrast, the sardine’s oceanic-based adaptations equip it to deal with intermittent episodes of poorly productive conditions and to take advantage of associated reduction in predation pressure on early life stages of their offspring. Based on the overall synthesis, the nimble, wide-ranging, actively opportunistic sardine appears notably well equipped to deal with climate-related disruptions and dislocations and even to profit from their adverse effects on predators and competitors. Global-scale multispecies population synchronies in the 1970s to the mid-1980s suggest that a variety of different species types might be flagged for investigation as perhaps embodying similar “active opportunist” attributes. If so, events and anecdotes might, as global changes proceed, be viewed within a developing universal framework that could support increasingly effective transfers of experience and predictive foresight across different species groups and regional ecosystems. Keywords: climate change, earth systems models, global climate models, representative concentration pathways. Introduction In the century that has passed since Johan Hjort’s (1914) seminal publication, much has been learned about the intricate linkages of physical and biological mechanisms operating within the structures of marine ecosystems. Even so, there has been precious little success in applying that progress towards improving fisheries management and marine conservation efforts, i.e. towards the “ultimate”-level goals of long-term preservation of the traditional economic and esthetic benefits that have come to be expected to flow forth from the world’s marine ecosystems. Perplexingly, our current understanding of the dynamics of these systems remains rife with puzzles and paradoxes (e.g. Bakun, 2011, 2012), and actionably reliable prediction continues to evade us (Houde, 2008). This is much in contrast to many other fields of modern science in which the spread of successful applications has been explosive. Certainly, part of the problem must be that we humans are not marine organisms, but are terrestrial ones. Our experiences, as well as our intuitions, are overwhelmingly terrestrially based. Not surprisingly, our conventional conceptual frameworks for understanding how marine ecosystem processes may influence population dynamics are, both at Hjort’s time and at present, rather simple reflections of terrestrial analogies. But the “marine world” is something qualitatively different and in many ways “beyond our human experience” (Bakun, 1996). For example, in terms of such references as numbers of trophic levels or varieties of dynamical feedbacks involved, marine systems are in nearly all cases much the more complex. Moreover, as historical data records have lengthened, it has become ever more evident that on longer time scales, marine ecosystems seem to be functioning as classical complex adaptive systems (Levin, 1998, 1999), characterized by dynamical non-linearities # International Council for the Exploration of the Sea 2014. All rights reserved. For Permissions, please email: [email protected] 2282 (Hsieh et al., 2005) and self-enhancing feedback loops (Bakun and Weeks, 2006). Dynamical systems of this type tend towards chaotic, non-predictable behaviour, calling into question the very efficacy of scientific management efforts. In particular, since non-linear mathematics do not necessarily yield unique solutions, potential consequences of various aspects of global change tend to become diffused in a nebulous array of multiple possibilities. Certainly, once it is realized that conventional assumptions of system stationarity are becoming increasingly untenable, the sorts of simple linear models (e.g. fitting of indices of reproductive success to one or several indices of correlated environmental or ecosystem mechanisms) that have become traditional in fisheries science, lose their credibility as reliable harbingers of the future. Fortunately, such a pessimistic perspective is contradicted by certain striking regularities and temporal-spatial correspondences that seem to evoke a more promising viewpoint. Among the most remarkable of these have involved interactions between the anchovy (genus Engraulis) and sardine (genera Sardinops and Sardina) species groups. Anchovies and sardines coexist at the crucial wasp-waist position (Rice, 1995; Bakun, 1996, 2006a; Cury et al., 2000) in the trophic structures of a surprising variety of important regional marine ecosystems. Their populations tend to be large, often comprising the greater part of the entire animal biomass of the local ecosystem in which they function. Therefore, they tend to support quite massive fisheries, such that variations in production from the anchovy –sardine pair have often been dominant factors in the overall variability in world fish production. In turn, the very efficient and powerful fisheries focused on these stocks exert important controls on their population dynamics. Notably, the two species groups have historically exhibited a tendency to alternate in ascendancy at the wasp waist of a given regional ecosystem on time scales of several years to several decades, generating differing ecosystem effects depending on which may be dominant at a particular time. For example, anchovies are largely zooplanktivores, whereas sardines are more omnivorous in that they have greater capability to effectively consume phytoplankton as well as zooplankton. Thus, anchovy dominance may promote higher ratios of phytoplankton to zooplankton (Cury et al., 2000), perhaps therefore favouring eutrophication and associated hypoxia. On the other hand, since herbivorous zooplankton may preferentially consume diatoms over dinoflagelates, the higher ratios of zooplankton that may be associated with sardine dominance may favour toxic “red tide” dinoflagelate blooms (Irigoien et al., 2005). Moreover, sardines tend to spread their operations over much wider ocean areas, whereas anchovies tend to remain concentrated in more restricted home-range zones. Thus, a change in dominance between the two has important consequences with respect to many aspects of geographic patterning of marine ecosystem processes. Puzzling issues with respect to the interactions of this pair of species groups include the following (Bakun and Broad, 2003). (A) The fact that sardines, which are a species group obviously adapted to highly productive ocean conditions (upwelling areas, etc.), often do better, at least in the eastern Pacific, during El Niño episodes—which paradoxically are characterized by abruptly lowered primary productivity. (B) The extraordinary fish productivity of the Peru– Humboldt large marine ecosystem (LME), which largely rests on the productivity of the anchovy –sardine species pair. A. Bakun (C) A pervasive tendency for out-of-phase population oscillations leading to alternating dominance of anchovies and sardines in any given regional ecosystem. (D) Basin-scale synchronies in sardine population expansions and contractions during the 1970s and the 1980s—although the involved populations exist in very different types of ecosystems, which accordingly could be expected to respond quite differently to the same large-scale forcing characteristics. An additional unexplained issue (which can here be labelled “E”) involves the fact that these two species types manage to cohabit a remarkable number of diversely configured regional-scale marine ecosystems, in apparent contradiction of the competitive exclusion principle (Hardin, 1960). Although it is difficult to rejoice over the existence of conspicuous gaps in our understanding, prominent existing paradoxical issues such as these do represent remarkable opportunities to hone directly in on essential mechanisms and thereby avoid becoming lost in irrelevant details and distractions. The wealth