Journal of

Plankton Research

plankt.oxfordjournals.org

J. Plankton Res. (2016) 38(2): 305– 316. First published online January 13, 2016 doi:10.1093/plankt/fbv117

Costa Rica Dome: Flux and Zinc Experiments

Vertical distribution of Eucalanoid copepods within the Costa Rica Dome area of the Eastern Tropical Pacific MELANIE L. JACKSON1* AND SHARON L. SMITH2 1

UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE, HORN POINT LABORATORY, CAMBRIDGE, MD

OF MARINE AND ATMOSPHERIC SCIENCE,

21613, USA AND 2ROSENSTIEL SCHOOL

4600 RICKENBACKER CAUSEWAY, MIAMI, FL 33149, USA

*CORRESPONDING AUTHOR: [email protected]

Received April 13, 2015; accepted December 7, 2015 Corresponding editor: Roger Harris

A variety of ecological strategies for tolerance of low-oxygen conditions within the Costa Rica Dome (CRD) area of the Eastern Tropical Pacific are documented for the copepod family Eucalanidae. During the summer of 2010, we compared the ecological strategies used by the Eucalanidae inside and outside the central CRD region. We compared the vertical and horizontal distributions of five species, Eucalanus inermis, Subeucalanus subtenuis, Subeucalanus subcrassus, Subeucalanus pileatus and Pareucalanus attenuatus together with Rhincalanus species, in the epipelagic (upper 200 m) among four locations, which we grouped into a section roughly crossing the core CRD area (inside– outside core CRD). The coastal area outside the CRD supported the most diverse assemblage, whereas overall abundance of Eucalanidae in the central CRD was 2-fold greater than outside and dominated by E. inermis (.60%). Eucalanidae in the central CRD had a shallow depth distribution, closely associated with the shallow thermocline (10 –20 m). There was no evidence of daily vertical migration in the central CRD, but E. inermis demonstrated vertical migration outside the CRD. The vertical abundance patterns of Eucalanidae in the CRD region reflect complex interactions between subtle physical – chemical differences and food resources. KEYWORDS: Eucalanidae; Eucalanus inermis; oxygen minimum zone; zooplankton biomass

I N T RO D U C T I O N Mesozooplankton (size range 0.2– 2 mm) are among the many small pelagic animals that migrate to depth in the

daytime to seek refuge from large predators (Vinogradov, 1970) and that make significant contributions to oceanic biogeochemical cycles because of their consumption of

available online at www.plankt.oxfordjournals.org # The Author 2016. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]

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phytoplankton and nanoplankton (Zhang and Dam, 1997). As a result, changes in mesozooplankton communities can be indicators of the effects of global climate change on pelagic ecosystems (Hays et al., 2005). Although the roles of mesozooplankton in marine ecosystems have been studied, the distribution of mesozooplankton in the open ocean is still poorly understood, especially in the tropical open ocean. As a part of the Costa Rica Dome FLUx and Zinc Experiments (CRD FLUZiE), during the summer of 2010, we investigated the distribution and abundance of copepod species in the family Eucalanidae during a period of suppressed summertime upwelling. The CRD is known for its seasonal (summer and early fall) upwelling caused by cyclonic wind stress curl and a coastal wind jet in the Eastern Tropical Pacific (ETP) Ocean (Fiedler, 2002). The summer of 2010 was an anomalous year, according to satellite images analyzed from 2004 to 2014, because of its lack of elevated Chl a at the surface during mid-summer (Landry et al., 2016a). Based on previously recorded vertical distributions of mesozooplankton, such low concentrations of Chl a may have resulted in changes in the abundance and distributions of some endemic mesozooplankton. The abundance and vertical distribution of the copepod family Eucalanidae, a family that includes Eucalanus, Subeucalanus and Pareucalanus (Cass, 2011; Cass and Daly, 2015), have been studied recently during fall/winter cruises (from 2007 to 2009) in the CRD area of the Eastern Tropical North Pacific (ETNP) Ocean (Cass et al., 2014; Cass and Daly, 2015). These studies determined that Eucalanus inermis, Subeucalanus subtenuis, Pareucalanus attenuatus and Rhincalanus spp. formed four groups of differing ecological strategies in the ETP based on their biochemical, physiological and behavioral characteristics (Cass and Daly, 2015). For example, Pareucalanus attenuatus and E. inermis have jelly-like bodies and lowprotein levels, allowing them to have lower metabolic oxygen demands, where S. subtenuis have no or few biochemical or physiological strategies to cope with low oxygen (Cass and Daly, 2015). The physiological attributes used by the Eucalanidae in the ETNP are likely adaptations for survival in low-oxygen regions, and as a result influence the vertical biological assemblages present. The organisms residing in the regions of low oxygen are expected to have compressed distributions in shallow, nearsurface oxygenated waters (Prince and Goodyear, 2006). The behavioral and physiological characteristics of these copepods have been addressed with respect to their vertical distribution; however, it is unclear whether these characteristics impact their distribution and abundance over horizontal gradients as well. Epipelagic marine ecosystems are known for having stronger vertical gradients than horizontal gradients in

