Possible transport pathways of diazotrophic Trichodesmium with Agulhas rings from the Indian Ocean into the Atlantic Ocean

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Possible transport pathways of diazotrophic Trichodesmium with Agulhas rings from the Indian Ocean into the Atlantic Ocean

https://doi.org/10.21203/rs.3.rs-3413584/v1

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Diazotrophic cyanobacteria such as Trichodesmium play a crucial role in the nitrogen budget of the oceans due to their capability to bind atmospheric nitrogen. Little is known about their interoceanic transport pathways and their distribution in upwelling regions. Trichodesmium has been detected using a Video Plankton Recorder (VPR) mounted on a remotely operated towed vehicle (TRIAXUS) in the southern and northern Benguela Upwelling System (BUS) in austral autumn, Feb/Mar 2019. The TRIAXUS, equipped with a CTD as well as fluorescence and nitrogen sensors, was towed at a speed of 8 kn on two onshore–offshore transects undulating between 5 and 200 m over distances of 249 km and 374 km, respectively. Trichodesmium was not detected near the coast in areas of fresh upwelling but was found in higher abundances offshore, mainly in subsurface water layers down to 80 m depth with elevated salinities on both transects. These salinity lenses can be related to northward moving eddies that have been detached from the warm and salty Agulhas Current. We provide the first indications that Trichodesmium can be transported with Agulhas rings from the Indian into the Atlantic Ocean.

Earth and environmental sciences/Biogeochemistry

Earth and environmental sciences/Ocean sciences

Trichodesmium

Benguela Upwelling System

Video Plankton Recorder

TRIAXUS

Agulhas rings

Nitrogen is an essential element in any form of life from bacteria to complex metazoans due to its necessity for protein biosynthesis. It is regarded as the limiting nutrient for phytoplankton production in most regions of the open ocean, especially in the surface waters of the tropics and subtropics [1–3]. The estimated loss of available nitrogen by new production and export in surface waters often exceeds the nitrate flux by diapycnal mixing of deeper water into the euphotic zone [3, 4], especially as the substitution of the lost nitrate from deeper layers is a slow process in stratified waters. It is assumed that biological fixation of atmospheric nitrogen (N₂) by diazotrophic cyanobacteria balances the loss in nutrient-poor regions, fuelling up to half of the new production [5] and therefore playing an important role in carbon uptake in the marine environment.

Cyanobacteria of the genus Trichodesmium are considered to be the dominant N₂ binding organism in tropical and subtropical oceans, affecting the influx of new nitrogen in global marine ecosystems [3, 6–9] by making up for 30–80% of oceanic N₂-fixation rates [10]. Trichomes of Trichodesmium can occur as macroscopic aggregates and can produce enormous blooms; for example, the red tides caused by Trichodesmium erythraeum give the Red Sea its name. As the N₂ binding enzyme nitrogenase is rapidly inactivated by O₂, other diazotroph bacteria separate N₂ fixation from O₂ evolving photosynthesis either in time, i.e., N₂ fixation by night, or in space by forming heterocysts to protect the enzyme. However, Trichodesmium is a nonheterocystous bacterium that performs N₂ fixation in the daytime. Bergmann and Carpenter [11] found spatial nitrogenase sequestration mechanisms in Trichodesmium, a cell type subsequently termed diazocytes.

While most of the studies describe N₂ fixation in tropical and subtropical regions of the open ocean [2, 3, 5, 12–14], only few is known about the contribution of diazotrophic bacteria to the nitrogen budget in coastal waters [15–17] and upwelling systems [18, 19]. A recent study by Tang et al. [17] showed unexpectedly increasing underway N₂-fixation rates from the oligotrophic Sargasso Sea to American coastal waters with the highest activities close to the coast, and some of the N₂-fixation hotspots coincided with high phosphorus concentrations near the surface.

We investigated the distribution of Trichodesmium in the Benguela upwelling system (BUS), one of the most productive upwelling systems in the world [20]. It is located off the west coast of southern Africa, bordering Angola, Namibia and South Africa (Fig. 1). The productivity of the system is driven by strong alongshore trade winds and upwelling of cold, nutrient-rich water into the euphotic zone. It is traditionally divided into a northern and a southern subsystem [21–23]. The northern BUS (nBUS) is located between the Angola-Benguela Front (14°S to 16°S), and the Lüderitz upwelling cell at approximately 26.30°S [24] is influenced by South Atlantic Central Water (SACW), intruding from the Angola Gyre. The southern BUS, fed by Eastern South Atlantic Central Water (ESACW) flowing in from the Cape Basin (sBUS), is limited in the south by the warm Agulhas Current at 34°S. The Agulhas Current is a strong warm and salty western boundary current originating in the southwestern Indian Ocean, following the continental shelf from Maputo to the Agulhas Bank, where it leaves the shelf and abruptly turns eastward in the Agulhas retroflection. By turning around rings detach from the current moving onward into the South Atlantic Ocean [25–27]. This ‘Agulhas leakage’ strongly varies on interannual to decadal timescales [28]. Marshall et al. [29] traced water mass circulations in the Agulhas Current using nitrate isotopes. They stated that nitrogen fixation occurs in the Agulhas Current, resulting in a low δ¹⁵N signature, and Agulhas rings indicate leakage of low-δ¹⁵N nitrogen into the South Atlantic. However, little is known about the interoceanic transport pathways of plankton organisms such as Trichodesmium in these rings or eddies.

Reports of the presence of Trichodesmium or indications of N₂ fixation in the Benguela Upwelling System (BUS) are inconsistent. While Wasmund et al. [19] found very low abundances of Trichodesmium and no evidence of N₂ fixation in the northern BUS, Sohm et al. [18] reported elevated N₂ fixation rates in or near the Benguela Current compared to the oligotrophic South Atlantic Gyre. They found that high NO₃⁻ concentrations did not exclude N₂ fixation in upwelling areas.

A remotely operated towed vehicle (TRIAXUS), equipped with several sensors and an attached Video Plankton Recorder (VPR), enables simultaneous measurements of biogeochemical and physical water mass properties combined with the occurrence of planktonic organisms over large distances. Because Trichodesmium colonies are easily damaged by conventional net hauls, Niskin bottles or buckets [30], noninvasive techniques such as underwater camera systems seem to be more appropriate to study these objects. By using the TRIAXUS mounted VPR, we will provide the first evidence of possible interoceanic transport pathways of Trichodesmium from the Indian Ocean into the Atlantic Ocean as well as provide information about its distribution in the Benguela upwelling region.

Trichodesmium colonies were detected using a VPR in both investigated regions of the BUS, with lower abundances in the nBUS than in the sBUS (Fig. 2a-d and 3a-d).

The blue algae occurred rarely at the surface but mostly between 30 and 60 m, down to 140 m in the north and 100 m in the south, respectively, and in waters of higher salinity >35.1 (Fig. 2b and 3b). In colder nitrate-rich upwelled waters close to the coast, Trichodesmium was not detected (Fig. 2a, 2c and 3a, 3c). In the north as well as in the south, Chl a values were slightly higher in the vicinity of the colonies (Fig. 2d and 3d). Most Trichodesmium colonies (Fig. 4) were detected in salinity bins between 35.30 and 35.39 in the sBUS and between 35.20 and 35.29 in the nBUS (Fig. 5).

A TRIAXUS mounted VPR proved to be a well-suited gear to detect fragile organisms such as Trichodesmium within its natural habitat: colonies could be quantified without being destroyed down to a depth of 200 m, and environmental data could be measured simultaneously, thus making it possible to relate these data to the occurrence of the organisms.

The low temperatures and increased nitrogen values near the coast compared to offshore waters indicate that coastal upwelling had taken place recently in both regions, with a stronger signal in the sBUS. It was apparent that Trichodesmium was absent in these cold, nutrient-rich onshore waters. Colonies were found further offshore in subsurface and deeper water layers at temperatures below 18°C on both transects but with distinctly higher abundances in the sBUS. Our data showed, in contrast to other investigations [13, 31, 32], that Trichodesmium was not limited to areas of warm water > 20°C. However, the abundance frequency was highest in water lenses with comparatively high salinity (see also Fig. 5).

The nBUS and sBUS are fed by different source waters, causing lower salinities of < 35 in the south due to the inflow of ESACW from the Cape Basin. The fact that the water lenses showed much higher salinities makes it likely that the salt anomalies are caused by Agulhas rings, which transport their persisting salt content to the South Atlantic [33], even though they lose their anomalous surface thermal content quickly to the atmosphere [34]. We assume that the elevated salinity concentrations are signs of eddies originating from the Agulhas Current and by moving northward taking the Trichodesmium colonies to the offshore regions of the Benguela Current. Such a mechanism of colony transport has been previously reported. Davis and McGillycuddy [35] used a towed VPR for quantification of planktonic organisms, i.e., for the detection of Trichodesmium. They described increased colony concentrations in warm and salty water of anticyclonic eddies during an east‒west transect in the North Atlantic but could not elucidate the underlying mechanisms of these findings.

Similar to our study, Davis and McGillycuddy [35] detected higher densities of Trichodesmium colonies in subsurface depths and assumed that such a distribution was rarely mentioned in other reports because net tows from greater depth would easily destroy and fragment fragile colonies, thus making the organism undetectable. They further assumed that the high abundances they found in deeper water indicated that previous calculations underestimated the N₂-fixation rates of Trichodesmium, and a correction of these calculations might even explain the missing nitrogen in the global nitrogen cycle. This would make Trichodesmium a crucial organism for primary production in the world oceans. However, increased nitrate values in the vicinity of the colonies were not measured in our study, whereas slightly higher Chl a concentrations in the surrounding Trichodesmium concentrations were detected. Whether this increase in chlorophyll is caused by or partly by Trichodesmium can only be speculated. Another reason for the sinking of the Chl a maximum with increasing distance from the coast, especially in upwelling regions, could be a deeper Chl a maxima because the penetration depth of light increases with decreasing suspended matter offshore.

In studies by Wasmund et al. [19] from seven cruises (66 stations) in the nBUS, Trichodesmium was detected only at two stations. If we assume that organisms are transported by eddies from the Indian Ocean into the BUS, the patchy occurrence of Trichodesmium can be explained by the strong interannual to decadal variation in Agulhas leakage [28]. Biastoch et al. [27] reported an increasing trend of Agulhas leakage caused by intensifying Southern Hemisphere westerlies. Model experiments predict a continuation of the increase with strengthening of the westerlies as a result of global warming [36], which could imply an increase in Trichodesmium abundance in the BUS.

A Video Plankton Recorder mounted on a towed and undulating TRIAXUS proved to be a suitable gear to study the fragile colonies of the diazotroph cyanobacterium Trichodesmium. Trichodesmium was detected in austral summer in the nBus as well as in the sBUS. However, colonies were absent in colder recently upwelled surface water, indicating a different source water mass for these cells. The higher abundance in water lenses of elevated salinity compared to surrounding waters provides evidence that detached Agulhas rings moving northward may transport Trichodesmium from the Indian into the Atlantic Ocean. Marshall et al. [29] traced water mass circulations in the Agulhas Current using nitrate isotopes and stated that nitrogen fixation occurs in the Agulhas Current and that Agulhas rings indicate leakage of low-δ¹⁵N nitrogen into the South Atlantic. We provide further evidence of this pathway by detecting N₂-fixing Trichodesmium in the Benguela Current region associated with water masses with an Agulhas signature.

During a cruise with the research vessel METEOR (M153) in February and March 2019 [37], two transects in the northern and southern Benguela Upwelling System (nBUS and sBUS) were examined (Fig. 1, Table 1). The expedition took place as part of the TRAFFIC project (Trophic transfer efficiency in the Benguela Current [23]). In addition to other devices, a TRIAXUS equipped with a CTD, a video plankton recorder (VPR) and a nitrate sensor was deployed (see below).

Table 1

Specifications of studied transects
Date	Time UTC	Lat	Long	distance
25–26 Feb 2019	15:25 − 09:18	-31.00 - -30.39	14.82–17.26	249 km
12–13 Mar 2019	20:13–21:33	-22.60 - -23.00	14.30–10.76	374 km

Remotely Operated Towed Vehicle - TRIAXUS

The TRIAXUS ROTV (Remotely Operated Towed Vehicle, MacArtney, Fig. 6) was used to conduct high-speed large-scale measurements. The TRIAXUS is a towfish with a possible towing speed between 2 and 10 knots and a vertical speed of up to 1 meter to undulate between 1 and a maximum of 350 meters. A lateral offset of up to 80 meters to either side of the ship makes it possible to avoid disturbance from the wake of the ship during measurement [38]. The ROTV was towed at a speed of 8 knots (4.1 m s^− 1), undulating with a vertical speed of 0.1 m s^− 1 from 5 m below the sea surface to a maximum depth of 200 m or at least 5 m above the sea floor. In addition to the VPR, the TRIAXUS was equipped with several other sensors, including a pumped Seabird Fast Cat SBE 49 CTD (see supplementary data nBUS Trichodesmium & sBUS Trichodesmium).

Video Plankton Recorder - VPR

The VPR (Seascan) is a digital underwater camera system equipped with a high-resolution digital camera (Pulnix TM-1040) that records 25 image frames s^− 1. A strobe (Seascan − 20 W Hamamatsu xenon bulb) provided the illumination for the images with a pulse duration of 1 µs that was synchronized with the camera shutter. The chosen field of view was 24 x 24 mm with a focal depth of ~ 60 mm at 246 mm from the lens. The image volume was 34.93 ml (33x33x33 mm), and the spacing between images was 0.163 m. The northern transect covered a distance of 374 km, and the southern transect covered 249 km, with an hourly mean sampling volume of 2.9 m³*h^− 1. In total, a volume of 73.62 m³ was analyzed.

Analysis and classification of images and sensor data were sent in real time to an onboard unit via a fiber optic cable. Imaged particles were extracted as regions of interest (ROIs) by Autodeck image analysis software (Seascan Inc.) and saved to the computer hard drive as TIFF files. Each ROI was tagged using a time stamp to allow merging with the hydrographic parameters that were written to a separate logfile.

Detection of Trichodesmium (software)

For automated plankton classification, training and application of deep learning models were performed with a GPU-supported TensorFlow [39] backend for Keras [40] under Python 3.7 [41]. Training sets developed by Plonus et al. [42] using VPR images taken during cruises in the North Sea and Baltic Sea were used and evaluated manually. On the studied images, Trichodesmium colonies could be easily recognized due to their unique form and the fact that they were very rarely photographed overlapping with other species. Free trichomes could not be securely identified, which is why only colonies were counted. Trichodesmium densities were calculated by taking the calibrated image volume of a single frame multiplied by the number of images taken.

Acknowledgment

BM and RK as well as the use of the RV Meteor were funded by a grant from the Federal Ministry of Education and Research in Germany (FKZ 03F0797C). We thank the crew and captain of the RV Meteor for their great support.

Author contributions: Writing and editing BM & RK. Data collection RK, BM, AH. Programing AH & RP.

Competing interest: The authors declare that they have no competing interests.

Data availability: All data needed to evaluate the conclusions in the paper are included in the paper or in the supplementary material.

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You are reading this latest preprint version

Possible transport pathways of diazotrophic Trichodesmium with Agulhas rings from the Indian Ocean into the Atlantic Ocean

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Abstract

Figures

Introduction

Results

Discussion

Conclusion

Material and methods

Remotely Operated Towed Vehicle - TRIAXUS

Video Plankton Recorder - VPR

Detection of Trichodesmium (software)

Declarations

References

Additional Declarations

Supplementary Files

Status:

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