Increasing deoxygenation (loss of oxygen) of the ocean, including
expansion of oxygen minimum zones (OMZs), is a potentially important
consequence of global warming. We examined present-day variability of
vertical distributions of 23 calanoid copepod species in the Eastern
Tropical North Pacific (ETNP) living in locations with different water
column oxygen profiles and OMZ intensity (lowest oxygen concentration and
its vertical extent in a profile). Copepods and hydrographic data were
collected in vertically stratified day and night MOCNESS (Multiple Opening/Closing Net and Environmental Sensing System) tows (0–1000 m)
during four cruises over a decade (2007–2017) that sampled four ETNP
locations: Costa Rica Dome, Tehuantepec Bowl, and two oceanic sites further
north (21–22∘ N) off Mexico. The sites had different
vertical oxygen profiles: some with a shallow mixed layer, abrupt
thermocline, and extensive very low oxygen OMZ core; and others with a more
gradual vertical development of the OMZ (broad mixed layer and upper
oxycline zone) and a less extensive OMZ core where oxygen was not as low.
Calanoid copepod species (including examples from the genera Eucalanus,
Pleuromamma, and Lucicutia) demonstrated different distributional strategies (implying different
physiological characteristics) associated with this variability. We
identified sets of species that (1) changed their vertical distributions and depth of maximum abundance associated with the depth and intensity of the
OMZ and its oxycline inflection points; (2) shifted their depth of diapause;
(3) adjusted their diel vertical migration, especially the nighttime upper
depth; or (4) expanded or contracted their depth range within the mixed
layer and upper part of the thermocline in association with the thickness of
the aerobic epipelagic zone (habitat compression concept). These
distribution depths changed by tens to hundreds of meters depending on the
species, oxygen profile, and phenomenon. For example, at the lower oxycline,
the depth of maximum abundance for Lucicutia hulsemannae shifted from ∼600 to
∼800 m, and the depth of diapause for Eucalanus inermis shifted from
∼500 to ∼775 m, in an expanded OMZ compared
to a thinner OMZ, but remained at similar low oxygen levels in both
situations. These species or life stages are examples of “hypoxiphilic”
taxa. For the migrating copepod Pleuromamma abdominalis, its nighttime depth was shallow
(∼20 m) when the aerobic mixed layer was thin and the low-oxygen OMZ broad, but it was much deeper (∼100 m) when the mixed
layer and higher oxygen extended deeper; daytime depth in both situations
was ∼300 m. Because temperature decreased with depth, these
distributional depth shifts had metabolic implications.
The upper ocean to mesopelagic depth range encompasses a complex interwoven
ecosystem characterized by intricate relationships among its inhabitants and
their environment. It is a critically important zone for oceanic
biogeochemical and export processes and hosts key food web components for
commercial fisheries. Among the zooplankton, there will likely be winners
and losers with increasing ocean deoxygenation as species cope with
environmental change. Changes in individual copepod species abundances,
vertical distributions, and life history strategies may create potential
perturbations to these intricate food webs and processes. Present-day
variability provides a window into future scenarios and potential effects of
deoxygenation.
Introduction
Increasing ocean deoxygenation (loss of oxygen), including expansion of
oxygen minimum zones (OMZs), is a potentially important consequence of
global warming (Breitburg et
al., 2018; Levin, 2018; Stramma et al., 2008). In the future, OMZs (oceanic
depth zones of low oxygen) are predicted to expand in geographic extent and
to have even lower oxygen concentrations in their centers compared to the
present. The zooplankton community from the mixed layer into the mesopelagic
is a key component of oceanic food webs, particle processing, and
biogeochemical cycles (Robinson et al., 2010;
Steinberg and Landry, 2017). From earlier work, some mesopelagic species are
known to be sensitive to environmental oxygen concentration and respond to
that variability by altering their distribution patterns
(Wishner et al., 2018, 2013; Seibel
and Wishner, 2019). If the OMZ expands on a broader scale, distributions and
abundances of many zooplankton species will likely be affected, with
potential consequences for oceanic ecosystems.
We previously noted the presence of zooplankton boundary layers (sharp peaks
of high zooplankton biomass and abundances of certain fish and copepod
indicator species) at the upper and lower edges (oxyclines) of the OMZ core
at two sites (Costa Rica Dome, Tehuantepec Bowl) in the Eastern Tropical
North Pacific (ETNP), as well as how the lower oxycline biomass peak shifted depth
by tracking oxygen concentration (Wishner
et al., 2013). These peaks of zooplankton concentration in the water column
were also locations of active trophic processing
(Williams et al., 2014), life history events
(diapause depths) for some species
(Wishner et al., 2013), and predator
concentrations (Maas et al., 2014).
Here, we examine the variability of vertical distributions of copepod
species living in locations with different water column oxygen profiles and
OMZ intensity (lowest oxygen concentration and its vertical extent in a
profile). We obtained quantitative vertically stratified zooplankton samples
from the surface to 1000 or 1200 m, with simultaneous hydrographic data,
from four cruises from 2007 to 2017 at several sites in the ETNP, an oceanic
region with a strong OMZ (Fiedler
and Talley, 2006; Karstensen et al., 2008; Paulmier and Ruiz-Pino,
2009). The tows sampled four different geographic
locations, each showing a distinctive shape of the vertical oxygen profile
through the OMZ. Some sites had a narrow shallow mixed layer, abrupt
thermocline, and extensive very low oxygen OMZ core, while others had a more
gradual vertical development of the OMZ (broad upper oxycline zone of
diminishing oxygen) and a less extensive OMZ core where the concentration of
oxygen was not as low. On the 2017 cruise, horizontally sequenced transects
and tows at three different depths within the OMZ exhibited considerable
submesoscale physical and biological variability (including kilometer-scale
features of oxygen); zooplankton abundance differences were associated with
oxygen differences of only a few micromolar
(µM; Wishner et al.,
2018). Here, we focus on copepod vertical distributions in order to compare
species-specific responses to large-scale spatial and temporal environmental
variability among the four different OMZ locations.
Many marine taxa, including zooplankton, are physiologically sensitive to
the oxygen partial pressure in their environment (Childress and Seibel,
1998; Seibel, 2011; Seibel et al., 2016; Seibel and Wishner, 2019). One
measure, typically viewed as an index of hypoxia tolerance, is Pcrit,
defined as the lowest experimentally determined partial pressure of oxygen
at which an individual of a species can maintain its oxygen consumption rate
(MO2). Recent work demonstrates that hypoxia does not specifically
select for a lower Pcrit but rather that the ratio of MO2 to
Pcrit is a reflection of the physiological capacity to extract and
transport oxygen, which is dependent on PO2 as well as a species'
activity level (Seibel and Deutsch, 2019). Species living in
extreme hypoxia, such as those in OMZs, have greater oxygen supply capacity
than do species living in air-saturated water. As a result, measured
Pcrit values are generally related to the environmental parameters
(temperature, oxygen, depth) where the species occurs
(Childress, 1975; Seibel, 2011).
Mesopelagic species living in OMZs have the lowest measured Pcrit values among animals (Seibel et
al., 2016; Thuesen et al., 1998; Wishner et al., 2018). For most of these
species, hypoxia tolerance is reduced at higher temperatures (Pcrit values are higher) because respiration increases, but one copepod species
(Lucicutia hulsemannae), living at the OMZ lower oxycline, has a reverse temperature response,
which is adaptive in this habitat where oxygen and temperature are inversely
correlated (Wishner et al., 2018). In situ abundances of some OMZ
species also respond to slight environmental oxygen variations at very low
oxygen concentrations (<10µM) at mesopelagic depths,
corresponding to their experimentally determined physiological tolerances
(Wishner et al., 2018). Here, we document oxygen and
temperature ranges at the depth of maximum abundance in vertical profiles
for a number of copepod species, as an indicator of the most metabolically
suitable habitat for each species at the time and place of collection.
Alterations in zooplankton distributions in response to oxygen may have
wider implications for ecosystem function and ultimately drive potential
societal impacts (e.g., fisheries effects). Present-day comparisons among
locations with different water column oxygen structure can be used as
proxies to illuminate potential future effects of OMZ expansion. We analyzed
zooplankton vertical distributions spatially and temporally, using key
copepod species as examples, to address the following important questions
about OMZ expansion effects:
Do mesopelagic copepod species adjust their depth distribution,
especially the occurrence of boundary layers at oxyclines, in association
with the shape of the vertical profile of oxygen?
Does the depth of diel vertical migration (DVM) for particular species
change in association with OMZ thickness and oxygen concentration, or do the
copepods continue to migrate to the same depth regardless of oxygen?
