Download The influence of midwater hypoxia on nekton vertical migration

1296
The influence of midwater hypoxia on nekton vertical migration
Sandra L. Parker-Stetter, John K. Horne, and Mariko M. Langness
Parker-Stetter, S. L., Horne, J. K., and Langness, M. M. 2009. The influence of midwater hypoxia on nekton vertical migration. – ICES Journal of
Marine Science, 66: 1296– 1302.
Hypoxia affects pelagic nekton, fish and large zooplankton, distributions in marine and fresh-water ecosystems. Bottom hypoxia is
common, but midwater oxygen minimum layers (OMLs) may also affect nekton that undergo diel vertical migration (DVM). This
study examined the response of pelagic nekton to an OML in a temperate fjord (Hood Canal, WA, USA). A 2006 study suggested
that the OML created a prey refuge for zooplankton. Using acoustics (38 and 120 kHz), the 2007 night DVM patterns of
nekton were quantified before (June, August) and during (September) an OML. All months had similar precrepuscular distributions
(.50-m depth) of fish and invertebrates. During the September evening crepuscular period, a zooplankton layer migrated upwards
(.1.5 m min21), but the layer’s rate of ascent slowed to ,0.5 m min21 when it reached the lower edge of the OML. The bottom
edge of the layer then moved below the OML and remained there for 13 minutes before moving through the OML at
.1.0 m min21. As in June and August, fish in September followed the upward migration of the zooplankton layer to the surface,
crossing through the OML. Our results suggest that the 2007 OML did not affect zooplankton or fish vertical distributions.
Keywords: acoustics, diel vertical migration, fish, hypoxia, zooplankton.
Received 8 August 2008; accepted 17 November 2008; advance access publication 10 February 2009.
S. L. Parker-Stetter, J. K. Horne and M. M. Langness: School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195-5020, USA.
Correspondence to S. L. Parker-Stetter: tel: þ1 206 221 5459; fax: þ1 206 221 6939; e-mail: [email protected].
Introduction
Diel vertical migration (DVM) is a common ecological strategy for
both fish and zooplankton. Whether undergoing DVM for
feeding, predator avoidance, or to maximize energetic efficiency
(Hays, 2003; Scheuerell and Schindler, 2003; Mehner et al.,
2007), organisms may migrate through hundreds of metres of
water (Pearcy et al., 1977; Heywood, 1996; Herring et al., 1998)
that differ in oceanographic properties. Based on biological tolerances, fish and zooplankton may alter their vertical or horizontal
distributions or both features at the same time relative to water
conditions (Andersen et al., 1997; Keister et al., 2000; Craig and
Crowder, 2005). Dissolved oxygen (DO) is one oceanographic
property that may differentially influence migration patterns.
DO affects fish and zooplankton distributions in marine, estuarine fresh-water systems throughout the world (Marcus, 2001;
Pollock et al., 2007). As a result, responses by a wide variety of
organisms to low DO conditions are well studied. Some species
of fish and zooplankton are highly tolerant of low DO, remaining
in hypoxic waters during all or some portion of their DVM cycle
(e.g. Wishner et al., 2000; Butler et al., 2001; De Robertis et al.,
2001). In contrast, some pelagic fish and zooplankton species
shift their distribution vertically or horizontally (e.g. Keister
et al., 2000) into water with higher DO but suboptimal thermal
or salinity characteristics (e.g. Fry, 1937; Horppila et al., 2000).
Differences in predator and prey responses to low DO may
affect both DVM and the resulting transfer of energy in aquatic
systems. If predators and prey are both intolerant of hypoxic conditions, the two may be constrained to a smaller, shared region of
the water column and result in high mortality of prey (Prince and
Goodyear, 2006). When prey, but not predators, are tolerant of
hypoxic conditions, a low DO refuge may form that reduces
prey mortality (e.g. Klumb et al., 2004). Such a refuge may sometimes facilitate a complex coexistence of predators that feed on a
common prey species during DVM (Horppila et al., 2000).
Monitoring fish and zooplankton distributions may provide a
proxy index for environmental health by identifying potential
shifts in trophic transfer in episodically or chronically oxygenstressed systems.
