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HORIZONS Cascading Migrations and Implications for Vertical Fluxes in Pelagic Ecosystems

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HORIZONS Cascading Migrations and Implications for Vertical Fluxes in Pelagic Ecosystems JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 3 j PAGES 349–355 j 2011 HORIZONS Cascading migrations and implications for vertical fluxes in pelagic ecosystems Downloaded from STEPHEN M. BOLLENS 1*, GRETCHEN ROLLWAGEN-BOLLENS 1, JOEL A. QUENETTE 1 AND ALEXANDER B. BOCHDANSKY 2 1 SCHOOL OF EARTH AND ENVIRONMENTAL SCIENCES, AND SCHOOL OF BIOLOGICAL SCIENCES, WASHINGTON STATE UNIVERSITY, 14204 NE SALMON CREEK 2 AVENUE, VANCOUVER, WA 98686-9600, USA AND DEPARTMENT OF OCEAN, EARTH AND ATMOSPHERIC SCIENCES, OLD DOMINION UNIVERSITY, HAMPTON BOULEVARD, NORFOLK, VA 23529, USA plankt.oxfordjournals.org *CORRESPONDING AUTHOR: [email protected] Received June 5, 2010; accepted in priniciple October 19, 2010; accepted for publication October 26, 2010 Corresponding editor: Roger Harris Diel vertical migration is widespread across diverse taxa in the world’s lakes and at Washington State University Libraries on February 22, 2011 seas, yet its biogeochemical consequences are still poorly understood. The biologi- cally mediated vertical flux of material in the ocean (also known as the “biological pump”) is a matter of major interest and concern, as it is thought to play an important role in regulating ocean carbon storage, and by extension, the global carbon cycle. Recent studies spanning multiple trophic levels from fish to dinofla- gellates have led us to a concept of coupled vertical migrations that we refer to as “cascading migrations”. That is, migrations that occur at one trophic level can affect the vertical migration of the next lower trophic level, and so on throughout the food web (e.g. carnivores affect the migrations of herbivores, which in turn affect the migrations of motile phytoplankton). Here we hypothesize that greater trophic complexity in the water column leads to enhanced cascading vertical migrations that in turn increase the vertical fluxes of materials and energy through the water column, both upwards and downwards. We recommend that a combination of observational, experimental and modeling approaches be employed to explicitly test this hypothesis. KEYWORDS: cascading; plankton; diel; vertical; migration INTRODUCTION (Bollens and Frost, 1989a,b; Lampert, 1989; Hays, Diel vertical migration (DVM) is amongst the most 2003), although non-biological factors such as light and common and conspicuous migrations on Earth. While transparency can also have important effects (Forward, this behavior is thought to have a variety of both proxi- 1988; Ringelberg, 2010; C.E. Williamson, in prep- mate and ultimate causes (i.e. immediate cues and aration). Dinoflagellate DVM has also been well docu- adaptive significances, respectively), for mesozooplank- mented (Eppley et al., 1968; Blasco, 1978; Cullen and ton such as copepods and cladocerans, it is now widely Horrigan, 1981; Schofield et al., 2006; Jephson and held that predator evasion often plays a critical role Carlsson, 2009), although in a pattern that is usually doi:10.1093/plankt/fbq152, available online at www.plankt.oxfordjournals.org. Advance Access publication December 8, 2010 # The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 3 j PAGES 349–355 j 2011 opposite or reverse that of most zooplankton, namely, The specific objectives of this paper are to: (i) present near the surface during the day and at depth during the concept of “cascading migrations”, (ii) briefly review night. We have recently observed that the vertical distri- the role of DVM in modulating vertical fluxes in pelagic bution and migration pattern of the phototrophic dino- ecosystems and (iii) suggest some directions for future flagellate Akashiwo sanguinea (previously Gymnodinium research. sanguineum and a well-studied vertical migrator) are altered by the presence of their copepod predators (Quenette, 2010). CASCADING MIGRATIONS These and other studies have led us to put forward the concept of “cascading migrations”, whereby zooplankti- For zooplankton such as copepods and cladocerans, vores such as fish or large invertebrates trigger DVM in there are now literally hundreds of well-documented Downloaded from mesozooplankton such as copepods, which in turn cases of DVM (see reviews by Cushing, 1951; Lampert, affect the opposite (or reverse) migrations in their dino- 1989; Hays, 2003; Pearre, 2003; Ringelberg, 2010; flagellate prey. Again, abiotic factors (e.g. light, nutri- C.E. Williamson, in preparation). These migrations ents) will also play a role in vertical migrations, but usually manifest themselves as organisms residing at the predator–prey interactions primarily drive the mesozoo- surface at night and at depth