Evolution of Environmental Adaptation of Lanternfishes

Early Paleogene pelagic sediments have rarely been explored for otolith research. Outer-shelf to upper-slope Paleocene sediments from Bavaria yielded fairly abundant stomiiform otoliths as the only reliable indicators of deep-water conditions (Schwarzhans Reference Schwarzhans2012). The early myctophid otolith finds from the Eocene are relatively sparse in a variety of inner- to outer-shelf and upper-slope environmental settings (Fig. 4). For instance, Diaphus? marambionis was found in middle Eocene sediments of Seymour Island, Antarctica, in a very shallow, nearshore environment, associated with abundant macrourid otoliths (Schwarzhans et al. Reference Schwarzhans, Mörs, Engelbrecht, Reguero and Kriwet2017). In New Zealand, too, myctophid otoliths are relatively rare in inner- to outer-shelf settings during the Eocene, being absent in genuine offshore bathyal sediments (Schwarzhans Reference Schwarzhans2019). Myctophids are, however, locally abundant in the middle Eocene of the Aquitaine Basin in SW France in outer-shelf to upper-slope environments (Nolf Reference Nolf1988; Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016) but mostly not exceeding 25% of the assemblage, except for certain locations in the late middle Eocene, where apparently they can reach up to 85% (Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016) (Fig. 4, Supplementary Material 3). These paleobiotopes are interpreted to have been located in a “deep neritic” environment (Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016). Recently, Schwarzhans (Reference Schwarzhans2019) described several assemblages from middle and upper Eocene sediments of New Zealand deposited at depths ranging from 200 to 700+ m. These assemblages provide a rare insight into Paleogene deep-sea fish faunas containing otoliths of the families Bregmacerotidae, Gonostomatidae, Sternoptychidae, Macrouridae, and Ophidiidae, but no Myctophidae (except for a very few in the most shallow-water location studied). We interpret the occurrence of myctophids in SW France and their absence in New Zealand as an indication that these fishes lived over the deep-shelf and upper-slope environments in the middle and late Eocene but were not yet adapted to a mesopelagic habitat. Based on the limited data currently available, it seems that they first thrived over the continental break beginning in the middle Eocene before expanding into the mesopelagic zone. However, the transition from a deep-shelf continental to a mesopelagic habitat likely occurred gradually, and it is therefore possible that such an ecological transition took place during the middle to late Eocene. For instance, the Macrouridae and Ophidiidae in the bathyal late Eocene of New Zealand were represented by a single species each, while different taxa existed on the shelf, indicating the initiation of a migration into deep waters and a progressive depth segregation of involved species. These assemblages also included representatives of families that currently do not live off the shelf (Hemerocoetidae and Platycephalidae), apparently an indication of a failed attempt to invade the deep sea. We interpret these findings as an evidence of the fact that during the Eocene bregmacerotids already lived in the mesopelagic zone and stomiiforms in the bathypelagic zone, while myctophids stayed over the shelf and the upper slope. Certain groups of typical extant benthopelagic fishes like macrourids and ophidiids (Neobythitinae) started to migrate into the deep sea during that period (Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016; Schwarzhans Reference Schwarzhans2019) (Fig. 4, upper left).

Figure 4. Aspects of the population of the deep-sea Myctophidae and selected other groups. Interpretation of bathymetric and oceanic habitat of selected teleost groups in the Eocene halothermal (HTC) ocean (upper left), Oligocene early thermohaline (THC) ocean (upper right), middle Miocene climate optimum (MCO) (lower left), and during the time of the biogenic bloom (lower right). Black arrows indicate presumed phases of down-slope or open-oceanic migrations. White arrows indicate presumed established diel vertical migration in myctophids.

