JPR Advance Access originally published online on July 16, 2008
Journal of Plankton Research 2008 30(11):1203-1206; doi:10.1093/plankt/fbn075
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HORIZONS |
Photoperiod may constrain the effect of global warming in arctic marine systems
Department of Biology, University of Oslo, PO Box 1066 Blindern, 0316 Oslo, Norway
* CORRESPONDING AUTHOR: stein.kaartvedt{at}bio.uio.no
Received on February 13, 2008; accepted on July 12, 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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Scenarios for climate change predict that global warming drives biogeographic boundaries polewards. However, reliable predictions of marine food web responses to climate change require understanding of the coupling mechanisms between trophic levels. The Arctic is characterized by extreme light regime (photoperiod) as well as extreme (low) temperatures, both with profound bearing on pelagic ecology but only temperature being affected by climate change. Here, I address the potential impact by the light climate on mesopelagic (mid-water) planktivorous fish and as a result their plankton prey. Mesopelagic fish abound in all oceans, except for the Arctic. I hypothesize that their lack of success in this environment is due to inferior feeding conditions imposed by the extreme light climate at high latitudes. Since photoperiod is unaffected by climate change mesopelagic fish may continue to be scarce, and large copepods such as Arctic Calanus spp. will continue to prevail even in a warmer climate. This hypothesis of photoperiod constraints on the effect of global warming in Arctic marine ecosystems may be tested in fjords with different temperatures and light conditions.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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Climate change affects geographic distributions of species. It has been predicted that global warming drives fish and key copepod species ranges toward the poles (e.g. Beaugrand et al., 2002
; Perry et al., 2005), although oceanic circulation may overrule this pattern on a regional scale (Greene and Pershing, 2007). However, reliable predictions of marine food web responses to climate change require understanding of the coupling mechanisms between trophic levels (Richardson and Schoeman, 2004). Most pelagic species not only have preferences and requirements for temperature, but also depend strongly on the light regime. As one move toward the poles, the seasonal changes in light intensity and day length become increasingly extreme, and it becomes necessary to discriminate the role of the light climate from that of temperatures for biogeographic boundaries of small fish and their plankton prey.
Light has fundamental impact on marine ecosystems as it drives both primary production and the interaction between visual predators and their prey. Primary production is confined to shallow, upper layers, which offer good feeding conditions for herbivores, but which also expose organisms to visually oriented predators. Light decreases exponentially with depth, leading to an abrupt decline in primary production as well as exposure to visual predators. These characteristics are decisive for interactions between predators and prey in pelagic ecosystems. The opposing needs of feeding and predator avoidance are often traded off by diel vertical migrations, in which organisms exploit the rich food of the upper waters under cover of darkness at night and seek refuge in deep, dim waters during daytime. While such behavior provides relative protection, predators may still forage visually in the upper layers at night, and dark adapted fish may spot prey visually even at several hundred meters depth during the day (Warrant and Locket, 2004).
The extreme light climate of the Arctic violates this general framework for predator–prey interactions, to which most species are adapted. The mid-night sun period in summer limits the options for safe foraging in the upper layers at night, and continuous darkness during winter prevents visual feeding in deep water at any time of day. These fundamental characteristics of Arctic pelagic ecosystems will define distributional patterns and life histories.
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MESOPELAGIC FISH AND CALANUS SPP |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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I here focus on predator–prey relationships between mesopelagic (mid-water) fish and copepods of the genus Calanus. These copepods have an essential role in high latitude Atlantic ecosystems as a link between primary production and fish. Species shifts among Calanus spp., with serious impacts on ecosystem functioning and commercially important fish species, have already been predicted as a consequence of climate change in boreal waters of the eastern Atlantic (Beaugrand et al., 2003
).
Four Calanus species commonly occur in the North Atlantic, each associated with specific water masses. Calanus helgolandicus is distributed in southern parts and the North Sea; C. finmarchicus has its core habitat in the Norwegian Sea and the Labrador Sea; C. glacialis usually inhabits Arctic shelf seas, whereas the main distribution areas of C. hyperboreus are the Greenland Sea, the Labrador Sea and the Arctic Ocean (Conover, 1988; Hirche, 1997; Skjoldal, 2004). Their life cycles encompass a long-lasting overwintering phase in deep water, which spans up to 
9 months.
