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, 16-17 IX, 21-22 X); 1985 (25- 26 IV, 25-27 VI, 20-22 VIII, 8-9 X, 14-15 X); 1986 (6-8 V, 9-10 VI, 5-6 VIII, 13-15 X). Selected representative vertical distributions are illustrated in Figures 1-4; data for other dates are available from thc author. On most sampling dates, duplicate day and night vertical series of samples were collected, usually near noon and midnight, on 2 successive days and nights with a vertically hauled closing net. In 1977- 1982 a I m (mouth diameter), messenger-operated "Puget Sound" net (Miller et aI., 1984), with 216 !lm mesh, sampled the 0-175 m water column in 25 m strata. In 1985-1986 sampling was done with a multiple-net sampler, configured like the Be net (Be, 1962), carrying five nets programmed to open and close at predetermined depths (Weikert and John, 1981). The sampler, with nets of I m x I m mouth opening and 333 !lm mesh, sampled at least five depth strata in a single vertical haul (175- 125,125-75,75-50,50-25,25-0 m); often the upper 25 m was subdivided (25-10, 10-0 m). Abundance of adult females of C. pacificus in preserved samples was determined from the mean abundance of females in replicate subsamples taken with a Folsom splitter, Stempel pipette, or automatic pipette. The precision of mean abundances in samples based on replicate subsamples varied depending on the number and types of subsam pies. For samples yielding estimates on the order of20 m-3 or greater in a depth stratum, the 95% confidence limits of the mean abundances were generally about 20% or less of the mean. Water samples were collected from five to seven depths in the upper 30 m for determination of chlorophyll a (Lorenzen, 1966) rctained on filters (Gelman GF/F) and on a 10 !lm (sometimes 5 !lm) Nitex screen. On most cruises at least two bottle casts for chlorophyll a determination were made on successive days. Vertical distribution of temperature was usually determined with a CTD, but occa- sionally by bathythermograph. On most dates egg production rate of adult females of C. pacificus was estimated from eggsproduced by females in overnight incubations. The method used in 1978-1979 was described by Runge (1985). In studies during 1981-1982 and 1985-1986 a different method was employed. Shortly after sunset adult females were collected in a vertical net haul, 150-0 m, and sorted into 4-5 screened (500 !lm) cylinders (10 to 20 females per cylinder) immersed in I liter beakers filled with unfiltered seawater pumped from about 30-m depth. The screens permitted eggsto sink out of the cylinders. Beakers were kept in the dark in a refrigerator maintained at 9 to 12°C,the temperature of the mixed layer or lower thermocline. After at least 12h incubation, females were recovered from the cylinders and the contents of the beakers filtered through 73 !lm mesh to collect eggs produced by the females. Incubations were usually done on two successive nights. Runge (1985) found that females of C. pacificus spawned at night, even if incubations began the previous dawn, and that spawning was unaffected by food avail- ability or temperature in short-term incubations. I confirmed the first observation on six dates in 1982 (Frost, unpublished). The vertical distribution of adult females of an oceanic population of C. pacificus was determined at two locations in the Gulf of Alaska: 50oN145°W on 26 July 1975, and 51°NI45°W on 25 July 1978. Duplicate day and night vertical series (8 samples per series) were collected with a multiple-net Tucker trawl (Frost and McCrone, 1974) hauled obliquely over 440-0 m (1975) or 200-0 m (1978). Samples 678 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

were analyzed for abundance of adult females of C. pacificus as described above. Single CTD lowerings and bottle casts were made on eaeh date for vertical distributions of temperature and chlorophyll a, but egg production rate of C. pacificus was not determined,

