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Spurilla braziliana (MacFarland, 1909)
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Saoirse Hannam 2019
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Summary | |
Nudibranchia, a mollusc within the subclass Opisthobranchia of the Gastropoda, are a speciose order that span the globe in intriguing and often attractive body forms. Fondly referred to as butterflies of the ocean (Wollscheid-Lengeling, 2001), their shell-less beauplan manifest in varied colours dependent on their ecology and feeding habitat. The animals are restricted to marine ecosystems, ranging from the depths of the ocean benthos to intertidal coastal habitats (Dominguez, 2008). Nudibranchs generally exploit sessile invertebrates such as cnidaria or sponges, which over time has allowed them to evolve certain abilities to aid these close relations (Greenwood, 2009). Members of the Aeolidida clade (or aeolid), for example, utilise cnidarian nematocysts by incorporating them for protection into their own body (Greenwood, 2009).
Most evidently, nudibranchs are recognised by their loss of a calcareous shell which is replaced by a soft colourful body. In the described species, Spurilla braziliana, I present an animal that feeds exclusively on sea anemones of intertidal habitats and breathes through multiple outgrowths of its body. These outgrowths are characteristic of Aeolidina, a suborder within Nudibranchia, and have much influence on their evolution and success. Much of the work on Spurilla spp. relates to the type species Spurilla neapolitana (e.g. Conklin & Mariscal, 1977; Schlesinger et al., 2009), providing a plethora of information related, but not always specific, to S. braziliana.
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Physical Description | |
Size and Colouration
As with most aeolid nudibranchs, S. braziliana exhibits an appearance that draws attention to its sprawling respiratory appendages. Bifurcated, paired cerata line the elongate body in a mass along the dorsal surface to reveal a mid-dorsal streak (Fig. 1). Ranging in colour from a deep-red to a light pink or orange (Fig. 2), the mid-dorsal streak extends from the anterior to the lower-mid-region of the animal where the cerata merge together (Fig. 1). Stalked rhinophores that extend from the head region reflect this pink or deep red colouration of the dorsal streak, but at their base are transparent (Fig. 3). The thin membrane of epidermis that tightens around the bulbous heart is generally clear or light grey, dotted by white pigments (Fig. 4). The cerata are lined with opaque cnidosacs (see Feeding and Defence) and white pigmented spots cover the entirety of the body (Fig. 5). A translucent, angular foot extends posteriorly beneath the tangle of cerata (Fig. 5).
External Morphology
The wide, elongate body plan of S. braziliana is characteristic of aeolid individuals, of which are recognised by the mass of crowded cerata atop their dorsal surface (Miller, 2001). Despite the crowded appearance, the long parallel projections are evenly spaced and taper together gradually as they approach the tail end (Fig. 1, 5B). These many cerata are cylindrical in form, longer than the rhinophores in mature adults and display tips that curve over the body (Fig. 5C). A muscular foot hides beneath the visceral mass of the body, but at its anterior protrudes as short and angled (Fig. 5B). S. braziliana exhibits the characteristic transverse lamellae along their short rhinophores (Fig. 3), which are present in all Spurilla species (Nimbs et al., 2016). Nudibranch vision is restricted to photosensitive acuity, made apparent by the two black dotted ocelli positioned directly behind the rhinophores (Fig. 3). Pointed oral tentacles protrude from the cephalic region immediately above the ventral surface and laterally of the animal. These were reduced in our specimen, suggesting a young adult yet to grow to sexual maturity. Perhaps most captivating of S. braziliana, however, is the prominent swelling of the pericardial region that sits in the upper region of the body between the parallel lines of cerata (Fig. 4) Positioning of the anus in Spurilla is cleioproctic, thereby indicating its location as dorsally situated, towards the right, anterior end of the body (Fig. 6). The reproductive opening is situated above it, beneath the first quarter of cerata (Dominguez, 2008).
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Ecology | |
Feeding and Defence
Aeolids, and thus by nomenclature S. braziliana, are carnivorous predators that prey primarily on Anthazoa (Greenwood & Mariscal, 1984; Carmona et al., 2013). Due to their restricted diets, aeolids are classified as stenophagous (Todd et al., 2001), making them susceptible to population disturbance dependent on prey abundance (Schlesinger et al., 2009). Their chemosensory rhinophores function to detect anthazoan organisms (Garese, 2013). Many specimens of aeolid nudibranchs have been observed to demonstrate aggressive tendencies in response to their stinging prey (Zack, 1974).
The ability to ingest and store toxic nematocyst is a key point of interest within Opisthobranchia (e.g. Grosvenor, 1904; Edmunds, 1966; Greenwood & Garrity, 1991; Greenwood, 2009). Cnidocyst storage protects individuals from feeding predators such as generalist fish (Marin, 2009), and replaces the protective function of the calcareous shell that is otherwise present in most members of Mollusca.
The structural makeup within the cerata (singular: ceras) include a terminal cnidosac and digestive diverticula, both separated by a thin layered sphincter (Fig. 6) (Conklin & Mariscal, 1977). Sensory cilia exist at the tip of each ceras. Once parts of a cnidarian victim are ingested, the associated cnidocyst cells (nematocysts, in all cases) eventuate through the diverticula (Greenwood, 2009). The diverticulata transport nematocysts into the cocooned cnidosac (Fig. 6). Given this defence mechanism, aeolid nudibranchs have had to evolve additional resilience processes that aid to limit harmful contact with nematocysts. A chitinous, cuticular lining of the gut – particularly the buccal cavity and oesophagus – prevents physical penetration of discharged nematocysts (Martin, 2003) and composite to this, protective chitinous epithelia cells of the skin and stomach form a protective lining to assist in feeding (Martin & Walther, 2002). These epithelia cells have been referred to as “sandbags” (Greenwood, 2009), regarding their ability to absorb fired nematocysts, and thus prevent damage to underlying muscle and basal lamina. Mucous is secreted upon contact with prey, aiding to protect the nudibranch predator when nematocysts are fired. During attack, the cnidosacs extrude the nematocyst cells out of a cnidopore to prevent harm by the potential predator. Field work indicates that retention of larger nematocysts is prevalent due to their more potent affects (Thompson and Bennett, 1969). Thus, scientists have concluded that this exceptional defensive strategy has been a critical one in the success of aeolid organisms (Greenwood, 2009).
Locomotion
A muscularised foot lining the ventral underside of the body allows S. braziliana to creep along the rocky shore benthos. Highly evolved, the foot adheres to boulders of rock, coral or similar such substratum, allowing the thick outer band of the foot to maintain constant contact (Behrens et al., 2005). The inner sole produces muscular contractions in waves that glide the animal forward and specialised glands secrete mucous for both adheration and protection from the substratum. Movement is slow, aided in part by a fine layer of cilia homologous with smaller opisthobranchs. Flexions of muscles allow momentary floating, but generally S. braziliana is observed crawling along a benthic structure.
Slow progressive movement of S. braziliana across a petri dish. Heart can be seen pumping posterior to the head region.
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Life History and Behaviour | |
Behaviour
Very little investigation has been made into the behaviour of S. braziliana, proving it difficult to describe. In the lab, the collected specimen was observed to have a relatively delayed response to a stimulant or probing. When a response was observed, however, it would generally contract its cerata and body into a ball-like structure, becoming less visible as its size decreased. Unfortunately, however, the collected specimen vanished during the building of this page, and thus little more observations were made.
Feeding behaviour of the type species S. neapolitana, however, has been studied (Conklin & Mariscal, 1977). Thus, the below describes what is known about Spurilla, and is intended for general understanding, rather than species-specific description.
S. neapolitana individuals were observed to approach food, contact it initially and then withdraw upon touch, followed by a final re-approach and then feed (Conklin & Mariscal, 1977). At initial touch, ceras were observed to flare, supposedly in response to the stinging cnidocysts. Specimens of the genus Spurilla have been observed to demonstrate aggressive tendencies in response to their stinging prey (Zack, 1974). After initial shock, the animal secreted mucous, thus enabling it to crawl over the prey structure to commence feeding. Once the nudibranch was full, it was observed to rest in place until the following day (Conklin & Mariscal, 1977).
Natural History
Like all nudibranchs, organisms of S. braziliana experience semalparity, reproducing only once in their life time before dying soon after (Todd, 1991). Although their hermaphroditic biology allows flexible internal fertilisation and copulation of one another, these animals have developed specialisations to negate the possibility of self-fertilisation. Experimentation as to what these may be is yet to be explored. At spawning, coiled eggs attach to a benthic substrate in a sticky ribbon-like mass (Schlesinger et al., 2009)(Fig. 7), allowing upwards of 10,000 eggs to develop into planktotrophic larvae.
Much of the life history of Spurilla is based on the well-studied type species, S. neapolitana. Fortunately, the life-cycle stages ascertained for this species have been observed in a variety of aeolids, and thus I concur that whilst remarks presented here about life cycles are general, they are the most accurate at present regarding the genus Spurilla. The major life stages noted are development via the following indirect stages: (1) embryonic, (2) planktonic (planktotrophic), (3) metamorphic, (4) juvenile and (5) adult (Schlesinger et al., 2009). Planktrophic veliger larvae exhibit the characteristic mollusc shell, operculum and mantle cavity for about 45 days before reaching metamorphic competency (Schlesinger et al., 2009). As planktotrophs, photosensitive eye spots have developed to form ocelli (Fig. 8).
Metamorphosis of the trophic specialist S. braziliana is induced by chemical exogeneous cues associated exclusively with Anthazoa (Hadfield and Switzer-Dunlap 1984). Schlesinger et al. (2009) observed that S. neapolitana had a variable metamorphic success rate dependent on food availability, indicating that species rigor was unstable and highly dependent on diet-specific metabolites. Thus, for successful settlement to occur, it is critical for the planktonic larvae to identify and establish in an area relative to their food-source (Hadfield and Switzer-Dunlap 1984). As metamorphosing juveniles increase in size, so too does consumption of their anemone prey, which, after appearance of initially short rhinophores, enables transition into adult stage. The shell is lost, and beneath it a light orange epidermis is exposed, which over time will develop to full colour.
For the next 60 days, young adults will feed and grow on their anemone prey to develop as mature and sexually reproductive adults (Schlesinger et al., 2009). Once copulation, fertilisation and laying of the fertilised eggs is achieved, the animals experience senescence associated with oviposition, which soon after is followed by demise.
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Anatomy and Physiology | |
Detorsion and general beauplan evolution
The evolutionary loss of the shell and mantle cavity has enabled nudibranchs to diverge significantly from the ancestral gastropod form. Detorsion simply means that the primitive twisted gastropod beauplan has been reversed in the more evolved opisthobranchs. So, unlike typical gastropod members, S. braziliana, along with most other nudibranch lineages, has reverted to an internal bilateral body plan. Thus, the organelles of the body are located posterior to the head to form the mantle (homologous with the ancestral mantle cavity), alongside the anus and gonoduct openings. This is why, in S. braziliana, both the anus and the reproductive pores are always on the right side of the body. Furthermore, the secondary gills represented by the cerata, evolved as a consequence of ancestral body deformation. Such detorsion occurs throughout the metamorphosis stage, whereby the initial spiral veliger shell, mantle cavity and propodium is lost in S. braziliana.
Digestive System
The feeding organs of S. braziliana comprises a buccal mass housing a jaw, odontopore, radula (and its associated musculature) and sharp, curved teeth (Miller, 2001). Digestion begins by rasping and grating of the prey by the penctinate (narrow protrusions) radula. These teeth become gradually smaller to fit the radula’s posterior region (Fig. 9) and the rasping action enforces damage by the chitinous teeth. The protactor and retractor muscles work together to drive the radula, before ingestion of the cnidarian and its nematocysts occurs. Nematocysts are transported by diverticula located within ceras structures (Fig. 6). For further information on ingestion of nematocysts, see Feeding and Defence. Atypical to most nudibranchs, salivary glands are absent within S. braziliana, with little understanding towards why this may be (Garese, 2013). The protected lined oesophogus transports nutrients into the mantle cavity and stomach, where digestive glands distribute them into organelles and cerata for uptake (Garese, 2013).
Circulation and Respiration Systems
The blood-filled hemocoel comprises the kidney, pericardial sac and the ovotestis (both male and female reproductive organs) (Rudman, 1974)(Fig. 11). In addition to providing transport of gas, nutrient and waste products, the body cavity acts as a semi-rigid hydrostatic skeleton. Sets of muscles are synergistically contracted and relaxed, altering the body shape in response to surrounding conditions and pressures.
The open circulatory system of nudibranchs functions via pumping of a two-chambered heart, immediately visible on the mid-dorsal streak (see video). Translucent hemolymph is oxygenated by both atriums into the cerata and flows through to the hemocoel body cavity. This strategy allows complete saturation of the tissues and organs to improve efficiency of nutrient and oxygen uptake, which in turn enables these high-energy animals to feed and function as elusive predators. The provided video demonstrates the captivating pumping action of S. braziliana, which can be noted upon first inspection.
Pumping movemement of S. braziliana. A thin membrane of epidermis reveals the translucent haemolymph.
Reproductive System
As hermaphrodites, individuals fertilise each other through the vaginal opening, ventral to the penal gland. In all members, the cleioproctic reproductive pore is located anteriorly, on the right side of the body (Fig. 12). The diaulic biology means that copulating pairs participate in an intercourse position coined ‘sidling’ (Zack, 1975), describing the apposition of the bodies. A swelling of the gonopore occurs before penis eversion and subsequent fertilisation (Schlesinger et al., 2009). Erection of the cerata initiates separation of the animals seconds after insemination.