Can distributional effects of aerobic habitat compression on epipelagic
copepod species be documented? Specifically, do mixed layer species have
different lower depth boundaries depending on the depth and abruptness at
which very low oxygen occurs?
MethodsSampling
Zooplankton samples were collected in day and night vertically stratified
net tows during four cruises to the ETNP (Fig. 1, Table 1). In October–November 2007
on R/V Seward Johnson and December 2008 on R/V Knorr (cruise 19502), sites at the Costa Rica Dome (CRD)
(9∘ N, 90∘ W) and Tehuantepec Bowl (TB) (13∘ N, 105∘ W) were sampled as part of the Eastern Tropical
Pacific (ETP) project. A few years
later as part of the Metabolic Index Project, R/V Oceanus (cruise OC1604B) in April 2016
occupied a station (OC) farther north at 22∘ N, 120∘ W,
and the next year in January–February 2017 R/V Sikuliaq (cruise SKQ201701S) occupied a station
(SKQ) at 21∘ N, 117∘ W. These station abbreviations are
used for graph labels in the figures.
Map showing station locations.
Cruises, stations, tows, and net depth intervals used in copepod
abundance graphs. Several tows were often combined to obtain detailed
vertical profiles to depth (see Sect. 2.1). D: day; N: night; NS: no
sample. Parameters for each tow (dates, times, locations) are in the BCO-DMO
data repository, and Table S1 (Wishner et al., 2019) provides depth and
abundance data for each net (see data availability section for DOI numbers).
At all locations, a series of vertically stratified MOCNESS (Multiple Opening/Closing Net and Environmental Sensing System)
(Wiebe et al., 1985) tows, along with simultaneous
hydrographic data, collected day and night zooplankton samples from depth
(1000 or 1200 m) to the surface (Tables 1 and S1, which is available in Wishner et al., 2019).
Standard tows sampled the entire 0–1000 m depth range in 100 or 200 m
intervals (8 or 9 nets). At most stations, additional fine-scale tows were
taken over various intermediate depth ranges, usually at sampling intervals
of 25, 50, or 150 m. Adaptive sampling targeting particular oxygen values
(physiology and oxycline tows) was also done. At SKQ, 2 sequential
day tows (Tows 718 and 719) and 1 night tow (Tow 720), which targeted the
350–650 m depth zone with eight sampling nets for each tow, opportunistically
encountered different vertical oxygen profiles, and some species
distributions responded to this variability. This tow series is referred to
as the “mid-depth comparison”. Results from horizontally sequenced tows at
specific mesopelagic depths within the OMZ, performed during the R/V Sikuliaq cruise,
were previously published (Wishner et al., 2018).
Zooplankton were sampled on the upcast portion of a tow close to noon or
midnight, and the hydrographic data from the MOCNESS sensors taken
simultaneously with the sampling were used. In a few instances when sensors
failed, hydrographic information for some depths was used from the downcast
portion of the tow or from a nearby conductivity–temperature–depth (CTD) cast. The MOCNESS was towed at a
speed of ∼1.5 kt along an oblique path; vertical speeds
during the deeper sampling upcast were typically 1 to 3 m min-1. Because OMZ zooplankton are sparse, large volumes of water
(typically 600 to >1000 m3) were filtered by each net for
the deeper samples, and those nets were open for ∼20 min
each. The duration of the deeper tows was ∼7 h (most of a day
or night, centered around noon or midnight). Shallower tows were shorter in
duration, and smaller volumes were filtered for the mixed layer and upper
water samples. Details of tows (time and location), depth intervals, and
volume filtered for each net are in Table S1 (Wishner et al., 2019) and the
BCO-DMO data repository (see the data availability section).
By combining data from multiple tows for a given location to construct a
full depth series, we were able to resolve fine-scale vertical distributions
within the OMZ and at its upper and lower boundaries. The process for
assembling vertical profiles from multiple tows was described in
Wishner et al. (2013) for the 2007 and
2008 cruises; a similar process was used for the other cruises although
depth strata varied (Table 1).
MOCNESS instrument
Two versions of the 1 m2 MOCNESS were used. The R/V Seward Johnson and R/V Knorr cruises used the
University of Miami's classic MOCNESS with the standard MOCNESS deck unit,
software, and sensors, with the oxygen sensor incorporated into the options
unit. The R/V Oceanus and R/V Sikuliaq cruises used the upgraded Scripps Institution of
Oceanography's MOCNESS in which a Sea-Bird 911CTD with hydrographic sensors
and software was physically attached to the MOCNESS frame and its software
integrated with the MOCNESS system (Wishner et al., 2018); the
bottle-closing CTD feature was transformed into a net bar release
controller. The basic net frame and nets, net bar release mechanism, and
flow meter were the same in both systems. The recent upgrades provided more
stable hydrographic sensor data and facilitated real-time adaptive sampling
with an improved shipboard data and graphical user interface. In the two
earlier cruises, the net mesh size was 153 µm; in the two later
cruises it was 222 µm. Sensors included pressure (depth),
temperature, salinity, in situ fluorescence, light transmission, PAR (later
cruises), and a TSK flow meter (for volume filtered). The oxygen sensor for
all cruises was a Sea-Bird SBE43, calibrated in advance of the cruises.
Sample processing, copepod sorting, and abundance data
At sea, cod ends upon retrieval were placed in buckets with plastic ice
packs to maintain cool temperature in the tropical heat. Fresh samples were
rinsed with filtered seawater into large 153 µm mesh metal sieves and
photographed. Most samples from the earlier cruises were then split in a
flat-bottomed Motoda splitter. Typically, a half split was preserved in
4 % sodium-borate-buffered formaldehyde in seawater solution for later
species identification, while other splits were used for experimental
studies, at-sea size-fractionated biomass measurements (first two cruises),
photography, and stable isotope analyses. Samples from the later cruises
were usually preserved whole without splitting, except for a few individuals
that were set aside for live experiments (and recorded at that time).
Onshore processing, including copepod sorting and identification, varied
among the cruises because of time and funding constraints. Onshore sorting
of copepods occurred months to years after a cruise. The 2007 CRD tows, most
of the 2016 OC tows, and most of the 2017 SKQ tows were sorted to
substantial species-level and life stage detail, while others (especially
some 2007 and 2008 TB tows) were sorted for only a few selected species. For
the 2016 and 2017 cruises, only larger copepods were counted after the
sample was poured through a 2 mm sieve in the lab, while copepods of all
sizes were counted in the 2007 CRD samples (targeting major groups). Splits
of the whole sample were used in most cases, with a target sample size of
100 calanoid copepods. In some instances for SKQ horizontal tows, Stempel
pipette aliquots of the small or large size fractions were checked and
quantified for particular taxa. About 22 000 identified copepods are
included in this paper's dataset.
Certain copepod species were consistently identified and visually searched
for in most tows, with a focus on the genera Lucicutia and Pleuromamma and the family
Eucalanidae. Many other copepod species were identified when present, except
for deeper TB samples (below 200 m) for which only targeted species were
quantified. Some species, especially ones that were rarer, smaller,
immature, or difficult to identify, were not always separated and were often
lumped into broader categories such as genus, family, or miscellaneous
calanoid. Because adult morphological features are typically needed for
species confirmation, identification targeted adult calanoid copepods. For
some species in which particular younger stages were abundant, easily
recognizable, and essential for ecological understanding, those stages were
counted separately. This was especially important for the copepod Eucalanus inermis, which had
an obvious diapausing layer sometimes associated with OMZ oxyclines.
Copepods were identified by an experienced technician (Dawn Outram) based on
the literature and websites, especially Razouls et al. (2005), website http://copepodes.obs-banyuls.fr/en (last access: 15 December 2019). Identifications of
individuals were done by hand with Nikon and Wild stereomicroscope and compound
microscopes, enabling more detailed species and life stage delineation than
possible with bulk sample electronic scanning. An upgraded microscope with
greater acuity was used for the 2016 and 2017 sample processing, allowing
greater species resolution. Other sample components – including
size-fractionated biomass; zooplankton stable isotope and body composition;
and abundances of other taxa including euphausiids, fish larvae,
cephalopods, and foraminifera – are reported elsewhere or are currently under
analysis (Birk
et al., 2019; Cass et al., 2014; Cass and Daly, 2014, 2015; Maas et al.,
2014; Williams et al., 2014; Wishner et al., 2018, 2013).
During the first two cruises, all individuals of the copepod E. inermis were scanned
by microscope for the presence of stored oil, an indicator of diapause. They
were categorized as containing oil (orange in color in these preserved
specimens), clear (no oil), or brownish (no oil but brown in color). A total
of 9998 specimens from all nets and tows, separated by life stage from
copepodite 3 to adult females and males, were examined. Only a subset of
these data is discussed in this paper.
