The relationship between zooplankton distribution and hydrography in oceanic waters of the Southern Gulf of Mexico

Journal of Marine Systems 192 (2019) 28–41

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The relationship between zooplankton distribution and hydrography in oceanic waters of the Southern Gulf of Mexico

T

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J. Färber Lordaa, , G. Athiéb, V. Camacho Ibarc, L.W. Daesslec, O. Molinaa a División de Oceanología, Centro de Investigación Científica y de Educación Superior de Ensenada, Carretera Ensenada-Tijuana 3918, Fraccionamiento Playitas, C.P. 22860 Ensenada, Baja California, Mexico b CONACYT - Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Calle Hidalgo 617, Río Jamapa, C.P. 94290 Boca del Río, Veracruz, Mexico c Universidad Autónoma de Baja California, Instituto de Investigaciones Oceanológicas, Carretera Ensenada-Tijuana 3917, Fraccionamiento Playitas, C.P. 22860 Ensenada, Baja California, Mexico

A R T I C LE I N FO

A B S T R A C T

Keywords: Gulf of Mexico Zooplankton Biovolumes Fluorescence Hydrography Bay of Campeche

Zooplankton was sampled in the Southern Gulf of Mexico, during autumn 2010, summer 2011 and winter 2013. Hydrographic data, dynamic topography and geostrophic velocities showed the presence of alternating cyclonic and anticyclonic gyres in the area, and a quasi-permanent gyre in the Bay of Campeche, with higher surface temperatures and lower salinities during autumn and summer, than in winter. Stronger rainfall was present during summer, which coincided with a strong salps “bloom” that considerably increased biovolumes. A significant difference in biovolumes was found for the three seasons, with highest zooplankton biovolumes during summer, and lowest during autumn. A shoaling of higher fluorescence and higher nutrients (Nitrate + Nitrite) was found in the BOC, in coincidence with higher biovolumes during the three seasons sampled. Multivariate analysis showed that the variables controlling the productivity were mainly fluorescence and nutrients for summer 2011 and winter 2013. Higher biovolumes were present in autumn, summer and winter at the same stations, being higher during summer. Data obtained show that the Bay of Campeche is a high productivity area, all year round, particularly inside the quasi-permanent gyre where high biovolumes were present in autumn, summer and winter, but with considerable seasonal variations in primary and secondary productivity, probably dependent in great measure from river discharge and rainfall.

1. Introduction The Gulf of México has been the subject of numerous oceanographic studies, mainly in its northern part, where hypoxic and anoxic conditions are present induced by the discharge of the Mississippi river (Turner and Allen, 1982; Biggs, 1992; Biggs and Sánchez, 1997; Rabalais et al., 2002; Turner, 2001). Among zooplankton studies, Lewis (1954) analyzed the vertical distribution of Euphausiacea in the Florida Current; Michel and Foyo (1976) described Caribbean zooplankton groups including Siphonophora, Heteropoda, Copepoda, Euphausiacea, Chaetognatha, and Salpidae; Hopkins (1982) studied the vertical distribution of zooplankton in the eastern Gulf of Mexico; and Mikkelsen (1987) studied the euphausiids from eastern Florida. Other works in the eastern Gulf of Mexico focused on single species, like the one describing the vertical distribution and feeding ecology of Euchaeta marina (Shuert and Hopkins, 1987); another study focused on the ecology of the genus Pleuromamma (Bennett and Hopkins, 1989), whereas Flock and Hopkins

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(1992) studied the vertical distribution, the species composition and feeding habits of sergestid shrimps, and Passarella and Hopkins (1991) studied the species composition and feeding habits of micronektonic cephalopod assemblages. In contrast to these regions, the hydrographic conditions in the Southern Gulf of Mexico (SGM; south of 25°N) are very different, where hypoxia or anoxia is not observed. In addition, few studies have been conducted on plankton related to hydrographical conditions in the oceanic waters of SGM and in particular in the Bay of Campeche (BOC; the semi-enclosed southern-most sector of the SGM south of 22°N; see Fig. 1), nor on seasonal changes in zooplankton abundance/biomass and its probable relationship with rainfall. The relationships between cool and warm rings and nutrients, and between nutrients, plankton and productivity in the Gulf of Mexico, were described by Biggs et al. (1988); Biggs (1992), and by Linacre et al. (2015) for the southern Gulf of Mexico. Biggs and Muller Karger (1994) also studied productivity, finding that the alternate presence of cyclonic and anticyclonic gyres enhances primary productivity in the

Corresponding author. E-mail address: [email protected] (J. Färber Lorda).

https://doi.org/10.1016/j.jmarsys.2018.12.009 Received 29 March 2018; Received in revised form 11 December 2018; Accepted 20 December 2018 Available online 28 December 2018 0924-7963/ © 2018 Published by Elsevier B.V.

