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Phyllodoce novahollandiae (Kinberg, 1866)
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Charlotte Dudal 2015
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Summary |
Brief summary | |
The Green Paddle Worm, Phyllodoce novaehollandiae, is a benthic predatory polychaete of the order Phyllodocida. It is a common invertebrate in sand-flat habitats, and is usually found crawling or swimming on the sediment surface during low tide. The bright green dorsal coloration and the leaf-shaped appendages are what give P. novaehollandiae its common name. This project provides a detailed description of this species, with a particular focus on its regenerative capabilities.
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Classification | |
Kingdom
Animalia
Phylum
Annelida
Class
Polychaeta
Subclass
Errantia (Aciculata)
Order
Phyllodocida
Suborder
Phyllodociforma
Family
Phyllodocidae
Subfamily
Phyllodocinae
Genus
Phyllodoce
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Names | |
The accepted name for the Green Paddle Worm is Phyllodoce novaehollandiae (Kinberg, 1866). Other names are Phyllodoce novaeholliandae and Phyllodoce novahollandiae. The parent of this species is Phyllodoce (Lamarck 1818).
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Identification Resources | |
The individuals collected for this study were identified using dichotomous keys found in Pleijel (1991; 1993), and Hutchings & Rainer (1979).
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Physical Description | |
Green Paddle Worms are long, thin, errant polychaetes (Fig. 1). Body coloration ranges from pale yellow to bright green. They have a dark triangular pigment spot on the prostomium and darker intersegmental pigment bands extended mid-dorsally to form an ellipse (Fig. 2) (Hutchings & Rainer, 1979). The body length and number of segments is variable (Pleijel, 1993). The length of individuals collected for this study (n=46) ranged from 9.2 to 16.1 cm, with a mean length of 12.1 cm (±2.02). The length and width of the head were approximately 0.17 cm and 0.12 cm respectively.
The Green Paddle worm has uniramous parapodia (Hutchings & Rainer, 1979). The dorsal cirri are elongate and foliose, resembling paddles (Fig. 3) (Pleijel, 1993). The notopodia of P. novaehollandiae are represented by the dorsal cirri only. The parapodial chaetae (16-20 per parapodium) are compound spinigers with shafts distally spinose and inflated, and have long narrow finely-serrated bases (Hutchings & Rainer, 1979).
The prostomium is heart-shaped, with a nuchal papilla in the posterior incision between the prostomium lobes (Fig. 4) (Hutchings & Rainer, 1979). Two spherical eyes (ocelli) are small pigment cups (Sushenko & Purschke, 2009). The first two segments are fused dorsally, free from the prostomium (Hutchings & Rainer, 1979). The characteristic that distinguishes Green Paddle Worms from all other phyllodocids is that they have four pairs of tentacular cirri on the first segments (Pleijel, 1993). Two pairs of antennae or tentacles are present on the prostomium (Pleijel, 1993). The antennae and tentacular cirri are subulate (Pleijel, 1993). The unarmed pharynx is bulbous proximally with numerous elongated papillae arranged in longitudinal rows (Fig. 5) (Hutchings & Rainer, 1979). The pygidium is simple and has one pair pygidial cirri (Fig. 6).
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| Figure 1 |
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| Figure 2 |
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| Figure 3 |
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| Figure 4 |
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| Figure 5 |
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| Figure 6 |
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Ecology |
Habitat | |
The Green Paddle Worm is a marine errant polychaete that is commonly found on estuarine sand flats, and is often associated with seagrass patches (Pleijel, 1993). The individuals collected for this project were found during low tide on a sand flat on the eastern shore of North Stradbroke Island, Queensland (Fig. 7). The slender body and green coloration of P. novaehollandiae enable it to hide between seagrass leaves to avoid predators (e.g. crabs, fish, birds) and effectively hunt for food (Lee et al., 2004). Anderson (1996) also found that P. novaehollandiae is often found among sedentary polychaetes of the genus Galeolaria, however, these were not observed in the sampling site.