of such “conundrums” represented in the list above (issues A though E) provides an essential inferential basis that underlies the conclusions and generalizations presented here. In the many years that fisheries scientists have been puzzling over these and other seemingly paradoxical patterns of correspondence and evident interaction, quite a collection of proposed hypotheses as well as ad hoc explanations have been amassed. At the point they are proposed, these generally provide a reasonable degree of empirical fit to the past data that largely motivated them. However, the degree of fit seldom holds up through subsequent years. A basic problem is that the standard experimental method is clearly not practical on the scales at which the earth’s coupled ocean –atmosphere system and its entrained marine biological processes interact to regulate dynamics of wide-ranging, mobile marine populations. Moreover, the rises and declines in dominant fishery resource stocks tend to play out over decadal or multidecadal time scales, whereas most available in situ dataseries, as well as acceptably homogeneous fisheries catch dataseries, do not exceed a few decades in length. As a result, the number of actual realizations of such major changes available in any real dataseries tends to be too small in any single regional case to empirically sort out the complexity of interactions among the various driving factors and non-stationary linkage mechanisms. Although constructing computer-driven simulation models to explore and demonstrate the outcomes of combining particular sets of mechanisms and processes is currently a very popular activity, such simulations can of course only reflect the knowledge and assumptions that were put into them; they cannot generate independent new data. Some alleviation of the insufficiency in empirical degrees of freedom may be sought via an interregional comparative approach. This requires a willingness to accept that parallel aspects of essential processes and relationships controlling the dynamics and interrelationships of highly similar species groups should operate in a generally analogous manner, after allowing for regional particulars, in different available regional situations. If this willingness exists, the comparative method (Mayr, 1982) opens the door to considerably augmented inferential power, although suitable analysis procedures may not necessarily be simple or straightforward. Generally, if a coherent hypothetical formulation should be found to be capable of explaining a number of paradoxical, or otherwise remarkable, observed patterns, scientific confidence expands. If it appears uniquely so (i.e. no other explanatory basis is found that can Active opportunist species as potential diagnostic markers for comparative tracking withstand serious examination), one may reasonably decide, at least tentatively, to place reliance on it. MacCall (2009a) listed a number of candidate mechanisms that may underlie anchovy–sardine interactions, most of which seem likely to be involved to greater or lesser degree at various times. For even more potential explanatory “ingredients”, one might refer to several of the chapters in the “Berlin Workshop” volume of Journal of Marine Systems (Alheit et al., 2009), and a succession of other symposium volumes and workshop reports stretching back to the pivotal “Lima Workshop” (Sharp, 1980). But here we first try to gain some independent discriminatory power to help navigate the labyrinth of proposed hypotheses and mechanisms. We do so by standing back a bit from the details and widening the focus to encompass a more general view of the two species groups in terms of what might be directly inferred from their apparent evolution, genetic characteristics, adaptations, and evolved capabilities. Certainly, the manifested comparative patterns (“A” though “E”, listed above) are so striking that the idea that they might spontaneously materialize from some variable mix of largely autonomous mechanisms strains credulity. Rather, a satisfying explanation would seem to require some overall organizing principle, basic to all the otherwise puzzling issues listed above, that could somehow weave together the outcomes of multiple active component mechanisms so as to logically lead to the pervasive patterns that are observed. Differing evolutions and adaptations To try to initiate a comparative inferential search at the most basic evolutionary level possible, it may be useful to begin by considering the differing developmental origins of the respective anchovy and sardine species groups. (The discussion that follows in this section is summarized diagrammatically in Figure 1.) Anchovies In gross aspect, the evolution of the anchovy (genus Engraulis) would seem to have had its primary basis in terrestrially conditioned habitats (river plume environments, estuaries, run-off-influenced semi-enclosed seas and bays, broad sedimentary continental shelves, etc.). For example, because of the westward tectonic movement of the American continents, high mountain barriers and narrow continental shelves characterize their western continental boundaries. As a result, the overwhelming portion of continental run-off flows to their Atlantic Ocean sides, which (being the “trailing” continental edge with respect to tectonic plate movement) tend to feature much broader continental shelves and very extensive shallow estuarine systems. Substantial anchovy (Engraulis) populations exist all along the temperate western Atlantic ocean boundary, with one of the largest anchovy populations of the world (E. anchoita) stretching along an enormous stretch of very broad South American continental shelf. In contrast, temperate sardines (Sardinops or Sardina) are entirely absent from the western side of the Atlantic. The pattern of association of anchovies with river plume/estuarine/terrestrial-conditioned environments continues to hold also on somewhat smaller scales—for example, among the intricately patterned Mediterranean Sea environments (Palomera and Rubies, 1996) and also recently within the North and Baltic Seas (Alheit et al., 2012). A revealing example comes from the Gulf of California, where one of the great rivers of North America, the Colorado, used to flow copiously into its upper (northern) end. That inflow has steadily vanished over the past century as a result of steadily increasing impoundment to supply agricultural irrigation for much of the 2283 southwestern United States. In the memory of fishers operating there in the latter 20th century, an anchovy had never been seen in the Gulf before 1986 (Hammann and Cisneros-Mata, 1989), when anchovies briefly appeared following an abrupt collapse of the local sardine resource. Later, a subsequent analysis of fish scale deposits in anaerobic sea floor sediments (Holmgren-Urba and Baumgartner, 1993) indicated that this was not the first time that anchovies had made an incursion into the Gulf of California, but in fact they had entirely dominated the fish biomass in the Gulf for most of the 19th century. This was when (and here is the illustrative point) the Colorado River was still pouring into the Gulf a major portion of the continental run-off from the great mountain ranges and high plateaus of the southwestern United States. The higher degree of affinity of anchovies for estuarine-affected habitats is clearly reflected in the much coarser gillraker structures that they employ as food gathering apparatus. As a result, they are incapable of filtering as small a size of food particles as sardines can (van der Lingen, 1994; van der Lingen et al., 2006). But anchovies may thus be able to suffer less clogging of these structures with terrestrial sediment material and other particulate matter that typifies run-off-influenced situations (unblocked flow of water through