Shift in polar benthic community structure in a fast retreating glacial area of Marian Cove, West Antarctica

Impact of glacial retreat on the benthic ecosystem

Most enriched POM δ¹³C concentration in the inner cove location (B2) indicates a potential melt-water input near the glacier (Table S2). The δ¹³C signature of diatoms showed a similar spatial concentration gradient along the cove, but was slightly more enriched than POM δ¹³C. This signature of freshwater influence has also been detected in other Antarctic regions. For example, the enriched δ¹³C of POM and diatoms in Potter Cove was recently reported¹⁶. In the enclosed environment beneath glaciers, δ¹³C might be enriched due to increased HCO₃⁻ utilization and production of organic materials¹⁷. The POM and diatom δ¹⁵N concentrations showed the lack of parallel gradients over the study area. The POM δ¹⁵N, especially phytoplankton values, is affected by their nutrient sources. Snow melt-water input occasionally appears from the local creeks throughout the Marian Cove, and the melt-water is associated with the nutrient input as well. Thus, the POM and diatom δ¹⁵N concentrations seemed to reflect the melt-water input throughout the cove.

The coastline of the inner locations (B1–B2; < 0.5 km to Marian Cove glacier) is covered by snow and ice during winter, and is exposed to the atmosphere during summer. The recent glacier retreats during the 2010s rendered the B1 location ice-free (Fig. 1a). In general, when ice cover melts, a rocky shore is revealed on which diatoms quickly emerge, ultimately attaining considerable biomass¹⁸. In our study area, a sea ice diatom F. striatula covered the inner intertidal rocky shore (B1–B2) like a thick carpet (Fig. 2b). This chain-forming species is likely a rapid colonizer in Marian Cove. Several species belonging to the genus Fragilaria have been previously reported as pioneering diatom taxa in ice-melting areas¹⁹ and estuary²⁰. The inner cove environment seemed to stimulate the early aggregation of chain-forming diatoms, indicating the presence of adaptative community responses in glacier retreat zone.

N. cf. perminuta was the most abundant species at all locations. N. cf. perminuta also dominated on limpet shells at all locations. Limpets are able to tolerate physical stress under rapid temperature change²¹; thus, N. cf. perminuta might share and endure the conditions of limpets by settling on the top of shells. The diatoms on limpet shell might also be exposed to the harshest environments. However, the large abundance of limpets in the benthic environment of Marian Cove might represent the best alternative habitat when lacking in soft bottom sediment, on which they were rarely distributed. N. cf. perminuta is presented in various region of Antarctica including Marian Cove, South Bay, and Ross Sea^5,22,23. The species has also been reported to dominate across various substrates such as cobble²⁴, most of macroalgae²⁵, surface of animals²⁶, and artificial substrate²², although it appeared less on macroalgae in this study area. Thereafter N. cf. perminuta is considered to be one of the best adapted species in Antarctica. The motility of limpets might also explain the broad occurrence of N. cf. perminuta; however, more information on its ecology is required²⁷.

The large numbers of euryhaline diatoms (including N. cf. perminuta) observed across all the locations indicated the presence of melt-water (freshwater) inputs around Marian Cove. However, the high numbers of marine species in subtidal locations (M1–M4) indicated low freshwater input in the deep waters of the cove (Fig. 1). Species diversity was much greater on the muddy bottoms of subtidal deep waters compared to intertidal substrates. Unlike the intertidal zone where few species dominated (F. striatula in inner cove (39.5%) and N. cf. perminuta in outer cove (68.5%)), sedimentary diatoms exhibited relatively high evenness (Table S6). Several diatoms belonging to the genera Navicula and Cocconeis were widespread subtidal species, occupying a distinct zone to intertidal habitats. Finally, relatively consistent proportions of subtidal diatom assemblages were recorded across all the surveyed locations. This phenomenon implies that thermohaline changes more prevailed by ice-melting and/or physical stress of ice-scouring in the intertidal areas than deep waters, supporting observations that shallow waters are relatively fragile to the effects of melting ice¹⁹.

Indicator species

Six indicator species were identified in Marian Cove (p < 0.05 in IndVal), with four species being representative of clusters A, B, C, and D, respectively (Fig. 3a, Table S7). Group A inhabited newly exposed ice-free areas, with dominance of F. striatula, being the indicator species. F. striatula has been reported as an indicator of cooler temperature with presence of floating sea ice throughout the austral summer¹⁰. In the meantime, results from the present study suggest that the species could also indicate the influence of broken pieces of floating sea ice which have drifted to the shore. F. striatula may have settled down on the intertidal zone after last sea ice melted, subsequently becoming a predominant indicator species as rapid colonizer to the newly exposed ice-free area. The indicator species of Group B was N. cf. perminata, which occupied the outer intertidal habitats. This species was able to withstand extreme conditions on hard substrate. The indicator species of Group C were Naviculoid diatoms such as N. glaciei (sea ice diatom) and Navicula directa, which occupied the inner subtidal sediment. N. glaciei seemed to be dominated through a similar process to the F. striatula in the intertidal zone. The dominated occurrence of N. glaciei and F. striatula found in the austral summer would reflect the presence of sea ice during the colder season followed by ice-melting at the time of sampling¹⁰. Of note, some earlier studies have reported the dominance of N. glaciei in the subtidal zone around the glacier retreating area^5,22. Two epiphytic diatoms, C. cf. pinnata²⁸ and P. kamtschaticum²⁹, were the indicator species of Group D. Although these diatoms inhabited sediment, the abundant epiphytic diatom reflected the available habitats for benthic diatoms in the deep waters of cove. The result was generally consistent with the previous studies that documented prevailed subtidal epiphytes on Antarctic macroalgae^23,25,29. These abundant macroalgae colonized in the outer subtidal zone, which might represent the preferable habitat for those taxa.

