Stable isotopes in bivalves as indicators of nutrient source in coastal waters in the Bocas del Toro Archipelago, Panama

Abstract

To examine N-isotope ratios (15N/14N) in tissues and shell organic matrix of bivalves as a proxy for natural and anthropogenic nutrient fluxes in coastal environments, Pinctada imbricata, Isognomon alatus, and Brachidontes exustusbivalves were live-collected and analyzed from eight sites in Bocas del Toro, Panama. Sites represent a variety of coastal environments, including more urbanized, uninhabited, riverine, and oceanic sites. Growth under differing environmental conditions is confirmed by δ18O values, with open ocean Escudo de Veraguas shells yielding the highest average δ18O (−1.0‰) value and freshwater endmember Rio Guarumo the lowest (−1.7‰). At all sites there is no single dominant source of organic matter contributing to bivalve δ15N and δ13C values. Bivalve δ15N and δ13C values likely represent a mixture of mangrove and seagrass N and C, although terrestrial sources cannot be ruled out. Despite hydrographic differences between end-members, we see minimal δ15N and δ13C difference between bivalves from the river-influenced Rio Guarumo site and those from the oceanic Escudo de Veraguas site, with no evidence for N from open-ocean phytoplankton in the latter. Populated sites yield relative 15N enrichments suggestive of anthropogenic nutrient input, but low δ15N values overall make this interpretation equivocal. Lastly, δ15N values of tissue and shell organic matrix correlate significantly for pterioideans P. imbricata and I. alatus. Thus for these species, N isotope studies of historical and fossil shells should provide records of ecology of past environments.

Paired bulk organic and individual amino acid δ15N analyses of bivalve shell periostracum: A paleoceanographic proxy for water source variability and nitrogen cycling processes

“…Adductor muscle and carbonate of bivalve shells has been shown to be an archive of the nitrogen isotope signature of the suspended organic matter that is the bivalve's food source (Minagawa and Wada, 1984;LeBlanc, 1989;Post, 2002;O'Donnell et al, 2003;Fukumori et al, 2008;Watanabe et al, 2009;Kovacs et al, 2010;Graniero et al, 2016;Gillikin et al, 2017). Our data show that periostracum also archives dietary nitrogen isotope composition throughout the clam's life.…”

“…Bivalve shells as a proxy archive offer the potential to further broaden the paleoceanographic utility of  15 N. Correlations of  15 N between shell-bound nitrogen (stored in the organic matrix of the carbonate) and soft tissue nitrogen suggest that the carbonate shells preserve a record of the  15 N changes in the bivalves (LeBlanc, 1989;O'Donnell et al, 2003;Carmichael et al, 2008;Watanabe et al, 2009;Kovacs et al, 2010;Versteegh et al, 2011;Graniero et al, 2016;Gillikin et al, 2017). In addition, bivalve shells offer the opportunity to extend absolutely dated, via crossdating methods (Black et al, 2016;Black et al, 2019), records of  15 N at the base of the food web well back beyond the instrumental record at a high resolution scale due to the fact that many of these shells grow in annual or sub-annual increments.…”

“…Such records have been identified as crucial in understanding ecosystem scale food web dynamics (Casey and Post, 2011). For example, there have been a wealth of studies recently looking at the potential of mollusks to record changes in nitrogen inputs into an ecosystem due to anthropogenic influences, both in the soft tissue of the bivalve (Watanabe et al, 2009;Graniero et al, 2016) as well as the organic matrix of the carbonate shell (Carmichael et al, 2008;Kovacs et al, 2010;Graniero et al, 2016;Oczkowski et al, 2016;Black et al, 2017). One challenge with this marine proxy is that nitrogen isotopes measured in biogenic marine proxy archives such as bivalves are not only a function of  15 N of dissolved nitrogen substrates (nitrate, nitrite, ammonium and urea) but also a function of their diet.…”

Use of stable isotope ratios of fish larvae as indicators to assess diets and patterns of anthropogenic nitrogen pollution in estuarine ecosystems

“…In addition, a good bioindicator species is common in a variety of environments, enabling it to be used in estimation of ecosystem health in various instances (Nikinmaa, 2014). Typical bioindicators that have been used to assess water quality and ecosystem function include bacterial and phytoplankton community composition (Paerl et al, 2003a,b), and stable isotope ratios of macroalgae (Raimonet et al, 2013), bivalves (Graniero et al, 2016), benthic deposit-feeders (Van Dover et al, 1992), and fish (Pruell and Taplin, 2015), among others. Because of their short generation times (typically weeks to months), most planktonic organisms are considered to be excellent bioindicators of global change as they respond quickly to shifts in the aquatic environment where they occur.…”

Using Stable Carbon and Nitrogen Isotopes to Investigate the Impact of Desalination Brine Discharge on Marine Food Webs

“…This measurement is useful in coastal waters which receive a complex mix of organic sources of both terrestrial and marine origin in particular (Bongiorni et al, 2015). The stable nitrogen isotope ratio is increasingly employed as a sensitive indicator of N sources in many ecosystems (McClelland et al, 1997;Vizzini and Mazzola, 2006;Orlandi et al, 2014;Graniero et al, 2016). Natural and anthropogenic N sources (the latter including fertilizer, sewage, aquaculture and manure) differ in terms of their δ 15 N value, and, consequently, values of benthic communities can reflect the relative contribution of these different sources (McClelland et al, 1997;Vizzini and Mazzola, 2006;Orlandi et al, 2017).…”