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Fig. 1. Stations sampled during the three cruises; 44 in November 2010, 42 in July 2011 and 20 during February–March 2013.

surface waters during winter and summer, and Castellanos and Gasca (1999) who studied the spring epipelagic euphausiids in relation to mesoscale features. Gasca et al. (2001) studied the summer distribution of euphausiids while Cnidaria were studied by Segura-Puertas and Ordoñez-López (1994) in the bank of Campeche and in the Mexican Caribbean. Suárez-Morales (1992) analyzed the species composition, abundance and zoogeography of pelagic copepods, while Cummings (1988) described the habitat dimension of calanoid copepods in the western gulf. Using a multivariate approach, Herrera-Castillo and Martínez-López (1992), studied the distribution of euphausiids in an anticyclonic gyre of the northwest Gulf of Mexico, but described a

western part of the gulf. Biggs et al. (1997) studied the plankton within the cold-core rings. However for the SGM, zooplankton biomass, its seasonal variability and its relationship with hydrography have not been well studied. In this region, many studies focused on different zooplankton groups. For example, James (1970, 1971) studied the euphausiids, Gasca and Suarez-Morales (1991) studied the siphonophores of the upwelling areas of the Campeche bank, Gasca (1993) analyzed the species and abundance of the siphonophores, and the same author studied the distribution of siphonophores during summer (Gasca, 1999). Other studies were performed on euphausiids of the SGM including Castellanos and Gasca (1996) who studied the euphausiids on 29

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Fig. 2. a). Hydrography of the three cruises (contour lines for temperature, color scale for salinity). A cooler area is always present around the Bay of Campeche; less evident for winter conditions. b). Sea Surface Temperature from satellite data, averaged during the dates of each of the three cruises (contours are every 0.25 °C). Black contours indicate temperature values.

western Caribbean Sea and the southern Gulf of Mexico have faunistic affinities. Lopez-Salgado and Suarez-Morales (1998) studied the copepod communities in surface waters of the Western Gulf of Mexico. For the SGM, Flores-Coto et al. (2009) made a review on the spatial distribution of ichtyoplankton, however their work focused only on the continental shelf. Flores-Coto et al. (2014) analyzed the factors

Pacific species that had not been reported for the Gulf of México. Castellanos and Gasca (1996) studied the distribution of euphausiids in surface waters of the Caribbean Sea for which 11 species were described, and found that the euphausiids dominant species was Stylocheiron carinatum, suggesting that 60% of the gulf fauna is represented by the genera Stylocheiron and Euphausia, and concluded that the 30

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Fig. 2. (continued)

and an inlet from the Lagoon to the sea, considered as fine scale. At the mesoscale level they propose that the circulation patterns of the southern Gulf of Mexico, together with the mixing processes, the continental waters discharges, and oceanic gyres are important factors explaining the distribution patterns of ichthyoplankton the community structure. Flores-Coto et al. (2009) made a compendium of their results in the southern Gulf of Mexico, they separate 4 ichthyoplankton assemblages, oceanic, transitional, neritic and coastal; but no attempt was made to relate their results to hydrography. Zavala-García et al. (2016) found that the continental water discharges and the zooplankton biomass follow a similar pattern in the continental shelf of the Bay of Campeche, on samples obtained during a 17 years period. These studies were, however, mainly directed to the study of fish larvae, with lesser emphasis on zooplankton biomass and its relationship with hydrography; also they were mostly performed over the continental shelf. Zavala-Hidalgo et al. (2006) described the seasonal upwelling on

affecting fish larvae distribution in the southern Gulf of Mexico during spring of 2006, mainly over the continental shelf, and they defined three different assemblages, the Yucatan, the Tabasco-Campeche and the Oceanic assemblages, associated with different hydrographic characteristics. Espinosa-Fuentes and Flores-Coto, (2004) and EspinosaFuentes et al. (2009) described the vertical distribution of zooplankton biomass and ichthyoplankton during an annual cycle between 1994 and 1995 on the continental shelf of the southern Gulf of Mexico, a relationship was found between ichthyoplankton density and zooplankton biomass during all the sampled seasons; the authors assumed that this is related to the seasonal continental discharge cycles (also discussed by Sanvicente-Añorve et al., 1998) and to vertical mixing; the near surface layers showing higher biomasses than the deeper ones. Sanvicente-Añorve et al. (2000) made an analysis of the ichthyoplankton distribution in different scales, from mesoscales for the Bay of Campeche, coarse scales for the adjacent waters of Laguna de Términos 31

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26.0°N

CHLOROPHYLL a 10

24.0°N 5 22.0°N 3 20.0°N

2 NOV 2010 (XIXIMI − 1)

LATITUDE

18.0°N 26.0°N

1 0.6

24.0°N

0.4 22.0°N 0.2

20.0°N JUL 2011 (XIXIMI − 2)

18.0°N 26.0°N

0.1 0.06

24.0°N 0.03

22.0°N

20.0°N

18.0°N 98.0°W

FEB−MAR 2013 (XIXIMI − 3) 95.0°W

92.0°W

0.01 mg/m

3

89.0°W

LONGITUDE Fig. 3. Surface chlorophyll concentration averaged during the dates of each of the three cruises (logarithmic scale in mg m−3) from satellite data. Black contours indicate the 200 m and 1000 m depth isobaths. Higher values are evident during the November 2010 cruise.