Hood Canal (WA, USA, Figure 1) is a temperate fjord that has
historically experienced low DO in bottom waters and the development of a midwater oxygen minimum layer (OML) during
autumn (Newton et al., 1995). An increased occurrence of fish
kills, and uncertainty about ecological disruptions as a result of
low DO, has led to fishery closures (Bargmann, 2003). A day/
night study in Hood Canal in 2006 suggested that the OML
might influence predator–prey dynamics by restricting the vertical
extent of fish, but not zooplankton, night-time vertical migration
(referred to as DVM in this paper; Figure 2).
The present study was undertaken to examine the dynamics and
potential effects of low DO on the DVM of zooplankton and fish.
Specific objectives were to characterize zooplankton evening crepuscular, i.e. +45 minutes from sunset, approximately civil twilight,
vertical migration, and assess the concurrent vertical distribution
of fish before and after the development of an OML.
Methods
Study site
Hood Canal (478350 000 N, 1228550 000 W) is located in Puget Sound,
WA, USA (Figure 1). Water exchange is limited by a shallow sill
(45 m) that precedes a deep channel (120 –180 m). The residence
# 2009 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved.
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Nekton vertical migration and midwater hypoxia
Figure 1. Map of Hoodsport study site in Hood Canal, WA, USA.
The shallow sill is located in the immediate northeast corner of the
map. The inset map displays the study-site location on the North
American west coast. The night-time survey grid is shown as an
expansion. Evening crepuscular sampling was at the centre of the
survey grid.
time of water in Hood Canal ranges from 40 d during summer to
250 d during winter (Babson et al., 2006).
long), with hull-mounted, 38- and 120-kHz, Simrad split-beam
transducers (ES 38-12, 128 3 dB beam width, 1000 W input
power; ES 120-7C, 78 3 dB beam width, 500 W input power) operated with Simrad ES60 transceivers, was used during June and
September. In August, 38- and 120-kHz, split-beam, Simrad transducers (ES 38-12, 128 3 dB beam width, 1000 W input power; ES
120-7C, 78 3 dB beam width, 500 W input power) operated with
Simrad EK60 transceivers were deployed on a towed body from
the RV “Mackinaw” (7 m long). All transceivers were operated
at 2 pings s21 and 0.512 ms pulse duration.
A 500 m500 m sampling grid (Figure 1) was surveyed .1.5 h
before and after sunset to provide day and night characterizations
of zooplankton and fish distributions. Daytime data are not presented in this paper. During the evening crepuscular period, the
vessel anchored or drifted at the centre of the grid to record
changes in vertical distributions.
Oceanographic data were collected by deploying a Conductivity–
Temperature–Depth (CTD) sensor (Seabird Seacat 19þ) from the
vessel (September) or an Oceanic Remote Chemical–Optical
Analyser mooring (ORCA; Dunne et al., 2002) located in the study
grid (June, August). Oceanographic profiles for temperature, salinity,
and DO were recorded within three hours of crepuscular sampling.
A light-intensity logger (Onset Computer Corporation,
Hobo-LI) was deployed on the bow of the vessel, just above the
waterline, to provide optical data for crepuscular analyses. These
data were smoothed with a super-smooth function that used
local cross-validation in the fit (Friedman, 1984).
Data collection
Acoustic data were collected on 11 June, 2 August, and 11
September 2007 at Hoodsport in Hood Canal (Figure 1). Two
vessels were used for the purpose. The RV “Centennial” (18 m
Acoustic data processing
The systematic variation in ES60 echosounder data (June,
September) was removed using the ES60adjust program (Keith
Figure 2. Hoodsport September 2006 (a) day (.2 h before sunset) and (b) night (.2 h after sunset), modified from Parker-Stetter and
Horne (2009). (i) DO profile with 2 mg l21 hypoxia value marked as a horizontal black dashed line, (ii) 38 kHz echogram image with bottom
shown as lower black region, (iii) % depth distribution of 38 kHz backscatter [NASC (sA), m2 nautical mile22], and (iv) individual fish
distribution from 38 kHz data (target strength, dB re 1 m2).
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et al., 2005). Acoustic data were processed with Echoview
4.40.64.11098 (Myriax Pty Ltd, 2008). Transducer parameters
(gain, Sa correction) were based on on-axis calibrations
done before (September) or after (June, August) the acoustic
surveys. Sound speed and absorption were calculated from the
CTD or ORCA oceanographic data collected during the
survey. Vessel noise in the mean volume-backscattering (Sv)
data (38 kHz ¼ 2125 dB re 1 m21, 120 kHz ¼ 2130 dB re 1 m21)
was removed by linear subtraction. Sv noise estimates were
projected into the 40 log r TS domain and removed by linear
subtraction. The sounder-detected bottom was examined,
corrected as needed, and a 0.5-m backstep buffer was applied.
