Caste-specific nutritional differences define carbon and nitrogen fluxes within symbiotic food webs in African termite mounds

Abstract Fungus-growing termites of the genus Macrotermes cultivate symbiotic fungi (Termitomyces) in their underground nest chambers to degrade plant matter collected from the environment. Although the general mechanism of food processing is relatively well-known, it has remained unclear whether the termites get their nutrition primarily from the fungal mycelium or from plant tissues partly decomposed by the fungus. To elucidate the flows of carbon and nitrogen in the complicated food-chains within the nests of fungus-growing termites, we determined the stable isotope signatures of different materials sampled from four Macrotermes colonies in southern Kenya. Stable isotopes of carbon revealed that the termite queen and the young larvae are largely sustained by the fungal mycelium. Conversely, all adult workers and soldiers seem to feed predominantly on plant and/or fungus comb material, demonstrating that the fungal symbiont plays a different nutritional role for different termite castes. Nitrogen stable isotopes indicated additional differences between castes and revealed intriguing patterns in colony nitrogen cycling. Nitrogen is effectively recycled within the colonies, but also a presently unspecified nitrogen source, most likely symbiotic nitrogen-fixing bacteria, seems to contribute to nitrogen supply. Our results indicate that the gut microbiota of the termite queen might be largely responsible for the proposed nitrogen fixation.

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Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology

Canadian Journal of Zoology ◽

10.1139/z99-165 ◽

2000 ◽

Vol 78 (1) ◽

pp. 1-27 ◽

Cited By ~ 727

Author(s):

Jeffrey F Kelly

Keyword(s):

Stable Isotopes ◽

Stable Isotope ◽

Carbon Isotope ◽

Isotope Ratio ◽

Trophic Ecology ◽

Nitrogen Isotope ◽

Isotope Ratios ◽

Food Chains ◽

Stable Isotope Ratios ◽

Carbon And Nitrogen

Differential fractionation of stable isotopes of carbon during photosynthesis causes C4 plants and C3 plants to have distinct carbon-isotope signatures. In addition, marine C3 plants have stable-isotope ratios of carbon that are intermediate between C4 and terrestrial C3 plants. The direct incorporation of the carbon-isotope ratio (13C/12C) of plants into consumers' tissues makes this ratio useful in studies of animal ecology. The heavy isotope of nitrogen (15N) is preferentially incorporated into the tissues of the consumer from the diet, which results in a systematic enrichment in nitrogen-isotope ratio (15N/14N) with each trophic level. Consequently, stable isotopes of nitrogen have been used primarily to assess position in food chains. The literature pertaining to the use of stable isotopes of carbon and nitrogen in animal trophic ecology was reviewed. Data from 102 studies that reported stable-isotope ratios of carbon and (or) nitrogen of wild birds and (or) mammals were compiled and analyzed relative to diet, latitude, body size, and habitat moisture. These analyses supported the predicted relationships among trophic groups. Carbon-isotope ratios differed among species that relied on C3, C4, and marine food chains. Likewise, nitrogen-isotope ratios were enriched in terrestrial carnivorous mammals relative to terrestrial herbivorous mammals. Also, marine carnivores that ate vertebrates had nitrogen-isotope ratios that were enriched over the ratios of those that ate invertebrates. Data from the literature also indicated that (i) the carbon-isotope ratio of carnivore bone collagen was inversely related to latitude, which was likely the result of an inverse relationship between the proportion of carbon in the food chain that was fixed by C4 plants and latitude; (ii) seabirds and marine mammals from northern oceans had higher nitrogen-isotope ratios than those from southern oceans; (iii) the nitrogen-isotope ratios of terrestrial mammals that used xeric habitats were higher than the ratios of those that used mesic habitats, indicating that water stress can have important effects on the nitrogen-isotope ratio; (iv) there was no relationship between body mass and nitrogen-isotope ratio for either bone collagen or muscle of carnivores; and (v) there was linear covariation between stable-isotope ratios of carbon and nitrogen in marine food chains (but not in terrestrial C3 or C4 food chains), which is likely a product of increases in carbon-isotope ratio with trophic level in marine food chains. Differences in stable-isotope composition among trophic groups were detected despite variation attributable to geographic location, climate, and analytical techniques, indicating that these effects are large and pervasive. Consequently, as knowledge of the distribution of stable isotopes of carbon and nitrogen increases, they will probably become an increasingly important tool in the study of avian and mammalian trophic ecology.

