Insights into the ecology of epibenthic calcareous foraminifera from a colonization study at 4000 m (Station M) in the NE Pacific Ocean

Abstract

Benthic foraminifera are an abundant and important component of modern and ancient deep-sea ecosystems, and these single-celled organisms generate a fossil record that facilitates the assessment of paleoceanographic changes through time. Despite recent advances in taxonomic and ecological information about deep-sea foraminifera, many basic questions remain, requiring a better understanding of ecological tolerances, morphologic plasticity, and distribution of deep-sea foraminiferal species. This study focuses on the phylogenetics, morphology, and colonization dynamics of deep-sea foraminifera at abyssal Station M in the eastern Pacific Ocean. After 368 days at 4000 m on the Pacific Ocean seafloor, 546 foraminifera ~80% of which were calcareous species, occupied elevated substrate experiments. Genetic analyses of the most abundant calcareous foraminiferal taxon indicate that this trochospiral species is a morphological variant of Cibicidoides wuellerstorfi (referred to as C. wuellerstorfi var. lobatulus). Although Pyrgo and other milioline foraminifera are commonly found within sediments, two morphological variants of Pyrgo colonized elevated substrates at the Station M study site. Many Pyrgo spp. and C. wuellerstorfi var. lobatulus, were covered in an organic cyst, perhaps as a feeding structure. These results suggest that these calcareous foraminifera are able to flourish in deep-sea settings where hard substrates are available, and may be more widely distributed and diverse in lower bathyal and upper abyssal habitats when elevated substrates are present.

Introduction

As global ocean conditions change and human influences on marine habitats increase, an understanding of the tolerances, preferences, and distribution patterns of deep-sea organisms is critical for predictions of potential impacts of environmental change on marine ecosystems, as well as to inform paleo-studies using fossil foraminifera. Climate change models predict a number of negative consequences for marine habitats, including the expansion of oxygen minimum zones (e.g. Diaz and Rosenberg, 2008; Moffitt et al., 2015), elevated temperatures and ocean acidification (e.g. Hale et al., 2011). In addition, deep-seafloor habitats with hard substrates are targeted for polymetallic mining that will damage poorly studied ecosystems (Amon et al., 2016; Goineau and Gooday, 2017; Vanreusel et al., 2016).

Benthic foraminifera are an abundant and important component of deep-sea ecosystems (e.g. Gooday and Jorissen, 2012; Gooday, 2003). These single-celled organisms generate a fossil record that facilitates the assessment of paleoceanographic changes through time (e.g. Gooday, 1994; Jorissen et al., 2007; Katz et al., 2010). Distribution patterns and determination of ecological tolerances of deep-sea benthic foraminifera have commonly been determined through analyses of core top sediments that typically include a mixture of living, living + dead, and fossil specimens (e.g. Dessandier et al., 2018; Gooday and Jorissen, 2012; Jorissen and Wittling, 1999; Jones, 2013; Mackensen et al., 1995; Mackensen and Douglas, 1989). Substantial differences exist between living populations and the living + dead assemblages found in core tops, especially those from habitats where fragile agglutinates occur and/or post-mortem dissolution of calcareous foraminifera is likely (Murray and Alve, 1999; Rathburn and Miao, 1995; Stefanoudis et al., 2017). In some cases, infaunal taxa exposed to corrosive pore waters within organic-rich sediments may be prone to post-mortem dissolution, while in other environments epifaunal foraminifera, those that live at or above the sediment-water interface, may be more susceptible to post-mortem destruction (e.g. Loubere and Gary, 1990). Benthic foraminifera are often among the pioneer organisms colonizing the deep-sea, including soft substrates (e.g. Hess et al., 2001) and hard, elevated surfaces (e.g. Beaulieu, 2001a, b; Burkett et al., 2016; Lutze and Thiel, 1989; Mullineaux, 1987). Abundant epifaunal foraminifera have been reported living in a variety of deep-sea habitats, including oxygen-poor conditions (Burkett et al., 2016; Rathburn et al., 2018; Venturelli et al., 2018). The presence of substrates (e.g. manganese nodules, Gooday et al., 2017a, b) and coarse grains at the sediment-water interface (e.g. Schönfeld, 2002; Venturelli et al., 2018) are believed to facilitate higher epifaunal abundances in areas of low oxygen (Venturelli et al., 2018). The use of artificial substrates is a reliable means to assess ecological tolerances of colonizing organisms in deep-sea habitats (e.g. Levin et al., 2006). Early artificial substrate experiments examining foraminiferal colonization included comparisons of colonization plates of slate deployed in areas of active, and nearby inactive, hydrothermal vents (Van Dover et al., 1988). More recently, Burkett et al. (2016) reported over 1000 specimens of Cibicidoides wuellerstorfi (epifaunal) colonizing elevated artificial substrates in active methane seeps and adjacent non-seep environments. These results were unexpected because sediment-based studies generally suggested that C. wuellerstorfi could not tolerate the dysoxic conditions of the study area (Burkett et al., 2016 and references therein). In one of the relatively few experimental studies that examined deep-sea foraminifera colonizing artificial substrates in regions characterized by muddy substrates, Beaulieu (2001a) found that calcareous epifaunal foraminifera were the dominant colonizers of glass rods deployed in the soft sediment environments of Station M (4000 m) in the eastern Pacific Ocean. Results of in situ studies such as those of Beaulieu (2001a) and Burkett et al. (2016) demonstrate the efficacy of in situ, deep-sea experiments using artificial substrates to assess foraminiferal ecology and tolerances, and highlight the need for investigations that target modern distribution and ecological tolerances of these paleoceanographically important organisms.

