δ13C and δ15N variability in Posidonia oceanica associated with seasonality and plant fraction

doi:10.1016/S0304-3770(03)00052-4

Aquatic Botany

Volume 76, Issue 3, July 2003, Pages 195-202

https://doi.org/10.1016/S0304-3770(03)00052-4 Get rights and content

Abstract

The carbon and nitrogen isotopic compositions of fractions of the seagrass Posidonia oceanica (L.) Delile in a Mediterranean shallow environment (Stagnone di Marsala, western Sicily) were investigated seasonally throughout 1998. The stable isotope ratios of seagrass leaves (intermediate and adult), rhizomes, leaf litter and aegagropiles were compared over 1 year in order to distinguish between seasonal and plant part variability. Significant differences in the isotopic composition tested using ANOVA were observed as a function of both plant fraction and season. There was an overall trend towards less discrimination against ¹³C in summer (average $δ^{13} C$ ∼ −10‰) than in winter (average $δ^{13} C$ ∼ −13‰). In contrast, greater $δ^{15} N$ enrichment was observed in winter (average ∼ 5‰) than in summer (average ∼ 3‰). The possibility of a link between $δ^{13} C$ and $δ^{15} N$ seasonal variability and seagrass physiology such as plant carbon balance and reserve dynamics is proposed to explain the observed patterns. The demonstration of seasonal and plant fraction variability in P. oceanica isotopic composition provides a broader perspective to seagrass ecological and physiological studies. Overall, the observed variability can be up to 4 and 5‰ for $δ^{13} C$ and $δ^{15} N$ , respectively, a range that largely exceeds that associated with the transition between consecutive trophic levels (1 and 3.5‰ for $δ^{13} C$ and $δ^{15} N$ , respectively).Our results corroborate the need for, at least, seasonal sampling designs to obtain a good understanding of organic matter fluxes into food webs and highlight the limitations in drawing general conclusions about food webs where a low seasonal sampling effort has been applied. They also suggest that stable carbon and nitrogen isotope ratios deserve attention as a possible valuable approach in seagrass ecophysiological studies.

Introduction

Since the late 1970s, food web investigations in seagrass-dominated ecosystems have benefited from the use of carbon and nitrogen stable isotopic compositions (Fry et al., 1977, Fry et al., 1987, Dauby, 1989, Boon and Bunn, 1994, Jennings et al., 1997, Lepoint et al., 2000, Pinnegar and Polunin, 2000). Isotopic signatures are informative because their changes associated with the transition between two consecutive trophic levels can be predicted from the initial isotopic signal in the primary producer (Michener and Schell, 1994).

Despite its essential role in evaluating the potential diet of a particular consumer, little attention has been paid so far to the natural isotopic variability of marine macrophytes, the scarcity of information being specially noticeable in seagrasses. The stable isotopic composition of marine phanerogames is highly variable, owing to physiological and environmental factors that are usually linked to each other (Hemminga and Mateo, 1996). Specifically, the most important factors inducing variation in seagrass isotopic signatures appear to be, in order of decreasing importance, interspecific variability, the isotopic signal of the sources for synthesis (i.e. dissolved inorganic carbon and the various assimilable forms of nitrogen and sulphur), irradiance, and temperature, the last two being particularly determinant for carbon isotope ratios and strongly associated with seasonality. To our knowledge, this study represents the first attempt to assess the seasonal variability of $^{13} C /^{12} C$ and $^{15} N /^{14} N$ in different plant parts and compartments of the seagrass Posidonia oceanica (L.) Delile. Our ultimate goal is to contribute to increasing the accuracy of food web stable isotopic investigations in this key Mediterranean seagrass.

Section snippets

Materials and methods

Whole P. oceanica plants and plant detritus were collected in January, April, July and November 1998 in the Stagnone di Marsala coastal sound (37°52′N; 12°28′E), a semi-enclosed basin of approximately 2000 ha in western Sicily, Italy, with an average depth of 1.5 m. Two openings (in the northern and southern parts) allow water exchange. Water temperature and salinity present a wide annual range (11.8–28.6 °C; 33.1–45.5 PSU, respectively; Sarà et al., 1999). The basin is oligotrophic, with

Results and discussion

The mean carbon and nitrogen isotopic compositions obtained in this study (Table 1) were of the same order as those reported in previous studies (−16.4 to −8.3‰ for $δ^{13} C$ and 2.8 to 3.5‰ for $δ^{15} N$ ; McMillan et al., 1980, Cooper and De Niro, 1989, Dauby, 1989, Jennings et al., 1997, Lepoint et al., 2000, Pinnegar and Polunin, 2000). Substantial significant differences were found associated with both seasonality and plant fraction (Table 2).