The picture changed drastically in the early Oligocene, as demonstrated by the unique otolith assemblages described by Nolf and Steurbaut (Reference Nolf and Steurbaut1988, Reference Nolf and Steurbaut1990, Reference Nolf and Steurbaut2004) from Pizzocorno and Vigoponzo in Italy and corroborated by the articulated skeletal remains from the Czech Republic, North Caucasus, Poland, Romania, and Ukraine (e.g., Přikryl et al. Reference Přikryl, Schwarzhans and Kovalchuk2017 and literature cited therein). The Italian faunas exhibit a diverse and rich assemblage of myctophid, macrourid, and ophidiid (neobythitine) otoliths, suggesting that myctophids moved off the shelf into the oceanic realm and macrourids and neobythitines ventured further into the deep sea and diversified (Fig. 4, upper right). This is the earliest record where myctophids represent the majority of an otolith assemblage in a pelagic environment characterized by bathyal depths (Fig. 3, Supplementary Material 3). The basal part of the early Oligocene is also remarkable for the occurrence of some large-growing “super-sized” Diaphus taxa (D. molossus and D. stafforaensis) (see Brzobohatý and Nolf Reference Brzobohatý and Nolf1995), with otoliths that reached sizes up to nearly 8 mm OL (Fig. 3, Supplementary Material 2).

During the late Oligocene and Neogene, lanternfishes apparently became a prominent mesopelagic fish family, and their otoliths started to dominate otolith assemblages in pelagic sediments (Nolf and Brzobohatý Reference Nolf and Brzobohatý2002; Schwarzhans Reference Schwarzhans2019) (Supplementary Material 3). All the major myctophid groups and a large part of the extant genera are known based on fossil otoliths (Fig. 2), which document a diversification pattern that is consistent with the molecular estimations proposed by Denton (Reference Denton2018). Due to the abundance of myctophid otoliths in offshore pelagic sediments since the Oligocene, we postulate that they were adapted to their current lifestyle, which possibly included diel vertical migrations. However, some species persisted on the shelf, for instance, in the North Sea Basin (Schwarzhans Reference Schwarzhans2010b) or tropical South America (Schwarzhans and Aguilera Reference Schwarzhans and Aguilera2013). During the late Oligocene up to the mid-Miocene climate transition (MMCT), the majority of the otolith-based Diaphus species remained below the 5 mm OL threshold (about 80–110 mm SL) (Fig. 3, Fig. 4, lower left). During the late Miocene, Pliocene, and Quaternary, an increase in the number of species is observed as well as the gradual occurrence of some large-growing Diaphus species (Fig. 3). This can be interpreted as an indication of the appearance of possibly more stationary, benthopelagic species on the continental slope, in addition to a sustained diversification of myctophids in the mesopelagic zone (Fig. 4, lower right).

The Rise of Myctophids in the Oceanic Trophic Web and Its Paleoceanographic Context

Extant myctophids feed primarily on planktonic crustaceans (copepods, euphasiids, and amphipods) in the epipelagic zone during their diel vertical migration (e.g., Tanaka et al. Reference Tanaka, Ohshimo, Sassa and Aoki2007). These planktonic crustaceans in turn feed mostly on phytoplankton, which nowadays consist mainly of diatoms and silicoflagellates (Sommer et al. Reference Sommer, Stibor, Katechakis, Sommer and Hansen2002). Planktonic crustaceans are rather rare in the fossil record (Briggs et al. Reference Briggs, Weedon, Whyte and Benton1993; Rigby and Milsom Reference Rigby and Milsom2000), so we have used diatom diversity and abundance as proxies for the primary productivity (Renaudie Reference Renaudie2016) relevant for myctophids (Fig. 3). The presence and abundance of diatoms are primarily linked to the availability of silicon and phosphorus. These elements can be abundant in upwelling systems (Sommer et al. Reference Sommer, Stibor, Katechakis, Sommer and Hansen2002) or can be consistently provided by terrestrial denudation and runoff from continents, with a considerable contribution from grasslands (Kidder and Gierlowski-Kordesch Reference Kidder and Gierlowski-Kordesch2005; Beerling and Osborne Reference Beerling and Osborne2006; Edwards et al. Reference Edwards, Osborne, Strömberg and Smith2010; Strömberg Reference