Information

What are these four large snails doing?


Hiking in some hills near Taipei after a rain, I saw lots of large snails out and about. Here "large" means the shells are say 8 cm long, and the snail itself fully stretched out 10 to 15 cm perhaps.

At one point I saw a cluster of four snails stuck together in a confusing way. The one on the right was slowly climbing uphill, pulling the other three along.

What is going on here? I see some connections between some of the snails, but I can't really understand most of what I'm looking at here, nor why four snails would be stuck together sideways like this.


These are probably giant African snails, Achatina fulica, an invasive species of land snails. The two snails in the middle are mating using love darts. The other two may be waiting for their turn.

See also: Wikipedia - Achatina fulica


These snails, Achatina fulica, belong to a family of land snails called Achatinidae. They are invasive and while being agricultural pests, can also be vectors of pathogens. The two snails in the middle are actually mating through a reciprocal simultaneous exchange of gametes through the sexual organs that are clearly visible. These species of land snails do not use love darts as suggested by Dr. Evenor.


What are these four large snails doing? - Biology

In Florida, there are three native and two introduced species of snails, belonging to five different families, that are known to feed on other snails. In addition, several introduced species of the Subulinidae are considered carnivorous, but little is known of their biology and identification is difficult.

The best known of the Florida predatory snails is the rosy wolfsnail, Euglandina rosea (Férussac, 1821), which was exported to Hawaii and other areas (Mead 1961) in vain attempts to control the giant African snail, (Achatina fulica Bowdich, 1821). A Mediterranean snail, the decollate snail, Rumina decollata (Linnaeus, 1758), is much heralded today (Fisher et al. 1980) in California as an effective biological control agent of the brown garden snail, Cornu aspersum (Müller, 1774). Relatively little is known of the other three species of snail-eating snails, two of which are less than 10 mm long. All of these Florida predaceous snails are easy to identify and the following account summarizes what is known of their distributions, identification and habits.

Euglandina rosea (Férussac 1821), rosy wolfsnail (Family Spiraxidae)

Identification: The shell is large, up to 76 mm in height and 27.5 mm in diameter, is thick and has prominent growth lines. The shape of the shell is fusiform with a narrow ovate-lunate aperture and a truncated columella. Typically, the shell color is brownish-pink. Adults measure 7-10 cm in length.

Figure 1. The rosy wolfsnail, Euglandina rosea (Férussac, 1821). Photograph by Lyle, J. Buss, University of Florida.

Figure 2. Top view of the rosy wolfsnail, Euglandina rosea (Férussac, 1821). Photograph by Paul M. Choate, University of Florida.

Figure 3. Reverse view of the rosy wolfsnail, Euglandina rosea (Férussac, 1821). Photograph by Paul M. Choate, University of Florida.

Distribution: In the United States: Alabama, Florida, Georgia, Hawaii, Louisiana, Mississippi, South Carolina and southeastern Texas. It is widespread in Florida, including the Keys. It is widespread, but usually found singly in hardwood forests, roadsides and urban gardens (Hubricht 1985).

Comments: This snail was chosen as a possible biological control agent of the giant African snail. Live specimens were sent to Hawaii in 1955 (Mead 1961). Although feeding in Achatina was observed, as well as on the Asian tramp snail, Bradybaena similaris (Férussac, 1821) and native tree snails (Hart 1978), no real control was achieved. The snail reproduced rapidly in Hawaii and, by 1958, 12,000 snails were harvested for release in other Hawaiian Islands, New Guinea, Okinawa, Palau Islands, Philippines and the Bonin Islands. Chiu and Chou (1962) gave details of the biology of Euglandina in Taiwan. Individuals live up to 24 months and adults lay 25 to 35 eggs in a shallow pocket in the soil. These hatch after 30 to 40 days. In Taiwan, Euglandina consumed as many as 350 Achatina during its lifetime. Euglandina rosea is now considered invasive in Hawaii as it has caused the extinction of eight native snail species.

Rumina decollata (Linnaeus 1758), the decollate snail (Family Subulinidae) (Back to Top)

Identification: The adult shell is large, being up to 45 mm in height and 14 mm in diameter. It only retains four to seven whorls in adulthood, the other eight to 10 whorls being lost. The shell is perforate, glossy and sculptured with prominent axial growth lines and fine spiral striae. The columella is straight, its lip margin reflexed but the outer lip is simple. The shell color is pinkish brown. It is not easily confused with any other snail in Florida.

Figure 4. Top view of the decollate snail, Rumina decollata (Linnaeus, 1758). Photograph by Paul M. Choate, University of Florida.

Figure 5. Reverse view of the decollate snail, Rumina decollata (Linnaeus, 1758). Photograph by Paul M. Choate, University of Florida.

Distribution: Native to the Mediterranean area, but introduced widely in the United States, Bermuda and Mexico. It is widespread, but localized, in the Sun Belt from California east to Florida and north along the Atlantic coast to Pennsylvania. Very localized populations in Florida are known from Pensacola (Dundee 1970), Miami, Key Vaca and Marathon.

Comments: This snail was long considered a minor plant pest (Brantlinger 1953), although recognized as omnivorous. In California (Fisher et al. 1980), studies showed this snail is an effective predator of half-grown brown garden snails in particular and, like the brown garden snail, prospered only in cultivated habitats with frequent irrigation. It is thought that rodents limit the feral spread of the snails. Decollate snails will feed on new sprouts, old leaves, especially those in contact with the soil, and fallen bruised fruit. Their value in controlling the brown garden snail is considered to outweigh their minor pest attributes in California. These snails are ground dwellers, living among leaves, and sometimes burrowing in the upper one inch of soil (Fisher et al. 1980).

