Larval fish assemblages of myctophids in the deep water region of the southern Gulf of Mexico linked to oceanographic conditions

Deep–Sea Research I 155 (2020) 103181

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Larval fish assemblages of myctophids in the deep water region of the southern Gulf of Mexico linked to oceanographic conditions Gonzalo Daud�en-Bengoa a, Sylvia Patricia Adelheid Jim�enez-Rosenberg b, Jesus C. Compaire a, Laura del Pilar Echeverri-García a, Paula P�erez-Brunius c, Sharon Z. Herzka a, * a b c

Departamento de Oceanografía Biol� ogica, Centro de Investigaci� on Científica y de Educaci� on Superior de Ensenada (CICESE), Ensenada, Baja California, Mexico Instituto Polit�ecnico Nacional–CICIMAR, La Paz, Baja California Sur, Mexico Departmento de Oceanografía Física, Centro de Investigaci� on Científica y de Educaci� on Superior de Ensenada (CICESE), Ensenada, Baja California, Mexico

A R T I C L E I N F O

A B S T R A C T

Keywords: Myctophidae Gulf of Mexico Fish larvae Larval transport Assemblage

In the Gulf of Mexico, the distribution of larval fish assemblages have been linked to continental shelf vs oceanic habitats and mesoscale structures such as cyclonic and anticyclonic eddies. Myctophids have a worldwide dis­ tribution and are one of the mesopelagic fish families with higher biomass, thus playing a key role in the trophic structure of oceanic communities. However, studies focused on their larval ecology and distribution within the gulf are limited. This study evaluated whether the formation of myctophid larval assemblages can be linked to local adult population spawning patterns and/or oceanographic conditions and surface transport. Ichthyo­ plankton samples were collected in August–September 2015 using standard bongo net tows. Stations extended throughout Mexico’s Exclusive Economic Zone (19� N–25� N) deep water region, including the Yucatan Channel. Myctophid comprised 24.6% of the standardized total larval abundance and were present at all stations. Two dominant assemblages (out of six identified with a Bray–Curtis dissimilarity analysis) were found in stations of the central gulf and the Bay of Campeche. The high proportion of preflexion larvae coupled with differences in hydrographic parameters and surface circulation between the central gulf and the Bay of Campeche, indicated that local adult fish populations and their spawning patterns likely contribute more to the formation of these assemblages than oceanographic conditions and surface transport. Stations from the northern Yucatan Peninsula located within the region of influence of the Loop Current shared a common assemblage, which may reflect biogeographic differences in the myctophid species composition between the northern Caribbean and western gulf. These results highlight the importance of adult distribution and local spawning, providing insight into biogeographic patterns during the early life stages of mesopelagic fishes in the Gulf of Mexico.

1. Introduction Knowledge of the relationship between spatial and temporal varia­ tions in taxonomic composition, abundance and distribution of fish larvae is essential to understand the processes that influence the struc­ ture of larval fish assemblages (Doyle et al., 1993; Kingsford, 1993). Larval fish assemblages are defined as a group of taxa present at a spe­ cific place and time (Flores-Coto et al., 2009; Lindo-Atichati et al., 2012; Sanvicente-A~ norve et al., 1998) influenced by biotic and abiotic factors. Among them, the most important are the spatiotemporal overlap of larvae due to simultaneous spawning of species (Laprise and Pepin, 1995), the aggregation of eggs and larvae resulting from oceanic cir­ culation processes (Bakun, 2006; Richards et al., 1993), and the

presence of food availability and suitable environmental conditions for growth and survival (Fuiman and Magurran, 1994; Mackenzie and Kiørboe, 2000). Larval fish assemblages studies allow for the definition of biogeographical provinces, habitat boundaries, inferring connectivity as well as proving baseline information for evaluating environmental and anthropogenic impacts (e. g. coastal freshwater transport to offshore regions, storms or oil spills). The circulation patterns and productivity of the southern Gulf of Mexico (hereafter GoM; south of 25� N) are strongly related to mesoscale oceanographic features of which the Loop Current (LC) is predominant. The LC enters the gulf through the Yucatan Channel and exits through �r, 2010). In the gulf, the LC extends into the the Florida Strait (Flo northern gulf with varying degrees of intrusion, and every 6–11 months

* Corresponding author. E-mail address: [email protected] (S.Z. Herzka). https://doi.org/10.1016/j.dsr.2019.103181 Received 12 June 2019; Received in revised form 7 October 2019; Accepted 22 November 2019 Available online 27 November 2019 0967-0637/© 2019 Elsevier Ltd. All rights reserved.