During warm periods, C. finmarchicus seems to become substituted by the more southern, similarly sized C. helgolandicus in the North Sea (Beaugrand et al., 2003). This substitution may impact recruitment of, for example, cod since C. helgolandicus occurs later in the season, introducing a miss-match in timing of available prey for the cod larvae (Beaugrand et al., 2003). Should we expect a corresponding species displacement with Arctic species being substituted by temperature adapted congenerics further to the north in the eastern Arctic oceans, as suggested by Beaugrand et al. (2002)? I argue that this may not be the case. Such extrapolations between geographical regions imply strict causal relationships between temperature and species distributions. However, at high latitudes, extreme light conditions may increasingly override temperature in defining predator–prey relationships and as a consequence the distribution of some species. The presence or absence of planktivorous mesopelagic fish, and its implications for plankton mortality, particularly during winter, may be important. The Arctic Calanus are larger than their temperate congenerics. The large size is interpreted as an adaptation to sustain long periods without feeding in the fluctuating and unpredictable Arctic environment (Skjoldal, 2004). On the down side, large size would make these species particularly vulnerable to visual predators (e.g. O’Brien et al., 1976).
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PHOTOPERIOD CONSTRAINT HYPOTHESIS |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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My arguments, which lead to a "photoperiod constraint hypothesis" with respect to the effects of global warming in marine Arctic ecosystems, originate from observations in Norwegian fjords. Surprisingly, the Arctic species C. glacialis prevails in the temperate waters of one of the well-studied southern Norwegian fjords, Lurefjorden (Bucklin et al., 2000
; Bagøien et al., 2001; Niehoff and Hirche, 2005). Other large planktonic organisms are also particularly abundant in this fjord. In the neighboring fjords, temperate species dominate, while C. glacialis is virtually absent. The basin water of Lurefjorden is 6–7°C year round. In contrast, the temperature of the Arctic waters where C. glacialis normally occurs is near to zero, whereas waters above 3–4°C are avoided (Kosobokova, 1999; Kwasniewski et al., 2003). For some reason, other than temperature, the Arctic species is the most successful in the temperate Lurefjorden.
A clue to its success lies in the unusually low winter mortalities in this fjord, which evidently relate to the unique predator regime (Bagøien et al., 2001). Lurefjorden’s basin waters lack mesopelagic fish, while less efficient invertebrate predators abound (Eiane et al., 1999, 2002; Bagøien et al., 2001). In contrast, mesopelagic fish prevail in neighboring fjords, and mortality of overwintering Calanus is high (Bagøien et al., 2001). The large size of the Arctic species offers a clue to their absence in most Norwegian fjords, since vulnerability to visual predators increases with prey size. In the absence of visual predators in their overwintering habitat, the larger Arctic form thrives even in temperate waters.
Mesopelagic fish seem to be excluded from Lurefjorden due to a much higher light absorbance than in adjacent water masses (Eiane et al., 1999; Aksnes et al., 2004; Sørnes and Aksnes, 2006; Sørnes et al., 2007). High light absorbance and hence reduced visual range results in poorer feeding conditions for visual predators in deep water. These findings led Aksnes and co-workers to test the correlation between fish abundance and optical properties (i.e. potential for visual feeding) also in other habitats. In a study of 12 fjords, mesopelagic fish abundance showed a strong, positive relationship with water clarity while zooplankton abundance and size correlated positively with an index of the water column darkness (Aksnes et al., 2004). In time series, fish abundance was highest in years with clearest water (Sørnes and Aksnes, 2006). Summarizing, the evidence is that when conditions for visual predation are good, fish prevail and then populations of (large) copepods decline rapidly (Bagøien et al., 2001, Aksnes et al., 2004). Overwintering mortality is a key parameter in the population dynamics of C. finmarchicus (Colebrook, 1985), and low winter mortality is a necessity for the success of the Arctic Calanus species because two long overwinterings may be needed to complete the life cycle (Skjoldal, 2004). The large Arctic species would be selectively preyed on by visual predators if present, but with few fish, large copepods dominate. The Lurefjorden example indicates that this holds true also at considerably higher temperatures than those normal in the Arctic.
