1008

The Journal of Experimental Biology 215, 1008-1016

© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.059014

REVIEW
Plankton distribution and ocean dispersal
Margaret Anne McManus1,* and C. Brock Woodson2
1
Department of Oceanography, University of Hawaii at Manoa, Honolulu, HI 96822, USA and 2Environmental Fluid Mechanics
Laboratory, Department of Civil and Environmental Engineering, Stanford University, Stanford, CA 94305-4020, USA
*Author for correspondence ([email protected])

Accepted 27 July 2011

Summary
Plankton are small organisms that dwell in oceans, seas and bodies of fresh water. In this review, we discuss life in the plankton,
which involves a balance between the behavioral capabilities of the organism and the characteristics and movement of the water
that surrounds it. In order to consider this balance, we discuss how plankton interact with their environment across a range of
scales – from the smallest viruses and bacteria to larger phytoplankton and zooplankton. We find that the larger scale
distributions of plankton, observed in coastal waters, along continental shelves and in ocean basins, are highly dependent upon
the smaller scale interactions between the individual organism and its environment. Further, we discuss how larger scale
organism distributions may affect the transport and/or retention of plankton in the ocean environment. The research reviewed
here provides a mechanistic understanding of how organism behavior in response to the physical environment produces
planktonic aggregations, which has a direct impact on the way marine ecosystems function.
Key words: persistent front, thin layer, plankton distribution.

Introduction Ocean physics: from the perspective of an organism

The spatial distribution of organisms in the ocean – from the The dynamics of the ocean are highly variable and are driven by
smallest plankton to the largest predators – is determined by multiple forcing factors such as solar insolation, winds, tides and
interactions between organism behavior and physical freshwater input. This variability in forcing leads to the
oceanographic structure and processes. The relative importance of development of distinct water masses of different hydrographic
physical structures and processes in driving organism distribution, properties in both vertical and horizontal dimensions. For
and consequently dispersal, is directly related to the swimming and example, because of these forcing factors the upper ocean is
behavioral capabilities of an individual or species. Although it is generally regarded as being lower in density, well mixed and
clear that large predators such as sharks, marine mammals and large devoid of the nutrients needed for phytoplankton growth, while
fishes can adjust to changes in their fluid environment with relative the deep ocean is generally regarded as being higher in density
ease, plankton cannot. Life in the plankton involves a balance and nutrient rich. A boundary exists between these surface and
between behavior and the organisms’ environment. Plankton is bottom water masses that is referred to as a pycnocline (a region
composed of viruses, bacteria, phytoplankton, zooplankton and the of rapid change in density). Because ocean density is largely
pelagic larvae of many marine invertebrates and fishes. This group dependent upon temperature and salinity, gradients in temperature
displays a wide range of behavioral capabilities that bridge the (thermocline) and salinity (halocline) often coincide with the
transition from being a passive particle to being able to determine pycnocline. In general, the strength of the pycnocline increases
vertical and horizontal position in the ocean (Fig.1). This species- and the vertical extent of the pycnocline decreases as one moves
specific transition often occurs at scales much smaller than from an offshore ocean environment into the coastal ocean. In
traditionally recognized because of the organisms’ ability to ‘blue-water’ offshore regions, there is little freshwater input. In
respond to ocean structure and processes. the coastal ocean, not only can there be greater freshwater input,
In this contribution, we briefly review the physical characteristics but also these are regions where the surface boundary layer
and the dynamics of the ocean from the organism’s point of view. (which responds to wind forcing) and the bottom boundary layer
We then review the known scales of interaction between plankton (which responds to tidal forcing) can interact. On a horizontal
and physical processes, and how these interactions lead to observed scale, ocean fronts develop where two spatially separated water
patterns in the environment. Two specific oceanographic features – masses with different hydrographic properties meet. Fronts are
aggregations at persistent ocean fronts and aggregations in often characterized by sharp horizontal changes (or gradients) in
subsurface thin layers – are used as examples of interactions between temperature as well as other properties. These gradients, the
organism behavior and physical oceanographic structure and pycnocline and the ocean fronts, are often regions that provide
processes. We then describe how these aggregations influence optimal growth conditions for organisms at the base of the food
organism distribution, oceanic dispersal and, in some cases, larval chain – the phytoplankton. There are frequently steep gradients
recruitment. Finally, we discuss coupled biological–physical models in flow velocity and even reversals in flow direction associated
being used to describe these interactions and some of the persistent with fronts and clines. Consequently, these regions are
features we observe in the sea. characterized by increased shear.

