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Systematics of a rare radiolarian—Coelodiceras spinosum Haecker (Sarcodina: Actinopoda: Phaeodaria: Coelodendridae) Harriet L. Patersona,b,, Stephane Pesantc,1, Peta Cloded, Brenton Knotta, Anya M. Waitec a
Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia b CSIRO Marine Research Private Bag No. 5, Wembley WA 6913, Australia c School of Environmental Systems Engineering, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia d Centre for Microscopy and Microanalysis, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia
Abstract We describe a specimen of Coelodiceras spinosum Haecker 1908 [Haecker, V., 1908. Tiefsee-Radiolarien. Wissenschaftliche ergebnisse der Deutschen Tiefsee-Expedition. 14, 1–706] (Sarcodina: Actinopoda: Radiolaria: Phaeodaria: Coelodendridae) collected in a sediment trap deployed in the Indian Ocean, 300 NM WNW off Perth, Western Australia, updating Haecker’s 1908 description. Our specimen was collected in the centre of a cold-core eddy at a depth of 300 m. The intact silica structure of the specimen lacked soft organic material, suggesting that the organism was dead when it entered the trap; the traps were deployed for 10 days and did not contain poison or preservative. In this paper, we expand the original description of C. spinosum by Haecker (1908) [Haecker, V., 1908. Tiefsee-Radiolarien. Wissenschaftliche ergebnisse der Deutschen Tiefsee-Expedition. 14, 1–706], using Scanning Electron Microscopy (SEM). Our specimen had three frenula and a short rhinocanna, differing from the single frenulum and long rhinocannae described by Haecker (1908) [Haecker, V., 1908. Tiefsee-Radiolarien. Wissenschaftliche ergebnisse der Deutschen TiefseeExpedition. 14, 1–706]. r 2007 Elsevier Ltd. All rights reserved. Keywords: Indian Ocean; Upwelling; Radiolaria; Silica flux; Zoogeography; Micropaleontology
1. Introduction Phaeodarians constitute a little studied group of small, omnivorous animals within the phylum Corresponding author. Fax: +61 8 6488 1015.
E-mail address:
[email protected] (H.L. Paterson). Current address: Observatoire Oce´anologique, Laboratoire d’Oce´anographie de Villefranche, BP. 28, 06234 Villefranche-surMer Cedex, France. 1
0967-0645/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2006.05.046
Sarcomastigophora, subphylum Sarcodina, superclass Actinopoda (Levine et al., 1980). Radiolarians were first described by Meyen (1834), and phaeodarians were first reported, from oceanic sediments, by Bailey (1856). The planktonic species Coelodiceras spinosum Haecker (1908), in particular, is rarely sampled (Popofski, 1926; Reshetnjak, 1966) due to its paucity in plankton assemblages, and limited representation in fossil records is further enhanced by dissolution of their silica shells (Reshetnjak, 1971;
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Dumitrica, 1973). A specific attempt was made to find phaeodarian shells during leg 21 of the deep sea drilling project (Dumitrica, 1973). While whole shells were rare, fragments were found in almost all deposits, but not in sufficient detail to allow identification (Tibbs and Tibbs, 1986). Knowledge of phaeodarians in plankton assemblages rests predominantly within the monographic treatises of Haeckel (1862, 1887) and Haecker (1908), all based on material collected during the epic voyages of the Challenger and the Valdivia in the 19th and early 20th centuries. In more recent accounts, Kling (1976), Takahashi and Honjo (1981), Gowing and Silver (1983), Gowing (1986, 1989), Kling and Boltovskoy (1999), and Yamashita et al. (2002) have reported phaeodarians in studies that focused on the distribution and feeding ecology of larger protists, and on silica fluxes. Specimens have been collected mainly in opening and closing nets, and sometimes in sediment traps (Takahashi and Honjo, 1983; Takahashi, 1984) and Swanberg et al. (1986) collected live specimens with a submersible. The subclass Radiolaria is divided into the superorders Phaeodaria and Polycystina. Phaeodarians are distinguished by three features: (1) a thick and a thin membrane around the central capsule; (2) a main opening or astropyle, located in the centre, which has a peculiar radiate operculum with tubular proboscis; and (3) a phaeodium, consisting of food vacuoles and waste products, notably silica, located in the calymma over the oral part of the central capsule (Haeckel, 1887). Other important features of this group are paired galeae and rhinocanna, multiple frenula (ligaments), and one valve (bivalved). The central mass of the cell is encapsulated in the valve that is articulated at the astropyle or mouth. The galeae, prominent apophyses of each half of the valve, support the styles or legs of the organism. Each galea has a tubular structure, the rhinocanna, which arises from the base of the galea and terminates at the articulation of the valve; it opens the galea to the calymma. Each rhinocanna is supported by frenula which connect the opening of the rhinocanna to a galea. A translation of Haecker’s (1908 p. 366) description is as follows: On the whole, butterfly shaped but compressed laterally. The galea is larger than the valve with curved faces, triangular in appearance. Rhinocannae snout shaped, longer than in Coelodiceras macrophylum. Rhinocannae almost reach the oral region at the margin of the valve.
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Open ends of the rhinocannae supported by frenula. Nasal tubes branch at obtuse angles, similar to C. macrophylum. Anchor threads found before termination of the style possessing two rows of teeth. Thorns/spikes on the terminal branches are well developed. Despite phaeodarians being a minor component of the plankton, they still contribute to the ecology of the ocean—by transfer of silica through vertical flux between the sediments and the water column (Takahashi and Honjo, 1983), and by their contribution to food webs (Gowing, 1986, 1989). Gowing (1989) showed that Antarctic phaeodarians are omnivorous, providing a trophic link between pico-phytoplankton and mesozooplankton, consuming items ranging from bacteria to large protists. Among their diets were diatoms, dinoflagellates and Chlorella-like cells. Gowing (1986) also found that phaeodarians were consumed by nonselective particle-feeding organisms such as the salp, Salp thompsoni. Their vertical distribution differs from that of other microphagous predators, with their greatest biomass often located below the photic zone where they feed on detrital material (Nimmergut and Abelmann, 2002). The contribution of phaeodarians to the silica flux stems from their siliceous skeleton, but more interestingly from the existence of the phaeodium, a cellular structure that contains concentrated silica in waste vacuoles. In the present paper, we document the capture of one specimen of C. spinosum in a mid-water sediment trap (300 m) and based on this specimen, we expand on the original description of C. spinosum by Haecker (1908), using Scanning Electron Microscopy (SEM). Finally, we comment on the global biogeographical significance of these animals. 2. Materials and methods The specimen was collected in October 2003, 300 NM off the coast of Western Australia (WA) during a multidisciplinary study onboard the RV Southern Surveyor investigating the biological significance of cold- and warm-core eddies (Fig. 1). The physical, chemical, and biological results are presented by Feng et al. (2007) and Waite et al. (2007). A free-drifting drogue with two sediment traps (100 and 300 m) was deployed. The traps consisted
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Fig. 1. The location of two eddies (cold-core, warm-core), all stations samples during investigation (J) and location of trap retrieval with specimen. (K). Insert: Australia showing location of study area.
of four replicate cylinders equipped with baffles and mounted on a cross frame with a minimum distance of 50 cm between pairs of traps and between traps and the mooring line (see Nodder and Alexander (1999) for methodological considerations of drifting sediment traps). A complete description and results are presented by Waite et al. (2007). The specimen of C. spinosum was collected on a taxonomic filter from the deeper sediment trap, after a deployment of 10 days in the cold-core eddy. It was subsequently isolated, air-dried, and carefully transported to the Centre for Microscopy and Microanalysis at The University of Western Australia. The specimen was mounted on a glass slide and examined, uncoated, in a Zeiss 1555 Variable Pressure Field Emission Scanning Electron Microscope. All images were collected in variable pressure mode at 10 kV. Size measurements were made from the digital image using ImageJ. 3. Results 3.1. Systematics Our specimen displayed the three characteristics of phaeodarians. However, instead of the single frenulum and long rhinocannae described by Haecker (1908), our specimen had three frenula and short rhinocannae. This specimen was distinguished from other similar forms by the number and
arrangement of styles, location of aboral tubes, and location of anchor hooks on the nassal styles and terminations of styles with corona of hooks. This specimen was dead when it was recovered from the trap and the soft organic material of the cell was missing and hence cannot be described here. There was, however, evidence of rhizopodal strands, a tent-like membranous structure supported by the styles. 3.2. General morphology 3.2.1. Soft parts The specimen (Fig. 2) was white and shiny when collected with organic veil, presumably of rhizopodal remains, and siliceous skeleton. The veil disintegrated over a period of 1 year leaving only the skeleton. There were no other soft body parts. 3.2.2. Body plan Diameter was o4.0 mm; the body plan was basically bilaterally symmetric but the symmetry was disturbed by unequal development of the three pairs of styles, which varied in length. In this paper, we use the sagittal plane to describe the main plane between the two galeae, and the left and right sides as indicated in Fig. 3, the transverse plane to delineate between the oral and aboral areas of the cell and the frontal plane to differentiate between the front and back with respect to the page
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orientation of Fig. 3. The nasal styles in the frontal plane are long but unequal with the left longer than the right. The nasal styles have bushes located between the third and fourth branches. Each of the two main styles on the left and right sides of the animal are unequal in length. Both galeae (Fig. 4) are tetrahedral, the bases triangular and slightly convex, and the styles
originate from the three corners of the galea base; the surface is predominately smooth with some pitting. The inner oral apex of each galea forms into a rhinocanna. Rhinocanna (Fig. 5), height approximately two-thirds the height of the galea, hollow, and open. The rhinocannae openings flare into a lip supported by three frenula (Fig. 5), which connect the outer lip of the rhinocanna back to the galea
Fig. 2. Coelodiceras spinosum: whole skeleton. Scale bar ¼ 200 mm.
Fig. 4. Coelodiceras spinosum: the two galeae (G) with styles, nasal (NS) and main (MS), arising from the corners. Scale bar ¼ 20 mm.
Fig. 3. Coelodiceras spinosum: drawing of whole skeleton, based on the SEM image in Fig. 2, showing left and right sides, nasal styles and main styles. Net veil, only partially drawn, covered entire specimen when captured. R, rhinocannae; F, frenulum; V, valves; and G, galea; A, aboral rubes. The transvers and sagittal planes are orientated 901 to the page.
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Fig. 5. Coelodiceras spinosum: showing the articulation of the two galeae (G), rhinocannae (R), frenulum (F) and valves (V); arrows show the extreme variation in width of the frenulum. Scale bar ¼ 20 mm.
Fig. 6. Coelodiceras spinosum: Distal tips of the styles, recurved teeth of corona visible and individual recurved teeth on the last branch of the style. Scale-bar ¼ 2 mm.
near the base of the styles. The valves (Fig. 5) located between the two galeae and rhinocannae are hemispherical and partially fenestrated. The surfaces of the galeae appeared smooth. In this specimen, the central capsule and calymma are missing and the two halves of the valve are not supported, with the openings of the rhinocannae separated. An indentation in the wall of the rhinocannae where they articulate may indicate the position of the mouth, facilitating connection between the mouth and the cytoplasmic mass of the phaeodium. 3.2.3. Style tips and distal branches Terminal branches regularly forked, with two equal, smooth, straight, forked branched diverging at right angles, end knobs (Fig. 6) with the corona comprising two or three rows of recurved teeth: the basal row with 14–16 teeth; the intermediate row with 11–12 teeth; and the crowning row with 4–5 teeth. Final branches with irregularly spaced thorns (length 5 mm; Fig. 6), resembling the recurved teeth. Preceding branches (Fig. 7) with slender thorns p18 mm in length. 3.2.4. Styles Six styles originating from the galeae corners branch between five and seven times. Each split produces evenly sized branches orientated at 901 to the previous. The base of each style between 90 and 100 mm wide, reducing after 100 mm length to 50 mm. Style width of 50 mm constant for the next two or three splits, then reducing to 40 mm. Styles narrow at the second last branch to 16 mm and the last
Fig. 7. Coelodiceras spinosum: Terminal branches with thorns. Scale bar ¼ 20 mm.
segment is 10 mm wide. The two nasal styles (left and right) located in the frontal plane (1670 mm and 1950 mm, respectively); the four main styles are paired, (left and right) located either side of the frontal plane. Total lengths are; left 1100 and 1250 mm, and right 1140 and 1250 mm. 3.2.5. Anchor bush Anchor bushes (Fig. 8A) present only on nasal styles between the third and fourth branches. Bushes composed of two parts: the main stem (Fig. 8B) 200 mm in length with 3–4 dichotomous branches, final branching bidentate, and p100 mm in length; second part composed of anchor threads (Fig. 8A) rising from the bidentate branches support the anchor hooks (Fig. 8C). The hooks are pick shaped with 22–26 small teeth. The hooks, 50 mm in
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3.2.7. Rhinocannae Each cylindrical rhinocanna (height 90 mm, diameter 150 mm: Fig. 5) rises from the galea and widen near the top, the opening flaring into a broad lip 30–40 mm wide. 3.2.8. Frenulum There are three frenula attached to each rhinocanna, each 140 mm long and associated with a style. They originate from the broad lip of the rhinocanna and attach to the galea 100 mm from the base of the rhinocanna, and 100–150 mm from the base of their associated style. The two frenula associated with the main styles narrow to 12 mm wide, thickness 5 mm, (Fig. 5) prior to their first level of attachment to the galea widen to 25 mm (two attachments), then narrow to 3 mm at the final attachment. The frenulum associated with the nasal style is broader (77 mm) and has a number of elongate fenestrae. 3.2.9. Aboral tubes One aboral tube (length 300 mm; Fig. 9) occurs in association with the base of each galea and valve, but it has not been possible to resolve its precise point of articulation. Main stem 80 mm, with one dichotomous branch, each extending 220 mm. 3.3. Oceanography The two eddies examined during this voyage formed on the shelf off Western Australia in April, 2003, and moved westwards to the location where they were examined in October, 2003. The cold-core (anticlockwise) and warm-core (clockwise) eddies
Fig. 8. Coelodiceras spinosum: showing anchor bushes of the nasal styles. (A) Entire anchor bush. (B) Main stem and dichotomous branches of anchor bushes, (C) Pick-shaped anchor hooks. Scale bar: A, B, 20 mm; C 10 mm.
length, 3 mm wide and from 5 mm in depth, thin towards the free end. 3.2.6. Valves The valves (Fig. 5) approximately cap shaped. The valve is fenestrated towards the equator, with the margin lace-like in appearance. The few fenestrae near the galea and rhinocanna are small (2 mm).
Fig. 9. Coelodicera spinosum: Aboral tubes (A) with valves and galea visible, left tube is seen with dichotomous branching, right tube after branching. Scale bar 20 mm.
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were moving in an anticlockwise direction around each other, with the warm-core eddy moving north, north east and the cold-core eddy progressively south west. There are two possible sources of the cell. As this was an upwelling region the cell may have originated from a greater depth. In support of this hypothesis, the temperature and salinity of the water ambient to the 300 m deep trap were 7.7 1C and 34.5, respectively. Isotherms in the centre of the eddy, a SeaSoar temperature transect of a complete cross section of the cold-core eddy, indicate that the water proximal to the sediment trap was upwelled (Waite et al., 2007). However, given that the cell was dead, it is possible that it was part of flux sinking out of the photic zone. 4. Discussion To date, there has been no addendum to the original description of C. spinosum given by Haecker (1908), undoubtedly reflecting the paucity of material, despite the collection of conspecific specimens from both the southern (Haecker, 1908), and the northern (Popofski, 1926), hemispheres. Our specimen shows close congruence with Haecker’s (1908) description with two exceptions: (1) Haecker’s specimens had only one frenulum, while ours has three and (2) the rhinocannae were long in Haecker’s specimen, while ours are short. This species is easily confused with Coelodiceras macrophylum, particularly given the apparent shortness of the rhinocannae. The greatest difference is in the structure of the aboral tubes, which are substantially different between these two species. C. macrophylum has two aboral tubes arising separately from the valve, while C. spinosum has one tube which forks once. Haecker’s illustration was redrawn by Popofski (1926) (Fig. 10) but without change to structural detail, and has been reproduced in a number of papers, including Reshetnjak (1966) and Kling and Boltovskoy (1999). The illustration presented here shows a reduction in the length of the nasal and main styles, in addition to a reduction in the prominence of the anchor threads on the nasal style. This individual also has a veil, which had presumably disintegrated on the specimens examined by Haecker. The present study has expanded the description of this species by providing an updated drawing and SEM images. Elucidating the biogeographic significance of this species is rendered difficult due to the scarcity of
Fig. 10. Coelodiceras spinosum: reproduced from Popofski 1926, scanned and available from http://www.radiolaria.org/ plate.htm?pl_id=36 Plate 4.
data (Fig. 11, Table 1). Haecker (1908) described this species as occupying the southern, cooled water of the Atlantic and Indian Oceans. However, Popofski (1926) and Reshetnjak (1966, 1971) identified this species also from cooler waters of the northern hemisphere in both the Atlantic and Pacific Oceans. In addition, Popofski (1926) reported this species from the North and South Equatorial Currents of the Atlantic, although the exact location was not given. Such widely disjunct distributions of planktonic organisms raise the question of their genetic relatedness. The methods of modern DNA analysis could be applied to such genera to determine if forms from separate oceans represent separate lineages and elucidate the phylogeographic history of the group. Alternatively, if the forms from the different oceans show little genetic separation, it presents an opportunity of using the species to trace advection of water masses. Acknowledgements We acknowledge financial support from The University of Western Australia (UWA) and the Strategic Research Fund for the Marine Environment (SRFME); technical support from the Centre for Microscopy and Microanalysis (CMM) and the Environmental Research Laboratory at the Centre
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60°N 30°N 0° 30°S 60°S
180°W
120°W
60°W
0°
60°E
120°E
180°W
Fig. 11. World distribution of Coelodicera spinosum. Grey shapes represent general phaeodarian investigations, black dots—location of C. spinosum.
Table 1 Location and dates of previous finds of Coelodiceras spinosum Year
Ship
Location
Total Depth m
No Individuals
Authors
2003 1953 1898
Southern Surveyor Vitjaz Valdivia
This volume Reshetnjak (1966, 1971), Reshetnjak (1966) Haecker (1908)
National
300 1000–2000 5000 2750 4500 600 500 500 400
1
1889
Indian Ocean Kamchatka Depression Benguela Agulhus Indian Ocean Irminger sea Labrador North equatorial current South equatorial current
5 1 1 2
Popofski (1926)
for Water Research (UWA). We acknowledge enthusiastic support from Dr. Brendan Griffin and his team at CMM; Ellen Hickman for illustrating the specimen; Carina Moeller for her translation of Haecker’s 1908 description; the contribution of the CSIRO National Research Facility R.V. Southern Surveyor. Particular gratitude is extended to Dr. Peter Thompson for his contribution towards conceiving and undertaking this research into Antipodean eddies.
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