(2011) and in deep waters by Kolodziejczyk et al. (2012); they hypothesize that these conditions are produced in part by the U shape of the SGM. In this paper we describe the hydrographic conditions observed in the SGM during three cruises that took place in three different seasons of different years, and relate them to the distribution of zooplankton. Even if this is not properly a seasonal study since sampling took place during different years, we can compare their seasonal signal. So far, no studies of seasonal changes in zooplankton biovolumes have been performed in the area. In addition, an analysis of different physical variables from satellite data, like sea surface height, current patterns, temperature, chlorophyll concentration and precipitation, during a sampling period, but also with long-term seasonal averages, provides valuable information on seasonality. The isolated hydrographic, phytoplankton and primary productivity studies give us a good description of the seasonal changes in the area, and are a good support for our study. The influence of the circulation, nutrient concentrations and environmental factors like rainfall are analyzed, applying multivariate

the western and southern shelves of the Gulf of Mexico. They found persistent Southeast winds in the inner shelf, from May to September, which are favorable for upwelling, but from September to April, the Northern winds present in the area are not favorable for upwelling. In the BOC, Martínez-López and Zavala-Hidalgo (2009) described the along-coast currents that affect the primary productivity. High productivity is caused by along-coast winds, producing a well- defined seasonal cycle of higher cross-shelf transport of waters rich in chlorophyll, in coincidence with higher precipitations and higher river discharges from July to October, increasing the input of nutrients. Coastal flows in opposite directions converge at the southeastern BOC, producing a flow of high chlorophyll towards open-ocean which results in higher primary, and probably also secondary productivity. PérezBrunius et al. (2013) found that cyclonic conditions in the western side of the BOC, previously reported by Vázquez de la Cerda et al. (2005), are quasi-permanent, with seasonal changes of intensity, leading to different circulation velocities within the area. Stronger currents were observed over the continental shelf in the BOC by Dubranna et al. 32

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Fig. 4. Maps of Absolute Dynamic Topography averaged during the dates of each of the three cruises (left panels, contours are every 5 cm) and geostrophic velocities derived from them (velocity scale is indicated at the top panel). Also shown are the average of a 13 years period between 2000 and 2013 (right panels). Faster circulation is evident during the November 2010 cruise. Alternate, and opposite direction gyres are evident in November 2010 and February–March 2013.

first cruise, 6–22 November 2010, CTD data were obtained only to 400 m. Samples for nutrients (NO3 + NO2, PO4, H4SiO4) were collected with 10 L Niskin bottles, filtered on board with pre-combusted (450 °C/ 2 h) filters (Whatman GF/F) and water was stored frozen in 50 mL tubes until analysis. At each station samples were collected at 12 depths, from 10 m to the bottom or from 10 to 1000 m, including from 3 to 6 samples in the upper 150 m. Nutrient analyses were carried out by means of a Skalar SANplus segmented-flow nutrient analyzer by protocols described in Gordon et al. (1993), whereby NO3 + NO2 determination was based on the sulfanilamide and N-1-N-diamine reactions and H4SiO4 determination is based on the molybdic acid reaction described by Armstrong et al. (1967); PO4 determination was based on the molybdic acid and hydrazine reactions as described by Bernhardt and Wilhelms (1967). Analytical precision and accuracy were determined by repeated measurements of intermediate calibration standards and Seawater Certified Reference Material for Nutrients (MOSS-1 or MOSS2; National Research Council, Canada). The integrated NO3 + NO2 concentration in the upper 150 m was estimated by generating a continuous profile based on the 3–6 discrete measurements obtained for this depth range, by interpolation with a spline function followed by integration with the quadl Matlab function. Regarding satellite data, Sea Surface Temperature (SST) data were obtained from the National Oceanic and Atmospheric Administration (NOAA); the product used was the daily Optimum Interpolation Sea Surface Temperature (OISST, Reynolds et al., 2007), which is a gridded product constructed by combining observations from satellites, ships and buoys. The product used was the Advanced Very High Resolution

Table 1 Mean Biovolumes by cruise. Cruise

Mean Bio-volume mL 1000 m−3

XIXIMI 1 November 2010 (including salps) XIXIMI 2 July 2011 (with Salps)

55.17 ± 2.96 (44) 274.28 ± 15.59 (42) 507.81 ± 95.91 (42) 174.11 ± 15.48 (20)

XIXIMI 3 February–March 2013 (without salps)

statistics in order to interpret differences in the seasonal distribution of zooplankton biovolumes. 2. Material and methods Three cruises in the SGM took place: XIXIMI 1 on 6–22 November 2010, XIXIMI 2 on 2–16 July 2011 and XIXIMI 3 on 19 February–10 March 2013. During XIXIMI 1, 44 stations were sampled, 42 during XIXIMI 2 and 20 during XIXIMI 3. The cruises followed the same paths and sequence of stations, except for the XIXIMI 3 cruise during which logistical problems reduced the number of sampled stations (Fig. 1). Zooplankton samples were obtained with a 333 μm size mesh, 60 cm bongo net, with oblique tows from 200 m to surface. Samples were preserved in buffered 5% formalin. Zooplankton biovolumes were obtained by the displaced volume method (Postel et al., 2000), and using the cylinder volume method for the filtered volumes, following the lectures of the previously calibrated flow meters (General Oceanics). At every station a CTD cast was performed from 0 to 500 m. During the 33

