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Variation in Reciprocal Subsidies Between Lakes and Land: Perspectives from the Mountains of California1 Jonah Piovia-Scott, Steven Sadro, Roland A

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Variation in Reciprocal Subsidies Between Lakes and Land: Perspectives from the Mountains of California1 Jonah Piovia-Scott, Steven Sadro, Roland A 1691 PERSPECTIVE Variation in reciprocal subsidies between lakes and land: perspectives from the mountains of California1 Jonah Piovia-Scott, Steven Sadro, Roland A. Knapp, James Sickman, Karen L. Pope, and Sudeep Chandra Abstract: Lakes are connected to surrounding terrestrial habitats by reciprocal flows of energy and nutrients. We synthesize data from California’s mountain lake catchments to investigate how these reciprocal subsidies change along an elevational gradient and with the introduction of a top aquatic predator. At lower elevations, well-developed terrestrial vegetation provides relatively large inputs of organic material to lakes, whereas at higher elevations, the paucity of terrestrial vegetation provides minimal organic input but allows for higher inputs of inorganic nitrogen. There are also pronounced elevational patterns in amphibians and aquatic insects, which represent important vectors for resource flows from lakes back to land. The introduction of trout can reduce this lake-to-land resource transfer, as trout consume amphibians and aquatic insects. We propose a conceptual model in which within-lake processes influence terrestrial consumers at higher elevations, while terrestrial inputs govern within-lake processes at lower elevations. This model contributes to a more general understanding of the connections between aquatic and terrestrial habitats in complex land­ scapes. Résumé : Les lacs sont reliés aux habitats terrestres qui les entourent par des flux réciproques d’énergie et de nutriments. Nous mettons en rapport des données tirées de bassins versants de lacs de montagne en Californie pour étudier les variations de ces apports réciproques le long d’un gradient altitudinal et après l’introduction d'un prédateur aquatique de niveau trophique supérieur. À basse altitude, une végétation terrestre bien développée fournit de relativement grands apports de matière organique aux lacs, alors qu’a` plus haute altitude, la rareté de la végétation terrestre fournit peu d’apports organiques, mais permet des apports d’azote inorganique plus importants. Des variations altitudinales marquées sont également observées chez les amphibiens et les insectes aquatiques, qui représentent d’importants vecteurs pour les flux de ressources des lacs vers la terre. L’introduction de truites peut réduire ce transfert de ressources des lacs vers la terre, puisque les truites consomment des amphibiens et des insectes aquatiques. Nous proposons un modèle conceptuel dans lequel les processus internes des lacs influencent les consommateurs terrestres a` plus haute altitude, alors que les apports terrestres régissent les processus internes des lacs de plus basse altitude. Ce modèle participe a` une compréhension plus générale des liens entre les habitats aquatiques et terrestres dans des paysages complexes. [Traduit par la Rédaction] Introduction each other (Vander Zanden and Gratton 2011), which hampers efforts The transport of energy and resources across habitat boundaries to forge a more holistic understanding of the dynamical interdepen- has important consequences for food-web dynamics and ecosystem dence of these linked aquatic and terrestrial systems. function (Polis et al. 1997, 2004; Loreau et al. 2003; Richardson and Terrestrial inputs exert a number of fundamental controls on Sato 2015). Most studies of cross-ecosystem resource subsidies have the structure and function of aquatic ecosystems. The overall level focused on a single direction of resource flow, e.g., the transport of of primary and secondary production that a lake supports is largely terrestrial organic matter into aquatic ecosystems (Caraco and Cole determined by nutrient concentrations (Naumann 1919; Carlson 2004). However, resources frequently move in both directions across 1977) that, in turn, are often dependent on watershed sources (Odum habitat boundaries, and these reciprocal linkages can play an impor- 1969; Hutchinson 1970). In addition to nutrients such as nitrogen and tant role in determining the trophic structure of landscapes (Nakano phosphorous, organic carbon has emerged as a second principal axis and Murakami 2001; Baxter et al. 2004; Leroux and Loreau 2011). governing aquatic ecosystems (Williamson et al. 1999). Terrestrially Among the best studied cross-boundary resource flows are those derived organic carbon can influence lake ecosystem function by between lakes and their surrounding catchments (Cole et al. 1994, acting as a metabolic substrate for heterotrophic microorganisms 2011; del Giorgio et al. 1999; Prairie et al. 2002; Gratton et al. 2008; (del Giorgio and Peters 1994; Pace et al. 2004), often leading to rates of Gratton and Vander Zanden 2009). However, reciprocal linkages be- ecosystem respiration that are higher than primary production, re- tween lakes and land have largely been studied in isolation from sulting in net ecosystem heterotrophy (Prairie et al. 2002; Hanson Received 1 December 2015. Accepted 22 May 2016. J. Piovia-Scott.* School of Biological Sciences, Washington State University, Vancouver, 14204 NE Salmon Creek Ave., Vancouver, WA 98686, USA. S. Sadro.* Department of Environmental Science and Policy, University of California, Davis, One Shields Ave., Davis, CA 95616, USA. R.A. Knapp. Sierra Nevada Aquatic Research Laboratory, University of California, 1016 Mt. Morrison Rd., Mammoth Lakes, CA 93546, USA. J. Sickman. Department of Environmental Sciences, University of California, Riverside, 900 University Ave., Riverside, CA 92521, USA. K.L. Pope. Pacific Southwest Research Station, US Forest Service, 1700 Bayview Dr., Arcata, CA 95521, USA. S. Chandra. Department of Biology, University of Nevada, Reno, 1664 N Virginia St., Reno, NV 89557, USA. Corresponding author: Jonah Piovia-Scott (email: [email protected]). *These authors contributed equally. 1This perspective is part of the special issue “Cross-ecosystem resource subsidies: from land to water and back again”, a product of a symposium held at the 145th Annual Meeting of the American Fisheries Society, Portland, Oregon, USA, August 2015. This work is free of all copyright and may be freely built upon, enhanced, and reused for any lawful purpose without restriction under copyright or database law. The work is made available under the Creative Commons CC0 1.0 Universal Public Domain Dedication (CC0 1.0). Can. J. Fish. Aquat. Sci. 73: 1691–1701 (2016) dx.doi.org/10.1139/cjfas-2015-0549 Published at www.nrcresearchpress.com/cjfas on 31 May 2016. 1692 Can. J. Fish. Aquat. Sci. Vol. 73, 2016 et al. 2003). Although terrestrial inputs of organic materials also ranges contain thousands of comparatively small (median size is support higher level consumers in both benthic (Hershey et al. 2006; approximately 2 ha), naturally formed lakes, nearly all of which are Solomon et al. 2011) and pelagic (Vander Zanden et al. 2006; Francis glacial in origin and occur at elevations between 1500 and 3500 m. and Schindler 2009; Cole et al. 2011) habitats, this effect can be weak Mountain lakes tend to be oligotrophic and clear-watered, which (Brett et al. 2009; Francis et al. 2011; Mehner et al. 2015) and the factors makes them highly sensitive to even small changes in terres­ that determine the extent to which terrestrial resources support trial inputs of nutrients or organic matter. Aquatic macrophytes are aquatic consumers remain poorly understood. relatively uncommon (with the exception of sedges in shallow litto­ For most lakes, the total amount of energy and resources trans­ ral zones), so the base of the aquatic food web is represented mostly ferred from the lake to the surrounding terrestrial habitats is likely by autotrophic and heterotrophic microorganisms (both ben­ to be dwarfed by terrestrial inputs to the lake (Vander Zanden and thic and pelagic). Gratton 2011). However, the resources flowing out of lakes (mostly in Perhaps most importantly from the standpoint of developing a the form of animal biomass) tend to be high-quality food items, and conceptual understanding of reciprocal lake–land resource subsi­ aquatic resources can be just as important to terrestrial animals as dies, California’s mountain lakes and their surrounding catch­ terrestrial resources are to aquatic animals (Bartels et al. 2012). The ments are characterized by strong elevation gradients that regulate emergence of aquatic insects (Gratton and Vander Zanden 2009; a number of ecologically important abiotic and biotic factors (Fig. 1). Bartrons et al. 2013; Dreyer et al. 2015) and amphibians (Regester et al. These include elevational gradients in temperature, terrestrial vege­ 2006; Gibbons et al. 2006; Schriever et al. 2013) are the best studied tation cover, and soil development. Elevation and catchment char­ lake-to-land resource flows, and these subsidies can have important acteristics can be broadly used to classify lakes as either high- or effects on terrestrial ecosystems (Richardson and Sato 2015). For ex­ low-elevation lakes, with the tree line (2000–2900 m depending ample, changes in consumer density and behavior associated with on latitude) as a good general delineation between the two. emerging aquatic insects can have cascading top-down effects on Low-elevation lakes are warmer and generally occur in catchments lower trophic levels in riparian areas surrounding streams (Henschel consisting of mixed coniferous forest with reasonably well-developed et al. 2001; Murakami and Nakano 2002; Sabo and Power 2002), and soils. In contrast, high-elevation alpine lakes are colder and typically the deposition
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