Biodiversity, ecosystem functioning, and abiotic factors are interrelated [1
]. Communities can be dominated by a few species with particular traits or by complementary species that are differently adapted to the habitat [1
]. The habitat frames relationships among species. The species composition of marine fish larval communities has been usually related to habitats in the “horizontal” dimension (e.g., the spatial distribution of species regarding abiotic variables [3
]). However, significant physical, chemical, and biological gradients in the vertical dimension of the water column influence the vertical distribution of fish larvae. The place where a larva is relative to these gradients profoundly influences the development and success of the larval phase. The horizontal advection of fish larvae from spawning to nursery areas also depends on the vertical position of the larvae in the water column [4
]. In general, the presence or absence of persistent clines in the open ocean can influence the vertical distribution and composition of larval fish assemblages [5
There has been an historical interest describing the species composition in tuna assemblages due to their economic and ecological importance as top predators. Juvenile and adult tuna species dominate in particular areas worldwide and separate niches across their vertical distribution when coexisting [6
]. Early in their life cycle, a variety of tuna species coexist in most spawning grounds worldwide with particular species dominating in the different areas [8
]. Temperature arises as a key variable explaining the presence of tuna larvae in all areas [12
]. As such, temperature is one primary variable explaining the worldwide distribution of major tuna spawning areas [18
] and recruitment variability [20
]. Other environmental variables such as salinity and fluorescence explain larval spatial segregation of tuna species at a small spatial scale [8
In contrast to the adult stage, niche segregation of tuna species with depth and companion species during the early life stages has been little studied. Atlantic bluefin tuna (BFT), as with other tuna species, reproduce in temperatures above 20 °C conducive for survival and development of eggs and larvae [24
]. Therefore, temperature is often the primary variable used to explain the shallow depth distribution of tuna larvae in environments with a strong seasonal thermocline where temperatures of 20 °C occur at around 20 m depth (e.g., Pacific bluefin tuna in the Nansei area [26
]; Albacore and BFT in the NW Mediterranean [27
]). However, tunas also reproduce in areas that lack a strong near-surface seasonal thermocline and where temperatures above 20 °C are mixed throughout the upper water column. Within these locations, little is known about the vertical distribution of tuna larvae [9
]. Pacific bluefin tuna larvae, Thunnus orientalis
, is the only species for which the vertical distribution has been compared across two spawning areas with different scenarios showing a shallower and narrower distribution in areas with a strong thermocline [28
]. Laboratory experiments show that BFT and bonito larvae occupy a wider depth range when temperatures are vertically homogeneous compared to when waters are stratified, in which case BFT larvae are confined to the surface mixed layer [27
]. Vertical temperature distributions may then play a major role on the vertical distribution of tuna species and companion species, a task that has received little attention in the literature.
Among the different spawning areas for BFT and other tuna species, the Gulf of Mexico (GOM) in the western Atlantic and the western Mediterranean Sea (MED) in the eastern Atlantic are the ones with a longer time series of annual samplings to study the horizontal distribution of larval fish assemblages, although using different methodologies [22
]. Integrated sampling has been conducted from the surface down to the 70 m depth in the MED [29
] and from the surface down to 200 m depth in the GOM [33
]. In both areas, BFT coexists with other tuna species: Thunnus atlanticus
, T. albacares
, T. obesus
spp., and Katsuwonus
spp., and the horizontal assemblages are dominated mainly by mesopelagic larvae. For both areas, increasing densities of tuna larvae have been reported since 2010; however, which taxa are increasing differs: BFT in the MED [34
] and Thunnus
spp. in the GOM [33
]. Differences in these integrated sampling methodologies make the comparison between assemblages difficult and further complicate the understanding of vertical processes that could enhance our understanding of the ecological role of bluefin tuna larvae in the larval fish community.
The BFT spawning season comprises April to June in the GOM and June to July in the MED [22
]. In both spawning areas the horizontal larval habitat is characterized by warm waters [22
]; however, water column properties differ between the areas [9
]. The vertical distribution of chlorophyll during the BFT spawning periods is similar in both areas, with maximum chlorophyll concentrations occurring around 80–90 m depth [9
]. Although salinity values are higher in the MED than in the GOM, the water column is isohaline in both sites, which is typical of open ocean waters [9
]. In contrast, the thermal stratification differs between the two spawning areas with a strong thermocline at 20 m in the MED and a deeper thermocline around 100 m in the GOM [9
]. Comparison of the water column properties in these two areas can help us understand how the thermal structure of the water column influences larval fish ecology and community structure.
Until now, no comparable data on the vertical distribution of BFT and the associated larval assemblages has been available. No studies have examined in detail how environmental conditions influence the vertical distribution of BFT larvae and their associated ichthyoplankton community in either the GOM or the MED. If temperature remains the primary variable explaining the vertical distributions of larvae, then we would expect tuna larvae to be found more deeply distributed in isothermal areas than in those that are thermally stratified. The aim of this study was: (1) to test the influence of thermal stratification on the vertical distributions of larval tuna, and (2) to determine whether the association between the vertical distributions of larval fish assemblages in BFT spawning grounds is influenced by environmental parameters.
This study finds that temperature influences vertical distribution of larvae in the MED and a combination of salinity and fluorescence values in the GOM. Our findings support previous work that has demonstrated that temperature is the primary variable explaining vertical distribution of fish larvae in regions where the water column is characterized by a strong thermocline [5
]. The strong thermal gradient in the MED also drives the composition of the larval fish assemblage where there is a clear faunal shift from above to below the thermocline (0–25 m). Our results are unique in that they show tuna larvae also inhabit the upper water layers in the GOM, where there is no thermal stratification and where the temperatures greater than 20 °C persist to depths of 80–100 m. The vertical distribution of the larval fish assemblage in the GOM is correlated with a combination of environmental variables including salinity and fluorescence values characteristic of surface waters.
The composition of the larval fish assemblage associated with BFT larvae in both spawning areas is strikingly similar, despite evidence that different environmental drivers influence the vertical structure of the assemblages. BFT larvae co-occur in the upper water layer with other tuna and specific mesopelagic species in both ecosystems. Co-occurrence of multiples species of tuna larvae in the first upper 20 m of the water column has been reported throughout the world [16
]. Our results corroborate these findings. In the MED, all tuna inhabited the upper 20 m, whereas in the GOM, tuna were found down to depths of 30 m, though most (66%) were in the upper 20 m. The WMD of Thunnus
larvae was almost same between GOM and MED however the WMD of the other scomber larvae in the MED was clearly shallower than that in the GOM (Figure 3
a and Figure 4
). In the MED, the thermocline is a sharp temperature boundary layer for the scombrid larvae, and they are forced to coexist in the first 20 m, whereas the optimal temperatures for scombrid larvae can be found from surface down to 100 m depth in the GOM. Under those conditions, scomber larvae can avoid coexistence among them by selecting a wider range of depths. Anyway, in the GOM, their condition of visual predators might also limit their vertical expansion. Horizontal habitat segregation in scombrid larvae has already been documented in the Pacific [8
], in the GOM [23
] and in the MED [51
]. It is to be expected that the same segregation can occur in the vertical distribution of taxa if the environmental conditions are within the taxa specific limits.
We found striking similarities in the depth distribution of the mesopelagic group between the two study areas. We hypothesize that the depth distribution of these individuals is influenced by the availability of their prey [52
]. In the GOM, more than half of the zooplankton biomass is found in the upper 200 m, with the majority of that occurring in the upper 50 m [53
]. In the MED, during the stratified period (when tuna spawning season takes place), zooplankton exhibits a very structured vertical pattern, with some groups presenting daily vertical migrations (copepods and ostracoda), whereas others remain both night and day at upper (cladocera) or deeper (appendicularia) layers [54
In contrast with the mesopelagic group, the demersal group exhibited quite different vertical distributions in the GOM and MED. Since the dispersal phase of a demersal fish must result in the fish returning to the benthic adult habitat, the dispersal trajectory of the larvae must be more precise than for pelagic individuals [55
]. As vertical distribution strongly influences horizontal advection, it is not surprising that the vertical distribution of these species differs between regions, as the oceanographic processes influencing circulation differ. In the MED, only the Labridae family was found deeper than the thermocline barrier (~20m) whereas families that show the ability to choose deeper distributions in the GOM (Triglidae and Anguillidae) remain in shallow waters in the MED. Apart from the abiotic variables included in the analysis, competition and other ecological interactions might be the cause of differences in the assemblage’s vertical distribution. In the MED, the shallow strong thermocline acts as a boundary layer for most of the taxa vertical distributions. The different groups must combine their physiological requirements in terms of abiotic tolerance, with the food availability and with the ecological interactions with other taxa such as competition or predation in a very narrow vertical layer. The absence of that shallow boundary layer in the GOM allows the assemblage to be more expanded in the vertical. In a transect crossing the tropical to equatorial Atlantic Ocean, with strong thermal stratification down to ~100 m, larval fish assemblages were found also occupying different vertical positions in relation to the physiological and ecological constraints [5
]. The relative distribution in the vertical among taxa was very similar to the one found in the GOM.