Although differences in $δ^{13} C$ between intermediate and

Acknowledgements

This work was funded by the Ministero Politiche Agricole e Forestali (MiPAF, Italy) and Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR, Italy). The authors thank Olga Invers and Linda Handley for stimulating the discussion on nitrogen dynamics.

References (35)

P.I. Boon et al.
Variations in the stable isotope composition of aquatic plants and their implications for food web analysis
Aquat. Bot.
(1994)
L.W. Cooper
Patterns of carbon isotopic variability in eelgrass, Zostera marina L., from Izembek Lagoon, Alaska
Aquat. Bot.
(1989)
P. Dauby
The stable carbon isotope ratios in benthic food webs of the Gulf of Calvi, Corsica
Cont. Shelf Res.
(1989)
B. Fry et al.
Stable carbon isotope evidence for two sources of organic matter in coastal sediments: seagrasses and plankton
Geochim. Cosmochim. Acta
(1977)
A.M. Grice et al.
Light intensity and the interactions between physiology, morphology and stable isotope ratios in five species of seagrass
J. Exp. Mar. Biol. Ecol.
(1996)
L.L. Handley et al.
Terrestrial plant ecology and $^{15} N$ natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old field
Adv. Ecol. Res.
(1997)
C. McMillan et al.
$^{13} C /^{12} C$ ratios in seagrasses
Aquat. Bot.
(1980)
T. Alcoverro et al.
Annual metabolic carbon balance of seagrass Posidonia oceanica: the importance of carbohydrate reserves
Mar. Ecol. Prog. Ser.
(2001)
Boudouresque, C.-F., Meinesz, A., 1982. Découverte de l’herbier de Posidonie. Parc National de Port-Cros, cahier no....
F.S. Chapin et al.
The ecology and economics of storage in plants
Annu. Rev. Ecol. Syst.
(1990)

L.W. Cooper et al.

Stable carbon isotope variability in the seagrass Posidonia oceanica: evidence for light intensity effects

Mar. Ecol. Prog. Ser.

(1989)

M.J. Durako et al.

Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum

Mar. Ecol. Prog. Ser.

(1992)

M. Duranceau et al.

Delta $^{13} C$ of CO₂ respired in the dark in relation to delta $^{13} C$ of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought

Plant Cell Environ.

(1999)

G.D. Farquhar et al.

Carbon isotope discrimination and photosynthesis

Ann. Rev. Plant Physiol. Plant Mol. Biol.

(1989)

B. Fry et al.

Review of stable isotopic investigation of food webs in seagrass meadows

Fla. Mar. Res. Publ.

(1987)

G. Giraud

Sur une méthode de mesure et de comptage des structures foliares de Posidonia oceanica (Linné) Delile

Bull. Mus. Hist. Nat. Marseille

(1979)

Handley, L.L., Scrimgeour, C.M., Rave, J.A., 1998. 15N natural abundance levels in terrestrial vascular plants: a...

Cited by (43)