The top 5 m of the water column was ignored to avoid transducer
saturation and inclusion of near-surface bubbles. Noise within the
water column, e.g. when passing over the anchor line or dropped
data pings, was removed manually.
Fish were classified using a 256 dB re 1 m2 TS minimum
threshold in both the 38 kHz Sv and TS data. This threshold was
based on the expected TS (Traynor, 1996) of the smallest fish captured, a 4-cm Pacific hake Merluccius productus, during the June
and September midwater trawling. No maximum fish-TS
threshold was applied to the data. Fish data were exported in
1 min horizontal by 5 m vertical bins.
For zooplankton classification, a 277 dB minimum Sv
threshold was applied to the 120 kHz data. This threshold was
the expected Sv from the lowest density of zooplankton
(2000 m23) found during 253-mm vertical net tows in July and
September (MML, unpublished data). As these tows were dominated by calanoid copepods (.75% by number Paracalanus
parvus and Calanus pacificus, MML, unpublished data), a TS of
2110 dB (Stanton and Chu, 2000) was assumed for TS estimation.
Values below the minimum threshold were assigned 2999 dB (0 in
the linear domain, Myriax Pty Ltd, 2008). To remove fish from the
zooplankton 120 kHz Sv data, the 38 kHz fish-TS data were used as
a mask. To account for offsets in transducer location and sampling
volumes, a 3 3 sample dilation (Myriax Pty Ltd, 2008) was used
to physically expand fish echoes that exceeded the 38 kHz, 256 dB
TS-minimum threshold. As masked-fish targets in the 120 kHz
data were not zero values for zooplankton, masked-fish regions
were excluded from zooplankton Sv calculations. If the zooplankton
distribution was reasonably uniform within each of the abovementioned bins, excluding masked regions would not influence Sv
estimates.
The upper and lower edges of the zooplankton layer were
defined on the 120 kHz Sv data using a combination of techniques.
First, minimum and maximum layer depths were visually defined
with an external buffer of +2 m. Data from this region were then
extracted by 1 min horizontal and 1 m vertical bins. Upper- and
lower-layer edges were defined for each 1-min-layer segment
where zooplankton backscattering approximately doubled
(Sv ¼ 2.5 –3 dB). The lower-layer edge depth was defined as the
maximum depth of the 1 m cell (e.g. for 50 –51 m, 51 m is the
designated depth), and the upper-layer edge depth was similarly
defined as the minimum depth of the 1 m cell. Layer-edge definitions were plotted, anomalous points, e.g. inclusion of fish
school remnants, were compared with the 120 kHz Sv echogram,
and layer-edge definitions were adjusted for individual 1 min segments. The zooplankton upper- and lower-layer edges were
smoothed to remove small variations that resulted from vessel
motion, using a super-smooth function fitted to the data using
local cross-validation (Friedman, 1984).
S. L. Parker-Stetter et al.
Fish and zooplankton distribution
Fish distribution was characterized using 38 kHz Sv data. Fish Sv
echograms were generated using Sv mean values for each 1 min
horizontal by 5 m vertical bins.
Zooplankton layer attributes were characterized using mean Sv,
depth in the water column, migration rate, and layer thickness. A
mean Sv was calculated for the upper- and lower-layer edges using
all 1 min segments in each sampled month. The migration rate of
the zooplankton layer (m min21) was calculated as the net change
in the upper- or lower-edge depth between successive 1 min horizontal bins. Layer thickness was defined as the difference between
upper- and lower-edge depths within each 1 min horizontal bin.
Results
The water column at Hoodsport was more stratified in August and
September than in June. In all months, surface water (,6 m)
had the highest temperature (11.6 –19.18C), highest DO (6.9–
11.3 mg l21), and lowest salinity (24.6–28.6 psu) values
(Figure 3a–c). In June and August, the lowest DO (,2.2 mg l21)
was near the bottom (.115 m, Figure 3a and b). In September,
an OML had developed and the lowest DO level (1.7 mg l21) was
at 22 m (Figure 3c). A small zone of low DO water (3.7 mg l21)
was also observed midwater (18 m) in June (Figure 3a). There
was no evidence of internal waves at any time. Light intensity
decreased through the crepuscular period, with the maximum
rate of light-intensity change from 22 to 27 min after sunset
(Figure 3a–c).