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 Plankton distribution and dispersal 1009

Scales of organism behavior

At microscopic scales, small organisms (e.g. viruses and bacteria)
are dominated by viscous forces. Swimming speeds of these small
organisms are much lower than ambient fluid velocities, and,
consequently, behavioral movements have little effect on their

Behavior
Physics

larger scale distribution patterns. In these cases, physical processes

and structure drive the observed distribution patterns. For all
organisms in a fluid environment, Reynolds numbers (Re):
Re  usL /  , (2)
where us is the organism’s swimming velocity, L is the organism’s
length and v is kinematic viscosity, describe the relative importance
us/Uh,v of inertial (usL) and viscous (v) forces. Similarly, characteristic
Fig.1. Relative influence of physics and behavior in driving the distribution
velocity ratios:
of organisms plotted against the ratio of swimming velocity (us) to Velocity ratio  us / Uv,h , (3)
characteristic velocity (us/Uv,h) where Uv,h refers to vertical and horizontal
flow, respectively. Organism groups are shown in approximate locations where Uv,h refers to vertical and horizontal flow, respectively,
across this continuum. define the ability of an organism to swim against a flow. At the
smallest scales mentioned above, Reynolds numbers and velocity
ratios are typically orders of magnitude less than unity. However,
Shear has been hypothesized to have a significant influence on as organism size and motility increase, the interaction of organism
the spatial structure of plankton patches in the ocean. Velocity shear behavior with physical processes becomes more complex (Fig.1).
(defined as the change in flow speed from one point in the ocean Even at the modest scales of phytoplankton, interactions
to another, divided by the distance between the two points) imparts between behavior and hydrodynamics begin to affect the larger
strain on a scalar patch in the ocean (Eckhart, 1948). Vertical scale distribution patterns of the population. In these cases,
velocity shear, S (with units of s–1), is defined as: Reynolds numbers and characteristic velocity ratios are still less
than one. As an example, vertically swimming dinoflagellates,
S  ⭸u / ⭸z . (1)
which are less than 0.5mm in length and have sustained swimming
In this formulation u is the horizontal flow and z is the vertical speeds of less than 0.5mms–1, can be trapped in a layer of elevated
dimension. In a two-dimensional flow with vertical variation in shear by gyrotactic trapping (Durham et al., 2009). In gyrotactic
velocity (Fig.2), a patch of plankton with initial dimensions (length) trapping, a weakly negatively buoyant, vertically swimming
of Lx in the horizontal and Lz in the vertical (Fig.2) is transported at organism with a non-symmetric center of mass may encounter a
different depth-dependent rates. The differences in transport result in critical strain rate that prevents the organism from maintaining a
the patch being strained by the sheared velocity profile and tilted vertical orientation. If this critical strain rate is exceeded, the
(Stacey et al., 2007). Therefore, Lx grows in time. Continuity swimming behavior leads to a spiraling pattern and aggregation of
(conservation of mass) in the flow then requires that the patch be multiple organisms. Even if the critical strain rate is not exceeded,
thinned vertically, as the product of Lx and Lz must be constant in the accumulation of phytoplankton in regions of low flow (e.g. Stacey
absence of changes in fluid density or mixing. It has been et al., 2007; Ryan et al., 2008) and diel migration of dinoflagellates
hypothesized that broad patches of plankton may be thinned by between light and nutrient resources can lead to significant
vertical shear due to current jets, frontal dynamics, internal waves or changes in the spatial structure and vertical location of entire
horizontal intrusions (Kullenberg, 1974; Franks, 1995; Stacey et al., phytoplankton populations (Cheriton et al., 2009; Sullivan et al.,
2007; Ryan et al., 2008). Most organisms, especially those in the 2010b). For example, in 2005 a team of oceanographers
plankton, cannot perceive the large-scale dynamics of the ocean. participating in the Layered Organization in the Coastal Ocean
However, gradients in ocean properties at the scale of meters can be Program in northern Monterey Bay, CA, USA, observed vertical
exploited through distinct behavioral responses. These behaviors, movement of the distribution of an entire population of
such as foraging and avoidance, when common to a population, can dinoflagellates. The highly motile dinoflagellate species Akashiwo
lead to distinct patterns in distributions across large areas of the sanguinea exhibited a diurnal vertical migration pattern, with
ocean. In the following section, the important scales of organism daytime distributions near the surface where light levels were
behaviors and swimming capabilities are discussed in relation to sufficient for photosynthesis, and night-time distributions at the
organism size, as they transition from being passive particles to being pycnocline where nutrient levels were increased relative to the
able to determine their vertical and horizontal positions in the ocean. surface (Cheriton et al., 2009; Sullivan et al., 2010b).