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Use of 13C and 15N Plant Label Near Natural Abundance for Monitoring Carbon and Nitrogen Partitioning

Functional Plant Biology ◽

10.1071/pp9940133 ◽

1994 ◽

Vol 21 (2) ◽

pp. 133 ◽

Cited By ~ 37

Author(s):

E Deleens ◽

JB Cliquet ◽

JL Prioul

Keyword(s):

Stable Isotopes ◽

Isotope Composition ◽

Nitrogen Partitioning ◽

Mass Spectrometers ◽

Carbon And Nitrogen ◽

Plant Matter ◽

Distribution Parameters ◽

Natural Range ◽

High Enrichment ◽

Enrichment Experiments

Tracing with stable isotopes by using naturally or weakly labelled compounds has become a reliable approach in metabolic studies due to the high precision of isotope measurement by mass spectrometers fitted for natural range. Rapid and numerous isotope ratio determinations are now possible due to the recent automation of analyses. Three methods of analysis of carbon and nitrogen partitioning are reviewed from experiments on maize plants: (a) use of natural differences in organ isotope composition; (b) labelling with industrial CO2 naturally depleted in 13C; (c) double C and N labelling with CO2 and NO3 slightly enriched in 13C and 15N. For method (c) which is the most precise, the obtaining of plant matter with 13C and 15N label near their natural isotope abundance (1.1% for C and 0.36% for N) as well the principles of exposure and apparatus for feeding plants are described. Calculations of distribution parameters (relative specific allocation, RSA, and partitioning, %P) are presented and compared with their use in high-enrichment experiments. The precision of parameters and the theoretical or practical limitations of the methods are discussed. We show that the use of stable isotopes near their naturally occurring concentrations allows the tracing of new C or N input with precision, and is suitable for monitoring long-term partitioning. The significant advantages of this method with respect to precision, security and cost of handling compared with high abundance or radioactive tracing are discussed.

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Stable Isotopes of Sulfur, Carbon, and Nitrogen as Indicators of Trophic Level and Fish Migration in the Lower Mackenzie River Basin, Canada

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f91-265 ◽

1991 ◽

Vol 48 (11) ◽

pp. 2258-2265 ◽

Cited By ~ 174

Author(s):

R. H. Hesslein ◽

M. J. Capel ◽

D. E. Fox ◽

K. A. Hallard

Keyword(s):

Stable Isotopes ◽

Local Food ◽

Fish Muscle ◽

Trophic Levels ◽

Food Chains ◽

Mackenzie Delta ◽

Lake Whitefish ◽

Carbon And Nitrogen ◽

Migrant Populations ◽

Specific Source

Stable isotopes of sulfur, carbon, and nitrogen were used to investigate the incorporation of nutrients into food chains (fish, invertebrates, and plants) and the influence of migration on the nutritional origins of fish in two freshwater systems in the Mackenzie Delta region. Sulfur isotope analyses of fish muscle showed that broad whitefish (Coregonus nasus) in Travaillant Lake and lake whitefish (Coregonus clupeaformis) in the Kukjuktuk Creek system were migrant populations which had grown mostly on sources outside the local food base. A marine food source was indicated for the lake whitefish, while no specific source was determined for the broad whitefish. The δ15N clearly defined the trophic levels in the local food chains in both systems. Fish were in three levels in Travaillant Lake. Amphipods were in a level below the lowest fish and sediments and macrophytes were in the lowest level. The Kukjuktuk Creek fish were in two levels above a level including macrophytes, amphipods, and zooplankton. The δ13C varied widely even within single fish species local to Travaillant Lake. The δ13C did not differentiate migrants from local fish. Plants of both the C3 and C4 photosynthetic pathway were indicated by carbon isotopes.