Zooplankton migrated from depths .75 m to depths ,10 m
during all months. The greatest migration occurred in June, with
the lower edge of the layer migrating from 106 to 16 m and the
upper edge migrating from 84 to 7 m (Figure 3a). August and
September had similar layer migration ranges, with the lower-layer
edge migrating from 80 to 20 m and the upper edge from 50
to 7 m (Figure 3b and c), suggesting that the presence of the
September OML (Figure 3c) did not influence layer-depth range.
Mean Sv for upper and lower zooplankton layer edges were,
respectively, 272.0 and 272.5 dB re 1 m21 in June, 280.3 and
282.2 dB re 1 m21 in August, and 274.6 and 274.4 dB re
1 m21 in September.
Layer thickness was similar among months, but the timing of
maximum thickness differed in September. Maximum layer thicknesses were between 23 and 31 m and the minima were between 9
and 16 m (Figure 3a–c). Changes in layer thickness during DVM
for a given month ranged from 14 to 20 m. In June and August,
maximum layer thickness was at the beginning of the survey at
57 min (June) and 63 min (August) before sunset, and decreased
to a minimum at the end of the survey (97 and 46 min after
sunset, Figure 3a and b). In September, maximum layer thickness
was 17 min before sunset (Figure 3c), but there was another
increase in thickness after sunset. In contrast to June and
August, the zooplankton layer thickness decreased to 18 m at
51 min after sunset in September but then increased, eventually
reaching 24 m at 65 min after sunset (Figure 3c). The initial
increase in thickness at 52 min after sunset corresponded to the
lower edge of the layer reaching the OML (Figure 3c).
Migration rates for the zooplankton layer varied between
20.53 and 1.78 m min21 (Figure 3a –c). In all months, the
highest migration rates were within 30 min of sunset
(Figure 3a –c). In June, migration rates peaked 3 min after the
maximum decrease in light intensity (Figure 3a) and 4– 7 min
Nekton vertical migration and midwater hypoxia
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Figure 3. Oceanography (left panels) and acoustic data (right panels) for Hoodsport in (a) June, (b) August, and (c) September 2007. Left
panel: DO (cyan), temperature (blue), and salinity (red) are plotted against depth. Right panel: zooplankton migration based on 120 kHz Sv
backscatter (yellow to red lines, scale indicates rate of migration), fish acoustic backscatter (Sv) at 38 kHz (shaded white– green – blue, scale
indicates backscatter intensity), and light intensity (black line) plotted against minutes from sunset (0 is sunset, negative values before, positive
values after) and depth for Crepuscular data. Night illustrates the vertical fish distribution from 38 kHz Sv data, collected .100 min after
sunset and averaged over the survey grid indicated in Figure 1, shown for comparison on the same depth scale. The bottom edge of the OML,
the point of the greatest change in DO concentration, is indicated on the September figure (horizontal, thin black line).
before the highest rate of decrease in light intensity in August and
September (Figure 3b and c). After reaching their maxima,
migration rates decreased as the layer continued to move
towards the surface in June and August (Figure 3a and b).
Whereas the upper-layer edge followed this pattern in
September, the lower edge slowed to 0.02 m min21 at 51–52 min
1300
after sunset at a depth of 30 m, just inside the lower boundary of
the OML (2.25 mg l21, Figure 3c). After entering the OML, the
lower edge of the zooplankton layer had a 13-min period of downward migration (20.04 to 20.53 m min21, Figure 3c). At 65 min
after sunset, the migration rate of the lower edge increased
upwards, reaching 1.04 m min21 before decreasing as the layer
approached the surface (Figure 3c).
Fish vertical distribution during the crepuscular period tracked
the DVM of zooplankton during each of the samples taken in June,
August, and September, respectively. In all months, fish were distributed in pelagic- or surface-associated schools, or within a deep
layer (Figure 3a–c). At the beginning of all surveys (45– 70 min
before sunset), the deep layer of fish was present at depths
.50 m (Figure 3a –c). In June, this layer began migrating coincidentally with the zooplankton, but was patchily distributed
.50 m (Figure 3a). During the June night-time survey, by
127 minutes after sunset, fish were uniformly distributed
between 30 m and the bottom, with intense pelagic- and
surface-orientated schools present (Figure 3a). In August and
September, the deep fish layer migrated coincidentally with the
zooplankton layer (Figure 3b and c) and had reached the surface
by the end of the crepuscular surveys (46 and 87 min after
sunset in August and September, respectively). The presence of
fish throughout the water column in August and September was
confirmed by the night-time surveys (348 min after sunset in
August, Figure 3b; 94 min after sunset in September, Figure 3c).