Strömberg2011; Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015; Pellegrino et al. Reference Pellegrino, Pierre, Natalicchio and Carnevale2018). In the shortened food webs characteristic of upwelling systems and in other oceanic settings with a high silica budget, the planktonic crustaceans occupy the immediate basal trophic level compared with myctophids (Sommer et al. Reference Sommer, Stibor, Katechakis, Sommer and Hansen2002), while in oligotrophic oceanic systems the food chain starts with picoplankton, resulting in a longer food chain (Sommer et al. Reference Sommer, Stibor, Katechakis, Sommer and Hansen2002). The shortened food chain typical of upwelling systems may sustain an efficient transfer of organic carbon to apex predators (Ryther Reference Ryther1969), thereby generating favorable conditions for the thriving of large filter feeders, that is, whales (Berger Reference Berger2007). Mysticete cetaceans are food competitors of lanternfishes for planktonic crustaceans, as well as their predators (Kawamura Reference Kawamura1980). We have therefore used the rather well documented fossil record of mysticete cetaceans (Fordyce and Barnes Reference Fordyce and Barnes1994; Berger Reference Berger2007; Marx and Uhen Reference Marx and Uhen2010; Marx et al. Reference Marx, Lambert and Uhen2016, Reference Marx, Buono, Evans, Fordyce, Reguero and Hocking2019; Bianucci et al. Reference Bianucci, Marx, Collareta, Di Stefano, Landini, Morigi and Varola2019) as a proxy for the evolutionary history of relevant competitors and predators of lanternfishes.

The rare myctophid otoliths from the late Paleocene to the middle Eocene are found in a variety of neritic settings (Schwarzhans Reference Schwarzhans1985, Reference Schwarzhans2019; Nolf Reference Nolf1988; Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016) and are small in size (Fig. 3, Supplementary Material 2 and 3), exhibiting a low degree of morphological diversity. Myctophid otoliths were locally abundant over outer-shelf settings since the late middle Eocene (Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016). The first major event that impacted lanternfish evolution appears to be the EOT. The EOT was characterized by a global cooling event and the termination of the foregoing greenhouse conditions apparently associated with a secular reduction of atmospheric CO₂ (Zachos et al. Reference Zachos, Dickens and Zeebe2008; Beerling and Royer Reference Beerling and Royer2011) and the onset of the Antarctic ice sheet (e.g., Lear et al. Reference Lear, Rosenthal, Coxall and Wilson2004). The EOT marked the transformation of the deep-ocean circulation from halothermal (HTC), primarily driven by density gradients linked to the salinity of the water masses, to thermohaline (THC), primarily driven by temperature gradients (McClain and Hardy Reference McClain and Hardy2010; Katz et al. Reference Katz, Cramer, Toggweiler, Esmay, Liu, Miller, Rosenthal, Wade and Wright2011). The HTC circulation resulted from the formation of warm, saline, low-oxygen deep waters induced by stratification, whereas the THC circulation resulted from the formation of high-latitude cold and oxygenated deep waters (Katz et al. Reference Katz, Cramer, Toggweiler, Esmay, Liu, Miller, Rosenthal, Wade and Wright2011; McClain and Hardy Reference McClain and Hardy2010; Norris et al. Reference Norris, Turner, Hull and Ridgwell2013). However, the exact sequence and timing of the events with respect to the different oceanic circulation patterns involved and their causes remain a matter of discussion (see, e.g., Katz et al. Reference Katz, Cramer, Toggweiler, Esmay, Liu, Miller, Rosenthal, Wade and Wright2011; Goldner et al. Reference Goldner, Herold and Huber2014; Coxall et al. Reference Coxall, Huck, Huber, Lear, Legarda-Lisarri, O'Regan, Sliwinska, van de Flierdt, de Boer, Zachos and Backman2018). Between 36 and 33 Ma, a combination of geodynamic and paleoceanographic events led to a general restructuring of the global ocean system, including the isolation of Antarctica and formation of the (initial) Antarctic Circumpolar Current (Kennett Reference Kennett1977; Kennett and Exon Reference Kennett and Exon2004; Scher and Martin Reference Scher and Martin2006; Barker et al. Reference Barker, Filippelli, Florindo, Martin and Scher2007; Strugnell et al. Reference