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light, temperature, salinity, density, dissolved oxygen concentration, current speed and direction and autotrophic and heterotrophic biomass (Longhurst, 1985). One mechanism that some copepods use to respond to such environmental gradients is diel vertical migration (DVM). During DVM, copepods move into deeper layers during the daytime to avoid predators, decreasing metabolic rates in colder deep waters and then moving back into the surface at night to feed. Copepods may modify their DVM, depending on the abundance of their predators (Bollens et al., 1992). DVM has also been observed in coastal upwelling regions, as a way for copepods to take advantage of favorable conditions (e.g. circulation patterns) in the coastal environment (Batchelder et al., 2002). These ideas suggest that differences in DVM may be present inside and outside of the CRD. Coastal upwelling may produce circulation patterns carrying copepods away from the coast. Over time, organisms can evolve mechanisms that allow robust development of populations in coastal zones (Peterson, 1998). Eucalanus inermis is one Eucalanoid species that is found with peak abundances within or near the chlorophyll maximum (Chen, 1986; Sameoto, 1986; Vinogradov et al., 1991; Saltzman and Wishner, 1997). Although the CRD and coastal upwelling regions are both recognized for their enhanced biological production, a drift array track from the summer of 2010 suggests a complex circulation pattern in the CRD region with possible entrainment of water and associated biological production toward the coast from within the CRD (Landry et al. 2016a). Thus, a coastward flow of water from within the CRD could result in a gradient in Eucalanidae distribution and DVM, which have not been observed in the CRD prior to this study. On the basis of this knowledge and the ecological strategies of Eucalanoid copepods (Cass and Daly, 2015), we hypothesized that their DVM would differ inside and outside of the CRD and that the populations of Eucalanoid species would be associated with the DVM patterns. Sampling during summer 2010 provided an opportunity to make an observational study to determine the distributions and abundances of the Eucalanidae inside and outside of the CRD and to close the seasonal sampling gap. Modifications of mesozooplankton distributions and DVM behaviors based on environmental conditions have been observed in a number of other studies (Hays, 2003; Gomez-Gutierrez and Robinson, 2006; Wishner et al., 2008; Palomares-Garcı´a et al., 2013) with most attention concentrated on copepods of the Calanidae family. While E. inermis is abundant and relatively well studied in the ETNP (Longhurst, 1985; Chen, 1986; Saltzman and Wishner, 1997; Wishner et al., 2013; Cass et al., 2014; Cass and Daly, 2015), this study will help to develop a

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clearer understanding of how ecological strategies impact their abundance and distribution over a horizontal gradient. Eucalanus inermis populations have been found in near-surface waters as well as in the upper and lower oxyclines of the oxygen minimum zone of the ETNP (Wishner et al., 2013). Building on the work of Cass and Daly (Cass and Daly, 2015), we focused on E. inermis conspecifics residing in shallower depths to learn how they differ from the individuals performing ontogenetic vertical migrations (OVMs) in the upper and lower oxyclines (Cass and Daly, 2015). Therefore, we used a geographic comparison of the shallower conspecifics’ distribution sampled in a section running across the CRD from outside to inside to provide insight into how vertical and horizontal gradients in environmental parameters influence the abundance and vertical distribution of the Eucalanidae.

METHOD Sampling and data collection Data were collected during the oceanographic cruise MV1008 on the R/V Melville, sampling five different locations (Fig. 1) in the CRD area from 22 June to 25 July 2010. Sampling was performed using a MOCNESS (Multiple Opening/Closing Net and Environmental Sensing System) (Wiebe et al., 1985) fitted with 222-mm mesh nets. One sample set was taken in the morning and one at night (beginning at 10:00 and 22:00 h local time, respectively) during each observational “cycle” that followed the drift-path of a satellite-tracked drifter with a mixed-layer drogue (Landry et al. 2016a). A conductivity– temperature –depth (CTD) cast was taken at each of the stations to 500 m for each of the allotted time periods just prior to the MOCNESS deployment.