Diel changes in the vertical position of fish larvae have not been addressed in this work. Sampling in GOM and in the MED was equally distributed throughout the 24 h of the day (Table S1
). No day-night differences were found among catches at the different depth strata. Previous studies in the GOM found no day-night differences in vertical positions or abundances of tuna larvae [56
]. In the MED, winter and summer diel vertical distributions of fish larvae from the surface to 200 m depth were systematically studied during intensive 48 h sampling periods [54
]. Most of the taxa that were found during summer at depth > 50 m did not show differences greater than 10 m in their day or night vertical positions. In the Atlantic Ocean, no day-night differences were found in the vertical pattern of most fish larvae [5
]. However, transforming stages of some mesopelagic taxa exhibited diel vertical migration. Very few transforming-stage individuals were found in our catches and they were not included in the analyses. Due to the narrow vertical range inhabited by tuna larvae, the study of ontogenetic diel migrations would require sampling with greater vertical resolution (<10 m) tows.
Water temperatures above 20 °C are related to suitable larval habitats for tuna species [18
]. In scenarios characterized by having a strong thermocline, this minimum temperature limit for the larval distribution (20 °C) has been linked to the vertical distribution of tuna larvae above the thermocline (e.g., [26
]), but it does not explain the vertical distribution of the tuna larvae found in the GOM, where the 20 °C limit is found to 95m deep and most of tuna larvae (80.6%) inhabit the upper 30 m.
Behavioral rearing experiments simulating vertical temperature gradients have demonstrated that BFT and bonito larvae are distributed throughout the water column in isothermal conditions as opposed to occupying specific depths when there is a sharp temperature gradient [25
]. In our study, regardless of thermal conditions, tuna larvae were primarily found in surface waters, suggesting another abiotic or biotic factor influences their vertical distribution. We hypothesize light level is the additional variable that influences the vertical distribution of tuna larvae. Along with temperature, light is among the most common of vertical cues for larvae in the ocean [57
]. BFT larvae are visual predators, feeding mainly during daylight hours [58
]. We propose that the vertical habitat of BFT larvae is defined by water masses with a combination of suitable temperature, high forage biomass, clear water and sufficient light level to observe prey [59
]. Unfortunately, no reliable light or turbidity data were available for the present work, but the coexistence with other ichthyoplankton groups in the first meters of the water column, where incident light is maximum, is compatible with the idea of where a visual predator should be positioned in the vertical to maximize foraging possibilities.
In recent years, the annual densities of BFT larvae have been increasing in both the MED and GOM [33
]. MED densities are significantly higher than those reported in the GOM. Knowledge of which species comprise the larval fish assemblages in major tuna spawning grounds is key to understand the ecological role of tuna larvae within the community. For BFT larvae, finding larval prey at the right place in the right time improves larval growth and survival [19
]. Rearing experiments have demonstrated selective piscivory in tuna larvae [60
]; however, we still know very little about the prey ingested by tuna in the wild. The narrow available vertical habitat for all the larval fish assemblage in the MED might force the coexistence of tuna larvae with its potential prey, unless horizontal niche segregation is possible. That could be one of the reasons behind the high tuna fish larvae densities found in the MED. Using common methodology is crucial when comparing larval fish assemblages between regions. The use of similar nets, sampling methodologies and environmental variables can help to compare spawning areas while avoiding significant methodological issues [56
]. Studies such as this one improve our knowledge about the composition of the larval fish community and expand our knowledge of the detailed vertical distribution of prey and tuna in their spawning grounds. One example is the high abundances of specific species of mesopelagic larvae found together with tuna that may ensure the availability of prey for the tuna larvae.