Strugnell, Rogers, Prodöhl, Collins and Allcock2008; Katz et al. Reference Katz, Cramer, Toggweiler, Esmay, Liu, Miller, Rosenthal, Wade and Wright2011; Houben et al. Reference Houben, Bijl, Pross, Bohaty, Passcjier, Stickley, Röhl, Sugisaki, Tauxe, van de Flierdt, Olney, Sangiorgi, Sluijs, Escutia and Brinkhuis2013), formation of the North Atlantic Deep Water Current induced by an increase in seawater density caused by polar cooling and following the submersion of the Arctic Ocean to North Atlantic swell for deep-water flow (Berger Reference Berger2007; Katz et al. Reference Katz, Cramer, Toggweiler, Esmay, Liu, Miller, Rosenthal, Wade and Wright2011; Borrelli et al. Reference Borrelli, Cramer and Katz2014; Coxall et al. Reference Coxall, Huck, Huber, Lear, Legarda-Lisarri, O'Regan, Sliwinska, van de Flierdt, de Boer, Zachos and Backman2018), demise of the Tethyan deep-water connection (Jovane et al. Reference Jovane, Coccioni, Marsili, Acton, Koeberl and Montanari2009; Steeman et al. Reference Steeman, Hebsgaard, Fordyce, Ho, Rabosky, Nielsen, Rahbek, Glenner, Sørensen and Willerslev2009; Zhang et al. Reference Zhang, Nisancioglu, Flatøy, Bentsen, Bethke and Wang2011), and denudation of adjacent uplifted terrains (Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015). The cooling and oxygenation of the deep oceanic masses induced migration of new taxa into the deep sea (Miller et al. Reference K. G., Katz and Berggren1992; Thomas Reference Thomas, Monechi, Coccioni and Rampino2007). Among fishes, these oceanographic changes resulted in an accelerated migration of benthopelagic fishes, for example, of the Macrouridae and Neobythitinae (Ophidiidae) (Nolf and Steurbaut Reference Nolf and Steurbaut1988, Reference Nolf and Steurbaut1990, Reference Nolf and Steurbaut2004; Lin et al. Reference Lin, Nolf, Steurbaut and Girone2016; Schwarzhans Reference Schwarzhans2019), into the deep sea. Conversely, Sibert et al. (Reference Sibert, Zill, Frigyik and Norris2020) did not recognize any state change in pelagic fish production and biodiversity during the EOT based on investigations of microfossil fish teeth from deep-sea drilling samples. However, due to the limited taxonomic resolution offered by ichthyoliths, it is not possible to identify the emergence and duration of fundamental changes of lifestyles, such as migration into the deep sea or the mesopelagic high ocean realms. The reorganization of the oceanic system and the formation of the THC led to the establishment of upwelling systems, particularly in the Southern Ocean (Berger Reference Berger2007). This, in combination with an assumed locally elevated silica influx from the continents (e.g., Antarctica; see Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015), is thought to have resulted in a massive radiation of diatoms both in terms of diversity and abundance (Lazarus et al. Reference Lazarus, Barron, Renaudie, Diver and Türke2014; Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015; Renaudie Reference Renaudie2016; Lowery et al. Reference Lowery, Bown, Fraass and Hull2020). The terminal Eocene is also the time of the first occurrence of mysticete whales (Fordyce and Marx Reference Fordyce and Marx2018; Buono et al. Reference Buono, Fordyce, Marx, Fernández and Reguero2019; Muizon et al. Reference Muizon, Bianucci, Martínez-Cáceres and Lambert2019), which, however, were not filter feeders. The early radiation of modern cetaceans has been interpreted as having been driven by this ocean restructuring (Fordyce Reference Fordyce, Prothero, Ivany and Nesbitt2003; Berger Reference Berger2007; Steeman et al. Reference Steeman, Hebsgaard, Fordyce, Ho, Rabosky, Nielsen, Rahbek, Glenner, Sørensen and Willerslev2009; Marx and Uhen Reference Marx and Uhen2010). As far as lanternfishes are concerned, Nolf and Steurbaut (Reference Nolf and Steurbaut1988, Reference Nolf and Steurbaut1990, Reference Nolf and Steurbaut2004) described the first exclusive bathyal otolith assemblage with a rich mesopelagic myctophid component from the basal Oligocene, a time during which the THC regime is thought to have been firmly established in the western Tethys (Coccioni and Galeotti Reference Coccioni, Galeotti, Prothero, Ivany and Nesbitt2003). Myctophids constituted about 30% to more than 50% of the otolith assemblage (calculated from Nolf and Steurbaut