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anticyclonic eddies break off periodically (Sturges and Leben, 2000) travelling towards the western gulf on a time scale of months, and eventually interacting with the continental shelf until their energy dis­ sipates (Dubranna et al., 2011). This influences the pelagic habitat where fishes spawn (Rooker et al., 2012; Teo and Block, 2010). The GoM is also characterized by the presence of a semipermanent cyclonic eddy in the Bay of Campeche (P� erez-Brunius et al., 2013), and other meso­ scale cyclonic and non-LC anticyclonic eddies that also affect circulation �mez and Salas de Leo �n, 1990; and productivity (Monreal-Go P�erez-Brunius et al., 2013). Kinetic energy (KE) is calculated from 2–D velocity fields and can be used to measure the intensity of mesoscale oceanographic features that can retain, disperse or transport larvae, and therefore can define the assemblages. Areas with higher KE (such as those found in the Yucatan Channel due to LC, and the vicinity of eddies in the central GoM) can play an important role in larval transport in the epipelagic region. Lower KE regions (such as the southern GoM) �zquez de la Cerda et al., 2005; Weatherly et al., (DiMarco et al., 2005; Va 2013); may have lesser dispersive or retentive potential and hence larvae might remain closer to adult spawning regions. Previous studies in the deep water region of the GoM have indicated that the presence of distinct larval assemblages of mesopelagic fishes can be linked to oceanographic features (Espinosa-Fuentes and Flores-Coto, 2004; Sanvicente-A~ norve et al., 2000). However, adult distribution and spawning habitats are a conditioning factor in the structure of the distinct larval assemblages (Flores-Coto et al., 2014; Richards et al., ~ orve et al., 1998), but there is very limited infor­ 1993; Sanvicente-An mation regarding the adults in the central and southern gulf. The Myctophidae (lantern fishes) is one of the families with higher biomass among mesopelagic fishes in the world oceans, comprising ~75% of the oceanic fish biomass (Catul et al., 2011; Richards, 2006; Sassa et al., 2004). The family’s high diversity and worldwide distri­ bution allows myctophid to be used as biogeographic indicators and tracers of oceanographic processes (De Macedo-Soares et al., 2014). Most Myctophidae species display continuous reproduction. Neverthe­ less, some species present spring-summer spawning peaks (Brandt, 1981; Gartner et al., 1989; Richards, 2006). Myctophids spawn in mesopelagic waters (800–1200 m), and eggs are fertilized as they rise to the surface; their positive buoyancy is attributable to the presence of oil globules (Marshall, 1979; Sundby and Kristiansen, 2015). Early devel­ opment occurs during this rise toward the surface, and hatching takes place at ca. 2 mm standard length (SL). Larvae develop in epipelagic waters (0–200 m) (Conley and Gartner, 2009; Sassa et al., 2004). Pre­ flexion lasts ~5 days, and larval stage ~50 days (Gartner, 1993; Land­ aeta et al., 2015). During transformation to juvenile larval size is between 9 and 23 mm SL (Moser et al., 1982). Larvae as well as adults are zooplanktivorous (Bernal et al., 2013; Conley and Hopkins, 2004; Sassa et al., 2004; Sassa and Kawaguchi, 2005). Adults perform diel vertical migrations from mesopelagic to epipelagic waters to feed due to the higher zooplankton biomass (Dalpadado and Gjøsæter, 1988; Gart­ ner, 1993; Hopkins and Baird, 1985). Studies focused on larval fish assemblages which include myctophids have been undertaken worldwide (De Macedo-Soares et al., 2014; �, 1992; Zarrad et al., 2013). Although there is a Sabat�es and Maso number of prior studies including myctophid larvae in the northern GoM (Lindo-Atichati et al., 2012; Muhling et al., 2013), those conducted in the south are more limited and have not examined the physical and biological processes underlying the formation of myctophid larval as­ semblages. Given the paucity of adult biomass surveys of myctophid species in Mexican waters, evaluating larval abundance and distribution is one way of making inferences about adult populations. The aim of the present study was to characterize the structure of the Myctophidae family larval assemblages in the southern GoM relative to adult spawning and surface circulation. Owing to the wide spatial dis­ tribution of myctophid adults in the deep water region of the GoM, similarities in ontogeny, rapid larval development relative to the pro­ longed temporal scale of mesoscale structures such as LC eddies, and the