RESULTS Seasonal and Interannual Variability in Die! Vertical Migration. - Data from 1985 and 1986 provide representative spring, summer and autumn patterns of vertical distribution and diel migration in adult females of Calanus pacificus (Fig. 1). In Dabob Bay the overwintering population emerges from diapause in early March (Frost, 1985), so for each year in Figure 1 the behavior of at least three distinct generations of females is portrayed. One significant feature of the data is that in spring females were either migratory or nonmigratory (Fig. 1A, D). Each pattern was observed in at least one other year (Fig. 2). In contrast, during summer and autumn females were invariably migratory in all eight years for which we have observations from one or both seasons. Thus, my data indicate that adult females exhibit interannual variability in migration behavior in spring, but seem to have a fixed, strongly migratory, behavior pattern in summer and autumn. The relationship of migration behavior to seasonal changes in food availability, in situ growth rate of females, and temperature is examined in the next two sections. The measure of food availability was the abundance of phytoplankton, estimated as the integrated standing stock of chlorophyll a in the upper 30 m. Both total chlorophyll a (i.e., that in particles retained on a Gelman GF/F filter) and the fraction in particles larger than 10 ~m are presented. The latter is in recognition that adult females of C. pacijicus feed inefficiently on particles smaller than about 10 ~m (Frost, 1972; 1977; Runge, 1980; Harris, 1982). The relatively strong relationship between this measure of food availability and growth rate of adult females of C. pacificus, at least in Puget Sound (Frost, 1985; Runge, 1985), is an argument for its utility, but in reality females are omnivores and may, under certain circumstances, obtain significant additional nutrition by feeding carniv- orously (Landry, 1981). Therefore, a second, independent, estimate of in situ nutritional conditions for adult females was based on their measured egg pro- duction rates. Temperature structure in Dabob Bay ranged from isothermal in winter to strong- ly thermally stratified in summer (Ohman, 1986, fig. 2). Because of weak tidal and wind mixing the seasonal thermocline was confined to the upper 25 m and often intersected the sea surface. Moreover, in all seasons thermal gradients below 25 m were very small «2°C/150 m; e.g., Figs. 3, 5). Thus, in the following sections the extent of thermal stratification will be characterized as the temperature dif- ference between the surface and 25 m. Vertical Distributions in Spring. - The two basic patterns of vertical distribution in spring (Fig. 2) were not obviously correlated with food availability measured as abundance of suitably-sized phytoplankton (i.e., cells> 10 ~m) in the surface layer (Table 1). Nor were they related to thermal stratification. In Dabob Bay the water column first becomes thermally stratified during late April or early May, the timing varying from year to year (Ohman, 1986, fig. 2). The nonmigratory patterns occurred under conditions of weak (1985) and strong (1982) thermal stratification, whereas the migratory patterns occurred when the temperature gra- dient was small (Table 1). On the other hand, on both occasions when females stayed in the upper layer (upper 75 m) day and night the egg production rates were very high (Table 1). It is not clear how females were sustaining the high egg production rates in May 1982, in view of the low phytoplankton stock (Table 1), FROST: DlEL VERTICAL MIGRATION IN CAL1NUS PAC/FICUS 679

1985 1986 o

50

100

1,901 1,788 1,305 1,027 150 50m-3

(A) 25-26 APRIL (0) 6-8 MAY 200 o

50

E

I 100 I- 5,637 0- 2,011 w 0 3,149 2,613 150 150 m-3

(B) 20-22 AUGUST (E) 5-6 AUGUST 200

0

50

3,451 100

3,240 150 10,013 I 150 m-3 100m-3

(C) 8-9, 14-15 OCTOBER (F) 13-15 OCTOBER 200 Figure 1. Vertical distribution of adult females of Calanus pacificus in Dabob Bay in 1985 and 1986. For each set of dates, day (clear) and night (blackened) vertical distributions are means of four vertical series of samples collected in pairs near noon and midnight on successive days (e.g., Fig. 2A, B). In this and later figures, italicized numbers beside or under histograms are water column abundances (numbers m-2). 680 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

o

50

100

1,300 1,425 1,825 1,400 2,6T5 2,208 1,950 1,9T5 150

(A) 25-26 APRIL 1985 200 o

50

E

I f- 100 a. W 0 150 2,615

(S) 6-8 MAY 1986 200 - o

50

100

150

200 7,239 6,6T6 301 510

(C) 27-28 MAY 1982 (0) 11-12 APRIL 1979 Figure 2. Vertical distribution of adult females of Calanus pac(ficus in Dabob Bay in spring. In A and B replicate vertical series of samples were collected near noon (clear histograms) and midnight (blackened histograms) on successive days; in C each histogram is the mean of paired day and night vertical series; in D (from Runge, 1981) each histogram is based on a single vertical series of samples.

but these observations were made just at the end of an intense phytoplankton bloom and both the nonmigratory behavior and high egg production rate could be holdovers from the bloom (see discussion and data in Frost, 1985). Alterna- tively, females could have been feeding omnivorously, utilizing stocks of small zooplankton (immature stages, including their own, or microzooplankton) and detritus produced during the phytoplankton bloom. I have no data to evaluate this possibility. It is tempting to infer from these observations (Fig. 2) that in spring females were nonmigratory during phytoplankton blooms in order to optimize their feed- ing, growth, and reproduction, hence fitness (Koslow and Ota, 1981). However, FROST: DlEL VERTICAL MIGRATION IN CALANUS PAc/FICUS 681

TEMPERATURE (OC) CHLOROPHYLL a (mg m-3) o 10 20 0 1.5 3.0 o

50

100

150

I (A) 20-22 AUGUST 1985

.§ 200 r I- a. o 10 20 0 3.0 6.0 W 0 o

50

100

150

(8) 5-6 AUGUST 1986

200

Figure 3. Vertical distribution of adult females of Calanus pacificus, and profiles of temperature and chlorophyll a, during August in Dabob Bay. In both A and B day (clear) and night (blackened) vertical distributions are means of four vertical series collected in pairs on successive days. See Table 3 for integrated phytoplankton abundance and egg production rates.

observations during summer and autumn cast considerable doubt on the impor- tance of food availability and temperature as controlling factors or modulators of diel vertical migrations, at least in these seasons. Vertical Distributions in Summer and Autumn. -In summer in Dabob Bay, when the water column was most strongly stratified thermally, adult females of C. pacificus were always migratory and ranged well into the thermocline at night (Fig. 3), A well-developed subsurface chlorophyll maximum, apparently associ- ated with the strong thermal stratification and depletion of dissolved nitrogenous nutrients in the uppermost 5-10 m (Shuman, 1978), was a characteristic pattern of phytoplankton distribution in summer in Dabob Bay (Fig. 3). Maximum con- centrations of chlorophyll a occurred at 5-10 m in August 1985 and at 10 min August 1986. Thus at night adult females aggregated in the layer (0-10 m) where concentrations of chlorophyll a were highest. The summer observations included years when phytoplankton abundances were both high and low, so that food 682 BULLETIN OF MARINE SCIENCE. VOL. 43. NO.3. 1988

Table I. Temperature gradient (~T, temperature difference between surface and 25 m), mean phy- toplankton stock, estimated as quantity of chlorophyll a in the upper 30 m (range, % of stock consisting of cells > 10 !Lm), and mean egg production rates of Calanus pacificus during spring of years when adult females were migratory and nonmigratory (see Fig. 2). Numbers in italics are numbers of chlorophyll profiles or numbers of females incubated. Data for 1979 from Runge (1985)

t>T Phytoplankton stock Egg production rate ee) (mg chI a'm-') (eggs' female "day') Nonmigratory pattern 27-28 May 1982 6.3 23.8 (22.3-25.3, 15%) 36.9 2 79 25-26 April 1985 2.2 245.1 (190.9-274.7,100%) 39.8 4 182 Migratory pattern 11-12 April 1979 2.5 72.8 (61%) 4.7 1 89 6-8 May 1986 3.2 15.6 (9.4-21.8, 22%) 0 2 150 availability, as well as growth conditions, had no discernible effect on migration behavior (Table 2). In autumn of 5 years females were always strongly migratory despite also ex- periencing widely different conditions of food availability, inferred either from abundance of suitably-sized phytoplankton cells or from egg production rate (Fig. 4, Table 3). Moreover, in October the migrations occurred when the water column was always virtually isothermal (Fig. 5). Thus, basically the same pattern ofvertical migration could occur in autumn, when the water column was nearly isothermal (Fig. 4A, D), as occurred in summer when the water column was thermally well stratified (Fig. 3). Vertical Distribution in the Gulf of Alaska. - In late July of 1975 and 1978, adult females of C. pacific us remained in the upper thermocline or mixed layer day and

Table 2. Mean phytoplankton stock, estimated as quantity of chlorophyll a in the upper 30 m (range, % of stock consisting of cells > 10 !Lm) and mean egg production rates of adult females of Calanus pacijicus in summer. On all dates females made diel vertical migrations (pattern as for August in Fig. I). Numbers in italics arc numbers of chlorophyll profiles or numbers of females incubated. Data for 1980 from Runge (1981). n.d., not determined

Phytoplankton stock Egg production rate Date (mg chI a'm-') (eggs·female-' 'day-') 9-10 July 1980 310.0* n.d. 1 9-10 July 1982 60.2 (55.6-62.4, 35%) 0 3 54 27-28 August 1982 86.0 (60.7-106.5,62%) 22.4 3 68 20-22 August 1985 28.2 (16.8-38.7, 8%) 4.2 4 188 5-6 August 1986 47.3 3.2 1 100 16-17 September 1982 1OI.2 (86.3-116.1,53%) 27.1 2 118

* In the subsurface chlorophyll maximum (12 m) 88% of chlorophyll was in particles retained un a 73-,u.m screen (Ohman, 1983). FROST: DIEL VERTICAL MIGRATION IN CALANUS PAClFlCUS 683

o

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2,488 2,660 410 407 E 200 (A) 23-24 OCTOBER1981 (B) 21-22 OCTOBER 1982 I l- ll. W o 0

50

100

150

11,013 10,124 3,240 3,451 200 (C) 8-9,14-15 OCTOBER1985 (0) 13-15 OCTOBER 1986

Figure 4. Vertical distribution of adult females of Calanus pacificus in Dabob Bay in October of four years. In A and B each histogram is the mean of paired vertical series of samples collected near noon (clear) and the following midnight (blackened); in C and D vertical distributions are means of four vertical series collected in pairs near noon and midnight on successive days. night (Fig. 6). The water column was strongly thermally stratified and phyto- plankton abundance was very low. The same nonmigratory pattern was observed in July 1971, by Marlowe and Miller (1975), and appears to be the typical summer pattern for C. pacificus in the open Gulf of Alaska. Model of Population Growth. -Although diel vertical migration is a conspicuous behavioral attribute of adult females of C. pacificus, observations in spring in Dabob Bay and in summer in the open Gulf of Alaska, together with previous results (Enright and Honegger, 1977; Koslow and Ota, 1981; Huntley and Brooks, 684 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

TEMPERATURE (Oe) 10 20 I

25

E

J: 50 l- n. w o

75

100 Figure 5. Vertical distribution of temperature in October offour years (dates in Table 4) when adult females of Calanus pacificus were strong diel vertical migrators (see Fig. 4). Based on bathythermograph (1981) or CTD casts to at least 50 m.

1982; Cox et aI., 1983; Alldredge et aI., 1984), indicate that the behavior is not genetically fixed in the species. The evolutionary implications and possible adap- tive significance of flexibility in migration behavior are best explored by comparing potential population growth rates of migratory and nonmigratory populations. Given information about the physiology of individual growth, development, and adult fecundity, and appropriate assumptions about food availability, survivor- ship, and reproducti ve life span, the potential population growth rate of C.pacific us can be calculated using a simple life table approach (McLaren, 1974; Ohman et aI., 1983). The following procedure was employed to calculate growth rate of populations of C. pacificus living at constant temperature. Thompson's equations (1982, figs. 1, 4) were used to calculate development time of eggs and time from egg hatching to the adult stage. The calculated development times for copepodid stages fall between those observed experimentally for C. pacificus by Vidal (l980b) and Landry (1983). The effect of temperature on adult body size (dry weight) in C. pacificus was determined, by inspection and linear interpolation, from means of the three maximum body weights at each temperature (8°, 12°, l5.5°C) in Vidal (l980a, fig. 1E). Clutch size was calculated using the relationship of dry weight to prosome length (Runge, 1980) and clutch size to prosome length (Runge, 1984). A life table was constructed assuming excess food, perfect survivorship, initiation of egg production X days after reaching sexual maturity [where X is equivalent to twice the eggdevelopment time (Frost, 1985, fig. 9) for spermatophore-bearing FROST: DIEL VERTICAL MIGRATION IN CALANUS PACIFICUS 685

Table 3. Mean phytoplankton stock, estimated as quantity of chlorophyll a in the upper 30 m (range, % of stock consisting of cells> 10 JLm) and mean egg production rates of adult females of Calanus pacificus in autumn when adult females always made diel vertical migrations (e.g., Fig. 4). On 28-29 September the water column was thermally stratified (- 5°C decrease between surface and 25 m), but on all dates in October the water column was virtually isothermal (Fig. 5). Numbers in italics are numbers of chlorophyll profiles or numbers of females incubated. Data for 1978 from Runge (1981)

Phytoplankton stock Egg production rate Date (mg chI Q'm-') (eggs·female-' 'day-I) 28-29 September 1978 130.0 (90%*) 33.5 1 28 23-24 October 1981 16.8 (14.7-20.2, 5%) o 3 138 21-22 October 1982 87.0 (86.8-89.0, 87%) 3\.0 2 115 8-9 October 1985 27.0 (14.8-40.0,5%) 0.6 4 90 13-15 October 1986 163.9 (106.0-222.0, 100%) 20.9 2 100

* Percent of chlorophyll retained on 5 .urn screen.