gill structures being essential also to respiration, an even more immediate need than food gathering). But crucially, precisely because of their coarsely meshed gillrakers, anchovies can efficiently deploy a comparatively much larger “filter basket” (reflected in their local common name often being some variation on “big mouth”). Therefore, anchovies are particularly efficient at gathering large food particles when such particles are plentiful (as they would tend to be in the run-off-dominated terrestrially conditioned nearcoastal or estuarine situations in which the genus appears to have primarily evolved). In accordance with this seeming affinity for terrestrial-conditioned environments, the anchovy seems to be quite local in its movements, exhibiting a tendency to both feed and reproduce within restricted, comparatively fixed geographical contexts (river plume edges, local coastal embayments, island complexes, etc.). Thus, the anchovy has evolved to be a relatively weak swimmer and migrator. In any case, their coarse filters would seem to make wide-ranging exploratory activity a risky proposition, in that once an anchovy may wander away from the geographically fixed locations where the larger food particles that it can efficiently gather may be reliably available, it runs serious risk of dangerous problems in gathering adequate food to sustain itself until it encounters the next suitable large-particle “oasis”. Thus, one might surmise that an anchovy would tend to be, in the terminology of Cury (1994), more “obstinate” than “opportunistic” in its migrational tendencies. An associated propensity for local population segmentation is confirmed by the anchovy’s comparatively much greater level of genetic diversity (Hedgecock et al., 1989; Grant and Leslie, 1996). The implication is that anchovies expend less of their acquired trophic energy in swimming and migrating than do sardines. Therefore, there is less need for the hydrodynamic advantages associated with larger size, and so the anchovy can afford to mature earlier and at a smaller size, in the process allotting a lesser portion of acquired energy to growth and a greater portion to reproduction and rapid population responses (Figure 1). Because predation in these highly productive shallow, near-coastal zones would be expected to be intense on all life stages, such energetic efficiency and rapidity of population response may be an absolute requirement for long-term population viability. The “anomaly” to this pattern presented by the remarkable success of the anchovy in the open ocean realm off Peru has been 2284 A. Bakun Figure 1. Summary diagram representing the adaptive sequences leading from evident “primary ecological origins” to produce the relative ecological advantages (unshaded text boxes) or disadvantages (shaded text boxes) exhibited by the respective anchovy and sardine species groups. attributed (Bakun and Weeks, 2008) partially to the special conditions of that very low latitude location which, because of the weakened coriolis effect, presents a particularly benign habitat that is characterized by strong enrichment, weak turbulent mixing, and long particle residence times. Except during El Niño situations when nutrient supply is disrupted, these attributes generate particularly dense accumulations of very large chain-forming diatoms and associated larger herbivorous zooplankton species. Thus, the normal Peruvian situation may present analogies to the comparatively turbid, large-particle conditions found in other more terrestrially conditioned anchovy habitats. On the other hand, during an El Niño episode, when the available particle spectrum characteristically shifts to a much smaller size range, the Peruvian anchoveta would seem to face quite a direct analogue to the feeding problems that might be faced by a “wandering anchovy” that attempts to transit between dispersed terrestrially determined habitats. Active opportunist species as potential diagnostic markers for comparative tracking Sardines Sardines, in contrast, tend to avoid turbid water situations. In particular, they appear to thrive where continental shelves may be narrow, in upwelling systems, and in the edge zones of strong oceanic boundary currents. They appear adept at opportunistically exploiting the benefits of energetically forced eddy fields and of a variety of transient, sporadically distributed convergent frontal situations that develop in more offshore oceanic waters. They are strong swimmers and, particularly for Sardinops, prodigiously wide-ranging migrators as befits their relative affinity to the less robustly patterned, more variably configured oceanic realm (i.e. the offshore frontal boundaries where upwelling-conditioned waters or continental shelf waters meet with oceanic waters, or within the favourable segments formed within the energetic eddy fields driven by lateral frictional interactions with strong oceanic boundary current flows). Here, substantial concentrations of food particles large enough to be efficiently gathered by anchovies tend to be relatively rare, and patches even of much smaller potential food particles are patchy, transitory, and more or less ephemeral. In such a case, exploration, innovation, and even a degree of “risky” capriciousness may be advantageous to sardines on an individual basis, while also yielding as a by-product diffused overall risk to the population as a whole. Moreover, in this less productive offshore zone, predation pressure would be relatively relaxed, except in zones of dynamic concentration such as convergent fronts or convergent eddy segments that may be vital to their reproductive success. But here the sardines’ highly mobile, exploratory tendencies may allow them to “get there first”, and then “get out” (or at least “do their reproductive business”) before larger pelagic predators also locating the zones (e.g. guided by the presence of flotsam and drifting objects that would begin to progressively accumulate rather immediately after the particular convergence zones develop) and arriving en masse to truncate the transient local advantage that the sardines may have initially enjoyed. At the population level, sardines are strikingly proficient at opportunistically expanding or altering the geographical locations and extents of their spheres of operation (Lluch-Belda et al., 1989; Kuroda, 1991). Their geographical gyrations are matched by radical abundance variations, suggestive of a “high-risk” opportunistic life strategy that seeks to initially overwhelm and then outmanoeuvre adverse ecological pressures by relentlessly ferreting out opportune “loopholes” (Bakun and Broad, 2003) in the ambient predation pressures wherever they might exist. This impression of wide-ranging, “high-risk” operation by the sardine is bolstered by genetic data (Lecomte et al., 2004) that, for example, indicates quite a recent sardine history in the northeast Pacific (a quarter million years) compared with the anchovy’s (5 million years). Such a comparatively recent “founder event” has also been supported by allozyme data, which indicated reduced levels of diversity relative to anchovies and other clupeoids (Hedgecock et al., 1989; Grant and Leslie, 1996). This degree of shallowness in genetic divergences among regional populations may be explained by two alternative models of population persistence and dispersal (Grant and Bowen, 1998). Either (1) Sardinops may have inhabited a limited area for most of the last 20 million years before expanding to the temperate corners of the Indian and Pacific regions in the last few hundred thousand years or (2) the various regional Sardinops populations may have been extinguished 2285 repeatedly and subsequently recolonized by opportunistic transoceanic or trans-equatorial migrants. The intervening “in-play” zones Thus, on the long term if not necessarily on the very short term, each of the sardine–anchovy pair in each regional case can probably pretty consistently be the “superior competitor” in their respective natural “home segment” of their regional habitat. Otherwise, they should at some point have been completely eliminated from the regional system. An example of an anchovy “home segment” might be the western side of the Adriatic Sea, where Coriolis force causes the plume of the Po River, along with commingling waters from other rivers flowing out of the Dolomite Alps, to hug against essentially entire Italian coast of the Adriatic, while the upwelling-conditioned zone off the Croatian coast on the opposite eastern side of that sea may better represent natural “sardine waters”. In the northwestern Mediterranean, the zones near the Rhone and Ebro River plumes would appear to be zones where the adaptations of the anchovy would tend nearly always to render it the superior competitor, whereas the vigorous turbulent eddy fields driven by the winter Tramontana/Mistral wind jets in the zone between may be difficult for anchovies while being manageable, and even offering favourable opportunities, to sardines. In the California system, the plume of the Columbia River and the run-off influenced near-coastal segments of the inner Los Angeles Bight (particularly before the impoundment of most natural run-off sources there) would seem to constitute favourable “home segments” for the respective northern and central subpopulations of northern anchovy (Engraulus mordax), while the offshore eddy fields and frontal systems where the upwellingconditioned neritic waters meet the warmer, more saline oceanic water masses would seem to constitute sardine “home segments”. [In view of considerations developed here, one may not find surprising the findings of van der Lingen et al. (2006) that natural selection has apparently optimized the digestive chemistry possessed by the two species groups to work particularly efficiently with respect to the size ranges of particles characterizing the “home segments” on which their viability may at times be totally dependent and to which the their respective physical capabilities appear likewise to have been optimized.] The intervening zones of the rich regional upwelling or boundary current conditioned systems where the two species groups co-occur are intermittently dominated by one or the other of the groups, rather than being characterized by a single superior competitor. These intervening zones tend to be highly variable on a variety of scales. And so one might imagine that, as a result, the directions of the selection pressures may be highly non-uniform in both time and space. This may have suppressed, or at least delayed, development of specific adaptations to that intervening zone itself. In such a case, that rate of immigration of individuals from the nearby home-base segments could have been sufficient to overwhelm any nascent-specific adaptations to that zone within either of the sardine or anchovy generic groups. To sum it up, we evidently have two species groups possessing differing strongly evolved adaptations simultaneously employing these adaptations to dominate, when possible, the richly productive but highly variable regional-scale habitats within which the more limited home-base segments of each are embedded (Figure 1). Whenever one or the other may achieve clear dominance, potential competitors for the dominant nektonic planktivore role are effectively eliminated, or at least “squeezed back” into primary home-base habitat segments that are particularly forgiving of their specific 2286 special problems and limitations. In the anchovy case, the home segment may be limited in extent while being subject to intense predation (e.g. from shore-based seabirds and marine mammals, nearcoastal demersal “ambush” fish predators, etc.). In the sardine case, lack of consistent availability of adequate food concentrations in those outer reaches of the neritic system may limit their ability to grow abundance in the face of a spectrum of predator species that have been in diverse ways evolutionarily equipped to deal with the arduous local conditions. This is what appears to render the extensive breadth of rich but variable intervening habitat such a prize. Excluding the “other” The process by which the alternative member of the anchovysardine pair may be actually eliminated has been a puzzle. For example, why do the two species not simply separate spatially, each occupying a portion of the habitat where its adapted characteristics may render it comparatively superior on average? Rather, one of the species tends to become overwhelmingly dominant over the major portion of the shared habitat where the other “subordinate” species collapses to what might be considered a very low-abundance “refuge” level (Bakun, 2006a) where it may be found operating mostly within schools of similar-sized individuals of the much more numerous “dominant” species (Bakun and Cury, 1999). Direct competition for food does not seem to be the answer. Nor does preferential predation on the other species’ eggs and larvae (each appears to cannibalize its own potential offspring as readily as the others). The set of “school trap” and associated “school-mix feedback” effects (Bakun and Cury, 1999; Bakun, 2001, 2005a) could perhaps hold at least part of the answer. But one wonders if this group of mechanisms (even acting at several levels: adult energy efficiency, successful fertilization of eggs, larval mortality, etc.) by itself could be potent enough to produce the quite consistently repeatable, sweeping nature of the effect. The possibility of involvement of infectious diseases via cycles of increased population density, associated increased efficiency of disease transmission, resulting infectious outbreaks and subsequent population collapses has for some reason been largely neglected in discussions of this set of issues, but probably should not be discounted in terms of some degree of possible involvement in the alternating dominance issue (i.e. item “C” of the list presented in the Introductory section), but it is not easy to see how disease cycles could constitute any consistent rationalization for the other items (items “A”, “C”, “D”, “E”, etc.) for which we are seeking a comprehensive theory. But, whatever the case, there can be no doubt that the very specificity of the respective anchovy and sardine adaptations must cause the two species groups to often react in strikingly differing ways to climatic or ecosystem variations. And we seem to drawn to a general conclusion that a major overall difference between the evolved ecological strategies of sardines and anchovies is that, of the two species groups, the sardine seems much more opportunistic with respect to major ecosystem variations. Anchovies, of course, are also r-selected (i.e. opportunistic) species, but in a different sense. That is, the sardine’s evolutionary history has evidently provided characteristics by which radical ecosystem variation may represent distinct opportunities that the sardine may be prepared to actively exploit. In contrast, the anchovy’s evolved characteristics may allow it to do rather well in a period of rather settled conditions or comparatively gentle, largely monotonic long-term trends in which it can take rather steady advantage of superior efficiency, but be unable to adapt to, and thus be seriously disrupted by, abrupt ecosystem change. Bakun and Broad (2003) illustrate this A. Bakun in terms of a financial stock market analogy, in which anchovies can be thought of as the “bulls” that do well in “good times” when conditions are benign, well behaved, and predictable, and sardines as the contrarian “bears” that during “bad times” are able to turn adversity into opportunity. To put this conceptual template in most simplistic terms, “normal” (i.e. stable or gently trending) favours the anchovy, whereas “disruption” (of the “normal”) favours the sardine. Resolving conundrums So, if it is accepted that their differing evolutionary histories may have effectively assigned the ecological role of obstinate “robust strategist” to the anchovy and the role of “nimble opportunity-seeker” to the sardine, let us expressly test this “comparative advantage” template terms of its ability to yield a resolution of each otherwise puzzling pattern of interrelationship (i.e. the “conundrums” “A” through “E”) outlined in the “Introduction” section. We briefly do this, item by item. Item “A”: sardines growing their abundance during poorly productive conditions In the eastern Pacific, in both the California Current and Humboldt Current systems, anchovies do well in highly productive conditions that characterize the multiyear time intervals between El Niño episodes. This is as is expected for a species obviously oriented to highly productive ocean zones. A seeming paradox is that sardines, equally obviously adapted to highly productive ocean zones (upwelling areas, etc.), often do better, at least in the eastern Pacific, during the conditions of abruptly lowered local low-trophic-level productivity that characterize El Niño episodes (Niquen and Bouchon, 2004). The inference drawn by Bakun and Broad (2003), supported by the empirical finding of Agostini et al. (2007), is that El Niño disrupts the pervasive larval predator pressures that appear so damaging that many fish species (e.g. coral reef fish, tunas, salmon, etc.) make extraordinary expenditures of migrational energy and/or losses of reproductive product to remove their earliest life stages from proximity to high concentrations of potential larval predators. Sardines, particularly those of the genus Sardinops, apparently are able to employ their prodigious long-range swimming capabilities and widely ranging opportunistic migrational tendencies to ferret out isolated temporal-spatial “pockets” where a minimally adequate larval food concentration may be available. This may allow sufficient advantage to be gained from the reduced levels of predation such that their highly leveraged reproductive mode can generate a substantial degree of reproductive success even in the face of rather slow growth, etc., compared with that possible in much more productive non-El Niño conditions under which devastating larval predation might completely overwhelm any benefit from accelerated larval growth rate. Item “B”: the extreme fish productivity of the Peru– Humboldt LME The evidently very benign situation off Peru may in large part be due to its low latitude position which results in strong upwelling-driven enrichment, uniquely long particle residence times, and low levels of turbulent mixing energy (Bakun and Weeks, 2008). These factors apparently combine to promote great abundances of diatom cells so large that they can be directly collected even by the particularly coarse filtering apparatus possessed by anchovies, while at the same time being harvested by a community of exceptionally large zooplankton that may constitute ideal objects of the raptorial Active opportunist species as potential diagnostic markers for comparative tracking feeding mode that appears the one most favoured by anchovies (van der Lingen et al., 2006). Following each El Niño disruption during which the ecosystem had been cleansed of profusions of undesirable components, then reset and renewed, the system remains well behaved and predictable in a cyclical sense (i.e. in the more or less repeatable sequence of highly productive transients and the fact that when there is no active El Niño episode underway, differing intensities of the opposite La Niña state do little to seriously alter the basic benign situation). It represents the essence of “anchovy heaven” in which predators of anchovy larvae can be swamped by the shear productive energy of an explosively growing post-El Ninõ anchovy population. Therefore, the efficient anchovy can remain temporarily unimpeded in pursuit of its highly productive “robust” population strategy. When the inevitable next El Niño does hit, the anchovy may be temporarily devastated. However, the sardine may turn the situation to its own distinct advantage by profiting reproductively from the associated reproductive failures of planktonic larval predator populations and of the absence of migratory nektonic predators that need much greater concentrations of zooplanktonic food than could be supplied from fish larvae alone and therefore may refrain from entering the habitat at all, either to feed or to deposit their voraciously predatory offspring. Moreover, the system cannot become durably stunted by development of malignant “eco-feedbacks”, such as has been hypothesized for the northern Benguella (Bakun and Weeks, 2006), because of the periodic cleansing and resetting of the ecosystem by El Niño. [For expanded detail on the cyclic sequence of proposed interacting mechanisms underlying the overall highly productive Peruvian situation, one may refer to Bakun and Weeks (2008).] Item “C”: alternating dominance and item “D”: basin-scale synchrony This particular proposed pattern of interaction could also be expected hold on the longer multiannual to multidecadal time scales. For example, during the period from the early 1970s to the mid-1980s, the eastern Pacific upwelling systems appear to have become more dominated by influence of offshore-oceanic waters (Alheit and Bakun, 2009), similarly characterized by smaller foodparticle spectra, etc. (To what extent this might represent some separate truly longer term phenomena at its base, or be largely a simple effect of a period of raised frequency and strength of individual El Niño episodes is unclear.) But whatever the precise nature of the cause, it can be understood why anchovies, when food particles become too small to be effectively filtered by the gillraker structures of anchovies, might give way to the finer filter-mesh-bearing sardines. In general, this set of considerations would appear to offer an answer to the alternating dominance issue for the eastern Pacific systems, at least for the period following 1970 that is the period for which the indication of alternating dominance may be truly credible (Bakun, 2005b). But how does one explain the northwestern Pacific? As stated earlier, in the neritic ecosystem of the northwest Pacific near Japan which is under the influence of the extremely energetic Kuroshio western boundary current system, the anchovy never approaches peak-abundance parity with the sardine (as is also the case in the particularly energetic upwelling system of the northern Benguela region). In these systems, the anchovy has seldom assumed a position of true dominance other than by virtue of the sardines’ abundance falling very low. According to our inferred conceptual template, sardines appear evolutionarily particularly well-equipped 2287 to take opportunistic advantage of system disruptions. The strong flows and intense turbulent eddy characteristics of these particularly energetic systems appear to offer continuous patterns of disrupted conditions in time and space of exactly the sort that the sardines’ evident adaptations seem designed to accommodate. More than 30 years ago, Skud (1982) had already identified a general pattern in a variety of fish that seem to form interrelated “pairs” (as anchovies and sardine seem to do), such that the population dynamics of the dominant species tends to respond to environmental factors, whereas those of the subordinate species respond to the abundance variations of the dominant one. Therefore, if we assign the dominant wasp-waist role in the neritic ecosystem near Japan as characteristically belonging to the sardine due to the intense nature of the Kuroshio system in which the regional-scale population at least partially operates, the observed out-of-phase alterations fall directly within Skud’s identified pattern. The early 1970s to mid-1980s period, during which sardine populations exploded all around the rim of the Pacific, was characterized by a steep decadal scale decline in the Southern Oscillation Index (SOI) that would of course have been related to an unusual combination of frequent and intense annual-scale declines (i.e. of El Niño episodes). Thus, the enhanced “El Niño” character of this period would naturally seem (see discussion of “item A” above) to favour sardine population growth in the eastern Pacific, if only in terms of a sum total of an increased frequency of successful annual growth episodes. Moreover, the long trend that culminated in a distinct change in the “mean level” of the various indices undoubtedly represented a degree of continually developing reorganization of various ecosystem distributions and relationships that probably involved significant natural evolutionary selection of many short life cycle ecosystem components. The sardine’s intrinsic exploratory, opportunistic tendencies, and capabilities would be expected to be invaluable in tracking a favourable ecological response to the rapidly reorganizing ecosystem context (as expressed in our simplified “comparative advantage” conceptual template, i.e. that “disruption favours the sardine”). Moreover, in addition to the uniquely steep decadal scale longterm trends of the early 1970s to the mid-1980s interval (“boxed” in Figure 2b), the period appears also to have been subject to uniquely energetic shorter 1- or 2-year interannual-scale climatic gyrations. For example, if one counts all the 1- or 2-year incremental differences in the various smoothed 51-year (1950– 2001) series of annual climatic indices assembled in Figure 2 of Tian et al. (2004) [more recently also reprinted as Figure 2 of Alheit and Bakun (2009)], the 13-year (1970– 83) segment contains: (a) the largest (‘81–‘82), the 3rd largest (‘75–‘77), the 4th largest (‘72–‘74), and the 5th largest (‘70–‘72) in the entire 51-year annual mean SOI series, (b) the largest (‘77–’79), the 2nd largest (‘70–’72), and the 4th largest (‘82–‘83) in the winter North Pacific Index series, (c) the largest (’76–’77) and the 2nd largest (’70–’72) in the winter Pacific Decadal Oscillation series, (d) the largest (’76–’77) in the winter Arctic Oscillation series, and (e) the largest (’77–’79) and the 2nd largest (‘73–‘74) in the winter Monsoon Index series. Again the pattern that “disruption favours the sardine” emerges very distinctly. In summary, the continual climatic disruptions that appear to have the characterized the early 1970s to mid-1980s period, coupled with the inference that “disruption favours the sardine”, appear to offer a linkage mechanism for the synchronous dynamics of the widely separated sardine populations located in the far corners of the Pacific basin. This coupled with the observed pattern of 2288 A. Bakun Figure 2. (a) Variations in the abundance of the largest sardine stocks of the Pacific Ocean plotted as percentages of maximum annual values for the period 1970 – 2000, based on landings data taken from the FAO files. (Before the 1990s, most California sardine landings were taken by the Mexican fishery inside the Gulf of California; beginning in the mid-1990s increasing contributions came from US and Canadian fisheries.) (b) “Low-passed: (via 5-point running means of annual mean values) versions of several prominent climatic index time-series. The shaded rectangle indicates the early 1970s to mid-1980s period of steep decadal-scale trends discussed in the text. (Panels redrawn and extended from Bakun and Broad, 2003). out-of-phase population variations of anchovies and sardines (Item C, in our list above) would then work together to rationalize the observed basin-scale synchrony (Item D). Item “E”: the “Law of two” So finally we come to the intriguing item “E” in the list given in the “Introduction” section. Why are there usually two dominant small pelagic species, an anchovy and a sardine, rather than just a single species that turns out to be the superior competitor in each local situation? And why would this intriguing “law of two” seem to hold, not only in highly productive temperate coastal upwelling ecosystems and in the likewise highly productive but dynamically quite different western boundary current situation of the northwest Pacific, but also reportedly in rather oligotrophic semi-enclosed peripheral seas such as the Mediterranean. Even within sub-basins of the Mediterranean, this “law of two” seems to hold in such quite differing physical/ecological situations as the Balearic and Adriatic Seas. Moreover, if more than one species, why not more than two? For example, a “cyclic advantage”-type explanation would require at least three competing species (Matsuda et al., 1991; Sinervo and Lively, 1996). A possibility is that there are ordinarily two, and only two, sufficiently distinct “home-base” habitat segments in any of these boundary ecosystems. One of these is characterized by terrestrial influences, significant turbidity, large suspended organic particles, etc. Here, the anchovy is superior and efficiently outcompetes any interloping other species of small pelagic planktivore. The other sufficiently distinct segment is at the nebulous, uncertain, temporally, and spatially extremely patchy offshore edge of the ecosystem where neritic and oceanic effects merge together. Here, opportunism and flexibility is at a premium, and food particles may typically be very small. Here, the sardine has the ability to “hang on” where potential Active opportunist species as potential diagnostic markers for comparative tracking small pelagic competitors (vertically migrating mesopelagic fish representing an essentially different strategy that does not truly compete with that of the sardine) and extremely damaging concentrations of predator stocks cannot. Therefore these two alternative species groups, anchovy and sardine, could be available and ready at any time, when conditions enable, to break out of their respective “home-base” habitat segments and seize dominance of the extensive intervening in-play zone (“Item ‘C’: alternating dominance and Item ‘D’: basin-scale synchrony” section) of the neritic habitat. According to the conceptual framework being inferred here, the enabling conditions for anchovy breakout might be a period of adequately vigorous primary productivity during which system disruptions tend to be minor (e.g. when after an El Niño episode, the system has stabilized and vigorous primary production resumes). Sardine breakout evidently may be favoured by a major system disruption such as an abrupt drop in primary production (as during an El Niño episode in the eastern Pacific) or by a period of steep trend of change (i.e. continuously progressing disruption) in which a capacity for nimble opportunism may be at a particular premium. A separate sardine genus for the North Atlantic The inference that sardines may depend on system disruption to most effectively exert their evolved opportunistic advantages might derive further credibility from the total absence from the North Atlantic basin of sardines of the genus Sardinops that have very successfully colonized the suitable temperate neritic boundary habitats in the Pacific (both hemispheres) and south Atlantic basins (Sardinops having been the basis of most of the inferences we have drawn with respect to sardines). Most knowledgeable colleagues could probably agree that Sardinops may exhibit opportunistic characteristics to a somewhat greater degree than does Sardina (certainly, Sardinops seems to be much more migratory of the two, as well as much more prone to abrupt distributional expansions and contractions). Sardina is the temperate sardine genus that is currently established in the North Atlantic basin which, of all the major ocean basins on earth, is the one most influenced by continental effects. Land surface possesses little heat storage capacity to serve as “climatic memory”, whereas water in its liquid state has a notably large heat storage capacity. The much larger areas of heatstoring ocean surface compared with land surface in the Pacific and in the southern hemisphere ocean basins allows the climates of these zones to “wander” on multiannual scales much more than in the North Atlantic area, where the interaction of heating and cooling of stationary continental landmasses with a quite precisely cyclic seasonal progression of height of the sun may force the local ocean climate into greater interannual regularity compared with the very large seasonal amplitudes to which the local ocean ecology must be adapted. Thus, one might speculatively conclude that the evolved opportunistic capabilities of the genus Sardinops could be less decisive in the North Atlantic than in the other major basins. Indeed, perhaps much of the evolution of the genus Sardina might actually have been based within the unique conditions of the Mediterranean where the external climate is dominated by continentality while the liquid-water environment exhibits a particularly “oceanic” character due to the relative nutrient impoverishment produced by the “negative estuary” mode of water exchange with the North Atlantic proper. In the continentally influenced North Atlantic, which may thus be less subject to interannual variation in the degree of its system disruption, the genus Sardina 2289 might simply manage to outcompete the genus Sardinops in the characteristic “sardine home-base” habitat segments on the European side of the North Atlantic. The western side of the Atlantic, with its shallow broad continental shelf and very high volume of continental run-off, may simply lack significant “homebase” habitat for sardines. Implications for effects of projected climate changes The foregoing process of step-by-step rationalization of the list of prominent conundrums (Subsections “A” through “E”, above) corroborates the earlier gross characterization (that was based on comparative morphological and behavioural aspects, as well as on inferred evolutionary, aspects) of anchovies as “efficient stay-athome specialists” and of sardines as “nimble wide-ranging opportunists”. Based on this characterization alone, one could guess that sardines might fare better than anchovies as rapid global changes transpire. However, our analysis has also pointed out a “home-base” anchovy environment as being one conditioned by continental run-off. A fairly recent consensus among climate models (Meehl et al., 2007) indicates that on a global-average basis, as greenhouse gases continue to accumulate in the earth’s atmosphere, precipitation will generally increase. This would tend to offer new or enhanced estuarine and coastal run-off-affected zones where anchovies may turn out to be superior competitors. However, the model consensus also suggests that a greater proportion of the subtropics may be affected by drought, which according to the framework developed herein should favour sardines. This tendency for moist regions to become wetter while dry regions become drier is in fact captured by the observational record as well as by models (John et al., 2009). Moreover, due to the increased atmospheric water vapour available to be released from a warmed atmosphere as precipitation due to orographic effects, the increase in rainfall amount is likely to be larger on the windward slopes of mountain ranges (Christensen et al., 2007). Mountain ranges border some of the most important marine ecosystems having wasp waists dominated by the sardine–anchovy species pair. In particular, increased rainfall in the near-coastal zones of Ecuador and Peru, as well as all along the Asian continental boundary of the northwestern Pacific, is indicated in the IPCC Regional Climate Projections (Christensen et al., 2007). Increased precipitation is also projected by IPCC along the North American Pacific continental boundary north of 408 latitude except during summer and, in the northwestern Atlantic, throughout the year along the coasts of the North and Baltic Seas; thus, in these areas, as the anchovy–sardine complexes expand northwards due to warming, they will be expanding into areas where precipitation is expected to be increasing as climate change proceeds, potentially favouring anchovies. This example discussion has of course only scratched the surface in terms of available material for such speculative inferences. To briefly mention another aspect, one currently prominent climate change projection is that the Pacific trade wind circulation may decline as climate change proceeds (Vecchi et al., 2006). The implication would seem to be that the ocean –atmosphere system of the Pacific might shift in the direction of a more chronic, if “low-level”, El Niño-like state. If so, since El Niño conditions have seemed to favour sardines over anchovies on both sides of the Pacific, this aspect might be expected to benefit sardines. But it might presage less intense individual El Niño episodes, which could lessen the “boom or bust” aspect of eastern Pacific marine ecosystems, i.e. perhaps leading to lowered base populations of seabirds and 2290 marine mammals, but conceivably to fewer or less serious incidents of periodic starvation of these highly visible “charismatic” species. Yet, another projection that has been put forth is that upwelling may intensify in the “classical” upwelling ecosystems as climate change proceeds (Bakun, 1990; Diffenbaugh et al., 2004), although it should be said that that particular prognosis remains somewhat controversial (Bakun et al., 2010; Wang et al., 2010). If so, among other major trophic consequences, because of the greater difficulty zooplankton have in maintaining population against increased offshore transport associated with intensified upwelling, the ratio of phytoplankton to zooplankton might be expected to increase (Bakun et al., 2010). This result, as well as the fact that anchovies seem to be somewhat less well adapted to intensified flow systems, would again seem to generally favour the more omnivorous highly mobile sardines over the largely zooplanktivorous, weaker-swimming anchovies. The implications are obvious, important, and diverse, e.g. on aspects including hypoxia, marine “dead zones”, red tides, etc., in addition to distinct effects on spatial aspects of ecosystem support to fishery resource dynamics, etc. (the very heavy use of “etc.” reflecting the very broad choice of potential examples relative to the space that can be afforded to them in a treatment such as this). The salient point here is that a simple conceptual framework such as has emerged from this limited discussion may provide one type of reference with which to try to gauge and begin to understand the nature and significance of developing patterns in ecosystems featuring the anchovy –sardine species pair. Will active opportunist species “steal the stage”? The early 1970s to mid-1980s period (highlighted in Figure 2), in which simultaneous sardine population explosions coincided with steep decadal scale changes in levels of various climatic indices, has featured prominently in our characterization of sardine as being adapted to a rapidly changing (i.e. “disrupted”) situation. Interestingly, this same period also featured strikingly similar “breakout” population increases and following declines in quite a large number of other marine species, particularly within the Pacific