Show your beaks and we tell you what you eat: Different ecology in sympatric Antarctic benthic octopods under a climate change context

Abstract

Sympatry can lead to higher competition under climate change and other environmental pressures, including in South Georgia, Antarctica, where the two most common octopod species, Adelieledone polymorpha and Pareledone turqueti, occur side by side. Since cephalopods are typically elusive animals, the ecology of both species is poorly known. As beaks of cephalopods are recurrently found in top predator's stomachs, we studied the feeding ecology of both octopods through the evaluation of niche overlapping and specific beak adaptations that both species present. A multidisciplinary approach combining carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope signatures, mercury (Hg) analysis and biomaterials' engineering techniques was applied to investigate the beaks. An isotopic niche overlap of 95.6% was recorded for the juvenile stages of both octopod species, dropping to 19.2% for the adult stages. Both A. polymorpha and P. turqueti inhabit benthic ecosystems around South Georgia throughout their lifecycles (δ¹³C: −19.21 ± 1.87‰, mean ± SD for both species) but explore trophic niches partially different during adult life stages (δ¹⁵N: 7.01 ± 0.40‰, in A. polymorpha, and 7.84 ± 0.65‰, in P. turqueti). The beaks of A. polymorpha are less dense and significantly less stiff than in P. turqueti. Beaks showed lower mercury concentration relative to muscle (A. polymorpha - beaks: 0.052 ± 0.009  μg g⁻¹, muscle: 0.322 ± 0.088  μg g⁻¹; P. turqueti - beaks: 0.038 ± 0.009  μg g⁻¹; muscle: 0.434 ± 0.128  μg g⁻¹). Overall, both octopods exhibit similar habitats but different trophic niches, related to morphology/function of beaks. The high Hg concentrations in both octopods can have negative consequences on their top predators and may increase under the present climate change context.

Introduction

Sympatry in Antarctic cephalopods has started to be addressed, in the sense that close-related species with similar ontogenetic/phylogenetic life-history strategies may display different patterns of genetic differentiation (Strugnell et al., 2017). Two species are considered sympatric when sharing the same geographical region thus frequently encountering each other while exploiting the available natural resources. To avoid competition and probable extinction of the inferior competitor, ecological niche theory predicts sympatric species exploit differently the habitat allowing their coexistence (Hardin, 1960). Niche differentiation, documented in various organisms, such as birds, reptiles (MacArthur, 1958; Pacala and Roughgarden, 1985) and cephalopods (Bennice et al., 2019), can occur by using different habitats or consuming different prey. However, few studies have documented competition between sympatric cephalopods, particularly in polar regions, failing to describe interspecific relationships that might influence marine biota. A better understanding of cephalopods will allow to understand interspecific relationships in the Antarctic ecosystem, as cephalopods play important roles by constituting strong links between trophic levels (Collins and Rodhouse, 2006; Xavier et al., 2018). Climate change associated environmental factors are likely to influence the current structure and functioning of Antarctic ecosystems (Constable et al., 2014; Gutt et al., 2015; Rintoul et al., 2018), thus raising concern about the future of keystone cephalopod species.

The octopods Adelieledone polymorpha (Robson, 1930) and Pareledone turqueti (Joubin, 1905) are the two most abundant sympatric species of benthic Antarctic cephalopods (family: Megaleledonidae) living on the South Georgia shelf (Collins et al., 2004). They are the main prey for some top predators, such as pinnipeds and commercially valuable fish like the Patagonian Toothfish, Dissostichus eleginoides (Negri et al., 2016; Rodhouse et al., 1992; Xavier et al., 2002). Around South Georgia, A. polymorpha and P. turqueti have been found down to 15–862 and 25–640 m deep, respectively (Allcock, 1997). Even though both species can be found at similar depths, P. turqueti is more abundant at shallower depths relative to A. polymorpha (Yau et al., 2002). Since both species produce large-egg hatchlings and seem to show high parental investment (e.g. brooding), adult dispersal is limited (Barratt et al., 2008; Schwarz et al., 2018; Villanueva and Norman, 2008). Notwithstanding, the arms of A. polymorpha have higher number of suckers of smaller diameter and its body is more fragile (i.e. more prone to damage when caught on nets) than P. turqueti, which might indicate that both species exploit habitats differently (Daly and Rodhouse, 1994). Great dissimilarities can also be found in the digestive system of the two species: different sizes of posterior salivary gland (PSG) and buccal masses; different beak morphology (Xavier and Cherel, 2009). Whilst P. turqueti beaks present features common to other benthic octopods, the lower beak of A. polymorpha has an unique shape that clearly differs from all other octopods (Allcock et al., 2003; Daly and Rodhouse, 1994), indicating that both species occupy different trophic niches. Previous dietary studies have recorded a broadly similar diet composed by amphipods, polychaetes and other invertebrates on both species, but differing in the identification of the presence of few remains of hard-shelled prey, octopods and fishes in the diet of P. turqueti (Daly, 1996; Piatkowski et al., 2003). As these both species possess clearly different beaks, such characteristics may allow a better understanding of the trophic differences found in their diets.