weak connectivity among regions of the GoM that has been proposed based on drifter studies for the region (Miron et al., 2017), we hypoth­ esized that the myctophid larval assemblages will mainly reflect adult spawning areas rather than surface transport. 2. Materials and methods 2.1. Study area Several studies define the GoM in regions based on its oceanographic features (e.g. LC and non-LC eddies) and biogeochemical properties. This features may constrain the distribution of water and its attributes, leading to a regionalization. Muller-Karger et al. (2015) characterized the surface waters of the deep water region (depths > 1000 m) of the GoM using a decadal time series of various surface ocean parameters, such as sea surface temperature, mixed layer depth (MLD), surface chlorophyll a concentration and net primary production estimates, and found differences among the northern, southern, eastern and western deep water regions. Higher sea surface temperatures and shallower MLD were found in the southeastern GoM compared with the western and northeast GoM. MLD was shallower in summer due to a weaker wind regime and higher temperatures; conversely a deeper mixed layer favored nutrient inputs into the euphotic zone and sustains higher productivity during the winter, with ecological implications for higher trophic level organisms (Muller-Karger et al., 2015). Damien et al. (2018) used a validated coupled circulation-biogeochemical numerical model to characterize the gulf-wide seasonal primary production and phytoplankton biomass. They proposed that the gulf can be divided into regions (southern, central and northern) that likely vary in regional productivity based on the winter chlorophyll concentration. Miron et al. (2017) used satellite–tracked surface drifters to examine the level of potential connectivity between regions, and indicated that the GoM can be divided into specific weakly interacting provinces over the time scale of a few months, namely the Bay of Campeche, the western and eastern GoM, including the Yucatan Peninsula and channel. These suggest regional differences in oceanographic conditions and dominant circu­ lation patterns, that likely have implications for assemblages structure. Therefore, sampling stations were grouped based on this regionalization (central GoM, Bay of Campeche and Yucatan Channel). 2.2. Sampling design Samples were collected during the XIXIMI–04 research cruise held on board the R/V Justo Sierra in late summer (August 27–September 16) of 2015 (Fig. 1). The overall goal of the XIXIMI–04 cruise was to establish baseline conditions of hydrographic, biogeochemical and ecological parameters in the Gulf of Mexico’s deep water region, and was not focused exclusively on the characterization of myctophids. Since it was held during the summer, results must be interpreted considering spawning seasonality. All stations were located in the deep water region (depths > 1000 m) of the GoM’s Mexican EEZ as well as in the Yucatan Channel (18� N–25� N, 82� W–95� W). A total of 54 stations located 75100 km apart were sampled in the central gulf (22� N–25� N, 87� W–97� W), in the Bay of Campeche (20� N–22� N, 92� W–97� W) and in the western Yucatan Channel (22� N, 87� W–86� W). Yucatan Channel stations were sampled twice. During the cruise, an anticyclonic eddy (Olympus) had recently de­ tached from the LC, and the remnant of a second anticyclonic eddy (Nautilus II) was also observed (Fig. 1). This second eddy formed in May 2015 (http://www.horizonmarine.com/loop-current-eddies.html). Zooplankton samples were collected with oblique tows from the surface to a depth of 200 m using a bongo net sampler (60 cm diameter, 335 μm mesh size). Each net was equipped with Sea–Gear Corporation model MF315 flowmeters to estimate filtration volumes. Samples were immediately preserved in 96% ethanol. Ichthyoplankton sampling using plankton nets does not require a permit for Mexican institutions working 2

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Fig. 1. Upper panel: Sampling stations during the XIXIMI-04 research cruise (August 27–September 16). Dashed and continuous lines represent the 200 m and the 1000 m isobath respectively. Central GoM (triangles), Bay of Campeche (squares), Yucatan Channel (dots). Lower panel: Olympus and Nautilus II anticyclonic eddies represented by sea surface height (SSH). Central GoM (triangles), Bay of Campeche (squares) and Yucatan Channel (dots).

3

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in Mexican waters. Zooplankton biomass was estimated as zooplankton biovolumes obtained using the displaced volume method (Postel et al., 2000). The later was used as a secondary productivity proxy (De Macedo-Soares et al., 2014; H�ebert et al., 2017; Somarakis et al., 2000). Ichthyoplankton samples were later sorted in the laboratory and myc­ tophid larvae were identified to the lowest possible taxa according to morphometric and meristic characteristics (Fahay, 2007; Richards, 2006). The main criteria for discriminating between Diaphus mollis and D. brachycephalus, which are morphologically similar, was that D. mollis larvae have later fin formation at same notochord flexion stage. In addition, postflexion larvae of D. mollis have 810 discrete postanal me­ lanophores, whereas in D. brachycephalus the postanal series coalesce to ~7 melanophores, with about 4 of them embedded above the anal base and several that are typically fused and that are observed posterior to anal insertion (Richards, 2006). Hence, our identification is consistent following the morphological criteria described in the literature. How­ ever, a recent study (Batta-Lona et al., 2019) indicate that morpholog­ ical identification of D. mollis yielded mixed results of five larvae that were identified based on COI. Hence, future studies should complement morphological identification with genetic analysis. Larvae were cate­ gorized according to their notochord flexion level (preflexion, flexion, postflexion and transformation). Larvae which could not be identified to species level were characterized at the family or genera level. Total and myctophid larval relative abundances were standardized as larvae per 1000 m3 filtered water.

was also equipped with a Seapoint chlorophyll a fluorometer. Mean water temperature between 0 and 200 m depth was calculated for each station. MLD calculations based on temperature criterion are widely presented in the literature. Following the procedure used by Monterey and Levitus (1997) a value of 0.5 � C was chosen to identify the MLD in the top 200 m of the water column (change of 0.5 � C per 1 m depth). Fluorescence was used as a proxy to determine the water column chlo­ rophyll a concentration and to estimate the depth of the fluorescence maximum. Sea surface height (SSH) data were obtained from AVISO (https:// www.aviso.altimetry.fr/en/home.html) and surface chlorophyll a con­ centration was obtained from E.U. Copernicus Marine Service Infor­ mation (CMEMS) (http://marine.copernicus.eu/). Estimates of mean current velocities and kinetic energy were acquired from the HYCOM (Hybrid Coordinate Ocean Model) consortium’s GoM ocean model (http://www.hycom.org). Mean velocities (m s 1) and kinetic energy (m2 s 2) were averaged for the top 200 m over 2 week-intervals throughout the duration of the cruise (August 6 to September 16). 2.5. Statistical analyses Statistical analyses were carried out to evaluate differences in stan­ dardized abundance of total fish and myctophid larvae, percentage of myctophid relative to total larvae, and proportion of preflexion mycto­ phid larvae relative to the sum of flexion, postflexion and transformation stages. Additionally, a comparison between day and night samplings were performed for each larval stage. Concerning the environmental variables, SSH, KE and in situ variables were compared among the central gulf, the Bay of Campeche and the Yucatan Channel. The regions used in the analyses were selected from previous studies in the GoM (Damien et al., 2018; Miron et al., 2017; Muller-Karger et al., 2015). Non-parametric Kruskal-Wallis (KW) test was applied because data did not fulfill the assumptions of normality and homogeneity of variance. A significance level of α ¼ 0.05 was used. A post-hoc t-test with a Bon­ ferroni correction for multiple comparisons was performed (Weisstein, 2004). Principal component analysis (PCA) was performed to identify sta­ tions with similar environmental (mean water temperature at 0–200 m, SSH, MLD) and biological (surface chlorophyll a concentration, zooplankton biomass and myctophid larval abundance) parameters to evaluate whether surface waters conditions were related with the as­ semblages identified in the cluster analyses. The R–project 3.4.1 (Team, 2013) statistical program was used for all analyses.

