Strong coupling between terrestrial and aquatic food webs found in Japanese mountain lakes

Lakes and ponds are important components of mountain ecosystems. Mountain lakes are mainly formed by volcanic craters, landslides and glaciers, which create beautiful alpine and subalpine landscapes and thus attract many tourists and hikers (cover photo). Such aquatic habitats also harbor rich and unique biodiversity including plants, animals, fungi and microbes.

In addition to the ecological importance, the geomorphological, hydrological and biogeochemical significance of mountain lakes are also known, as they integrate the upstream watershed processes and influences the natural and human ecosystems located downstream in their embedded catchments. Therefore, lakes are now considered to provide high ecosystem service values in  mountainous landscapes.

Field sampling in a subalpine mountain lake (Daigaku-numa Pond) located in the Daisetsu-Kogen swamp, Hokkaido, Japan. Lake water and plankton samples were collected from an inflatable boat using samplers.

Ecologists have long recognized the strong coupling between terrestrial and aquatic food webs. For example, in small headwater streams shaded by dense forest canopy cover, stream fish such as trouts and charrs intensively prey on terrestrial arthropods (e.g., caterpillars, spiders, ants, etc.) falling into streams. Fungi, bacteria and aquatic insect larvae (e.g., leaf-shredding caddisfly and stoneflies) in forested streams process vast quantities of leaf litter supplied from riparian vegetation. Such ecosystem functioning of headwater stream communities influences the regional carbon cycling through the decomposition of terrestrial organic matter and resulting release of carbon dioxide. Lake ecosystems are also strongly linked  to their surrounding catchments by material flux. Terrestrially derived resources such as dissolved and particulate organic matter exported from soils and vegetation often support heterotrophic organisms (e.g., planktonic bacteria, zooplankton, benthic invertebrates and fish) in lakes. Furthermore, the emerging adults of aquatic insects become a significant energy source of riparian predators, such as insectivorous birds, spiders, lizards, bats, etc. Thus, transfer of organic matter  across the terrestrial-aquatic boundary is an important factor for the rich biodiversity of both aquatic and terrestrial habitats. However, the linkage of aquatic and terrestrial food webs in mountain lake ecosystems was only recently elucidated.

To study the input and importance of terrestrial organic matter in mountain lake food webs, we performed filed surveys in 49 alpine, subalpine and montane lakes in Japan (elevation = 420–2,700 m, Figs 1 and 2). We collected organisms covering whole lake food webs, such as phytoplankton, bacterioplankton, zooplankton, benthic animals and fish, as well as various carbon species, for the measurement of stable carbon isotope contents (¹²C and ¹³C) to identify the source and flow of organic matter in the lakes. The sampling campaigns travelling through the northern part of Japanese archipelago revealed that lake size is critically important for the degree of connectivity between lakes and terrestrial ecosystems. We found that in the smallest lakes (area = ca. 10^2-10^3 m²), ¹³C contents of dissolved organic and inorganic carbon showed isotopic signatures close to terrestrial plants, implying that organic matter present in lake waters is predominantly of terrestrial origin and dissolved inorganic carbon (such as dissolved CO₂) is derived mainly from the decomposition of terrestrial organic matter.

Aquatic animals also depend on terrestrial organic matter. Primary consumers of benthic food webs (e.g., midge larvae and shredding stoneflies) in small mountain lakes also showed stable carbon isotope signature similar to terrestrial organic carbon. The degree of dependence on terrestrial organic matter by carnivorous animals, such as dragonfly larvae, diving beetle, predaceous caddisfly and salamanders, are also higher in smaller lakes (Fig. 3). In lakes smaller than 10^3 m², more than half of carbon atoms that constitute the body of predators were estimated to be of terrestrial origin. The results imply that organic matter supplied from surrounding terrestrial ecosystems supports lake food webs and drives organic matter transfer from lower to higher trophic level consumers in small mountain lakes.

A typical top predator (Hinobius salamander) of small mountain lakes supported by terrestrial resources. Photo taken in the Hachiman-numa Pond, Mt. Hachimantai, Japan.

These findings suggest that integrated management strategy across the land-water boundary is necessary to conserve mountain lake ecosystems. Moreover, lake ecosystems are known to be responsive to anthropogenic environmental change such as climate change, atmospheric pollutant deposition, and local human activities of their watersheds. In particular, small water bodies located in high elevation ecosystems are susceptible to ongoing climate change due to their shallow depth and low water volumes. A most striking projected change with global warming and resulting change in treeline may be the increased export of dissolved organic matter leached from soils in the terrestrial catchments. Our statistical models expect that the projected increase of organic matter inputs may enhance the degree of dependence on terrestrial carbon by heterotrophic microorganisms, but warmer temperature will also stimulate in situ primary productivity through phytoplankton. Thus, we still don't know what will happen exactly to mountain lakes in warmer environments. Further concern raised from our study is that planktivorous fish introduced for commercial and/or recreational use could trigger the cascading trophic interactions and reduce zooplankton (large cladocerans and calanoid copepods), thereby increasing phytoplankton and altering the biogeochemical cycling of mountain lakes. Because small lakes in alpine and subalpine ecosystems may be ultra sensitive to environmental changes, the reduction of multiple anthropoghenic disturbances in the whole catchment area is necessary to maintain mountain lake ecosystems supported by terrestrial ecosystems.