Haplotrema concavum (Say, 1821), gray lancetooth (Family Haplotrematidae) (Back to Top)

Identification: The shell is large, 10 to 22 mm in diameter and 5 to 10 mm in height, and depressed with 5 to 5 1/2 whorls. The whorls are convex with deeply impressed sutures. The umbilicus is broadly open, about 1/3 shell diameter. The shell is moderately strong, shining and smooth except for irregular axial striations and occasional fine spiral incised lines. The aperture is round to lunate. The parietal callus is yellowish, usually with a thickened edge. The shell color is white to very pale brown (dead) or greenish-white to light yellow (alive).

Figure 6. The gray lancetooth, Haplotrema concavum (Say, 1821). Photograph by Bill Frank, www.jaxshells.org.

Figure 7. The gray lancetooth, Haplotrema concavum (Say, 1821). Photograph by Bill Frank, www.jaxshells.org.

Distribution: Southern Canada to the Gulf States and west to eastern Nebraska and Oklahoma (Hubricht 1985). In Florida, it is presently known only from counties bordering the Apalachicola River.

Comments: Found in humid hardwood forests, living in leaf litter at tree bases, or under rotting logs. Pilsbry (1946) states that this family is rapacious, but Hubricht (1985) found this species feeding on dead shells more often than living snails, suggesting that this species may be using other snails as a source of lime rather than as prey. In Florida, these snails, especially juveniles, could be confused with the smaller, introduced species of Oxychilus. However, the much broader and open umbilicus of Haplotrema is distinctive.

Huttonella bicolor (Hutton, 1834), two-toned gulella (Family Streptaxidae) (Back to Top)

Identification: The shell is small, 5 to 7.5 mm in height and 1.5 to 2.0 mm in diameter), elongate and sturdy. Shell color is very pale brown to white live specimens are bright orange due to body color. Shell sculpture is smooth, except at sutures where axial riblets are present. Well developed axial ribs are present behind apertural lip and in the umbilical region. Aperture with four prominent teeth.

Figure 8. The two-toned gulella, Huttonella bicolor (Hutton, 1834). Drawing by Bill Frank, www.jaxshells.org.

Distribution: Introduced from Orient (Burch 1962) or southern Africa (Dundee 1974). Widespread in the Caribbean region. In the United States, apart from Florida, it is also known from Louisiana, Mississippi, South Carolina, and Texas (Dundee 1974). It is also found in Brazil, Nicaragua, Australia (Northern Territory), and the Pacific area.

Comments: This snail is apparently an effective predator of Subulina octona (Bruguière, 1798) (Mead 1961) and pupillids (Dundee and Baerwald 1984). In Florida, the presence of four apertural teeth is diagnostic except for some tiny species of Pupillidae which are distinguished by their ovate or pupate shapes.

Varicella gracillima floridana Pilsbry, 1907, a predatory snail (Family Oleacinidae) (Back to Top)

Identification: The shell is small, 6 to 8 mm in height and 1.5 to 1.7 mm in diameter), elongate, somewhat scariform and thin. The whorls number 8 to 8 1/2, and are convex with deeply impressed sutures. Shell sculpture is distinctive with about 25 straight, narrow axial ribs, between which are six to eight fine axial striae. The shell is imperforate, the aperture ovate, and the outer lip slightly sigmoid, arching forward at middle but receding at base. The columella is straight and slightly calloused. Shell color is pale brown.

Figure 9. Varicella gracillima floridana Pilsbry 1907. Photograph by John Slapcinsky, University of Florida.

Distribution: Collected only from the Florida Keys and the Miami area. The subspecies Varicella g. gracillima (Pfeiffer 1851) occurs in Western Cuba (Pilsbry 1946).

Comments: These snails live under leaf litter, logs and rocks, usually in hardwood hammocks. No studies have been made of their biology, but Burch (1962) implied they are predatory on other snails.

Selected References (Back to Top)

  • Brantlinger. 1953. A European Snail. Arizona Cooperative Economic Insect Report 3: 849.
  • Burch JB. 1962. How to Know the Eastern Land Snails. Wm. C. Brown Co., Publishers, Dubuque, Iowa. 214 pp.
  • Chiu Shui-Chen, Ken-Ching Chou. 1962. Observations on the biology of the carnivorous snail, Euglandina rosea Ferussac. Bulletin Institute of Zoology, Academia Sinica 1: 17-24.
  • Dundee DS. 1970. Introduced Gulf Coast Mollusca. Tulane Studies in Zoology and Botany 16: 101-115.
  • Dundee DS. 1974. Catalog of introduced molluscs of eastern North America (North of Mexico). Sterkiana 55: 1-37.
  • Dundee DS, Baerwald RJ. 1984. Observations on a micropredator Gulella bicolor (Hutton) (Gastropoda: Pulmonata: Streptaxidae). Nautilus 98: 63-68.
  • Fisher TW, Orth RE, Swanson SC. 1980. Snail against snail. California Agriculture (Nov.-Dec.): 3 pp.
  • Hart AD. 1978. The onslaught against Hawaii's tree snails. Natural History Magazine (December): 46-56.
  • Hubricht L. 1985. The distributions of the native land mollusks of the eastern United States. Fieldiana, Zoology (new series) No. 24: i-viii, 1-191.
  • Mead AR. 1961. The Giant African Snail a Problem in Economic Malacology. University of Chicago Press, 257 pp.
  • Pilsbry HA. 1946. Land Mollusca of North America (North of Mexico). Academy of Natural Sciences Philadelphia Monographs No. 3, 2:1-520.