Abundances within each net, usually reported as number of individuals per (1000 m)3, were calculated after accounting for split size and volume
filtered (Table S1, Wishner et al., 2019). Abundances in vertical
distribution graphs are plotted at the mid-depth of the sampling interval.
Water column abundance (reported as number of individuals m-2 for a
selected depth range, usually 0–1000 m) was calculated by multiplying each
sample abundance by the depth range of that sample and then summing those
values for the complete sample series over the total selected depth range.
Species selection for this paper and depth of maximum abundance
To clarify critical issues about OMZ effects on zooplankton, we selected a
subset of 23 species from the extensive full species list (over 300 species)
in order to highlight specific responses to OMZ variability (Table 2). We
chose these species based on their abundance and frequency of occurrence
(presence–absence) in the different locations and cruises and their
usefulness as examples to illustrate different types of distributional
responses to variability in the shape (and lowest oxygen concentration) of
the oxygen profile. In a set of graphs, we show day and night vertical
distributions of particular species relative to the oxygen profile from each
sampling location and time (when that species was present).
The depth of maximum abundance (DMA) was defined as the single net and its
depth interval with the highest abundance for a particular species day and
night at each station during each cruise, with all tows considered (Table 3). The MOCNESS sensor data during the time of collection (upcast) were used
to delineate the habitat parameters (oxygen and temperature ranges) at the
DMA (Table 3); these are from the particular tow and net listed (DMA tow and
net ID in Table 4). Most species also occurred (at lower abundance) over a
broader vertical range beyond the single DMA net, as evident in the figures
and Table S1 (Wishner et al., 2019). Some species exhibited bimodal
distributions. It should be noted that because each net in a MOCNESS tow
encompassed a range of depths and consequently a range of hydrographic
values, it is unknown where within that range the collected animals were
actually located. However, our fine-scale sampling in many cases encompassed
very narrow environmental intervals such that we could constrain the OMZ
habitat preferences and tolerances (oxygen and temperature ranges) for many
species.
Depth of maximum abundance (DMA) for the species (adults) discussed
in the text along with environmental data from MOCNESS sensors for that
habitat (depth, oxygen, and temperature for the DMA net). Species names
(first row in the top and bottom halves of the table) are shortened (full
names in Table 2) and are listed in the same order as in Table 2. Data are
listed under each parameter by cruise (see Table 1 for cruise abbreviations)
and for both day (D) and night (N) when available. Nighttime data for the TB
cruises are not shown since only a few species were identified from those
tows. “×” indicates situations where the species was not recorded, either
because it was not present or not identified. “None” indicates situations
where the species was searched for but not found, i.e., abundance of 0 and
consequently no associated environmental data. NA for oxygen means not
available (oxygen sensor malfunction). Ranges for depth (DMA, m), oxygen
(DMA Ox, µM), and temperature (DMA Temp, ∘C) are shown for
the DMA net. Ranges, rather than means, are given, because each net covered
a depth (and habitat) interval, and it is not known where within that
interval the animals occurred.
Species abundances in the DMA net (maximum abundance for that cruise)
(adults, number (1000 m)-3) and also water column abundances (adults, number m-2 for the 0–1000 m depth interval except 0–750 m for CRD07 day) for each species on each cruise. Species names (first row
in the top and bottom halves of the table) are shortened (full names in
Table 2) and are listed in the same order as in Table 2. Data are listed
under each parameter by cruise (see Table 1 for cruise abbreviations) and
for both day (D) and night (N) when available. Nighttime data for the TB
cruises are not shown since only a few species were identified from those
tows. “×” indicates situations where the species was not recorded, either
because it was not present or not identified. “None” indicates situations
where the species was searched for but not found, i.e., abundance of 0 and
consequently no DMA net. The DMA net ID provides easy access to pertinent
data in Table S1 (Wishner et al., 2019). For the net ID, the first three
digits are the tow number, and the fourth digit is the net number in that
tow.
Hydrographic profiles from MOCNESS sensors are shown in Fig. 2 for each
location for both the full sampling range (0–1000 m) and the upper water
column (0–200 m). We selected one oxygen profile from each site and year to
represent that location in the vertical abundance graphs, although abundance
profiles were derived from combining multiple day and night tows (see Sect. 2.1 and 2.3). In a few cases, we discuss small-scale distributional
variability between sequential tows at the same location, especially the
mid-depth comparison series at SKQ. Figure S1 in the Supplement shows all
MOCNESS oxygen profiles at each station to provide a sense of oxygen
variability among tows at the same location.
Hydrographic data. Top row: hydrographic profiles for 0–1000 m
(noted as “All depths”). Each station (colors) is represented by one
profile for each variable; all stations are included for that variable in
one graph. Stations are noted by abbreviation and year. Two versions of the
oxygen profiles are shown: a full range version (0–250 µM) to
encompass oxygen from the surface to depth (top left) and a higher-resolution version with a smaller oxygen range (0–60 µM) to highlight
the OMZ core and oxycline variability between stations (top row, second from
left). Second row: similar profiles for the upper water column (noted as
“Upper 200 m” and with its depth range indicated by the bracket on the
“All depths” plot). Only a single oxygen range is used for this
well-oxygenated part of the water column. Bottom row: Temperature–salinity
diagram (bottom left) and two temperature–oxygen diagrams, with the first (bottom
middle) encompassing the full range of these variables and the second
(bottom right) highlighting the smaller temperature and oxygen ranges and
variability associated with the OMZ core and oxyclines at the different
stations (data range shown by the outlined box in the “All depths” oxygen
and temperature plots).
The OMZ water column consists of several ecological zones, previously
described, each of which has a characteristic hydrographic structure and
forms the habitat for a suite of organisms and processes (Wishner et
al., 2008, 2013). Zonal boundaries depend on both the shape of the oxygen
profile and oxygen concentration, and boundary depths vary by profile. We
describe these zones briefly below to introduce terminology and provide a
framework for analysis. The mixed layer is the water column above the
thermocline with high oxygen and temperature. The upper oxycline (UO), which
begins just below the thermocline, has decreasing oxygen with depth and may
be abrupt or broad. The OMZ core has the lowest oxygen values stable over a
depth range; at these locations OMZ core oxygen was often <∼ 1–2 µM but was always detectable. The lower oxycline
(LO) starts at the inflection point at the base of the OMZ core where oxygen
begins to increase with depth. The LO is often characterized by a sharp
subsurface peak in zooplankton biomass and abundance and the presence of
specific indicator taxa. Oxygen would continue to increase below our
sampling range.
The lowest oxygen values in the OMZ core during these cruises occurred at
CRD and TB (values down to 1.0 µM). The mixed layer was very thin at
both CRD and TB, with the start of the thermocline at 16–34 m in different
tows and with temperature and oxygen decreasing rapidly below. However, TB
in 2007 had a subsurface oxygen intrusion in the upper oxycline zone, so the
OMZ core did not begin until about 350 m and extended to 550 m, similar to
the OMZ core extent at CRD that same year. TB in 2008 had the most
vertically extensive OMZ core (oxygen values of 1.1–1.5 µM) extending
from depths of 80–700 m, with an abrupt thermocline and almost nonexistent
upper oxycline. It was also notable for the occurrence of double subsurface
fluorescence peaks, one near the shallow thermocline (∼40 m)
as expected and also a deeper peak at ∼120 m within the low-oxygen water of the OMZ core.
The mixed layer extended deeper at the northern stations, OC and SKQ.
Fluorescence peaks near the thermocline were deeper (∼ 80–100 m) at OC and SKQ, compared to the thermocline-associated peak
(∼50 m) at CRD. At OC and SKQ, the oxygen profile was more
rounded in shape without a clear-cut extensive OMZ core. The upper oxycline
was broad, with relatively high oxygen concentration down to ∼450 m. The OMZ core was narrow (only ∼25 m thick,
∼ 525–550 m at OC and at more variable depths between 400 and 600 m in different tows at SKQ). Oxygen values in the core at OC reached only as
low as 3.6 µM, substantially higher oxygen than at CRD or TB. SKQ had
some low oxygen values of 1.0 µM for parts of particular net
intervals, especially in the mesopelagic horizontal tows during transects
through submesoscale features (Wishner et al., 2018).
Temperature decreased with depth below the thermocline and was similar
through the mesopelagic at all these stations (Fig. 2). Mixed layer salinity
was comparatively low except at the OC and SKQ stations, which were farther
north than those of the earlier cruises, and where there was a subsurface
salinity minimum (∼ 80–250 m), likely an influence of the
southern extent of the California Current.