females], and production of a clutch of eggs daily for 10 days (PaffenhOfer, 1970; Runge, 1984). For a population living at 13°C the realized rate of population increase (r) is 0.149 day-l (Table 4A). Any delay of development to the adult stage, such as that due to lower temperature, causes the population growth rate to be lower. Thus, for a population growing with perfect survivorship at 9°C, the realized rate of increase drops to 0.103 day-l (Table 4B),even though adult females attain much larger body size and have much larger clutch size than females growing at 13°C. From these two examples it appears likely that if individuals in the population are migratory, and spend any portion of a day below a thermocline, their popu- lation growth rate will be less than that of a population remaining always in or above the thermocline. Extreme cases of migration across a thermal gradient in Dabob Bay are illustrated in Figure 3. If on these occasions females of C.pacificus aggregated in the layer of the subsurface chlorophyll maximum, then they would have experienced, during their daily vertical migrations from 75 m (daytime) to 10 m or 5 m (night), a temperature range of between 3° and 8°C. Three conservative assumptions were made in constructing a life table for a migratory population of C. pacificus: (a) individuals, including eggs (c. pacificus females broadcast eggsnear the surface at night: Runge, 1985), are nonmigratory and live in the surface layer (13°C)from eggfertilization until the end of copepodid stage III (CIII), (b) that diel vertical migration commences in copepodid stage IV (CIV) and persists throughout the remaining lifetime of the copepods, and (c) that migratory individuals (CIV, CV, and females) spend half of the day in deep water (9°C) and half at the depth of the subsurface chlorophyll maximum (B°C). De- velopment times were calculated from Thompson's equations (1982, fig. 1, tables 7, 8), assuming that migratory individuals developed at a mean temperature of 11°C.The body size of adult females (269 f.Lg dry weight) was estimated as follows. Body size of newly molted CIV was 41 f.Lg, the average of mean weights of CIII and CIV in Vidal (1980a, fig. lB, C). Vidal could not discern an effect of tem- perature on body size ofCll1 or CIV, a feature evident also in the marine copepod Pseudocalanus sp. (McLaren, 1974). The mean incremental growth from CIV to adult female at 11°Cwas 228 f.Lg, based on linear interpolation of data for 8° and 686 BULLETIN OF MARINE SCIENCE, VOL. 43, NO, 3, 1988

TEMPERATURE o 5

220

0.5 m-3 330 I E 31 31 (A) ~ 440 ~3' 134 I I- 0 ll. W 0

50 9

100

150

58 168 67 264 (8) 200

Figure 6. Vertical distribution of adult females of Calanus pacificus (histograms) and temperature in the Gulf of Alaska, A, 50oN145"W (26 July 1975); B, 51°NI45°W (25 July 1978). Note different depth scales. Phytoplankton abundance, estimated as chlorophyll a integrated over 0-30 m, was low: 10,8 mg m-2 (A), 14.0 mg m-2 (B).

12°Cin Vidal (l980a, fig. 1C, E). Clutch size was calculated from dry weight as before, but time before start of egg production is 3.7 days, i.e., twice the egg development time at 11°C(Thompson, 1982, 1.84 days, fig. 1). This is consistent with observations (Frost, 1985, fig. 9). Assuming, again, excess food and perfect survivorship, the realized rate of population increase for the migratory population of C. pacificus is 0.141 day-I (Table 4C). This is less than the value for a population living continuously at 13°C(Table 4A). The nearly 3-day delay in development of the migratory stages, relative to nonmigrators, more than counterbalances their increased body size and fecundity. Viewing diel vertical migration as a behavior subject to natural selection, it is difficult to see how the behavior confers a selective advantage on migratory individuals. However, the difference in realized rate of increase for migrators and nonmi- grators is not very great (Table 4A, C) and an obvious selective advantage would FROST: DlEL VERTICAL MIGRATION IN C4LANUS PAC/FICUS 687

Table 4. Life table calculations of realized rate of increase (r) for populations of Calanus pacificus developing in different thermal environments. For columns A and B the populations are assumed to develop at constant temperature; for column C the population is assumed to develop from fertilized egg to copepodid stage IV (CIV) at 13°C, then spend 12 h of each day at 13°C and 12 h at 9°C, simulating a diel vertical migration across a 4°C thermal gradient. To calculate r, development times, sizes (dry weights) at sexual maturity, time of first spawning, and clutch sizes were estimated as described in the text. The first row in each life table is the elapsed time from fertilized egg to appearance of adult females. Upon initiation of egg production (second row in each life table), females produce clutches of eggs (50:50 sex ratio) daily for 10 days. The value ofr was obtained by iteratively solving ~,lxmxe-" = 1.000, where x is age (days), Ixis age-specific survivorship, and mx is age-specific fecundity

A B C 13"C 9°C Migratory (CIV-adult)

Development timcs Development times Development times Egg 1.51 days Egg 2.24 days Egg 1.51 days Hatch-adult 29.05 days Hatch-adult 45.34 days Hatch-adult 31.22 days Adult female 251 /ig Adult female 288 ""g Adult female 269 ""g Clutch size 54.0 eggs Clutch size 64.0 eggs Clutch size 58.4 eggs

Life table Life table Life table

I, x m,

30.6 47.6 32.7 33.6 27.0 52.1 32.0 36.4 29.2 34.6 27.0 53.1 32.0 37.4 29.2 35.6 27.0 54.1 32.0 38.4 29.2