Fig. 1. Area of study. Day –night cycles where zooplankton were collected with a MOCNESS during the summer of 2010 (Cycles 1 –5) with day and night tows shown within each cycle.

MOCNESS samples were taken over the upper 1000 m, with the sampling depths being 0 – 25, 25 – 75, 75– 100, 100– 200, 200– 300, 300 – 450, 450 –600, 600– 750 and 750 – 1000 m. These sampling strata were determined after the CTD casts in order to capture the thermocline and fluorescence peak, typically including water from above, within and below the fluorescence peak. The volume of water filtered was determined by a flow meter on the MOCNESS frame. Immediately after each tow, the cod ends were split with a Folsom splitter, with 30% of the sample going to the Pelagic Collections at the Scripps Institution of Oceanography. Fifty percent was preserved in 5% neutral formalin to be used for taxonomic analyses in the present study, and the remaining 20% was used for dry weight measurements. We analyzed the preserved fraction using a Wild M5 dissecting microscope and a Wild M20 – 42056 compound microscope at the Rosenstiel School of Marine and Atmospheric Science, University of Miami. Sampling sites were grouped based on geographical position (Fig. 1) into an approximate section located across the core CRD area (Landry et al. 2016a). Sampling during Cycle 3 was farthest from the coast and northwest of the core CRD region; it consisted of a day and night tow. Sampling for Cycles 2 and 4 in the core region of the CRD consisted of four tows. Sampling for Cycle 5, closer to the coast of Central America and outside the core CRD, was made up of one day and one night tow. Sampling for Cycle 1 was close to Cycle 5, but consisted of only one tow, which was done at night. For this study, samples from four depth strata were used: 100 – 200 m, 75– 100 m, 25– 75 m and 0 – 25 m.

Species abundance For species abundance, samples were split into smaller subsamples for species identification and enumeration in the laboratory. Only the Eucalanidae were removed from each of the subsamples observed, to determine their species and whether they were female, male or copepodites. During this process, Rhincalanus species were also removed due to their high abundance in many samples. Data for abundance were standardized to individuals per cubic meter (ind. m23) for each of the subsamples analyzed. The different Eucalanidae species were distinguished from one another based on morphological analysis under the microscope and some practice with Fleminger’s (Fleminger, 1973) methods using glandular pores and sensilla for Eucalanidae identification. The most frequent species were Eucalanus inermis (Giesbrecht, 1892), Subeucalanus subtenuis (Giesbrecht, 1888) and Pareucalanus attenuatus (Dana, 1849). Median depths, defined as the depths above and below which 50% of the animals were

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found, were calculated to compare vertical distributions of the species across the CRD region (Cheney, 1985).

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used R CRAN v. 3.1 with an R-studio v. 0.98 interface for all statistical analyses (R Development Core Team, 2014).

Statistics Canonical correspondence analysis (CCA) was performed to characterize the relationships among the different species in vertical distribution, abundance and environmental variables (Ter Braak, 1986; PalomaresGarcı´a et al., 2013). The CCA was used to analyze the species abundance matrix, which directly relates variation in the patterns of the abundance of the copepod community to variation in environmental variables (Ter Braak and Prentice, 1988). The environmental matrix contained the average values within each depth stratum for the five environmental parameters measured (mean temperature, mean practical salinity, mean dissolved oxygen concentration, mean fluorescence and depth of the thermocline). In addition, categorical variables were included in the environmental matrix: time of the day (day vs. night) and depth (in situ sampling depth layers 12.5, 37.5, 50, 62.5, 87.5 or 150 m). A Monte Carlo test was used to determine the significance of the correlations among the environmental factors listed in the matrix and the abundances and locations of the species of Eucalanidae collected in each stratum. The results are shown in a bi-plot with environmental variables as vectors and sampling stations as points in ordination space. The importance of an ordination axis was measured by eigenvalues, and the percentage of variance of the species data explained by the axes was determined from the eigenvalues and the sum of all unconstrained eigenvalues (Ter Braak, 1986). In order to interpret the ordination axes, correlation coefficients among environmental variables and each ordination axis were calculated. The signs and relative magnitudes of the correlation coefficients indicate the relative importance of each environmental variable in predicting the Eucalanidae community composition (Ter Braak and Prentice, 1988). CCA provided insight into the main aspects of variability in the vertical and spatial distribution as a function of the five gradients of environmental conditions. A multi-response permutation procedure (MRPP) was performed to test the null hypothesis (Ho) that there was no significant difference in the abundance of the Eucalanidae species observed in the day– night cycles (Cycles 2 – 4) within the CRD region versus the day – night cycles outside of the core CRD (Cycles 1 and 5). The CCA and MRPP procedures are nonparametric tests that do not require copepod abundance to be normally distributed and work well when species distribution is skewed (Palmer, 1993). We applied the vegan package 2.0 – 10 for CCA and MRPP analyses (Oksanen et al., 2015), and we