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Fig. 5. The biovolumes of zooplankton over the fluorescence at the depth of the 26 isopycnal. For the July 2011 cruise we plot only the bio-volumes values until 400, higher values are the numbers in red, here including salps. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Radiometer (AVHRR), which has 1/4o spatial resolution and is available from 1981 to the present (see Banzon et al., 2016, for more detail). Chlorophyll concentration in seawater was obtained by the Moderate Resolution Imaging Spectroradiometer (MODIS), which is a key sensor aboard the Aqua satellite (http://oceandata.sci.gsfc.nasa. gov). MODIS-Aqua is operated by the Ocean Biology Processing Group (OBPG), which serves as the Distributed Active Archive Center (DAAC), for all Ocean Biology (OB) data produced or collected under NASA's Earth Observing System Data and Information System (EOSDIS). Because of the clouds-free conditions required for the ocean color measurement, which are not common in summer over the Campeche Bank, particularly during the XIXIMI 2 campaign, we decided to use the

8-day average product with a high spatial resolution of 4.6 km in latitude and longitude. Maps of Absolute Dynamic Topography (MADT) and geostrophic velocities derived from them are gridded products distributed by COPERNICUS Ssalto/Duacs multimission altimeter. The product used here is the most recent Delayed-Time mean absolute dynamic topography (DT-MADT, all sat merged), which uses information from up to four satellites at a given time, using all the available altimeter missions (i.e., Topex/Poseidon, Altika, Jason-1 and 2, Envisat, GFO, ERS-1 and 2 and Geosat). Both data sets have 1/4° spatial resolution and are daily available; however these gridded products are interpolations without higher-frequency signals than 7 days, which is the highest time 34

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Fig. 6. Average precipitation rate during the three cruises (left panels, contours are every 1 mm·day−1). Average rainfall for the same seasons and during 13 years period (2000–2013) is also shown (right panels). Higher values are evident in July 2011 and in the 13 years average for the same month.

3. Results

resolution resolved by these satellites. Statistical analyses of the obtained data included comparison of means and regression analysis performed with the Sigmaplot program, and factor analysis performed with the program Statistica, for which ten variables were included. Due to the fact that sampling for nutrients did not include a 500 m depth, nutrient sections were plotted only to 400 m, while data obtained with CTD were plotted from 0 to 500 m. Daily precipitation rate data were obtained from the North American Regional Reanalysis (NARR, http://www.esrl.noaa.gov/psd) Project, an extension of the NCEP Global reanalysis, which is run over the North American Region. This data, with spatial resolution of 1/3° in latitude and longitude, is a combination of the very high resolution NCEP Eta Model together with the Regional Data Assimilation System, which significantly assimilates precipitation along with other variables. NCEP Reanalysis data was provided by the NOAA/OAR/ESRL PSD, Boulder, Colorado, USA. OISST data were provided by the NOAA-NCEI National Centers for Environmental Information and acquired from: https://www.ncdc.noaa.gov/oisst. The Ocean color data (ID doi: https://doi.org/10.5067/AQUA/MODIS_OC.2014.0) provided by the NASA is supported by the Ocean Biology Processing Group at NASA's Goddard Space Flight Center (2014): MODIS-Aqua sensor, Ocean-Color Data, NASA OB.DAAC, https://doi.org/10.5067/AQUA/MODIS_OC. 2014.0. Accessed on 07/28/2015.

The hydrography of the SGM shows a cooling around the BOC (particularly near stations 40, 41 and 46), with also lower salinities during summer and autumn, but not during winter, with seasonal variations (Fig. 2a). A similar pattern is observed with the SST from satellite data averaged over the period of cruises, which vary from 25° to 27 °C in autumn 2010; from 27° to 30 °C in summer 2011 and from 22° to 25 °C in winter 2013 (Fig. 2b). Interestingly, for both XIXIMI 2 and XIXIMI 3 cruises, the thermocline was almost absent, but in certain stations we did find very low temperatures (e.g., like stations 40, 41 and 46). During winter (February–March), temperatures show a different pattern, with greater cooling in the northern part of the study area and higher temperatures in the BOC; also a sharp front north off the Yucatan peninsula is observed, associated with the Loop current coming from the Caribbean in the eastern Gulf of México. Chlorophyll satellite images show higher values in the BOC on the continental shelf, especially during autumn (November; Fig. 3). The quasi-permanent (meaning that this kind of circulation pattern is not always present) cyclonic gyre is present in the most southwestern part of the BOC (Fig. 4), as previously shown by Pérez-Brunius et al. (2013). MADT together with the geostrophic circulation of the area (Fig. 4) show the alternation of cyclonic and anticyclonic gyres along the continental shelf at the BOC. This alternation promotes the transport of coastal 35

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Fig. 7. (a) The 95°W, north-south transect for the three cruises. We plotted the fluorescence with the bio-volumes and the station number. Higher values of zooplankton are coincidental with higher fluorescence. (b) The 21°N, east-west transect for the three cruises. Again we plotted the fluorescence with the bio-volumes and the station number. The same trend is evident on the same area as Fig. 7a. The position of the 95°W transect is shown.