Stable isotope and fatty acid analysis reveal the ability of sea cucumbers to use fish farm waste in integrated multi-trophic aquaculture
2022, Journal of Environmental Management
Stable isotope ratios, carbon (δ¹³C) and nitrogen (δ¹⁵N), and fatty acids validated the trophic connection between farmed fish in a commercial nearshore fish farm and sea cucumbers in the Mediterranean Sea. This dual tracer approach evaluated organic matter transfer in integrated multi-trophic aquaculture (IMTA) and the ability of sea cucumbers to incorporate fish farm waste (fish faeces and uneaten artificial fish feed) into their tissue. Between October 2018 and September 2019, Holothuria (Roweothuria) poli Delle Chiaje, 1824, co-cultured at IMTA sites directly below one of the commercial fish cage , at 10 m and 25 m from the selected fish cage, and at two reference sites over 800 m from the fish farm. Sea cucumbers were sampled from each site in February, May and September, except at 0 m due to mass mortalities recorded here in the first month of study. Isotopic mixing models revealed that fish farm organic waste was the dominant dietary source for H. poli in IMTA at 10 m and 25 m from the cage. The contribution of marine plant-derived organic matter, Posidonia oceanica leaves and rhizomes, was least important. The isotopic signatures of sea cucumber tissues at reference sites were not explained by the sampled food resources. Importantly, fatty acid profiling revealed a high abundance of individual terrestrial plant fatty acids, such as oleic (18:1n-9), linoleic (18:2n-6) and eicosenoic (20:1n-9) acids in sea cucumber tissue at 10 m and 25 m from the fish cage, presumably linked to the terrestrial plant oil content of the fish feeds. At the reference sites, sea cucumber tissues were characterised by higher relative abundance of arachidonic acid (20:4n-6) acid, and the natural marine-based eicosapentaenoic (20:5n-3) and docosahexaenoic (22:6n-3) acids. These analyses revealed important differences in the composition of H. poli between the IMTA and reference locations, driven by aquaculture-derived waste near fish cages. Moreover, this study revealed temporal variation in food availability and quality, and possible differences in the physiological responses of H. poli. Stable isotope analysis and fatty acid profiling provided complementary evidence for the important dietary preferences of H. poli and validated the potential of sea cucumbers to uptake aquaculture organic waste as part of inshore fish–sea cucumber IMTA. It reveals the important implications that an established trophic link has on the viability of using sea cucumbers for the development of IMTA and the sustainable expansion of aquaculture.
Increasing nutrient inputs over the last 500 years in an Italian low-impacted seagrass meadow
2022, Marine Pollution Bulletin
Citation Excerpt :
Hence, our data suggest that long-term anthropogenic inputs may have affected consumer-resource interactions in marine food webs by altering the N budget of coastal ecosystems, as also argued by Elser et al. (2000), Hall (2009) and Hessen et al. (2004). The δ15N values recorded in the most recent layer of the matte were within the range of values (approximately 2–5‰) found by other studies of P. oceanica meadows in low-impacted sites in the Mediterranean Sea (Dolenec et al., 2006; Fourqurean et al., 2007; Lassauque et al., 2010; Lepoint et al., 2003; Vizzini et al., 2003, 2005). The increase in δ15N and N content observed over time further suggest that the observed long-term patterns can be ascribed to a general increase in anthropogenic organic N inputs in coastal waters.
Posidonia oceanica is a seagrass endemic to the Mediterranean and it has been widely used as a bioindicator. We studied the layers of a 500-year-old matte using a multiproxy approach (δ¹³C, δ¹⁵N, ¹⁴C and C and N concentrations in seagrass debris) in order to evaluate the potential of P. oceanica as a long-term environmental indicator of N pollution and CO₂ emissions. From 1581 to 1800, accumulation rate was ca. 0.35 cm year⁻¹, while in the last 100 years it has amounted to ca. 0.51 cm year⁻¹. We observed increasing δ¹⁵N values with height in the vertical matte profile, indicating an increase in anthropogenic organic N inputs over time. In contrast, no clear trend in the δ¹³C values was observed. This study reconstructs the long-term impact of human activities on a seagrass meadow located off the Italian coast, yielding long-term background information that can help managers to implement efficient plans.
Post-LGM multi-proxy sedimentary record of bottom-current variability and downslope sedimentary processes in a contourite drift of the Gela Basin (Strait of Sicily)
2021, Marine Geology
Depositional systems accumulating under the combined influence of along-slope currents and downslope sediment-gravity flows are frequent in several continental margins. Despite being well-documented in terms of how these opposing depositional processes shape the margin architecture, many aspects related to their interaction and distinctive characters of resulting sediment accumulations remain elusive. Here we focus on the Gela Basin, the foredeep of the Maghrebian fold-and-thrust belt in the Strait of Sicily, where the Levantine Intermediate Water (LIW) and the Modified Atlantic Water (MAW) are confined by margin morphology, which amplify their velocities. Two sediment cores located on the upper and lower slope of the Gela Basin document the overlapping of along- and downslope processes since the very last phase of the Last Glacial Maximum (LGM). Detailed analysis of several proxies including sedimentary structures, sortable silt, geochemical elemental composition, oxygen and carbon isotopes, ichnofacies and foraminifera assemblages helped to disentangle the sedimentary imprints of contourites (including variations in bottom-current velocity through time) and downslope gravity-driven processes (turbidity currents and mass-transport processes).
The slope experienced exceptionally high sedimentation rates up to 1300 cm kyr⁻¹ during the last phase of LGM and early phase of Heinrich Stadial 1 (HS1), which rapidly decreased before Heinrich Event 1 (< 100 cm kyr⁻¹). The high accumulation rates were driven by a combination of sediment input from the inner and mid shelf and lateral advection promoted by strong bottom-currents under the action of the LIW. An abrupt and brief intensification (+ 7.8 cm⁻¹) of the MAW speed during the early phase of HS1 affected the stability of the sediment drifts, which were growing since the previous interglacial and contributed to the emplacement of mass-transport deposits around 17 kyr BP. During the post-glacial sea-level rise pulses, before and during the Heinrich Event 1, the two sediment cores registered contrasting bottom-current velocities, suggesting a progressive shoaling of the LIW and modifications at the interface between the LIW and the MAW, in response to the increased fresh water discharge from the Atlantic. Our findings suggest that sea-level fluctuations can change the thickness and core-depth of the Central Mediterranean water masses, leading to intervals of enhanced bottom-current erosion and margin instability along the outer shelf and upper slope.