2.3. Characterization of larval fish assemblages The Biological Value Index (BVI) proposed by Sanders (1960) was used to identify dominant taxa, which ranks the species in order of dominance based on the larval percentage of occurrence and their relative abundance. Dominant species were selected with the Accumu­ lated Biological Value Index (% BVI), which is obtained by dividing the BVI by the total value and multiplying it by 100. With the taxa ordered by dominancy, % BVI values were summed until it reached a value of 50%. This value was used as a fixed cutoff value taking into account that �n-Villa et al., 2010; it is not consistently defined in the literature (Galva Ríos-jara et al., 2008). To assess the presence of larval fish assemblages, taxa specific abundance data was fourth root-transformed to attenuate the weighting of abundant species (Field et al., 1982). Assemblages were calculated using a cluster analysis with a Bray-Curtis similarity matrix (Bray and Curtis, 1957), because it is insensitive to the absence of taxa in some stations. A first cluster was performed with the 32 identified species and a second with the eight dominant taxa based on the % BVI. An Analysis of Similarity (ANOSIM; Clarke et al., 2008) was applied to the Bray-Curtis similarity matrix, testing the distances among samples in the same group compared to that observed between samples of different groups (sig­ nificance level α ¼ 0.001). Cluster divisions were generated considering a 60% similarity between assemblages (corresponding to an α ¼ 0.001). Assemblages were defined as three or more grouped stations. This value was chosen due to the large number of grouped stations with a 50% similarity value, and the large number of groups yielded when using a similarity of 70%. Additionally, a Similarity Percentage Analysis (SIMPER; Clarke and Gorley, 2006) was performed to determine the richness and contribution of each taxa based on their average abundance within each assemblage. The PRIMER-E6 software (Clarke and Gorley, 2006) was used to perform all tests.

3. Results The average standardized total larval abundance was 867 � 994 larvae 1000 m 3 (mean � SD), with a maximum of 5621 larvae 1000 m 3 at station F36, located in the western portion of the Bay of Cam­ peche (Fig. 2A). The Bay had significantly (K–W test, p ¼ 0.0001) higher standardized abundances 1470 � 1333 larvae 1000 m 3 than the central gulf 495 � 320 larvae 1000 m 3 and the Yucatan Channel 373 � 195 larvae 1000 m 3. The standardized abundance of myctophids was 145 � 94 larvae 1000 m 3, with a maximum of 461 larvae 1000 m 3 at station E33 located in the Bay of Campeche (Fig. 2B). The central gulf, Bay of Campeche and Yucatan Channel had an abundance of 131 � 63, 373 � 119 and 86 � 55 larvae 1000 m 3 respectively. However, myctophid abundance did not differ significantly among regions (K–W test, p ¼ 0.196). The mean percentage of myctophid larvae relative to the total larval abundance was 24.6 � 13.1% (mean � SD). The mean percentage was significantly (K–W test, p ¼ 0.003) higher in stations of the central gulf (33.6 � 10.5%) compared to the Bay of Campeche (19.6 � 12.8%) and the Yucatan Channel (21.39 � 10.20%) (Fig. 2C). A total of 64 taxa of the Myctophidae family were identified,

2.4. Oceanographic conditions Hydrographic parameters, oceanographic conditions and mesoscale structures relative to sampling stations were characterized by coupling in situ measurements, remote sensing and a circulation model. Hydro­ graphic data were obtained at each station with a SBE 9Plus CTD that 4

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Fig. 2. Larval abundance and stage–specific relative abundances (A) Standardized abundance of total fish larvae and (B) myctophid larvae, expressed as larvae 1000 m 3. Note that scales differ between maps. (C) Percentage of myctophid larvae relative to total larvae. (D) Proportion of preflexion (white) myctophid larvae relative to the sum of flexion, postflexion and transformation stages (red). Placement of Yucatan Channel stations were separated for clarity, but represent double of sampling of stations along the east–west axis.

