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Pectenodoris trilineata (Adams & Reeve, 1850)
Three-lined Pectenodoris


Mizuki Uemura 2015

Summary

Three-lined Pectenodoris, Pectenodoris trilineata, is a small species of nudibranch and a member of the coral reef community of tropical and subtropical waters (1). They can be found in depths ranging from 8m to 23m and their northern-most distribution is South China Sea and their southern-most limit is Heron Island, Australia (2). The body of the animal is violet and outlined in white, and has three characteristic longitudinal white with yellow stripes running down the mantle (3). Due to the loss of an external gastropod shell, like many other nudibranchs, P. trilineata evolved defensive mantle glands which secrete toxic mucous (4). They are closely associated with their sponge prey, Dysidea sp. which they feed upon and transform its compounds to be used as defensive secretion. Their colour groups present on the body suggest that they use Müllerian mimicry as a defense against visually guided predators (2). Pectenodoris trilineata belong to the monophyletic family Chromodorididae, and their evolutionary history is entirely recreated through phylogenetic evidence due to the lack of fossil records (5). 

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Pectenodoris trilineata (Adams & Reeve, 1850)
Photo taken by Mizuki Uemura at University of Queensland, St. Lucia.


Even though nudibranchs exhibit simple behaviours and lifestyle, they have a very sophisticated sensory system. One P. trilineata specimen was found in the coral rubble collected from the north crest of Heron Island and was sectioned to investigate and analyse their internal anatomy, with a particular focus on sensory structures.

Physical Description
Size

The specimen observed from the coral rubble collected from Heron Island Reef was 3.1mm long. Adults reach an average length of 7mm to 8mm with a maximum length of 11mm (6). 


Colouration

The mantle and foot are violet in colour with a pink tinge towards the centre of the animal (3). The mantle is outlined in white (3) and consists of three longitudinal white stripes which can vary in different specimens (7) (Fig. 1). The middle line is the broadest and longest, and has a thin yellow line running down the centre (6). The middle line starts from in front of the rhinophores to the branchial pocket at the posterior, where it splits to surround or partially surround the branchial pocket (7). The lateral lines are shorter and can be completely absent in some specimens (6). The rhinophore stalks are violet with white and orange coloured clubs. The naked gills have a similar colour sequence, with a violet base, white mid-region and orange tip (7). 

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Figure 1: "Pectenodoris trilineata. Showing colour variation in a group of specimens from Heron Is, Queensland. The three white dorsal lines are variable and in some cases the outer pair can be completely absent" (7).


External morphology

The body shape is elongate to broadly oval and the tail extends past the posterior margin of the mantle (3). The head has a pair of rhinophores which are lamellate in structure (Fig. 2) (8). The rosette of branched gills is simple and surrounds the anus which opens posteriorly (8). A unique characteristic of the genus Pectenodoris lies within the mantle, where there are a series of large sub-epidermal mantle glands which open ventrally (7). 

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Figure 2: Illustration of a rhinophore that has a lamellate structure, as seen in Pectenodoris trilineata (8).

Ecology
This P. trilineata specimen was found in the coral rubble collected from the crest on the north side of Heron Island Reef.  Pectenodoris trilineata are primarily found in tropical and subtropical waters (1). They are a common species and are always closely associated with their prey species the blue sponge, Dysidea sp. (1). These sponges are usually found in indentations on the underside of coral slabs or rubble (6). Up to five individuals have been recorded to be found buried in a single sponge and “presumably the animals never leave this microhabitat throughout their entire lives” (6). There are very few records of nudibranch predators possibly due to their toxic mucous secretion from their defensive mantle glands and aposematic colouration (6). 

Life History and Behaviour
Life history

Like all other organisms on earth, life of a nudibranch is tightly correlated to the cycles of abundance of their foods. The lifespan of P. trilineata is not known however, nudibranchs that feed on prey that are prevalent, slow-growing and present all year round such as sponges, live for approximately a year (8, 6). Since the lifespan of nudibranchs are relatively short, once they reach sexual maturity, they have limited time to find a partner and sexually reproduce (4). 


Feeding

Nudibranchs can detect chemical compounds given off by prey organisms using their oral palps and rhinophores, which trigger a feeding stimulus (4, 9).  Like most molluscs, nudibranchs possess a unique feeding structure called the radula which is used to grind and ingest their food (6). This organ consists of a chitinous ribbon with numerous, minute teeth on its upper surface. Nudibranchs that graze on sponges, such as P. trilineata, replace their radula ribbon frequently via conveyer belt system, i.e. new teeth continuously replace the old front teeth that have been eroded (6). 


Respiration

The ‘naked’ dorsal gills at the posterior end of the animal, is responsible for the extraction of oxygen from the surrounding sea water (9). When the animal is threatened, the delicate external gills are capable of quickly retracting inside the protective branchial pockets (4, 6), as seen in Figure 3.

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Figure 3: On the left is a photograph of Pectenodoris trilineata when the gills were retracted inside the branchial pocket. On the right is when the gills were relaxed and expanded. Photo taken by Mizuki Uemura at University of Queensland, St. Lucia.  


Locomotion 

Nudibranchs crawl across the substrate on their flat and flexible foot which is positioned right underneath the mantle. “The foot comprises two muscular bands: a thick, encircling outer band that is constantly in contact with the substrate and a sole, which is an elongate inner strip of tissue” (4). The outer muscular band is chiefly used to grab and cling onto uneven surfaces (4). Crawling is made possible by the secretion of a viscous layer of mucous from specialised mantle glands and the beating of cilia (4). The coordinated transverse wave motion produced by muscular contraction moves backwards, i.e. in the opposite direction to which the nudibranch is moving (10). Young nudibranch’s movement is primarily driven by the beating cilia along the base of the foot (10). 
Pectenodoris trilineata locomotion
Video taken by Mizuki Uemura at University of Queensland, St. Lucia.

 
Reproduction 

Nudibranchs are simultaneous hermaphrodites therefore, they possess both male and female reproductive organs. Copulation is mutual, so both individuals donate and store the partner’s sperm packet (8). The genital opening is found on the right side of their neck and mating is achieved when the individuals face in opposite directions with their right sides in close proximity (8). When the genital papillae of each individual’s touch, the penis enters the partner’s female duct (4). Sperm then travels to the receptaculum seminis which is a temporary storage organ (4). From there, the sperm fertilises the egg in the hermaphroditic duct (4).

The fertilised egg is sent to the female gland mass which has similar functions to an ovary/uterus and undergoes a series of stages:
  1. A nutritive layer is added to the egg inside the albumen gland
  2. An outer layer of the egg is then laid out in the membrane gland
  3. The numerous eggs are adhered together into a ribbon in the mucous gland (4)
The egg ribbon is deposited in an anticlockwise circle (Fig.4) from the oviduct located on the animal’s right side. Since the oviduct is on the right side of the body, laying eggs in this direction is the most effective in making a neat spiral shape (4).  The egg ribbon is usually laid directly on the prey species, or on a prominent object nearby (8). Hermaphroditism can be an advantage since any sexually mature conspecific they encounter is a potential partner, which means they can increase the likelihood of fertilisation and fecundity (8). 

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Figure 4: A photograph of Pectenodoris trilineata laying its egg ribbon in a counter-clockwise direction. Photo taken by Rory Ferguson at Perhentian Islands, Malaysia (9).


Development

Nudibranchs have planktotrophic development, therefore the eggs hatch as minute larvae (known as veliger) that drift in the plankton to feed (Fig. 5) (11, 6). The digestive gland produces extra-cellular enzymes which aid in cellular ingestion of food particles during the larval stages (12). The larva will only settle and metamorphose into an adult once it achieves metamorphic competence and only in the presence of its particular prey species; in the case of P. trilineata, it would be the Dysidea sp. sponge (8). Living in the plankton comes at a cost, since the larvae are exposed to predators in the open ocean for extensive periods which results in low survival rates. Therefore, to sustain viable populations, each individual lays a large batch of eggs (4). Due to the short lifespan of nudibranchs, the time taken to grow can be exceedingly rapid, especially in warmer waters (6). 


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Figure 5: “Left: free-swimming veliger larva of a nudibranch. Note shell and operculum, and absence of eyes and radula. Scale bar = 0.05mm (after Williams 1980). Right: crawling larva of a nudibranch immediately after settlement and metamorphosis. Scale bar = 0.1mm (after Rivest 1978)” (7).


Anti-predator behaviour

Over evolutionary time, nudibranchs have lost their external shell, a unique feature of gastropods. To compensate for this, they have evolved various sophisticated defense mechanisms and behaviours against predators (4). A common strategy used by animals is aposematic colouration and/or distinct body patterns to advertise that they are toxic to visually guided predators. This form of anti-predator defence is more likely to be learned and memorised by predators for longer (13). Although P. trilineata is small and usually well hidden in crevices, the colour groups of P. trilineata are thought to represent Müllerian mimicry, a strategy used as a defense against predation (5). Chromodorididae transform, concentrate and incorporate diterpenoids and other metabolites obtained from their sponge diet into their mantle glands in the skin to produce toxic mucous (14, 5). 

Anatomy and Physiology
One specimen of P. trilineata was found during the investigation of cryptic coral reef communities in the coral rubble from Heron Island Reef. The specimen was fixed and relaxed using magnesium chloride; this ensured that the gills and rhinophores were not retracted and in their “natural” state. The specimen was then preserved in 70% ethanol and sent off to the histology lab to be sectioned longitudinally along the frontal plane. The slides were stained using haemtoxylin and eosin (H&E). 

The research project was based around the internal anatomy of the animal, with a particular focus on the sensory system. There has been minimal research done on the sensory system structures in Chromodorididae especially on the species P. trilineata, therefore it is interesting and potentially useful to understand their neurological anatomy. 


Digestive system

The oral tube as seen in Figure 6 is approximately four times the length of the buccal bulb (7). In Pectenodoris, the radular ribbon, jaw plates and jaw rodlets are very small and delicate structures (2). “Morphology of the teeth is unique within the Chromodorididae. There is a small chitinous plate in the midline and the first lateral on each side of the midline is a wide vertical plate with a recurved flange bearing 11 or 12 sharply pointed denticles” (Fig. 7) (7). The salivary gland contains two main parts: the proximal part, which has a globular shape and the distal part which connects to the oesophagous and formed by numerous glandular cells (15). The stomach epithelium is loosely folded and the folding becomes deeper as it approaches the intestine (15). The kidney connects to the pericardium via piriform syrinx and its thin epithelium is highly vacuolated (15). The anus can be found next to the nephroproct and has a highly convoluted and ciliated epithelium (15).
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Figure 6: "Pectenodoris trilineata; dissection showing arrangement of viscera and mantle glands; A, foregut (oral partly distorted in fixation); B, reproductive system" (7). 



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Figure 7: "Pectenodoris trilineata; scanning electron micrographs of radula; A, complete half-row on left side of radula; B, central region, with reduced median teeth; C, Teeth 1-3 (left); D, Teeth 3-7 (left); Scale = 10μm in all cases" (7). 


Reproductive system

The reproductive organs of nudibranchs are situated on the right hand side of the organism. The unique features of P. trilineata “reproductive system (Fig. 8) are the extremely narrow vaginal duct and the large and sausage-like exogenous sperm sac which open together at the end of the duct” (7). The specimen used for the histology sections was smaller than a half of the usual adult size, which is 7-8mm long. However, the male gonad and ciliated syrinx were identified (Fig. 9D) but no sperm was detected. This suggests that the reproductive organs were developed but the specimen could have been sexually immature. The prostate and mucous gland covers a large portion of the body, as seen in Figure 9E. Johnson & Gosliner (1998) described the prostate to narrow towards the ejaculatory portion and terminate at the long and narrow muscular penial bulb. The mucous gland comprises a large area since it is an essential organ for producing the gelatinous mass used to bond the numerous eggs together into a ribbon (4). 

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Figure 8: "Pectenodoris trilineata (Adams and Reeve, 1850), reproductive system. Abbreviations: am = ampulla, bc = bursa copulatrix, ej = ejaculatory portion of vas deferens, fg = female gland mass, p = penis, pr = prostate, rs = receptaculum seminis, u = uterine duct, v = vagina, vg = vestibular gland" (2).


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Sensory system
 

Nudibranch eyes as seen in Figure 9B, is simply a pigment spot deeply imbedded within the head tissue (4), located directly laterally from the cerebropleural ganglia (15). The melanin at the inner face of the retina appears as small dark spots (Fig. 9B) (15). The primitive eyes are connected to the simple long optic nerve which sends messages to the optic ganglia (9). Their primitive eyes are incapable of forming images or distinguishing colours however, there is evidence that they are light-sensitive (4). A pair of large nerves connects the rhinophores to the brain and the nerve endings contain two cell types (4). One type is the dendritic cells which is responsible for chemical reception (4). The second type is the “ciliated cells which function as mechanoreceptors and used to detect vibrations or changes in pressure waves” in the surrounding ocean (4). Statocysts which are situated between the cerebropleural and pedal ganglia (15), function as gravitational or hydrostatic sensors, which help the animal to interpret spatial orientation (4). The rhinophores detect chemical compounds in the environment and oral tentacles which is primarily used to provide a sense of touch, can also have a similar function (4). The rhinophores as seen in Figure 9A, is densely packed with blood vessels which appear as dark purple dots. 

The central nervous system (CNS) is located where the pharynx and the anterior region of the oesophagous meet, and forms a circumoesophageal ring (15). 
Nudibranchs have multiple types of ganglia: 
  • The buccal ganglia which is very small in size is positioned underneath the buccal mass
  • A pair of small, pedunculate rhinophoral ganglia are located where the rhinophores emerge 
  • The cerebral and pleural ganglia are fused together to form the cerebropleural ganglia, which is the largest part of the CNS (Fig. 10). 
  • The pedal ganglia is located beneath the cerebropleural ganglia and the oesophagous (Fig. 9C)
  • The optic ganglia is connected to the simple eyes via the optic nerve (15)
The perineurium (Fig. 10) which functions as a protective sheath surrounding the ganglia, are formed from fibroblasts and some dispersed muscle cells (15). The cerebropleural connective tissue is responsible for connecting the hemispheres of the cerebropleural ganglia together (Fig. 10). The cerebropleural ganglia consists of “four categories of nerve cell bodies on the basis of their size: giant, large, medium-sized and small” (15). In the P. trilineata histology sections, the small and medium-sized neurons were detected in both the cerebropleural ganglia and pedal ganglia (Fig. 9C and 10). 

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Respiratory system

The gills located in the posterior region of the animal were richly innervated with neurons and blood vessels which appear as large and small dark purple spots, respectively (Fig. 9F). Pink retractor muscle fibres were found embedded in each gill which allows the animal to retract its gills into the branchial pocket. Schrödl & Wägele (2001) described the gill epithelium to be flat and ciliated.


Defense system

The series of large single defensive mantle glands of P. trilineata open ventrally along the mantle and was seen regularly in numerous histology slides (Fig. 9A) (7). Pectenodoris trilineata generally have 1-3 greatly enlarged posterior mantle glands which may vary within the species, shown in Figure 11 (2). Small glandular follicles were present in the ciliated foot epithelium (Fig. 9G) but they are used for secreting the mucous trail to aid in crawling.


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Figure 11: "Pectenodoris trilineata (Adams & Reeve, 1850), distribution of mantle glands" (2). 

Evolution and Systematics
Doridoidea express numerous anatomical and physiological adaptations which suggest that they have an intricate evolutionary history. However, Doridoidea lack a fossil record, thus there is limited information on “their evolutionary history, origin, possible extinction events, and time and causes of major radiations” (5). This means that the evolution of Doridoidea can only be hypothesised based on phylogenetic evidence (5). In nearly all the molecular analyses conducted by Turner & Wilson (2007), P. trilineata was consistently formed in a well-supported clade with the Indo-Pacific species of Mexichromis, supporting that they have a sister group relationship. This information provides further evidence that P. trilineata derived from Chromodorididae, and supports no close relationship with Chromodoris or Noumea (16).

Pectenodoris trilineata belongs to the monophyletic family Chromodorididae, which has a sister group relationship with Actinocyclidae (Fig. 12) (1). There is growing interest in the “exploration of Chromodorididae ecology, natural products chemistry, colour pattern evolution and natural history however there is not a complete, well-supported phylogeny of the chromodorid nudibranchs” (1). Human error including false identification of the species in ecological and chemical studies can result in misleading conclusions (1). Pectenodoris trilineata shares 97% of identical sites in molecular data with Pectenodoris aurora therefore, P. aurora is the closest living relative (17).

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Figure 12: "Preliminary hypothesis of the phylogenetic relationships of the Doridina, based on a compilation of several published phylogenetic analyses" (5). 

Biogeographic Distribution
Pectenodoris trilineata are distributed around the tropical western margins of the Pacific, and is limited northerly by the Tropic of Cancer and southerly by the Tropic of Capricorn (2). The northern-most limit of P. trilineata distribution is the South China Sea and the southern-most limit is Heron Island, Queensland (Fig. 13) (2). The species is almost entirely confined to the intertidal zone on the outer edge of windward reefs (6). They are usually found in depths ranging from 8m to 23m (2) however, it is rare to find specimens in the subtidal zone (up to 20m) (6). 


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Figure 13: The known biogeographic distribution of Pectenodoris trilineata, represented by a red dashed line (18).

Conservation and Threats
Pectenodoris trilineata are a common species (11) and not listed as threatened. However, obvious threats to this species could be from human impact such as waste water discharge via ocean outfalls and storm water runoff from the mainland (19). Water pollution may have direct impact on P. trilineata or Dysidea sp. sponge, or “indirect effects on either one of them through effects on other members of the ecosystem” (19). Coastal pollution has been known to obstruct pelagic larval dispersal in the common non-harvested seastar larvae (19), which could potentially have similar effects upon P. trilineata veliger larvae. Their lengthy development period as a plankton in the open ocean alongside their high fecundity rate gives them an opportunity for wide geographic dispersal, which is a distinct advantage in survival of the species. However, planktotrophic development can come with a few disadvantages, including increased likelihood of experiencing adverse environmental conditions and the constant struggle of finding suitable prey, which could potentially cause a population to collapse (4).

References
  1. Johnson, R & Gosliner, T 2012, ‘Traditional taxonomic groupings mask evolutionary history: a molecular phylogeny and new clasification of the chromodorid nudibranchs’, PLoS ONE, vol. 7, no. 4, pp. 1-15.
  2. Johnson, R & Gosliner, T 1998, ‘The genus Pectenodoris (Nudibranchia: Chromodorididae) from the Indo-Pacific, with the description of a new species’, Proceedings of the California Academy of Sciences, vol. 50, no. 12, pp. 295-306.
  3. Yonow, N, 2001, ‘Results of the Rumphius Biohistorical Expedition to Ambon (1990). Part 11. Doridacea of the families Chromodorididae and Hexabranchidae (Mollusca, Gastropoda, Opisthobranchia,Nudibranchia), including additional Moluccan material’, Zoologische Mededelingen, vol. 75, pp. 1-50.
  4. Behrens, D 2005, Nudibranch behavior, New World Publications Inc. Florida.
  5. Valdes, A 2004, ‘Phylogeography and phyloecology of dorid nudibranchs (Mollusca, Gastropoda’, Biological Journal of the Linnean Society, vol. 83, pp. 551-559.
  6. Willan, R & Coleman, N 1984, Nudibranchs of Australasia, Neville Coleman's AMPI, Springwood.
  7. Rudman, W 1984, ‘The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera’,  Zoological Journal of the Linnean Society, vol. 81, pp. 115-273.
  8. Picton, B & Morrow, C 1994, A field guide to the nudibranchs of the British Isles, Immel Publishing Ltd.. London.
  9. Coleman, N 2008, Nudibranchs encyclopedia: catalogue of Asia/Indo-Pacific sea slugs, Neville Coleman's Underwater Geographic.
  10. Coleman, N 2001, 1001 Nudibranchs - catalogue of Indo-Pacific sea slugs, Neville Coleman's Underwater Geographic Pty Ltd.
  11. Coleman, N 1989, Nudibranchs of the South Pacific. 
  12. Thompson, T 1959, ‘Feeding in nudibranch larvae’,  Journal of the Marine Biological Association of the United Kingdom, vol. 38, pp. 239-248.
  13. Cheney, KL, Cortesi, F, How, MJ, Wilson, NG, Blomberg, SP, Winters, AE, Umanzor, S & Marshall, NJ 2014, ‘Conspicuous visual signals do not coevolve with increased body size in marine sea slugs’,  Journal of Evolutionary Biology, vol. 27, pp. 676-687.
  14. Cimino, G, De Rosa, S, De Stefano, S, Sodano, G & Villani, G 1983, ‘Dorid nudibranch elaborates its own chemical defense’, Science, vol. 219, no. 4589, pp. 1237-1238.
  15. Fischer, M, Velde, G & Roubos, E 2006, ‘Morphology, anatomy and histology of Doto uva Marcus, 1955 (Opisthobranchia: Nudibranchia) from the Chilean coast’, Contributions to Zoology, vol. 75, no. 3/4, pp. 145-159.
  16. Turner, L & Wilson, N 2007, ‘Polyphyly across oceans: a molecular phylogeny of the Chromodorididae (Mollusca, Nudibranchia)’,  Zoologica Scripta, vol. 37, no. 1, pp. 23-42.
  17. Ortigosa, D & Valdes, A 2012, ‘A new species of Felimare (formerly Mexichromis) (Gastropoda: Opisthobranchia: Chromodorididae) from the Yucatan Peninsula, Mexico’, The Nautilus, vol. 126, no.3, pp. 98-104.
  18. U.S. Central Intelligence Agency, 2013, Perry-Castañeda Library, viewed 28 May 2015, <http://www.lib.utexas.edu/maps/world_maps/world_physical_2013.pdf>
  19. Goddard, J, Schaefer, M, Hoover, C & Valdes, A 2013, ‘Regional extinction of a conspicuous dorid nudibranch (Mollusca: Gastropoda) in California’,  Marine Biology, vol. 160, pp. 1497-1510.
  20. Schrödl, M & Wägele, H 2001, ‘Anatomy and histology of Corambe lucea Marcus, 1959 (Gastropoda, Nudibranchia, Doridoidea), with a discussion of the systematic position of Corambidae’, Organisms Diversity & Evolution, vol. 1, pp. 3-16.