Authors: Kurt Auffenberg and Lionel A. Stange, Florida Department of Agriculture and Consumer Services, Division of Plant Industry T.R. Fasulo, University of Florida
Originally published as DPI Entomology Circular 285. Updated for this publication.
Photographs: Paul M. Choate, Lyle J. Buss and John Slapcinsky, University of Florida Bill Frank, www.jaxshells.org
Drawing: FDACS-Division of Plant Industry
Web Design: Don Wasik, Jane Medley
Publication Number: EENY-251
Publication Date: November 2001. Latest revision: July 2011. Reviewed: December 2017. Reviewed: February 2021 .

An Equal Opportunity Institution
Featured Creatures Editor and Coordinator: Dr. Elena Rhodes, University of Florida


Absurd Creature of the Week: This Slug Has Such a Big Penis It Has to Mate Upside Down

To revist this article, visit My Profile, then View saved stories.

To revist this article, visit My Profile, then View saved stories.

If you read this column with even the slightest regularity, you know that the animal kingdom has no shortage of weird sex. Like that of the parasite that devours a fish's tongue and mates in its mouth. Or the little marsupial that has so much sex it bleeds internally and goes blind and dies. I could go on.

None of it’s particularly elegant. So may I present to you the acrobatic, upside-down sex of the leopard slug, done hanging from a branch on a line of slime. But why, when other slugs do the horizontal tango perfectly fine on the ground? Well, a lot of it has to do with the leopard slug’s gigantic penis, of course.

First things first: Slugs are hermaphrodites, and that’s a neat evolutionary move. Not only does it all but guarantee that any two sexually mature slugs can come together to make babies, it also means that when they do mate, both parties can end up fertilized. In fairness, though, the big disadvantage to hermaphroditism is that it's more energetically costly to produce both eggs and sperm, as opposed to one or the other.

So, when two leopard slugs find each other, they make their way up a tree and onto a branch. Here they curl around each other and ramp up their release of slime—big time. This appears to be a different formulation than your average leopard slug goo, according to Ben Rowson, a limacologist (that’d be a slug scientist) at the National Museum Wales. The pair will then descend on a slimy rope. “That rope of slime that they hang from can be very strong,” Rowson says. “It's strong in the moment, but also when it dries out. It's a fairly tough structure, really.”

Still curled around each other, hanging and gently twirling, the slugs simultaneously unravel their alien-blue penises, which come out of the right side of their head. They do this with hydrostatic pressure, pumping fluids into the penis to enlarge it more and more (the slugs use the same method for controlling their famous eye stalks, by the way).

The penises are very mobile, it's almost as if they've got a mind of their own.

“These penises, they start off small, but within a few moments you can see just how big they are—they become almost bigger than the slugs themselves,” says Rowson. “The penises are very mobile, it's almost as if they've got a mind of their own. They're quite complicated structures, and they move continuously and they can change their form quite a lot.”

I’m just going to keep quoting Rowson here, because this stuff is gold. The penises “wrap around each other and they form this kind of chandelier configuration, which is very strange, with these flaps around the edge with a frill on it. And that can pulsate up and down and in and out as the slugs are rotating around. It's quite the elaborate interaction."

All the while liquid is pumping into the hugging penises. “They're pushed out by the fluid inside the body, but these things are so big that I think they take up most of the fluid that's inside,” Rowson says. “So the rest of the slug looks a bit drained or flattened while all the fluid is in the genitalia.”

When everything is sufficiently inflated, the transfer of sperm begins. And when everyone is sufficiently fertilized, the slugs will haul themselves back up the rope, though sometimes one partner will simply drop to the ground. Regardless, one of them will consume the slime rope to recoup the resources lost in excreting it. (Interestingly, another slimer, the velvet worm, hunts by spraying its prey with goo. After it has entrapped and eaten the victim, it too devours the spent glue. In nature, you see, there’s no sense in letting resources go to waste.)

The fertilized slugs go off and lay their eggs in soil or a moist log or what have you. Come spring, the eggs will hatch into tiny slugs, thus completing the strange saga that is the leopard slug penis intertwining.


Animal Diversity Web

Achatina fulica originated in the coastal areas and islands of East Africa, where it presumably got the nickname, “Giant African Snail.” The snail inhabits countries ranging from Mozambique in the south, to Kenya and Somalia in the north. It is not only found in East Africa on the coastal areas and islands, but it has also been introduced to many other countries in Africa, along with many countries worldwide. The snail has been introduced into countries as far apart as the United States to Australia, and countries in-between. Achatina fulica is not a migratory species and has therefore been introduced through other means to the countries outside of East Africa, possibly through agricultural transportation, commerce, trade, vehicle attachment, smuggling, and other accidental and purposeful ways. ("Achatina fulica", 2014a "Giant African snail", 2013 "Lissachatina fulica", 2014 "Snails (Giant East African Snail)", 2012 Cowie, 2010 Egonmwan, 2007 Stokes, 2006 Vogler, et al., 2013)

Habitat

The giant African land snail has a natural habitat located in Africa, where there is a tropical climate with warm, year round temperatures, and high humidity. The snail has adapted and has been able to thrive in temperate climates as well. This species prefers areas of low to mid-elevation, with temperature preference between nine degrees Celsius and twenty-nine degrees Celsius. Achatina fulica can survive less ideal conditions, such as two degrees Celsius by hibernation and thirty degrees Celsius by aestivation. The snail can be found in agricultural areas, coastal areas, wetlands, disturbed areas, forests, urban areas, and riparian zones. The snails need temperatures above freezing and preferably high humidity in order to thrive the best. They have adapted to dry and cooler areas, however, by being able to hibernate in soft soil during the unfavorable weather conditions. ("Achatina fulica", 2014a "Snails (Giant East African Snail)", 2012 Cowie, 2010 Stokes, 2006 Vogler, et al., 2013)

  • Habitat Regions
  • temperate
  • tropical
  • terrestrial
  • Terrestrial Biomes
  • savanna or grassland
  • forest
  • Other Habitat Features
  • urban
  • agricultural
  • riparian

Physical Description

The giant African snail can be distinguished from other snails due to their large size when mature, the snail can reach up to eight inches (30 centimeters) in length with a diameter of four inches (10 centimeters). The snail can reach up to thirty-two grams in weight. The snail has the physical features that are associated with the phylum Mollusca, including a shell. The shell of Achatina fulica is cone-shaped and has a height that is twice that of the width. When the snail is mature and full-grown, the shell will normally consist of seven to nine whorls. The color of the snail differs depending on the environment, as some are primarily brown or dark colored, with dark stripes and streaks that run across the whorls, while others are reddish-brown with pale yellow vertical markings. ("Achatina fulica", 2014a "Achatina fulica", 2014b "Giant African Land Snail", 2008 "Giant African snail", 2013 "Pest Alert", 2011 "Snails (Giant East African Snail)", 2012 Cowie, 2010 Stokes, 2006)

  • Other Physical Features
  • ectothermic
  • heterothermic
  • bilateral symmetry
  • Average mass 32 g 1.13 oz
  • Range length 30 (high) cm 11.81 (high) in

Development

The fertilized eggs of A. fulica are laid in a nest, or in the dirt and leaves, so as to protect and disguise the eggs. The eggs then hatch and become immature snails, which grow to adulthood in about six months. Achatina fulica is one of many land snails, which do not have a larvae phase like other Gastropod species. ("Achatina fulica", 2014a "Achatina fulica", 2014b)

Reproduction

Achatina fulica is hermaphroditic each individual snail has both male and female reproductive parts. There are no distinguishing parts separating sexes because each snail contains both sex reproductive systems. They do not self-fertilize, so the snails need to mate with another snail of their species. As a Stylommatophiora , Achatina fulica does not mate randomly the snails mate with respect to age and size of other snails. Immature, small snails that are still growing produce only spermatozoa, while larger, mature adults produce both spermatozoa and ova. There is an age dependent mate choice when it comes to young snails because they need and prefer older adults to mate with. Young giant African snails copulate at all hours of the night, while older adults mate in the middle of the night. The snails choose their mates with respect to size and age, but the reproductive stage-dependent mate is a more attractive mate than the body size-dependent mate choice. Mating occurs when one snail encounters a prospective partner that the individual snail deems acceptable to mate with. When two individual snails mate, there is a possibility that gametes will be transferred to each one by the other simultaneously. However, this is only the case if the snails are around the same size. If there is a size difference, the larger snail will act as the female and the gametes will only be transferred from the smaller snail to the larger snail, mating unilaterally. ("Achatina fulica", 2014a "Giant African Land Snail", 2008 "Giant African snail", 2013 "Lissachatina fulica", 2014 "Pest Alert", 2011 Cowie, 2010 Egonmwan, 2007 Tomiyama, 1996)

When two A. fulica encounter and deem each other worthy mates, they will mate by one mounting the shell of the other. The mating will begin once the two snails exchange sperm with one another. The sperm is used to fertilize the eggs in the snails, but it can also be stored inside the body for up to two years. The fertilized eggs are laid between eight and twenty days after mating has occurred, and are deposited in nests or among rocks and soils on the ground. The eggs usually hatch at temperatures above fifteen degrees Celsius. The eggs, under the right conditions, will hatch after eleven to fifteen days into small snails. The number of eggs that an individual snail lays often depends on the maturity and age of the snail and is between 100 to 500 eggs. Giant African snails have no specific season of mating, as they are able to produce new clutches every two to three months. ("Achatina fulica", 2014a "Giant African snail", 2013 Egonmwan, 2007 Tomiyama, 1996)

  • Key Reproductive Features
  • iteroparous
  • year-round breeding
  • sequential hermaphrodite
    • protandrous
    • internal
    • Breeding interval The giant African snail breeds every two to three months.
    • Breeding season Breeding can take place any time of the year.
    • Range number of offspring 100 to 500
    • Average number of offspring 200
    • Range gestation period 11 to 15 days
    • Average age at sexual or reproductive maturity (female) 6 months
    • Average age at sexual or reproductive maturity (male) 6 months

    The parents of Achatina fulica do not contribute to the lives of their offspring except for fertilization and laying of the eggs in nests or soil. Once the eggs are hatched, the small individuals are on their own and adopt the territory that their parent provided them. (Cowie, 2010 Egonmwan, 2007)

