How are the vertical migrations of copepods controlled?

Journal of Experimental Marine Biology and Ecology 329 (2006) 86 – 100 www.elsevier.com/locate/jembe

How are the vertical migrations of copepods controlled? Konrad Thorisson * Marine Research Institute, P.O. Box 1390, 121, Reykjavik, Iceland Received 29 November 2004; received in revised form 6 June 2005; accepted 15 August 2005

Abstract Using Calanus finmarchicus (Gunnerus) as a model organism, a hypothesis is suggested to explain the diel and seasonal vertical migrations of herbivorous copepods in boreal and polar waters. The hypothesis is based on the following assumptions. Hungry copepods are assumed to react to food smell by increased swimming. High lipid content is assumed to turn the copepods upside down. Light avoidance is assumed to operate solely while the copepods are satiated. The following three major peaks in downflux of phytoplankton remains are assumed to reach 1000 m depth or more: pre- and post-spring bloom peaks and the autumn increase. A minor bafternoon peakQ in short-range downflux of phytoplankton is also assumed to exist. The assumptions are used to explain the following main traits in copepod migrations. The afternoon increase in downflux of phytoplankton material induces upward swimming of hungry copepods. If satiated, light avoidance brings them down again at dawn. The late stages of many species of copepods accumulate large amounts of lipids and if the above assumptions are valid, they will be turned upside down and swim down if activated. During midsummer, the downflux does not reach deep water and the copepods are assumed to spend some time in midwater until they moult. Copepods moulting from stage V into female adults use up to half of their lipids to produce eggs, which are more anteriorly located. This is assumed to turn their bodies back into an upright position and the copepods are assumed to swim up to the surface again when they smell sinking phytoplankton remains. Fat copepods are assumed to follow the downflux of phytoplankton material down to diapause depths, especially at the end of the spring bloom and in autumn. It is assumed that enough lipids are used up during the diapause to turn the copepods into head-up position again. The smell of fast-sinking fecal pellets containing prebloom phytoplankton is assumed to bring the copepods up from diapause again in late winter. The probable implications for the survival of cod larvae are discussed. D 2005 Elsevier B.V. All rights reserved. Keywords: Calanus finmarchicus; Cod larvae; Diel migrations; Phytoplankton; Seasonal migrations

1. Introduction In the marine environment, a major part of the energy transfer from primary production to fish passes through the zooplankton. Through their extensive diel and seasonal vertical migrations, the zooplankton animals also make some of the energy from the euphotic layer available to deeper layers (Longhurst and Wil* Tel.: +354 5752000; fax: +354 5752001. E-mail address: [email protected]. 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.08.011

liams, 1992). The most prominent group of animals in this flow of energy are the copepods, in particular the oldest stages. This especially holds true at higher latitudes, where a single species of copepods e.g. Calanus finmarchicus can comprise more than half of the zooplankton biomass over extensive areas (Jaschnov, 1970; Heath et al., 1999; Planque and Batten, 2000). Due to their importance in the marine food web, copepods have been studied intensively for more than a century. As detailed descriptions of the various forms of vertical migrations are easily obtained (e.g. Cushing,

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1951; Hutchinson, 1967), only those aspects that are necessary to explain the proposed hypothesis will be mentioned here. However, it may be helpful to mention a brief history of some of the ideas and hypotheses that led to our present understanding of zooplankton migrations. In 1882, T. Fuchs suggested that the diel vertical migrations of some freshwater crustaceans might be influenced by the light intensity (Longhurst, 1976). Both Rose and Russel later added to the hypothesis and formulated it more precisely for marine copepods (Russel, 1926). Since then, many attempts have been made to explain both the mechanism (Ostvedt, 1955; Rudjakov, 1970; Yayanos et al., 1978; Bollens et al., 1994; Heath, 1999) and the advantages (Hardy, 1956; McLaren, 1963; Zaret and Suffern, 1976; Kerfoot, 1985; Backhaus et al., 1994; Hays, 1995) of these massive migrations. Hardy and Gunther (1935) suggested that migrating behaviour may be modified by hunger and, later, the hunger–satiation hypothesis emerged (Conover, 1968; Pearre, 1979), supported by the laboratory experiments of Huntley and Brooks (1982). The predator evasion hypothesis has some explaining power and has been gaining increasing support (Zaret and Suffern, 1976; Stich and Lampert, 1981; Bollens and Frost, 1989). The effect on copepod buoyancy of the high compressibility and large thermal expansion of wax esters is also slowly emerging (Yayanos et al., 1978; Visser and Jonasdottir, 1999; Campbell and Dower, 2003). All these milestones and many others were important additions to our understanding of the vertical migrations. Some details are still missing, however, especially concerning the seasonal migrations. The hypothesis presented here is one possible way of fitting most of the existing, complicated, and sometimes contradictory evidence on the vertical migrations of copepods into one framework. The hypothesis rests on a few assumptions which do not seem to contradict present knowledge but have not been proven either. Herbivorous copepods in boreal and polar waters are the main subjects of the hypothesis. The model animal is the intensively studied C. finmarchicus, but data on other (mostly) herbivorous copepod species are also used to fill in the picture. In a few cases data on cladocerans from fresh water are also mentioned, as similar behaviour of these animals hint at a wider appeal of some aspects of the present model (Clarke, 1932; Johnsen and Jakobsen, 1987). Different species of copepods have different life strategies, however (Head et al., 1985; Hays et al., 2001; Gislason, 2003), and the overwintering survival strategies of some copepods are radically different from those of C. finmarchicus. Some copepod species produce resting or diapause

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eggs (Johnson, 1980; Lindley, 1990), other species are active all year round (Heinrich, 1962) and lipid storage is very variable between species (Davis, 1976; Tiselius, 1992; Norrbin, 1994). In spite of these differences, some of the basic principles may apply to a variable degree to other herbivorous and omnivorous copepod species, to other areas, to some carnivorous copepod species and even to some freshwater cladocerans. 2. The hypothesis The assumptions of the present hypothesis are the following: – Satiated copepods maintain low activity, but avoid bright light – Hungry copepods increase their swimming activity when they smell food – High lipid content may reverse the direction of swimming. To make the hypothesis work, there are two additional requirements concerning the phytoplankton: 1) there needs to be an afternoon/evening increase in the downflux of phytoplankton material during the productive season; 2) there also needs to be a considerable increase in downflux of marine snow to deep water, a) shortly before the spring bloom, b) right after the spring bloom, and c) during the autumn maximum in phytoplankton. There are some indications that these requirements may be fulfilled and supporting references will be given when appropriate. The scope of this paper, however, only permits a limited discussion of the phytoplankton-related topics. To simplify the description of the hypothesis that follows, let us assume that the assumptions above are valid. 2.1. Diel migrations Starting in the mixed surface layer in the early hours of a summer day, satiated copepods are hanging motionless or slowly sinking with their antennae stretched out, in a head-up position. At sunrise, the satiated copepods start swimming downwards to avoid the bright daylight. Many copepod species end up below the thermocline, at say 50–150 m depth, where the light level is presumably more comfortable. The copepods rest down there for a few hours, until they become hungry again. Even if hungry, however, the copepods maintain their low level of activity as long as they do not smell food. It is suggested here that the amino acids released from the decomposing phytoplankton cells

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2.2. Seasonal migrations

within marine snow aggregates trigger the ascent of the copepods in the afternoon/evening. As the copepods smell food, the hungry ones start swimming upwards as their natural position in the water is head up. As swimming and feeding are closely linked activities in many copepod species, they feed as they swim towards the phytoplanktonrich surface waters. The copepods can probably become satiated in an hour or two during blooms but when phytoplankton is scarce it may take longer and satiation may even not be attained before dawn. Those copepods that manage to become satiated soon after sunset become inactive, and probably sink slowly during the next 3–6 h. They may still be in the phytoplankton-rich layer when they become hungry again and, triggered by the food smell, they begin feeding and swimming upwards again. This will create a second maximum of copepods at the surface just before dawn. At sunrise, however, all satiated copepods swim down to lower light levels. During blooms, the water is less transparent and the light level comfortable for copepods may lie above the thermocline, which will keep the copepods constantly in the convective mixed layer. The high primary production increases the downward flux of marine snow so that even the copepods sinking below the thermocline are encouraged to swim up again as soon as they become hungry since they avoid bright light only when satiated. At times this unsynchronized behaviour of individual copepods may give the impression of no diel migration. A similar situation may prevail throughout the short summer at high latitudes.