Reference Nolf and Steurbaut2004; Fig. 3, Supplementary Material 3). Intriguingly, there is an apparent acme of diatom diversity and abundance during the terminal Eocene/basal Oligocene associated with a short-term occurrence of gigantic mysticete predators (Marx et al. Reference Marx, Buono, Evans, Fordyce, Reguero and Hocking2019) and certain supersized Diaphus species (Fig. 3, Supplementary Material 2). It is interesting to note that this late Eocene–early Oligocene pulse in diatom radiation and upscaling of certain whales and myctophids coincided with a putative increase in silica influx to the sea, particularly in the Southern Ocean (Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015). The Antarctic species Diaphus? marambionis was originally considered to be of early Eocene, Ypresian age (Schwarzhans et al. Reference Schwarzhans, Mörs, Engelbrecht, Reguero and Kriwet2017), but the strata from which it was obtained has more recently been referred to the Bartonian, based on the stratigraphic scheme published by Buono et al. (Reference Buono, Fordyce, Marx, Fernández and Reguero2019). It was found at the same location and level as the earliest-recorded basking shark (Cetorhinidae; Cione and Reguero Reference Cione and Reguero1998; Welton Reference Welton2013) and in a slightly older level than the abovementioned gigantic mysticete predator in Antarctica (Fig. 3). The size of the otoliths of Diaphus and Eomyctophum species shows a gradual increase from 1.6–3.0 mm OL in the early Eocene to 3.3–7.7 mm OL in the basal Oligocene.

Shortly after the basal Oligocene, the otolith sizes of the Diaphus species drop back into the range of 2.0–5.0 mm OL, a pattern that persisted throughout the late Oligocene to the early middle Miocene (Fig. 3, Supplementary Material 2). In fact, their small size is so remarkable in samples that it can be regarded as a reliable stratigraphic feature for their distinction from the Late Miocene and Pliocene myctophid assemblages. Similarly, there are no more records of giant mysticetes in this time interval. Also, the abundance and diversity of diatoms seemingly dropped back to the level of a generally increasing background trend, except for a single short-lived abundance peak in the late Oligocene (Renaudie Reference Renaudie2016). The abundance of myctophid otoliths reached high levels in pelagic environments during this time (Nolf and Brzobohatý Reference Nolf and Brzobohatý2002; Schwarzhans Reference Schwarzhans2019; Fig. 3, Supplementary Material 3), with the caveat, however, that relatively few bathyal otolith assemblages are known from the late Oligocene and early Miocene. The morphological diversity of myctophids generally continued to increase, and during the early to early middle Miocene (Burdigalian to Langhian), the majority of extant genera came into existence (Fig. 2) (see also molecular phylogenetic estimates of Denton [2018]). The present highly diverse genus Diaphus, however, was represented by a relatively modest number of species in this interval (4 to 10 species per time interval), still displaying a relatively low level of morphological diversity. In mysticete cetaceans likewise, the disparity increased, and the first bulk filter feeders appeared (Marx and Fordyce Reference Marx and Fordyce2015; Marx et al. Reference Marx, Lambert and Uhen2016; Fordyce and Marx Reference Fordyce and Marx2018). The body size of the mysticetes during that time interval barely reached 8 m in total length (Slater et al. Reference Slater, Goldbogen and Pyenson2017; Bianucci et al. Reference Bianucci, Marx, Collareta, Di Stefano, Landini, Morigi and Varola2019). The cause of this decrease in the size of lanternfishes (as exemplified by the most common genus Diaphus) and mysticete cetaceans and the associated reduction in diversity of diatoms is still not well understood. It may be related in some ways to a phase of global warming, that is, the late Oligocene warming (LOW) and the Miocene climate optimum (MCO) in the early Miocene (Burdigalian) and the early middle Miocene (Langhian). Cermeño et al. (Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015) associated the observed decrease in diatom abundance and diversity with a reduced level of silica input in the Southern Ocean and a generally somewhat lowered silica influx in the global oceanic system.