R E S U LT S The general environmental conditions observed over the CRD region are described in this issue (Landry et al. 2016a; Selph et al., 2016), allowing us to focus on the Eucalanoid abundance and distribution as a function of environmental conditions. Detailed distributions of temperature, nutrients, dissolved oxygen, Chl a, phytoplankton primary production and taxon-specific growth rates in the upper 100 m of the water column during the five observational cycles conducted in the summer of 2010 are provided in Selph et al. (Selph et al. 2016). Conditions during summer 2010 were notable for having strongly depressed near-surface Chl a values. In fact, in 2010, we encountered the lowest concentrations of summertime Chl a measured by satellite in a decade, 2004 – 2014. A moderate El Nin˜o event preceding the cruise is considered the cause of the reduced surface Chl a concentrations (Landry et al., 2016a). In the extended depth plots of Fig. 2, temperature profiles were similar among Cycles 2 – 4; however, the sampling sites outside of the CRD and near the coast (Cycles 1 and 5) had deeper thermoclines (30– 40 m) than the other cycles (Fig. 2D and H). Within the central area of the CRD (Cycles 2 and 4; Fig. 2A, C, E and G) and offshore to the northwest (Cycle 3; Fig. 2B and F), fluorescence profiles typically had one peak at about the thermocline depth, whereas the nearshore sites outside of the CRD (Cycles 1 and 5; Fig. 2D and H) had overall lower fluorescence with two peaks, one approximately at the top of the thermocline and another at the base. For sampling stations during Cycles 2 – 4 (CRD and NW CRD region), oxygen rapidly declined between 30 and 40 m, whereas the profiles of Cycles 1 and 5 showed the main decrease in oxygen concentration occurring at 60 – 70 m (Fig. 2). We restricted our study to samples taken from the upper 200 m, because much of the mesozooplankton biomass was found in shallower depths. Within this upper layer, we observed that S. subtenuis, E. inermis and Rhincalanus spp. were the most abundant species (making up 99% of total abundance), whereas S. subcrassus and P. attenuatus were the least abundant Eucalanidae. Compared with previous records, total adult E. inermis numbers were similar to those recorded for the winter and fall of 2007– 2009 (Cass and Daly, 2015). However, S. subtenuis and P. attenuatus abundances were approximately 10-fold lower than during the fall and winter of 2007 – 2009 (Cass and Daly, 2015).

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Fig. 2. Depth profiles of dissolved oxygen (D-Oxygen, mM), temperature (8C) and fluorescence (V) during day– night cycles. (A) Cycle 2– Day, (B) Cycle 3– Day, (C) Cycle 4– Day, (D) Cycle 5– Day, (E) Cycle 2 –Night, (F) Cycle 3 –Night, (G) Cycle 4– Night, (H) Cycle 5– Night.

Abundance and depth distribution Overall, six species of Eucalanidae were identified during the cruise. Cycle 5 (nearshore and outside of the CRD) was the only site that had all six copepod species. Subeucalanus subtenuis, E. inermis and Rhincalanus spp. were present during all of the day– night cycles, whereas S. subcrassus and P. attenuatus were absent at different times during Cycles 2 – 4 (NW of and inside the CRD). Although the diversity of Eucalanidae species was greater outside of the CRD and toward the coast, overall abundance was approximately 2-fold greater during Cycles 2 –4 (the CRD center and NW offshore) compared with Cycle 5 (outside of the CRD and nearshore). Most species resided primarily near the thermocline in Cycles 2 –4, whereas Cycle 5 showed deeper vertical distributions of all Eucalanoid species found. In the Eucalanidae, Eucalanus inermis was the most abundant copepod in all of the samples except for Cycle