    Lifespan/Longevity

    Achatina fulica can live on average between three and five years, with some individuals reaching as old as ten years. There is not much difference between the lifespans in the wild and in captivity. In their natural habitat, predators are a main cause of mortality of Achatina fulica , however as they have become an invasive species, their new habitats contain close to zero predators. The snails usually die due to natural causes or non-favorable living conditions. Recently, there have been developments in molluscicides that have been impactful on killing this species, in order to better control their population in unwanted areas. ("Achatina fulica", 2014a "Lissachatina fulica", 2014 Cowie, 2010)

    • Range lifespan
      Status: wild 10 (high) years
    • Typical lifespan
      Status: wild 3 to 5 years
    • Typical lifespan
      Status: captivity 3 to 5 years

    Behavior

    Achatina fulica is a solitary species. The parents do not have an impact in their offsprings’ lives once the eggs are hatched, so the solitary behavior is intact from the beginning. It is not possible for A. fulica to self-fertilize, so courtship and interaction is a necessary aspect of their lives. Movement is an important aspect of their lives as it is necessary for mating, finding food, and escaping threats. Achatina fulica secretes a slime-like substance that allows for smooth and easy travel during its movement. The substance protects and allows travel across rough and sharp surfaces. Achatina fulica is a nocturnal species and lies dormant during the day. The snails often bury themselves in soil, in order to stay cool and remain hidden from threats. Giant African snails can also survive cold conditions by aestivating they become slow and sluggish as they wait for warmer and more desired conditions to occur. ("Lissachatina fulica", 2014 "Pest Alert", 2011)

    • Key Behaviors
    • terricolous
    • nocturnal
    • motile
    • sedentary
    • aestivation
    • solitary

    Communication and Perception

    Achatina fulica does not need to communicate often, as it is not a social species. The time of communication among the species takes place in the process of mating, as one will mount the back of another individual. Communication takes place as there is a change in the position of the head, along with changes in the movement of the body. The changes in the body and head are communication cues that indicate that the mating process will continue. Achatina fulica does not have hearing as a sense, so it relies on its other senses to perceive the environment. This species also has caudal tentacles the upper pair of tentacles have eyes at the tips and the lower pair have the sensory organ that allows for smell. This species has a strong sense of smell, which assists in finding food sources. The combination of smell and sight is how this species perceives the environment around them and allows for the detection of food, mates, and potential threats. ("Achatina fulica", 2014a "Giant African snail", 2013 Cowie, 2010 Egonmwan, 2007)

    Food Habits

    Giant African snails are herbivores. Achatina fulica feeds primarily on vascular plant matter, having no preference whether it is living or dead matter. This snail species has a strong sense of smell that assists in attracting and leading the individuals to garden crops and other plant resources. These snails have different preferences with their ages young members of this species feed on decaying matter and unicellular algae. They also prefer soft textured Musa (bananas), Beta vulgaris (beets), and Tagetes patula (marigolds). More mature and developed African snails prefer to feed on living plants and vegetation. The mature snails broaden their spectrum of preferred plants to consume including: Solanum melongena (eggplant), Cucumis sativus (cucumber), Cucurbita pepo (pumpkin), and many others. This species has also been found to feed on other snails, lichens, fungi, and animal matter. The radula, a distinguishing characteristic of Gastropods, is essential in the ability to eat a variety of foods. The radula is a toothed ribbon used to scrape or cut food, and allows for the ability to pick up food and begin the digestive process with ease. ("Achatina fulica", 2014a "Giant African Land Snail", 2008 "Lissachatina fulica", 2014 "Snails (Giant East African Snail)", 2012 Cowie, 2010)

    • Primary Diet
    • herbivore
      • folivore
      • frugivore
      • Animal Foods
      • mollusks
      • Plant Foods
      • leaves
      • wood, bark, or stems
      • seeds, grains, and nuts
      • fruit
      • flowers
      • lichens
      • algae
      • Other Foods
      • fungus
      • detritus

      Predation

      Achatina fulica has a shell from the beginning of its life until the end. The shell is used for protection against the environmental conditions and potential predators. The shell also provides protection for the internal organs against outside forces. The colors of A. fulica tend to be more earthy tones, as to not stand out in its environments and to be more camouflaged from the sight of their predators. Predators of Achatina fulica includes many species of rodents, wild boars, terrestrial crustaceans, and other species of snails. ("Giant African Land Snail", 2008 "Lissachatina fulica", 2014 "Snails (Giant East African Snail)", 2012)

      • Known Predators
        • Christmas Island red crab, Gecarcoidea natalis
        • cannibal snail, Euglandina rosea
        • land snail, Gonaxis quadrilateralis
        • fire ants, Solenopsis geminata
        • hermit crabs, Paguroidea
        • Malayan field rat, Rattus tiomanicus
        • Polynesian rat, Rattus exulans
        • Rice-field rat, Rattus argentiventer
        • wild boar, Sus scrofa
        • New Guinea flatworm, Platydemus manokwari

        Ecosystem Roles

        Achatina fulica has several different ecosystem roles. This species decomposes and consumes dead vegetation. The benefit of this ecosystem role is that the snail assists in recycling nutrients and the building blocks essential to life. Giant African snails are also part of the food chain, as they are a source of food to many predators. This species is also a host to parasitic organisms, such as Angiostrongylus cantonensis, the rat lungworm. The parasitic organisms live and thrive on this host and can be transported to other hosts, such as humans, through the consumption of the snails. ("Achatina fulica", 2014a "Achatina fulica", 2014b Carvalho, et al., 2003 Cowie, 2010 Stokes, 2006)

        Economic Importance for Humans: Positive

        Snails are often seen as a delicacy for humans and A. fulica is no exception. Humans around the world consume giant African snails as a source of protein when prepared correctly. This species is also a cheap alternative in some regions as a source of fish feed in fish farming, as they breed quickly and in large amounts. Achatina fulica can also be beneficial in making fertilizer, chicken feed, and biological compounds in clinical and experimental laboratories. ("Achatina fulica", 2014a "Lissachatina fulica", 2014 Stokes, 2006)

        Economic Importance for Humans: Negative

        Giant African snails are an invasive species across that world. It has become illegal to have possession of these snails in countries where it has been introduced. Achatina fulica has a large and broad diet preference the dietary habits of this species cause a high loss in crops for farmers. They are considered an agricultural pest, costing farmers not only their crops but also economic costs. This species is also a carrier of many parasitic organisms, including organisms that harm people and plants. Serious illness and diseases can erupt in humans if they consume giant African snails. Achatina fulica also destroys and pollutes its surroundings, including soil. When an individual of this species dies, the calcium carbonate found in the shells neutralizes the soil the neutralization of the soil and the altering of its properties affect the types of plants that can grow in the soil. Achatina fulica can cost cities, states, or countries millions of dollars in not only agricultural costs, but also in attempts to control this invasive species. ("Achatina fulica", 2014a "Achatina fulica", 2014b "Giant African Land Snail", 2008 "Lissachatina fulica", 2014 "Species Profiles: Giant African Snail", 2014 Carvalho, et al., 2003 Cowie, 2010 Stokes, 2006)

        Conservation Status

        Achatina fulica is not currently vulnerable, threatened, nor endangered.

        • IUCN Red List Not Evaluated
        • US Federal List No special status
        • CITES No special status
        • State of Michigan List No special status

        Contributors

        Taylor Hoffman (author), Grand View University, Nicole Pirie (author), Grand View University, Felicitas Avendano (editor), Grand View University, Dan Chibnall (editor), Grand View University, Angela Miner (editor), Animal Diversity Web Staff.

        Glossary

        Living in Australia, New Zealand, Tasmania, New Guinea and associated islands.

        living in sub-Saharan Africa (south of 30 degrees north) and Madagascar.

        living in the Nearctic biogeographic province, the northern part of the New World. This includes Greenland, the Canadian Arctic islands, and all of the North American as far south as the highlands of central Mexico.

        living in the southern part of the New World. In other words, Central and South America.

        living in the northern part of the Old World. In otherwords, Europe and Asia and northern Africa.

        living in landscapes dominated by human agriculture.

        having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

        helps break down and decompose dead plants and/or animals

        an animal which directly causes disease in humans. For example, diseases caused by infection of filarial nematodes (elephantiasis and river blindness).

        uses smells or other chemicals to communicate

        particles of organic material from dead and decomposing organisms. Detritus is the result of the activity of decomposers (organisms that decompose organic material).

        animals which must use heat acquired from the environment and behavioral adaptations to regulate body temperature

        union of egg and spermatozoan

        an animal that mainly eats leaves.

        A substance that provides both nutrients and energy to a living thing.

        forest biomes are dominated by trees, otherwise forest biomes can vary widely in amount of precipitation and seasonality.

        an animal that mainly eats fruit

        An animal that eats mainly plants or parts of plants.

        having a body temperature that fluctuates with that of the immediate environment having no mechanism or a poorly developed mechanism for regulating internal body temperature.

        ovulation is stimulated by the act of copulation (does not occur spontaneously)

        fertilization takes place within the female's body

        referring to animal species that have been transported to and established populations in regions outside of their natural range, usually through human action.

        offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

        having the capacity to move from one place to another.

        the area in which the animal is naturally found, the region in which it is endemic.

        found in the oriental region of the world. In other words, India and southeast Asia.

        reproduction in which eggs are released by the female development of offspring occurs outside the mother's body.

        the business of buying and selling animals for people to keep in their homes as pets.

        condition of hermaphroditic animals (and plants) in which the male organs and their products appear before the female organs and their products

        Referring to something living or located adjacent to a waterbody (usually, but not always, a river or stream).

        reproduction that includes combining the genetic contribution of two individuals, a male and a female

        mature spermatozoa are stored by females following copulation. Male sperm storage also occurs, as sperm are retained in the male epididymes (in mammals) for a period that can, in some cases, extend over several weeks or more, but here we use the term to refer only to sperm storage by females.

        uses touch to communicate

        that region of the Earth between 23.5 degrees North and 60 degrees North (between the Tropic of Cancer and the Arctic Circle) and between 23.5 degrees South and 60 degrees South (between the Tropic of Capricorn and the Antarctic Circle).

        the region of the earth that surrounds the equator, from 23.5 degrees north to 23.5 degrees south.

        A terrestrial biome. Savannas are grasslands with scattered individual trees that do not form a closed canopy. Extensive savannas are found in parts of subtropical and tropical Africa and South America, and in Australia.

        A grassland with scattered trees or scattered clumps of trees, a type of community intermediate between grassland and forest. See also Tropical savanna and grassland biome.

        A terrestrial biome found in temperate latitudes (>23.5° N or S latitude). Vegetation is made up mostly of grasses, the height and species diversity of which depend largely on the amount of moisture available. Fire and grazing are important in the long-term maintenance of grasslands.

        living in cities and large towns, landscapes dominated by human structures and activity.


        Freshwater Snails of Florida ID Guide

        Throughout the 19th and 20th Centuries malacologists made frequent field trips to explore river systems that were poorly known, and to revisit others that were renown for their rich and unique assemblages of species. The focus on most investigations was on rivers north of Florida, and little attention was given to the Florida fauna. Until recently the entire knowledge of the Florida freshwater snail fauna was based on miscellaneous papers dealing with single species, groups of closely related species or single river systems.

        Wm. J. Clench and Ruth P. Turner (1956) published a survey of the fauna from the Suwannee River west to the Escambia River. This study was a landmark contribution to the malacology of the southeast, and it summarized the known fauna of western Florida. It also was the first adequately illustrated faunal summary published on the Southeast. Since then a great amount of fieldwork has taken place throughout Florida, and many additions to the fauna have come to light. Some were range extensions for species known to occur in adjacent areas. Others were new taxa not found in earlier surveys.

        It became increasingly important to provide an identification manual of the freshwater snails of Florida for many reasons. There were no references to cover the entire state. Those available covered only part of the state or part of the fauna. Our knowledge of the fauna has greatly increased during recent years, and a summary of this information was desirable to facilitate other kinds of study. The bio-economic importance of snails to environmental issues has become increasingly relevant because of the impact that economic development has on Florida waterways. The first edition of The Freshwater Snails of Florida: a Manual for Identification was published in 1984. It was well received, and it served the interests and needs of many people. As was anticipated, further work on the systematics of the southeastern freshwater snail fauna created the need for subsequent revision in 1999, and for this updated version.

        Vernacular manes used in this manual are consistent with the standardized list of vernacular names for North American freshwater snails recently established by the American Fisheries Society (Turgeon, et al, 1998). Vernacular names are given only for species. Subspecies bear the same name as the nominate subspecies, as is consistent with the standard used by the American Fisheries Society for fishes, and by other societies for other classes of animals. This manual recognizes 113 species and subspecies that occurring in Florida and the list will increase with time.

        The manual treats only those genera that occur in freshwater. It is presented in the form of key supplements with illustrations and habitat information to facilitate identifications. It should be remembered that it is only a key which emphasizes shell characters. Occasionally it may be necessary to turn to other information sources to determine identifications with a greater degree of certainty.. It should also be remembered that many groups have not been studied sufficiently, and the reader may have material that adds to or contradicts previously recorded information. It is hoped that this manual will stimulate other biologists to contribute to our knowledge of freshwater mollusks. The reader will discover how very little we know about any genus occurring in Florida.

        Fred G. Thompson (1934-2016)
        (Fmr.) Curator of Malacology
        Florida Museum of Natural History
        University of Florida
        Gainesville, Florida 32611-7800

        Preparing Specimens for Identification

        Adequate preservation begins when the specimens are collected. Live snails for shell studies should be preserved in 70 percent alcohol. Never preserve shell specimens in formalin. Formalin will corrode the shell and thereby eliminate color, delicate sculpture, and the periostracum — the thin “skin” coating present on most shells.

        Formalin does not even serve as a good fixative or preservative for long-term anatomical studies. After a few years in storage glandular tissues in the female reproductive system deteriorate, and the process gradually spreads to destroy all but the terminal genital structures. It matters not that the specimens are stored in 70 percent alcohol after having been fixed in formalin. The deterioration process is not reversible. This is particularly so in the Pulmonata. However, formalin is an excellent fixative for short-term preservation.

        It is important to save some specimens for anatomical studies. This is essential in the case of the Hydrobiidae. Live field samples should be divided into two groups, one to be preserved for shells, the other to be preserved for anatomical specimens. The latter are placed in a small container filled with pond water. Do not use tap water since copper ions from the plumbing system may contaminate the tap water and kill the snails prematurely. Scatter a few granulated menthol crystals on the water surface and allow the container to sit for 10-15 hours, at which time the snails should be extended from the shell and insensitive to probing with a needle. A little practice may be necessary to perfect this relaxing procedure. Specimens then are placed in a fixative such as 10 percent formalin or Bouin’s Solution. The fixative may damage the shell, but that is unimportant for anatomical purposes. After the snails have been in the fixative for a few minutes to several hours, depending upon their sizes, they should be rinsed in water and transferred to 70 percent ethyl alcohol. The radula can be studied by dissecting out the buccal mass and macerating it in clorox or sodium hydroxide. The radula is then thoroughly rinsed in distilled water, stained, and mounted on a microscope slide.

        Shell specimens should be cleaned and air-dried. Some shells may be heavily encrusted with mineral deposit and algae, which may obscure details of the sculpture and color. Dipping them in a dilute solution of oxalic acid and gently scrubbing them with a fine brush can clean such specimens. The shells should be rinsed frequently in tap water during the cleaning process to prevent etching by the acid. After the shells are thoroughly rinsed, they can be air-dried in cardboard trays. The bodies of large snails, such as viviparids and pilids, should be pulled from the shell. Opercula should be glued to cotton plugs and replaced within the aperture.

        Small- or medium-sized snails need to be identified with the aid of a binocular dissecting microscope that is equipped with an ocular micrometer calibrated to 0.1 mm accuracy so that precise measurements can be made. Opercula of minute snails can be studied most easily by removing them from the animal and viewing them with transmitted light.


        Peculiarities of Snail Anatomy

        Lourdes Ortega Poza / Getty Images

        Snails have a single, often spirally coiled shell (univalve), they undergo a developmental process called torsion, and they possess a mantle and a muscular foot used for locomotion. Snails and slugs have eyes on the top of tentacles (sea snails have eyes at the base of their tentacles).