abundance was 5.84-fold greater (2197 ± 3234 for summer and 375 ± 338, for autumn); no salps were found in winter 2013. There was a significant difference between the biovolumes of the three cruises (Kruskal-Wallis: H2105 = 80.155, P < 0.001) without salps. As shown in Fig. 6, rainfall was higher during summer, intermediate during autumn and lower during winter, similar to the trend of the 13-year period average. For the biovolumes, no-significant differences between day and night were found for the three cruises (XIXIMIM1, November 2010: H241 = 0.031, P = 0.86. XIXIMI 2, July 2011: H239 = 0.005, P = 0.944, without macrozooplankton. H239 = 0.125, P = 0.723, with macrozooplankton. XIXIMI 3 F219 = 0.388 P = 0.542). The isopycnals of a north to south transect at 95° W, and for a west east transect at 21°N, were plotted for each cruise, including fluorescence and the biovolumes (Fig. 7a and b). A rise of the isopycnals was present in the BOC, corresponding to the quasi-permanent gyre, in coincidence with higher zooplankton biovolumes and shallower higher fluorescence values. Nutrients, especially nitrate + nitrite, also showed a similar trend as for the isopycnals for both transects (see Fig. 8 and b). A multivariate analysis was performed for data of the summer 2011 and winter 2013 cruises only, because physical data for the autumn cruise were not complete. The first two factors explained 64.2% of the variance (Fig. 9). The first factor is positively correlated with the three variables included for fluorescence, maximum of Fluorescence (F Max), and the mean fluorescence of the first 50 and 120 m (F50 and F120), being F120 the variable with the highest correlation. The second factor is negatively correlated with the data for the depth of the 26 isopycnal, the mean temperature of the first 300 m, and positively correlated with nutrient concentrations integrated for the first 150 m (see Table 2). Fig. 9 shows that all stations with higher biovolumes are grouped near the above mentioned positively correlated variables and opposed to the

waters from the continental shelf to the open ocean (particularly in autumn along 95°W and in winter at 94°W) and also favors the transport in the opposite direction, (i.e. towards the continental shelf). The mean geostrophic circulation for 13 years shows similar trends (Fig. 4), mainly for the gyre in the BOC. The quasi-permanent cyclonic gyre is present in the southwestern part of the BOC, with higher intensity in winter and autumn. In summer however, it is still observed but with much less intensity but not in the average pattern (2000−2013), suggesting that the cyclonic gyre is not the dominant feature of the dynamics in summer (July). Higher values of biovolumes were defined as those higher than the mean biovolumes for each cruise, including the positive standard error (Table 1). Higher biovolumes coincided with the quasi-permanent gyre in the BOC, during the three sampling seasons (Fig. 5). It's interesting to note that the autumn cruise showed a smaller standard error, than the other two cruises; 28 stations showed biovolumes above the mean for the autumn cruise, whereas for the other two cruises only 10 stations were above the mean, which is probably signalling more uniform trophic conditions. However, during summer, after strong rainfall, higher biovolumes were present, with a large increase of salps, which, due to their size, considerably increased the biovolumes. Even without salps, the biovolumes of the remaining zooplankton groups were much higher than in winter and autumn (Fig. 5, includes salps). From autumn to summer the mean zooplankton biovolumes increased 4.97 times when salps were removed from the comparison, and 9.20 times if salps were included. Differences were smaller between summer and winter, with mean biovolumes being 1.57 times higher in summer without salps, and 2.90 higher including salps (Table 1). There was a significant difference between the abundances of salps for summer and autumn (Kruskal-Wallis, H = 24.73 P ≤0.001 D.F. = 43); salps mean summer 36

Fig. 8. (a) Nutrients (Nitrates + Nitrites) for the N-S transect at 95°W, for the three cruises. (b) Nutrients (Nitrates + Nitrites) for E-W transect at 21°N for the three cruises; station 38 corresponds to the position of the 95°W transect. The same trend as for the fluorescence with biovolume data is present.

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3

Mutltivariate Analysis Summer 2011 and Winter 2013 40.3

Summer 2011 Gyre

2

37.2 46.2 45.2 40.2 39.2

Winter 2013 Gyre 37.3

38.2 41.2 41.3 35.3 1.3 46.3 42.31.2 Nut 42.2 32.3 36.3 47.3 39.3 Bv 47.2 F 120 F Max 31.3 43.3 44.3 T Ab.F 50 38.3 3.25 3B.3 7.3 20.2 4.2 5.2 7.2 32.2 15.2 2.2 43.2 4.3 3.344.2 33.2 19.2 21.2 16.2 D5.3 F Max 18.2 12.2 8.2T 50 3.2 D10.2 26 T T17.2 300 22.2

Factor 2

1

0

-1

11.2

36.2

30.2

31.2

27.2 25.2

-2

23.2 24.2 -3

-2

-1

0

1

2

3

Factor 1

4

5

6

Factor

Fig. 9. Multivariate analysis of the summer 2011 and winter 2013 cruises. Squares are the variables and dots the stations per cruise (2 Summer 2011, 3 winter 2013) Bv: Biovolume. Tab: Total zooplankton abundance. F50: Mean fluorescence for the first 50 m. F120: Mean Fluorescence for the first 120 m. FMax Fluorescence maxima per station. T 50: Mean temperature of the first 50 m. T 300: Mean temperature for the first 300 m. D FMax: Depth of the Flourescence maximum. D 26 T: Depth of the 26 °C. Nut: average nutrients for the first 150 m.

negatively correlated variables (26 isopycnal, and the mean 300 m temperature) of the second factor, and the positively correlated integrated nutrients of the first 150 m, of the second factor also; as well as near to the total abundance variable (TAb). The biovolumes (Bv) variable is found near all these positively correlated variables of the first factor, it is thus assumed that fluorescence is the main factor controlling these conditions and, that at the same time, these conditions are given at lower temperature and higher nutrient contents. Two groups are well defined in our analysis: one corresponds to summer conditions in the BOC and the other to winter conditions. The separation of these two groups is derived from the different seasonal conditions, which are important in water temperature and biovolumes. As was explained above, biovolumes were considerably greater in summer than in winter, but stations with higher biovolumes (Fig. 6) are practically the same under similar physical conditions for both seasons. Some stations of both summer and winter cruises are overlapped (Fig. 9), but mostly clearly separated. Coincidental stations, i.e. stations that were present in both winter and summer in their respective summer and winter groups of Fig. 9, are characterized by high biovolumes. Even though a smaller number of stations were sampled in

Table 2 Variables contributions. Variable

Factor 1

Factor 2

1. 2. 3. 4. 5. 6.

−0.458600 −0.349552 0.906970 0.252528 0.127223 −0.253284

−0.551967 −0.841898 0.235062 0.435343 −0.648871 −0.915480

0.831244 0.913443

0.139406 0.314804

0.427958

0.723618

Depth Fluorescence Maximum F Max Depth 26 density D26T Fluorescence Maximum F Max Biovolume Bv Mean Temperature of the first 50 m T50 Mean Temperature of the first 300 m T300 7. Mean Fluorescence of the first 50 m F50 8. Mean Fluorescence of the first 120 m F120 9. Integrated Nutrients Nitrates + Nitrites for the first 150 m Nut 10. Total Abundance TAb Explained variability Proportion total

0.473961 0.179362 3.232335 3.191705 0.323233 0.319170 Total first two factors: 64.24040%

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a)

then, after that, higher fluorescence did not result in higher biovolumes.

Ln Biovolume vs.Fluorescence Max. XIXIMI 2 and 3

Fluorescence Maximum

1.2

4. Discussion There is a quasi-permanent mesoscale cyclonic gyre in the SGM, located in the BOC, with smaller eddies that favor the upwelling and the offshore transport of water. This produces seasonal bursts of phytoplankton and a subsequent intensification of secondary productivity, but with large seasonal variability. The thermocline is almost absent in most of the areas and during the three cruises. At certain stations we do find particularly low temperatures like at stations 40, 41 and 46 of both XIXIMI 2 and 3 cruises, in coincidence with high biovolumes. There is clear indication that the BOC is a quasi-permanent high productivity area in the SGM as indicated by our data for the three seasons sampled (autumn, summer and winter). The quasi-permanent cyclonic gyre is present in the southwestern part of the BOC (south of 21°N and west of 94°W), as previously shown by Pérez-Brunius et al. (2013), with higher intensity in winter and autumn. In summer the gyre is still observed in our study (July 2011), even though with lesser intensity (actually, this feature has almost no signal in the 13-years average of MADT and geostrophic currents). The occurrence of higher biovolumes in correspondence to shallower isopycnals, higher nutrients concentrations in the upper water layer and higher fluorescence values, is a clear indication that the BOC is an area of higher productivity all year round. Also, it shows considerable seasonal changes, being higher during autumn, probably due to the terrigenous input from the river discharges in the area. Grazing by zooplankton is probably producing reduced chlorophyll values during summer when higher zooplankton biovolumes were found, especially considering the presence of a “bloom” of salps, a voracious group of organisms that feed on a very wide range of different sized particles. The higher productivity in the BOC and its large seasonal variability observed in our study, as well as for the riverine discharge characterized by a strong seasonal signal corresponding to greater rainfall during summer and part of autumn, is consistent with reports from previous studies in the region (Martínez-López and Zavala-Hidalgo, 2009). This signal is also evident from the biovolumes, producing during summer a salps bloom with 9.2 times the biovolumes compared to autumn. Not all the former studies of zooplankton distribution in the area analyzed its relationship with hydrography data, thus only few comparisons with our study are possible. Flores-Coto et al. (2009) found that zooplankton biomass over the continental shelf is greater in summer than in winter, but their study area does not coincide with our area, and they did not analyse directly the relationship with hydrography. Our sampling did not coincide with the highest river discharge season, shown by Martínez-López and Zavala-Hidalgo (2009) to be from July to October for the Papaloapan-Coatzacoalcos Rivers, but coincided with the beginning and the end of that period. However, these authors found that primary productivity was higher in the area with higher cross-shelf chlorophyll in the BOC, in November. However, Zavala-García et al. (2016) analyzed the seasonal river discharge changes, in relation to zooplankton biomasses, for 5 different shelf areas, and found a coincidence of both variables. This relationship was more evident in the two areas south of the BOC study area, which supports the hypothesis of the possible influence of the river discharge, on the higher zooplankton biomass during the rainy season. As explained above, the offshore current resulting from the colliding coastal currents in this area (Martínez-López and Zavala-Hidalgo, 2009) is probably transporting coastal waters towards open ocean, thus increasing the productivity of the deep-waters studied. In the present work a strong seasonal signal was identified. Stronger currents were found in the continental shelf of the BOC by Dubranna et al. (2011), who hypothesized that this was due, in part, to the U shape of the Gulf of México, which helps in the formation of two along-shore coastal currents of opposing direction. This is a condition that was also observed by Pérez-Brunius et al.

