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Ecological Stoichiometry of the Mountain Cryosphere

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Ecological Stoichiometry of the Mountain Cryosphere REVIEW published: 26 September 2019 doi: 10.3389/fevo.2019.00360 Ecological Stoichiometry of the Edited by: Mountain Cryosphere Michelle Evans-White, University of Arkansas, United States Ze Ren 1†§, Nicolas Martyniuk 2†§, Isabella A. Oleksy 3†‡§, Anshuman Swain 4†§ and Reviewed by: Scott Hotaling 5*§ Rana El-Sabaawi, University of Victoria, Canada 1 Flathead Lake Biological Station, University of Montana, Polson, MT, United States, 2 Laboratorio de Limnología, INIBIOMA, Edward Hall, CONICET—Universidad Nacional del Comahue, Bariloche, Argentina, 3 Natural Resource Ecology Laboratory, Colorado State Colorado State University, University, Fort Collins, CO, United States, 4 Department of Biology, University of Maryland, College Park, MD, United States, United States 5 School of Biological Sciences, Washington State University, Pullman, WA, United States James Cotner, University of Minnesota Twin Cities, United States Roughly 10% of the Earth’s surface is permanently covered by glaciers and ice sheets *Correspondence: and in mountain ecosystems, this proportion of ice cover is often even higher. From an Scott Hotaling ecological perspective, ice-dominated ecosystems place harsh controls on life including [email protected] cold temperature, limited nutrient availability, and often prolonged darkness due to †These authors have contributed snow cover for much of the year. Despite these limitations, glaciers, and perennial equally to this work snowfields support diverse, primarily microbial communities, though macroinvertebrates ‡Present address: Isabella A. Oleksy, and vertebrates are also present. The availability and mass balance of key elements Cary Institute of Ecosystem Studies, [(carbon (C), nitrogen (N), phosphorous (P)] are known to influence the population Millbrook, NY, United States dynamics of organisms, and ultimately shape the structure and function of ecosystems § ORCID: worldwide. While considerable attention has been devoted to patterns of biodiversity Ze Ren orcid.org/0000-0002-1473-2697 in mountain cryosphere-influenced ecosystems, the ecological stoichiometry of these Nicolas Martyniuk habitats has received much less attention. Understanding this emerging research orcid.org/0000-0002-2423-7040 Isabella A. Oleksy arena is particularly pressing in light of the rapid recession of glaciers and perennial orcid.org/0000-0003-2572-5457 snowfields worldwide. In this review, we synthesize existing knowledge of ecological Anshuman Swain stoichiometry, nutrient availability, and food webs in the mountain cryosphere (specifically orcid.org/0000-0002-9180-2222 Scott Hotaling glaciers and perennial snowfields). We use this synthesis to develop more general orcid.org/0000-0002-5965-0986 understanding of nutrient origins, distributions, and trophic interactions in these imperiled ecosystems. We focus our efforts on three major habitats: glacier surfaces (supraglacial), Specialty section: This article was submitted to the area beneath glaciers (subglacial), and adjacent downstream habitats (i.e., glacier- Behavioral and Evolutionary Ecology, fed streams and lakes). We compare nutrient availability in these habitats to comparable a section of the journal Frontiers in Ecology and Evolution habitats on continental ice sheets (e.g., Greenland and Antarctica) and show that, in Received: 22 July 2019 general, nutrient levels are substantially different between the two. We also discuss Accepted: 11 September 2019 how ongoing climate warming will alter nutrient and trophic dynamics in mountain Published: 26 September 2019 glacier-influenced ecosystems. We conclude by highlighting the pressing need for Citation: studies to understand spatial and temporal stoichiometric variation in the mountain Ren Z, Martyniuk N, Oleksy IA, Swain A and Hotaling S (2019) cryosphere, ideally with direct comparisons to continental ice sheets, before these Ecological Stoichiometry of the imperiled habitats vanish completely. Mountain Cryosphere. Front. Ecol. Evol. 7:360. Keywords: alpine, glacier biology, nutrient dynamics, C:N, supraglacial, subglacial, glacier-fed lakes, glacier-fed doi: 10.3389/fevo.2019.00360 streams Frontiers in Ecology and Evolution | www.frontiersin.org 1 September 2019 | Volume 7 | Article 360 Ren et al. Stoichiometry of the Mountain Cryosphere INTRODUCTION lakes and streams as far as the world’s oceans (Hotaling et al., 2017a). Thus, ecological stoichiometry can provide mechanistic Approximately 75% of the freshwater on Earth is frozen at insight into connections among different environments, any given time (Jain, 2014; Talalay et al., 2014). This global interactions between trophic levels, and can act as a means “cryosphere” includes continental ice sheets, mountain glaciers, to link the influences of glacier melt dynamics on ecosystem snowfields, permafrost, and sea ice. Beyond extreme cold structure and function in cryosphere-associated environments and frequent subzero temperatures, frozen environments place and beyond. additional harsh controls on life including a lack of available In this review, we provide the first synthesis of ecological water, high ultraviolet radiation, and highly dynamic, but stoichiometry in the mountain cryosphere. We identify generally limited, nutrient supplies (Anesio and Laybourn-Parry, mountains (and by proxy, mountain ecosystems) in the same 2012). Nevertheless, the cryosphere supports diverse biological way as a related review (Moser et al., 2019), which used the communities on the surface of glaciers and continental ice definition provided by Körner et al. (2017): mountainous areas sheets (Anesio et al., 2009; Hotaling et al., 2017a), beneath exhibit more than 200m of elevation difference within a 2.5′ them (Hamilton et al., 2013), in their meltwater (Hotaling grid cell, irrespective of elevation. Our motivation for focusing et al., 2019a), in permafrost (Jansson and Tas, 2014), and on the mountain cryosphere was 3-fold. First, much is known in sea ice (Boetius et al., 2015). Even though these biotic of the general stoichiometry of continental ice sheets (i.e., communities are dominated by unicellular microbial life (e.g., Greenland and Antarctica), however there has been considerably bacteria and algae: Boetius et al., 2015; Anesio et al., 2017; less focus on similar mountain ecosystems and thus, it is unclear Hotaling et al., 2017a), macroinvertebrates (e.g., ice worms how comparable the two environments are. Second, mountain and rotifers; Shain et al., 2016; Hotaling et al., 2019b) and glaciers and snowfields harbor extensive biological diversity, vertebrates (e.g., gray-crowned rosy finches; Rosvold, 2016) including multiple trophic levels from microbes to birds (e.g., are also represented. However, rising global temperatures are Anesio and Laybourn-Parry, 2012; Hotaling et al., 2019a). driving widespread recession of the cryosphere (Lyon et al., Third, many human populations rely on mountain glacier 2009; Notz and Stroeve, 2016; Roe et al., 2017) with profound meltwater for agriculture, hydropower, and drinking water implications for biodiversity (Hotaling et al., 2017b), human (Milner et al., 2017), highlighting the potential relevance of populations (Pritchard, 2017), and ecological feedbacks (e.g., ecological processes occurring in headwaters beyond adjacent trophic interactions and biogeochemical cycles, Hood et al., biotic communities. 2009; Sommaruga, 2015; Milner et al., 2017). Therefore, Within the mountain cryosphere, we focus on three distinct, understanding the interplay between resource availability and but interconnected, habitats: the supraglacial zone, subglacial biological communities across cryosphere-associated habitats, zone, and downstream glacier-fed streams and lakes (Figure 1). as well as how climate change may alter them, is a pressing The supraglacial zone encompasses the interface between surface research need. ice/snow and atmospheric conditions. The subglacial zone The field of ecological stoichiometry, which seeks to comprises the area where glacier ice interacts directly with understand the balance of energy and chemical elements bedrock and meltwater. And, glacier-fed streams and lakes in ecological interactions and processes (Sterner and Elser, include the downstream habitats which are directly adjacent to 2002), provides a valuable framework for understanding how glaciers (Figure 1). By considering the mountain cryosphere in a ecosystems function. The availability and mass balance of key stoichiometric framework, we clarify key environment-organism elements [carbon (C), nitrogen (N), and phosphorous (P)] interactions, including the effects of nutrients on psychrophiles place crucial controls on the population dynamics of organisms (organisms capable of living in extremely low temperatures) (Cross et al., 2005), ultimately regulating the structure, function, and their reciprocal effects on biogeochemical processes (e.g., and processes of ecosystems (Sterner and Elser, 2002; Elser respiration, nitrification) and habitat characteristics (e.g., snow et al., 2007). On mountain glaciers and snowfields, solar albedo, light attenuation). For each habitat, we address two radiation, atmospheric CO2, allochthonous (e.g., arthropod stoichiometric questions: (1) What is the origin, availability, fallout, Edwards, 1987; black carbon, Skiles et al., 2018), and and variation (spatial and temporal) of C, N, and P? What autochthonous (e.g., cryoconite hole metabolism, Anesio et al., dynamics of stoichiometric ratios exist? (2) To what extent 2009; snow algae primary productivity,
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