The lack of overlapping indicator species across the groups supported clear distinct of benthic diatom assemblages among the groups. Overall, our analyses revealed the presence of dynamic, sensitive, and distinct micro-benthic community that was responding to ice melting under the rapidly changing polar environment. In fjord-shaped coves, such as Marian Cove in the present study area, the sea ice of the inner part is the last to disappear. Interestingly, both indicator species of the inner part, viz. F. striatula and N. glaciei were sea ice diatoms, which are released with melting ice during austral spring^10,30. Considerable abundance of diatoms in the inner cove overlapped that of the sea ice diatom. Previous studies also reported that the sea ice diatoms are released into the water column after the sea ice has melted²² and they may settle down on other substrates such as surface of macroalgae²³. Thus, the high abundance of these species likely reflects a temperature cooling event in the area proximal to the glacier retreat region.

Role of benthic diatoms on shift in polar community

Studies investigating the ecological responses of polar benthic organisms to glacier retreat remain limited. Our mini-review demonstrated that ecological responses vary depending on the target taxa present (Fig. 4). The diversity and abundance of macroalgae tends to be lower in inner cove^31,32. In comparison, the diversity and abundance of small organisms, such as meiofauna and diatoms, is higher in the inner cove. During our survey, we documented large benthic diatom blooms in the inner cove (Fig. 2b and Fig. S1b), with previous studies supporting this phenomenon^33,34. The elevated number of epibiotic diatom species in blooms occurring in the subtidal zone potentially indicate the presence of a mature benthic community that is less influenced by ice-melting events. The phenomenon of enriched massive chain-forming diatoms observed in the subtidal zone of Marian Cove was recently documented^5,33. Of note, a higher diatom growth near the glacier at the initial phases of experiment using artificial substrates (macroalgae) was documented in Potter Cove, which is adjacent to Marian Cove³⁵.

To expand our focus on shift of polar benthic community structure, we conducted a mini-review and analyzed meta-data from literatures including the present study (Fig. 5). The result demonstrated that diversity and abundance of polar benthic organisms significantly vary with respect to ecological functioning groups. In other words, the functional diatom groups collectively contributed towards shifting the entire polar benthic community. The polar benthic community shift under the impacts of glacier retreat could be described in three stages. First, the new habitat exposed from retreating glacier and melting ice, then the diatoms melted out from sea ice during the warmer season. These diatoms formed a chain-like union of cells and quickly settled to the newly exposed substrates such as cobble and sediment. Life-forms and cell size are responses to various environmental condition¹². The diatoms appeared to have a strategy to survive the fast-evolving harsh environment, which involved energy-efficient chain clustering³⁶. Interestingly, sea ice pennate diatoms, such as F. striatula, dominated the intertidal zone, whereas centric diatoms, such as Paralia sp., dominated the subtidal zone.

Next, subsequently, microalgal dynamics would stabilize bottom habitats, providing refuge and potential diets to upper trophic organisms, such as meiofauna and/or macrofauna. A considerable number of copepods were observed that inhabited and ate the bushes of chain-form diatom, in the intertidal zone (Fig. 5). Limpets were the dominant macrofauna in the intertidal zone of the Marian Cove. In the subtidal zone, both meiofauna and macrofauna communities were characterized by dominance of opportunistic taxa (nematode³⁷ and opportunistic ascidian³⁸).

Finally, the diversified and enriched stage refers to the flourishing benthic communities through ecologically diverse diatom groups and abundant diatom (bloom) in the subtidal zone⁵, and higher diversity of meiofauna and macrofauna (Fig. 5). Ecological status in the outer intertidal zone, say old habitat, also represented stable community structure with predominance of tolerant species, viz., small motile naviculoid diatoms, to harsh conditions such as salinity fluctuation, wave action, etc.

The diatom communities inhabiting the subtidal zone were divided into two types. First, the dominance of epiphytic diatoms (> 30%) was featured in the subtidal sediments. Second, the chain-form diatom lived on macroalgal and/or macrofaunal colonies in the form of bushes, of which observation was documented by Ahn et al., 2016. Macrofaunal communities in the outer cove represented the matured colonization of macrofauna and/or megafauna, with dominant species including clams, sponges, ascidians, and echinoderms (author observation). During this stage, extensive algal mats of chain-forming diatoms attached to fauna are evidenced, representing the most mature colonization of the benthic polar community⁵. Thus, polar benthic communities are developed through the support of the benthic diatom, a rapid colonizer^35,39, and promoted to diversified and enriched communities in the fast-evolving, harsh polar environment.

The current study is novel in that it investigated both intertidal type habitats and subtidal deep waters simultaneously for polar benthic diatoms. Interestingly, benthic diatom assemblages exhibited diverse ecological responses (with respect to occurrence, distribution, and diversity) to the given environmental settings associated with glacier retreat. First, epilithic diatoms primarily consisted of chain-forming species, which dominated the intertidal cove. Second, epibiotic diatoms on limpets show constant species composition regardless of sampling position (in both inner and outer cove). Finally, the species diversity of epiphytic diatoms varied greatly across locations, but tended to increase in older habitats (viz., habitats that were exposed earlier), confirming the occurrence of micro-floral community shift. Overall, benthic diatoms seem to represent appropriate and promising indicator taxa for monitoring and/or predicting the status of the sensitive polar benthic community and associated long-term changes under the current climate change regime.

Source: Ecology - nature.com