including 32 to species level, 25 to genus and 7 to family level (Table 1). Number of identified taxa and larvae, and standardized abundance was higher in the species level compared with the genus and family level. The predominant genus was Diaphus, with 14 taxa (4 species and 10 type species). D. mollis was the most abundant species, with a mean abundance of 26 � 26 larvae 1000 m 3 and the highest frequency of occurrence, appearing in 84% of the sampled stations. On average, 62.5% of myctophid larvae were in preflexion, 18.75% in flexion, 12.5% in postflexion and the remaining 6.25% were undergoing trans­ formation to the juvenile stage. Larvae in preflexion were predominant in all three regions (Fig. 2D). Significantly greater abundances were found in stations collected at night compared to those sampled during the day in postflexion larvae (mean � SD; 20.94 � 26.33 vs. 7.66 � 9.77 larvae 1000 m 3; K–W test, p-value ¼ 0.025) and transformation larvae (4.60 � 6.24 vs. 0.70 � 2.60 larvae 1000 m 3; p value < 0.001). On the other hand, preflexion (71.73 � 59.87 vs. 80.23 � 52.84 larvae 1000 m 3) and flexion stage (41.43 � 35.03 vs. 25.92 � 22.02 larvae 1000 m 3) larvae did not show

significant differences in the abundances between night and day (pvalue ¼ 0.349 and 0.321, respectively). The Sanders BVI indicated that eight taxa were dominant. These taxa were: Diaphus mollis, D. brachycephalus, Benthosema suborbitale, Noto­ lychnus valdiviae, Diogenichthys atlanticus, Ceratoscopelus warmingii, Lampanyctus alatus and Diaphus sp. 01 (Table 2). The 8 dominant taxa represented 64% of the standardized myctophid abundance. The results of the cluster analysis with all 32 species indicated two assemblages of four grouped stations with a similarity > 60% appeared in the cluster (dot and triangle symbols; Fig. 3). The ANOSIM test for this cluster showed significant differences between groups (R ¼ 0.986, p < 0.001). The two assemblages did not present a coherent distribution, with grouped stations scattered in central and southern GoM and the Yucatan Channel. The remaining stations did not assemble into any group (crosses for symbols). Table 2 Dominant taxa based on the Sanders Biological Value Index considering a 50% cumulative BVI cut-off value.

Table 1 Counts of number of identified taxa, number of identified larvae and standard­ ized abundance. Percentage of each count is shown between brackets.

Number of taxa Number of larvae Sum std. abundance

Species level

Genus level

Family level

Total

32 (50%) 1301 (88%) 6159.4 (88%)

25 (39%) 166 (11%) 785.8 (11%)

7 (11%) 9 (1%) 47 (1%)

64 (100%) 1476 (100%) 6992.2 (100%)

5

Taxa

Relative abundance (%)

Percentage of occurrence (%)

% BVI

% Cumulative BVI

D. mollis D. brachycephalus B. suborbitale N. valdiviae D. atlanticus C. warmingii L. alatus Diaphus sp. 01

17.4 9.3 7.9 7.4 7.1 5.6 4.0 2.6

76.4 65.4 50.9 56.4 36.4 50.9 43.6 43.6

10.8 7.8 7.0 6.4 5.6 5.1 4.1 3.9

10.8 18.7 25.6 32.0 37.6 42.7 46.8 50.7

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Fig. 3. Myctophid larval assemblages in the southern GoM. Upper panel: Cluster analysis of 32 Myctophidae species. Triangle and dot symbols represent the assemblages (more than three grouped stations at a similarity of 60%) indicated with the ANOSIM test. Crosses represents stations that did not group into assemblage. Lower panel: Distribution of assemblages in the study area. Black lines represent the dominant mesoscale structures during the XIXIMI-04 cruise (August 27–September 16, 2015).

Results of the cluster analysis with the 8 dominant taxa indicated the presence of six assemblages which included three or more stations; all had a similarity > 60% among stations and differed significantly based on the ANOSIM test (R ¼ 0.853, p < 0.001; Fig. 4). The dominant assemblage, the western gulf assemblage, grouped 19 stations in the western extent of the central gulf and the Bay of Campeche. Three sta­ tions were grouped into a northern Yucatan assemblage (circles). Four

other assemblages A, B, C and D grouped 8, 6, 3 and 3 stations (triangles, diamonds, squares and asterisks, respectively) that were found scattered throughout the central and southern GoM and Yucatan Channel. Crosses represent stations that were not grouped into assemblages with a > 60% similarity. For the most cohesive assemblages (western gulf and northern Yucatan), results of the SIMPER (Table 3) analysis indicated that the so6

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Fig. 4. Myctophid larval assemblages in the southern GoM. Upper panel: Cluster analysis of dominant Myctophidae taxa. Western gulf (dot), northern Yucatan (circle), A (triangle), B (diamond), C (square) and D (asterisk) assemblages grouped three or more stations. Stations represented by crosses indicate a lack of grouping. Lower panel: Distribution of assemblages in the study area. Dashed lines represent grouped assemblages and black lines the dominant mesoscale structures during the XIXIMI-04 cruise (August 27–September 16, 2015).

called “western gulf” assemblage was comprised of the 8 taxa (Table 3). The contribution of each taxa to the similarity score differed between assemblages. D. mollis contributed 18% to the similarity among the stations of the western gulf assemblage. Four taxa (D. mollis, B. suborbitale, N. valdiviae and D. brachycephalus) explained 67% of the similarity among stations. The north Yucatan assemblage was comprised of 2 taxa; D. mollis which contributed 51% to the similarity and

D. brachycephalus with 49% similarity. Assemblages A, B, C and D had average similarities of 67%, 69%, 74% and 67% respectively. Although D. mollis and D. brachycephalus were both present in all assemblages except in assemblage D, the average abundances differed and other taxa were present in these assemblages. The dissimilarity among the four assemblages was greater than 45%. Mean water temperature at 0–200 m, MLD, SSH and KE were 7

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Table 3 Results of the SIMPER analysis applied to the assemblages identified in the cluster analysis. Average abundance (Av. Abd.), Average Similarity (Av. Sim.), Similarity Standard Deviation (Sim./SD), Taxa Contribution (Contrib. %), Cu­ mulative contribution (Cum. %).

