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Syllis prolifera, Krohn 1852
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Genevieve Panter 2015
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Summary | |
Syllis prolifera (Krohn 1852) is a marine annelid worm [Class: Polychaeta; Order: Phyllodocida; Family: Syllidae; Genus: Syllis] living on the hard substrate in shallow intertidal communities. S. prolifera is omnivorous feeding on a variety of food sources ranging from algae and marine detritous, to diatoms and small marine invertebrates. It has a high tolerance to low pH levels and dessication from intertidal wave action and exposure at low tide. Belonging to the genus Syllis, S. prolifera reproduces sexually via stolonization of the gonochoric adults. S. prolifera can be found living amongst a range of corals, algae, hard substrates and sponges amongst other habitats, and can be found in shallow warm waters around the world.
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Physical Description |
General Morphology | |
Syllis prolifera is an errant Polychaete species within the Family Syllidae, Genus Syllis. The external morphology of Syllis prolifera is very important in identifying it to species level. Like all polychaetes it has a segmented body plan with parapodia; the majority of the body comprising serially repeating segments (metamerism). The body plan features a pre-segmental prostomium (head), a vermiform (grub like) body shape with more than 15 segments (typical of Syllidae), parapodia on each segment, dorsal tentacles on each metameric body segment and a post-metameric-segment pygidium containing the anus (Wilson et al. 2003; Rouse & Pleijel 2001; Fauchald 1977).
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Size | |
Length: 8mm
Width: 1mm
Number of segments: >15
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Prostomium | |
The prostomium (head region) contains at least part of the brain (Rouse & Pleijel 2001), has two pairs of eyes without lenses, three articulated antennae and unarticulated simple palps.
The three antennae include a median antennae situated between the two sets of eyes, and two lateral antennae located near the front of the prostomium, either side of the median antennae, extending out above the palps. Each antennae is a sensory projection, supplied with nerves from the first part of the brain (Fauchald 1977).
Palps are paired, unarticulated (smooth), semi-spherical in shape and separated to their base (Wilson et al. 2003).
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| Figure 1 |
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Eversible Pharynx | |
The eversible pharynx comprises the highly muscular foregut. In Syllids it has no jaws, a smooth surface and a distal ring of papillae (Wilson et al. 2003). The pharynx of all polychaetes within Syllis, including Syllis prolifera, has a single tooth (Fauchald 1977).
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First Segment | |
The pre-segmental peristomium would usually come after the prostomium in polychaetes, however in Syllis prolifera and other Syllids the peristomium is only present in juveniles (Rause & Pleijel 2001). In the adult form the only remnants of the peristomium remain around the mouth (Rause & Pleijel 2001). The first segment after the prostomium in Syllis prolifera has two pairs of anterior tentacular cirri, projecting anteriorly either side of the prostomium (Wilson et al. 2003). Unlike the metameric body segments, the first segment has no parapodia and no dorsal cirri.
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| Figure 2 |
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Metameric Segmentation | |
Each metameric segment comprising the majority of the body has uniramous parapodia where the neuropodium is present and the notopodium is absent (Fauchald 1977; Rause & Pleijel 2003). Parapodia are fleshy, unjointed, segmental appendages used in manipulation of the environment (movement) and as sensors (Fauchald 1997). The neuropodium is the ventral half of the parapodia.
The neuropodium has a small, cylindrical sensory projection called a ventral cirrus on the underside (inferior side). Each neuropodium has approximately six chaetae protruding from the centre, three smooth, hairlike, capillary chaetae and three compound chaetae. Compound chaetae have heterogomph articulation with a distinctly asymmetrical joint, oblique to the length of the shaft (Fauchald 1977).
Situated above the each parapodia is an articulated dorsal cirrus (Wilson et al. 2003; Rause & Pleijel 2001; Hutchings 1984). Dorsal cirri form a pattern, with dorsal cirri on segments 2,4,6,8 etc. directed dorso-laterally and dorsal cirri on segments 3,5,7,9 etc. directed laterally (Rause & Pleijel 2001).
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| Figure 3 |
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| Figure 4 |
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Pygidium | |
The pygidium is the last section of the body. It is post-segmental, differing from the metameric segments along the rest of the body length (Fauchald 1977). As the terminal segment it contains the anus and is also the growth zone, with growth of the pygidium forming new metameric segments (Rause & Pleijel 2001). The pygidium also has two flattened, articulated dorsal cirri, which do not move, and a pair of uniramous parapodia.
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| Figure 5 |
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Colour Pattern | |
Syllis prolifera is transparent with purple dotted lines crossing the body left to right in the middle of each segment and between each segment. Dorsal tentacles are also covered in fine purple dots, visible under a powerful dissecting microscope.