Due to morphological and trophic specific traits in A. polymorpha and P. turqueti, our research aims to test for differences in habitat use and trophic ecology of these sympatric octopod species and assess their specific roles in the Antarctic marine ecosystem. It is hypothesized that both octopods occupy benthic habitats within the South Georgia coastal region while exploring trophic niches composed of different prey communities. The different methods of exploiting different sorts of prey are made possible by functional morphological adaptations that both species possess, such as the diverse characteristics of their beaks (Allcock et al., 2003; Daly and Rodhouse, 1994). As cephalopod diversity of South Georgia marine ecosystems and the pivotal role that these organisms have on marine food webs are still not entirely understood, filling existing gaps of knowledge is crucial to fully understand the benthic functional diversity and which ecological drivers dictate the community (Alvito et al., 2014; Collins et al., 2004; Xavier et al., 2003). Furthermore, the gathered knowledge will inform future conservation measures implemented through the recently established South Georgia and South Sandwich Islands Marine Protected Area (Hogg et al., 2016; Rogers et al., 2015; Trathan et al., 2014).

To accomplish this study, beaks of A. polymorpha and P. turqueti were analysed morphologically and their habitat and trophic levels investigated using a multidisciplinary approach:

• Applying novel biomaterial engineering techniques, including scanning electron microscopy (SEM), X-ray diffraction (XRD), high-resolution microcomputed tomography (μCT) and nanoindentation test (NNI), provide detailed information on microstructure, composition and density of hard tissues (Cárdenas et al., 2004; Miserez et al., 2007). Since both species are closely related, we expected to find no differences in the beak's microstructure between them, with beak morphology being the key factor in determining physical properties, such as stiffness.

• Stable isotope analyses have been successfully applied to study the trophic signals in cephalopod beaks (Cherel and Hobson, 2005; Zimmer et al., 2007). Through stable isotope ratios of carbon (¹³C/¹²C, δ¹³C) and nitrogen (¹⁵N/¹⁴N, δ¹⁵N) applied in different regions of the beaks, we studied ontogenetic shifts in species' habitat and trophic ecology. Values of δ¹³C were used to determine habitat (e.g. higher vs lower latitude, inshore vs offshore) and δ¹⁵N values to trophic niche (Cherel and Hobson, 2007; Hobson and Welch, 1992). Since A. polymorpha and P. turqueti are benthic octopods, we believe that both inhabit coastal ecosystems on the South Georgia shelf throughout their lifecycle. Ontogenetic dietary shifts are expected in both species, although a broader range of δ¹⁵N values is expected to be found in P. turqueti due to its more generalist feeding behavior (Daly, 1996; Piatkowski et al., 2003).

• Mercury has been successfully applied to trophic studies before, as its concentration is biomagnified along trophic levels (Atwell et al., 1998; Bargagli et al., 1998). We expect that P. turqueti feeds on prey of higher trophic levels thus presenting higher total mercury (T-Hg) concentrations in its tissues relative to A. polymorpha. As little is known about cephalopods' beaks mercury uptake, T-Hg concentrations on beaks will also be assessed and compared to T-Hg concentrations in the same individual's muscle. T-Hg concentrations on beaks are expected to be lower relative to muscle.