When phytoplankton is abundant in the surface waters the oldest stages of many copepod species (especially stages CIV and CV) deposit large amounts of fat in their oil sacs. Initially the oil sack of C. finmarchicus is sausage shaped (Fig. 1b) and extends along the entire length of the body. The more dorsally situated (Fig. 1b) low density oil may balance the body to a more horizontal position at this stage. Additional lipids, however, are mostly deposited into the posterior part of the oil sack (Fig. 1c). The lipids are of a considerably lower density than the surrounding seawater, hence the center of gravity of the copepods is moved forward and the copepods are turned upside down. The abundant phytoplankton in the surface waters encourages hungry copepods to swim, and because fat copepods are pointing downwards, they swim downwards. After some time, at intermediate depths, stage CIV copepodites will moult into stage CV and stage CV copepodites will moult into sexually mature adults. In the females, a large part of the lipids is used for egg production. The lipid-rich eggs are distributed more anteriorly in the body (Fig. 1a) and if positively buoyant will add to the buoyancy of the anterior end and help to turn the female copepod back into the head-up position. After moulting of stage CIV into stage CV, the oil is probably distributed more thinly inside the larger body, which may decrease the buoyancy of its posterior end. Individuals that are not turned all the way into a head-up position may be encouraged by phytoplankton smell to swarm by horizontal swimming. However,

eggs oil

oil

oil

a

b

c

Fig. 1. Calanus finmarchicus. (a) A drawing of a female with eggs in ovary. Note more anterior distribution of eggs at this stage. Just before spawning, the egg mass may, however, extend through the whole length of the body. (b) Lean form of a stage CV copepodite with oil sack of relatively uniform width. (c) Fat form of CV with large oil sack, which fills up about half the body volume. Note the more posterior distribution of the oil. In extremely lipid rich cultivated individuals the oil can fill almost the whole body, but if this happens in nature is not known. Images (a) and (b) are from Marshall and Orr (1955); (c) courtesy of Dr. K. Tande, Norway.

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when the upwards-pointing copepods are encouraged to swim by phytoplankton smell, they swim back towards the surface and start feeding and/or spawning. It is here assumed that there are three annual peaks in the downflux of marine snow, i.e. just after the spring bloom of phytoplankton, after the autumn increase and in late winter before the formation of a stable thermocline. Just after the spring bloom, the peak in downward flux of phytoplankton material will encourage some of the fat copepods (the ones containing the most lipids?) to swim all the way down to diapause depth (Irigoien, 1999). In autumn fat copepods will be assisted in their diapause descent by sinking cold water containing phytoplankton material. By the autumn, however, some copepods at diapause depth may have attained the vertical head-up position. These individuals may be cued by the autumn pulse of downflux to swim up to the surface again, to meet with the meagre survival potential of winter. C. finmarchicus spend their diapause at about 500– 1500 m depth depending on latitude (how deep the organic matter reaches?), and possibly also depending on their lipid content (Jonasdottir, 1999). Whether the copepods reach some kind of a bbuoyancy equilibriumQ at the diapause depth is unclear, but if so, it is probably unstable and fat copepods may be flipped over from a tail-up position above this bequilibriumQ level to a headup position below. The encouragement to spend energy by swimming for food must be very low, however, because of the low concentration of food particles at this depth especially during winter. The low ambient temperature below 500 m depth lowers the metabolic rate of the overwintering copepods even further. In midwinter, the CV copepodites in diapause start to mature sexually and, during the maturation period, the female C. finmarchicus breaks down about half of its stored wax esters (Gatten et al., 1980) which reduces the buoyancy of the posterior end. In a similar manner to the copepods in midwater during summer, the center of gravity of these females is moved backwards and these copepods will then be pointing upwards again. With increased downflux of marine snow in late winter, the smell of decaying prebloom phytoplankton encourages the copepods to start swimming again, and they will swim upwards as they are already pointing in that direction. Copepods low in lipids in autumn may have to spend the winter in the convective mixed layer with a corresponding high mortality. Together with the CV copepodites and adults resurfacing during the autumn downflux, they may nonetheless play an important role in the seasonal cycle of migrations. As the surviving

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animals in late winter feed on the prebloom phytoplankton, they release fast-sinking fecal pellets that increase the magnitude and downward reach of the downflux which will increase the chances of copepods in diapause receiving this prebloom signal. 3. Discussion of assumptions Before a general discussion is attempted, the assumptions stated above for the present hypothesis will be reviewed separately, together with some supporting and contradicting references. 3.1. Satiated copepods maintain low activity, but avoid bright light Feeding and movement are closely linked functions in many copepod species (van Duren and Videler, 1996) and, as the copepods stop feeding when satiated (Frost, 1975; Head et al., 1985), the urge to move will be reduced. Satiated copepods have been observed to hang motionless, with their antennae stretched out, in a head-up position (Hardy and Bainbridge, 1954) and as Cushing (1951) suggests, bThus the midnight departure of plankton animals from the surface might well be due to the fact that the activity of individuals has been reducedQ. Furthermore, as the first two naupliar stages depend on egg reserves we can probably assume that they do not become hungry and maintain low activity during these developmental stages (Titelman and Kiorboe, 2003). As soon as they become dependent on external food, however, the third stage nauplii become hungry and start swimming upwards (Durbin et al., 2000). Despite the reduced activity level of the satiated copepods they swim downwards when they encounter bright light (Russel, 1926; Hardy and Bainbridge, 1954). The feeding urge seems to be stronger than light avoidance, however, as the following quote on Calanus pacificus indicates: bWhen phytoplankton was abundant and individual ingestion rates were high, copepods performed high-amplitude migrations. As food availability declined, however, and the competition for food increased, migration amplitudes decreased and then ceased altogether so that copepodites remained in the relatively food-rich surface waters at all timesQ (Huntley and Brooks, 1982). Similar results have been reported for Calanus agulhensis (Hugget and Richardson, 2000), Calanus chilensis, Eucalanus inermis, Eucalanus subtenuis, Centropages brachiatus (Boyd et al., 1980) and even for some freshwater cladocerans (Johnsen and Jakobsen, 1987).

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Light avoidance is not without exceptions however (Clarke, 1934; Marshall and Orr, 1955). In Arctic regions, Calanus hyperboreus and Calanus glacialis stay close to the surface during both night and day, although they may stop feeding during the day (Head et al., 1985). The present hypothesis cannot explain the diel variation in feeding, however, unless the digestion is slowed considerably by the low (even sub-zero) ambient temperatures (Dagg and Wymann, 1983). In polar areas, where the autumn increase in phytoplankton is practically an extension of the spring bloom, there is steady downflux of material during the whole summer (Noji et al., 1999). If the above assumptions are valid, the steady downflux will trigger upward swimming as soon as the copepods become hungry. Hence, at all times, some individuals will be swimming up while others are sinking and thus the overall depth distribution will not change much during a 24-h period (Pearre, 1979). Copepods bumping against the surface film, even in bright sunlight (Cushing, 1951; Marshall and Orr, 1955), is another exception to the light avoidance. According to the present hypothesis this may happen when the phytoplankton concentration is too low so that the copepods do not manage to become satiated. In the afternoon, when the phytoplankton cells increase their production and release dissolved free amino acids, lean copepods are encouraged to swim upwards, including those that happen to be close to the surface. The dawn increase in numbers at the surface reported for copepods, as well as for many other zooplankton groups (Cushing, 1951), may seem incompatible with light avoidance. During phytoplankton blooms, however, C. finmarchicus is able to fill its stomach in about 1–2 h (Simard et al., 1985). The animals digest a full stomach in about 1–3 h (Huntley et al., 1987; Dagg and Wymann, 1983; Simard et al., 1985) although digestion may be faster in smaller species. The copepods probably get hungry again within the next 2–3 h (Simard et al., 1985; Stearns, 1986; Pavlova, 1994), and it is here assumed that the copepods sink passively when they are not feeding (Cushing, 1951; Rudjakov, 1970). The dawn increase can thus be explained as a second ascent of hungry copepods close to dawn. If the above reasoning holds, it would mean that no dawn increase could take place in low concentrations of phytoplankton, or if the nights are short. Both effects are conceivable (Bogorov, 1946; Huntley and Brooks, 1982) and those effects may be an easily investigated check on the present line of reasoning.