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Ln(Biovolume) vs Fluo. Mx XIXIMI 2 (Summer) Ln(Biovolume) vs Fluo. Mx XIXIMI 3 ( Winter) Fig. 10. (a) Ln Biovolume vs. Fluorescence maxima for each stations and for the summer and winter cruises. (b) Ln Biovolume vs. Fluorescence maxima for the station with higher biovolumes of zooplankton.

winter compared to summer, as indicated above, 8 out of the 12 stations in the winter group of Fig. 9 with high biovolumes coincided with stations sampled in summer (Sts. 36, 37, 38, 39, 40, 41, 42 and 46), and only two stations did not coincide (Sts. 5 and 45 for summer, but St. 45 was not sampled in winter), whereas Sts. 47 and 3B showed high biovolumes in winter, but not in summer. The regression (non-significant) between fluorescence maxima and the Ln of biovolumes for both summer and winter shows a similar trend (Fig. 10a). We also used only the higher zooplankton biovolumes (Fig. 10b), those found grouped in the multivariate analysis; with the fluorescence maxima, both figures show that there is a peak at intermediate values of fluorescence, and 39

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5. Conclusion

(2013), who showed that cyclonic wind-stress curl produces a quasipermanent condition of circulation, which is maintained by the topographic characteristics of the basin. As shown by Zavala-Hidalgo et al. (2006), a large chlorophyll-a content is present along the inner shelf of the eastern Campeche Bank, from May to September, which, with the aid of the circulation described by Dubranna et al. (2011) in the BOC, may be influencing the higher biovolumes found during July 2011. Our multivariate analysis defines two areas with high biovolumes, which are both inside the quasi-permanent gyre, one for summer and one for winter. The circulation of water masses was similar in both seasons, with the same stations showing higher biovolumes. However, the intensity is different, which is shown by the separation of these two groups of stations for the seasons analyzed, in two different years. During winter, station 40 showed significant lower temperatures. This station is separated from the groups of stations along the same first factor axis. Our multivariate analysis shows that for both seasons studied, the same conditions are giving higher zooplankton concentrations in and around the same area, proof of a quasi-permanent higher productivity area inside the gyre. Also, for summer and winter, a regression between fluorescence maxima and Ln of biovolume shows a relationship (not significant) between them. However, above a certain level (around 0.6 mg m−3), fluorescence apparently does not have any influence on biovolumes (Fig. 10a and b). An outlier of fluorescence was found, which affected this regression, but did not reflect higher biovolumes. Precipitation is apparently playing a major role in the higher productivity of the region, especially during summer. Higher rainfall is evident during the summer sampling period (Fig. 6), which is supported by a longer-term trend of these conditions showing the same profile, and the consequent increased input of nutrients in the continental shelf, especially in the BOC. A core of low temperature and salinity was observed near the coast (~96°W, ~20°N, Figs. 2 and 3), which was not clearly associated with a pattern of intense cyclonic circulation (Fig. 4). Chlorophyll also shows higher values around the area, but especially on the continental shelf (Fig. 3), which is likely related to the along-coast wind-forced currents which produce a flux of nutrient-rich waters towards the open-ocean to the north, enhancing primary and secondary productivity (see Martínez-López and Zavala-Hidalgo, 2009: ZavalaHidalgo et al., 2006). Higher zooplankton biovolumes coincide with the higher fluorescence observed at the 26 kg/m3 isopycnal, as shown in Fig. 7a and b, for the three cruises, and for winter and summer cruises in the multivariate analysis (Fig. 9). Slight differences in chlorophyll were found between the cruises (Fig. 3); during autumn (November 2010), the higher productivity area is slightly displaced to the north, whereas in summer and winter higher values were closer to the continental shelf. This may be due to the presence of a cyclonic/anticyclonic pair of eddies located near 95°W that favor the cross-shelf water transport (Fig. 4). Also, the considerably greater biovolumes during summer are probably the consequence of larger nutrient input from the rivers that discharge in the area (Martínez-López and Zavala-Hidalgo, 2009; Zavala-Hidalgo et al., 2006). An interesting feature of the area is also the alternate presence of cyclonic and anticyclonic gyres, as described by Pérez-Brunius et al. (2013), and confirmed here in the mesoscale circulation features of the area (MADT in Fig. 4), in which higher velocities in the BOC are observed during autumn and winter than during summer. Further analysis of the mesoscale circulation features of the area helped us to better understand their relationship with other variables, like fluorescence. Nutrients (Nitrate + Nitrite), showed a shoaling of higher values in the BOC (See Fig. 8a and b), a good indicator of favorable conditions and the higher productivity that followed. Multivariate analyses showed that for summer and winter, the same stations with the same positions sampled had higher zooplankton biovolumes, thus confirming the quasi-permanent presence of the higher productivity gyre in the BOC, at least for these two seasons.