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Biogeographic Distribution | |
Local Habitat
S. braziliana are most often found in intertidal rocky shore communities. The pictured specimen was found in the Moreton Bay region of Australia, in a sand patch at low tide (26.6797° S, 153.1385° E). Finding the organism in sand is unusual of its ecology, and I suspect this to be due to tide disturbance, rather than the selective specificity of the animal. The Moreton Bay region, whilst a zone of the Great Barrier Reef, is more southern than the tropical region, indicating the temperate climatic preference of the species. An increase in observations have been noted along the New South Wales and Victorian coastlines (Bridle, 2017), indicating migration of the species as sea temperatures gradually increase. In association with their sea anemone prey, S. braziliana individuals are often spotted hiding behind rocks in shadowed crevices of intertidal and sub-tidal pools.
Global Distribution
Venturing further from Australian shores, these novel species have a broad global distribution, with first identification in Alagoas, Brazil (MacFarland, 1909). Today, several observations have been recorded in both Northern and Southern hemispheres, notably in Florida, Columbia, Cuba, Mexico (Carmona et al., 2014), Jamaica, Puerto Rico (Miloslavich et al., 2010), the Caribbean Sea (Valdes et al., 2006) and extending into the Pacific Ocean, Japan (Hamatani, 2000), China (Lin, 1992), Australia (Willan, 2006; Bridle, 2017) and Hawaii (Kay, 1979). Intriguingly, their distributions are highly distinct from one another, leading researchers to believe that recent dispersal throughout the Pacific is probably a result of human-mediated transport (Gosliner, 1980).
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Evolution and Systematics | |
Phylogeny case study: the cryptic species complex of Spurilla.
S. braziliana belongs to the Aeolidiidae family, one of the largest nudibranch families within the clade Aeolidida. Aeolid nudibranchs are recognised by their pectinate radular teeth, and their tapering elongated bodies (Miller, 2001). The definition of the monophyletic genus Spurilla, however is considerably more ambiguous. This is because features that exist in Spurilla appear in multiple members of Aeolidiidae, posing a challenge when it comes to genus description. The most robust of these characteristics is the synapomorphic perfoliate, lamellate rhinophores that extend from the cephalic region. Generally, Spurilla have curved or arched cerata, but this feature alone cannot be used to assertively distinguish the genus.
The taxonomic status of S. braziliana within Spurilla has been studied to identify their relation to the type species, S. neapolitana (Carmona et al., 2013). Extremely similar in anatomical and morphological features, molecular studies have instead sought to differentiate the two based on mitochondrial and nuclear genes (Carmona, 2013; Carmona, 2014). Consisting of four cryptic species, Spurilla is a monophyletic genus with various synapomorphies, both molecular and morphological. When analysed, all four species are distinctly different in genetic make-up, however due to the chromatic variability of the type species, S. braziliana has previously been incorrectly identified as a junior synonym of S. neapolitana (Hadfield et al., 1984). This is unsurprising given that the two species are the most similar in appearance. Fortunately, we now know that S. braziliana is the only member of its genus present in the Pacific Ocean (Carmona et al., 2014), and therefore we can confidently conclude that organisms fitting its physical description in Australia are likely a member of the species.
Classification and Systematics
Phylum: Mollusca (Linnaeus, 1758)
Class: Gastropoda (Cuvier, 1795)
Subclass: Heterobranchia (Gray, 1840)
Infraclass: Opisthobranchia (Milne-Edwards, 1848)
Order: Nudibranchia (Blainville, 1814)
Suborder: Aeolidina (Odhner, 1934)
Family: Aeolidiidae (Gray, 1827)
Genus: Spurilla (bergh, 1864)
Species: Spurilla braziliana (MacFarland, 1909)
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Conservation and Threats | |
Due to the elusive nature of nudibranchs, individuals of the order are generally difficult to quantify for population analysis. For this reason, population and abundance numbers of S. braziliana are unknown and have, to date, not been investigated. Our only evidence of population increase is an increased number of sighting reports. Carmona et al. (2013) speculated that the distinct Pacific localisation of S. braziliana is probably due to recent human-mediated introduction. Evidence to support this is the genetic homogeneity of Pacific specimens, whereas those in northern regions are generally more chromatic in diversity. Thus, their recent establishment in Pacific environments suggests suitability to the environmental climate with no immediate evidence of threat.
Aeolid sea slugs, however, can be a reliable indicator of environmental variation due to their fleeting life cycles and specialised diet preferences. Such aspects of their ecology expose them to environmental pressures from climate change, which potentially could cause population decline. The southward spread observed in Australian nudibranch specimens (Carmona et al., 2013; Nimbs et al., 2016) suggests such a trend may occur as sea temperatures continue to rise, forcing organisms to seek cooler climates.
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References | |
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