Fig.2. A sketch of the effect of velocity shear

on a patch of fluid. In a two-dimensional flow
with vertical variation in velocity, a patch of
Lx
plankton with initial dimensions of Lx in the
Lz horizontal and Lz in the vertical is transported
at different depth-dependent rates. Redrawn
from Stacey et al. (Stacey et al., 2007).

U=U0+αz Time

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1010 M. A. McManus and C. B. Woodson

Moving up a trophic level, at the sizes of small zooplankton, noted, however, that foraging responses of larger organisms to
Reynolds numbers and characteristic velocity scales are lower trophic level prey tie these distributions to the ocean physics
transitional and of similar order to unity (0.1–10.0). For these that drive patterns at smaller scales, the importance and prevalence
organisms active behaviors, such as vertical movement to of which are described in the next section.
maintain depth and foraging in the vertical, can form
aggregations (Wolanski and Hamner, 1988; Turchin, 1991; Pattern and distribution in the ocean
Genin, 2004). Many species of copepods exhibit elaborate Even with its immense productivity, the oceans of the world have
hierarchical foraging behaviors involving specific responses to relatively low production across much of their domain. Basic
velocity shear, density gradients and food resources. Such scaling of the ocean environment suggests that a well-mixed
behavioral hierarchy suggests that copepod foraging is cued into euphotic zone could not support the high levels of production
the oceanographic mechanisms that lead to plankton patchiness observed (Mullin and Brooks, 1976). From micro-organisms to
(Woodson et al., 2005; Woodson et al., 2007). Such behaviors phytoplankton, nutrient resources would be too low to support
suggest that copepods can utilize physical cues to identify substantial growth. At increased spatial and temporal scales, if the
regions where there is higher probability of prey resources. ocean properties were homogeneous, small grazing organisms (e.g.
However, shear does not induce feeding behavior, and additional copepods, krill, sardines, anchovies) would not be able to meet
cues (e.g. chemical exudates from photosynthesis, food presence, energetic requirements (Mullin and Brooks, 1976). For example, if
etc.) are required to induce feeding (Woodson et al., 2007). the ocean were well mixed, individual prey items for many
Foraging behaviors can lead to aggregation in food resource zooplankton would be of the order of 10–100cm apart with no cues
patches (Menden-Deuer and Grunbaum, 2006; Woodson et al., for the detection of additional prey particles given an encounter
2007), and to movement into regions with reduced flows. with an initial prey item. An individual copepod needs to locate of
Organisms that maintain their position in regions of reduced flow the order of 1000 prey items each day just to meet energetic
would be transported horizontally shorter distances than those requirements. Fortunately, for marine organisms (and fisherfolk),
organisms outside regions with reduced flow (McManus et al., the ocean is highly structured as a result of basic hydrodynamics,
2005) (reviewed by Woodson and McManus, 2007). and it is this structure, coupled with organism behavior, that drives
The vertical characteristic velocity ratio (us/Uv) for small the patchiness of predators and prey alike (e.g. Wolanski and
zooplankters, including marine invertebrate larvae, is typically one Hamner, 1988; Daro, 1988; Genin, 2004), which in turn fuels the
or larger. These organisms can actively swim against vertical flows bountiful productivity of marine ecosystems.
to maintain their position near convergent fronts, propagating internal In addition to the high level of patchiness across multiple scales
tidal bores, within pycnoclines or near the bottom (Forward and in the ocean, spatial scaling is not isotropic because vertical scales
Tankersley, 2001; Pineda, 1999; Genin, 2004; Genin et al., 2005). are highly compressed relative to horizontal scales. This asymmetry
Such behaviors can lead to aggregation and distinct distribution in spatial scales is due to the fact that (1) ocean basins are broad and
patterns among zooplankton. This ability also allows zooplankters to shallow (e.g. with dominant width scales of ~10,000km and mean
exploit flows associated with tides and other periodic motions to depths of 4km), (2) changes in density caused by variations in
enhance directed transport (Forward and Tankersley, 2001; Naylor, temperature and salinity can confine vertical fluid motion, and (3)
2006). The ability to maintain vertical position will also be influenced photosynthetically active radiation (PAR), which is the light that
by the amount of turbulence in the water column (McManus et al., photosynthetic organisms use for growth, decays exponentially from
2003). In a study undertaken in a small fjord off the coast of the surface with depth. Consequently, patchiness and ocean structure
Washington State, researchers observed persistent subsurface in the vertical is of the order of meters. Small organisms in the ocean
aggregations of mysids (see section entitled ‘Thin plankton layers’). have evolved to exploit this asymmetry such that most zooplankton
The authors suggested that the mysids were actively migrating to the and smaller organisms forage using vertical migrations and larger
pycnocline to produce this aggregation. The subsurface aggregations organisms often employ both vertical and horizontal searches for
were temporarily dispersed only when turbulence was enhanced as prey and resources. Ocean structure that provides an environment for
a consequence of the passage of solitons (e.g. solitary internal biological patchiness is common in the vertical as well as the
waves). In other words, the aggregations were maintained when the horizontal despite the disparity in spatial scales. This disparity simply
mysid migration speeds were greater than the vertical velocities implies that organisms of different size and behavioral capabilities
associated with active mixing and turbulence, and the animal exploit vertical and horizontal structure differently. As an example,
aggregations broke down when the vertical mixing was greater than ocean fronts develop where two spatially separated water masses
the animal’s migration speed. The disturbance by the passage of with different hydrographic properties meet. These areas are known
solitons was only temporary and the aggregations of mysids reformed as biological hotspots for many higher trophic level organisms. We
in less than an hour (McManus et al., 2003). expand upon this example in the following section.
For larger animals living at larger spatial scales, behavior may We would like to emphasize that the goal of this manuscript is
drive observed patterns in organism distribution. For these to convey the notion that the spatial distributions of organisms in
organisms, Re and velocity ratios are much greater than unity. Most the ocean (from the smallest plankton to the largest predators) are
small fishes can sustain a swimming speed of tens of cms–1 except determined by interactions between organism behavior and
during very early pelagic life stages. These velocities are orders of physical oceanographic structure and processes. We discuss two
magnitude larger than the observed sustained vertical velocities in examples (thin layers and persistent fronts) that demonstrate these
the ocean (which are on the order of 1mms–1), with rare exceptions interactions; however, there are numerous other examples that
observed during intermittent large surface wave events, internal could have been used, for example ocean eddies or aggregations of
waves and intense wind-driven turbulence (e.g. D’Asaro et al., organisms at the interface of the internal tidal bores. We have
2007). For these larger organisms, behaviors ranging from foraging chosen thin layers and persistent fronts as examples because over
to predator avoidance, mating and migration are the dominant the past two decades we have played crucial roles in the discovery
factors influencing population distributions (Fig.1). It should be and quantification of these features.

