Distribution, vertical migration, and trophic ecology of lanternfishes (Myctophidae) in the Southwestern Tropical Atlantic

Highlights

• Lanternfishes are a highly diverse and abundant fish family of the Southwestern Tropical Atlantic.

• Lanternfishes presented a high variability of prey composition and migratory behaviour.

• At least 73% of lanternfishes observed here vertically migrate to the surface to feed at night.

• Lanternfishes act as a secondary prey for epipelagic predators and a central food source for deep-sea species.

• Lanternfish assemblages are not strongly affected by the thermohaline structure and current systems of the region.

Abstract

Lanternfishes (Myctophidae) are among the most abundant, widespread, and diverse fish groups in the world ocean. They account for a significant part of oceanic fish biomass and play crucial roles in various ecosystem processes, including carbon sequestration and nutrient recycling. However, despite the increasing risks they face (e.g. global warming, plastic pollution, and exploitation of deep-sea resources), many aspects of the lanternfishes ecology still remain poorly known. Here, we investigate the species composition, vertical migration, and trophic ecology of lanternfishes in the Southwestern Tropical Atlantic (SWTA) and the influence of physicochemical factors on their horizontal structuring. We show that lanternfishes are a highly diverse and an abundant fish family of the SWTA, comprising at least 33 species and contributing 40% of all fish collected (in number). We reveal that some of these species may differ in their patterns of prey composition and migratory behaviour, leading to multidimensional niches, underestimated trophic links (e.g. gelatinous organisms), and several mechanisms to avoid competitive exclusion. At least 73% of the lanternfish species reported here seem to migrate to the surface to feed at night. Additionally, they are a central food source for mesopelagic and bathypelagic predators, thereby connecting shallow and deep-sea ecosystems. Finally, we show that the structure of lanternfish assemblages is not strongly affected by environmental conditions analysed here (i.e., throughout the thermohaline structure and current systems), leading to weak horizontal assemblage separation.

Introduction

Lanternfishes (Myctophidae) are amongst the most abundant, widespread, and diverse fish groups in the world ocean (Gjøsaeter and Kawaguchi, 1980, Catul et al., 2011). This family includes 254 species that are generally small (mean maximum length of 90 mm) and are dominant in pelagic environments (Poulsen et al., 2013, Priede, 2017, Fricke et al., 2020, Cherel et al., 2020). Most myctophid species migrate vertically to the surface to feed at night and actively transport the carbon they ingest to deep waters during the day (Catul et al., 2011). Moreover, they play a significant role in energetic pathways by consuming zooplankton and providing forage for numerous epipelagic (e.g. tuna, mammals, squids, and diving seabirds) and deep-sea (e.g. viperfish, lancetfish, and moonfish) predators (Sutton and Hopkins, 1996, Cherel et al., 2010, Choy et al., 2013, Rosas-Luis et al., 2014, Eduardo et al., 2020b). These traits are crucial for connecting epipelagic and deep-sea ecosystems and oceanic carbon storage (Catul et al., 2011, Sutton, 2013, Cavan et al., 2019).

Many species of this notable fish group remain poorly known despite facing increasing risks of several kinds (St. John et al., 2016, Martin et al., 2020). While there is a lack of scientific information on the diversity and ecology of lanternfishes in most oceanic basins, the side effects of global warming (Levin et al., 2019), plastic pollution (Davison and Asch, 2011), and exploitation of deep-sea resources are accelerating (Hidalgo and Browman, 2019, Drazen et al., 2020). Further investigations on the ecology and conservation of lanternfishes are recommended. Research has already addressed important aspects of their taxonomy (e.g., Wisner, 1976, Nafpaktitis et al., 1977, Hulley, 1992, Martin et al., 2018), distribution (e.g. Costa et al., 2014, Olivar et al., 2017, Cherel et al., 2020, Sutton et al., 2020), morphometry (Tuset et al., 2018, Eduardo et al., 2020c, López‐Pérez et al., 2020), vertical migration (Watanabe et al., 1999, Olivar et al., 2012, Olivar et al., 2017, Annasawmy et al., 2018, Wang et al., 2019) and trophic ecology (e.g. Hudson et al., 2014, Bernal et al., 2015, Olivar et al., 2018, Contreras et al., 2018, Annasawmy et al., 2020, Czudaj et al., 2020, Bode et al., 2021). These studies demonstrated that lanternfishes present a broad range of vertical and feeding behaviours (Hopkins and Gartner, 1992, Watanabe et al., 1999, Catul et al., 2011). However, less attention has been given on how lanternfish species are scattered over different patterns of resource use (niche partitioning), as a means to avoid resource competition.

Understanding niche partitioning among lanternfishes is central to resolving the paradox between ecological theories demonstrating competitive exclusion and the fact that many of these species are morphologically and ecologically similar but do not drive one another to extinction (Schoener, 1974, Hopkins and Gartner, 1992, Finke and Snyder, 2008). Additionally, understanding niche partitioning helps clarify the coexistence of sympatric species and how resource use shapes their contribution to ecological processes (i.e., fluxes of carbon and nutrients; Brandl et al., 2020). Examining the use of resources in the unified framework of niche segregation, however, requires simultaneous information on biophysical and ecological aspects that are usually lacking. As an example, niche segregation typically occurs along three axes: diet (feeding ecology), space (habitat), and time (feeding chronology; Schoener, 1974). For lanternfishes, this information is sparse and restricted to just a few locations (Hopkins and Gartner, 1992, Hopkins et al., 1996, Hopkins and Sutton, 1998, Catul et al., 2011). Moreover, most previous studies addressing the trophodynamics of these species did not include predators and were based solely on stomach contents. Further approaches (e.g., stable isotopes, fatty acids, and genetics) should be included to provide a comprehensive picture of resource uses. Additional data on the trophic ecology of lanternfishes would help to clarify their trophic links and thus niche differentiation.

Another key point in the study of lanternfishes is how physical drivers shape their diversity and community structure. Variations in temperature, oxygen, and upper circulation processes play important roles in the ecology and movement of deep-pelagic species (Bertrand et al., 2010, Proud et al., 2017, Boswell et al., 2020). However, only a few studies, focusing on restricted locations, have been performed addressing the influence of these oceanographic variables in lanternfishes (Olivar et al., 2017, Milligan and Sutton, 2020). Oceanic islands and seamounts of the Southwestern Tropical Atlantic (SWTA), for instance, are interesting locations to study the influence of physical drivers on biological communities, as they sustain distinctive biodiversity and are considered as Ecologically or Biologically Significant Marine Areas (EBSAs; CBD, 2014). Additionally, this region includes different biogeographic provinces with contrasting thermohaline features, current systems, and water-mass properties, leading to diversification of biodiversity and ecosystems (Bourlès et al., 1999, Assunção et al., 2020, Dossa et al., 2021, Costa da Silva et al., 2021, Tosetto et al., 2021).

We conducted an integrative study of the ecology of lanternfishes, taking advantage of a comprehensive dataset collected in the SWTA. First, we assessed their vertical migration and trophic ecology by coupling information on their abundance, vertical distribution, habitat (oxygen, temperature and fluorescence), and trophodynamics. We did this by exploring the main trophic links of lanternfishes through the analysis of stable isotopes (carbon and nitrogen) of size fractions of zooplankton, gelatinous organisms, crustaceans, fish larvae, and epipelagic and deep-sea fish predators. Second, we assessed the importance of the influence of oceanographic features on lanternfishes by comparing their species composition, spatial distribution, and assemblage structuring under two different physicochemical scenarios. Finally, we discuss the functional roles of lanternfishes.