Discussion
The 2007 OML in Hood Canal may have affected the upward
migration of zooplankton, but did not ultimately affect the night
distributions of fish and zooplankton. This suggests that the
potential prey refuge created by the OML in 2006 did not occur
during the 2007 sampling. The formation of a low DO prey
refuge in Hood Canal is probably a function of the intensity of
the OML and organism-specific tolerance levels.
The vertical extent, timing, and migration rates of zooplankton
in this study agree with the results of other DVM studies. In Dabob
Bay, a large bay within the Hood Canal, two calanoid copepods
(Calanus pacificus and Metridia lucens) and an euphausiid
(Euphausia pacifica) undergo regular DVM from depths .50 m
into surface waters ,25 m (Bollens and Frost, 1991; Bollens
et al., 1992; Dagg et al., 1998). As was also observed in the
present study, ambient light levels are the dominant trigger for
the onset of upward migration in copepods and euphausiids
(e.g. Heywood, 1996; Liljebladh and Thomasson, 2001). Upwardmigration rates found in this study, up to 1.78 m min21, are
within the range of DVM rates (0.48–3.2 m min21) measured
for euphausiids, copepods, and amphipods in other marine
systems (e.g. Wiebe et al., 1992; Heywood, 1996; Liljebladh and
Thomasson, 2001).
During upward migration, the lower edge of the zooplankton
layer appeared to react to the OML by decreasing speed and
moving downwards in the water column. The DO concentration
at Hoodsport of 2.25 mg l21 exceeded the limit of 2.0 mg l21 for
hypoxic water. Horppila et al. (2000) suggested that the gradient,
not the DO concentration itself, may restrict the movement. As
salinity, temperature, and light levels were stable at the depth of
the zooplankton response, it is unlikely that these factors contributed to changes in ascent rate and direction.
The apparent response of the lower but not the upper edge of
the zooplankton layer to the OML may indicate that the layer
S. L. Parker-Stetter et al.
comprised multiple species or life stages of one zooplankton
species with different oxygen sensitivities. Copepod life stages frequently occupy water with different oxygen levels during
non-DVM periods, suggesting an oxygen preference (Wishner
et al., 2000; Loick et al., 2005). However, many marine copepod
species are capable of migrating into, out of, or through low-DO
waters during DVM (Besiktepe, 2001; Koppelman and Weikert,
2005; Castro et al., 2007). Mutlu (2003) observed that during vertical migrations of Calanus euxinus into and out of a hypoxic zone,
when the DO was ,0.5 mg l21, the copepods became torpid and
their migration rate decreased. Within hypoxic water, C. euxinus
migrated at rates of 0.49 m min21 (upwards) and 0.34 m min21
(downwards; Mutlu, 2003). These values are within the range
observed when the lower zooplankton edge encountered the
OML in this study. The presence of E. pacifica in midwater-trawl
catches, despite being absent from zooplankton samples, provides
circumstantial evidence that the zooplankton layer comprised
multiple species. As euphausiids may adapt physiologically to
hypoxic conditions (Childress and Seibel, 1998), euphausiid presence in the migrating zooplankton layer may have contributed
to the different responses of the upper and lower edges.
Fish distributions in Hood Canal at night extended into nearsurface waters, suggesting that the OML was not a barrier to DVM
in September. Some studies have suggested that when an oxygen
gradient is present, fish remain in waters with .4.0 to
4.5 mg l21 DO (Horppila et al., 2000; Eby and Crowder, 2002;
Klumb et al., 2004). In contrast, other studies have found fish
associated with DO levels of 1 –2 mg l21 during DVM and
non-DVM periods (Butler et al., 2001; Bell and Eggleston, 2005;
Cornejo and Koppelmann, 2006). Little is known about the DO
tolerance of Pacific hake, the dominant fish in our midwater
trawls (Parker-Stetter and Horne, 2009). Hamukuaya et al.