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 Plankton distribution and dispersal 1011

Persistent fronts
Fronts, common features of all marine ecosystems from estuaries to
the open ocean, are formed by a variety of physical mechanisms. For
many decades, the scientific community has known that life forms
as diverse as phytoplankton, crustaceans, fish, marine mammals and
birds alter their distribution in the presence of oceanic fronts (Pingree
et al., 1975; Owen, 1981; Le Fevre, 1986). However, it has been
shown only recently that ocean fronts [which have previously been
linked to larval recruitment (Roughgarden et al., 1991; Wing et al.,
1995)] when ‘persistent’ can drive recruitment patterns across large
spatial scales over time scales of nearly a decade (Woodson et al.,
2012). Persistent ocean fronts, which are common in upwelling
regions near changes in topography and bathymetry, can have
gradients in physical, chemical and/or biological properties.
Persistence through time leads to both passive and behavioral
accumulation of organisms. These persistent ocean fronts play
important roles in the connectivity of marine populations and, in turn,
the spatial distribution of entire marine ecosystems.
Many intertidal and benthic marine species have a planktonic
larval phase, and populations in the intertidal zone are heavily
influenced by the supply of these larvae (Paine, 1966; Dayton, Fig.3. Front probability for Monterey Bay region for a 2week period in June
1971; Caley et al., 1996; Connolly and Roughgarden, 1998). Larvae 2007 computed using the probabilistic method described in Woodson et al.
(Woodson et al., 2012).
are released into the water where they are transported and dispersed
by oceanographic processes. Larvae then return to adult habitats
after a planktonic stage, which may range from a few hours to
several months depending upon the species and the environmental organisms) to these features, we can make a better estimate of the
conditions. Convergent fronts, which are present in many coastal dispersal patterns of plankton and recruitment of larvae in the
waters, have been shown to aggregate organisms that are passive marine environment, and the resilience of marine ecosystems.
or have weak swimming capability (e.g. phytoplankton). Because
of reduced mixing, elevated nutrients and adequate light levels, Thin plankton layers
ocean fronts can also be regions of enhanced phytoplankton It is common to have a subsurface stratified region (or a pycnocline)
growth. The resulting increased phytoplankton biomass at ocean trailing estuarine fronts, near-shore upwelling fronts and tidal
fronts can lead to the active aggregation of stronger swimming mixing (shelf-sea) fronts. Within the coastal marine environment,
organisms searching for food [e.g. larvae, zooplankton and larger planktonic organisms frequently congregate below the surface in
predators (Bjorkstedt et al., 2002; Genin, 2004; Genin et al., 2005; the base of the pycnocline in vertically thin layers (Fig.4). While
Landaeta and Castro, 2006; Woodson and McManus, 2007)]. of limited vertical extent (usually <3m), these thin plankton layers
Because of the increased food resources at ocean fronts, stronger can persist in the marine environment over large temporal and
swimming organisms spend a longer percentage of time foraging horizontal spatial scales and often contain concentrations of
in these regions and, as a result, their relative dispersal distances organisms several orders of magnitude greater than those above and
can be decreased (Woodson and McManus, 2007). below the layer (Sullivan et al., 2010a).
Using 8years of satellite sea surface temperature (Fig.3) and Previously undetectable, thin layers are now observable as a result