Temperature–salinity and temperature–oxygen graphs illustrate the different
water masses and metabolic habitats encountered (Fig. 2, bottom row). The
high-resolution temperature–oxygen graph (bottom right) highlights the small-scale habitat variability of the OMZ and oxyclines (see also
Wishner et al., 2018). In different locations, animals at the
same mesopelagic depth (i.e., same temperature) could experience quite
different oxygen regimes; animals tracking a specific oxygen concentration
might live at different depths (and temperatures).
Copepod distributions and responses to oxygen profile variability
Copepod distributions are presented in a series of graphs and tables
described below. Environmental data (ranges for depth, oxygen, and
temperature) in the DMA net are shown in Table 3. Abundances (number (1000 m)-3) in the single net at the depth of maximum abundance (DMA) for each species day and night, along with day and night water column abundances
(number m-2 usually for the 0–1000 m depth interval) for that species
on that cruise, are in Table 4. Abundances of each species in all tows and
nets are in Table S1 (Wishner et al., 2019).
OMZ oxycline and OMZ core species that shift depth and track oxygen
These were primarily mesopelagic species, most with no diel vertical
migration, whose peak abundance was associated with the inflection point at
the upper edge (UO) or lower edge (LO) of the OMZ core. These species showed
distributional shifts associated with the changing depth of the inflection
points and the OMZ core on the different cruises (details below). Peak
abundances often occurred abruptly in a very narrow depth interval (a single
or only a few sampling nets) and could be several orders of magnitude higher
than in adjacent nets.
Lucicutia hulsemannae. This copepod (Markhaseva and Ferrari, 2005), formerly called
L. grandis, is considered to be an indicator species of the LO (Wishner
et al., 2000, 2013). Its peak abundance (Table 4) occurred at the LO
inflection point at the base of the OMZ core in the tows with lowest oxygen
and most extensive OMZ (Fig. 3, Table 3). Its maximum abundance in a single
net (997 individuals (1000 m)-3) (Table 4) occurred at 600–625 m at CRD
in 2007, with oxygen in that interval at 1.7–5.9 µM and temperature
at 6.3–6.5 ∘C (Table 3). It was also very abundant at TB in 2008
(maximum of 781 individuals (1000 m)-3) (Table 4), but in this case
that peak occurred deeper (800–825 m) and thus at lower temperature
(5.5–5.6 ∘C), just below the extensive OMZ core of lowest oxygen
(Table 3). This net sampled a more constrained oxygen range (1.8–2.4 µM) confirming that this species can thrive in extremely low oxygen water (Wishner et al., 2018). At OC and SKQ, where oxygen was not as
low and where the oxygen profile was more rounded without a clear-cut OMZ
core, L. hulsemannae was distributed more broadly throughout the overall OMZ and both
oxyclines (Fig. 3), and its water column abundance (7–16 m-2 from
0–1000 m) was usually lower (Table 4). Maximum abundances (65–92 individuals (1000 m)-3) (Table 4) were also substantially less (with one exception)
and occurred shallower (450–550 m at OC; 500–600 or 600–650 m at SKQ) at
these northern stations, although temperature at depth was similar to CRD
(Table 3). During SKQ in horizontally sequenced tows reported elsewhere,
this species also had strong physiological and distributional responses to
very small (several µM) oxygen differences and had higher abundances
in lower oxygen (Wishner et al., 2018). In the SKQ mid-depth
comparison series, the highest abundances were usually associated with the tow
and nets with lower oxygen (Fig. 4). Younger stages, from copepodite 2 to 5,
were recorded, and often abundant, in many of the same nets and depths as
the adults. No adults or young stages were found in shallow samples. L. hulsemannae thus
appears to be actively growing and developing within this extremely hypoxic
part of the OMZ.
Vertical distributions relative to oxygen: lower oxycline species.
Vertical distributions day (red) and night (dark blue) relative to the
oxygen profile (light blue) at each station from 0 to 1000 m. Stations are
noted at the top (station abbreviation and year), and each column comes from
the indicated station. Each row is a different species. Missing boxes are
locations and cruises where the species was not recorded. “No data”
indicates that the species was either not present or not identified to
species in those samples. “Absent” indicates that the species was searched
for but not found (abundance = 0). Abundances (number (1000 m)-3) are
for adults (combined females and males) and come from nets and tows listed
in Table 1. Abundances are plotted at the mid-depth of the sampling
interval. Horizontal abundance axes vary to highlight the peaks. Table S1
(Wishner et al., 2019) provides numerical abundance data for each net.
Vertical distributions of three species relative to oxygen for the three
sequential tows (2 days, 1 night) in the mid-depth comparison series at
SKQ 17. Oxygen profiles from each tow (color coded by tow; see legend) are
shown in the left graph. Species distributions from each tow are color coded
to match the oxygen profile. The depth range for these profiles is 350–650 m. These species responded to the slight variations in oxygen between tows.
A congeneric species, Lucicutia ovalis, occurred in the deeper LO several hundred meters
below L. hulsemannae and consequently at lower temperature and higher oxygen levels (Table 3, not graphed). It also shifted depth between locations and was deeper at
CRD (1100–1200 m) and TB (900–1000 m) (stations with a thick OMZ) than at OC
(700–750 m). It was less abundant than L. hulsemannae and was not found on the SKQ cruise
(perhaps due in part to its small size and likely absence from the large
size fraction that was sorted).
Disseta palumbii. This widely distributed species in the family Heterorhabdidae (Razouls et al., 2005–2019) was also typical of the LO, but
its abundance peaked about 50–100 m deeper than L. hulsemannae (Fig. 3). Consequently, the
oxygen at its DMA was slightly higher and the temperature lower than for L. hulsemannae (Table 3). Its water column abundance and maximum abundance were highest at the
stations where OMZ oxygen was higher, and it was more abundant at OC and SKQ
than in earlier cruises (Fig. 3, Table 4). Younger stages (copepodites 4 and
5) were present in some cruises at similar depths to adults and were
sometimes more abundant than adults.
Another Heterorhabdidae species complex, Heterostylites longicornis/longioperculis, was very abundant from the UO
through the OM to the LO and was another characteristic species of this
habitat (Fig. 3). It was likely a mixture of two species that are difficult
to separate microscopically (Razouls et al., 2005–2019), so
it was treated as one entity. In contrast to D. palumbii, abundances were highest in the
earlier cruises at CRD and TB08 (Table 4), where it co-occurred with L. hulsemannae at the
LO in very low oxygen. At OC and SKQ where it was less abundant, it occurred
primarily in the UO and shallower than L. hulsemannae and D. palumbii. Oxygen values in its habitat at
SKQ were similar to the low values of earlier cruises, but in OC its
shallower peaks (100–250 m) were at higher oxygen (Table 3). Younger stages
occurred at many of the same depths.
Two Aetideidae species, Gaetanus kruppi and Gaetanus pseudolatifrons, and two Augaptilidae species, Euaugaptilus magnus and
Euaugaptilus nodifrons, also demonstrated distributional separation between congeners within the
LO zone (Fig. 5). G. kruppi occurred shallower than G. pseudolatifrons and usually at lower oxygen and
higher temperature (Table 3) because it was closer to the LO inflection
point. Both were most abundant at CRD. E. magnus was clearly a LO species, while E. nodifrons had
a distribution pattern split between the UO and LO. These latter two species
were identified only from the later cruises.
Vertical distributions relative to oxygen: congeneric species from
three genera. Each row shows two species (adults) from a particular genus at the
same stations (listed at the top and repeated for each half of the figure).
Each row is a different genus. See Fig. 3 caption for more explanation.
Several other species, including Metridia brevicauda, Metridia princeps, and Paraeuchaeta californica, also showed a split distribution
pattern with peaks of adults usually at both the UO and LO sides of the OMZ
core but almost no specimens in the OMZ core itself or in shallow water
(Figs. 6, 7). The predominant peak for M. brevicauda adults (Fig. 6) was typically in the
UO, while the predominant peak for P. californica, M. princeps, and E. nodifrons could be either in the LO or UO
(Fig. 7). P. californica and E. nodifrons in the LO occurred deeper and at higher oxygen than the LO
secondary peak of M. brevicauda. The LO peak (at 675–700 m) for M. princeps was especially clear-cut
at CRD (Table 3) since this species was not present shallower there;
however, its highest total water column abundance was at SKQ (Table 4) where
it occurred over a broader depth range at both the UO and LO.