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| Figure 6 |
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Ecology |
Habitat | |
Syllids are free-living, common shallow-water forms, most numerous on hard substrates (Fauchald 1977).
Cinar (2003) described most Syllidae as living on the surface of the seabed, associated with “rocks, algae, spermatophytes, sponges, hydroids, corals and tunicates”. S. prolifera has been found inhabiting the outer surfaces and canals of sponges, corals, bare rock, large bivalves and rocky substrates with algal coverage (Cinar 2003).
S. prolifera is found in high densities in intertidal marine communities (Serrano et al. 2006), where the wave exposure, thermal conditions, nutrient concentrations and shallow depths require polychaete species such as S. prolifera to have a high endurance to dessication. As a continuously reproducing species it may have an advantage towards a high colonisation success in shallow intertidal depths, as it has a high regeneration rate (Serrano et al. 2006). This may function as an opportunistic feature, as S. prolifera abundance on hard substrata has been found to increase with increasing environmental stress (Giangrande et al. 2005).
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Diet | |
Omnivorous
Species of Syllidae are carnivorous, preferably feeding on colonial and other small invertebrates (Fauchald and Jumars 1979). All species within Syllis have long been considered carnivores (Fauchald & Jumars 1979), using the tooth on their pharynx to latch onto prey and suck out contents (Rause & Pleijel 2001). S. prolifera, however, is suggested to be omnivorous (Giangrande et al. 2000). Supporting omnivory in S. prolifera is a study by Casu et al. (2009), finding the diet of S. prolifera to contain diatoms, algae and sedimentary organic matter (detritus), evidencing detritivorous and herbivorous feeding strategies.
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Life History and Behaviour | |
REPRODUCTION STRATEGIES AND BEHAVIOUR
All Syllids are gonochoric (separate sexes: male and female).
S. prolifera reproduces sexually via stolonization (schizogamy) epitoky, swarming and external fertilisation (Franke 1999). The resultant metatrochophore larvae develops into a juvenile, then into an adult. This process of sexual reproduction, whilst primitive, is extremely complex and allows the adult to survive reproduction, recover and reproduce again.
Epitoky via stolonization:
Individuals undergo epitokous metamorphosis where their morphology, physiology and behaviour are notably modified.
1st – The adult (atokous form) sexually matures
2nd – Sexually mature adult metamorphoses at the pygidium to form an attached sexual stage – the stolon (Epitokous form)
3rd – pygidium with anus reforms on the adult form whilst attached to the head of the stolon
4th – Stolon (epitoke) breaks away from atokous adult form
5th – Stolon (epitoke) swims into the pelagic zone, swarming with other stolons.
6th – Swarming stolons broadcast spawn their gametes in the surface waters where fertilisation occurs
7th – Fertilised eggs sink to the substrate and hatch within 24-48hrs
8th – Fertilised eggs hatch as metatrochophore larvae and begin crawling through the adult habitat
9th – metatrochophore larvae develop into adults (atokous form)
Dicerous stolons as found in S. prolifera lack a mouth and pharynx and their gut wastes away. They have a stolonial head with large cerebral ocelli (eyes) connected to a stolonial brain, and have masses of sexual gametes to spawn. Their musculature is designed to allow fast swimming when swarming and broadcast spawning (Franke 1999). Each adult produces stolons of the same sex i.e. a female produces a female stolon, with eggs; a male produces a male stolon, with sperm.
Timing of Reproduction:
Optimal timing of reproduction is based on the annual cycle, the lunar cycle, the day cycle, the tidal cycle, chemical signalling and hormones.
Annual Cycle – a combination of day length (photoperiod) and water temperature.
Water temperature must be a minimum of ~13oC for sexual reproduction to occur.
Most important of the two is day length (photoperiod). Photoperiods of 12-13hr light per day indicate seasonality of spring and summer. The minimum water temperature is likely to be reached during these seasons. If the photoperiod is less than 12-13hrs per day, reproduction will not occur.
Lunar Cycle – suggested to affect sexual development of adults and swarming of stolons in surface waters.
Sexual development begins a few days before the new moon. Sexual development takes approximately 2 weeks to complete, resulting in a mass release of stolons, days before the full moon. This results in the mass swarming of stolons in surface waters around the time of the full moon. Experiments have found the reproductive cycle to be linked to the lunar cycle.
Day Cycle - S. prolifera stolon swarming occurs in the morning, shortly after sunrise in response to photic stimulation. Neither swarming nor spawning occur in darkness.
Tidal Cycle – Swarming always occurs at high or low tide when there is the least turbulence.
Chemical signalling – Broadcast spawning synchronisation within populations increases the rate of fertilisation and is controlled by chemical signalling – the use of pheromones.