The BOC is a permanent high productivity area, supported by larger velocities during winter and autumn, but lower during summer. Higher summer productivity is apparently supported by higher riverine input, derived from heavy rainfall in the southern part of the BOC. Multivariate analysis confirms that the same area has higher productivity during summer and winter. The presence of anticyclonic and cyclonic gyres in the BOC helps in the dissemination of nutrient-rich waters towards the open ocean, increasing their productivity: primary productivity first (during November), followed by higher secondary productivity during summer, supported by the greater input of nutrients from rainfall in the area around the BOC. Acknowledgements We want to thank Dr. Julio Sheinbaum Pardo (CICESE), for providing the hydrographic data. To Esperanza Alvarez and José Luis Cadena for biovolumes determinations. Ignacio Romero VargasMárquez and Cesar Almeda (CICESE) helped with some of the figures. We also want to thank two anonymous reviewers, for their valuable work. Eduardo Ortiz Campos for nutrient analyses. This study was supported by the project “Environmental monitoring of the baseline conditions in the deep waters of the Gulf of Mexico in response to the Deepwater Horizon platform oil spill”, in collaborative agreement among Government Mexican Institutions (INECC, SEMARNAT, CONABIO) and the Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE). NOAA_OI_SST_V2 data were provided by the NOAA/OAR/ESRL PSD, Boulder, Colorado, USA, from their Web site at https://www.esrl.noaa.gov/psd/. MADT data was distributed by Copernicus Emergency Management Service (European Union, 2012–2018). Chlorophyll data were provided by NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group; (2014): Sea-viewing Wide Field-of-view Sensor (SeaWiFS) Ocean Color Data, NASA OB.DAAC. https://doi.org/10.5067/ORBVIEW-2/SEAWIFS_OC. 2014.0. References Armstrong, F.A., Stearns, C.R., Strickland, J.D., 1967. The measurement of upwelling and subsequent biological processes by means of the Technicon AutoAnalyzer and associated equipment. Deep-Sea Res. 14, 381–389. Banzon, V., Smith, T.M., Chin, T.M., Liu, C., Hankins, W., 2016. A long-term record of blended satellite and in situ sea-surface temperature for climate monitoring, modeling and environmental studies. Earth Syst. Sci. Data 8, 165–176. https://doi.org/ 10.5194/essd-8-165-2016. Bennett, J.L., Hopkins, T.L., 1989. Aspects of the ecology of the calanoid copepod genus Pleuromamma in the eastern Gulf of Mexico. Contr. Mar. Sci. Univ. Tex. 31, 119–136. Bernhardt, H., Wilhelms, A., 1967. 1967. The continuous determination of low level iron, soluble phosphate and total phosphate with the AutoAnalyzer. Technicon Symp. I, 386. Biggs, D.C., 1992. Nutrients, plankton and productivity in a warm/core ring in the western Gulf of México. J. Geophys. Res. 97 (C2), 2143–2154. Biggs, D.C., Muller Karger, F.E., 1994. Ship and satellite observations of chlorophyll stocks in interacting cyclone-anticyclone eddy pairs in the western Gulf of Mexico. J. Geophys. Res. 99, 7371–7384. Biggs, D.C., Sánchez, L.L., 1997. Nutrient-enhanced primary productivity of the TexasLouisiana continental shelf. J. Mar. Syst. 11, 237–247. Biggs, D.C., Vastano, A.C., Ossinger, R.A., Gil-Zurita, Pérez-Franco A., 1988. Multidisciplinary study of warm and cold-core rings in the Gulf of Mexico. Mem. Soc. Cienc. Nat. La Salle, Venezuela 48 (3), 12–31. Biggs, D.C., Zimmerman, R.A., Gasca, R., Suárez-Morales, E., Castellanos, I., Leben, R.R., 1997. Note on plankton and cold-core rings in the Gulf of Mexico. Fish. Bull. 95, 369–375. Castellanos, I., Gasca, R., 1996. Eufásidos (Crustacea: Euphausiacea) de aguas superficiales del sur del Golfo de México (invierno y verano, 1991). Caribb. J. Sci. 32, 187–194. Castellanos, I., Gasca, R., 1999. Epipelagic euphausiids (Euphausiacea) and spring mesoscale features in the Gulf of México. Crustaceana 72, 391–404. Cummings, J., 1988. Habitat dimensions of calanoid copepods in the western Gulf of Mexico. J. Mar. Res. 42, 163–188. Dubranna, J., Pérez-Brunius, P., López, M., Candela, J., 2011. Circulation over the continental shelf of the western and southwestern Gulf of Mexico. J. Geophys. Res. 116, C08009. https://doi.org/10.1029/2011JC007007.

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