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| Figure 7 |
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Sediment Processing | |
As for many benthic invertebrates, P. novaehollandiae plays an important role in sediment processing, bioturbation and nutrient cycling of estuarine habitats (Queiros et al., 2013). Weimin, Batley & Ahsanullah (1992) used this species to determine the heavy metal composition of sediments in their habitat, with a particular focus on zink, lead, and cadmium.
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Life History and Behaviour |
Asexual Reproduction: Regeneration Experiment | |
Introduction
The ability of polychaetes to regenerate lost structures after non-lethal predation has been described in many occasions across varying species (Bely, 2014). The degree of regenerative capabilities differs between polychaetes, as different evolutionary events led to diverse survival strategies (Bely, 2014). This capability to regenerate lost body parts enables polychaetes to reproduce asexually through fragmentation and fission, and provides an ecological benefit (Lindsay, Jackson & Forest, 2008).
The regenerative ability of a number of species of the family Phyllodocidae have been tested, showing that regeneration of both anterior and posterior ends is possible (Aguado & Helm, 2015; Olive & Moore, 1975; Rohrkasten, 1983). However, no studies have investigated the asexual reproductive capabilities of P. novaehollandiae. This experiment aims to investigate the regenerative capabilities of P. novaehollandiae, testing the ability of this species to regenerate both anterior and posterior ends, when amputated at different lengths along the body.
Methods
Specimen collection
Forty six randomly selected individuals of P. novaehollandiae were collected on a sand flat, during low tide, on the eastern shore of North Stradbroke Island, Queensland. To allow for acclimatization to laboratory conditions all specimens were held in an aquarium for a week prior to the experimental phase.
Amputation & observation
Ten specimens with intact and fully grown anterior and posterior ends were selected for the regeneration experiment. The total length of each worm (at rest) was measured prior to amputation. Using a scalpel, five worms were cut in half and five were cut in quarters. Each new amputated worm (section) was transferred into a petri dish containing 1 cm of fresh sea water. The water in each petri dish was changed daily, and no sediment or food were provided to the animals to make comparison between decerebrate and cerebrate worms possible. Sections were held in separate petri dishes to prevent individuals interacting and possibly damage each other. The thirty sections were held under these conditions for four weeks, and each week sections were inspected for any signs of regeneration using a stereoscopic microscope. When taking photographs, individuals were relaxed using ice or magnesium chloride (MgCl₂).
Results
Week 1&2
One week after amputation all sections had healed their wounds (Fig. 8b). After two weeks, 35% of amputated anterior ends showed signs of a new prostomium developing, as a blastema was visible (Fig. 8c), while 70% of amputated posterior ends had new pygidium and new segments with developing parapodia (Fig. 8d).
Week 3&4
During week three and four 27% of sections have died. After three weeks, 35% of amputated anterior ends still showed signs of regeneration, but with little to no difference to previous observations. All amputated posterior ends that showed regeneration in previous weeks continued to grow their new segments and pygidium.
Overall, sections that grew in week one continued to do so over the four weeks, while sections that did not show any new growth in week one did not show any later on (or have died). In general, there is no significant difference in growth rate between worms that were cut in half and worms that were cut in quarters.
Discussion
The results of this study show that P. novaehollandiae is capable of regenerating both anterior and posterior ends. Figure 8c shows the formation of a mass of proliferating cells, also known as a blastema, which is characteristic of the early phases in the formation of a new prostomium (Bely, 2014; Pfeifer & Dorresteijn, 2012).
The growth rate of the posterior ends was found to be greater than the rate of anterior regeneration. This could be due to the greater complexity of processes involved in the regeneration of an anterior structure (Bely, 2014). During the regeneration of the prostomium, the central nervous system forms from the “old” ventral nerve cord, which gives rise to the brain (cerebral ganglia) (Orrhage & Eibye-Jacobsen, 1997; Pfeifer & Dorresteijn, 2012). This process is much more complex compared to the processes of caudal regeneration, and therefore takes more time to complete (Pfeifer & Dorresteijn, 2012). Lindsay, Jacobson & Forest (2008) demonstrated that the prostomium of a polychaete worm has a slower growth rate when the cerebral ganglia are amputated. Furthermore, the amount of stored nutrients available to each individual section would impact the survival of the organism and the rate at which regeneration occurs (Olive & Moore, 1975).
Understanding the ability of benthic polychaetes is ecologically important, as non-lethal loss of tissues provide a significant energetic input to higher trophic levels of estuarine habitats (Lindsay, Jacobson & Forest, 2008). A longer and more detailed study on the regeneration of P. novaehollandiae is recommended, as it would provide better understanding of the later stages of prostomial regeneration. Testing for differences in regeneration rates in different environmental conditions (e.g. temperature) would also be beneficial.
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| Figure 8 |
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Sexual Reproduction | |
Green paddle worms, as members of the family Phyllodocidae, are gonochoristic (Rouse & Pleijel, 2001). Similar to many other polychaetes, each segment has its own gonads found in the connective tissue. Germ cells are shed into the coelom and growth of the gametes is completed in the coelomic fluid (Rouse & Pleijel, 2006). Gametes are spawned through the metanephridia and fertilisation occurs externally (Rouse & Pleijel, 2006). A large number of P. novaehollandiae were found to aggregate on intertidal flats (Fig. 9), forming reproductive groups composed of multiple males and a single female (Rouse & Pleijel, 2006). Zygotes undergo spiral cleavage and form a trochophore larva typical of the Lophotrochozoa. Member of the family Phyllocidae have shown two types of reproductive strategies: 1) embryos are kept in a gelatinous mass, or 2) fertilized eggs are abandoned in the water column (Wilson, 1991). Although the sexual reproduction of P. novaehollandiae has not been studied, it is thought that this species follows the second strategy (Rouse & Pleijel, 2006).
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| Figure 9 |
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Larval Development | |
Different types of trochophore larvae occur in each of the polychaete families, as some traits have been lost or gained by particular lineages (Lacalli, 1988). The larva of Phyllodocids is a large planktotrophic trochophore (Voronezhskaya & Ivashkin, 2010). The general structure of the Phyllodoce larva is shown in Figure 10. The Phyllodoce larva differs from that of other genera in that it lacks a metatroch (Lacalli, 1988). However, the prototroch is well developed and is thought to compensate for the loss of the metatroch (Voronezhskaya & Ivashkin, 2010). Another unique feature of the Phyllodoce larva is that it has specialized neuromuscular junctions, but lacks neurociliary synapses (Lacalli, 1985), meaning that it has a greater control over muscular movement than over ciliary movement. The limited behavioural capabilities in these larvae is thought to be a consequence of a slow neural development, where the brain (or cerebral ganglion) develops progressively and is most functional only in late larval stages, before metamorphosis (Lacalli, 1985).
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| Figure 10 |
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Behaviour | |
Locomotion
The Green Paddle Worm swims and crawls over surfaces using its well-developed parapodia and chaetae (Pleijel, 1993). The eyes (ocelli) and other sense organs allow for precise movement on the substrate (Sushenko & Purschke, 2009).
Movement of the body is the result of the combined action of the appendages, the body-wall muscles, and the hydrostatic skeleton (coelomic fluid) (Filippova et al., 2010). In predatory polychaetes such as those found in the family Phyllodocidae the longitudinal muscle layer is better developed than the circular muscle layer (Filippova et al., 2010).
During slow crawling the parapodia and chaetae alternatively move pushing against the substrate. The coordinated movement of the numerous parapodia is controlled by neuropodial muscles in each segment (Filippova et al., 2010). At any point in time during locomotion, the parapodia on opposite sides of the same segment are 180 degrees out of phase, to prevent interference between appendages. This creates a wave of parapodial motion that passes from the posterior to the anterior (see Video 1).
During rapid swimming or crawling the same mechanism described above applies, together with lateral body undulations produced by longitudinal muscle contractions (Filippova et al., 2010) (see Video 2). The wave created by this muscle contraction coincides with the parapodial wave, where the parapodial power stroke occurs at the crest of the body wave (Filippova et al., 2010).
Phyllodocids have polyneuronal innervation, where one muscle fibre is innervated by more than one neuron, and the speed and force of muscular contraction depends on the summed effects of all neurons (Filippova et al., 2010).
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Video 1. Movement of parapodia in P. novaehollandiae under a stereoscopic microscope.
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Video 2. Body movement of P. novaehollandiae while crawling and swimming.
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Feeding
Green Paddle Worms crawl and feed at the sediment surface during low tide, avoiding competitors and predators (Lee et al., 2004) (see Video 3). The carnivorous P. novaehollandiae preys upon small invertebrates such as crustaceans, molluscs and segmented worms (Lee et al., 2004). Green Paddle Worms detect food items with their nuchal organ (a chemoreceptive organ) and grasp their prey using their unarmed evertable pharynx (Lee et al., 2004) (see Video 4). The ocelli also aid in the collection of food, as they are used to detect changes in light intensity and direction (Sushenko & Purschke, 2009). Furthermore, all sensory appendages (antennae, tentacular cirri, dorsal and ventral cirri, and pygidial cirri) bear mechanoreceptors and chemoreceptors, which contribute to the predatory success of this species (Lee et al., 2004).
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Video 3. Feeding behaviour of P. novaehollandiae on a sand-flat of North Stradbroke Island, Queensland.
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Video 4. Feeding behaviour of P. novaehollandiae showing the use of the pharynx.
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Defence mechanisms
Mucus secreting cells of P. novaehollandiae are found in the epidermis (Hutchings & Murray, 1984). This mucus protects the surface of the body and is occasionally used as a defence mechanisms against predators or sudden environmental changes (Hutchings & Murray, 1984). During the experimental phase of this study, a significant increase in mucus production was observed when live individuals were held on ice or kept dry.
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Anatomy and Physiology | |
As part of the polychaetes, the internal structures of the trunk of P. novaehollandiae are segmented (Anderson, 1996). Segmental structures include the appendages (parapodia), coelomic cavities, nephridia and gonads (Rouse & Pleijel, 2001; Wilson, 1991). The musculature, nervous system, hemal system, and digestive system are non-segmental, and extend throughout the worm (Anderson, 1996; Voronezhskaya & Ivashkin, 2010).
The body wall of Green Paddle Worms consists of a fibrous collagenous cuticle, a mono-layered epidermis, a connective-tissue, and a muscular layer (Pleijel, 1993). The body has two layers of striated muscles: a circular outer layer and a longitudinal inner layer (Filippova et al., 2010). In each segment, parapodial muscles control the movement of the parapodia (Fig. 11) (Filippova et al., 2010). To the best of my knowledge, the central nervous system has not been studied in the genus Phyllodoce, but is thought to be similar to that of Phyllodocids (Orrhage & Eibye-Jacobsen, 1998; Voronezhskaya & Ivashkin, 2010). The anterior dorsal brain consists of a pair of subpharyngeal ganglia located in the prostomium (Voronezhskaya & Ivashkin, 2010). A pair of ventral longitudinal nerve cords run throughout the body length, and in each segment they bear a pair of joined ganglia (Fig. 11) (Orrhage & Eibye-Jacobsen, 1998; Voronezhskaya & Ivashkin, 2010). Segmental nerves then run from these ganglia to the body wall, where they innervate the musculature and sensory structures of that segment (Orrhage & Eibye-Jacobsen, 1998; Voronezhskaya & Ivashkin, 2010). The escape response of paddle worms is enabled by specialised giant axons in the longitudinal nerve cords (Voronezhskaya & Ivashkin, 2010).
In P. novaehollandiae, each segment has a pair of coelomic cavities, isolated from segment to segment by transverse septa (Anderson, 1996). The left and right cavity are separated by mesenteries (Anderson, 1996) (Fig. 11). The coelomic cavities aid in circulation, together with a well-developed hemal system (Rouse & Pleijel, 2001). The principal blood vessels of polychaetes are found in the mesentery and consist of a dorsal blood vessel (anterior flow) and a ventral blood vessel (posterior flow) (Fig. 11) (Anderson, 1996; Rouse & Pleijel, 2001).
A complete gut extends between the mount and the anus, and is divided into three regions: 1) an ectodermal foregut, which includes a muscular eversible pharynx and a ciliated esophagus, 2) an endodermal midgut, which includes the stomach and the intestine, and 3) an ectodermal hindgut (Anderson, 1996).
Gas exchange occurs across the dorsal body wall, parapodia, and gills (Hutchings & Rainer, 1979). The notopodial cirrus of P. novaehollandiae is flattened and has a ciliated band that functions in gas exchange (branchial lobe) (Anderson, 1996). Parapodial vessels connect these gills to the hemal system (Hutchings & Rainer, 1979).
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| Figure 11 |
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Evolution and Systematics | |
Sveshnikov (1991) discussed that members of the order Phyllodocida evolved following two main morpho-ecological trends: 1) occupation of an ecological niche, and 2) polymerization of the body. Phyllodocids are considered a centre of ecological, genetic and species diversity, as they have representatives of epibionts, intrabionts, planktonic forms, commensals, parasites and interstitial forms (Sveshnikov, 1991). Polymeric forms of the ancestral polychaete Dinophilida are represented by 35% of the species in the orders Phyllodocida and Eunicida (Sveshnikov, 1991). Rousset et al. (2007) further argued that such high diversity is likely to be a result of an “explosive radiation” of annelids during the Cambrian.
Rouse & Fauchald (1997) supported the hypothesis that the order Phyllodocida is monophyletic, however, recent molecular studies of 43 taxa within this group have rejected this hypothesis (Rousset et al., 2007). Rousset et al. (2007) places the Phyllodoce as the sister group of Eteone, Eulalia and Notophyllum, however, this study argued that the sparse sampling of Phyllodoce species (500 species) led to unreliable results for this genus. In contrast, a study on the structure of the central nervous system among genera of Phyllodocidae places Phyllodoce as sister group of Chaetoparia and Notophyllum (Eklof, Pleijel & Sundberg, 2007). Clearly, further studies are needed in order to clarify the phylogeny of species within the order Phyllodocida.
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Biogeographic Distribution | |
Members of the family Phyllodocidae are found in a wide range of habitats, such as estuarine, marine (inshore and shelf), slope (200-2000m), and deep sea (>2000m) (Pleijel, 1993). Phyllodocids are very widespread, as members of this family have been recorded in:
- Australia
- New Zealand
- Northern Europe
- North and South America (Pacific and Atlantic coast)
- Gulf of Mexico
- Northwest Pacific
- South Africa
- Arctic
- Antarctic
- Southeast Asia
P. novaehollandiae has a much more limited distribution, as it is only found in littoral or shallow water habitats of eastern Australia (Fig. 12) (Pleijel, 1993).
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| Figure 12 |
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Conservation and Threats | |
Specific threats to P. novaehollandiae have not been identified. Lewis, Davenport & Kelly (2003) investigated the effects of the removal of macroalgal mats on Phyllodoce maculata. This study showed no significant decline in numbers or significant changes in distribution (Lewis, Davenport & Kelly, 2003). In some cases, this species showed a potential for colonization of cleared sites, where numbers of P. maculate increased in recently cleared sites (Lewis, Davenport & Kelly, 2003). However, the response to such changes may be species specific, hence we cannot assume that P. novaehollandiae would show the same behaviour.
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References | |
Aguado, MT, Helm, C (2015). Description of a new syllid species as a model for evolutionary research of reproduction in annelids. Org. Divers. Evol. 15: 1-21.
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