The short period of the MMCT during the Serravallian marked the onset of a further stage of global cooling and change in deep-ocean circulation (Flower and Kennett Reference Flower and Kennett1994). Diatom diversity increased again (Lazarus et al. Reference Lazarus, Barron, Renaudie, Diver and Türke2014), showing a distinct peak in abundance (Renaudie Reference Renaudie2016). The continental denudation in response to the main phase of Alpine–Himalayan orogenesis (Peucker-Ehrenbrink et al. Reference Peucker-Ehrenbrink, Ravizza and Hofmann1995) and the global affirmation of phytolith-rich, grass-dominated ecosystems are regarded as the main drivers for the rising fluxes of silica responsible for the renewed diatom burst (Kidder and Gierlowski-Kordesch Reference Kidder and Gierlowski-Kordesch2005; Edwards et al. Reference Edwards, Osborne, Strömberg and Smith2010; Strömberg Reference Strömberg2011; Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015). Both mysticete cetaceans (Bianucci et al. Reference Bianucci, Marx, Collareta, Di Stefano, Landini, Morigi and Varola2019) and myctophids, particularly of the genus Diaphus, show an increase in diversity and size (Fig. 3). Myctophid otoliths are firmly established as the dominant group in otolith assemblages from pelagic sediments (50%–80%; Fig. 3), for example, in the Mediterranean (Brzobohatý and Nolf Reference Brzobohatý and Nolf2000), tropical West Africa (Schwarzhans Reference Schwarzhans2013c), and New Zealand (Schwarzhans Reference Schwarzhans2019) (Supplementary Material 3).

Beginning with the late Miocene, the myctophid speciation rate continued to accelerate until today, which is consistent with the molecular estimation proposed by Denton (Reference Denton2018), particularly within the genus Diaphus (Fig. 3, Supplementary Material 2). Myctophid otoliths are the most common in all studied pelagic sediments, with percentages ranging between 40% and 95% of the specimens (Fig. 3, Supplementary Material 3). A dramatic increase occurred in the sizes of the otoliths in some lanternfishes, for example, certain species of the genera Diaphus, Lampadena, Myctophum, Notoscopelus, and Symbolophorus. Within the species-rich genus Diaphus, maximum otolith sizes increased from 6.7 mm OL in D. pedemontanus (Robba, Reference Robba1970) in the Tortonian to 8.7 mm OL in D. coatesi Schwarzhans and Aguilera, Reference Schwarzhans and Aguilera2013 in the Piacenzian and Gelasian, and eventually to 10.5 mm OL in the extant D. adenomus (Schwarzhans and Aguilera Reference Schwarzhans and Aguilera2013) (Fig. 3, Supplementary Material 2). Late Miocene and younger pelagic sediments can often be readily recognized because of the abundance of large myctophid otoliths, always associated with a number of small-sized species as well. The late Miocene (Tortonian) to Recent interval was also characterized by mysticete gigantism (Bianucci et al. Reference Bianucci, Marx, Collareta, Di Stefano, Landini, Morigi and Varola2019) that culminated with the evolution of the extant blue whale, the largest animal that ever existed on Earth. Mysticete diversity was at its peak during the late Miocene and early Pliocene, followed by a drastic decrease since the late Pliocene (Marx and Fordyce Reference Marx and Fordyce2015). The decrease of the diversity of mysticete cetaceans took place primarily at the expense of smaller species, while gigantism developed further. The gigantism has been interpreted as a reaction to the Arctic glaciation, changes in the distribution and availability of continental shelf habitats, and a greater need to migrate between high-latitude feeding and low-latitude breeding habitats (Berger Reference Berger2007; Marx and Fordyce Reference Marx and Fordyce2015). This is the only interval in the investigated time frame in which the evolution of lanternfishes (i.e., rapid diversification) diverged from that of mysticetes (i.e., diversity contraction). Diatom diversity and abundance increased during this time interval, though with a slight reduction during the Quaternary (Lazarus et al. Reference Lazarus, Barron, Renaudie, Diver and Türke2014; Renaudie Reference Renaudie2016). It is widely believed that the main driver of the diatom radiation and mysticete diversification and gigantism was the so-called biogenic bloom that occurred between 8 and 4 Ma (Cortese et al. Reference Cortese, Gersonde, Hillenbrand and Kuhn2004; Filippelli Reference Filippelli2008). We speculate that the biogenic bloom and its associated expansion of the oxygen minimum zones (see Dickens and Owen Reference Dickens and Owen1994) also represent the main trigger for the increase of diversity and size of the genus Diaphus. Two main mechanisms are currently considered as responsible for the biogenic bloom: an increased input of silica in the oceans caused by the uprising of C₄-type grasslands on the continents (Kidder and Gierlowski-Kordesch Reference Kidder and Gierlowski-Kordesch2005; Strömberg Reference Strömberg2011) and their associated wildfire cycles (Beerling and Osborne Reference Beerling and Osborne2006; Edwards et al. Reference Edwards, Osborne, Strömberg and Smith2010; Pellegrino et al. Reference Pellegrino, Pierre, Natalicchio and Carnevale2018); and the massive erosion of the newly formed alpine mountain chains, especially the Himalayas, which released silica and phosphorus to the marine biosphere (Filippelli Reference Filippelli2008; Cermeño et al. Reference Cermeño, Falkowski, Romero, Schaller and Vallina2015). The initiation of the modern coastal upwelling systems during the late Miocene may have further contributed to the biogenic bloom (Berger Reference Berger2007). The occurrence of supersized Diaphus species that started during the late Miocene (Messinian) and accelerated throughout the Pliocene up to today (Figs. 3, 4) can be tentatively related to the lifestyle of certain large-growing species that abandon diel vertical migration patterns and stay at depths between 300 and 1000 m. The causes of this adaptation remain unknown, although they are likely related in some ways to the abundance of suitable larger, benthic prey. A similar cause may be evocated for the occasional occurrence of large-growing specimens of Lobianchia gemellarii (Cocco, Reference Cocco1838) that occur in expatriate flocks, that is, specimens occurring outside the usual distribution range of the species that do not reproduce because of the unfavorable conditions, mostly temperature related, but may continue to grow to very large sizes (see O'Day and Nafpaktitis Reference O'Day and Nafpaktitis1967; Nafpaktitis Reference Nafpaktitis1968; Hulley Reference Hulley, Whitehead, Bauchot, Hureau, Nielsen and Tortonese1984). Supersized L. gemellarii otoliths, presumably from expatriate flocks, have been observed in the Piacenzian and Gelasian of southern Japan (Schwarzhans and Ohe Reference Schwarzhans and Ohe2019).