Carbon and nitrogen allocation strategy in Posidonia oceanica is altered by seawater acidification
2017, Science of the Total Environment
Citation Excerpt :
Our results are consistent with previous findings on tropical seagrass communities, indicating that additional CO2 influenced C uptake and increased the biological discrimination against the heavier isotope when C source was more abundant (Takahashi et al., 2016). Among different C metabolites, lignin extracted from leaves was 13C depleted with respect to holocellulose and NSC (Vizzini et al., 2003). This could be explained taking into account that lignin, as other secondary metabolites, is depleted in 13C compared to primary photosynthetic products (Brugnoli and Farquhar, 2000).
Rising atmospheric CO₂ causes ocean acidification that represents one of the major ecological threats for marine biota. We tested the hypothesis that long-term exposure to increased CO₂ level and acidification in a natural CO₂ vent system alters carbon (C) and nitrogen (N) metabolism in Posidonia oceanica L. (Delile), affecting its resilience, or capability to restore the physiological homeostasis, and the nutritional quality of organic matter available for grazers. Seawater acidification decreased the C to N ratio in P. oceanica tissues and increased grazing rate, shoot density, leaf proteins and asparagine accumulation in rhizomes, while the maximum photochemical efficiency of photosystem II was unaffected. The ¹³C-dilution in both structural and non-structural C metabolites in the acidified site indicated quali-quantitative changes of C source and/or increased isotopic fractionation during C uptake and carboxylation associated with the higher CO₂ level. The decreased C:N ratio in the acidified site suggests an increased N availability, leading to a greater storage of ¹⁵N–enriched compounds in rhizomes. The amount of the more dynamic C storage form, sucrose, decreased in rhizomes of the acidified site in response to the enhanced energy demand due to higher shoot recruitment and N compound synthesis, without affecting starch reserves. The ability to modulate the balance between stable and dynamic C reserves could represent a key ecophysiological mechanism for P. oceanica resilience under environmental perturbation. Finally, alteration in C and N dynamics promoted a positive contribution of this seagrass to the local food web.
The effect of the quality of diet on the functional response of Mytilus galloprovincialis (Lamarck, 1819): Implications for integrated multitrophic aquaculture (IMTA) and marine spatial planning
2017, Aquaculture
Citation Excerpt :
3. A solution of refractory organic matter with a high C/N ratio (> 15–20; Vizzini et al., 2003) was obtained using fresh leaves of Posidonia oceanica, properly dried and minced (mimicking oligotrophic waters subsidized with highly refractory organic matter for secondary consumers). In doing so, fresh leaves of P. oceanica were cleaned off epiphytes and later dried in an oven at 60 °C for 24 h. Dry leaves were ground and reduced to a powder and passed through a 100 μm mesh.
The integrated multi-trophic aquaculture (i.e., IMTA) is a practice combining organisms with different trophic levels with the final purpose of transforming the continuous waste of food by targeting species into nutrient input for other non-target species. This practice very often involves filter feeders, such as bivalves, by the use of which bioenergetics budgets are strongly influenced by the quality and quantity of different foods. However, to date, scant information is available, to really understand the rebounds of food availability on the growth performances of these harvested biomasses in the natural environment. By choosing the mussel Mytilus galloprovincialis as a model, this study aims to (1) characterize the functional response of the species to define all parameters related to food intake strategies and (2) to investigate how responses change as a function of varying food sources. Laboratory procedures have been designed to evaluate the clearance rates (CR) and assimilation efficiencies (AE) of M. galloprovincialis with varying food concentrations, while different diets (i.e., seagrass, phytoplankton, and pellets) have been provided to investigate how differently they reach saturation. Results show that in the presence of phytoplankton and seagrass as food sources, the feeding strategies of M. galloprovincialis follow a II-type Holling's curve, while it shows a I-type Holling's curve when pellet food is provided. Investigating the behavioural components of functional responses may improve our ability to predict where to place shellfish cultures, as it may be useful in the context of IMTA management and in addressing siting studies.
Our paper focuses on a question central to understanding and predicting the likely impacts of one among the most important human economic activity like the aquaculture in coastal habitats. The main question deals with the possibility to combine experimental procedures with the new mechanistic functional trait based bioenergetic models in order to effectively predict life history traits of cultivated species.
N-Alkanes and stable C, N isotopic compositions as identifiers of organic matter sources in Posidonia oceanica meadows of Alexandroupolis Gulf, NE Greece
2015, Marine Pollution Bulletin
We analyzed n-alkane contents and their stable carbon isotope composition, as well as the carbon and nitrogen isotope composition (δ¹³C, δ¹⁵N) of sediment organic matter and different tissues of Posidonia oceanica seagrass sampled in Alexandroupolis Gulf (A.G.), north-eastern Greece, during 2007–2011. n-Alkane contents in P. oceanica and in sediments showed similar temporal trends, but relative to bulk organic carbon content, n-alkanes were much more enriched in sediments compared to seagrass tissue. Individual n-alkanes in sediments had similar values than seagrass roots and rhizomes and were more depleted in ¹³C compared to seagrass leaves and sheaths, with δ¹³C values ranging from −35‰ to −28‰ and from −25‰ to −20‰, respectively. n-Alkane indexes such as the Carbon Preference Index, carbon number maximum, and n-alkane proxy 1 (C₂₃ + C₂₅/C₂₃ + C₂₅ + C₂₉ + C₃₁) indicate strong inputs of terrestrial organic matter, while the presence of unresolved complex mixtures suggests potential oil pollution in some sampled areas.