42.6 I 27.0 61.6 1 32.0 45.4 I 29.2

r = 0.1494 day-I r = 0.1027 day I r = 0.1408 day-I

be afforded to the migratory individuals if under otherwise identical conditions they experienced lower mortality rate than migratory individuals. In particular, if young nonmigratory developmental stages of a migratory population suffered the same mortality rate as those of a nonmigratory population, but the older migratory developmental stages experienced reduced mortality, then there would be potential for enhanced population growth of the migratory population relative to the nonmigratory population. To evaluate this possibility using the life table approach, perfect survivorship is no longer assumed. Rather, a constant mortality rate is found for the nonmi- gratory population such that its realized rate of increase is zero (i.e., population at steady state, Table 5A). If the migratory population (first migrating at copepodid stage IV across a 4°Cthermal gradient) experiences the same mortality rate during development, then its population growth rate is, as expected (because mortality acts longer on the migratory, more slowly developing stages), less than that of the nonmigratory population (Table 5B). However, a 50% reduction in mortality rate of only the migrating stages (CIV, CV, adult females), presumed to be the result of their avoidance of the surface layer in the daytime, leads to a substantial advantage in population growth rate (Table 5Q. Assuming simple exponential population growth, stable age distribution and equal initial populations, after only 30 days the migratory population would be more than twice (2.24 times) as large as the nonmigratory population. In fact, only a 12% reduction in mortality rate in the migratory stages gives the migratory population the same population growth rate as the nonmigrating population. 688 BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

Table 5. MortaJity rate (d), survivorship, and hfe tabJe caJcuJations ofreaJized rate of increase Ir) for populations of Calanus pacificus. A, population developing at constant temperature (DOC)and with a mortality rate giving a growth rate of zero. Band C, populations developing from eggto copepodid stage IV (CIV) at 13°C,then spending 12 h of each day at 13°e and 12 h at 9°e, simulating a diel vertical migration across a 4°e thermal gradient. Population in B experiences the same mortality rate as that in A. In population e the migratory copepodid and adult stages experience a mortality rate one-half that of A and B. The value of r was calculated over 10 clutches as described in Table 4; mortality rate of spawning adults is the same as that for elV -adult

A B C d: egg-CIV (day-I) 0.1493 0.1493 0.1493 Survivorshp to CIV 0.0453 0.0453 0.0453 d: elV-adult (day-I) 0.1493 0.1493 0.0746 Survivorship to adult 0.0104 0.0076 0.0185 r 0.0000 -0.0085 0.0274