Ocean basin [for references, see Benson and Trites (2002) and many sources cited therein] but also more generally scattered throughout the entire global ocean system [for references and sources for additional citations, see Bakun (2005b)]. These included some of the largest, most important fishery resource populations in the North Pacific zone (e.g. Alaska pollock, sockeye salmon, pink salmon, chum salmon, yellowfin sole, Pacific hake, Pacific cod, and many others). In the tropical Pacific Ocean, additional examples included yellowfin and skipjack tunas, various lobsters, seabirds, and coral reef fish, and even phytoplankton and zooplankton distributions. Apparent echoes of this pattern in the Atlantic have involved various stocks of northern cod, as well as extraordinary outbreaks of normally rather uncommon fish species such as triggerfish and snipefish. This leads to an intriguing question. Might the stocks of other species that mirrored the sardine rises during that unique period of steep climatic trends potentially be likewise viewed as “active opportunist” species? And might stocks that appear to have acted during that period in an opposite “anchovy” sense perhaps be usefully viewed, at least hypothetically, as “efficient specialists” that may react adversely to rapid ecosystem changes, but might be able to outpace their less efficient rivals in tracking somewhat more gradual ecosystem trends? If so, we perhaps will have found a sort of new “philosopher’s stone” for turning ostensibly random information into distinguishable emerging patterns that A. Bakun may aid recognition of some overall order within the apparent chaos of complex-adaptive marine ecosystem responses. An initial step could be examination in a similar manner to that illustrated here (e.g. gleaning some enhanced mechanistic understanding via rationalization of existing apparent conundrums in each case, etc.) of each of the species groups and ecosystem types conforming to the same sequential pattern. Undoubtedly such an interregional pattern –recognition exercise could constitute fascinating collaborative intellectual activity. And if successful, and appropriately coordinated, the effort might well contribute towards significantly accelerated understanding and enhanced prediction skill during the coming challenging period of rapid global changes. [One may guess that a similar envisioned need for a coordinated “broader view” of marine ecosystem operation may have been what led Johan Hjort to become a “founding father” of the International Council for the Exploration of the Sea (ICES), within which he served as the Norwegian delegate from its founding in 1902 to 1938, when he was elected ICES President, a position he held until his death in 1948.] Given the vexing lack, in the full century that has elapsed since Hjort’s landmark publication, of substantial progress by the “applied science of fisheries oceanography” towards its major goal of improving fisheries management and marine conservation (Hare, this volume; Houde, 2008), a greater degree of “outsidethe-box thinking” would seem to be called for. Hjort’s celebrated contemporary, Albert Einstien, is said to have remarked that “The eternal mystery of the world is its comprehensibility”. So why has not fishery oceanography produced the sort of revolutionary advances in applications that other sciences have? In answer, it might perhaps be appropriate to cite a second quote from Doctor Einstien: “things should be made as simple as possible, but not simpler”. The currently prevalent reductionist approach addresses an expanding multitude of potential simple mechanisms, each of which is likely to be more or less active at one time or other. One can of course model and simulate these ad infinitum. But since the important events to be understood and ultimately predicted (population collapses, etc.) seem most often to occur on interdecadal time scales, one wonders how the multitude of interacting factors could ever be sorted out sufficiently confidently to support strong corrective actions (Bakun and Weeks, 2006), even in the unlikely event that the system structures would be stationary in a temporal sense, which would seem unlikely in this era of progressing global environmental change? It seems in fact that fisheries oceanography may be caught in a sort of quagmire in which ever more resources seem to be required to follow an ever more reticulated path that seems never to get us much closer to its major goal. Thus, it may be useful to seek more integrated, more holistic approaches wherein an expanded “universe” of diverse experiences might be assembled together within innovative conceptual frameworks that could facilitate recognition of informative emergent patterns ensuing from the superposition of multiple hierarchies of interacting component mechanisms. The notion elaborated in this paper of classifying fish populations according to apparent degrees of evolved opportunistic capabilities and behaviours might perhaps be considered as one possible initial step, even if only a “baby step”, in that direction. Concluding remarks Some readers might feel frustrated that this attempt at a synthesis focusing on anchovies and sardines may not have pointed very directly to any concrete model supporting specific predictions with respect Active opportunist species as potential diagnostic markers for comparative tracking to that particular pair of species groups. But as stressed in the introductory section of this discussion, we seem to be dealing with complex adaptive systems that may be governed ultimately by nonlinear feedbacks. Therefore, earlier hopes for effectively employing a linked sequence of simple linear models appear to be receding (MacCall, 2009b). Drawing a musical analogy, one might say that to a careful “listener”, the real generative action in the ocean system may play less like a set recipe and more like a complex symphony, replete with shifting rhythms and haunting, often scarcely perceived, recurring themes that may never be precisely repeatable. Does such a realization signify defeat? One would think not. It just might have to be accepted that a better approach may be one much less focused on specific model-based predictions and annually reformulated management advice, but rather more directed towards an acquired level of understanding and accumulated experience that supports reasoned expectations as to the “probability vs. consequence” spectrum of potential outcomes of actions undertaken. One simple illustrative example taken from an entirely different context may be that of a particular antibiotic (a different type of likewise valuable, but destructible, resource). One may not be able to reliably predict precisely when a certain antibiotic will begin to fail. But sufficient understanding and experience have accumulated to point out what will make it fail more rapidly (e.g. feeding it to pets and farm animals, ceasing use before a prescribed course of treatment has been completed, etc.). As Houde (2008) has expressed it “Understanding the causes of recruitment variability is a desirable goal; ‘solving the problem’ may be an unrealistic goal”. The value of seeking a spectrum of outcomes, as opposed to narrowly focusing towards identification and elaboration of a most probable outcome, is worth stressing. For example, can one afford to focus totally on maximizing of production of a particularly favoured resource species while ignoring significantly less likely but perhaps much more menacing possibilities (such as transformation of the wasp waste of an ecosystem to durable dominance by infestations of jellyfish, or by hypoxia-producing bacteria, etc.), which may be potentially lurking as yet unrealized out in the tails of the probability distributions? 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