Deep scattering layers composed of mesopelagic fish are found in all oceans, except in the Arctic (Garrison, 2005). On the basis of the evidence from fjord studies, I hypothesize that the absence or scarcity of mesopelagic fish at high latitudes relates to light. High light attenuation and reduced visual range in deep waters seem to hamper feeding and thus reduce or exclude mesopelagic fish populations in some temperate fjords with larger zooplankton as a consequence (Eiane et al., 1999; Bagøien et al., 2001; Aksnes et al., 2004). Similarly, I argue that the Arctic combination of 24 h of daylight during summer and 24 h of darkness during winter has a negative impact on feeding conditions for mesopelagic fish sufficient to prevent the establishment of sustainable populations, and in its extension determines plankton species abundances and size composition. Sameoto (1989) argued that cold waters and/or few hours of darkness during summer, which limited nocturnal feeding migrations to upper layers, excluded mesopelagic fish (Benthosema glaciale) from the northern zone of the Baffin Bay. I add that continuous darkness during winter would prevent visual feeding at depth even for the dark-adapted mesopelagic fish, which otherwise may detect overwintering copepods visually at several hundred meters depth during the day (c.f. Warrant and Locket, 2004). A strict delineation of the "Arctic" with respect to photoperiod will likely not apply, since organisms may drift in gyres that span many latitudes.
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TESTS OF THE HYPOTHESIS |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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Although there is evidence for a relationship between the abundance of mesopelagic fish and light climate (cf. the referenced work by Aksnes and co-workers), the suggested cascading effects from mesopelagic fish on the plankton composition can be challenged. Large seasonally migrating copepods apparently co-occur with abundant mesopelagic fish elsewhere (such as Neocalanus spp. in the northern Pacific; e.g. Frost and McCrone, 1979
; Conover, 1988; Mackas et al., 2007). Furthermore, the proposed hypothesis is based on limited evidence where light attenuation, rather than photoperiod, constrain visual foraging and thereby zooplankton size and species composition (Eiane et al., 1999; Bagøien et al., 2001; Aksnes et al., 2004). This calls for tests. The actual result of Arctic warming provides one such test, but likely dedicated fjord studies can teach us more about the light constraints versus temperature on pelagic ecosystems in shorter time.
The photoperiod constraint hypothesis involves two elements: (i) that large Arctic Calanus species may prevail in temperate waters without mesopelagic fish and (ii) that the distribution of mesopelagic fish is restricted by the photoperiod. The first element can be tested by addressing the zooplankton species and size composition in fjords where recent reports suggest similar predator regimes to that in Lurefjorden (unpublished). Both elements may be tested by mapping the abundance of mesopelagic fish, zooplankton size and species composition in fjords exposed to different photoperiods, but where the fjord basins have similar temperature and vice versa. Fjords are distributed along a latitudinal, and therefore photoperiod gradient, but basin water temperatures often rather relate to the sill depth, which determines the temperature of the source water (e.g. Hopkins et al., 1989; Zhou et al., 2005). The hypothesis predicts that the effect of photoperiod on the pelagic fauna should dominate, or modulate, the effect of temperature. The suggested design would allow for rejection of the proposed hypothesis.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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If light is a main factor determining the success of mesopelagic fish and in turn some large Arctic plankton, this has bearing upon climate scenarios addressing global warming in Arctic regions. In a warmer climate, the light climate at high latitudes will continue to limit feeding conditions for mesopelagic fish, so that large plankton will continue to prevail. My emphasis on mesopelagic fish as predators is due to the long overwintering period(s) which Calanus spp. spend at mesopelagic depths, and since mesopelagic fish appear to be more efficient predators on overwintering Calanus spp. than invertebrates (Bagøien et al., 2001
). My arguments do no account for potential impacts on some other predators, such as horizontally migrating herring (Clupea harengus) which in the present climate avoid the coldest Arctic waters during their summer feeding migrations (Skjoldal, 2004). Regardless, the light climate is a major characteristic defining northern ecosystems and needs to be incorporated in assessments of high latitude climate change scenarios. |
FUNDING |
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TOPABSTRACTINTRODUCTIONMESOPELAGIC FISH AND CALANUS...PHOTOPERIOD CONSTRAINT...TESTS OF THE HYPOTHESISCONCLUSIONSFUNDINGREFERENCES |
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Research Council of Norway.
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ACKNOWLEDGEMENTS |
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Josefin Titelman and Dag L. Aksnes provided valuable comments on an earlier version of this paper.
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Notes |
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Corresponding editor: Roger Harris
Written responses to this article should be submitted to R. P. Harris at r.p.h{at}pml.ac.uk within two months of publication. For further information, please see the Editorial ‘Horizons’ in Journal of Plankton Research, Volume 26, Number 3, Page 257.
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