Below the thermocline there is less phytoplankton to encourage the copepods to feed when they get hungry again, at least until in the afternoon, and thus they do not resurface until close to dusk. Dagg and Wymann (1983) proposed an alternative explanation for the long time between meals below the thermocline. Their view is that the gut clearance may be temperature-dependent and a longer non-feeding period below the thermocline could thus be a consequence of the lower temperature. 3.2. Hungry copepods increase their swimming activity when they smell food Bainbridge (1953) found that more C. finmarchicus swam upwards in the presence of cultures of diatoms than in filtered seawater. Starved female Temora longicornis also swam faster than non-starved ones in the presence of Rhodomonas sp. (van Duren and Videler, 1996). With no food present, the basic swimming speed of adult Temora longicornis seems to be close to 2 mm s 1, but when food is offered, the swimming speed of the animals increases to 5 mm s 1 or more (van Duren and Videler, 1995, 1996). The swimming behaviour of some copepods in the presence of phytoplankton, however, is characterized by a decrease in average swimming speed and an increase in bpauseQ behaviours compared to their swimming behaviour in filtered seawater (Buskey, 1984; van Duren and Videler, 1995). Some of the copepods in these experiments may have been satiated, however, and although the activity of copepods may be increased by food smell, the act of catching, handling and ingesting may result in a slower overall travelling speed (Buskey, 1984; Tiselius, 1992) when phytoplankton is abundant. However, not only intact phytoplankton cells can activate the copepods. For example the copepod Pseudocalanus minutus increased its average swimming speed and the number of burst swimming, when presented with filtered phytoplankton exudate (Buskey, 1984). Furthermore, it has also been shown that dissolved free amino acids alone stimulate feeding responses in copepods (Poulet and Ouellet, 1982; Gill and Poulet, 1988). The bfood smellQ that the copepods react to when hungry may thus be amino acids. 3.3. High lipid content may reverse the direction of swimming The most common position of copepods in the water is probably the head-up posture (Hardy and Bainbridge, 1954). When phytoplankton is most abundant in the surface waters, however, the oldest stages of many

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copepod species deposit large amounts of lipids in their oil sacs (Miller et al., 1998; Jonasdottir, 1999). In the genus Calanus the lipid content can reach over 70% of dry weight (Lee, 1974; Bamstedt, 1986). As long as the oil content is moderate the oil sack of C. finmarchicus is sausage shaped (Fig. 1b) and extends along the entire length of the body (Marshall and Orr, 1955). Additional lipids, however, seem to be deposited mostly into the posterior part of the oil sack (Fig. 1c). The contents of the oil sack are pure wax esters (Miller et al., 1998) and the average density of wax esters is only 0.86 (Lewis, 1970). The average density of proteins, on the other hand, is 1.33 (Denton and Marshall, 1958). The uneven distribution of lipids and proteins in fat copepods (Fig. 1c) must result in a stable upside-down position even when the specific gravity of the whole copepod is equal to that of the surrounding water. If, however, the specific gravity of the copepods is less than the specific gravity of the seawater, the copepods will, solely by the drag of the antennae, be oriented with their tails facing upward (Rudjakov, 1970). Not all copepod species store such large quantities of lipids, however, and some copepod species, especially the smaller ones, neither accumulate large amounts of lipids (Norrbin et al., 1990) nor do they enter diapause during the winter (Davis, 1976). Hence, the following applies only to those species that do. Both in situ observations and experiments with C. finmarchicus show minimum lateral movement and that, at any one time, some of the active copepods are swimming up and some are swimming down (Bainbridge, 1952; Simard et al., 1985). In the presence of food, starved copepods seem more upwards oriented: b. . .a greater proportion of animals swimming up was always found amongst samples that had been obtained several days previouslyQ (Hardy and Bainbridge, 1954). The lipid content of the animals does indeed seem to influence their behaviour, as the few C. finmarchicus animals found in the surface layers during winter contain much less fat than those that swim down to deeper layers (Hirche, 1983; Jonasdottir, 1999). Similar results have been reported for C. hyperboreus. Individuals of Metridia pacifica containing small lipid reserves migrated to the surface to feed, while individuals of the same species with large oil sacks remained, both day and night, close to the bottom at about 150 m depth (Hays et al., 2001). 3.4. The phytoplankton-related requirements As mentioned earlier the hypothesis has some additional requirements concerning phytoplankton. As the term phytoplankton is a collective term for a diverse assemblage of very different organisms, it should be

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noted that for the purpose of this paper the main concern is with the diatoms group, a pivotal player in the main blooms. During prebloom and summer, other groups (mostly smaller) are more important. If every detail of the present hypothesis is to work, all the above requirements must be fulfilled but in spite of the support from the literature given below some of these statements will remain debatable. Nonetheless, for the sake of clarity, these assumptions will, in the General discussion section that follows, be treated as justified. 3.4.1. Afternoon/evening increase in downflux of phytoplankton material Natural phytoplankton assemblages have diel periodicity in growth and diatom cell division (Eppley et al., 1967, 1971; Smayda, 1975), and there is a pronounced diel variation in the concentration of dissolved free amino acids in surface waters, with highest concentrations in the afternoon/evenings (Mopper and Lindroth, 1982). There also seems to be a diel variation in the sinking of phytoplankton, usually with increased sinking rate in the afternoon (Sournia, 1974; Anderson and Sweeney, 1977; Bienfang et al., 1983). The sinking rate, of the order of 1 m day 1 (Bienfang, 1981) is too slow, however, to mediate the signal of increased primary production to the copepods below the thermocline within hours. Marine snow, however, may be able to carry the signal up to 100 times faster (Shanks and Trent, 1980) and large fecal pellets from large copepods, euphausiids and salps sink even faster (Small et al., 1979; Andersen and Nival, 1988). There is also diel variation in the downflux of marine snow (Lampitt et al., 1993a; Graham et al., 2000) and large zooplankton animals may remove marine snow from the surface waters during the night and release it again in fecal pellets during the day in deep water (Lampitt et al., 1993b; Graham et al., 2000). 3.4.2. Increased downflux in late winter, at the end of spring bloom and in late autumn A peak in downflux right after the spring bloom is well established (Lampitt et al., 1993a; Smith et al., 2002). The elevated downflux can reach at least several hundred meters down (Bishop et al., 1977; Hargrave and Taguchi, 1978; Silver and Gowing, 1991), but as the organic content of the marine snow is rapidly reduced (Bishop et al., 1977), repackaging by e.g. non-diapausing copepods, migrating euphausiids and amphipods may be needed to carry the signal down to 1000 m depth or more (Lampitt et al., 1993b; Graham et al., 2000). High chlorophyll values, comparable to early bloom levels may also be reached a month

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before the start of the spring bloom proper (Richardson et al., 1999). Hence, during several weeks before the spring bloom a substantial amount of organic matter is available for precipitation in the form of marine snow (Lampitt et al., 1993a; Graham et al., 2000; Noji et al., 2001) or inside fecal pellets. This peak in downflux of organic matter may be the signal that encourages the copepods in diapause to swim up to the surface waters again in late winter. There may be a third peak in downflux in the autumn (Lohrenz et al., 1992; Noji et al., 1999). The autumn peak in primary production is more irregular and not as strong as the spring bloom, however, but when it is prominent it will probably stimulate increased downflux of organic matter as well (Taylor, 1989). 4. General discussion It should be stressed here that some aspects of copepod migrations may be more easily explained by simple reactions to environmental stimuli or internal clocks. It has, for example, been suggested that different times of descent combined with a slow development rate during diapause may be the triggering mechanism for ascent in late winter (Heath, 1999). That the largest animals emerge first (Miller et al., 2000) seems not easily compatible with this suggestion however. A simple preference for some low light level may be enough to keep carnivorous copepods constantly close to the maximum of their prey density. There is also the possibility suggested by Huntley (1988) that the copepods respond to an integral of past forces, instead of just to the present values. If the required assumptions presented here turn out to be valid, however, the present hypothesis can explain the majority of the diel and seasonal vertical migrations of many herbivorous copepods including C. finmarchicus. Although phytoplankton is less important in the diet of omnivorous copepods, it is nonetheless conceivable that the same phytoplankton related mechanisms are used to direct their migrations. If all suggested ideas of the present hypothesis are to be tested, however, some new data are undoubtedly required, although some aspects can probably be tested with data that already exists. That exercise might be worthwhile, however, if only to get a new perspective on the somewhat stale problem of the vertical migrations of copepods. It is tempting to try to fit more data into the present hypothesis e.g. by speculations such as that reverse migrations may be caused by the upside-down position of fat copepods and therefore only those species that