(1998) suggested that juvenile Cape hake (Merluccius capensis)
avoided waters with ,0.7 mg l21 DO. Jørgensen et al. (2007)
hypothesized that DO levels of 1.1 –1.3 mg l21 may have decreased
escapement of adult hake from trawls by reducing swimming performance. Results from the present study suggest that adult and
juvenile hake crossed the oxygen gradient, beginning at
2.43 mg l21, at the base of the OML and traversed a 19 m layer
of water with DO as low as 1.74 mg l21. In 2006, when fish
DVM appeared to be constrained, DO levels were 1.48 mg l21 at
the base of the OML and as low as 0.66 mg l21 in the middle of
the OML (Parker-Stetter and Horne, 2009). As we can find no
other explanation for differences in fish distributions at night
between 2006 and 2007, we infer that DO levels within the OML
exceeded Pacific hake tolerances in 2006, but not in 2007.
Separation of zooplankton and fish within acoustic data was
based on catches from non-closing gears. The use of opening –
closing midwater and zooplankton nets could refine identification
of DVM constituents. For zooplankton, an opening–closing net
could identify the dominant species in the upper and lower
edges of the layer and clarify the observed differences in migration
rates and potential responses to the OML. Although results from
this study suggest that vertical ascents were not disrupted by the
OML, more precise identification of migrating fish and zooplankton may reveal that the various fish-age groups or zooplankton life
stages respond differently to it.
Trophic-energy transfer in September 2007 was probably unaffected by the OML. Despite the apparent response of zooplankton
to the OML during DVM, the night survey suggested that fish and
zooplankton overlapped vertically, making predation possible.
Nekton vertical migration and midwater hypoxia
In contrast, fish access to zooplankton prey was almost certainly
limited by the OML in September 2006 (Parker-Stetter and
Horne, 2009). The complex range of potential responses to an
OML, coupled with variation in OML formation and strength,
emphasizes the need to examine potential disruptions of trophic
linkages as a result of low-DO refugia.
Acknowledgements
We thank Dan Hannafious and Sean Hildebrandt (Hood Canal
Salmon Enhancement Group), Greg Bargmann and Debbie
Farrer (Washington Department of Fish and Wildlife), and
David Barbee and Cairistiona Anderson (University of
Washington) for field assistance. Jeff Cordell and Nissa Ferm
(University of Washington) are thanked for assistance with zooplankton samples. We also thank the captains and crews of the
University of Washington RV “Centennial” and the FV
“Memories”. Allan Devol and Wendi Ruef (School of
Oceanography, University of Washington) are thanked for providing ORCA buoy data. Funding was provided by the Hood Canal
Dissolved Oxygen Programme through a Naval Sea Systems
Command contract #N00024-02-D-6602 task 50.
References
Andersen, V., Sardou, J., and Gasser, B. 1997. Macroplankton and
micronekton in the northeast tropical Atlantic: abundance, community composition and vertical distribution in relation to different trophic environments. Deep Sea Research I, 44: 193 – 222.
Babson, A. L., Kawase, M., and MacCready, P. 2006. Seasonal and
interannual variability in the circulation of Puget Sound,
Washington: a box model study. Atmosphere-Ocean, 44: 29 – 45.
Bargmann, G. 2003. Poor water conditions prompt fishing closure in
Hood Canal for all finfish except salmon and trout. Washington
Department of Fish and Wildlife News Release, 12 September 2003.
Bell, G. W., and Eggleston, D. B. 2005. Species-specific avoidance
responses by blue crabs and fish to chronic and episodic hypoxia.
Marine Biology, 146: 761– 770.
Besiktepe, S. 2001. Diel vertical distribution, and herbivory of copepods in the south-western part of the Black Sea. Journal of
Marine Systems, 28: 281– 301.
Bollens, S. M., and Frost, B. W. 1991. Ovigerity, selective predation,
and variable diel vertical migration in Euchaeta elongata
(Copepoda, Calanoida). Oecologia, 87: 155 – 161.
Bollens, S. M., Frost, B. W., and Lin, T. S. 1992. Recruitment, growth,
and diel vertical migration of Euphausia pacifica in a temperate
fjord. Marine Biology, 114: 219 – 228.
Butler, M., Bollens, S. M., Burkhalter, B., Madin, L. P., and Horgan, E.
2001. Mesopelagic fishes of the Arabian Sea: distribution, abundance and diet of Chauliodus pammelas, Chauliodus sloani,
Stomias affinis, and Stomias nebulosus. Deep Sea Research II, 48:
1369– 1383.