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Tracing the flux of aquaculture-derived organic wastes in the southeast arm of Lake Malawi using carbon and nitrogen stable isotopes

Aquaculture ◽

10.1016/j.aquaculture.2012.04.030 ◽

2012 ◽

Vol 350-353 ◽

pp. 8-18 ◽

Cited By ~ 22

Author(s):

Mangaliso J. Gondwe ◽

Stephanie J. Guildford ◽

Robert E. Hecky

Keyword(s):

Stable Isotopes ◽

Lake Malawi ◽

Organic Wastes ◽

Nitrogen Stable Isotopes ◽

Carbon And Nitrogen

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Carbon and nitrogen stable isotopes of copepods in a tidal estuarine system in Maryland, USA

Regional Studies in Marine Science ◽

10.1016/j.rsma.2021.101620 ◽

2021 ◽

Vol 42 ◽

pp. 101620

Author(s):

Blessing O. Edje ◽

Paulinus Chigbu

Keyword(s):

Stable Isotopes ◽

Estuarine System ◽

Nitrogen Stable Isotopes ◽

Carbon And Nitrogen ◽

Tidal Estuarine System

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Carbon and nitrogen stable isotope signatures of deep-sea meiofauna follow oceanographical gradients across the Southern Ocean

Progress In Oceanography ◽

10.1016/j.pocean.2013.01.001 ◽

2013 ◽

Vol 110 ◽

pp. 69-79 ◽

Cited By ~ 14

Author(s):

Gritta Veit-Köhler ◽

Katja Guilini ◽

Ilka Peeken ◽

Petra Quillfeldt ◽

Christoph Mayr

Keyword(s):

Stable Isotope ◽

Southern Ocean ◽

Deep Sea ◽

Nitrogen Stable Isotope ◽

Carbon And Nitrogen ◽

Stable Isotope Signatures

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Assessment of trophic relationships between symbiotic tropical ophiuroids using C and N stable isotope analysis

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315406014494 ◽

2006 ◽

Vol 86 (6) ◽

pp. 1443-1447 ◽

Cited By ~ 3

Author(s):

D. Fourgon ◽

G. Lepoint ◽

I. Eeckhaut

Keyword(s):

Stable Isotopes ◽

Potential Benefit ◽

Feeding Habits ◽

Isotope Analysis ◽

Tracer Experiment ◽

Trophic Relationships ◽

Nitrogen Stable Isotopes ◽

Carbon And Nitrogen ◽

C And N ◽

The One

Analyses of the natural abundance of carbon and nitrogen stable isotopes were performed to investigate the feeding habits of two ophiuroids, Ophiomastix venosa and Ophiocoma scolopendrina, and to assess the potential benefit obtained by the symbiotic Ophiomastix venosa juveniles. A tracer experiment was also carried out to clarify the contribution of algae to the nitrogen uptake amongst the tested ophiuroids. Our results suggest that Ophiocoma scolopendrina adults occupy a higher position in the food web than Ophiomastix venosa and mainly feed on neuston. In contrast, O. venosa adults feed on the alga Sargassum densifolium and on organic matter associated with sediment. Free juveniles and symbiotic juveniles of O. venosa have intermediate δ13C values between both adult species. The high proportion of 13C in the symbiotic juveniles compared to the one in their conspecific adults indicates that their diet slightly differs from the latter and is closer to that of Ophiocoma scolopendrina. This raises the hypothesis that symbiotic juveniles steal neuston from their associated host, O. scolopendrina.

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