deposit large amounts of lipids bfloat upQ in this way. Until the present hypothesis is either proven wrong or supported by some experimental evidence, however, it is too early to try to fit every detail of the vertical migrations of the copepods into it. Nevertheless, some supporting and contradicting evidence concerning the main migration traits are worth mentioning. 4.1. Synchronization of migrations The diel vertical movements of copepods are probably never completely harmonious (Hardy and Gunther, 1935; Simard et al., 1985). Low stock of phytoplankton may e.g. keep some C. pacificus individuals at the surface after sunrise (Huntley and Brooks, 1982), while other individuals of the same species may become satiated at various times of the night. The same applies for the copepods below the thermocline if the stated assumptions are valid, since some individuals will be aroused earlier than others and swim up to the surface during daylight hours. On the seasonal scale the harmony is obviously not perfect either. In spring, some individuals of e.g. C. finmarchicus may be ascending late from deeper waters (Ostvedt, 1955), possibly even after the spring bloom, while other individuals of the same species may simultaneously be descending towards an early diapause (Hirche, 1996; Heath, 1999). Some of the individuals that enter diapause early may even be encouraged by the downward flux of marine snow and phytoplankton in autumn to ascend from diapause early (Heath et al., 2000). It comes as no surprise then that students of diel and seasonal vertical migrations have been reporting divergent, mixed and sometimes contrasting results. 4.2. Predator avoidance A factor not specifically addressed in the present hypothesis is the possible influence of predators on the vertical movements of copepods (Zaret and Suffern, 1976; Kerfoot, 1985). By the above suggested mechanism, however, the copepods will avoid visually aided predators simply by spending the day below the euphotic zone, but only when well fed. Satiated copepods will thus no longer risk predation to get food, but instead they avoid strong light and thereby avoid predation during the day. When predators are present, an increased range, or even a reversal, of diel vertical migrations has sometimes been registered and this has been interpreted as predator avoidance. Such is probably the case with the reported short distance predator avoidance of Acartia

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hudsonica (Bollens et al., 1994), but some cases of more far reaching avoidance may be chemically induced (Neill, 1990). Where enormous schools of pelagic or mesopelagic fish roam, however, the margins of distribution of the copepods may conceivably be moved by tens of meters, perhaps by a combination of short distance avoidance and annihilation of the top and/or bottom margins of their vertical distribution (Bollens and Frost, 1989; Gasser et al., 1998). Predators do not necessarily increase the diel vertical migration, however, since Dale and Kaartvedt (2000) observed that the strongest diel vertical migration of C. finmarchicus was where the abundance of the visual predators herring and mackerel was the lowest. 4.3. Energy used during diapause Visser and Jonasdottir (1999) report that fat copepods reach bequilibrium densityQ at depth even if they are positively buoyant at the surface. According to their calculations the average C. finmarchicus will be overwintering at around 700 m depth (Visser and Jonasdottir, 1999). The high compressibility and large thermal expansion of lipids, however, makes the neutral buoyancy unstable (Campbell and Dower, 2003). The similar lipid contents of stage CV in deep water throughout the winter (October–March) has been interpreted as low energy cost of diapause and molting (Jonasdottir, 1999). This is not necessarily the case, however, as the leaner individuals may leave the diapause depths early. Use of lipids during the winter may also shift the bequilibriumQ depth upwards. As an example the average winter depth of C. finmarchicus south of Iceland decreases from 850 m in late November to 400 m in late January (Gislason et al., 2000). In any case, it is not to be expected that the difference in lipid levels between repeated samples of copepods from the same depth strata is representative of the energy used up during diapause. 4.4. Arousal in late winter It has been suggested that it is the increasing light intensity in late winter that triggers the ascent of the copepods from the deep water diapause (Russel, 1927; Miller et al., 1991). This view is hard to accept, however, for the following reasons. At the diapause depth for C. finmarchicus at about 408N, which is about 500 m, maximum light intensities in summer are probably close to the limit of the light sensing capability for crustacea (Miller et al., 1991). In boreal waters the surface illumination is appreciably lower and at the

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arousal time in February the surface illumination is much lower still. To make things more difficult, the resting depth for the copepods at high latitudes is 2–3 times deeper (Ostvedt, 1955). It is thus highly unlikely that light can be directly responsible for the spring ascent of Calanus. The temperature stability below 1000 m depth makes a temperature-based cue for ascent hard to accept as well. Furthermore, in upwelling areas in the tropics the emergence of copepod species such as Calanoides carinatus (Kroyer) can hardly be explained by the negligible seasonal light changes (Idrisi et al., 2004). The emergence from diapause is highly asynchronous, which suggests that it is not triggered by simple environmental cues. The arousal mechanism proposed here is the increased downward flux of phytoplankton and marine snow in spring, before the stabilization of a thermocline at the surface. The spring maximum in downward flux of phytoplankton material matches approximately with the emergence, and it varies interannually in time, duration and magnitude. The timing of the maximum in marine snow flux (Smith et al., 2002) is roughly simultaneous with the ascent time of the copepods (Ostvedt, 1955), and the depth to which organic matter reaches (Bishop et al., 1977) is about the same as the overwintering depth of C. finmarchicus (Kaartvedt, 1996). Further, the delayed time of spring bloom with latitude (Strass and Woods, 1988; Dale and Kaartvedt, 2000) is one possible explanation of the general tendency of C. finmarchicus in low latitudes to emerge from diapause earlier than those at higher latitudes (Planque and Batten, 2000). 4.5. High latitudes The actual amount of lipids necessary to survive the overwintering period and to produce eggs or sperm in spring may be influenced by whether the neutral buoyancy depth (Visser and Jonasdottir, 1999) is within or below the convective mixed layer (Irigoien, 2004). Only a limited number of the animals descending in midsummer, however, may survive until the next spring (Irigoien, 1999). For C. hyperboreus, the first stage able to survive the winter may actually be stage CIII (Ostvedt, 1955) but the example given here will be the more common stage CIV. At high latitudes, where the summer is extremely short the generation time of some copepods, e.g. C. hyperboreus, can exceed 1 year (Conover, 1965). As winter sets in, some copepodites may only have reached stage CIV and, when they return to the surface from diapause the next spring, they moult into stage CV. If the summer is productive enough, they

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may be able to reach the adult stage and spawn. Alternatively, the rest of the short summer will be spent depositing fat as stage CV. Sexual maturation and spawning then has to wait for the prebloom production in the third year. At very high latitudes, the growth season may even be short enough so that the only animals able to complete the generation cycle in the second year are those that descended during the first autumn as fat stage CV copepodites. 4.6. Tropical/subtropical areas Between about 508N and 508S the environmental conditions are more stable than at higher latitudes (Longhurst et al., 1990). The persistent pycnocline acts as a barrier for nutrient replenishment and to the sinking of the phytoplankton (Silver and Gowing, 1991). Phytoplankton species are generally small and the productivity is rather low with low seasonality (Heinrich, 1962; Bienfang and Harrison, 1984). The local copepod species do not enjoy the same competitive advantage as copepods in higher latitudes and other zooplankton taxa are more prominent in these waters. It is probably exceptional if copepods become fat enough, according to the present hypothesis, to be turned upside down and thus they stay constantly in surface waters. In the mixed surface layer some of the copepods probably manage to become satiated during each night, however, and those individuals are presumably driven down by the dawn light. Usually, there is a deep chlorophyll-a maximum in these waters (Bienfang and Gundersen, 1977; Bienfang et al., 1983), which will release amino acids during the afternoon, which may trigger these copepods to swim upwards at dusk. 4.7. Upwelling areas There are strong indications that diel vertical migrations in upwelling areas are directly linked to food availability (Hugget and Richardson, 2000). If the above assumptions hold, the present hypothesis may also help to explain how the life cycle of copepods is maintained in upwelling areas. Each pulse of upwelling deep water provides the necessary nutrients for a growth spurt of phytoplankton. Provided that the upwelling pulse is of sufficient duration, some copepods will manage to finish the development from eggs to stage CV and deposit enough fat to be turned upside down during the pulse. When the available nutrients are finished, aggregates of phytoplankton cells probably start to sink down to deep waters (Smith, 2001). If the assumptions of the present hypothesis hold, the

fat copepodites will then follow the downward flux of marine snow, into the deep landward countercurrent, to be returned in the next upwelling pulse as spawning stock. 4.8. Shelf areas C. finmarchicus usually endures its winter diapause at 500–1500 m depth (Ostvedt, 1955; Longhurst, 1976) and its diel vertical migrations can reach down to 200 m depth or more (Longhurst, 1976). As the bottom depth in continental shelf areas is usually less than 200 m, both seasonal and diel vertical migrations can be radically different from those in deeper waters. Some of these constraints may be too stringent, hence this species may be unable to reach the minimum in metabolism necessary to survive the winter (Hirche, 1983; Ingvarsdottir et al., 1999). Instead there are a number of other copepod species that thrive in shallow waters, some by using different methods of winter survival like resting eggs e.g. some Temora and Acartia species (Johnson, 1980; Uye, 1985; Lindley, 1990). The larvae of many fish species depend on copepod eggs and nauplii as first food but most of the above mentioned shelf species of copepods are smaller than C. finmarchicus and their eggs and nauplii are of suboptimal size as first food for fish larvae such as cod (Bainbridge and McKay, 1968; Thorisson, 1989). Good spawning grounds for the most sought after fish on the continental shelf may thus have evolved where there is a secure immigration of large copepods like C. finmarchicus every spring from deeper waters. 4.9. Implications Imagine, for a moment, that the present hypothesis is valid. Then, how would different environmental conditions affect, e.g. the stock of C. finmarchicus, and how would the cod stock, in turn, be effected through different survival rates of the cod larvae? The spawning of the Icelandic cod usually lasts for about 6 weeks and is most intense during some 3 weeks in late April to early May (Jonsson, 1982; Marteinsdottir, 2001). The median or peak spawning of cod is remarkably stable around the last week of April. The timing of the spring bloom of phytoplankton, however, is much more variable and the maximum interannual difference in its timing may be about 4 weeks (Thordardottir, 1986; Gudmundsson, 1998). As the spawning of C. finmarchicus is tightly linked to the phytoplankton bloom (Colebrook, 1979), the surfacing and spawning of the copepods is also quite variable in time

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(Corten, 2000; Irigoien, 1999). The nauplii of C. finmarchicus are the staple food of first feeding cod larvae (Bainbridge and McKay, 1968). A peak spawning of C. finmarchicus in late May is thus probably the most favourable timing for the year-class of the Icelandic cod, but as the most intense spawning of cod lasts for about 3 weeks, one week sooner or later is probably not that all-important. A given seasonal development of phytoplankton in boreal waters is presented schematically in Fig. 2a, and assumed to be an average for some imagined area south of Iceland. The main features are a gradual prebloom a

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Fig. 2. Schematic presentation of three hypothetical forms of the annual succession of primary production in boreal waters. (a) Stratification of surface layers extends over an average length of time. (b) Duration of stable stratification 1 month shorter than the average. (c) A prolonged surface stratification lasts one month longer than in an average year. Stippled area = period of stable stratification of surface layers, grey line = primary production, thick black line = potential downflux of organic matter.

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increase, a short but intense spring bloom, low but variable summer production and a fairly large autumn increase. The annual development will vary considerably from year to year but the spawning time of both copepods and fishes and the feeding, growth and development of their offspring are presumably adapted to this average form of succession of the phytoplankton conditions. The overall length of the season for primary production in boreal waters is fairly predictable for a given location as it is delimited by a minimum radiation of visible light (Sverdrup, 1953; Smayda, 1959). The new production, on the other hand, is highly dependent on the formation of a pycnocline (stippled areas in Fig. 2) that reduces the vertical transport of phytoplankton cells out of the illuminated surface layers. At the same time, it prevents the replenishment of nitrate from below. The formation (and breakdown) of the pycnocline depends e.g. on radiation, warming, currents, salinity and, last but not least, the wind stress. The length of the calm production period can probably vary interannually by several weeks depending on weather conditions (Brander et al., 2001). During the productive season, if there is no pycnocline present or if the standing stock of phytoplankton is decreasing, some potential downflux material exist (Fig. 2). According to the present hypothesis the downflux can mobilize both the ascent and descend of copepods to and from deeper layers. Given the above seasonal changes (Fig. 2a), there will be an ascent/descend period for the copepods after the spring bloom and a major descend period during the autumn increase, according to the present hypothesis. There is also a major ascent of copepods during the prebloom increase of the phytoplankton. The dense schools of copepods in the surface waters in spring will graze down the spring bloom peak, resulting in a massive copepod spawning (Marshall and Orr, 1955) at just the right time for the first feeding cod larvae in early May (Fig. 2a). Small phytoplankton cells cope best in the nutrient poor water just after the spring bloom (Levasseur et al., 1984). These cells are of ideal size for the first feeding stages of copepod nauplii (Marshall and Orr, 1955) and the nauplii in turn are the staple food of cod larvae. The primary production during summer, may give rise to some downflux peaks, probably consisting primarily of fecal pellets, which may stimulate a couple of summer generations of copepods to resurface and spawn. If successful, these summer generations may add substantially to the numbers in the copepod stock. The copepods descending during the autumn increase, spend only about 4–5 months in diapause.

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Therefore, a large percentage of these animals will probably survive to restock the surface waters the following spring. The downflux after the spring bloom may also induce some diapause descend of copepods (Ostvedt, 1955), but probably with very low returns. These copepods will either resurface the following autumn to face the inhospitable winter conditions or, attempt to outlast in diapause the whole 9–10 months until the next spring. Now, let us assume that storms delay the stratification of the surface waters in spring by 2 weeks and that the pycnocline is broken down 2 weeks earlier than the average in autumn (Fig. 2b). The long prebloom period will probably ensure that most of the animals in diapause ascend in spring, but some of the resulting copepod nauplii may arrive too late to become potential food for the cod larvae. Because of the reduced time scale, one less summer generations of copepods may be produced until the autumn increase cuts in, but due to the high level of radiation still remaining the autumn increase will be extended in time and level of production, which should add to the diapause stock of copepods. This scenario thus seems particularly favourable for copepods, which may explain the success of large copepods like C. finmarchicus and C. hyperboreus in the windy conditions at high latitudes. Data from the Continuous Plankton Recorder show different reactions for different Calanus species, however, where the concentrations of C. finmarchicus correlate strongly with the reverse of the NAO index, but the C. helgolandicus numbers fluctuate with the NAO (Fromentin and Planque, 1996). The opposite temperature affinities of these two species may partly explain the above difference (Planque and Fromentin, 1996) but as the zooplankton samples are taken from less than 10 m depth they may not be representative for the whole stock. Let us now imagine unusually calm weather and cloudless skies in spring that will result in very early stratification, say 2 weeks earlier than usual (Fig. 2c). According to the present hypothesis, this would presumably result in fewer than average copepods surfacing in spring and a minimal spring spawning. To make things worse for cod, the copepod spawning would already be over a couple of weeks before the cod larvae hatch. Most of the copepod offspring have thus probably reached copepodite stages when it comes to first feeding of cod and have thus become too large to be swallowed by the cod larvae. Let us also assume that the stratification persists until 2 weeks later than the average. When the stratification is finally broken down, the level of radiation is

already so low that the primary production will soon die out with only a minimum autumn increase (Fig. 2c). As a result, fewer individuals will presumably enter diapause and many copepods may end up spending the winter in surface waters with extremely low survival rates. The presence of an autumn increase is thus probably equally important for the outcome of the copepod spawning as is the timing of the spring bloom. In spite of the long season of primary production, which may allow for more summer generations, the above scenario will probably reduce the diapause stock of copepods and may be extremely unproductive for the year-class of cod that will hatch the following year. Irigoien gives an example of a low primary production in summer and a negligible autumn increase in 1971 (Irigoien, 1999, his Fig. 5). The resulting bdiapause materialQ consisted solely of CV copepodites that descended in June and did not survive the 10-month period to the following spring. On the other hand, the copepods descending in autumn 1972 returned strongly during the following spring (Irigoien, 1999, his Fig. 6). In short, the arguments imply that a shorter than average stratification season may have a positive influence on the C. finmarchicus stock but may be mildly negative for the year-class of cod. An earlier than average stratification and long growth season on the other hand seems to be detrimental to the copepod stock and very negative for the survival of cod larvae. In the literature one can find both contradicting and supporting evidence for these statements (Platt et al., 2003; Brander et al., 2001) and the matter needs to be looked at more closely. The best survival of cod larvae may, however, be realized if there is a large increase in phytoplankton production during the autumn and if the stratification of surface waters is reached at the average time or later during the following spring. Acknowledgements Thanks are due to Astthor Gislason, James Begley, Kristinn Gudmundsson, Margret Audunsdottir, and the anonymous referees for their critical reading of earlier versions of the manuscript and their helpful suggestions. [SS] References Andersen, V., Nival, P., 1988. A pelagic ecosystem model simulating production and sedimentation of biogenic particles: role of salps and copepods. Mar. Ecol. Prog. Ser. 44, 37 – 50. Anderson, L.W.J., Sweeney, B.M., 1977. Diel changes in sedimentation characteristics of Ditylum brightwelli: changes in cellular

K. Thorisson / J. Exp. Mar. Biol. Ecol. 329 (2006) 86–100 lipid and effects of respiratory inhibitors and ion-transport modifiers. Limnol. Oceanogr. 22 (3), 539 – 552. Backhaus, J.O., Harms, I.H., Krause, M., Heath, M.R., 1994. An hypothesis concerning the space-time succession of Calanus finmarchicus in the northern North Sea. ICES J. Mar. Sci. 51, 169 – 180. Bainbridge, R., 1952. Underwater observations on the swimming of marine zooplankton. J. Mar. Biol. Assoc. U.K. 31, 107 – 112. Bainbridge, R., 1953. Studies on the interrelationships of zooplankton and phytoplankton. J. Mar. Biol. Assoc. U.K. 32, 385 – 447. Bainbridge, V., McKay, B.J., 1968. The feeding of cod and redfish larvae. Spec. Publ. Int. Commun. Northw. Atl. Fish. No 7. Northwestlant 1–3, 1963 Part I, pp. 187 – 217. Bamstedt, U., 1986. Chemical composition and energy content. In: Corner, E.D.S., O’Hara, S.C.M. (Eds.), The Biological Chemistry of Marine Copepods. Science Publications, Oxford, pp. 1 – 58. Bienfang, P.K., 1981. Sinking rate dynamics of Cricosphaera carterae Braarud: I. Effects of growth rate, limiting substrate, and diurnal variation in steady-state populations. J. Exp. Mar. Biol. Ecol. 49, 217 – 233. Bienfang, P., Gundersen, K., 1977. Light effects on nutrient-limited oceanic primary production. Mar. Biol. 43, 187 – 199. Bienfang, P.K., Harrison, P.J., 1984. Sinking-rate response of natural assemblages of temperate and subtropical phytoplankton to nutrient depletion. Mar. Biol. 83, 293 – 300. Bienfang, P., Szyper, J., Laws, E., 1983. Sinking rate and pigment responses to light-limitation of a marine diatom: implications to dynamics of chlorophyll maximum layers. Oceanol. Acta 6 (1), 55 – 62. Bishop, J.K.B., Edmond, J.M., Ketten, D.R., Bacon, M.P., Silker, W.B., 1977. The chemistry, biology, and vertical flux of particulate matter from the upper 400 m of the equatorial Atlantic Ocean. Deep-Sea Res. 24, 511 – 548. Bogorov, B.G., 1946. Peculiarities of diurnal vertical migrations of zooplankton in polar seas. J. Mar. Res. 6, 25 – 32. Bollens, S.M., Frost, B.W., 1989. Predator-induced diel vertical migration in a planktonic copepod. J. Plankton Res. 11 (5), 1047 – 1065. Bollens, S.M., Frost, B.W., Cordell, J.R., 1994. Chemical, mechanical and visual cues in the vertical migration behavior of the marine planktonic copepod Acartia hudsonica. J. Plankton Res. 16, 555 – 564. Boyd, C.M., Smith, S.L., Cowles, T.J., 1980. Grazing patterns of copepods in the upwelling system off Peru. Limnol. Oceanogr. 25 (4), 583 – 596. Brander, K.M., Dickson, R.R., Shepherd, J.G., 2001. Modelling the timing of plankton production and its effect on recruitment of cod (Gadus morhua). ICES J. Mar. Sci. 58, 962 – 966. Buskey, E.J., 1984. Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food. Mar. Biol. 79, 165 – 175. Campbell, R.W., Dower, J.F., 2003. Role of lipids in the maintenance of neutral buoyancy by zooplankton. Mar. Ecol. Prog. Ser. 263, 93 – 99. Clarke, G.L., 1932. Quantitative aspects of the change of phototropic sign in Daphnia. J. Exp. Biol. 9, 180 – 211. Clarke, G.L., 1934. Further observations on the diurnal migration of copepods in the Gulf of Maine. Biol. Bull. (Woods Hole) 67, 432 – 455. Colebrook, J.M., 1979. Continuous plankton records: seasonal cycles of phytoplankton and copepods in the North Atlantic Ocean and the North Sea. Mar. Biol. 51, 23 – 32.

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Conover, R.J., 1965. Notes on the molting cycle, development of sexual characters and sex ration in Calanus hyperboreus. Crustaceana 8, 308 – 320. Conover, R.J., 1968. Zooplankton—life in a nutritionally dilute environment. Am. Zool. 8, 107 – 118. Corten, A., 2000. A possible adaptation of herring feeding migrations to a change in timing of the Calanus finmarchicus season in the eastern North Sea. ICES J. Mar. Sci. 57, 1261 – 1270. Cushing, D.H., 1951. The vertical migration of planktonic crustacea. Biol. Rev. 26, 158 – 192. Dagg, M.J., Wymann, K.D., 1983. Natural ingestion rates of the copepods Neocalanus plumchrus and N. cristatus calculated from gut contents. Mar. Ecol. Prog. Ser. 13, 37 – 46. Dale, T., Kaartvedt, S., 2000. Diel patterns in stage-specific vertical migration of Calanus finmarchicus in habitats with midnight sun. ICES J. Mar. Sci. 57, 1800 – 1818. Davis, C.C., 1976. Overwintering strategies of common planktic copepods in some North Norway fjords and sounds. Astarte 9, 37 – 42. Denton, E.J., Marshall, N.B., 1958. The buoyancy of bathypelagic fishes without a gas-filled swimbladder. J. Mar. Biol. Assoc. U.K. 37, 753 – 767. Durbin, E.G., Garrahan, P.R., Casas, M.C., 2000. Abundance and distribution of Calanus finmarchicus on the Georges Bank during 1995 and 1996. ICES J. Mar. Sci. 57, 1664 – 1685. Eppley, R.W., Holmes, R.W., Strickland, J.D.H., 1967. Sinking rates of marine phytoplankton measured with a fluorometer. J. Exp. Mar. Biol. Ecol. 1, 191 – 208. Eppley, R.W., Carlucci, A.F., Holm-Hansen, O., Kiefer, D., McCarthy, J.J., Venrick, E., Williams, P.M., 1971. Phytoplankton growth and composition in shipboard cultures supplied with nitrate, ammonium, or urea as the nitrogen source. Limnol. Oceanogr. 16 (5), 741 – 751. Fromentin, J.M., Planque, B., 1996. Calanus and environment in the eastern North Atlantic: II. Influence of the North Atlantic Oscillation on C. finmarchicus and C. helgolandicus. Mar. Ecol. Prog. Ser. 134, 111 – 118. Frost, B.W., 1975. A threshold feeding behavior in Calanus pacificus. Limnol. Oceanogr. 20 (2), 263 – 266. Gasser, B., Payet, G., Sardou, J., Nival, P., 1998. Community structure of mesopelagic copepods (N500 Am) in the Ligurian Sea (Western Mediterranean). J. Mar. Syst. 15, 511 – 522. Gatten, R.R., Sargent, J.R., Forsberg, T.E.V., O’Hara, S.C.M., Corner, E.D.S., 1980. On the nutrition and metabolism of zooplankton: XIV. Utilization of lipid by Calanus helgolandicus during maturation and reproduction. J. Mar. Biol. Assoc. U.K. 60, 391 – 399. Gill, C.W., Poulet, S.A., 1988. Responses of copepods to dissolved free amino acids. Mar. Ecol. Prog. Ser. 43, 269 – 276. Gislason, A., 2003. Life cycle strategies and seasonal migrations of oceanic copepods in the Irminger Sea. In: Jones, M.B., Ingolfsson, A., Olafsson, E., Helgason, G.V., Gunnarsson, K., Svavarsson, J. (Eds.), Migrations and Dispersal of Marine organisms. Hydrobiologia, vol. 503, pp. 195 – 209. Gislason, A., Astthorsson, O.S., Petursdottir, H., Gudfinnsson, H., Bodvarsdottir, A.R., 2000. Life cycle of Calanus finmarchicus south of Iceland in relation to hydrography and chlorophyll a. ICES J. Mar. Sci. 57, 1619 – 1627. Graham, W.M., MacIntyre, S., Alldredge, A.L., 2000. Diel variations of marine snow concentrations in surface waters and implications from particle flux in the sea. Deep-Sea Res. 47, 367 – 395.