Castro, L. R., Troncoso, V. A., and Figueroa, D. R. 2007. Fine-scale vertical distribution of coastal and offshore copepods in the Golfo de
Arauco, central Chile, during the upwelling season. Progress in
Oceanography, 75: 486 –500.
Childress, J. J., and Seibel, B. A. 1998. Life at stable low oxygen levels:
adaptations of animals to ocean oxygen minimum layers. Journal
of Experimental Biology, 201: 1223– 1232.
Cornejo, R., and Koppelmann, R. 2006. Distribution patterns of mesopelagic fishes with special reference to Vinciguerria lucetia Garman
1899 (Phosichthyidae: Pisces) in the Humboldt Current Region off
Peru. Marine Biology, 149: 1519– 1537.
Craig, J. K., and Crowder, L. B. 2005. Hypoxia-induced habitat shifts
and energetic consequences in Atlantic croaker and brown shrimp
on the Gulf of Mexico shelf. Marine Ecology Progress Series, 294:
79 – 94.
1301
Dagg, M. J., Frost, B. W., and Newton, J. 1998. Diel vertical migration
and feeding in adult female Calanus pacificus, Metridia lucens and
Pseudocalanus newmani during a spring bloom in Dabob Bay, a
fjord in Washington USA. Journal of Marine Systems, 15: 503 – 509.
De Robertis, A., Eiane, K., and Rau, G. H. 2001. Eat and run: anoxic
feeding and subsequent aerobic recovery by Orchomene obtusus
in Saanich Inlet, British Columbia, Canada. Marine Ecology
Progress Series, 219: 221 –227.
Dunne, J. P., Devol, A. H., and Emerson, S. 2002. The Oceanic Remote
Chemical/Optical analyzer (ORCA)—an autonomous moored
profiler. Journal of Atmospheric and Oceanic Technology, 19:
1709– 1721.
Eby, L. A., and Crowder, L. B. 2002. Hypoxia-based habitat compression in the Neuse River Estuary: context-dependent shifts in
behavioral avoidance thresholds. Canadian Journal of Fisheries
and Aquatic Sciences, 59: 952– 965.
Friedman, J. H. 1984. A variable span smoother. Technical Report 5,
Laboratory for Computational Statistics, Department of
Statistics, Stanford University, CA.
Fry, F. E. J. 1937. The summer migration of the cisco, Leucichthys
artedi (Le sueur), in Lake Nipissing, Ontario. The University of
Toronto Studies, Biological Series, 44.
Hamukuaya, H., O’Toole, M. J., and Woodhead, P. M. J. 1998.
Observations of severe hypoxia and offshore displacement of
Cape hake over the Namibian shelf in 1994. South African
Journal of Marine Science, 19: 57 – 59.
Hays, G. C. 2003. A review of the adaptive significance and ecosystem
consequences of zooplankton diel vertical migrations.
Hydrobiologia, 503: 163– 170.
Herring, P. J., Fasham, M. J. R., Weeks, A. R., Hemmings, J. C. P., Roe,
H. S. J., Pugh, P. R., Holley, S., et al. 1998. Across-slope relations
between the biological populations, the euphotic zone and the
oxygen minimum layer off the coast of Oman during the southwest
monsoon (August, 1994). Progress in Oceanography, 41: 69– 109.
Heywood, K. J. 1996. Diel vertical migration of zooplankton in the
Northeast Atlantic. Journal of Plankton Research, 18: 163 – 184.
Horppila, J., Malinen, T., Nurminen, L., Tallberg, P., and Vinni, M.
2000. A metalimnetic oxygen minimum indirectly contributing
to the low biomass of cladocerans in Lake Hiidenvesi—a diurnal
study on the refuge effect. Hydrobiologia, 436: 81– 90.
Jørgensen, T., Engås, A., Johnsen, E., Iilende, T., Kainge, P., and
Schneider, P. 2007. Escapement of Cape hakes under the fishing
line of the Namibian demersal sampling trawl. African Journal of
Marine Science, 29: 209 – 221.
Keister, J. E., Houde, E. D., and Breitburg, D. L. 2000. Effects of
bottom-layer hypoxia on abundances and depth distributions of
organisms in Patuxent River, Chesapeake Bay. Marine Ecology
Progress Series, 205: 43 – 59.
Keith, G. J., Ryan, T. E., and Kloser, R. J. 2005. ES60adjust.jar. Java
software utility to remove a systematic error in Simrad ES60
data. CSIRO Marine and Atmospheric Research, Castray
Esplanade, Hobart, Tasmania, Australia.
