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<I>Calanus Pacificus,</I> a Planktonic

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<I>Calanus Pacificus,</I> a Planktonic BULLETIN OF MARINE SCIENCE, 43(3): 675--{j94, ]988 VARIABILITY AND POSSIBLE ADAPTIVE SIGNIFICANCE OF DIEL VERTICAL MIGRATION IN CALANUS PACIFICUS, A PLANKTONIC MARINE COPEPOD Bruce W Frost ABSTRACT Adult females of a population of Calanus pacificus inhabiting a temperate fjord, Dabob Bay (Washington), exhibited seasonal and interannual variability in diel vertical migration. This variation was unrelated to food availability, in situ growth rate of females, and thermal stratification of the water column. A model of population growth of C pacificus, utilizing a life table approach founded on current knowledge of relevant physiological processes, was used to predict growth rates of migratory and nonmigratory populations and to test the implications of several alternative hypotheses for the adaptive significance of diel vertical migration. It was found that hypotheses invoking metabolic advantages for diel migrants (i.e., that dieI vertical migration is a foraging strategy optimizing individual growth rate) cannot, even when properly recast in terms of population growth, account for observed migration behavior. Rather, the model suggested a significant causal role for mortality op- erating differentially on migratory and nonmigratory individuals. The observations of mi- gration behavior in Dabob Bay are consistent with results of the model of population growth, which point unambiguously toward predator avoidance as the major selective advantage of dieI vertical migration in C pac!ficus. Mounting circumstantial evidence and theoretical arguments implicate pre- dation as a major driving force for diel vertical migrations of planktonic animals inhabiting lakes and areas of the ocean where advective losses are negligible (Zaret and Suffern, 1976; Wright et al., 1980; Stich and Lampert, 1981; Ohman et aI., 1983; Fancett and Kimmerer, 1985; Gliwicz, 1986a; 1986b; Lampert, 1987). However, the difficulty of directly and unambiguously demonstrating, in specific instances, that die1 vertical migration is a predator evasion strategy (e.g., by observing migration behavior under experimental manipulation of predator pop- ulations) has impeded progress in understanding the role of predation (Kerfoot, 1985).Nevertheless, competing alternative hypotheses, when subjected to rigorous experimental and theoretical probing, have been found wanting. For example, potentially testable, alternative hypothetical explanations of diel vertical migration fall into two general categories of optimizing strategies: foraging behavior optimizing individual growth rate (the so-called metabolic models: McLaren, 1963; Enright, 1977),and habitat selection optimizing population growth rate (the demographic models: McLaren, 1974; Ohman et aI., 1983). Diel vertical migration across a thermal gradient is an essential feature of both classes of models. As pointed out by McLaren (1974) and Orcutt and Porter (1983), the metabolic models are incomplete explanations of the evolution of migration behavior be- cause the consequences of optimized individual growth rate are not specified in terms of population growth. However, even when properly recast in terms of population growth (McLaren, 1974), the metabolic models, as well as the de- mographic models, apparently cannot account for observed migratory behavior if based solely on the physiology of population growth as currently understood. Thus, although plausible circumstances can be perceived in which individuals in a migratory subpopulation could grow as fast as individuals in a nonmigratory, surface-dwelling subpopulation of the same species (McLaren, 1974; Enright, 1977), theoretically this cannot by itself confer to the migratory subpopulation 675 676 BULLETIN OF MARINE SCIENCE, VOL. 43, NO, 3, 1988 an advantage in population growth relative to the nonmigratory subpopulation (Wright et aI., 1980; Ohman et aI., 1983), Recent experimental tests confirm the theoretical arguments, at least for freshwater planktonic cladocerans (Orcutt and Porter, 1983; Stich and Lampert, 1984), A surface-dwelling, nonmigratory sub- population will proliferate in numbers faster than a subpopulation whose indi- viduals migrate through a thermal gradient, Unless there is some other disad- vantage to residing continuously in the surface layer, such as higher mortality rate due to predation or a subtle interactive effect of temperature and food concen- tration on individual growth (Vidal, 1980a) or survival, there is no obvious reason, predicated solely on the physiology of population growth, for migratory behavior to arise and persist in populations of planktonic animals. In some planktonic species diel vertical migration is temporally or geographi- cally variable, and study of such species could provide clues to the origin and causal mechanisms of migration behavior (Ohman et aI., 1983). Seasonal and inter-generational variations in diel vertical migration were recently investigated in a population of the marine planktonic copepod Calanus pacificus Brodsky off Southern California (Enright and Honegger, 1977; Koslow and Ota, 1981; Huntley and Brooks, 1982). Although it was suggested that seasonally variable migration behavior in adult females of Calanus pacificus is mediated by availability offood, the specific mechanisms proposed were contradictory. Thus, Koslow and Ota (1981) obtained observations which they suggested were consistent with the idea that when food was very abundant adult females were nonmigratory, or remained shallowly distributed in the water column, in order to optimize their growth and reproduction. Strong diel vertical migrations would presumably occur when food was scarce. On the other hand, Huntley and Brooks (1982) inferred that optimal conditions for feeding and growth (high concentrations of food) promoted the strongest diel vertical migrations in older copepodid stages of C.pacificus, whereas during periods of food scarcity older copepodid stages remained near the surface at all times. Neither interpretation seems entirely compatible with the observa- tions of Enright and Honegger (1977), which indicated strong diel vertical mi- gration by copepodid stage V and adults of C. pacificus during mid spring, late spring, and early summer (see also Mullin, 1986); only timing of the upward migration appeared to vary between seasons, but Enright and Honegger (1977) had no information on food availability. In contrast, Cox et ai. (1983) found no evidence of diel vertical migration in older copepodid stages and adults of C. pacificus during early summer. Alldredge et ai. (1984) observed small-scale geo- graphical variation in vertical distribution and diel vertical migration in copepodid stage V of C. pacificus offBaja California. Based on these observations, C.pacificus seems to exhibit considerable flexibility in vertical distribution and diel vertical migration, but a coherent pattern of variation is not obvious. We examined the relationship between growth rate, estimated as eggproduction rate, and food availability for adult females in a population of Calanus pacificus inhabiting Dabob Bay, Washington (Runge, 1985; Frost, 1985). As part of this investigation, carried out in 1977-1982, and in a more recent study in 1985- 1986, we also determined diel changes in vertical distribution of adult females in three seasons. Strong seasonality in phytoplankton abundance and thermal strat- ification in Dabob Bay (Frost, 1985; Ohman, 1985; 1986) permitted observations of vertical distribution under a broad range of environmental conditions. I report these observations below. In addition to occupying shelf and slope waters of the eastern temperate Pacific Ocean from Baja California to the Aleutian Islands, C. pacificus ranges broadly across the oceanic subarctic Pacific region (Brodsky, 1965). Because environ- FROST: DlEL VERTICAL MIGRATION IN CALANUS PACIFICUS 677 mental conditions for oceanic populations differ greatly from those experienced by shelf/slope populations, some data on vertical distribution of an oceanic pop- ulation in the Gulf of Alaska will also be presented, thus expanding the range of conditions under which vertical distribution of C. pacificus has been observed. However, in this paper I emphasize seasonal and interannual variability in diel vertical migration of adult females of C. pacificus in Dabob Bay, and attempt to interpret the variation in migration behavior with reference to recent hypothetical explanations of diel vertical migration. A model of population growth of migratory and nonmigratory populations of C. pacificus will provide the context for eval- uating the possible adaptive significance of variability in dieI vertical migration. MATERIAL AND METHODS The vertical distribution of adult females of Calanus pacificus was determined at various times of the year at a central, deep (195 m maximum depth) station in Dabob Bay (47°45.5'N, 122°49.5'W). Dabob Bay is particularly suitable for study of diel vertical migration of zooplankton because, due to the bathymetry of the bay and negligible river inflow, tidally-induced horizontal motions in the bay are small (Kollmeyer, 1965; Ebbesmeyer, 1973; McGary and Lincoln, 1977; Jamart and Winter, 1978) and estuarine circulation is negligible (Barnes and Ebbesmeyer, 1978). It is reasonable to presume that the same planktonic population was sampled over periods of a few days. Sampling dates were: 1977 (9-10 VII); 1978 (28-29 IX); 1979 (15-16 III, 11-12 IV, 4-5 VI, 8-9 VIII); 1980 (9-10 VII); 1981 (23-24 X); 1982 (1-2 IV, 29-30 IV, 27-28 V, 9-10 VII, 27-28 VIII,
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