98

K. Thorisson / J. Exp. Mar. Biol. Ecol. 329 (2006) 86–100

Gudmundsson, K., 1998. Long-term variation in phytoplankton productivity during spring in Icelandic waters. ICES J. Mar. Sci. 55, 635 – 643. Hardy, A.C., 1956. The Open Sea. Its Natural History: the World of Plankton. Collins, London. Hardy, A.C., Bainbridge, R., 1954. Experimental observations on the vertical migrations of plankton animals. J. Mar. Biol. Assoc. U.K. 33, 409 – 448. Hardy, A.C., Gunther, E.R., 1935. The plankton of the South Georgia whaling grounds and adjacent waters 1926–1927. Discov. Rep. 11, 1 – 456. Hargrave, B.T., Taguchi, S., 1978. Origin of deposited material sedimented in a marine bay. J. Fish. Res. Board Can. 35, 1604 – 1613. Hays, G.C., 1995. Ontogenetic and seasonal variation in the diel vertical migration of the copepods Metridia lucens and Metridia longa. Limnol. Oceanogr. 40 (8), 1461 – 1465. Hays, G.C., Kennedy, H., Frost, B.W., 2001. Individual variability in diel vertical migration of a marine copepod: why some individuals remain at depth when others migrate. Limnol. Oceanogr. 46 (8), 2050 – 2054. Head, E.J.H., Harris, L.R., Abou Debs, C., 1985. Effect of daylength and food concentration on in situ diurnal feeding rhythms in Arctic copepods. Mar. Ecol. Prog. Ser. 24, 281 – 288. Heath, M.R., 1999. The ascent migration of Calanus finmarchicus from overwintering depths in the Faroe–Shetland channel. Fish. Oceanogr. 8 (Suppl. 1), 84 – 99. Heath, M.R., Backhaus, J.O., Richardson, K., McKenzie, E., Slagstad, D., Beare, D., Dunn, J., Fraser, J.G., Gallego, A., Hainbucher, D., Hay, S., Jonasdottir, S., Madden, H., Mardaljevic, J., Schacht, A., 1999. Climate fluctuation and the spring invasion of the North Sea by Calanus finmachicus. Fish. Oceanogr. 8 (Suppl. 1), 163 – 176. Heath, M.R., Fraser, J.G., Gislason, A., Hay, S.J., Jonasdottir, S.H., Richardson, K., 2000. Winter distribution of Calanus finmarchicus in the Northeast Atlantic. ICES J. Mar. Sci. 57, 1628 – 1635. Heinrich, A.K., 1962. The life histories of plankton animals and seasonal cycles of plankton communities in the oceans. J. Cons.Perm. Int. Explor. Mer 27, 15 – 24. Hirche, H.J., 1983. Overwintering of Calanus finmarchicus and Calanus helgolandicus. Mar. Ecol. Prog. Ser. 11, 281 – 290. Hirche, H.J., 1996. Diapause in the marine copepod, Calanus finmarchicus—a review. Ophelia 44, 129 – 143. Hugget, J.A., Richardson, A.J., 2000. A review of the biology and ecology of Calanus agulhensis off South Africa. ICES J. Mar. Sci. 57, 1834 – 1849. Huntley, M., 1988. Feeding biology of Calanus: a new perspective. Hydrobiologia 167/168, 83 – 99. Huntley, M., Brooks, E.R., 1982. Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar. Biol. 71, 23 – 31. Huntley, M.E., Marin, V., Escritor, F., 1987. Zooplankton grazers as transformers of ocean optics: a dynamic model. J. Mar. Res. 45, 911 – 945. Hutchinson, G.E., 1967. Introduction to lake biology and the limnoplankton. A Treatise on Limnology: Vol. 2. Introduction to Lake Biology and the Limnoplankton. Wiley and Sons, New York. Idrisi, N., Olascoaga, M.J., Garraffo, Z., Olson, D.B., Smith, S.L., 2004. Mechanisms for emergence from diapause of Calanoides carinatus in the Somali current. Limnol. Oceanogr. 49 (4 Part 2), 1262 – 1268.

Ingvarsdottir, A., Houlihan, D.F., Heath, M.R., Hay, S.J., 1999. Seasonal changes in respiration rates of copepodite stage V Calanus finmarchicus (Gunnerus). Fish. Oceanogr. 8 (Suppl. 1), 73 – 83. Irigoien, X., 1999. Vertical distribution and population structure of Calanus finmarchicus at station India (598N, 198W) during the passage of the great salinity anomaly, 1971–1975. Deep-Sea Res. I 47, 1 – 26. Irigoien, X., 2004. Some ideas about the role of lipids in the life cycle of Calanus finmarchicus. J. Plankton Res. 26, 259 – 263. Jaschnov, W.A., 1970. Distribution of Calanus species in the seas of the Northern Hemisphere. Int. Rev. Gesamten Hydrobiol. 55 (2), 197 – 212. Johnsen, G.H., Jakobsen, P.J., 1987. The effect of food limitation on vertical migration in Daphnia longispina. Limnol. Oceanogr. 32 (4), 873 – 880. Johnson, J.K., 1980. Effects of temperature and salinity on production and hatching of dormant eggs of Acartia californiensis (Copepoda) in an Oregon estuary. Fish. Bull. 77 (3), 567 – 584. Jonasdottir, S.H., 1999. Lipid content of Calanus finmarchicus during overwintering in the Faroe–Shetland channel. Fish. Oceanogr. 8 (Suppl. 1), 61 – 72. Jonsson, E., 1982. A survey of spawning and reproduction of the Icelandic cod. Rit Fiskid. VI (2), 1 – 45. Kaartvedt, S., 1996. Habitat preference during overwintering and timing of seasonal vertical migration of Calanus finmarchicus. Ophelia 44, 145 – 156. Kerfoot, W.C., 1985. Adaptive value of vertical migration: comments on the predation hypothesis and some alternatives. Contrib. Mar. Sci. 27, 91 – 113 (Suppl.). Lampitt, R.S., Hillier, W.R., Challenor, P.G., 1993a. Seasonal and diel variation in the open ocean concentration of marine snow aggregates. Nature 362, 737 – 739. Lampitt, R.S., Wishner, K.F., Turley, C.M., Angel, M.V., 1993b. Marine snow studies in the Northeast Atlantic Ocean: distribution, composition and role as a food source for migrating plankton. Mar. Biol. 116, 689 – 702. Lee, R.F., 1974. Lipid composition of the copepod Calanus hyperboreus from the Arctic Ocean. Changes with depth and season. Mar. Biol. 26, 313 – 318. Levasseur, M., Therriault, J.C., Legendre, L., 1984. Hierarchical control of phytoplankton succession by physical factors. Mar. Ecol. Prog. Ser. 19, 211 – 222. Lewis, R.W., 1970. The densities of three classes of marine lipids in relation to their possible role as hydrostatic agents. Lipids 5 (1), 151 – 153. Lindley, J.A., 1990. Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern Britain. Mar. Biol. 104, 209 – 217. Lohrenz, S.E., Knauer, G.A., Asper, V.L., Tuel, M., Michaels, A.F., Knap, A.H., 1992. Seasonal variability in primary production and particle flux in the northwestern Sargasso Sea: U.S. JGOFS Bermuda Atlantic time-series study. Deep-Sea Res. 39 (7/8), 1373 – 1391. Longhurst, A.R., 1976. Vertical migration. In: Cushing, D.H., Wals, J.J. (Eds.), The Ecology of the Seas. W.B. Sounders Co, Philadelphia, pp. 116 – 137. Longhurst, A., Williams, R., 1992. Carbon flux by seasonal vertical migrant copepods is a small number. J. Plankton Res. 14 (11), 1495 – 1509. Longhurst, A.R., Bedo, A.W., Harrison, W.G., Head, E.J.H., Sameto, D.D., 1990. Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep-Sea Res. 37 (4), 685 – 694.