Small sub-unit ribosomal DNA (SSU rDNA) is a suitable marker for genetic identification of planktonic and benthic foraminifera (André et al., 2014; Pawlowski et al., 2013). Genetic investigations of protists have revealed high diversity and have led to the discovery of several cryptic species (De Vargas et al., 1999; Pawlowski et al., 2014). Some lineages of planktonic and shallow-water benthic foraminifera have high molecular variability (Darling et al., 2004; Hayward et al., 2004; Pillet et al., 2013), while some abyssal benthic foraminifera have shown a low genetic diversity (Lecroq et al., 2009; Pawlowski et al., 2007). Despite recent advances in taxonomy and ecology of deep-sea foraminifera, many basic questions remain about functional morphology, morphologic based species differentiation, and dispersion and distribution methodologies of foraminiferal species (Alve and Goldstein, 2002, 2003; Bernhard et al., 2012; Kucera et al., 2017).

Benthic foraminiferal dispersion is thought to be possible through four different mechanisms. Three of these mechanisms are passive and include: direct release of gametes, zygotes, or of embryonic juveniles (e.g. propagules) into the water column at a reproductive event; a meroplanktonic juvenile life stage and transportation via currents; and entrainment of different growth stages into the water column and subsequent transport (Alve, 1999). The active (fourth) mechanism of transport is through self-locomotion, the rate of which is limited to a few centimeters per day (Alve, 1999). Transportation of embryonic juveniles is likely to be the main mechanism of transportation, especially for attached, tubular, and larger foraminifera. Propagules of foraminifera can remain in a cryptic state and establish a substantial bank of individuals in water depths and environments very different from those occupied by conspecific adults (Alve and Goldstein, 2003; Goldstein and Alve, 2011). It is unknown how long propagules of deep-sea species are able to remain dormant (possibly for days to years, Alve, 1999) or how far they are able to disperse, but given the global distribution and abundance of most species of benthic foraminifera, it is thought that the propagule bank is well established and is the mechanism behind the ability of foraminifera assemblages to rapidly colonize disturbed habitats (Goldstein and Alve, 2011).

The goal of this study was to evaluate the phylogenetics, morphology, and colonization dynamics of calcareous benthic foraminifera at Station M (4000 m) in the Pacific Ocean. The specific objectives were to: 1) compare the genetic profile of Cibicidoides specimens colonizing artificial substrates (Seafloor Epibenthic Attachment Cubes or SEA³s) at Station M with those of other Cibicidoides species from other locations around the globe; 2) compare the morphological characteristics of the tests of Cibicidoides specimens collected at Station M with those of genetic conspecific specimens from other locations; 3) assess colonization, including abundances, substrate attachment, and taxonomy of foraminifera attaching to SEA³s that have remained on the seafloor at Station M for ~ one year.