DISCUSSION The model of population growth of Calanus pacificus. based on current knowl- edge of relevant physiological processes, clearly demonstrates the potential im- portance of mortality, operating differentially on migratory and nonmigratory individuals, to the occurrence of diel vertical migration. Presumably the source of mortality is predation, and an argument will be made for it below. To reiterate a point made by Wright et al. (1980), in studies of the adaptive value of diel vertical migration, predation cannot be discounted, without direct evidence, as a primary causal factor. Implicit in this inference from the model is the notion that predation acts to selectively remove nonmigratory genotypes within the prey population, thereby conferring an advantage to the migratory genotypes that are, over time, increas- ingly expressed within the population. The model suggeststhat replacement could be very rapid, a matter of a few weeks in the case of C. pacificus, if predation rates were high on nonmigratory individuals and food was abundant. Weider (1984) and Dumont et al. (1985) found intraspecific genetic variation associated with differences in vertical distribution and diel vertical migration in freshwater cladocerans. However, this does not exclude the alternative possibility that changes in vertical distribution and migration occur simply, and even much more rapidly, as a result of phenotypic responses of individual prey to the presence of their predators. Induction of prey responses by chemical exudation of predators is known to occur in diverse prey organisms, including zooplankton (Havel, 1987), and die1vertical migration may be similarly induced when predators become very abundant. Thus, the model of population growth places lower limits on the tempo of the population response of prey to differential mortality. Nevertheless, the model should be probed to determine the extent to which violations of its as- sumptions negate its predictions. This will also provide a context for evaluating existing alternative hypothetical explanations of diel vertical migration. Diel vertical migration across a thermal gradient has been accorded considerable significance in the hypotheses of McLaren (1974) and Enright (1977). Residence for part of the day in deep, cool water enhances growth of migratory individuals relative to surface-dwelling nonmigrators, and ultimately results in adult females oflarger body size and with larger clutch size. However, the model clearly shows that although such habitat selection can work to produce larger, more fecund females, it also serves to retard their development, and therefore is a powerful FROST: DIEL VERTICAL MIGRATION IN CALANUS PAC/FICUS 689 limitation to population growth (Table 4). This effectwas appreciated by McLaren (1974) and Longhurst (1976), and has been observed experimentally for freshwater cladocerans (Orcutt and Porter, 1983; Stich and Lampert, 1984). The model is conservative in representing the effect of thermal retardation of development in diel vertical migrators. The assumed pattern of vertical migration (12 h near the surface, 12 h at depth) was based on observed timing of migration in relation to the diel cycle oflight in species of Calanus (Marshall and Orr, 1955; Enright and Honegger, 1977). At times of the year between the summer solstice and autumnal equinox individuals will spend more than the assumed half day at depth, further retarding their development and population growth, relative to nonmigratory populations. Moreover, any tendency for migrators to prematurely or intermittently descend out of the surface layer at night (Pearre, 1973),increasing their residence time in deep water, will also further delay development and retard population growth. Such behavior has not been observed in species of Calanus (Marshall and Orr, 1955; Enright and Honegger, 1977; but see Harding et aI., 1986). Various suggestions have been made about possible effects of food availability on the occurrence of diel vertical migration in species of Calanus (Bohrer, 1980; Boyd et aI., 1980; Koslow and Ota, 1981; Huntley and Brooks, 1982). There is no clear evidence in my data from Dabob Bay for any effect of food availability on vertical migration in C. pacificus. In model calculations it is assumed that food is available in excess. Food limitation is common for C. pacificus (Frost, 1985; tables 1-3; Runge, 1985), and could retard development and result in smaller adult body size of migrators (Vidal, 1980a; 1980b), but it is not clear that food limitation could differentially affect migratory and nonmigratory subpopulations of a species. Also, of course, it is implicitly assumed that diel vertical migrators can obtain at least the same daily nutrition at night as do surface-dwelling, non- migratory individuals that potentially feed all day. Starvation-enhanced ingestion is now well documented in C. pacificus; nocturnal feeders can easily achieve the same daily ration as copepods exposed continuously to food (Runge, 1980; Mackas and Bums, 1986; Hassett, 1986; Mobley, 1987). They also assimilate ingested food with high efficiency(Landry et a1., 1984). This phenomenon was, in fact, an essential element of Enright's (1977) mode1.However, there is increasing evidence of intermittent, usually nocturnal, feeding even in surface-dwelling, nonmigratory species, including Calanus (Baars and Oosterhuis, 1984; Daro, 1985; Head et aI., 1984; 1985; Nicolajsen et aI., 1983). In assuming excess food in the model no obvious bias is introduced in favor of migratory or nonmigratory modes of be- havior. To apply Vidal's (1980a) laboratory observations on growth and adult size of C. pacific us in the model it is assumed that migrators, in their diel vertical mi- gration and nocturnal feeding, incur no additional energetic costs relative to in- dividuals remaining continuously in the surface layer. The energetic costs of swimming and feeding in zooplankton are completely open issues (Torres and Childress, 1983; Abou Debs, 1984; Ikeda and Dixon, 1984; Miller and Landry, 1984; Ki0rboe et a1., 1985; Lampert, 1986). The literature suggeststhat there may be variation among species, but this seems unlikely. In any case, until these issues are resolved experimentally, the specific implications of increased metabolic costs of feeding and swimming in migratory animals cannot be quantitatively evaluated in the model. It can be said, however, that any significant additional cost incurred by migrators, relative to nonmigrators, will likely retard development and cer- tainly reduce growth of the migratory population, making migration, in the ab- sence of differential mortality, an even less plausible behavior than indicated by 690 BULLETIN OF MARINE SCIENCE, VOL. 43, NO, 3, 1988