K. Thorisson / J. Exp. Mar. Biol. Ecol. 329 (2006) 86–100 Marshall, S.M., Orr, A.P., 1955. The Biology of a Marine Copepod. Oliver and Boyd, Edinburgh. Marteinsdottir, G., 2001. The spawning of the cod (in Icelandic). Hafrannsoknir 56, 79 – 81. McLaren, I.A., 1963. Effects of temperature on growth of zooplankton, and the adaptive value of vertical migration. J. Fish. Res. Board Can. 20 (3), 685 – 727. Miller, C.B., Cowles, T.J., Wiebe, P.H., Copley, N.J., Grigg, H., 1991. Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar. Ecol. Prog. Ser. 72, 79 – 91. Miller, C.B., Morgan, C.A., Prahl, F.G., Sparrow, M.A., 1998. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol. Oceanogr. 43 (3), 488 – 497. Miller, C.B., Crain, J.A., Morgan, C.A., 2000. Oil storage variability in Calanus finmarchicus. ICES J. Mar. Sci. 57, 1786 – 1799. Mopper, K., Lindroth, P., 1982. Diel and depth variations in dissolved free amino acids and ammonium in the Baltic Sea determined by shipboard HPLC analysis. Limnol. Oceanogr. 27 (2), 336 – 347. Neill, W.E., 1990. Induced vertical migration in copepods as a defence against invertebrate predation. Nature 345, 524 – 526. Noji, T.T., Rey, F., Miller, L.A., Borsheim, K.Y., Urban-Rich, J., 1999. Fate of biogenic carbon in the upper 200 m of the central Greenland Sea. Deep-Sea Res. 46, 1497 – 1509. Noji, T.T., Miller, L.A., Skjelvan, I., Falck, E., Borsheim, K.Y., Rey, F., Urban-Rich, J., Johannesen, T., 2001. Constraints on carbon drawdown and export in the Greenland Sea. In: Schafer, P., Ritzrau, W., Schluter, M., Thiede, J. (Eds.), The Northern North Atlantic. Springer, Berlin, pp. 39 – 52. Norrbin, M.F., 1994. Seasonal patterns in gonad maturation, sex ratio and size in some small, high-latitude copepods: implications for overwintering tactics. J. Plankton Res. 16 (2), 115 – 131. Norrbin, M.F., Olsen, R.E., Tande, K.S., 1990. Seasonal variation in lipid class and fatty acid composition of two small copepods in Balsfjorden, northern Norway. Mar. Biol. 105, 205 – 211. Ostvedt, O.J., 1955. Zooplankton investigations from weather ship M in the Norwegian Sea, 1948–49. Hvalradets Skr. 40, 1 – 93. Pavlova, E.V., 1994. Diel changes in copepod respiration rates. Hydrobiologia 292/293, 333 – 339. Pearre, S., 1979. Problems of detection an interpretation of vertical migration. J. Plankton Res. 1 (1), 29 – 44. Planque, B., Batten, S.D., 2000. Calanus finmarchicus in the North Atlantic: the year of Calanus in the context of interdecadal change. ICES J. Mar. Sci. 57, 1528 – 1535. Planque, B., Fromentin, J.M., 1996. Calanus and environment in the eastern North Atlantic: I. Spatial and temporal patterns of C. finmarchicus and C. helgolandicus. Mar. Ecol. Prog. Ser. 134, 101 – 109. Platt, T., Fuentes-Yaco, C., Frank, K.T., 2003. Spring algal bloom and larval fish survival. Nature 423, 398 – 399. Poulet, S.A., Ouellet, G., 1982. The role of amino acids in the chemosensory swarming and feeding of marine copepods. J. Plankton Res. 4 (2), 341 – 361. Richardson, K., Jonasdottir, S., Hay, S.J., Christoffersen, A., 1999. Calanus finmarchicus egg production and food availability in the Faroe–Shetland channel and North Sea: October–March. Fish. Oceanogr. 8 (Suppl. 1), 153 – 162. Rudjakov, J.A., 1970. The possible causes of diel vertical migrations of planktonic animals. Mar. Biol. 6, 98 – 105. Russel, F.S., 1926. The vertical distribution of marine macroplankton: IV. The apparent importance of light intensity as a controlling factor in the behaviour of certain species in the Plymouth area. J. Mar. Biol. Assoc. U.K. 14 (2), 415 – 440.

99

Russel, F.S., 1927. The vertical distribution of plankton in the sea. Biol. Rev. 2 (3), 213 – 262. Shanks, A.L., Trent, J.D., 1980. Marine snow: sinking rates and potential role in vertical flux. Deep-Sea Res. 27, 137 – 143. Silver, M.W., Gowing, M.M., 1991. The bparticleQ flux: origins and biological components. Prog. Oceanogr. 26, 75 – 113. Simard, Y., Lacroix, G., Legendre, L., 1985. In situ twilight grazing rhythm during diel vertical migrations of a scattering layer of Calanus finmarchicus. Limnol. Oceanogr. 30 (3), 598 – 606. Small, L.F., Fowler, S.W., Unlu, M.Y., 1979. Sinking rates of natural copepod fecal pellets. Mar. Biol. 51, 233 – 241. Smayda, T.J., 1959. The seasonal incoming radiation in Norwegian and Arctic waters, and indirect methods of measurement. J. Cons.-Perm. Int. Explor. Mer 24, 215 – 220. Smayda, T.J., 1975. Phased cell division in natural population of the marine diatom Ditylum brightwelli and the potential significance of diel phytoplankton behavior in the sea. Deep-Sea Res. 22, 151 – 165. Smith, S., 2001. Understanding the Arabian Sea: reflections on the 1994–1996 Arabian Sea expedition. Deep-Sea Res., II 48, 1385 – 1402. Smith, S.L., Henrichs, S.M., Rho, T., 2002. Stable C and N isotopic composition of sinking particles and zooplankton over the southeastern Bering Sea shelf. Deep-Sea Res. 49, 6031 – 6050. Sournia, A., 1974. Circadian periodicities in natural populations of marine phytoplankton. In: Russel, F.S., Yonge, M. (Eds.), Adv. Mar. Biol., vol. 12, pp. 325 – 389. Stearns, D.E., 1986. Copepod grazing behavior in simulated natural light and its relation to nocturnal feeding. Mar. Ecol. Prog. Ser. 30, 65 – 76. Stich, H.B., Lampert, W., 1981. Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293, 396 – 398. Strass, V., Woods, J.D., 1988. Horizontal and seasonal variation of density and chlorophyll profiles between the Azores and Greenland. In: Rothschild, B.J. (Ed.), Toward a Theory on Biological– Physical Interactions in the World Ocean. Kluver Academic Publishers, Dordrecht, pp. 113 – 136. Sverdrup, H.U., 1953. On conditions for the vernal blooming of phytoplankton. J. Cons.-Perm. Int. Explor. Mer 18, 287 – 295. Taylor, G.T., 1989. Variability in the vertical flux of microorganisms and biogenic material in the epipelagic zone of a North Pacific central gyre station. Deep-Sea Res. 36 (9), 1287 – 1308. Thordardottir, T., 1986. Timing and duration of spring blooming south and southwest of Iceland. In: Skreslet, S. (Ed.), The Role of Freshwater Outflow in Coastal Marine Ecosystems. Springer-Verlag, Berlin, pp. 345 – 360. Thorisson, K., 1989. The food of larvae and pelagic juveniles of cod (Gadus morhua L.) in the coastal waters west of Iceland. Rapp. P.V. Reun.-Cons. Int. Explor. Mer. 191, 264 – 272. Tiselius, P., 1992. Behavior of Acartia tonsa in patchy food environments. Limnol. Oceanogr. 37 (8), 1640 – 1651. Titelman, J., Kiorboe, T., 2003. Motility of copepod nauplii and implications for food encounter. Mar. Ecol. Prog. Ser. 247, 123 – 135. Uye, S., 1985. Resting egg production as a life history strategy of marine planktonic copepods. B. Mar. Sci. 37 (2), 440 – 449. van Duren, L.A., Videler, J.J., 1995. Swimming behaviour of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar. Ecol. Prog. Ser. 126, 153 – 161. van Duren, L.A., Videler, J.J., 1996. The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioral responses to chemical cues. J. Plankton Res. 18 (5), 805 – 818.

100

K. Thorisson / J. Exp. Mar. Biol. Ecol. 329 (2006) 86–100

Visser, A.W., Jonasdottir, S., 1999. Lipids, buoyancy and the seasonal vertical migration of Calanus finmarchicus. Fish. Oceanogr. 8 (Suppl. 1), 100 – 106. Yayanos, A.A., Benson, A.A., Nevenzel, J.C., 1978. The pressure– volume–temperature (PVT) properties of a lipid mixture from a

marine copepod, Calanus plumchrus: implications for buoyancy and sound scattering. Deep-Sea Res. 25, 257 – 268. Zaret, T.M., Suffern, J.S., 1976. Vertical migration in zooplankton as a predator avoidance mechanism. Limnol. Oceanogr. 21 (6), 804 – 813.