chlorophyll a imagery (which is a standard proxy for phytoplankton of advances in high resolution sampling methods and technology.
concentration), in addition to an 8year time series of recruitment Results from two decades of research reveal that thin plankton layers
data for both barnacle and rockfish larvae from the Partnership for are a crucial component of marine ecosystem dynamics. Far from
Interdisciplinary Studies of Coastal Oceans program, Woodson et being unusual or rare, thin layers of plankton are common features
al. (Woodson et al., 2012) found that coastal ocean fronts that and can be found in a wide variety of environments (Bjornsen and
maintained their average spatial location over periods of years are Nielsen, 1991; Donaghay et al., 1992; Cowles and Desiderio, 1993;
correlated with regions of high chlorophyll concentration, as well Dekshenieks et al., 2001; Cowles, 2003; McManus et al., 2003;
as increased recruitment of invertebrate and fish species across the McManus et al., 2005; Cheriton et al., 2007; McManus et al., 2008;
entire California Current Large Marine Ecosystem (CCLME). The Ryan et al., 2008; Cheriton et al., 2009; Ryan et al., 2010). Thin
CCLME is located along the west coast of the US, in the eastern plankton layers have been shown to contain up to 75% of the total
Pacific. It extends between 32°N and 46°N, covering a distance of biomass in the water column (Holliday et al., 2010; Sullivan et al.,
1810km. Woodson et al. (Woodson et al., 2012) found positive 2010b). Thus, they can be concentrated areas of intense biological
correlations between the long-term (8year) location of persistent activity (Sullivan et al., 2010a).
fronts and the recruitment of the larvae of important community- In order to understand the formation, maintenance and
building and commercially important species. The novel part of this dissipation of a thin planktonic layer, one must consider the
study is the ability to identify regions with fronts that recur across physical, chemical and biological mechanisms acting in concert on
time scales of nearly a decade, and to relate these features to the a layer. For thin layers to form and persist in the marine
dispersal and recruitment of plankton. This type of long-term environment, the divergent processes acting on the layer cannot
assessment was not previously possible. With new knowledge of exceed the convergent processes (Osborn, 1998; McManus et al.,
the long-term persistence of these features, combined with our 2003; Stacey et al., 2007). Convergent and divergent processes can
understanding of the behavioral response of larvae (and other be physical or biological. Some examples of convergent processes

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1012 M. A. McManus and C. B. Woodson

Mean water level (m)

A 1

−1
ap440 (m–1)
B 0
1

10 0.5
0
U (m s–1)
C 0 0.2

10 0

−0.2
V (m s–1)
D 0 0.2

10 0

−0.2
Temperature (°C)
E 0
16
10 14
12
Salinity
F 0 33.7

10 33.6

33.5
σt (kg m–3)
G0 25.5

10 25

24.5
22:00 23:00 00:00 01:00 02:00 03:00 04:00 05:00 06:00
26−27 August 2005 (h:min)

Fig.4. Time series of data from 21:30h on 26 August to 06:00h on 27 August 2005. (A)Water level (m) from a bottom-mounted acoustic Doppler current
profiler (ADCP), (B) ap440 (m–1), a proxy for phytoplankton biomass from 99 consecutive profiles (~4min each) with a high-resolution profiler, (C) eastward
(U) and (D) northward (V) current velocity (ms–1) measured by a vessel-mounted ADCP, and high-resolution profiler measurements of (E) temperature (°C),
(F) salinity and (G) density (t; kgm–3). Solid black lines indicate the upper and lower boundaries of the ap440 layer. For B–G, y-axis is depth (m). Redrawn
from Cheriton et al. (Cheriton et al., 2009).

are straining by shear, as well as active swimming to physical, oscillations caused by internal waves must also be considered
chemical and/or biological gradients on the part of both (Cheriton et al., 2009).
phytoplankton and zooplankton. Some examples of divergent In a study undertaken in a small fjord off the coast of Washington
processes are turbulent mixing and behavioral movement away State, researchers (McManus et al., 2003) observed thin subsurface
from physical disturbances in the water column. layers of mesozooplankton. These researchers suggested that a
In 2005, Steinbuck and colleagues, working in northern biological mechanism involving migratory behavior brought
Monterey Bay, examined thin subsurface layers of dinoflagellates mysids to the pycnocline where dense thin layers of phytoplankton
and the small scale physical processes associated with these layers were also located. The researchers observed that mesozooplankton
(Steinbuck et al., 2009). They found that a high dinoflagellate layers were temporarily dispersed only when turbulence levels
swimming speed was required during layer formation to overcome exceeded the speed of vertical migration during the passage of
turbulent mixing and to match the observed formation time. solitary internal waves (McManus et al., 2003). These fine-scale
However, after formation a reduced swimming speed was required structures were shown to modify animal behavior. This
to maintain the layer. Cheriton and colleagues point out that modification of behavior and position, in turn, impacts the way
ephemeral vertical displacements of these layers caused by the marine ecosystems function.
passage of solitary internal waves can have a greater influence over In another undertaken in Monterey Bay in 2006, Benoit-Bird
layer maintenance than shear by straining or by organism found that fish (the Pacific sardine Sardinops sagax and the
swimming (Cheriton et al., 2009). Thus, for a model to accurately northern anchovy Engraulis mordax) were attracted to zooplankton
describe thin layer dynamics in an environment with internal thin layers (Benoit-Bird, 2009). Fish were shown to spend
waves, the convergent and divergent effects of the vertical significantly more time within zooplankton layers, modifying their

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 Plankton distribution and dispersal 1013

usual behavior when thin zooplankton layers were present. Tracks

of individual fish revealed they were diving down through a
zooplankton layer before spiraling slowly upwards through the
layer. The upward portion of this behavior corresponded with a
dramatic decrease in the intensity of acoustic scattering (a proxy
20
for zooplankton density), resulting in the appearance of ‘holes’ in
the layer, which reformed minutes after the fish departed (Benoit-

Depth (m)
Bird, 2009). The conclusion was that thin layers could have 30
significant ecological effects throughout the food chain. As
organisms increase in size, organism behavior becomes
increasingly important for thin layer dynamics. 40
While Benoit-Bird (Benoit-Bird, 2009) discusses the temporary
disruption of thin layers of zooplankton by individual predatory fish 10
movements, she points out that the thin layers were resilient over 10
time to the apparent foraging fish. Following the work of Huntley 0
0
and Zhou (Huntley and Zhou, 2004), however, one must consider Across (cm s–1) –10 –10 Along (cm s–1)
that large schools of fish might have the ability to produce enough
turbulence to mix out these layered structures. Huntley and Zhou Fig.5. An example of the spatial coincidence between thin layers and
analyzed data on the hydrodynamics of swimming of 100 marine changes in the direction of horizontal current velocity in northern Monterey
species, across a range of sizes from bacteria to blue whales (Huntley Bay on 6 September 2003 at 21:00 h. Velocity profiles are represented as
and Zhou, 2004). They concluded that turbulent energy dissipation vectors; thin layer vertical ranges are shown by the shaded bars. Redrawn
in the presence of schooling animals could be three to four orders of from Ryan et al. (Ryan et al., 2008).
magnitude greater than the background average rate of turbulent
energy dissipation. Making concurrent observations of turbulence
and organism distribution is quite difficult in the field (see Katija, After a comprehensive review of the published literature, we
2012). Following the theoretical treatment of the subject by Huntley (Woodson and McManus, 2007) presented a meta-analysis of
and Zhou (Huntley and Zhou, 2004), Kunze et al. (Kunze et al., 2006) horizontal dispersal distances from 59 historical oceanographic
and Katija (Katija, 2012) present evidence that vertically migrating studies that concurrently documented oceanographic conditions
organisms can enhance turbulent mixing in the water column. This and in situ organism distributions. Out of 59 studies that met their
could be an important source of fine-scale turbulent mixing in the search criteria, 78% reported organism aggregations that were
ocean. It may be a key mechanism by which nutrients are periodically associated with fronts or clines (e.g. pycnocline, thermocline,
transported across the pycnocline of strongly stratified systems, thus halocline). These associations were consistent across multiple
providing the fuel for the lower trophic levels that the schooling fish trophic levels, from phytoplankton to whales.
require for sustenance (Kunze et al., 2006). In spite of the presence of frontal jets associated with frontal
In the most spatially comprehensive study available, thin features, biological accumulation is often focused at or near the
plankton layers were identified in 2000km of over 80,000km of region of reduced flow where high horizontal shear results from
airborne LIDAR data collected from a variety of oceanic and changes in flow direction. In some cases, such as shelf-break fronts,
coastal waters. The characteristics of thin layers varied over this this condition extends to the sea floor and thus acts as a barrier to
vast spatial expanse. Many of the observed layers were self- offshore transport throughout the water column (reviewed by
contained features consistently <3–4m in vertical extent, and Woodson and McManus, 2007). Association with such regions of
1–12km in horizontal extent. Other thin layers were portions of low flow velocity reduces the transport and dispersal of plankton
much more spatially expansive layers that had regions where the populations.
layer became thicker, and thus were no longer classically defined Flow reversals at fronts and clines are ubiquitous in coastal
as ‘thin layers’ (Churnside and Donaghay, 2009). The areas systems worldwide (Mann and Lazier, 2006). Because flows are
surveyed were inclusive of upwelling regions, areas with often reduced in these regions of reversal, dispersal distances for
significant freshwater inflow and warm core ocean eddies. larvae and zooplankton in these regions could be hundreds of
kilometers less than many present-day dispersal estimates
Organism transport in fronts and clines (Woodson and McManus, 2007). This pattern holds across several
In a 2002 study in northern Monterey Bay, researchers (McManus taxonomic groups of zooplankton including copepods (weak
et al., 2005) found that zooplankton layers – most likely swimmers), krill (relatively strong swimmers), invertebrate larvae
composed of one species of krill, Thysanoessa spinifera – were and fish larvae. Reduced transport implies that individual
located near the base of the pycnocline, either within the layer of populations might be more isolated than currently accepted, and
no motion or in regions with low current velocities (<6cms–1). that patterns of dispersal and connectivity could be highly
These organisms are active swimmers and were most likely structured.
associated with the pycnocline because of increased
phytoplankton densities in this region. Because the majority of Modeling plankton distributions and oceanic dispersal
these organisms were located in regions of the water column with It has been established that marine organisms across a range of
low current velocities, this vertical positioning may result in a scales, from microscopic plankton to higher level predators, are
decrease in the horizontal dispersal distance of these organisms located in regions of the ocean with strong physical gradients.
within this system. An example of the spatial coincidence between These concurrent biological and physical distributions have
thin layers and changes in direction of horizontal current velocity tremendous implications for the physiological state of the marine
is given in Fig.5. organism, as well as for oceanic dispersal.

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1014 M. A. McManus and C. B. Woodson

Because of their size and lifespan, it is possible to track larger with larval size was tested. In the first simulation, predation
predators. For example, loggerhead turtles with Argos satellite pressure decreased with increasing larval size. In the second
tracking tags have been followed as they traveled along a basin- simulation, predation pressure increased with increasing larval size.
wide chlorophyll front – the transition zone chlorophyll front, In the third simulation, predation pressure was constant across all
which is located at the boundary between the low chlorophyll larval sizes. Simulation one showed the highest survivorship when
subtropical gyre and the high chlorophyll subarctic gyre (Polovina the predation pressure decreased with increasing larval size.
et al., 2001). Because of the ability to track these animals, and Additional simulations showed that the interaction between vertical
locate the transition zone chlorophyll front with satellite remote migration and predation determined the percentage of the cohort
sensing, we now understand that apex predators use this feature as that survived to settlement size. The results from this modeling
a migratory pathway across the North Pacific (Polovina et al., study reaffirm the assertion by Landry (Landry, 1976), and Steele
2001). and colleagues (Steele, 1976; Steele and Henderson, 1992) that the
For microscopic plankton, like larvae, the task of tracking form of the mortality term used in models is crucial in determining
oceanic dispersal is much more complex. Coupled the accuracy of the simulated distributions.
biological–physical oceanographic models provide one set of tools While coupled biological–physical oceanographic models are
that are increasingly being used to predict larval dispersal patterns increasingly being used to calculate larval dispersal, there are
(Cowen and Sponaugle, 2009; Metaxas and Saunders, 2009). shortcomings to this approach. First, many physical models under-
Physical oceanographic models calculate water movement and resolve features of water flow that are important to community
physical attributes within a study grid. Biological models, which dynamics. Because of large horizontal and/or vertical grid sizes,
range in complexity, attempt to mimic processes occurring during and in some cases because of long time averaging, many physical
the larval lifespan. Results from coupled biological–physical circulation models under-resolve features like near-shore persistent
numerical models show that pelagic larval duration, larval behavior fronts, vertical stratification and internal tidal bores. This is
and larval mortality have pronounced effects on larval distribution unfortunate because features like persistent fronts, vertical
and dispersal patterns (Dekshenieks et al., 1996; Dekshenieks et al., stratification and internal tidal bores have been associated with
1997; Paris and Cowen, 2004; Pfeiffer-Herbert et al., 2007; North larval transport and recruitment in observational studies (Pineda,
et al., 2008). 1999; McManus et al., 2005; Woodson et al., 2012). In addition,
Because pelagic larval duration varies with environmental because physical flows become non-linear close to shore, many
factors, species-specific models have been developed in which physical circulation models do not extend into the inner shelf and
larval growth rate is a function of environmental factors near-shore regions. Thus, processes that would transport larvae
(Dekshenieks et al., 1993). Environmental factors that have been from the shoreline to 1–2km offshore (and back again) are not
shown to alter growth rate of a specific species in the laboratory included in many modeling studies. Second, the biological
include (but are not limited to) temperature and food concentration components of these coupled models rarely incorporate species-
(Davis, 1958; Davis and Calabrese, 1964; Huntington and Miller, specific organism behaviors that contribute to distribution patterns.
1989; Olson and Olson, 1989; Pechenik, 1987; Scheltema and This can happen for a variety of reasons. As one example – many
Williams, 1982). Model results suggest that the length of time models of basin-scale processes produce daily-averaged output.
larvae are in the water column can affect both dispersal and These models cannot resolve higher frequency processes like
settlement patterns (Siegel et al., 2003). diurnal migration or foraging behavior. Another reason that these
A crucial component that is often neglected in coupled coupled models rarely incorporate species-specific organism
biological–physical oceanographic models is larval behavior. behavior is that the behaviors are simply not known. The scientific
While many larvae are not capable of swimming against horizontal community should make an effort to understand and quantify these
currents, they are capable of swimming vertically (Mileikovsky, behaviors, whenever possible. For, without these capabilities,
1973; Mann, 1986). The ability to change depth allows larvae to calculated larval dispersal patterns may be incorrect. It is important
move into different strata of the water column, where current to remember that this is an iterative process, which requires
direction can differ significantly. Observations of larval behavior ongoing discussions between ecologists, oceanographers and
in the laboratory and observations of ontogenetic position in the modelers. With each new study, our scientific community gets a
field have been used to parameterize behavioral components for step closer to the answer (Galindo et al., 2010).
biological models (Dekshenieks et al., 1996; Pfeiffer-Herbert et al.,
2007). Coupled biological–physical numerical models including Review and conclusions
larval behavior show that behavior significantly changes larval In this contribution, we have highlighted how persistent mesoscale
dispersal trajectories (Rothlisberg, 1983) and ultimately population and fine-scale physical structures in the ocean, coupled with passive
connectivity (Paris et al., 2007). If larvae position themselves and active organism responses, lead to persistent structures in
within fronts, and clines, it is highly likely that their dispersal marine populations (Dekshenieks et al., 2001; Woodson and
distances will be much shorter than those hypothesized based upon McManus, 2007; Sullivan et al., 2010a; Woodson et al., 2012).
pelagic larval duration alone (reviewed by Woodson and The ocean is highly structured as a result of basic
McManus, 2007). hydrodynamics, both horizontally and the vertically – this structure
The relative importance of different factors causing larval is most pronounced in coastal waters. For example, in a horizontal
mortality (e.g. predation, starvation, physiological stress) is not plane when two water masses with different hydrographic
known (Morgan, 1995). Mortality is often referred to as the ‘closure properties meet, there is a high probability one will encounter an
term’ in modeling studies (Steele, 1976; Steele and Henderson, ocean front. Because of reduced mixing, elevated nutrients and
1992). Dekshenieks and colleagues developed a numerical model adequate light levels in these areas, ocean fronts can be regions of
to assess the effect of different forms of size-specific and depth- enhanced phytoplankton growth. The resulting increased
dependent predation on larval survivorship (Dekshenieks et al., phytoplankton biomass at ocean fronts can lead to the active
1997). Three simulations were run, in which variable predation aggregation of stronger swimming organisms searching for food

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 Plankton distribution and dispersal 1015

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