Table 4. Thus, the model seems conservative and unbiased on this assumption as well. In the model calculations it is assumed that females spawn once daily for ten days and that clutches are 50% female. Both assumptions are conservative (Paf- fenh6fer, 1970; Runge, 1984; Fleminger, 1985). Life table calculations show that lengthening reproductive life span beyond ten days has a very minor effect on estimates of realized rates of increase (e.g., < 5% increase in r for five additional clutches). Similarly, although skewing of the sex ratio of offspring will affect estimates ofr, there is no a priori reason to expect a differential effect on migratory and nonmigratory populations. However, variations in sex ratio of adult copepods can be experimentally induced (Fleminger, 1985) and it is conceivable that mi- grators could have a sex ratio different from nonmigratory populations. Enhance- ment of the female proportion in either population would, of course, enhance its population growth rate. The final major assumption underlying the model is that the migration begins in copepodid stage IV (CIV). This is based on field observations of Cal anus species (Marshall and Orr, 1955; Krause and Trahms, 1982; Williams and Conway, 1984; Mullin, 1986). In fact, migration has been observed, under somewhat unnatural conditions, as early as stage CI in C. pacific us (Huntley and Brooks, 1982). Life table calculations (assuming perfect survivorship, Table 4) show that for C. pa- cificus no advantage is gained by onset of vertical migration in stages younger than CIV; this simply further retards development and decreases population growth rate relative to that reported in Table 4C. By demonstrating the inadequacy of alternative hypotheses (i.e., those of McLaren, 1974, and Enright, 1977), the model points unambiguously toward differential mortality as the ultimate cause of diel vertical migration in C.pacificus. The observations in Dabob Bay provide circumstantial evidence and a possible source of the differential mortality. When diel vertical migration occurred in C. pacificus, it always involved noc- turnal occupation of the surface layer (Figs. 1-4). Although Enright (1977) pro- posed an explanation for nocturnal ascent, based on optimal utilization of phy- toplankton production, there is no evidence, in Dabob Bay or elsewhere (Welschmeyer and Lorenzen, 1985; Whitledge and Wirick, 1983), for the required pattern of phytoplankton standing stock (i.e., greater stock of phytoplankton at sunset) that Enright assumed. Vidal (1980a) made the novel suggestion that, because of the interactive effect of low food concentration and high temperature on growth rate, diel vertical migration might be necessary under such conditions for the survival of older copepodid stages and adults of C. pacific us. This might account for the occurrence of diel vertical migration in summer when the water column is strongly thermally stratified and phytoplankton abundance is often very low. However, such a phys- iological constraint, though certainly possible, would not account for the exclu- sively nocturnal occurrence of C. pacificus in the surface layer; diurnal or even asynchronous forays into the surface layer (Pearre, 1979) ought to be equally effectivebehaviors. Moreover, in Dabob Bay C. pacificus females continued their diel vertical migration in autumn when the water column was cool, essentially isothermal, and frequently contained abundant food (Table 3, Fig. 4). The depth to which females of C.pacificus migrate in the daytime is also relevant to Vidal's (1980a) hypothesis. Observations in spring (Fig. 2A, C) show that nonmigratory females can aggregate day and night in the upper 50 m. Yet when migratory in spring and summer they descended below 50 m in the daytime, and typicallyaggregatedbetween 75 and 125 m (Figs. 2B,D, 3).If the vertical migration FROST: DIEL VERTICAL MIGRATION IN CALANUS PAC/FICUS 691

served merely the physiological necessity to be in cool water for part of the day, then there would be no need for individuals to descend below 50 m because the water column is essentially isothermal below 25 m (Fig. 3). An effect of seasonal variation in solar radiation can be discounted because typical migratory and nonmigratory behavior can occur in the same season (Fig. 2). I hypothesize from these observations and the results of the model of population growth that diel vertical migration in adult females of C. pacific us represents their active daytime avoidance of the portion ofthe water column where they are most vulnerable to visually orienting zooplanktivores (most likely, planktivorous fishes). Seasonal and interannual variation in diel vertical migration could be due to seasonal and interannual variation in abundance of their predators, much as was hypothesized for seasonally and interannually variable reverse diel vertical mi- gration of Pseudocalanus sp. (Ohman, 1983; Ohman et aI., 1983). According to this hypothesis, when mortality exerted by zooplanktivores is low, populations of C. pacificus remain in the surface layer day and night, as expected from the predictions of the model of population growth. Surface swarming, frequently observed in older copepodid stages and adults of species of Calanus (Marshall and Orr, 1955; Cox et aI., 1983) could be taken as indicating low mortality rates due to visual predators. When mortality imposed by visual predators is intense, populations shift into the diel vertical migratory mode of behavior; the shift could be rapid if the response is phenotypically based, slower if the response emerges by selective removal of nonmigratory individuals. When migratory, individuals select a daytime depth based on vulnerability to visual detection by zooplankti- vores. A test of this hypothesis is in progress, for during the study in Dabob Bay in 1985and 1986we also assessed the abundance and distribution ofplanktivorous fishes in hydroacoustic surveys and with several types of nets.

ACKNOWLEDGMENTS

I thank D. Thoreson, J. Newman, J. Lehner-Fournier, S. Bollens, S. Jonasdottir, C. Mobley, w. Peterson, and J. Postel for assistance on various cruises, and G. Heron for analyzing many of the zooplankton samples. Research supported by U.S. National Science Foundation, most recently under grants OCE-8108673 and OCE-8408929. Contribution No. 1739 from the School of Oceanography, University of Washington. This paper was presented as part of the Zooplankton Behavior Symposium funded by Skidaway Institute of Oceanography.

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DATEACCEPTED:April 12, 1988.

ADDRESS:School o/Oceanography WB-lO, University 0/ Washington, Seattle, Washington 98195.