4 at night (core of the CRD; Fig. 3F). Eucalanus inermis made up .60% of the Eucalanidae community assemblage during Cycles 2 and 3 (the CRD center and NW offshore) and 40% during Cycle 5 (outside of the CRD and nearshore). Subeucalanus subtenuis was the next most abundant species in all of the samples, residing mostly in the upper 25 m (Fig. 3). In contrast, E. inermis and Rhincalanus spp. were present throughout the 200-m sampling range. Samples taken nearshore and outside of the CRD (Cycles 1 and 5) showed a broader vertical distribution of E. inermis compared with that of Cycles 2 – 4. During Cycles 2 and 4 (inside the CRD), median depths of the Rhincalanus spp. distribution were some of the deepest observed (Fig. 4A and C). Overall, P. attenuatus and S. subcrassus were the least abundant, and their greatest abundance was observed during Cycles 1 and 5, which were nearshore and outside the CRD (Fig. 3G and H). Depending on the time of the day or cycle location, some variability in depth of maximum abundance of

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Fig. 3. Vertical profiles for Eucalanidae during day –night cycles. Numbers of individuals per m3 are given for each depth interval in the upper 200 m. (A) Cycle 2 –Day, (B) Cycle 2 –Night, (C) Cycle 3– Day, (D) Cycle 3– Night, (E) Cycle 4– Day, (F) Cycle 4– Night, (G) Cycle 5 –Day, (H) Cycle 5– Night. Note that depth intervals are not the same in all cycles.

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Fig. 4. Median depth of Eucalanidae during day– night cycles. (A) Cycle 2– Day and Night, (B) Cycle 3– Day and Night, (C) Cycle 4 –Day and Night, (D) Cycle 5 –Day and Night. The vertical error bar lines represent the upper and lower median depth range.

E. inermis was observed. During Cycle 3 (NW of central CRD), in the abundance maximum of E. inermis between 25 and 75 m, numbers were greater during the day compared with night (Fig. 3C and D) implying possible reverse DVM. Although the depth intervals were somewhat different for Cycle 5, we observed greater abundance of E. inermis in the 50 – 100 m layer during the day (Fig. 3G and H). During Cycles 2 – 4, total numbers of E. inermis were significantly greater in the 25– 50 m or 25– 75 m depth ranges. During Cycle 5, E. inermis had a broader water-column distribution than in other cycles. Comparing the daytime and nighttime median depths of species provided insight into whether they undertook

DVM in the CRD. Median depth of E. inermis during the daytime was 37.5 m deeper than observed at night during Cycle 5 (Fig. 4D), but the median depths during Cycles 2 – 4 remained the same over the day – night cycle (40 – 50 m; Fig. 4A, B and C). From our determination of median depths for E. inermis, we saw no obvious DVM in Cycles 2 –4. The median depths for Rhincalanus spp. were the same at night for Cycles 2 – 4 (150 + 50 m), but the median depth during day and night of Cycle 5 was shallower (87.5 + 12.5 m). A test comparing median depths over all cycles and all times showed that there were no significant differences in day and night median depths for E. inermis, S. subtenuis or Rhincalanus spp. (Student’s

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Table I: Copepod species assemblage correlations with axes of the correspondence canonical analysis (CCA) from inside and outside of the CRD during all day– night cycles Multidimensional axes

1

2

3

4

Eigenvalues Species-environment correlation Cumulative percentage variance of species data Cumulative percentage variance of species-environment relations

0.345 0.605 0.582

0.206 0.361 0.366

0.018 0.031 0.051

0.001 0.002 0.041

0.605

0.966

0.998

1.000

t-test, P . 0.05). Subeucalanus subcrassus and P. attenuatus were not included in this test since they were absent during different times of Cycles 2 – 4.

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Table II: Correspondence canonical analysis (CCA) based on environmental conditions observed during the summer of 2010 in the CRD, using the conditions measured at each of the recorded sampling depth layers during the day– night cycles Environmental variables/axes

Axis 1

Axis 2

Axis 3

Axis 4

Temperature (8C) Practical salinity Oxygen concentration (mM) Fluorescence (V) Sampling station depth (m) Thermocline depth (m)

2 0.613 0.548 2 0.528 0.042 0.624 0.119

2 0.388 0.351 2 0.484 2 0.157 0.032 2 0.361

0.627 2 0.681 0.608 0.513 2 0.393 0.252

0.125 2 0.183 0.173 0.192 2 0.033 2 0.864

The Pearson and Kendall correlations (r . 0.60) are shown in bold.

