Marine Vertebrates Impact the Bacterial Community Composition and Food Webs of Antarctic Microbial Mats

Abstract

The biological activity of marine vertebrates represents an input of nutrients for Antarctic terrestrial biota, with relevant consequences for the entire ecosystem. Even though microbial mats assemble most of the biological diversity of the non-marine Antarctica, the effects of the local macrofauna on these microecosystems remain understudied. Using 16S rRNA gene sequencing, 13C and 15N stable isotopes, and by characterizing the P and N-derived nutrient levels, we evaluated the effects of penguins and other marine vertebrates on four microbial mats located along the Antarctic Peninsula. Our results show that P concentrations, C/N and N/P ratios, and δ15N values of “penguin-impacted” microbial mats were significantly higher than values obtained for “macrofauna-free” sample. Nutrients derived from penguin colonies and other marine vertebrates altered the trophic interactions of communities within microbial mats, as well as the relative abundance and trophic position of meiofaunal groups. Twenty-nine bacterial families from eight different phyla significantly changed with the presence of penguins, with inorganic nitrogen (NH4+ and NO3–) and δ15N appearing as key factors in driving bacterial community composition. An apparent change in richness, diversity, and dominance of prokaryotes was also related to penguin-derived nutrients, affecting N utilization strategies of microbial mats and relating oligotrophic systems to communities with a higher metabolic versatility. The interdisciplinary approach of this study makes these results advance our understanding of interactions and composition of communities inhabiting microbial mats from Antarctica, revealing how they are deeply associated with marine animals.

The impact of marine vertebrates on polar terrestrial invertebrate communities

“…To address some of these issues, Bokhorst et al (2019b) only sampled equivalent substrates (the same moss species) from sites with and without ornithogenic influence, reporting increased abundance of nematodes. Studies reporting lower nematode abundance in fertilised areas often included different vegetation types between ornithogenically-influenced and non-influenced sites (Smykla et al 2018), or were based on work at sites separated by several hundred kilometres (Almela et al 2022). These differences highlight that, at present, insufficient comparable studies are available to enable the role that nutrients can play in shaping Antarctic terrestrial communities to be assessed with confidence.…”

“…One study focused exclusively on nematodes (Raymond et al 2013). The remaining six studies included multiple invertebrate groups, including those mentioned previously as well as tardigrades, rotifers and the microfaunal groups of ciliates and testate amoebae (Petz 1997;Sinclair 2001;Porazinska et al 2002;Smykla et al 2018;Bokhorst et al 2019a;Almela et al 2022).…”

“…Notwithstanding the type and location of vertebrate aggregation, nutrients originating from their faeces do not remain within the area but can enrich ecosystems even up to many kilometres away (Erskine et al 1998;Crittenden et al 2015;Bokhorst et al 2019a). As the nutrient loading diminishes with distance from the vertebrate aggregation, vegetation can benefit from the additional nutrients and flourish (Sinclair et al 2006;Smykla et al 2007;Zwolicki et al 2015;Almela et al 2022) with beneficial consequences for associated fauna.…”

“…Allochthonous nutrients typically promote vegetation growth, significantly modify its structure and composition, and have a cascade of impacts through other trophic levels and on various ecosystem processes (e.g. (Mulder et al 2011;Otero et al 2018;De La Peña-Lastra 2021;Almela et al 2022). Vertebrate fertilisation of terrestrial habitats has been reported from the polar regions (Panagis 1985;Smith 1988Smith , 2008Smith and Froneman 2008;Zmudczyńska et al 2012;Zwolicki et al 2016b;Bokhorst et al 2019a, b), where low temperatures, and limited nutrient and water availability often constrain physiological and community processes (Thomas et al 2008).…”

“…This fertilization effect is often quantified through analyses of nitrogen content of plant material, and causally linked to a marine origin using nitrogen stable isotopes (δ 15 N) (Erskine et al 1998;Crittenden et al 2015;Bokhorst et al 2019a, b). Plants and algae, both living and dead, may be directly consumed by invertebrates (Hodkinson et al 1994;Zawierucha et al 2019;Almela et al 2022). Favourable microenvironmental conditions are created amongst foliage (including within macroscopic algal and other microbial mats) and in the underlying soil, providing shelter from cold, drought, abrasion and excessive solar radiation for both invertebrates and their food including algae, fungi, bacteria and larger prey (Coulson et al 2003;Bokhorst et al 2007;Thomas et al 2008).…”