during the day, although plankton (copepod) migrations, which cascade into the “reverse” pattern is also sometimes possible for plankt.oxfordjournals.org effects on dinoflagellate migrations. smaller zooplankton (e.g. Ohman et al., 1983; Frost and What is far less clear, however, is the importance of Bollens, 1992). Rather than always being “hard wired” vertical migrations to the vertical fluxes of material and inflexible, DVM sometimes reflects individual be- through the water column. The biologically mediated havioral flexibility (e.g. Bollens and Frost, 1991a, b) and vertical flux of material in the ocean (also known as the variable body condition (Hays et al., 2001), including “biological pump”) is a matter of major interest and the possibility of making multiple, short-term vertical concern, as it is thought to play an important role in forays and feeding bouts into and out of vertical layers at Washington State University Libraries on February 22, 2011 regulating ocean carbon storage, and by extension, the of food (Bochdansky and Bollens, 2004; Leising et al., global carbon cycle. The biological pump has primarily 2005; Pierson et al., 2009). While different zooplankton been understood to affect the downward flux of species, and even individuals within a given species, can material; however, the involvement of vertical migrators exhibit enormous variability in the timing and magni- opens the possibility for a bidirectional flux. tude of their migrations, depending on the exact Quantifying and predicting vertical fluxes becomes even environmental conditions at the time, there is broad more important in an era of continued global climate consensus that avoidance of predators such as visually change, which is expected to result in both increased orienting planktivorous fish and/or carnivorous invert- CO2 entering the ocean and increased stratification ebrates is the primary driver of DVM in zooplankton (vertical heterogeneity) as a result of global warming (Lampert, 1989; Bollens and Frost, 1989a,b; Hays, (Palacios et al., 2004). Thus knowing how vertical 2003). migrations and vertical fluxes interact is of broad Many species of dinoflagellates have also been oceanographic relevance and importance. observed to undertake vertical migration in a wide Our concept of “cascading migrations”, combined range of coastal and open ocean habitats, often residing with the brief review below of the role of DVM in mod- at the surface during the day and residing at depth at ulating vertical fluxes, leads us to the following specific night (Eppley et al., 1968; Blasco, 1978; Villarino et al., and testable hypothesis. Namely, that greater trophic 1995; Kamykowski et al., 1998; Ault, 2000; Park et al., complexity (i.e. an increase in the number of trophic 2001; Merzouk et al., 2004; Lee et al., 2005; Moorthi levels) in the water column leads to enhanced (i.e. more et al., 2006; Schofield et al., 2006; Ryan et al., 2009). numerous) cascading vertical migrations that in turn Some of these taxa are considered toxic or otherwise repackage and redistribute materials and energy harmful, and are therefore of particular interest and through the water column. As a result, vertical fluxes of concern. Both light (from the surface) and nutrients materials and energy are increased, both downwards (often at depth, in stratified waters) have been shown to and upwards. (An alternative hypothesis is that greater play central roles as drivers of dinoflagellate DVM in trophic complexity would lead to weaker trophic inter- laboratory studies (Heaney and Furnass, 1980; Cullen actions, and thus weaker vertical migrations and and Horrigan, 1981; Kamykowski, 1981; MacIntyre reduced vertical fluxes.) Near the end of this paper, we et al., 1997; Kamykowski et al., 1999; Erga et al., 2003; make specific recommendations for how this and Doblin et al., 2006; Jephson and Carlsson, 2009; related topics might be most fruitfully investigated. Schaeffer et al., 2009). 350 S. M. BOLLENS ET AL. j CASCADING MIGRATIONS AND IMPLICATIONS FOR VERTICAL FLUXES However, our recent experiments have shown that for Bollens, 2005), whereas the smaller, herbivorous cope- one common coastal dinoflagellate, A. sanguinea, vertical pods Pseudocalanus spp., which are preyed upon by the distribution and migration is influenced not only by larger carnivorous taxa, often undertake “reverse” light and nutrients, but also by copepod grazers DVM (Ohman et al., 1983; Frost and Bollens, 1992). (Quenette, 2010). This is similar but different to the Again, the concept is that DVM that occurs at one now well-known phenomenon of carnivorous predators trophic level cascades and can cause opposite (or out of inducing vertical migrations in zooplankton (Bollens phase) migrations at the next lower trophic level. and Frost, 1989a, 1991a, b; Lampert, 1989; Bollens
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