Klumb, R. A., Bunch, K. L., Mills, E. L., Rudstam, L. G., Brown, G.,
Knauf, C., Burton, R., et al. 2004. Establishment of a metalimnetic
oxygen refuge for zooplankton in a productive Lake Ontario
embayment. Ecological Applications, 14: 113 – 131.
Koppelman, R., and Weikert, H. 2005. Temporal and vertical distribution of two ecologically different calanoid copepods
(Calanoides carinatus Krøyer 1849 and Lucicutia grandis
Giesbrecht 1895) in the deep waters of the central Arabian Sea.
Marine Biology, 147: 1173– 1178.
Liljebladh, B., and Thomasson, M. A. 2001. Krill behaviour as
recorded by acoustic Doppler current profilers in the
Gullmarsfjord. Journal of Marine Systems, 27: 301 – 313.
Loick, N., Ekau, W., and Verheye, H. M. 2005. Water-body preferences
of dominant calanoid copepod species in the Angola-Benguela
frontal zone. African Journal of Marine Science, 27: 597– 608.
1302
Marcus, N. H. 2001. Zooplankton: responses to and consequences of
hypoxia. In The Effects of Hypoxia on Living Resources, with
Emphasis on the Northern Gulf of Mexico, pp. 49– 60. Ed. by
N. N. Rabalais, and R. E. Turner. American Geophysical Union,
Coastal and Estuarine Series, 58.
Mehner, T., Kasprzak, P., and Hölker, F. 2007. Exploring ultimate
hypotheses to predict diel vertical migrations in coregonid fish.
Canadian Journal of Fisheries and Aquatic Sciences, 64: 874 – 886.
Mutlu, E. 2003. Acoustical identification of the concentration layer of
a copepod species, Calanus euxinus. Marine Biology, 142: 517 – 523.
Myriax Pty Ltd. 2008. Echoview. Myriax Software Pty Ltd, Hobart,
Tasmania, Australia.
Newton, J. A., Thomson, A. L., Eisner, L. B., Hannach, G. A., and
Albertson, S. L. 1995. Dissolved oxygen concentrations in Hood
Canal: are conditions different than forty years ago? Puget Sound
Research ‘95 Proceedings, Puget Sound Water Quality Authority,
Olympia, Washington, pp. 1002– 1008.
Parker-Stetter, S. L., and Horne, J. K. 2009. Nekton distribution and
midwater hypoxia: a diel, seasonal prey refuge? Estuarine, Coastal
and Shelf Science, 81: 13 – 18.
Pearcy, W. G., Krygier, E. E., Mesecar, R., and Ramsey, F. 1977. Vertical
distribution and migration of oceanic micronekton off Oregon.
Deep Sea Research, 24: 223 – 245.
S. L. Parker-Stetter et al.
Pollock, M. S., Clarke, L. M. J., and Dube, M. G. 2007. The effects of
hypoxia on fishes: from ecological relevance to physiological
effects. Environmental Reviews, 145: 1 – 14.
Prince, E. D., and Goodyear, C. P. 2006. Hypoxia-based habitat compression of tropical pelagic fishes. Fisheries Oceanography, 15:
451– 464.
Scheuerell, M. D., and Schindler, D. E. 2003. Diel vertical migration by
juvenile sockeye salmon: empirical evidence for the antipredation
window. Ecology, 84: 1713 – 1720.
Stanton, T. K., and Chu, D. 2000. Review and recommendations for
the modelling of acoustic scattering by fluid-like elongated zooplankton: euphausiids and copepods. ICES Journal of Marine
Science, 57: 793– 807.
Traynor, J. J. 1996. Target-strength measurements of walleye pollock
(Theragra chalcogramma) and Pacific whiting (Merluccius productus). ICES Journal of Marine Science, 53: 253– 258.
Wiebe, P. H., Copely, N. J., and Boyd, S. H. 1992. Coarse-scale horizontal patchiness and vertical migration of zooplankton in Gulf
Stream warm-core ring 82-H. Deep Sea Research, 39: S247– S278.
Wishner, K. F., Gowing, M. M., and Gelfman, C. 2000. Living in
suboxia: ecology of an Arabian Sea oxygen minimum copepod.
Limnology and Oceanography, 45: 1576– 1593.
doi:10.1093/icesjms/fsp006