Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals

Abstract

Stable isotopes of neonatal vertebrates reflect those of their mother's diet and foraging location. Evaluating feeding strategies and habitat use of neonates is consequently complicated by the maternal isotopic signal and its subsequent elimination with growth. Thus, methods that measure the loss of the maternal signal, i.e. when the isotopic signal of a neonate reflects its own diet, are needed. Values of δ(13)C and δ(15)N were measured in liver and muscle tissues of <1 year old bull (Carcharhinus leucas) and Atlantic sharpnose (Rhizoprionodon terraenovae) sharks and related to age using, total length, date sampled and umbilical scar stage (USS). We observed a decline in δ(13)C and δ(15)N values with age that was different among species, similar among isotopes, and greater in liver than in muscle; highlighting that retention of the maternal signal is dependent on species-specific life history and tissue characteristics. USS was most effective for assessing the loss of the maternal isotopic signal in the faster growing Atlantic sharpnose shark, but was less effective for the slower growing bull shark. Total length and date sampled were overall less effective and may be more informative for slower growing species when coupled with USS, as variable size at birth and misclassification of animals >1 year old, which remain in nursery habitats, increase the variability of the isotopic values. Consideration of the maternal signal and measuring its loss are thus necessary when analyzing the stable isotopes of young animals, as there is potential to misinterpret feeding strategies, over-estimate trophic position and incorrectly assign carbon source.

Maternal transfer of organohalogenated compounds in sharks and stingrays

“…For the bonnethead litter, the mother was found to have higher (Olin et al, 2011). However, these results do not apply for the stingray litter and bonnethead litter for which muscle tissues were available for stable isotope analyses.…”

Do vertebral chemical signatures distinguish juvenile blacktip shark (Carcharhinus limbatus) nursery regions in the northern Gulf of Mexico?

“…The neonatal life stage is particularly stressful for elasmobranchs and can be associated with a decline in body mass (Duncan and Holland 2006) and high mortality (Heupel and Simpfendorfer 2002;Duncan and Holland 2006). Neonates rely on maternal nutrient reserves in the form of an enlarged liver to compensate for the lack of foraging experience (Hussey et al 2010;Olin et al 2011). Because the liver plays an important role in Mn homeostasis (Aschner and Aschner 2005;Madejczyk et al 2009), metabolising liver tissue may result in excess Mn entering the bloodstream that becomes deposited in the vertebrae during the first weeks or months of life.…”

Fatty acids and stable isotopes as indicators of early-life feeding and potential maternal resource dependency in the bull shark Carcharhinus leucas

“…For these sharks, it is likely that the carbon isotopic signal in muscle tissue is not directly reflective of diet (see Matich et al 2010, Olin et al 2011 (Ducatez et al 2008). Use of maternal provisioning, in the form of an enlarged liver, was also demonstrated for juvenile dusky sharks Carcharhinus obscurus based on declining liver mass and hepatosomatic index and a declining condition factor based on total body mass and length (Hussey et al 2010).…”

“…4) may represent sharks whose isotopic compositions are both completely dependent and increasingly or completely independent of maternal composition (see Olin et al 2011). This concept explains the presence of group iii, i.e.…”

“…Furthermore, stable isotopic composition of neonatal animals has been demonstrated to reflect maternal diet and foraging location instead of neonatal diet, and this complication must be considered when interpreting isotope values in neonates and juveniles, especially for tissues with slow isotopic turnover times (e.g. muscle tissue in elasmobranchs; MacNeil et al 2005, Olin et al 2011. Fatty acid signatures are particularly useful for dietary studies because fatty acids from a prey item are taken up into consumer adipose and muscle tissue with relatively minor or predictable modifications (Iverson et al 2004).…”