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Observations on the Tubicolous Annelid Magelona Alleni

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Observations on the Tubicolous Annelid Magelona Alleni Journal of the Marine Observations on the tubicolous annelid Biological Association of the United Kingdom Magelona alleni (Magelonidae), with discussions on the relationship between cambridge.org/mbi morphology and behaviour of European magelonids Original Article Kimberley Mills1,2 and Kate Mortimer1 Cite this article: Mills K, Mortimer K (2019). Observations on the tubicolous annelid 1Department of Natural Sciences, Amgueddfa Cymru – National Museum Wales, Cathays Park, Cardiff CF10 3NP, Magelona alleni (Magelonidae), with Wales, UK and 2School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK discussions on the relationship between morphology and behaviour of European magelonids. Journal of the Marine Biological Abstract Association of the United Kingdom 99,715–727. Feeding, defecation, palp behaviour and motility of the tubicolous annelid, Magelona alleni https://doi.org/10.1017/S0025315418000784 were observed in a laboratory environment. Both surface deposit, and to a lesser extent, sus- Received: 24 May 2018 pension feeding were exhibited, with the ingestion of sand grains, and of smaller amounts of Revised: 21 August 2018 foraminiferans and administered commercially available suspension. Predominantly sand Accepted: 23 August 2018 could be seen moving through the gut, resulting in conspicuous defecation, not previously First published online: 8 October 2018 observed in other magelonid species. During this ‘sand expulsion’ behaviour, individuals Keywords: turned around in a network of branched burrows. The posterior was extended from the bur- Anus; burrowing; defecation; diet; feeding row and substantial amounts of sand were expelled in a string-like formation, involving guilds; Magelona johnstoni; Magelona mirabilis; mucus. The posterior morphology of M. alleni differs greatly compared with other Magelona sacculata; pygidium; tubes European magelonid species, in possessing a large terminal anus, likely related to its diet. Author for correspondence: In contrast to what has been recorded for other magelonids, M. alleni appears predominately Kimberley Mills, Email: [email protected] non-selective. The current paper adds credence to the idea that multiple feeding modes exist within the family. Tube-lined burrows were observed to be primarily permanent, and motility of the species reduced in comparison to other magelonids. The differences noted between M. alleni and other species is most likely linked to its tubicolous lifestyle. The effect of environ- mental parameters on observed behaviours is discussed. Introduction The Magelonidae is a small family of annelids found worldwide, with distinctly flattened, spade-like prostomia. They possess a pair of ventrally inserted, papillated palps unique to the family. The majority of Magelona species occupy sandy-muddy habitats (Uebelacker & Jones, 1984) at shallow depths (Rouse, 2001a; Blake, 2006), although deep-water species have been described (Hartman, 1971; Aguirrezabalaga et al., 2001). The family is predomin- ately distributed in coastal areas and on continental shelves (Hernández-Alcántara & Solís-Weiss, 2009). Magelonids have been primarily described as surface deposit feeders (Jones, 1968; Uebelacker & Jones, 1984). Suspension feeding has been reported for Magelona johnstoni Fiege, Licher & Mackie, 2000 (Mortimer & Mackie, 2014) and additionally suggested for other magelonid species by Hartmann-Schröder (1971), Wolff (1973) and Rouse (2001a). Conversely, Jumars et al.(2015) indicated that subsurface feeding (primarily based on obser- vations of Magelona pitelkai Hartman, 1944) and carnivory may be more common within the family than previously indicated. Fauchald & Jumars (1979) considered feeding to be selective, with selectivity increasing in nutrient-poor conditions. Diets of a number of magelonid species have been described to include crustaceans, crust- acean larvae, silt, detritus, sandy detritus, sand, diatoms, algal cysts, spores, tintinnids, mol- luscs, worms and other small animals (McIntosh, 1911; Hunt, 1925;Mare,1942; Jones, 1968; Hartmann-Schröder, 1971; Wolff, 1973; Kühl, 1974). Despite these records, knowledge of species-specific diets is lacking. Additionally, Mortimer & Mackie (2014) suggested the like- © Marine Biological Association of the United Kingdom 2018 lihood of interspecific variation in diets of co-existing European magelonids. In general, magelonids have been reported to be relatively motile, burrowing more or less continually through sediments (Jones, 1968; Fauchald & Jumars, 1979; Mortimer & Mackie, 2014). Although some species such as Magelona polydentata Jones, 1963, Magelona variola- mellata Bolívar & Lana, 1986, Magelona longicornis Johnson, 1901 (Jones, 1971), Magelona cincta Ehlers, 1908, Magelona falcifera Mortimer & Mackie, 2003, Magelona symmetrica Mortimer & Mackie, 2006 and Magelona alleni Wilson, 1958 have previously been reported to construct tubes (Mortimer et al., 2012; Mortimer, 2017), no information on the permanency of tubes has been recorded. Currently, nine European magelonids are described (Fiege et al., 2000; Aguirrezabalaga et al., 2001; Mortimer et al., 2011): Magelona filiformis Wilson, 1959, Magelona wilsoni Glémarec, 1966, Magelona minuta Eliason, 1962, Magelona mirabilis (Johnston, 1865), Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 25 Sep 2021 at 05:47:03, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315418000784 716 Kimberley Mills and Kate Mortimer M. johnstoni, Magelona lusitanica Mortimer, Gil & Fiege, 2011, temperatures for Plymouth (10–17 °C). An aquarium pump and Octomagelona bizkaiensis Aguirrezabalaga, Ceberio & Fiege, large air stone were employed to aerate the water and create a cur- 2001, Magelona equilamellae Harmelin, 1964 and M. alleni. The rent and continuous flow within the tank. Observations were car- latter species is readily distinguished from all other European ried out under ambient photoperiods. Magelona in having sub-equal abdominal lamellae (Fiege et al., 2000). It possesses a wider-than-long prostomium and a con- Tank observations spicuous reddish pigment band on posterior thoracic chaetigers, as described by Wilson (1958)(Figure 1B). Initially, three individuals were observed for a 6-month period Defecation in magelonids has not been previously described, (July 2017–January 2018) through time-lapse photography (see and due to their fragility upon collection, many magelonid species Figure 1A, Canon EOS 6D 20.2 MP DSLR camera, Canon EF descriptions do not contain figures or information of the poster- 100 mm f/2.8 L Macro IS USM lens), with a further three indivi- ior region. Consequently, there has been minimal attention direc- duals observed during 2018. At first, captures were carried out at ted at the morphology of the pygidium. At present, the pygidia of differing intervals, ranging from 30 s to 5 min, either throughout 16 magelonid species have been illustrated (Mortimer, 2017). the day or night, to ascertain the best times for undertaking obser- Rouse (2001a), primarily based on the type description and illus- vations. It was then determined that 24 h capture periods at 3 min tration of Magelona sacculata Hartman, 1961, stated that the intervals, 6 days a week, would provide comprehensive results. magelonid anus is terminal. However, early illustrations from However, further captures at shorter intervals were carried out McIntosh (1878)ofM. mirabilis (possibly M. johnstoni, see in order to investigate particular behaviours. Observations were Fiege et al., 2000) clearly show the anus in a distinctly ventral pos- additionally made throughout using a microscope held horizon- ition. Unfortunately, the majority of subsequent illustrations are tally as described by Mortimer & Mackie (2014). from a dorsal view, and the position of the anus is not clearly visible. In situ experiments In order to add clarity, posterior regions of several European species and M. sacculata have been investigated in comparison Worms were initially offered a variety of foods, the choice of to M. alleni. Furthermore, the present paper aims to increase cur- which was based on information from previous magelonid obser- rent understanding of the behaviour and diet of magelonids, vations and what is known about magelonid diets (e.g. Jones, including the first record of defecation for the family. The tubico- 1968; Taghon et al., 1980; Forbes et al., 1996; Williams, 2002). lous lifestyle of M. alleni is discussed in relation to all observed Based on initial trials it was decided that two food suspensions behaviours. (SeAquariums Invertfood and NTLABS Invertebrate Food, mixed equally), both containing plankton and essential nutrients, would be gently administered into the water column above the Materials and methods tank every 7 d using a plastic pipette. Observations through the Animal collection and processing microscope were made directly afterwards to determine reactions and corresponding behaviours, in addition to ongoing time-lapse Benthic samples were collected from Jennycliffe Bay, Plymouth ′ ′ photography. Sound (50°20.91 N 4°07.71 W, 8 m, muddy sand) from RV Approximate palp length (overall length, ratio at surface) was ‘ ’ Sepia on 27 March 2017 using a short-armed, chain-rigged calculated using a line gauge from time-lapse photographs for Van Veen grab. Samples were gently washed with copious comparison to other European Magelona species. Sand expulsion amounts of seawater
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