Males spawn regardless of the presence of females, whereas females require the presence of spawning males in order to spawn. It is suggested by Franke (1999) that female spawning is in response to a pheromone released from the sperm duct glands with the male sperm.
Hormones – The biological process of sexual reproduction is an endocrine two-step-system, incorporating two hormones: prostomial hormone and proventricular hormone.
Proventricular hormone blocks sexual development. Prostomial hormone induces sexual development by inhibiting the production or release of the proventricular hormone.
General life length:
In lab studies, some S. prolifera individuals reproduced 15 times before dying.
Stolons have very short lives once separated from the atokous adult form. Stolons are designed to reach the surface waters, swarm and broadcast sperm, shortly after which they die.
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| Figure 7 |
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Evolution and Systematics |
Classification | |
Kingdom: Animalia
Phylum: Annelida
Class: Polychaeta
Subclass: Errantia
Order: Phyllodocida
Suborder: Nereidiformia
Family: Syllidae
Subfamily: Syllinae
Genus: Syllis
Species: Syllis prolifera
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Synonomy | |
The division of polychaete species into phylogenetic Families and Genera has been a highly disputed science, with many species being grouped multiple times based on different select features in common (Fauchald 1977). With gene sequencing, accurately identifying sister taxa has become a lot easier in recent years (Aguado et al. 2012). S. prolifera (Krohn 1852) is the accepted name for this species, however it has many names synonymous with it.
According to the World Register of Marine Species (WoRMS) they are:
Gnathosyllis zonata (Haswell, 1886)
Pionosyllis prolifera (Krohn, 1852)
Syllis (Typosyllis) bouvieri (Gravier, 1900)
Syllis (Typosyllis) prolifera (Krohn, 1852)
Syllis (Typosyllis) zonata (Haswell, 1833)
Syllis armandi (Claparede, 1864)
Syllis bouvieri (Gravier, 1900)
Syllis fiumensis (Ehlers, 1864)
Syllis fluminensis (Ehlers, 1864)
Syllis lussinensis (Grube, 1863)
Syllis nigrans (Bobretzky, 1870)
Syllis zonata (Haswell, 1833)
Typosyllis (Syllis) nigrans (Bobretzky, 1870)
Typosyllis (Syllis) prolifera (Krohn, 1852)
Typosyllis (Typosyllis) prolifera (Krohn, 1852)
Typosyllis bouvieri (Gravier, 1900)
Typosyllis nigrans (Bobretzky, 1870)
Typosyllis prolifera (Krohn, 1852)
Typosyllis zonata (Haswell, 1833)
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Evolution | |
Phylogeny
Both Syllinae and Syllis are monophyletic groups. In both instances the common ancestor to the group is unknown.
All species within Syllinae reproduce via schizogamy, derived secondarily through a common monophyletic ancestor to the group (Aguado et al. 2012). Schizogamy within Syllidae evolved secondarily twice. Once within Autolytinae and once for all of Syllinae. The primitive state of sexual reproduction in Syllidae is epigamy (Aguado et al. 2012).
A rapid evolution of the family Syllidae has been proposed by Aguado et al. (2012), in keeping with rapid evolutions in other polychaete families.
Five different forms of stolon have evolved within Syllinae. Differences in stolon type might define different monophyletic groups. S. prolifera belongs to a clade with dicerous stolons (Aguado et al. 2012). Dicerous stolons as found in S. prolifera lack a mouth and pharynx and their gut wastes away. They have a stolonial head with large cerebral ocelli (eyes) connected to a stolonial brain, and have masses of sexual gametes to spawn. Their musculature is designed to allow fast swimming when swarming and broadcast spawning (Franke 1999).
Polychaete Evolutionary Features
Parapodia: Parapodia are fleshy, unjointed segmental appendages in polychaetes, not found in other classes of Annelida (Fauchald 1977). Parapodia assist in movement through the water and around the marine environment. In Syllis prolifera this movement involves navigating the hard substrate of the intertidal zone.
Chaetae: Unlike other annelids in which chaetae occur across the epidermis, in polychaetes the chaetae occur in clustered bundles within, and protruding from, parapodia. Chaetae evolved in polychaetes from the ectoderm. Ectodermal cells migrated to a clustered ventral position during development, where bundled filaments and lateral cells formed the structure of each chaetae. Chitin provides the strength and stiffness of each chaetae (Fauchald 1977).
Syllidae Evolutionary Features
Proventricle: the highly muscular inner pharynx is a synapomorphy of Syllidae species.
Dorsal cirri with regular alternation pattern: is a synapomorphy of Syllidae species.
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Biogeographic Distribution | |
Syllids are found in seas all over the world, especially on coral reefs, in warm waters, and at shelf depths (Rause & Pleijel 2001).
S. prolifera is found in shallow, intertidal, benthic marine communities with temperatures between 15oC-25oC, in Australia, the Mediterranean Sea and Africa.
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Conservation and Threats | |
Status: Not Threatened
Polychaetes, with their diverse modes of feeding, have important roles in marine benthic communities; detritivores turning over sediment and recycling nutrients whilst carnivores control population growth of prey species. Polychaetes are highly dense on marine benthic substrates and have been used as indicators of species richness and community patterns in response to environmental disturbance on soft-bottom substrates for years. It has been suggested by Giangrande et al. (2005) that certain polychaete species be used as indicators of effects of habitat disturbance on rocky-bottom substrates as well.
One of these tolerant polychaete species suggested as an “indicator species” is S. prolifera. S. prolifera has been found to increase in abundance with increased stress from factors such as pollution (Giangrande et al. 2005). S. prolifera populations were found to decrease from large amounts of sediment caused by a Power Station. It is possible that this decrease in population size was due to interference of reproduction in S. prolifera. The sexual reproduction of S. prolifera depends strongly on linked elements such as photoperiod, turbulence level and lunar cycle (Franke 1999). Increased turbidity from the Power Station and altered photoperiods from increased sedimentation would signal poor conditions, preventing sexual reproduction.
Industrialisation of coastal areas near reefs and rocky substrates puts S. prolifera populations at risk of declining, with the potential to be removed from the habitat entirely. The small size (8mm long) of S. prolifera means the worm has low motility on a macrohabitat scale and as such would require microhabitats to take refuge in during harsh conditions such as increased sedimentation (Serrano et al. 2006). Increased sediment is damaging to these habitats (Giangrande et al. 2005), and declining or disappearing S. prolifera populations would signify a significant disturbance to the habitat that may not be reconcilable. However, the abundance and large biogeographic range of S. prolifera means it is unlikely as a species to become threatened with extinction by small-scale events of disturbance.
Another potential threat to invertebrates in shallow depths is ocean acidification. CO2 in the atmosphere has significantly increased since the industrial revolution and partial pressure of CO2 at ocean surfaces is predicted to increase significantly within this century (Ricevuto et al. 2014). This is predicted to increase ocean surface water acidity by reduced pH of 0.4 U. Whilst ocean acidification is likely to affect many marine invertebrates including plankton, S. prolifera is unlikely to be directly negatively impacted as it has a high tolerance to very low and variable pH (Ricevuto et al. 2014)
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References | |
Aguado, M.T., Martin, G.S., & Siddall, M.E. 2012. “Systematics and evolution of syllids (Annelida, Syllidae)”. Cladistics, vol. 28, pp. 234-250.
Bartolomaeus, T. & Purschke, G. 2005. “Morphology, Molecules, Evolution and Phylogeny in Polychaeta and Related Taxa”. Springer
Cinar, M.E. 2003. “Ecological features of Syllidae (Polychaeta) from shallow-water benthic environments of the Aegean Sea, eastern Mediterranean”. Journal of the Marine Biological Association of the United Kingdom, vol. 83, pp. 737-745.
Fauchald, K. 1977. “The Polychaete Worms: Definitions and Keys to the Orders, Families and Genera”. Natural History Museum of Los Angeles County, Science Series, vol. 28, pp. 1-190
Fauchald, K. & Jumars, P. 1979. “The diet of worms: a study of Polychaete feeding guilds”. Oceanography Marine Biology Annual Review, vol. 17, pp. 193–284.
Franke, H.D. 1999. “Reproduction of the Syllidae (Annelida: Polychaeta)”. Hydrobiologia, vol. 402, pp. 39-55.
Giangrande, A., Licciano, M., & Pagliara, P. 2000. “The diversity of diets in Syllidae (Annelida: Polychaeta)”. Cah Biology Marine, vol. 41, pp. 55–65.
Giangrande, A., Licciano, M. & Musco, L. 2005. “Polychaetes as environmental indicators revisited”. Marine Pollution Bulletin, vol. 50, pp. 1153-1162.
Ricevuto, E., Kroeker, K.J., Ferrigno, R., Micheli, F. & Gambi, M.C. 2014. “Spatio-temporal variability of polychaete colonization at volcanic CO2 vents indicates high tolerance to ocean acidification”. Marine Biology, vol. 161, pp. 2909-2919.
Rouse, G.W. & Pleijel, F. 2001. “Polychaete”. Oxford University Press
Serrano, A., San Martin, G., & Lopez, E. 2006. “Ecology of Syllidae (Annelida: Polychaeta) from shallow rocky environments in the Cantabrian Sea (South Bay of Biscay)”. Scientia Marina, vol. 70, pp. 225-235.
Wilson, R.S., Hutchings, P.A., & Glasby, C.J. 2003. “Polychaete Interactive Identification Guide”. DVD
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