Vertical distributions relative to oxygen for Metridia brevicauda (adults) at each
station (top row). Second and third rows: life history stage distributions
(color-coded bar graphs) are shown for CRD in 2007 night and day (to 750 m,
the deepest depth with both night and day abundance data) and for TB in 2008
for the upper water column (0–200 m, the only depth range with life history
stage counts for that cruise) night and day. Abundance axes vary. Bars are
plotted by sample order with increasing depth. See the vertical profiles
(top row) and Tables 1 and S1 (Wishner et al., 2019) for depth ranges for each net and Table 3 for
the DMA. See Fig. 3 caption for more explanation of the vertical profiles.
Vertical distributions relative to oxygen: upper oxycline species
and those with split oxycline distributions. Two species are shown in each
row with stations repeated for each half. See Fig. 3 caption for more
explanation.
Oxygen where M. brevicauda was most abundant was 1.0–5.7 µM with a temperature of
10.0–10.8 ∘C (Table 3) in the UO of CRD in 2007 (300–350 m,
maximum adult abundance (Table 4) in this net of 15 958 (1000 m)-3),
indicating the ability of this species to thrive at very low oxygen (similar
to L. hulsemannae) but at somewhat higher temperature. Younger smaller life history stages
of M. brevicauda were quantified in the CRD and TB08 cruises (counted only from 0 to 200 m and
from 550 to 1000 m in TB08) (Fig. 6), but not in later cruises, when only the large
copepod size fraction (>2 mm) was sorted (and small taxa like
M. brevicauda may have been underrepresented). Younger stages (copepodites 2–5)
occurred at similar depths as adults, while the youngest stage (copepodite
1) was very abundant (up to 23 589 (1000 m)-3 at night) in TB08,
primarily in the lower mixed layer (50–100 m). This life history
distribution pattern suggested active reproduction at depth, with
ontogenetic migration of the youngest stages up into the well-oxygenated
warmer mixed layer at some times.
The Scolecitrichidae copepods Lophothrix frontalis and Scaphocalanus magnus were common UO components during the OC
and SKQ cruises (not differentiated during earlier cruises), with possible
DVM within the UO (Fig. 7). Peak daytime abundance of L. frontalis was located at
425–468 m (oxygen 4.6–7.4 µM), while at night it was at 100–150 or
200–250 m where oxygen was much higher (Table 3). S. magnus occurred somewhat deeper
(extending from the UO into the OMZ core) and its possible DVM was deeper.
Both species also had higher abundances in the higher-oxygen profile of the
SKQ mid-depth comparison series (Fig. 4).
Eucalanus inermis, a copepod that diapauses in the OMZ
The Eucalanidae copepod E. inermis was especially abundant at CRD and TB where it
formed concentrated diapausing layers at the UO and LO inflection points
(Fig. 8). These were considered diapausing layers because of their life stage
composition and the presence of stored oil in many individuals. Stored oil,
an indicator of diapause, was visibly apparent as an orange colored material
inside many preserved copepods during the first two cruises. Individuals
from the diapausing layer that had no obvious stored oil were either
brownish or clear in preserved samples. From the total of 9998 E. inermis individuals
examined microscopically for oil (all tows and nets on these two cruises),
there were 334 adult females from the four DMA nets listed in Table 4 (plus
two additional DMA nets, ID numbers 6371 and 6368, from tows at CRD in 2008
not included in Table 4). From 67 % to 93 % of adult female E. inermis in the
diapausing layers (DMA nets) during these six tows contained stored oil (total
of 269 individuals), as did high proportions of the older immature males
(copepodites 4 and 5) also present there. Oil presence was not quantified on
the later cruises, but actively swimming specimens from near-surface samples
examined live at sea were transparent, with some, but not all, having some
transparent stored oil.
Vertical distributions relative to oxygen for Eucalanus inermis adults day and
night at each station (top row), and daytime life history stage
distributions (color-coded bar graphs) at each of these stations (two bottom
rows). Abundance axes vary. Bars are plotted by sample order with increasing
depth. At CRD in 2007, daytime data extended only to 750 m. See the vertical
profiles (top row) and Tables 1 and S1 (Wishner et al., 2019) for depth ranges for each net and
Table 3 for the DMA. See Fig. 3 caption for more explanation of the vertical
profiles.
Multiple layers (near surface, UO, LO) with different life stage composition
and relative abundances occurred at both locations during the first two
cruises (Fig. 8). Adult diapausing copepods were primarily females, but
large concentrations of copepodite 4 and 5 males and a few adult males, as
well as some younger stages, occurred in these same samples. Locations of
the diapausing animals were the UO and LO layers, while young stages, as
well as some presumably nondiapausing adults, occurred near the surface. The peak abundance of diapausing adults (33 912 (1000 m)-3) (Table 4) was
located in a layer at 300–350 m (UO) during CRD in 2007 (Table 3), while at
CRD in 2008 the peak abundance (19 242 (1000 m)-3) (Table 4) was at
the LO at 500–550 m (Table 3). At TB in 2007 the peak adult abundance occurred
at the UO (20–80 m), whereas the next year at TB the maximum adult
abundance was at the LO at 775–800 m (Table 3). At the LO, when the
diapausing layer was fortuitously sampled as an entity in a single net, it
occurred as a monospecific aggregation located just above the more diverse
LO community (e.g., L. hulsemannae and associates), as noted earlier
(Wishner et al., 2013). During 2008 at TB,
there was also a very high concentration of copepodite 1 and 2 stages (total
of 211 894 (1000 m)-3) at 60–80 m at the UO, indicating that
reproduction and development had occurred recently (Fig. 8). Similar
near-surface layers of mixed life stages, including many immature specimens,
were also found at CRD in both years. During the last two cruises,
abundances at those more northerly stations were substantially lower (but
still included immature life history stages) and were not as sharply
layered, occurring within the broad UO (400–550 m). There was no
concentrated layer of diapausing animals on these later cruises. No DVM was
evident for any cruise.
E inermis diapausing layers (Table 4) were located at extremely low oxygen, 1.0–5.7 µM (except for the shallow layer at TB in 2008 where the net probably
sampled across zones) (Table 3). These layers were at the edges of the OMZ
core but usually not at the lowest oxygen of the OMZ. The large percentage
of animals with stored oil in these layers and the sharpness of layer
boundaries were strong indicators that this species undergoes its diapause
in a precisely defined zone of extremely low oxygen. Our sampling did not
address seasonal cycles at particular locations, so we do not know the
temporal progression of reproduction and development or how long diapause
layers persisted at depth in low oxygen. The brownish or clear specimens may
have been animals that had depleted their oil reserves.
Other common copepod species from the family Eucalanidae observed during the
cruises did not have the obvious diapause behavior of E. inermis. Eucalanus californicus and Eucalanus spinifer were
moderately abundant farther north during the latter two cruises (not found
at CRD and not separately identified at TB) (Fig. 5); they are common in the
California Current and subtropics respectively (Goetze, 2003; Goetze and
Ohman, 2010). They occurred primarily within the broad UO, with E. californicus being
slightly deeper and also having many copepodite stages 4 and 5. These
species occurred at somewhat higher oxygen than the E. inermis diapausing animals
(Table 3).
Diel vertical migrators and OMZ intensity
Copepod species in the genus Pleuromamma (family Metridinidae) are well known as strong
diel vertical migrators, including species that descend to mesopelagic
depths during the day in the ETNP (Haury, 1988; Hirai
et al., 2015; Razouls et al., 2005). Three of these species provided
insight into varying strategies in response to differences in OMZ and mixed
layer vertical extent and differences in oxygen values among cruises (Fig. 9). We expected that their daytime depth would be most affected by OMZ
variability as they coped with different conditions during their diel
transit. However, for Pleuromamma abdominalis and Pleuromamma quadrungulata, it was the nighttime depth that changed with
the shape of the oxygen profile, while the daytime depth remained similar
across cruises for each species (Table 3). For example, for P. abdominalis, its nighttime
depth was 20–30 m at CRD in 2007 in the high-oxygen mixed layer above the
sharp thermocline and low oxygen below but 100–150 m at OC in 2016 and
50–75 m at SKQ in 2017 where the mixed layer was broader and higher oxygen
extended deeper. Daytime depth was 250–350 m at all these stations in the UO
just above the OMZ core.
Vertical distributions relative to oxygen: diel vertical
migrators. Each row is a different species. For the Pleuromamma species, which were
searched for and identified in all tows, missing figures represent locations
with zero abundances.
Pleuromamma johnsoni (Ferrari and Saltzman, 1998) tended to occur deeper during
the day than the other species (400–450 m at CRD in 2007 and SKQ in 2017)
and had some day and night layers associated with the LO below the OMZ core
(Fig. 9). At TB in 2008, with its vertically extensive OMZ, abundant daytime
layers of P. johnsoni occurred at both 250–300 m in the OMZ core (oxygen 1.2–1.4 µM, temperature 10.8–11.3 ∘C) (Table 3) and 850–875 m at
the LO inflection point (oxygen 2.5–4.3 µM, temperature
5.2–5.4 ∘C). There was also an especially abundant nighttime layer
of P. johnsoni (20 059 individuals (1000 m)-3) at the thermocline (Fig. 9), where
oxygen and temperature were higher (50–60 m, oxygen 21.8–82.6 µM,
temperature 19.7–24.2 ∘C).
There were also clear-cut geographic differences in presence–absence and
abundance among these species (Fig. 9, Table 4), with P. abdominalis most abundant at CRD
in 2007 and P. quadrungulata most abundant at OC in 2016 and SKQ in 2017 but absent at CRD
in 2007. P. johnsoni was most abundant at TB but absent at OC in 2016, whereas the
other two Pleuromamma species were absent at TB in both years (except for one juvenile
specimen of P. abdominalis). Pleuromamma species were specifically targeted for identification at all
stations and nets, so these presence–absence comparisons are strongly
supported. Whether these patterns resulted from distinct environmental
preferences associated with habitat availability (oxygen and temperature
combinations) or from other temporal and spatial changes or ecological
factors cannot be resolved with our sampling.
Epipelagic habitat compression and mixed layer species responses
Four abundant species that occurred primarily in the warm well-oxygenated
mixed layer or near the thermocline were used to examine the aerobic habitat
compression hypothesis by comparing copepod abundances from cruises with
substantial difference in the shape of oxygen profiles. The first two
cruises had a narrower aerobic mixed layer habitat with an abrupt transition
to the OMZ core, while the last two cruises had a broader aerobic mixed
layer and more gradual UO. There were several complications associated with
choosing representative epipelagic taxa. Many upper water column tropical
copepods were small or hard to identify (i.e., Clausocalanus spp.) or occurred primarily as
immature stages; these were not a focus of this OMZ project, and many were
not identified to species. During some cruises, the mixed layer was sampled
only as a single net interval and not subdivided into multiple strata, so
small-scale distributional differences there were not defined. Also, these
four species, generally smaller in size than the deeper living copepods
discussed earlier, may have been relatively undersampled during the later
cruises when a slightly larger mesh size was used and only the >2 mm size fraction sorted; however, this should not affect within-cruise
distributional patterns.
The Eucalanidae copepod Subeucalanus subtenuis, the Paracalanidae copepod Mecynocera clausi, and the Lucicutiidae
copepod Lucicutia flavicornis were most abundant shallower in the thermocline at the first two
stations (20–30 m at CRD in 2007, 40–60 m at TB in 2008) but occurred
deeper and in lower abundance within the broader mixed layer (usually 75–100 m) on the later cruises (Fig. 10). Maximum abundances (Table 4) reached
33 647 (1000 m)-3 (S. subtenuis during CRD in 2007, 20–30 m, Table 3). There was
no clear signal of DVM for these species, although our sampling cannot rule
out small-scale shifts within the mixed layer. For these abundant epipelagic
copepods, the vertical range contraction observed in distributions in the
two earlier cruises compared to the later ones was likely a response to
habitat compression of the aerobic mixed layer.
Vertical distributions relative to oxygen: epipelagic species.
Each row is a different species. The depth axis for these graphs is 0–200 m.
The uppermost point in the graphs includes the sampling interval that
extends to the sea surface (plotted at the mid-depth of the interval). See
Fig. 3 caption for more explanation.
Another abundant copepod, the Heterorhabdidae Haloptilus longicornis, occurred at the base of the
mixed layer in the first two cruises (100–150 m at CRD in 2007 and 60–80 m
at TB in 2008 during the day) but substantially deeper within the UO
(200–300 m during the day) in the latter two cruises (Fig. 9). Because of
the different shapes of the oxygen profiles, oxygen at these very different
daytime depths was similar and moderate (13.1–61.2 µM), except at TB
in 2008, which had lower oxygen. However, temperature was about 3 ∘C lower at the deeper daytime depths in the latter cruises compared to the
shallower earlier ones (Table 3). Additionally, H. longicornis exhibited a short DVM up to
75–100 m at night at two of the stations.
DiscussionOverview
The unique feature of our work is the effort to document precise habitat
conditions pertinent to metabolic requirements (oxygen and temperature) at
depths where particular species are most abundant, as well as how the shapes of
their vertical abundance profiles are modified in concert with the changing
vertical profiles of oxygen in these extreme OMZ habitats.
Although the ETNP copepod fauna and, in some cases, distributional
relationships to oxygen have been studied previously in numerous locations
and programs (Fernández-Álamo and Färber-Lorda,
2006), the sampling schemes, technology, and scientific foci differed from
ours. Chen (1986) analyzed vertical distributions for both
individual copepod taxa and large multispecies samples, collected with
opening–closing bongo nets, at stations along a transect from Baja
California to the Equator during the Krill Expedition. Copepod vertical
distributions in the Costa Rica Dome, long known as a productive feature
important to fisheries (Fiedler,
2002; Landry et al., 2016), have been reported (Décima
et al., 2016; Fiedler, 2002; Jackson and Smith, 2016; Landry et al., 2016;
Sameoto, 1986; Vinogradov et al., 1991; Wishner et al., 2013). Copepod
vertical distributions from MOCNESS tows near the Volcano 7 seamount in the
ETNP (13∘ N, 102∘ W) were described by
Saltzman and Wishner (1997).
Many studies also analyzed vertical distributions of some of these species
in adjacent subtropical regions, including the central north Pacific
(Ambler and Miller, 1987; Landry et al., 2001; McGowan
and Walker, 1979) and the southern extent of the California Current off Baja
California (Jiménez-Pérez and Lavaniegos,
2004; Longhurst, 1967) where there is a strong OMZ. Mesopelagic copepod
distributions in other strong OMZs worldwide have also been detailed in the
Eastern Tropical South Pacific off Peru and Chile (Escribano et al.,
2009; Judkins, 1980; Tutasi and Escribano, 2020), the southeastern Atlantic
(Bode et
al., 2018; Teuber et al., 2013a, b, 2019), and the Arabian Sea
(Smith and Madhupratap, 2005;
Wishner et al., 2008).
Many earlier zooplankton studies did not collect the comprehensive
hydrographic data available from modern electronic CTD and oxygen sensors,
did not sample and target specific oxyclines and fine-scale vertical strata
with precision control, did not extend to deeper mesopelagic depths, or
occurred before the recent perspective of OMZ deoxygenation impacts that
guides present research (Breitburg et al., 2018).
It is also essential to have species-level and life stage identification
(not just biomass, size class, or large taxonomic grouping) to understand
the multifaceted interactions and evolutionary adaptations of diverse
zooplankton to the strong persistent (but variable) oxygen gradients of
OMZs. OMZ oxygen is far more variable spatially and temporally than is
generally appreciated, even at mesopelagic depths (Fig. 2), and copepod
distributions responded to both large and subtle differences.
The physical oceanographic complexity of oxygen distributions and sources in
the ETNP, including spatial and temporal variability, has also long been an
active topic of investigation (e.g., Deutsch et al., 2011;
Fiedler and Talley, 2006; Margolskee et al., 2019; Wishner et al., 2018).
However, although we compared vertical distribution differences relative to
oxygen gradients among locations and cruises, our sampling was not designed
to elucidate responses to the many other spatially and temporally variable
environmental forces pertinent to this region, such as climate cycles (El
Niño–Southern Oscillation) or the dynamic variability of the major regional
ocean currents or deep advective flow (Kessler, 2006).
OMZ, oxycline, and “hypoxiphilic” taxa
Oxycline-associated and OMZ species showed a remarkable ability to alter
their vertical distributions to conform to different oxygen profile shapes
at different locations. Many taxa had very narrow oxygen habitat ranges and
strong layering, indicative of precise habitat preference and exceptional
tolerance for low oxygen. These species tended to alter depth (and
temperature) while maintaining a relatively constant oxygen level (Table 3).
Important caveats overall are that (1) we focused primarily on adults
(except for species previously noted) and (2) total population
distributions, even for adults, often extended over broader depth and oxygen
ranges beyond the DMA.
We propose the term “hypoxiphilic” to describe species whose population
distributions, especially maximum abundances, are focused in habitats with
very low oxygen. This term is best used in a comparative sense (without an
exact oxygen definition) to allow flexibility for use in other regions and
ecological situations and with other taxa, since we know little about the
in situ low-oxygen physiology of many species (Teuber et
al., 2013b; Thuesen et al., 1998). L. hulsemannae is the most obvious hypoxiphilic
copepod (both adults and young stages living in very low oxygen at multiple
locations here and in prior work). Earlier studies of its gut contents
indicated recent omnivory (Gowing and Wishner, 1992), suggesting
active feeding, as well as growth, in this habitat. Other possible
hypoxiphilic copepods in this area at this time included D. palumbii, G. kruppi, E. magnus, E. spinifer,
diapausing stages of E. inermis, and M. brevicauda adults, but less is known about the vertical and
geographic distributional variability of all life history stages for these
species.
Diapausing in the OMZ
E. inermis is endemic to the ETP, occurring both north and south of the Equator (Chen,
1986; Fleminger, 1973; Goetze, 2003, 2010; Goetze and Ohman, 2010; Hidalgo
et al., 2005a, b; Jackson and Smith, 2016; Sameoto, 1986). It is known
to inhabit extremely low oxygen water (Boyd
et al., 1980; Escribano et al., 2009; Judkins, 1980; Saltzman and Wishner,
1997; Wishner et al., 2013), as well as oxygenated depths, and has unique
physiological and biochemical adaptations for the low-oxygen environment
(Cass et al., 2014; Cass and Daly, 2015).
Overall population distributions at particular locations in this and prior
work usually encompassed a range of oxygen concentrations, although most
earlier studies had relatively broad sampling strata that did not isolate
specific oxygen ranges or did not have electronic oxygen sensors colocated
on the zooplankton sampling systems. DVM by this species, usually over a
relatively short depth range between the near surface and UO, was reported
by some authors at some times and places but not others (Escribano et al.,
2009; Jackson and Smith, 2016). We previously identified apparent diapause
layers at the upper and lower OMZ boundaries at the CRD and TB stations in
2007–2008 (Wishner et al., 2013), and
Saltzman
and Wishner (1997), Sameoto (1986), and Vinogradov et al. (1991) also noted
abundance peaks associated with OMZ edges in the CRD and other ETNP
locations. Diapause layers in our study varied in depth at different times
and stations, allowing the copepods to remain in a constant-low-oxygen
habitat.
Use of extremely low oxygen habitats for diapause is likely a predator
avoidance mechanism during an extended period of inactivity. Metabolic
adaptations that enable long-term survival for copepods in this habitat,
while not specifically studied, likely include metabolic suppression and
fuel (lipid) storage. Metabolic suppression, typically triggered by
epigenetic mechanisms facilitated by microRNAs, enables a variety of animals
to survive temporary resource limitation and involves shutting down
energetically costly processes such as translation and transcription, ion
transport and protein synthesis (Biggar and Storey, 2010;
Storey and Storey, 2004). The high proportion of animals with stored oil in
these remarkably sharp narrow monospecific layers, composed primarily of
adult females and older copepodite stages, were strong indicators of
diapause. No obvious gut contents were visually noted in these specimens.
E. inermis that was collected at all depths at CRD and TB had stable isotope signatures
indicative of feeding at the surface and not on deeper material
(Williams et al., 2014), suggesting inactivity
at depth. The seasonal ontogenetic and reproductive cycle of E. inermis was documented
at a location off Chile, but the sampling depth was too shallow (75 m) to
elucidate deeper diapause behavior (Hidalgo et al.,
2005a, b). Another calanoid copepod, Calanus pacificus, also has an apparent diapause
layer just above the anoxic bottom water of the deep Santa Barbara Basin off
California (Alldredge et al., 1984; Osgood and
Checkley, 1997) and Calanoides carinatus in the Arabian Sea and Benguela Current diapauses at
depth just below the extensive OMZ (Auel
and Verheye, 2007; Smith et al., 1998; Smith, 1982; Wishner et al., 2008).
Diel vertical migration into low oxygen
Species in the genus Pleuromamma have been studied intensively in the ETNP with regard
to their extensive DVM into low-oxygen water, as previously noted. However,
unlike resident oxycline and OMZ core taxa, these species appeared to
require a period of time at night in well-oxygenated water, presumably to
pay off the oxygen debt incurred during daytime residence in low oxygen. It
was surprising that the part of their diel distribution that changed with
differing oxygen profiles was the shallow nighttime depth, not the deep
daytime depth. They continued to migrate to the same depth in the day at
different locations, presumably determined by light penetration, and likely
an avoidance response to visual predators
(Wishner et al., 2013). At night, they
came up only until they encountered the depth at which there was sufficient
oxygen, within or just above the thermocline, although the temperature was
higher at their nighttime depth when the thermocline was shallow, and
metabolic costs would be elevated. The thermocline was also usually a peak
of zooplankton biomass (Wishner et al.,
2013) and fluorescence (Fig. 2), so food was abundant there as well. Thus,
the upper nighttime depth likely resulted from the combination of higher
oxygen, food availability, and avoidance of even higher temperature in
shallower waters.
Pleuromamma species traveled over different depth ranges within low-oxygen water to
their daytime depth at the different stations. Our sampling could not
resolve whether they moved faster or took longer to make the journey when
the depth range was greater, i.e., how long an individual resided in the low-oxygen water in different circumstances and what the comparative metabolic
costs might be for the migration. It is also unknown whether all of these
species undergo metabolic suppression when in low oxygen, as do many
euphausiids and other strong migrators (Seibel et al., 2016, 2018).
Teuber et al. (2013a, b, 2019) found that Pleuromamma species in the eastern tropical Atlantic
had high thermal and hypoxia tolerances and classified these species as
adaptive migrants on the basis of functional traits. Active transport by
diel vertical migrators is a critical mechanism of export flux in the CRD
(Stukel et al., 2018), and export fluxes appear to be
relatively inefficient in locations with OMZs (Berelson
et al., 2015). Strong presence–absence differences among stations,
especially for Pleuromamma, suggested that some locations may have exceeded the
metabolic capabilities of particular species of diel vertical migrators,
which could be a factor affecting export flux.
Aerobic habitat compression and epipelagic copepods
The aerobic habitat compression hypothesis was supported by the
distributional shifts of several abundant epipelagic species that occurred
over a broader depth range at stations where the well-oxygenated mixed layer
extended deeper. However, our sampling strata, which focused on the
mesopelagic, did not resolve small-scale details, such as short DVM within
the mixed layer or thermocline. Additionally, our taxonomic focus on adults
of larger easily identified species excluded numerous smaller epipelagic
copepods and immature stages. Higher-resolution mixed layer sampling and
more taxonomic breadth is required to thoroughly address this issue for ETNP
copepods. The high oxygen concentration within the mixed layer would not be
a metabolic constraint, but, of course, many other ecological factors could
affect distributions.
Metabolic implications
Animal metabolic rates are highly variable depending on physical factors,
including temperature and oxygen, as well as on the ecological and
evolutionary requirements for energy to support growth, reproduction,
predator–prey interactions, and basic maintenance (Seibel and Drazen, 2007).
The factorial aerobic metabolic scope (FAS, the maximum as a factor of
minimum metabolic rate) typically ranges from about 2 to 6, depending on
temperature (Killen et al., 2016; Seibel and Deutsch, 2019). The FAS at any
given temperature can be estimated as the ratio of environmental PO2
(below the Pcrit for maximum metabolic rate) to the Pcrit for
resting metabolic rate, which is numerically equivalent to the metabolic
index described by Deutsch et al. (2015). This means that the maximum
available environmental PO2 is usually a factor of 2–6 above the
critical PO2 for resting metabolism, depending on temperature.
For species exposed to air-saturated water, including vertical migrators
during their nighttime forays into shallow water, any reduction in PO2
will result in a quantifiable reduction in maximum capacity and FAS. In this
light, our observations that the nighttime depth distribution of vertical
migrators responded more strongly to variations in oxygen content than did
the deeper daytime depth are not surprising. Migrators descend during the day
to depths consistent with predator avoidance in low light. If the oxygen at
those depths is below the Pcrit, then metabolic suppression is
triggered, which dramatically increases tolerance time to low oxygen (Seibel
et al., 2014, 2016, 2018).
