Squid As a Vector for Trace Element Bioaccumulation in New Zealand’s Food Webs
Cephalopods are known for their high bioaccumulation capacity of trace elements, particularly for Cd and Hg. With growing interests for alternative marine protein sources, due to overfishing and climate change, the importance of cephalopods for human consumption is increasing, which in turn creates additional pressures on already stressed trophic systems. Arrow squid (Nototodarus gouldi and N. sloanii) play a pivotal role in New Zealand’s food web: both as prey for a plethora of marine mammals, seabirds and fish species and as one of New Zealand’s main fishery targets for human consumption. The greater-hooked squid (Moroteuthopsis ingens) are also abundant and ecologically important, but have been less well studied as they have highly ammoniacal tissues and are not commercially fished. Due to their commercial and/or ecological importance, and the opportunity to compare squids of muscular body composition with those that are highly ammoniacal, these three species were selected as focus organisms. New Zealand waters are active regions, shaped by geothermal and volcanic activities, which are natural sources for trace elements. Concentration data for trace elements in Southern Hemisphere cephalopods are currently sparse, and this study aims to fill the existing knowledge gaps. In order to investigate the role of squids in the transfer of trace elements within New Zealand’s waters, a series of four complementary studies were undertaken. First, trace element concentrations (As, Cd, Co, Cr, Cu, Fe, Hg, Ni, Mn, Pb, U, V, and Zn) were assessed in different tissue types of Nototodarus sloanii from the Chatham Rise to analyse the bioaccumulation in edible muscular tissues and other organs. Arrow squid are an important vector of particularly Cd to top predators which was revealed by high concentrations in the digestive gland tissue. Next, the total body burden of the squids was calculated and toxicological and dietary consequences for predators (including humans) were assessed. Mean observed concentrations in the muscular tissues, which are consumed by humans, and simulated in-vitro digestion analysis, showed that concentrations were overall below the maximum permissible levels for the toxic elements As, Cd, Hg and Pb. However, a contamination of edible mantle tissue with digestive gland fluids was observed in market arrow squid, which might pose a risk for human consumers.
Third, regional patterns of trace element concentrations were assessed in arrow squid samples (both Nototodarus species) from multiple sampling locations within New Zealand’s Exclusive Economic Zone. Regional differences were particularly significant for As and Hg, with the West Coast exhibiting the highest overall concentrations (max. mantle concentrations, As= 59.58 µg g-1 dw; Hg= 2.13 µg g-1 dw), and for Cd with the highest measured concentrations in the Taranaki region (digestive gland Cd= 788.46 µg g-1 dw). Fourth, the muscular, non-ammoniacal arrow squid trace element concentrations were compared with an ammoniacal, non-commercially fished species, Moroteuthopsis ingens, from the Chatham Rise. Concentrations of Hg were higher in female M. ingens, likely due to their their deeper habitat and thus a higher Hg exposure when compared with arrow squid. Otherwise, no major differences in trace element whole-body burden or storage within the mantle and digestive gland were observed, suggesting that the ammoniacal nature of the tissues does not affect trace element bioaccumulation. Finally, trace element concentrations were measured in one of the arrow squid’s main predators, the long-finned pilot whale, Globicephala melas edwardii, representing one of the first trace element studies on cetaceans in New Zealand waters and the first globally for this subspecies. Analysis of blubber, kidney, liver, muscle revealed extremely high kidney Cd and liver Hg concentrations. Based on trace element analysis of arrow squid from the cetaceans’ stomachs and estimated intake calculations, arrow squid seem to be a vector of trace elements, in particular Cd, to this apex predator. This thesis establishes a baseline for arrow squid, Moroteuthopsis ingens and Globicephala melas edwardii trace element concentrations for future measurements of toxins within New Zealand’s waters. It further investigates potential impacts of arrow squid consumption on humans and strongly suggests that they can be considered important vectors in terms of trace element transfer to top predators. The data included in this thesis have implications for New Zealand’s food security, commercial squid stock management, and conservation of charismatic megafauna and the broader marine community.