Effect of environment Four environmental ordination axes captured 55% of the total variability in Eucalanidae abundance over the upper 200 m of the CRD. The first axis is negatively correlated with temperature (r ¼ 20.61) but positively correlated with sampling depth (r ¼ 0.62), which emphasizes the effect of the vertical temperature gradient (Table II). As a result, Axis 1 in the CCA bi-plot depicts the vertical temperature gradient with depth, whereas the second axis reflects the differences in the Eucalanidae assemblages inside and outside the central CRD area (Fig. 5). Eucalanus inermis, S. subtenuis and P. attenuatus comprised the majority of the Eucalanidae sampled in the CRD, and were the most widely distributed among the day – night cycles, based on their central placement in the multivariate ordination (Fig. 5). Eucalanus inermis abundance has a strong positive association with Axis 2 because they were more abundant in the center and northwest portions of the CRD (Cycles 2 and 3; Fig. 5). Subeucalanus subtenuis and P. attenuatus were located in the left half of the Axis 1 ordination, indicating a relatively strong association with warmer temperatures and more oxygenated waters, consistent with their higher abundance outside of the CRD center (Fig. 5). Rhincalanus spp. are located in the right half of Axis 1, based on their abundance maxima at depths .80 m, whereas P. attenuatus and S. subtenuis are located on the left half of Axis 1 since they were associated with conditions observed in near-surface waters. Subeucalanus subtenuis, P. attenuatus, S. subcrassus and Rhincalanus spp. are all located in the bottom half of Axis 2 based on their greater abundances outside of the CRD region. Although the CCA bi-plot separated the Eucalanidae assemblages based on the cycle locations, with the top half of Axis 2 showing a strong association with Cycles 2 and 3 (inside the CRD),

Fig. 5. CCA of copepod abundance as a function of seven environmental variables recorded during the day –night cycles inside and outside of the CRD. The CCA sampling stations for each depth layer and environmental vectors with species are oriented on the same CCA plot.

the MRPP showed that the copepod assemblage outside of the CRD was not significantly different from the assemblage within the CRD (P ¼ 0.147).

DISCUSSION Comparison of Eucalanidae abundance and diversity among cycles Vertical distributions and abundances of Eucalanidae have been explored extensively in the CRD region with respect to their physiology and biochemistry; however, their vertical and horizontal distributions relative to environmental gradients have rarely been studied. We found that the cycles outside of the CRD and nearshore (Cycles 1 and 5) were characterized by all six of the Eucalanidae species, whereas S. subcrassus and P. attenuatus were absent during either night or day in the CRD and NW of the CRD region (Cycles 2 – 4). A similar pattern was observed in a comparison of the onshore and

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offshore abundances of S. subcrassus in the OMZ of the Arabian Sea, although the depths analyzed were in the 300– 1000 m range (Wishner et al., 2008). Prior to this study, S. subcrassus’ vertical depth distribution and ecological strategies have not been described as extensively as the other Eucalanidae species. A previous work has shown that the species within the CRD region exhibit a variety of ecological strategies to adapt to environmental conditions, such as E. inermis’ and P. attenuatus’ high water content ( jelly-like) that is indicative of lower weightspecific metabolism and S. subtenuis’ high-protein and low-lipid composition (Cass and Daly, 2015), indicative of life at the surface and greater swimming activity. Subeucalanus subtenuis, S. subcrassus and P. attenuatus are known for their similar vertical depth distributions (Longhurst, 1985; Chen, 1986; Saltzman and Wishner, 1997; Wishner et al., 2013; Cass and Daly, 2015), but the variability in their response depending on horizontal gradients has not been examined as closely. It was not obvious whether P. attenuatus effectively adapted to the environmental conditions within the CRD, based on its absence; however, S. subtenuis was always present within the CRD, potentially because of its swimming abilities. When S. subcrassus and P. attenuatus were present within the CRD, they were restricted to the upper 20 m, whereas conditions outside the CRD (both NW of the CRD and nearshore) allowed them to extend down to 80 and 100 m, respectively. These results indicate that P. attenuatus’ and S. subtenuis’ contrasting body compositions allowed them to alter their vertical depth distribution and abundance to the environmental conditions inside and outside of the CRD region in different ways, whereas P. attenuatus and S. subcrassus adapted to the environmental conditions in a similar fashion. Overall Eucalanidae abundance was greater in the central CRD region (Cycles 2 and 4), with E. inermis dominating the copepod assemblage. Eucalanus inermis can dominate the central CRD region by coupling low metabolic rates with lactate dehydrogenase activity, which allows it to occupy a greater vertical range under lowoxygen conditions (Vin˜a, 2002; Cass et al., 2014; Cass and Daly, 2015). This study indicates that E. inermis may use its physiological flexibility to dominate regions of the CRD area characterized by environmental conditions that are not favorable for other members of the Eucalanidae.

Vertical migrations The vertical distribution of copepods in the Pacific Ocean has been separated into three types: (i) no migrations, same depth maxima during day and night to a maximum depth of 75 m, (ii) ontogenetic migration only and (iii) daily and ontogenetic migrations (Ambler and

Miller, 1987). Various studies have discussed the vertical distributions of E. inermis and proposed the existence of OVM (Saltzman and Wishner, 1997; Hidalgo et al., 2005a; Escribano et al., 2009; Wishner et al., 2013; Cass and Daly, 2015). Eucalanus inermis have been observed to perform an ontogenetic vertical descent to, and longterm residence in, the upper and lower boundaries of the OMZ in the Tehuantepec Bowl and the CRD (Wishner et al., 2013). In the coastal zone of northern Chile, an area containing an intense OMZ, adult E. inermis females ascend daily at night from depth (.60 m) to the surface (0 –30 m) and subsurface (30– 60 m) (Hidalgo et al., 2005a). We observed a similar nighttime ascent of E. inermis outside of the central CRD (Cycle 5) during our study (Fig. 5D), whereas the vertical distribution of E. inermis adult females remained unchanged in the central CRD during day– night cycles (Cycles 2 and 4). Although our study only focused on the adult Eucalanidae residing in the upper 200 m, the separation of day– night median depths for E. inermis outside of the CRD (Cycle 5) indicates that they can perform both daily and probably ontogenetic migrations. Our observations provide evidence for a change in DVM in response to environmental conditions within the CRD region. Many investigators have observed that peaks in zooplankton abundance occur directly above a subsurface Chl a maximum (Longhurst, 1976; Williamson et al., 1996), and it is typical for herbivorous species of copepods to remain near the thermocline in the Chl a maximum for the majority of the day, with little diel migration (Ferna´ndezA´lamo and Fa¨rber-Lorda, 2006; Palomares-Garcı´a et al., 2013). The variability in median depth was often large in our study. The narrow depth intervals chosen in the upper 200 m allowed us to connect Eucalanidae distributions with environmental conditions inside and outside of the CRD. To strengthen our conclusions, we assessed the lipid sac volumes and egg production rates of E. inermis as an indication of the quality of the environment. The lipid sac is involved with many processes such as reproduction, food storage, ontogeny and diapause (Lee et al., 2006). Lipid sac volume measurements and egg production data were limited, but together they suggested that the best environment for E. inermis occurred outside of the CRD near the coast. Based on knowledge that E. inermis feeds in the surface layer (Cass et al., 2014), further work comparing lipid storage by E. inermis across the CRD would provide knowledge of whether selected regions of the CRD are better for providing E. inermis with energy during times of reduced feeding at depth, and whether E. inermis is capable of performing DVM. Other than E. inermis, S. subtenuis was the only other Eucalanidae species in this study that exhibited DVM

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patterns throughout the CRD region, but based on its low abundance it is relatively less clear. In the central CRD and NW of the CRD (Cycles 2 and 3), S. subtenuis performed a small migration to the surface at night, whereas E. inermis remained at a median depth of 45 m. On the basis of S. subtenuis’ swimming abilities and the fact that E. inermis dominated the Eucalanidae community, we suggest that S. subtenuis uses this strategy to compete for food. Prior work has concluded that S. subtenuis is the most active Eucalanoid species (Cass and Daly, 2015), and its fatty acid profiles (storage lipids) are very similar to E. inermis, suggesting that these species may have similar life history strategies (Cass et al., 2014). Our study confirms that these strategies that were previously observed during winter and fall were also present during a summer experiencing reduced upwelling conditions. Copepods demonstrate DVM or OVMs in coastal areas along eastern boundary systems, such as the California, Humboldt, Agulhas and Canary currents. These migrations serve to keep the majority of the population nearshore in waters with typically lower temperatures and higher autotrophic biomass (Batchelder et al., 2002). Observing E. inermis undergoing DVM outside of the CRD (Cycle 5) is particularly interesting since in Cycle 5 larger phytoplankton cells contributed in a major way to carbon biomass and productivity (Landry et al., 2016b; Taylor et al., 2016) and the measured grazing impact of mesozooplankton on the phytoplankton community was also high (De´cima et al., 2016). This implies a potential link between expressed DVM and the availability of appropriate prey resources. However, other factors, such as seasonal changes in hydrography or the presence of a stronger OVM (Carr et al., 2008), must also be involved because mesozooplankton community grazing and the large phytoplankton contribution to production were also high for Cycle 3 (De´cima et al., 2016), where a significant migration was not observed.

Influence of environment and comparison with previous years Although we found no significant relationships among cycle locations and Eucalanidae abundance, the abundances of Eucalanidae species were correlated with sampling depth and temperature. Thermocline depths varied from 30 to 40 m during Cycles 1 and 5 (nearshore outside the CRD) to between 10 and 20 m in the central CRD region (Cycles 3 and 4), potentially resulting in differences in abundances and vertical distributions of species among the cycles (Fig. 3C – E). During the cruise, Chl a values within the upwelling center of the CRD (Cycles 2 and 4) were highest, 0.4 mg L21 (Selph et al., 2016; Taylor et al., 2016). However, direct grazing rates of

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the mesozooplankton community, as assessed by gut fluorescence, were relatively low during these central CRD cycles compared with Cycles 3 and 5, reflecting the greater dominance of primary production by picophytoplankton at the central CRD stations (De´cima et al., 2016). The potential for E. inermis to exert control on the cyanobacteria associated with fluorescence peaks has been suggested by Hidalgo et al. (Hidalgo et al., 2005b). Eucalanus inermis in the central CRD region could be linked to picophytoplankton production via protozoan grazing pathways, allowing E. inermis to take advantage indirectly of the region’s large populations (typically . 106 cells mL21) of the picocyanobacterium, Synechococcus spp. (Stukel et al., 2013). The Eucalanidae abundance within the center of the CRD was compared with previous observations made by Cass and Daly (from 2007 to 2009) to determine whether the reduced upwelling and lower surface Chl a resulted in a change in the abundance of these organisms. We found that E. inermis abundance remained unchanged under these conditions, whereas S. subtenuis and P. attenuatus numbers were greatly reduced. These results indicate that E. inermis may be more resilient in terms of changes in productivity than S. subtenuis and P. attenuatus.

CONCLUSIONS This study characterized the summertime Eucalanidae assemblage during what is presumed to be a reduced upwelling year, with greatly suppressed surface expression of Chl a. The large differences in Eucalanidae abundances between years most likely reflect primary production or community structure effects of the moderate El Nin˜o conditions preceding our cruise. The region outside of the CRD center supported a more diverse assemblage of Eucalanidae compared with the central CRD, suggesting that central CRD conditions might restrict species distributions due to subtle differences in physical – chemical conditions or to relatively low contributions of larger phytoplankton to system productivity. Most notably, this is the first study to investigate differences in Eucalanidae distribution across the CRD region. Inside the CRD, E. inermis dominated the Eucalanidae community composition due to its ability to cope with the shallow thermocline and sharp gradients in temperature, nutrients and dissolved oxygen in the euphotic zone. In contrast, the environment outside of the CRD, near the coast, supported more species of Eucalanidae and allowed for a greater vertical distribution because of food availability and physical –chemical conditions. It was clear that outside of the CRD near the coast was a better environment for almost all of the species analyzed. Overall, from this

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spatial comparison, we found evidence that some Eucalanoid copepods in the CRD adapted their vertical distributions in response to environmental conditions, and these adaptations led, in turn, to variations in horizontal distributions.

AC K N OW L E D G E M E N T S We thank the captain, crew and technicians aboard the R.V. Melville and Chief Scientist M. R. Landry and his students for their help and input. In addition, we thank D. Sorarrain-Pilz for her taxonomic expertise and her time training M.L.J. We greatly appreciate the comments of three anonymous referees.

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