View all citing articles on Scopus

View full text

δ13C and δ15N variability in Posidonia oceanica associated with seasonality and plant fraction

Abstract

Introduction

Section snippets

Materials and methods

Results and discussion

Acknowledgements

Aquat. Bot.

Aquat. Bot.

Cont. Shelf Res.

Geochim. Cosmochim. Acta

J. Exp. Mar. Biol. Ecol.

Adv. Ecol. Res.

Aquat. Bot.

Annual metabolic carbon balance of seagrass Posidonia oceanica: the importance of carbohydrate reserves

Mar. Ecol. Prog. Ser.

The ecology and economics of storage in plants

Annu. Rev. Ecol. Syst.

Stable carbon isotope variability in the seagrass Posidonia oceanica: evidence for light intensity effects

Mar. Ecol. Prog. Ser.

Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum

Mar. Ecol. Prog. Ser.

Delta 13C of CO2 respired in the dark in relation to delta 13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought

Plant Cell Environ.

Carbon isotope discrimination and photosynthesis

Ann. Rev. Plant Physiol. Plant Mol. Biol.

Review of stable isotopic investigation of food webs in seagrass meadows

Fla. Mar. Res. Publ.

Sur une méthode de mesure et de comptage des structures foliares de Posidonia oceanica (Linné) Delile

Bull. Mus. Hist. Nat. Marseille

$δ^{13} C$ and $δ^{15} N$ variability in Posidonia oceanica associated with seasonality and plant fraction

Delta $^{13} C$ of CO₂ respired in the dark in relation to delta $^{13} C$ of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought