Ethological analysis of the trace fossil Zoophycos: hints from the Arctic Ocean

In the Arctic Ocean, winters are characterized by total darkness, near total ice coverage and basically no primary productivity, whereas summers are characterized by constant daylight, open waters and polynias resulting in high primary productivity. It has been speculated that this extreme seasonality should result in an adaptation by the benthic organisms to the pulsed flux of food to the sea floor (Van Averbeke et al. 1997). However, so far, benthic studies have failed to identify any specialization in this direction among Arctic benthic organisms (Vanreusel et al. 2000). The trace fossil Zoophycos described in this study from cores taken on the Lomonosov Ridge therefore could be the first concrete evidence supporting the idea of a specialized behaviour as a response to seasonal fluctuations in food flux in the Arctic Ocean. Although Zoophycos has been reported from the Greenland Sea and the Yermak Plateau (Chow et al. 1996) and has been noted in Quaternary Arctic deep-sea core material (Clark et al. 1980), this is the first time the occurrence and distribution of Zoophycos in the Arctic Ocean has been studied with any detail.

The trace fossil Zoophycos consists of lobed or spiralled spreiten, often with a marginal tube surrounding the spreite, and a central shaft connecting the trace with the sediment surface (Fig. 1). In late Quaternary strata, the trace fossil appears to be confined to marine settings, where the water depth exceeds 1 km, and X-ray radiographic studies have provided a good picture of the morphology of the trace fossil (Wetzel & Werner 1981; Löwemark & Schäfer 2003; Wetzel 2010). Despite the fact that Zoophycos has been found in a number of various settings from the Cambrian (Alpert 1977) to the present (Wetzel & Werner 1981; Wetzel 2008), the producers of this complex trace fossil still remain unknown, and there is no consensus regarding the behavioural explanation.

Conclusions regarding the ethology of trace fossils can be best drawn from studies in areas where conditions are favourable and the traces occur in large quantities, such as the South China Sea (Löwemark et al. 2006) or the West African margin (Wetzel & Werner 1981). However, rare occurrences in regions else typically devoid of the trace fossil can tell something about the boundary conditions limiting the existence of the behaviour and therefore contribute to a better understanding of the factors governing the trace fossil.

The Arctic Ocean is in many ways an extreme ocean with its huge shelf areas compared with the basins, the limited connections to the world oceans, the very low temperatures and the perennial ice coverage in large parts of the Arctic. The aim of this study was first to report the presence and distribution of Zoophycos from this inaccessible region. Second, and more important, the aim was to draw conclusions about the behaviour of the causative organism from the occurrence of the trace fossil in this extreme environment.

The study area

Geography and hydrography of the Arctic basin

The Arctic Ocean is separated into the Amerasian and the Eurasian basins by the Lomonosov Ridge, which rises steeply from the abyssal plains up to water depths around 1000 m in the shallowest parts (Fig. 2). In the central part of the ridge, near the North Pole, an intra-ridge basin with a sill depth of 1870 m allows an exchange between the Amerasian and Eurasian deep waters (Jakobsson et al. 2003a, b). In the Amerasian basin, two ridge systems, the Alpha and the Mendelev ridges, separate the Makarov abyssal plain from the Canadian abyssal plain. The Eurasian basin is in turn split into the Amundsen and the Nansen basins by the Gakkel Ridge. Close to the Fram Strait, two elevated platforms, the Morris Jesup Rise and the Yermak Plateau, are found.

Modern surface circulation and sea-ice transport are controlled by the Arctic wind system and are dominated by the anti-cyclonic Beaufort gyre covering large parts of the Amerasian Basin and the Transpolar Drift, which transports sea-ice across the Eurasian Basin from the Siberian shelves out to the Atlantic Ocean through the Fram Strait. As Arctic sediments are dominated by ice rafted material, the position of the boundary between the Beaufort Gyre and the Transpolar Drift consequently plays an important role for the composition of the sediment (e.g. Sellén 2009). Decreasing sea-ice coverage during summer months leads to dramatic increases in primary productivity due to more open waters and constant daylight (Arrigo et al. 2008) with phytoplankton and ice-algae being the main primary producers (Horner & Schrader 1982). Intermediate and deep water circulation is dominated by the inflow of intermediate Atlantic waters that describe a cyclonic gyre in the Eurasian basin, but also enters the Amerasian basin, where it forms a separate cyclonic gyre. The deep waters of the Arctic are formed by the mixing of this intermediate, saline water with extremely cold, relatively fresh waters from the shelf areas. This deep water forms a deep gyre with one limb flowing along the base of the Lomonosov Ridge before leaving the Arctic through the Fram Strait (Björk et al. 2010; Rudels et al. in press).

Material and methods

In this study, 12 cores taken during the icebreaker expeditions YMER80 (Boström & Thiede 1984), Arctic Ocean 96 (Jakobsson et al. 2001), LOMROG07 (Jakobsson et al. 2008a, b) and LOMROG09 (Marcussen & LOMROG Scientific Party in press) to the Arctic Ocean were used (Table 1). The cores typically consist of light yellow-grey mud with varying amounts of ice rafted debris (IRD), cyclical occurrences of brown, Mn-rich layers and occasional layers of distinctly different colour and composition, e.g. pinkish carbonate-rich layers or dark grey IRD-rich layers. The sediment in general contains very low organic carbon and biogenic carbonate content.

Physical properties were analysed for most cores either onboard during cruise or post-cruise at the Core Processing Laboratory in Stockholm using a GEOTEK Multi Sensor Core Logger. Variations in Mn-content were determined using an Itrax XRF-core scanner (Croudace et al. 2006) at Stockholm University. Resolution and exposure times were adjusted individually to the different cores, but range from 0.2 to 5 mm, and exposure times typically vary between 5 and 20 seconds. X-ray radiographs for identification of trace fossils and physical and chemical sediment structures were prepared by pushing thin (<1 cm thick) plastic boxes into the sediment (c.f. Löwemark & Werner 2001). The boxes were then cut out from the core using a nylon string, placed in plastic bags and brought to the Department of Geosciences at the University of Bremen for conventional X-ray radiography (55 kV/3 mA for 3 minutes).

Results

Morphology of Zoophycos

X-ray radiographs allows trace fossils to be studied in great detail and although the Zoophycos spreiten in the studied cores are rather small and sparse, the radiographs from the central part of the trace fossil leave little doubt that the spreiten observed are part of Zoophycos (Fig. 3). In the studied material, no open marginal tubes could be discerned. Rather, the marginal tubes appear to be stuffed with denser material. The spreiten sometimes occur in conjunction with filled, Thalassinoides-like burrows, making it difficult to conclude whether they are oblique cuts of Thalassinoides or Zoophycos spreiten. The Zoophycos observed display only two or three whorls unlike the Zoophycos observed on the continental slopes off Europe and West Africa, which often consist of a large number of whorls stretching over vertical distances of several tens of centimetres (Wetzel & Werner 1981; Löwemark & Schäfer 2003). In LOMROG09-PC05, a few specimens with multiple whorls of spreiten coiled around the central part of the trace fossil were observed. The distance from the topmost part of the structure to the lowest whorl is less than 10 cm, and although no observations could be made on the shaft connecting the trace to the sediment surface, a maximum burrowing depth of less than 20 cm is estimated given the small size of the uppermost whorls. The Zoophycos in Figure 3 actually shows a close resemblance to the morphology described by Kotake (1989) with small, Spirophyton-like whorls in the upper part gradually changing to lobate spreiten in the lower part of the system.

In LOMROG09-PC10, mostly solitary spreiten were observed. This could be partly due to the lower individual density resulting in less complete sampling of the specimen, showing only parts of the structures. The identification of Zoophycos spreiten is sometimes complicated by the presence of diagenetic bands that occasionally may show superficial resemblance to horizontal spreiten (Fig. 4). All Zoophycos spreiten seen in the radiographs showed a homogenous internal structure, not displaying any sign of the type of lamellae often described from Zoophycos. However, this could be partly due to cutting plane effects and the small number of observations does not allow any firm conclusions. For comparison, in a comprehensive study including Zoophycos spreiten from over hundred cores, Löwemark & Schäfer (2003) found 61% of the spreiten to be homogeneous with the rest showing at least some lamellae.

Stratigraphical distribution of Zoophycos

The Zoophycos spreiten are not randomly distributed in the cores, but occur clustered around certain intervals characterized by mottled, brownish sediment with enhanced Mn-levels. These brownish, mottled layers are believed to represent interglacial or interstadial intervals when less sea ice led to higher primary productivity and consequently higher food flux resulting in more vigorous bioturbation. Concomitant strengthening of the deep water circulation also led to the precipitation of Mn, causing the brownish colour of the sediment (Scott et al. 1989; Jakobsson et al. 2000; Löwemark et al. 2008). Zoophycos spreiten were present in intervals of enhanced IRD content, such as at 200 cm in LOMROG09-PC10.

Chronostratigraphical control is notoriously poor in Arctic deep water sediments due to the scarcity of nano- and micro-fossils, making both isotope- and biostratigraphy difficult (Spielhagen et al. 2004; Backman et al. 2009). Absolute dating methods such as optically stimulated luminescence have been applied with some success (Jakobsson et al. 2003a, b; Berger 2006), whereas radiogenic methods using ¹⁴C or ¹⁰Be have proven problematic (Sellén et al. 2009). Nevertheless, by correlating lithostratigraphic marker horizons and cyclical variations in Mn with the well-dated core AO96-12pc (Jakobsson et al. 2000), a tentative age model can be established for the two cores containing Zoophycos (Fig. 5). From the age model, it can be deduced that the Zoophycos occur during marine isotope stage (MIS) 11 and MIS 17 in core LOMROG09-PC05, and during MIS 5 and MIS 15 in LOMROG09-PC10. Obviously, although Zoophycos only occur in connection with interglacials/interstadials, not all of the brownish, Mn-rich layers contain Zoophycos.

Discussion

Conclusions drawn from a relatively small number of X-ray radiograph records of course have limited bearing, but the conspicuous lack of Zoophycos in the shallower sites, with less calm conditions, and the presence of Zoophycos in some of the deeper sites confirms a preference for calm conditions and moderate sedimentation rates as observed in other oceans (Wetzel & Werner 1981; Löwemark & Schäfer 2003; Löwemark et al. 2006). The position of the cores containing Zoophycos also supports the idea that the trace fossil is produced as a response to strong seasonal variations in food flux. The area around the central Lomonosov Ridge is today characterized by an extreme seasonal change in primary productivity, with high production rates during summer and close to zero production during winters. In contrast, the areas around the Morris Jesup Rise and the Lomonosov Ridge off Greenland belong to the most ice infested areas of the Arctic Ocean (Comiso et al. 2008) with only limited primary productivity even during peak summer. However, the cores retrieved in this region were also taken at water depth around 1000 m or less, and are thus less likely to contain Zoophycos anyway. The sediments on these sites have also been impacted by stranded icebergs causing extensive scouring, deformation and reworking of the sediment (Jakobsson et al. 2010). It is unknown how these activities influence bioturbation, but in the light of Zoophycos producer’s known affinity for calm conditions, it seems unlikely that iceberg scouring would benefit the construction of Zoophycos.

The concentration of Zoophycos in intervals with thicker or more numerous Mn-cycles, and the lack of Zoophycos in intervals with no or only weakly developed brown, Mn-rich layers indicate that the trace makers responsible for the construction of Zoophycos have a strong preference for interglacial conditions. This is not surprising, as glacial conditions in the Arctic are characterized by perennial sea-ice cover, stagnant deepwater circulation and strongly decreased food flux to the sea floor. Besides large variations in IRD, there are only minor down-core variations in the composition of the sediment. It therefore seems likely that variations in environmental conditions such as food flux, rather than substrate consistency and composition governs the occurrence of Zoophycos. This is further supported by observations of Zoophycos in extremely IRD-rich sediments in the northern North Atlantic (Löwemark & Schäfer 2003). Substrate variation consequently does not exert a primary control on Zoophycos distribution.

In sediments on the West African continental slope, Wetzel & Werner (1981) found Zoophycos to be limited to sediments with TOC between 0.3 and 1.8% and with sedimentation rates below 20 cm/ky. Extreme numbers of spreiten were found in the South China Sea in a core with sedimentation rates around 3 cm/ky (Löwemark et al. 2006). Central Arctic sediment, with TOC values typically around 0.5–1% clearly fall within these limits, whereas the sedimentation rates around 1–2 cm (Stein 2008; and references therein) are unusually low for slope settings. A more likely control of Zoophycos distribution, however, is food flux. Variations in the biomass, which is directly coupled to the food flux, show that biomass in the Arctic Ocean is comparable to the lower end of the spectrum observed in the Atlantic Ocean (Piepenburg 2005) and other oligotrophic regions in the world (Vanreusel et al. 2000). Biomass was found to be higher on ridges than on plains, probably due to input by deep water currents (Clough et al. 1997; Deubel 2000). In other oceans, lateral transport of organic-rich material has been shown to be of major importance (Jahnke et al. 1990; Rao & Veerayya 2000). Consequently, the slightly enhanced food fluxes at the sites where Zoophycos was found probably reflect the lower boundary conditions under which the Zoophycos trace maker can exist. Although Zoophycos occurrences are linked to food content and food flux, previous studies using radiocarbon measurements on the material in the Zoophycos spreiten showed that the material in the spreiten stems from the sediment surface and has been deposited deep in the sediment (Löwemark & Werner 2001; Leuschner et al. 2002), thus making a deposit feeding behaviour unlikely (Leuschner et al. 2002; Löwemark & Schäfer 2003). Detailed studies of morphologically similar Zoophycos from Pliocene deep marine strata in Japan also show that the producer introduced material from the sediment surface rather than feeding on material in the sediment (Kotake 1991, 1992, 1994). Carbon isotope measurements comparing spreiten material in Zoophycos with surrounding substrate lend no support (Löwemark et al. 2004) to the idea that the trace fossil could be a gardening structure (Bromley 1991; Fu & Werner 1995).

Therefore, the combined preference for calmer settings and enhanced food flux (compared with the average Arctic Ocean) in a setting that is characterized by extreme seasonal variations in food flux strengthens the hypothesis that the Zoophycos trace fossil is constructed as a cache where food is collected during rich times to be used during leaner intervals. This further implies that the Zoophycos structure was in use by its producer over extended periods of time covering several seasonal cycles. Conversely, the presence of Zoophycos in an environment strongly influenced by seasonality could be the first evidence in support of the adaptation to seasonality among benthic organisms postulated by Van Averbeke et al. (1997).

Furthermore, the sparse and isolated occurrences of Zoophycos also suggest a larval phase in the trace maker’s life cycle. It is difficult to envisage that the remote areas on the central Lomonosov ridge could be colonized in the short interstadial intervals when conditions were favourable unless the trace makers re-entered the Arctic Ocean as larvae from the Atlantic and then populated suitable substrates. Further support for this mechanism for colonization comes from the fact that the macrofauna in the Arctic Ocean mostly is of Atlantic type, with only a few endemic species (Kröncke 1994). Similar types of re-colonization of semi-isolated basins have been suggested for the Mediterranean (Bouchet & Taviani 1992).

Conclusions

The observations made on the distribution of Zoophycos in the Arctic Ocean sediments allow the following conclusions: