The bases of the physical description of periwinkles are often related with the spiral univalve shell shape. As gastropods, they can withdraw they body inside the calcareous shell produced by glands in the mantle. The gastropod’s shells have a specific shape with can be used for identification and cladistics studies (BRUSCA & BRUSCA, 2002). The Littorinidae family is known for own large, thin shells with variable coloration and sometimes brightly (REID, 1986).

The body has bilateral symmetry and is divided in head, visceral mass (inside the shell) and foot used of locomotion, Figure 1, which is the most easy viewed soft part of a gastropod (RUPPERT et al., 2004).

The L. filosa basic bauplan as well as a gastropod, is defined for an anterior part, the head, the visceral mass that stays inside the shell and a big muscular foot, used in the movement of these animals (BRUSCA & BRUSCA, 2002).

Sclerotized cuticle, single layer epidermis and muscles are the three layers of the body of a gastropod. The water loss is a constant problem for these animals as they do not have a specialized cuticle to avoid it but they may withdraw inside their shells to prevent water loss. Terrestrial species also have to spend with mucus that facilitate the water wasted (BRUSCA & BRUSCA, 2002). The dorsal body is surrounded by the mantle, where are located the shell glands, responsible for the shell secretion. There is an invagination of the visceral mass that forms with the shell, the mantle cavity, where is located the gills, the anus, nephridiopores and gonopores (RUPPERT et al., 2004).

Figure 1. Representation of the gastropod basic bauplan. Illustration by Gustavo
 Zoppello Toffoli, 2015 with reference to (BRUSCA & BRUSCA, 2002).

The color of the head and the foot of the gastropods are used for taxonomical propose too. In Littoraria species, the color of the body are linked with the polymorphic color of the shells, as described by Reid (1986):

“For example, in Littoraria filosa the animals with pure yellow shells are entirely unpigmented, in darker shells animal pigmentation becomes more pronounced, especially on the head, until animals are dark grey in brown shells”

In L. filosa the peculiar feeding structure of the gastropods is pink colored and is called radula, located in the head as well as the sensory structures that composed by a pair of eyes in the base of a pair of tentacles Figure 1 (REID, 1986). The operculum is the structure used for close the animal inside of the shell when it is windrowed. This structure is used for prevent desiccation and as a shield against predators. The operculum in L. filosa is thin and paucispiral and very similar to the other species from the genus Littoraria (REID, 1986).

Shell Morphology                                           

             Gastropods are univalve animals and their shells can vary in size from microscopic to more than 40 cm in some species. The distinctive characteristic of the group is the conical spiral around the axis called columella that forms the spire divided in whorls by the sutures that are the lines where the whorls attach to the others (BRUSCA & BRUSCA, 2002). The body whorl is in the base of the shell and is where the aperture is located which is used for body retraction or extension by action of the columellar muscle (RUPPERT et al., 2004). See Figure 1:

The shell in periwinkles are constituted from outside to inside by a thin organic periostracum, two or three prismatic layers that differs in their composition but are all caucareous and the nacreous layer made of calcareous and conchin lamellas as the Figure 2 shows (BRUSCA & BRUSCA, 2002).

Is important to remember that the shell is produced by addiction of organic or inorganic elements and the different material deposition in the inner and in the outer layers is responsible for the spiral formation and it is metabolic expansive requiring substantial sources of the ambient (RUPPERT et al., 2004). Although for example, calcium carbonate is common abundant in mangrove environment even in high tidal levels (REID, 1986)

The color varies according to the periostracum pigments or by pigments in the caucareous layers. The origin of the pigments may be related with the diet or may be synthetized by the gastropod. This pigment addiction can be related with cryptic behaviors (RUPPERT et al., 2004).

In Littoraria genus are mainly associated with mangrove habitats, the shape of the shells are apparently uniform despite some variations, and there are some evidences that the planktonic dispersal behavior is responsible for this combined characteristic. L. filosa has a thin, dextral shell (clockwise spiraled).

As a supralittoral specie, L. filosa has a thin, light shell, which might be for decrease the risk of dislodgment, as they stay attached in the leaves just by the action of the mucus. Another hypothesis about the thickness of the shell may be related with predators in low levels which selecting individuals for thicker shells, letting the individuals with less thicker shells occupy high levels (REID, 1986). The character of a supralittoral specie that occupy high leaves may be influencing in the size of the shell. Without wave action, the shells can be bigger and will not be washed out from the leaves, also, the higher tolerance of larger individuals against physical conditions as suggested by Vermeij, 1973b in Reid (1986). The more narrowed shape of the shell may be influenced by an allometric result of the increase of the size (REID, 1986).

Works with L. filosa has shown that in breeding periods, the shell growth ceases, the apertural lip is flared and thickened, and after the growth continued, it is possible to be seen in some adult individuals (REID, 1986). However, this flared characteristic is not seen in all adult individuals what may be, according to Sewel (1924) cited by Reid, 1986, related to the habit of occupying high tidal levels as the breeding period occurs at the same time of high rainfalls and temperatures what may interfere in the growing rates. Then, the flaring and thickening of the outer lip of the aperture may not be related with breeding periods.

The sexual dimorphism is not very apparent and is variable. Despite the fact that females have apparently larger shells, and males have lower spire height (REID, 1986).

Despite the not useful characteristics of the protoconch (first whorl) that is smooth and from the second whorl (protoconch 2) for taxonomy, is important to remember that the protoconch is secreted by planktonic larvae and due to the protection of the mangrove habitat, this first whorl can be found even in adult individuals (REID, 1986).

The shell sculpture in Littoraria is the most useful and important taxonomic characteristic, used for distinguish the diverse species as is possible to see in the diagnosis part. However, some species cannot be distinguished by shell characteristics needing the verification of the geographical range (REID, 1986). Due to the high intertidal preferred position in outer mangrove trees, the control of the body temperature in L. filosa is very important. Its shell is strong sculpted, a characteristic that can improve the loss of temperature by increasing the superficial area (REID, 1986).

L.filosa lives on the high foliage of mangroves trees and is considered one of the most polymorphic Littoraria species. The different colour patterns can be found on the same tree. In Avicennia marina (the preferred tree of L. filosa), the color varies from light ground color, yellow and orange pink which defines the variation spectrum of the colors (REID, 1986).

Many studies about the polymorphism of the shell color are already done and some thermal regulations evidences are found by Reid (1987) and Parsonage & Hughes (2001). Despite the suppositions relating this characteristic with crypsis selection by birds (JOHANNESSON & EKENDAHL, 2001) and at lower levels of the trunks by crabs (REID, 1986), the main factor ruling the polymorphism in L. filosa is the parasitoid fly Sarcophaga megafilosia as reported by (MCKILLUP & MCKILLUP, 2002 and 2007).

Photo: Some examples of shell polymorphism in L. filosa. Gustavo Zoppello Toffoli, Wellington Point - Queensland, 2015 
 

The diagnosis of Littoraria filosa as postulated by Reid, 1986:

     "Shell: thin; columella narrow, rounded; primary grooves 5-7(9), spacing markedly unequal, increasing anteriorly; last whorl with 9-11 strong, narrow carinae, the spaces between with numerous irregularly spaced spiral grooves; colour highly polymorphic, brown, yellow or orange pink, with or without pattern of brown dashes aligned at suture to form short stripes, numbering 10-12 on last whorl. Animal: penis bifurcate, filament large, narrowing only at tip; ovoviviparous."

Key to Shells

According to the key for shell identification proposed by Reid, 1986 L. filosa is identified by the following charachteristics:

1          Columella narrow, rounded, not excavated    .           .           .           .           .           2

-           Columella excavated or flattened, usually wide         .           .           .           .           8

2          Sculpture of 9-11 narrow carinae on last whorl; colour polymorphic             L. filosa

-           Sculpture of low or rounded ribs, or numerous fine riblets    .           .           .           3

Adapted to a terrestrial life, L. filosa has as its preferred substrate, the leaves of the grey mangrove Avicennia marina where the group achieve the greatest diversity and abundance (REID, 1986). However, it shares the habitat with other littorinids, each specie specialized for a specific height level related with the tide inundation and rain that have been showed as the most important factors influencing the zonation of these periwinkles. (REID, 1986).

The pattern of distribution through the mangrove tree species appears to be related with the preferred height, some leaf dwelling species as L. filosa, L. luteola and L. albicans  are described as more frequent on the leaves of A. marina whereas some other species that prefer to live on the trunks or on the roots are more dispersed (REID, 1986). In relation to the horizontal zonation a pattern has been noticed by the authors that Littorinids occurs in all the mangrove forest but they begin to be scarce far away from the sea edge (REID, 1986) and L. filosa is less abundant in more wave-exposed mangrove areas (REID, 1985).


Photo: L. filosa can be found in various locations in a tree. They can be found alone or in patches. Gustavo Zoppello Toffoli, Wellington Point - Queensland, 2015

The main tree periwinkles’ predators are birds and crabs. The crab predation decrease with the height, then, for the high level tree L. filosa, this kind of predation is just important when the females are releasing the larvaes and in dry conditions when the periwinkles goes down to obtain moisture. The birds may cause more damage as they usually search for food flying. However, the L. filosa use to graze on the underside of the leaves what difficult the detection for the flying predators.

Researches have been shown that the principal predator of L. filosa is the parasitoid fly Sarcophaga megafilosia as reported by (MCKILLUP & MCKILLUP, 2002 and 2007). The polymorphic characteristic of the shell have been used for avoid the deposition of larvaes near from the snail by the female flies that will occasionally kill the periwinkle (MCKILLUP & MCKILLUP, 2002)

         From the Littorinidae family, periwinkles are found in the intertidal habitat as rocky shores, mangroves and saltmarshes all around the world. L. filosa is a high-level tree-obligate periwinkle adapted to a terrestrial life able to live up to 3 meters above ground (Avicennia zone, Magnetic Island, Queensland) that climbs to avoid submersion during the high tides (REID, 1986). Mostly found on Avicennia marina (grey mangrove) leaves (Photo) and sometimes trunk (REID, 1986; RUPPERT et al., 2004).

Photo: A. marina mangrove habitat. Gustavo Zoppello Toffoli, Wellington Point - Queensland, 2015

The snails stays in high levels even in low tides just descending to the water to get moisture or in order to release the larvaes. As an adaptation to the semi-terrestrial habit, L. filosa developed an ovoviviparous characteristic. The female maintain the embryos between the gills and when they are developed, she goes down to the water and release the veliger larvaes. The horizontal mobility is restricted to trees with branches in contact due to the inability of these periwinkles to move on mud as described by Reid (1986).

Depending on the weather conditions, periwinkles may face some dry conditions, which makes them withdraw inside the shell and staying attached to the leaves by action of the mucus (REID, 1986), while the entire animal is inside the shell, closed by the operculum.

The L. filosa is a leaf dwelling specie that feed on the underside of A. marina leaves, scraping the leaf hairs seldom opening holes through the leaves (REID, 1986). For some species that lives on other mangrove tree species, the hairs from underside of A. marina leaves may not be the main food source, however, L. filosa practically is not found grazing on other mangrove tree species, then, probably the A. marina leaves hair is probably an important source of food for this specie.

As described by many authors before Reid (1986), the copulation only occurs in moisture conditions. The behavior of L. filosa is the same as described of other Littorinids where the males look for females attaching to any other individual as they are only able to verify the sex by trying to insert the penis into the bursa cupulatrix.

Intraspecific mating occurs without evidences of hybrids individulas. In the case of a meeting of males, they rapidly separates. The male lean to the anterior right side of the female body and inserts the penis into the aperture, the act is short but the male remains attached for several hours (REID, 1986).

The Body Features

As gastropods, L. filosa are coelomate animals, but in their body, the coelom can just be found as a vestige structure surround the heart and part of the intestine as the pericardial chamber and the perivisceral coelom respectively whereas the main chamber consist of several cavities composing an open circulatory system (BRUSCA & BRUSCA, 2002).

            An important feature of the periwinkle bauplan is the planispiral coiling of their body inside the shell, forming whorls that are positioned outside of the antecessor whorl. Although no live gastropod has a planispiral shel, instead of that, their shell varies in more than one plan of an asymmetric whorl formation  (RUPPERT et al., 2004).

            These animals must deal with a heavy structure attached in their dorsum, the shell. Due to the planispiral shape, the center of gravity of the body is taken upwards what makes difficult to maintain the shell erect (RUPPERT et al., 2004). The asymmetrical conispiral shape of the shell solved this problem. Instead the shell grow upwards, it grows dislocated from the body axis, repositioning the center of gravity (Figure 1) and facilitating the movement of the animal (RUPPERT et al., 2004).

Figure 1. Representation of the evolution of the asymmetry in gastropod shells. Vision from above. Illustration by Gustavo Zoppello Toffoli, 2015 based on Ruppert et al. 2004.

            A notable step in the gastropod development that is also one of the synapomorphies of the modern groups is the phenomenon called torsion. A remarkable twist of 180° counterclockwise (that occurs during the late veliger larval development without change the head and foot positions. The visceral mass is twisted changing the right/left side of structures when compared the larvae with the adult. The torsion of the gut let it with a U-shape and the nerves are also twisted. In the end of the process the gills, nephriopores, hypobranchial glands, osphradia and the anus are now posterior positioned as is possible to see in the Figure 2 (RUPPERT et al., 2004; BRUSCA & BRUSCA, 2002).

Figure 2. Causes of the torsion in gastropods body. (left - hypothetical untorted ancestral; right -
gastropod after torsion. Illustrated by Gustavo Zoppello Toffoli, 2015 based on Ruppert et al. 2004.

Some theories have been used to justify this torsion as that the posterior position of the mantle cavity may improve ventilation, the posterior position of the osphradium allow the animal to verify the ambient before rather than after entering in the water. However, the twist, put the anus and nephriopores in a position close to the mouth and head what caused a sanitation issue that interfere with the gills/lung ventilation, some specializations evolved to deal with this problem (RUPPERT et al., 2004).

Foot

            The foot is a muscular structure responsible for the movement of the gastropods that can be related with feeding, prey capture, reproduction and in females, molding of the eggs. It is linked by the columellar muscle that is responsible for extension and retraction of the foot. In the sole, there are the tarsos muscles directly responsible for the locomotion (RUPPERT et al., 2004).

 
Photo: The bottom part of a L. filosa, is possible to see the large muscular foot. Gustavo Zoppello Toffoli, Wellington Point - Queensland, 2015

           
Movement

            The sole is broad and flat, properly for movement in diverse substrates. There are glands that secretes mucus that facilitate the attachment and locomotion The snail can chemically change consistence of the mucus from sticky gel to liquid depending on the need (RUPPERT et al., 2004). The L. filosa as a tree living snail, is considered a hard bottom terrestrial gastropod that uses waves of the tarsos muscles to move on the leaves and trunks (RUPPERT et al., 2004). The direction of the movement of the sole muscles varies depending on the species, it can be in direct waves, retrograde waves or bipedal when the left and the right side of the foot alternate the direction of the waves (BRUSCA & BRUSCA, 2002).

Radula

Radula is the unique mollusk structure used for feeding. Is constituted by a band of recurved chitinous teeth. Associated with strong muscles, the radula projects from the pharynx (BRUSCA & BRUSCA, 2002) and is used for L. filosa snails scrape the surfaces of the leaves where they feed (REID, 1986). The radula is an important feature for cladistics and may be the characteristic that supports some groups (BRUSCA & BRUSCA, 2002).

The description of the L. filosa radula is wrote as “length to 17 mm, saw-toothed type, central rachidian cusp elongate and pointed, cusps of paired teeth equilaterally triangular and the lateral with slight gap aterior to main cusp”, by Reid (1986).

 Gut

Periwinkles have complete guts and their digestion is mainly extracellular. The mouth is located inside of a buccal cavity where the radula apparatus leads. Some glands releases saliva and enzymes into the anterior gut. The esophagus connect the foregut to the stomach that will end in the digestive ceca where the absorption and the intracellular digestion occurs. The intestine links the stomach region to the anus located in the mantle cavity (BRUSCA & BRUSCA, 2002; RUPPERT et al., 2004). See Figure 1:

Figure 1. Digestive system of a land snail. Illustred by Gustavo Zoppello Toffoli, 2015 modified of Brusca & Brusca, 2002.




Photo: Faeces of L. filosa indicated by the narrows. (fresh in the right image and dry in the left image). Gustavo Zoppello Toffoli, Wellington Point - Queensland, 2015

As L. filosa is more terrestrial but still an amphibious species, their nitrogenate excreta may be mainly ureotelic instead of ammonotelic. The kidneys of the gastropods consists in tubular metanephrids like the annelids as Figure 1 shows (BRUSCA & BRUSCA, 2002). Due to the torsion, the nephridiopore is located in the mantle cavity near from the anus (RUPPERT et al., 2004).

Figure 1. Metanephridium structures. Illustrated by Gustavo Zoppello Toffoli, 2012, adapted
of Hickman et al. 2004.

L. filosa cannot avoid losing water, but in dry periods they can decrease the metabolic rate and withdraw inside their shell and close the operculum keeping attached to the leaf until good water source conditions (RUPPERT et al., 2004).

            The gas exchange occurs through modified gills, surface of the mantle cavity and the body surface (BRUSCA & BRUSCA, 2002). The coelom of the body of gastropods is reduced and the principal body cavity is the hemocoel that works as an open circulatory system which the vessels are twisted due to the torsion (RUPPERT et al., 2004). There is one muscular atrium that receives oxygenated blood from the gills whereas the more musculated ventricle pump it to the head and the visceral mass. The blood in gastropods works for the internal transport with help of the hemocianin pigment but the main role of the blood system is its function as a hydrostatic skeleton (RUPPERT et al., 2004). The Figure 1  represents the basic circulatory system with association to the gills.

Figure 1. Circulatory system, showing the hemolymph flow. Illustred by Gustavo Zoppello Toffoli, 2015
adapted from Brusca & Brusca 2002.

           The nervous system is composed by an anterior ganglia and paired ventral cords. Due to the torsion, the parts of the nervous system that links the head and the foot with the visceral mass is torted forming the visceral loop (BRUSCA & BRUSCA, 2002). See Figure 1. 

            The L. filosa sense organs include a pair of simple eyes positioned in the base of the cephalic tentacles and appear to be just for light detection, a pair of cephalic tentacles that act as a tactile structure, osphradia that has a sensitive chemic function related with water quality and statocystis in the foot for movement detection (REID, 1986; RUPPERT et al., 2004).

Figure 1. Ganglia disposition in hypothethical untorted ancestral (left) and torted adult of gastropod. Illustrated
by Gustavo Zoppello Toffoli, based on Brusca & Brusca 2002.

            They have just one gonad which is linked to the right nephridium by the gonoduct. L. filosa is a dioecious specie; the male has a penis that stays behind to the right cephalic tentacle that gives assistance to the sperm transference and also a prostate gland responsible for seminal fluids production. The female has an ovary that extend through the digestive gland, a thin, transparent oviduct and a seminal receptacle responsible for the sperm storage and production of the egg capsule. However, as an ovoviviparous specie, there is not a capsule covering the eggs in L. filosa.

            The penis characteristic is used in taxonomic classification as well as palial oviducts and sperm nurse cells (REID, 1986).

Figure 1. Male reproductive system, mantle cavity opened. Adapted from Reid, 1986
(authorized image usage). ©David G. Reid

            Periwinkles, as protostomes, have a typical spiral cleavage (BRUSCA & BRUSCA, 2002). The development in L. filosa is indirect with formation of a larval stage called trochophore similar to the annelids, then, giving way to a molluscan exclusive larval stage called veliger that already has some of the adult structures (BRUSCA & BRUSCA, 2002). See Figure 1 below:

Figure 1. Model of a veliger larvae of a snail (lateral view). Illustred by Gustavo Zoppello Toffoli, based on Ruppert
et al., 2004.

As an adaptation to the semi-terrestrial habit, L. filosa developed an ovoviviparous characteristic releasing the veliger larvaes into the water for a planktonic stage of life (REID, 1986). This type of larvae is responsible for the dispersion of the specie and it is interfered by the ocean currents (RUPPERT et al., 2004).

The settlement process is not well studied but due to the distribution, probably it occurs in mangrove trunks, roots and pneumatophores by a chemical selective process. After the settlement, if favorable conditions, the larvae will metamorphose to the adult form (RUPPERT et al., 2004).