Table 4 In situ, satellite-derived variables and kinetic energy (mean � SD): comparison among central gulf (CG), Bay of Campeche (BoC) and Yucatan Channel (YC).

Western gulf Average similarity: 68.00 Species

Av. Abd.

Av. Sim.

Sim./SD

Contrib. %

Cum. %

D. mollis B. suborbitale N. valdiviae D. brachycephalus D. atlanticus C. warmingii Diaphus sp. 01 L. alatus

5.18 4.67 4.69 4.08 3.82 3.04 3.16 2.01

12.39 11.55 11.45 10.32 8.39 6.31 4.40 3.20

1.62 2.24 2.59 2.29 1.80 1.33 0.69 0.75

18.22 16.98 16.83 15.17 12.34 9.27 6.47 4.71

18.22 35.20 52.03 67.20 79.55 88.82 95.29 100

Northern Yucatan Average similarity: 67.39 Species Av. Abd. D. mollis 7.74 D. brachycephalus 6.23

Av. Sim. 34.30 33.09

Sim./SD 6.42 5.07

Contrib. % 50.89 49.11

Cum. % 50.89 100

Assemblage A Average similarity: 67.22 Species Av. Abd. D. mollis 5.67 N. valdiviae 3.58 L. alatus 1.72 D. brachycephalus 2.02 D. atlanticus 0.91

Av. Sim. 36.25 15.94 7.58 6.05 1.39

Sim./SD 3.91 1.35 1.04 0.71 0.34

Contrib. % 53.94 23.72 11.28 9 2.07

Cum. % 53.94 77.65 88.93 97.93 100

Assemblage B Average similarity: 68.81 Species Av. Abd. D. mollis 4.38 B. suborbitale 3.14 D. brachycephalus 2.92 C. warmingii 2.35 D. atlanticus 1.56 L. alatus 0.80

Av. Sim. 24.09 15.15 13.21 10.16 5.55 0.66

Sim./SD 6.14 4.41 1.27 1.32 0.77 0.26

Contrib. % 35.01 22.02 19.20 14.76 8.06 0.95

Cum. % 35.01 57.03 76.22 90.98 99.05 100

Assemblage C Average similarity: 74.40 Species Av. Abd. D. brachycephalus 3.80 D. mollis 3.36 Diaphus sp. 01 3.06 C. warmingii 1.46

Av. Sim. 26.43 24.27 18.20 5.51

Sim./SD 5.29 19.17 306.87 0.58

Contrib. % 35.52 32.62 24.46 7.40

Cum. % 35.52 68.14 92.60 100

Assemblage D Average similarity: 66.88 Species Av. Abd. D. mollis 3.46 N. valdiviae 2.67 D. atlanticus 2.52

Av. Sim. 32.79 26.2 7.89

Sim./SD 4.15 4.74 0.58

Contrib. % 49.02 39.18 11.80

Cum. % 49.02 88.20 100

Variable

CG

BoC

YC

K–W

Mean temp. (� C) 0–200m MLD (m)

23.29 � 1.55

21.29 � 1.16

25.07 � 2.22

37.90 � 11.00 a 82.70 � 18.00 b 0.11 � 0.03 d

36.90 � 6.60

49.68 � 2.80

61.10 � 27.80 c 0.17 � 0.06

75.35 � 11.61 bc 0.09 � 0.01 d

< 0.001 < 0.001 0.006

17.51 � 1.10 0.01 � 1.00

9.19 � 1.00

Max. Fluor. Depth (m) [Surface chl a] (mg m 3) SSH (cm) KE (m2 s 2)

2.50 � 1.20 0.12 � 0.18

a

0.49 � 0.25

< 0.001 < 0.001 < 0.001

Post-hoc comparison using Bonferroni T-test. Letters show non-significant mean differences at the 0.05 level.

component (PC2) explained 18.33% of the variance, and was comprised by biological parameters (surface chlorophyll a concentration, zooplankton biomass and myctophid larval abundance). Two main groups of stations were discernible in the PCA (Fig. 6): those within the Bay of Campeche and those in the central gulf and Yucatan Channel. The stations in the Bay of Campeche were correlated with a shallower MLD, lower average water temperature at 0–200 m and sea surface height, and higher surface chlorophyll a concentration, zooplankton biomass and myctophid larval abundance. The central gulf and Yucatan Channel stations were correlated with high sea surface heights, average temperature at 0–200 m and MLD, and lower surface chlorophyll a concentration, zooplankton biomass and myctophid larval abundance. 4. Discussion Results of this study provide information on how myctophid larval assemblages of the dominant taxa are mainly modulated by adult spawning rather than surface transport in the deep water region of the southern GoM. The distribution and abundance of myctophid fish spe­ cies generally corresponded with previous reports for the GoM (Richards ~ orve et al., et al., 1993; Rodríguez-Varela et al., 2001; Sanvicente-An 1998). The uniformity of larval myctophid abundance and distribution in the three defined regions in the southern GoM is consistent with previ­ ous studies concerning myctophids in the northern gulf and LC region (Richards et al., 1993; Sutton and Hopkins, 1996). Although there were no significant differences in the abundances among regions examined in this study, the highest myctophid abundances were found in the Bay of Campeche compared to stations in the central gulf and Yucatan Channel, thus agreeing with findings of Rodríguez-Varela et al. (2001). This could be due to the well–documented greater availability of nutrients and food in the Bay of Campeche compared with the central gulf (Furnas and �mez and Salas de Leo �n, 1990; Salas-de-Leo �n Smayda, 1987; Monreal-Go et al., 2004). Higher productivity and higher food availability may sustain a higher biomass of adults and therefore more spawning, as well as providing larvae with food availability that may favor a higher sur­ vival during the larval period (Houde and Hoyt, 1987; Lasker, 1981) in comparison with lower productivity areas. The higher percentage of myctophid larvae (as a percentage of total abundance) in the central gulf is likely due to adults being dominant in waters far from the continental shelf (Catul et al., 2011), leading to greater larval abundances of Myctophidae than larvae of other families from coastal or neritic habitats. This finding agrees with results of Muhling et al. (2012), who found the highest percentage of occurrence of myctophids in the deep water region of the GoM’s US EEZ. Relative abundances determined in the present study were higher than those within the GoM and the Caribbean Sea reported by

significantly higher in the Yucatan Channel, followed by the central gulf and with lowest values in the Bay of Campeche. While, the depth of maximum fluorescence was significantly higher in the central gulf compared to the Bay of Campeche, and mean surface chlorophyll a concentration was significantly higher in the Bay of Campeche compared to the other two regions (Table 4). Geostrophic velocities and KE snapshots derived from the HYCOM model (Fig. 5), showed that geostrophic velocities in the Yucatan Channel were mainly anticyclonic. Conversely, in the Bay of Campeche the velocities were cyclonic. Although the main velocities of the central gulf were anticyclonic, some areas presented cyclonic velocities. These conditions remained consistent during the duration of the cruise. The first two components of the PCA performed to identify grouping stations according to physical and biological parameters explained 69.65% of the variance. The first component (PC1) accounted for 51.62% of the variance, and was comprised by environmental parame­ ters (mean water temperature at 0–200 m, SSH and MLD). The second 8

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Fig. 5. Oceanographic surface conditions of the GoM. Left: HYCOM-model mean velocities (m s 1). Right: mean kinetic energy (m2 s 2) divided into two–week interval from August 6 to September 16 (0–200 m).

Rodríguez-Varela et al. (2001), where only 16.70% of the larvae iden­ tified belonged to the Myctophidae family. However, lower percentages of myctophid larvae were found in some western stations closer to the continental shelf of the Bay of Campeche (D26) and Yucatan Peninsula ~ orve et al. (C24, C25 and G44). These results agree with Sanvicente-An (1998), who indicated that mesopelagic families such as the Myctophi­ dae in the Bay of Campeche were predominantly low in abundance compared with families from coastal and neritic habitats such as Gobiidae and Engraulidae, presumably due to offshore transport from the continental shelf. Results of the present study agree with the cited literature and provide compelling evidence that myctophids have a widespread distribution in the southern GoM and that the highest pro­ portion of myctophids occurs in oceanic areas. The high proportion of preflexion larvae reported in this study re­ flects the occurrence of local spawning. The majority of species of the Myctophidae family exhibit continuous reproduction throughout the year and short time–periods for preflexion (Brandt, 1981; Gartner et al., 1989; Kinzer and Schulz, 1985; Richards, 2006). Hence, the predomi­ nance of preflexion larvae in the three defined regions within the gulf suggests a wide–ranging distribution of spawning adults. Additionally, the smaller proportion of postflexion larvae in the plankton is consistent

with a high mortality rate during the early stages of development (e.g. predation, inter and intra–specific competition for food, or lack of food availability) (Fuiman and Werner, 2002; Houde and Hoyt, 1987). Other possible causes of the smaller proportion of postflexion and trans­ formation larvae might be due to gear avoidance or diel vertical migration to deeper waters during daylight (Catul et al., 2011). The later may explain why postflexion and transformation larval abundances were higher during the night compared with samples collected during the day (Balon, 1984; Youson, 1988). The dominant identified taxa were very similar to those found by Rodríguez-Varela et al. (2001) in the GoM and Caribbean Sea. Addi­ tionally, agreement between the results of the present study regarding the myctophid species composition with that reported by Felder and Camp (2006), suggests that the 18 genera identified in this study are consistently found in the GoM. However, larval transport from the Caribbean Sea to internal waters of the gulf due to the LC and anticy­ clonic eddies that detach from the LC may also contribute to the pres­ ence of these genera during larval stage, at least for periods reflecting the duration of the larval stage (weeks). Nevertheless, the abundance and distribution of the dominant taxa identified in this study and in prior studies in the GoM were similar. As other authors suggested (Brandt, 9

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Fig. 6. Principal component analysis with a 69.65% explained variance. PC1 (sea surface height, mean temperature at 0–200 m and mixed layer depth) with an explained variance of 51.62%. PC2 (surface chlorophyll a concentration, zooplankton biomass and myctophid larvae abundance) with an explained variance of 18.33%. Bay of Campeche (red), Central (green), Yucatan Channel (blue). Variables are represented by orange vectors.

1981; Gartner et al., 1989; Kinzer and Schulz, 1985; Richards, 2006), this might indicate that adult species occupy similar oceanic habitats and have similar reproductive periods and spawning regions. The assemblages of dominant species in the central gulf were influ­ enced by the LC and Olympus and Nautilus II anticyclonic eddies. However, in the Bay of Campeche, only the western gulf assemblage was predominant. The later was present in the western central gulf and the Bay of Campeche and was mainly associated with weak cyclonic struc­ tures. D. mollis and D. brachycephalus had the greatest abundance and widest distribution, in agreement with findings of Rodríguez-Varela et al. (2001), showing that Diaphus is a cosmopolitan genus in the deep water region of the gulf. The assemblages were mainly defined by dif­ ferences in taxon–specific abundances rather than the presence or absence of specific taxa. This also suggests that larval distribution was defined by adult spawning of the dominant taxa. The presence of the western gulf assemblage in the central gulf and the Bay of Campeche indicate that there are spawning grounds and seasonality of a similar adult community in both regions. These results agree with the available information on the life history of these species, such as B. suborbitale, N. valdiviae and Diaphus spp. which spawn annu­ ally. However, the higher abundances of Diaphus might be due to this genus have spawning peaks during summer (Brandt, 1981; Gartner et al., 1989; Kinzer and Schulz, 1985). The LC has been shown to serve as an important transport mecha­ nism of water and biological assemblages into the GoM (Muhling et al., 2013; Richards et al., 1993; Weatherly et al., 2013). In this study, the north Yucatan assemblage (stations A8, A9 and A10) was found within the area of influence of the Olympus eddy, an anticyclonic eddy that originated from the LC. The species from this assemblage (D. mollis and D. bracycephalus) coincide with reports of high abundances of species from the Diaphus genus in the Caribbean Sea and warm LC waters (Houde et al., 1979; Muhling et al., 2013; Richards et al., 1993). The formation of this assemblage could be due to: (1) larval retention by the anticyclonic eddy, which has been reported in prior studies (Cruz-G� omez et al., 2008; Salas de Le� on and Monreal Gomez, 2005), and (2) similarity of the adult myctophid community within the LC and in

LC-derived eddies, which has also been described in prior studies (Brandt, 1981; Kinzer and Schulz, 1985; Richards, 2006). Stations grouped in the dominant taxa assemblages A, B, C and D were not observed in a particular region, and were found at stations located between the Olympus and Nautilus II anticyclonic eddies and in the Yucatan Channel, as well as some stations in the western gulf (along 22� N and 23� N). As mentioned above, Richards et al. (1993), and Muhling et al. (2013) found that the LC influences myctophid assem­ blages in the Yucatan Channel transporting them into the gulf. Although the main feature that may transport larvae into the gulf are detached anticyclonic eddies from the LC (Muhling et al., 2013; Richards et al., 1993). Vukovich and Maul (1985) reported that eddies move westward at ca. 4 km day 1, taking about 225 days to reach the western gulf. Given the average larval period of myctophids (50–60 days;Gartner, 1991), it is unlikely that larvae could survive or arrive as preflexion larvae in the western gulf if spawning occurred within the region of influence of the LC. Similarly, rough northward transport calculations showed that it would take about 83 days to reach the central GoM (24–25� N) from the Bay of Campeche (21–22� N) with an average speed of ca. 4 km day 1. Hence, the most feasible explanation of the dominant assemblages is that the adults of the species were distributed throughout the gulf in mesopelagic waters and that spawning occurred locally. The regions that were identified based on the oceanographic condi­ tions included in the PCA analysis (central GoM, Bay of Campeche and Yucatan Channel) were similar to those found by previous authors using different criteria (Damien et al., 2018; Miron et al., 2017; Muller-Karger et al., 2015). However, these regions did not match with the spatial distribution of the myctophid larval assemblages of dominant taxa. This seems to strengthen that myctophid larvae were not strongly influenced by the differences in the oceanographic conditions of the Bay of Cam­ peche, central GoM and Yucatan Channel. The lack of defined assemblages in the cluster with 32 species was caused by the inclusion of rare taxa, which led to stations that did not group into assemblages. Rare species are characterized by low abun­ dance and frequency of occurrence (Sokal and Rohlf, 1995). The dif­ ference in the assemblage structure when considering the dominant taxa 10

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and the 32 species in the cluster analysis suggests that rare species may have very different distribution patterns. However, some of the rare species we documented (e.g. Hygophum hygomi, Myctophum obtusiroste, M. selenops, Symbolophorus rufinus) coincide with those found in the eastern GoM and northern Sargasso Sea (Conley and Gartner, 2009; Miron et al., 2017; Gartner et al., 1989). Nevertheless, the lack of in­ formation on the abundance and distribution of myctophid adults in the deep water region of Mexico’s EEZ makes it difficult to ascertain whether the low abundance of rare species reflects the low abundance of adults, species–specific seasonal spawning or selective mortality.

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