Methane carbon supports aquatic food webs to the fish level

Abstract

Large amounts of the greenhouse gas methane (CH(4)) are produced by anaerobic mineralization of organic matter in lakes. In spite of extensive freshwater CH(4) emissions, most of the CH(4) is typically oxidized by methane oxidizing bacteria (MOB) before it can reach the lake surface and be emitted to the atmosphere. In turn, it has been shown that the CH(4)-derived biomass of MOB can provide the energy and carbon for zooplankton and macroinvertebrates. In this study, we demonstrate the presence of specific fatty acids synthesized by MOB in fish tissues having low carbon stable isotope ratios. Fish species, zooplankton, macroinvertebrates and the water hyacinth Eichhornia crassipes were collected from a shallow lake in Brazil and analyzed for fatty acids (FA) and carbon stable isotope ratios (δ(13)C). The fatty acids 16:1ω8c, 16:1ω8t, 16:1ω6c, 16:1ω5t, 18:1ω8c and 18:1ω8t were used as signature for MOB. The δ(13)C ratios varied from -27.7‰ to -42.0‰ and the contribution of MOB FA ranged from 0.05% to 0.84% of total FA. Organisms with higher total content of MOB FAs presented lower δ(13)C values (i.e. they were more depleted in (13)C), while organisms with lower content of MOB signature FAs showed higher δ(13)C values. An UPGMA cluster analysis was carried out to distinguish grouping of organisms in relation to their MOB FA contents. This combination of stable isotope and fatty acid tracers provides new evidence that assimilation of methane-derived carbon can be an important carbon source for the whole aquatic food web, up to the fish level.

Figure 1. Methane oxidizing bacteria fatty acids (MOB FA %) and carbon isotope ratios (δ¹³C ‰) in organisms.

MOB FA % represents the sum of the MOB fatty acid markers 16∶1ω8c, 16∶1ω8t, 16∶1ω6c, 16∶1ω5t, 18∶1ω8c and 18∶1ω8t, expressed as percentage of total fatty acids. Ca- Chaoborus sp., Ce- Ceratopogonidae, Ch1- Chironomidae sp.1, Ch2- Chironomidae sp.2, Eph- Campsurus sp., F1- Tetragonopterus argenteus, F2- Astyanax cf. bimaculatus, F3- Parauchenipterus galeatus, F4- Crenicichla sp., F5- Potamorhina squamoralevis, F6- Cyphocharax sp., F7- Anadoras grypus, F8- Leporinus friderici, F9- Steindachnerina brevipinna, Eich- Eichhornia crassipes, Zoo- Zooplankton. Fishes are represented by squares, macroinvertebrates by circles, zooplankton by cross and the plant by diamond. The different colors indicate the type of food sources expected to dominate: green indicates herbivory on plant material, blue herbivory on bottom filamentous algae, red carnivory and brown detritivory. Other types of feeding may occur and can result in variability. The data points separate into two major groups, denoted A and B.

Figure 2. Dendrogram from UPGMA cluster analysis based on a Bray-Curtis similarity matrix of organisms according to MOB FA contributions.

The isotope ratios of carbon (δ¹³C ‰ vs. PDB) were included for comparison. Ca- Chaoborus sp., Ce- Ceratopogonidae, Ch1- Chironomidae sp.1, Ch2- Chironomidae sp.2, Eph- Campsurus sp., F1- Tetragonopterus argenteus, F2- Astyanax cf. bimaculatus, F3- Parauchenipterus galeatus, F4- Crenicichla sp., F5- Potamorhina squamoralevis, F6- Cyphocharax sp., F7- Anadoras grypus, F8- Leporinus friderici, F9- Steindachnerina brevipinna, Eich- Eichhornia crassipes, Zoo- Zooplankton. The FA 16∶1ω8c, 16∶1ω8t, 16∶1ω6c, 16∶1ω5t, 18∶1ω8c and 18∶1ω8t were used as MOB markers.

Figure 3. Schematic illustration of the incorporation of carbon of aerobic methane oxidizing bacteria (MOB) into the food web of a tropical shallow lake.

Particulate and dissolved organic matter (POM and DOM, respectively) of autochthonous and allochthonous origin support anaerobic methane (CH₄) formation. CH₄ is oxidized by MOB and CH₄-derived carbon is transferred to higher trophic levels subsidizing pelagic and benthic organisms, reaching the fish level. Arrows with different colors indicate potential food sources: black- MOB; green- herbivory on phytoplankton and/or plant material; blue- herbivory on bottom filamentous algae; red- carnivory on aquatic and/or terrestrial organisms; brown- detritivory.