In contrast, permanent residents of the lower oxycline and OMZ core have
much lower Pcrit values. L. hulsemannae, for example, has the lowest Pcrit ever
measured for an animal (minimum values of 0.1 and 0.3 kPa; mean values
of 0.38 and 0.67 kPa at 8 and 5 ∘C, respectively), comparable to
only two other known OMZ specialists, the pelagic red crab, Pleuroncodes planipes (Quetin and
Childress, 1976), and the shrimp, Gennades spp. (Wishner et al., 2018). Using the
minimum values and assuming a typical FAS ranging from 2 to 6 (Seibel and
Deutsch, 2019; Killen et al., 2016), we suggest that the maximum available
environmental PO2 to which L. hulsemannae is ever exposed is ∼1.8 kPa
at 5 ∘C and ∼0.6 kPa at 8 ∘C. These
values are very close to the highest values at which L. hulsemannae was captured in the
present study. The minimum oxygen pressures recorded across the habitat for
L. hulsemannae (0.77 to 0.30 kPa at different locations) are very near the mean
Pcrit values and about 2–3 × the minimum Pcrit values, thus providing little
aerobic scope at those depths. The reverse temperature effect observed for
L. hulsemannae, in which higher temperature results in a lower Pcrit despite a higher
metabolic rate, ensures a FAS similar to that known to bound the latitudinal
distributions of many marine species (Deutsch et al., 2015). The reverse
temperature effect is adaptive in the lower oxycline of the OMZ where
temperature decreases while oxygen increases with increasing depth.
The unique metabolic adaptations for hypoxia tolerance of L. hulsemannae, especially its
reverse temperature response, result in a nearly constant ratio
(∼ 1 to 2) of environmental PO2 to the mean Pcrit
across the inhabited depth range. In fact, Wishner et al. (2018) showed that
when this ratio (the metabolic index; Deutsch et al., 2015) approaches 2,
abundance declines. Using the minimum, rather than the mean, values measured
for L. hulsemannae suggests higher ratios (∼ 2–6), which may better
represent the in vivo abilities of the species and is more consistent with values
shown to support marine animal populations (Deutsch et al., 2015). A ratio
below 1 suggests that the species is incapable of meeting its resting needs,
whereas a ratio above 1 allows a proportional increase in the scope for
aerobic activities, including locomotion, growth, and reproduction. The
minimum PO2 at the minimum temperatures reported at all stations
results in a drop in the metabolic index consistently below 1 (using mean
values). Although our sampling regime cannot pinpoint the precise conditions
under which individual animals are found, the metabolic index suggests that
this species may not be able to tolerate the most extreme low oxygen at low
temperature. Because critical PO2 and its temperature sensitivity vary
considerably among species, it is not possible to estimate metabolically
available habitat for species lacking Pcrit data or those for which
data exist at only a single temperature.
Conclusions
Individual copepod species demonstrated different distributional strategies
in response to present-day variability of oxygen vertical profiles in the
ETNP region. We identified sets of species that (1) changed their vertical
distributions and depth of maximum abundance associated with the depth and
intensity of the OMZ and its oxycline inflection points; (2) adjusted their
diel vertical migration, especially the nighttime upper depth; (3) shifted
their depth of diapause; (4) or expanded/contracted their depth range
within the mixed layer and upper thermocline in association with the
thickness of the aerobic epipelagic zone (Table 2). Congeners, closely
related species in the same genus, often showed similar adaptation
strategies that were centered at different depths. Hypoxiphilic species
had their highest abundances in low-oxygen habitats. These species examples
represented a range of calanoid copepod families and trophic ecologies. We
expect that similar distributional adaptations to OMZ variability occur
across a broad suite of copepod groups, as well as other zooplankton and
fish taxa. The schematic diagram Fig. 11 depicts potential zooplankton
distributional responses to OMZ expansion, based on present-day patterns.
Schematic illustration of OMZ expansion effects on zooplankton
distributions. The bracket indicates the most aerobic habitat of the water
column (mixed layer plus upper oxycline). The dashed line represents diel
vertical migration. The layer of diapausing E. inermis is shown just above the lower
oxycline. This figure updates earlier depictions (Seibel, 2011; Wishner et
al., 2013; Seibel and Wishner, 2019) with new information from this study.
Combinations of environmental oxygen concentration and temperature, two
critical determinants of metabolic rates, defined habitats with the highest
abundances for each species at each site. In different locations, animals
living at, or transiting through, the same depth (same temperature) could
experience quite different oxygen regimes: for example, the daytime
migration paths of Pleuromamma species. Animals requiring a specific oxygen partial
pressure might be forced to live at different depths (and temperatures): for
example, the lower oxycline copepod L. hulsemannae and thermocline inhabitant H. longicornis. Thus,
animals at locations with different oxygen profiles experienced different
oxygen regimes, but the same temperature, at a particular mesopelagic depth,
while animals whose peak distributions varied in depth experienced different
temperature regimes often at the same oxygen level. Previous work
demonstrated that zooplankton can and do respond to very small oxygen and
temperature differences in both oceanic and coastal locations
(Pierson et al., 2017; Roman et
al., 2019; Svetlichny et al., 2000; Wishner et al., 2018). Of course, many
other ecological and environmental conditions affect habitat choice and
population abundance, but it is likely that the extremely low oxygen of the
ETNP OMZ is a critical controlling factor in this region.
As is becoming apparent from numerous studies, the upper ocean to
mesopelagic depth range is a complex interwoven ecosystem with intricate
relationships among its various inhabitants and their environment. It is
also a critically important zone for oceanic biogeochemical and export
processes that can be affected by oxygen gradients and hosts key food web
components for commercial fisheries. Among the zooplankton, there will
likely be winners and losers as ocean deoxygenation continues in the future
and becomes more widespread. Changes in individual copepod species
abundances, vertical distributions, and life history strategies may create
perturbations to these intricate food webs and processes. For example,
hypoxiphilic taxa, such as L. hulsemannae, as well as the other oxycline and OMZ
species, might increase in abundance and expand their depth range until
other physiological (temperature) or ecological (food, predators) barriers
become overwhelming. Present-day variability provides a window into future
scenarios (Fig. 11), but much more research is required to fully elucidate
and quantify consequences.
Data availability
All data needed to evaluate the conclusions in the paper
are present in the paper and in two online repositories: the supplementary
Table S1 that includes copepod species abundances in each net for these tows
(Wishner et al., 2019, 10.23860/dataset-wishner-2019) and the
BCO-DMO repository that includes time and location data for each MOCNESS
tow, https://www.bco-dmo.org (last access: 20 January 2020), 10.1575/1912/bco-dmo.786098.1 (Wishner, 2020a), and
10.1575/1912/bco-dmo.787329.1 (Wishner, 2020b).
Upon publication, the full paper will be deposited in the BCO-DMO
database (with a DOI), as required for National Science
Foundation-funded projects. Extensive files of continuous hydrographic data
from MOCNESS tows are available from Karen F. Wishner. Additional data related to this
paper may be requested from the authors.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-17-2315-2020-supplement.
Author contributions
KFW led the writing effort, with substantial
contributions from all co-authors. KFW directed the MOCNESS sampling
component including analyses of zooplankton abundances and distributions,
with assistance at sea and in the lab by all co-authors. DO sorted and
identified most of the copepods and processed and graphed data. BAS directed
the metabolic sampling and experiments at sea and led the analyses and
writing of those sections of the paper.
Competing interests
The authors declare that they have no conflict of interest.
Special issue statement
This article is part of the special issue “Ocean deoxygenation: drivers and consequences – past, present and future (BG/CP/OS inter-journal SI)”. It is a result of the International Conference on Ocean Deoxygenation, Kiel, Germany, 3–7 September 2018.
Acknowledgements
We thank the captains, crews, and marine technicians of all the ships and the institutional marine offices (University of Miami, Woods Hole Oceanographic Institution, University of Washington, University of Alaska). MOCNESS instruments and technical support were provided by the University of Miami and Scripps Institution of Oceanography, with assistance from Erich Horgan, James Lovin, Peter Wiebe, Carl Matson, and John Calderwood. Kendra Daly and Brad Seibel served as cruise chief scientists. Many students, technicians, and colleagues helped at sea and in the lab over the years with the MOCNESS tows, sample processing, and data analyses, especially Thomas J. Adams, Nicole Charriere, Kendra Daly, Curtis Deutsch, Charles Flagg, Sarah Frazar, Jason Graff, Jamie Ivory, Amy Maas, Jillon McGreal, Marianne McNamara, Megan O'Brien, Danielle Moore, Jocelyn Pelser, Brennan Phillips, Shannon Riley, Chris Roman, C. Tracy Shaw, and Rebecca Williams.
Financial support
This research has been supported by National Science Foundation grants OCE0526545 (Kendra Daly), OCE0526502 (Karen F. Wishner, Brad Seibel), OCE1459243 (Brad Seibel, Karen F. Wishner, Chris Roman), and OCE1458967 (Curtis Deutsch). The University of Rhode Island's Graduate School of Oceanography's summer REU program, SURFO, funded Sarah Frazar and Shannon Riley (NSF grants OCE-0851794 and OCE1460819) and the Coastal Institute contributed to publication costs. Faculty and student funding was also provided by our institutions.
Review statement
This paper was edited by Kenneth Rose and reviewed by two anonymous referees.
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