        Reproductive biology of the "Copey" snail Melongena melongena (Linnaeus, 1758) in Cispata Bay on the Caribbean coast of Colombia.

        ABSTRACT The reproductive cycle of the "Copey" snail Melongena melongena at Cispata Bay was examined from October 1998 to September 1999. Gonad maturation was studied through macroscopic and microscopic observations on the gonads of females >70 mm (total shell height), showing that individuals were mature throughout the year, but with a period of maximal maturity in March which coincided with the time of maximum recruitment. The mean size at first maturity was 52 mm for males and 65 mm for females. A small number of intersex individuals (4%) (masculinized females, with a normally developed ovary and a rudimentary penis feminized males with a normally developed testis and gonopore) occurred at intermediate sizes. The proportion of males in the population decreases with the increase in individual size, with only females present at the biggest sampled size-class (mean size of 98.5 mm shell height), suggesting protandric hermaphroditism. If this is proven to be true, artisanal fishing preferring larger animals, could severely interfere in the success of reproduction.

        KEYWORDS: Reproductive cycle, Melongena melongena, Caribbean, protandric hermaphroditism, intersex,.

        The "Copey" snail Melongena melongena (Linnaeus, 1758) is widely distributed in the Gulf of Mexico, the Caribbean and the Antilles. The snail lives on the shallow areas of coastal lagoons, mangroves and estuaries, being an important component of the fauna on soft or muddy bottoms. The snail tends to concentrate on areas with high densities of its prey, which are bivalves, other gastropods, ascidians and carrion (Hathaway & Woodburn 1961, Hawkins 1973, Rodriguez 1976, Flores 1980, Cosel 1986, Morton 1986, Dalby 1989, Villareal 1989, Bowling 1994). Considering this behavior, fishers sometimes use mangrove roots, covered with the mitilid Mytilopsis soller as bait, letting the snails aggregate on the bait from one day to the next. The method of collection of these snails includes walking over the bottom and locating the snails beneath the mud with the foot. By doing this, the fishers are not able to discriminate size, all sizes being fished. M. melongena attains sizes up to 200 mm of shell height (Clench & Turner 1956, Abbott 1974, Flores 1980, Diaz & Puyana, 1994). In Cispata Bay individuals between 12 and 151 mm shell height are found, the mean size of capture being 57 mm.

        M. melongena copulates from December to July in Colombia (Rodriguez 1976) and then produces egg capsules. Egg masses of M. melongena have a common basal layer. The number of capsules produced fluctuates between 27-31, located along a string which measures up to 218 mm in length. Some modified, sterile egg capsules are produced and serve to anchor the egg mass on the soft bottom. This sterile capsules are smaller than fertile capsules, but have the same shape and are spaced approximately 28 mm apart at one end of the string. The average distance between fertile capsules along the string is only 6 mm, this distance getting shorter towards the last capsules produced. Egg masses are mostly buried in soft bottoms close to the vegetation on the coast. The capsules contain al least 185 to 290 embryos according to D'Asaro (1997), or 300 to 400 embryos according to Flores (1980), each embryo measuring 250 to 300 [micro]m. The development within the capsules takes 20 to 25 days. By day 16 a well developed veliger larvae is observed, having four large velar lobes with a double row of strong cilia on their outer edges. The foot and operculum are well developed, the larvae apparently being able to crawl. By day 25 or older, when removed from the capsule, the larvae no longer protruded the velar lobes, but they crawl actively and could rapidly turn over the shell with the aid of the foot. When the capsules open, most of the young snails, now incapable of swimming, immediately crawl and appeared to be feeding (Clench and Turner 1956)

        Rodriguez (1976) reported that the smallest mature females found in Cartagena Bay measured 80 mm and the males 65 mm of shell height. Besides this observations by Rodriguez, information on the gonad maturation of M. melongena in Colombia is scarce.

        With few exceptions, prosobranch gastropods are gonochoric, typically with internal fertilization, although some species demonstrate protandric hermaphroditism (Gallardo 1989). Rodriguez (1976) identified M. melongena females with shell heights between 40 and 62 mm having an incipient development of the penis. Species related to M. melongena, such as Busycon carica and M. corona, have similar characteristics (Castagna & Kraeuter 1994, Zetina 1999).

        Previous observations have suggested that in nursery habitats, small individuals were mostly males and in areas where growth and maturation occur, larger individuals were predominantly females (Hathaway & Woodburn 1961, Woodbury 1986, Zetina 1999). Intersex individuals and sex dominance in different size categories, suggest that M. melongena may be a consecutive protandric hermaphrodite. This requires verification, since artisanal fishing activities, which prefer larger sizes, may negatively affect the population by seriously altering sex proportions. The fishery for M. melongena occurs throughout the Caribbean, but as the snail is only used for local consumption, it does not appear in the statistics. Nevertheless, the fishery is important, for example Hernandez (2001) estimating for the Cispata Bay area (the bay and nearby sloughs) that 70% or the total biomass of the snail population is fished, representing for local fishers ca. 30% of their total income. The meat of the snail is mainly used around the Caribbean to offer appetizers (the popular "botanas") in beach restaurants of tourist areas.

        The objective of the present study was to describe the reproductive cycle and pattern of recruitment, sex ratio and the presence of intersex individuals in M. melongena in Cispata Bay. This in formation should provide a base for fisheries resource administrators to design biologically sound management measures for this resource.

        Individuals of M. melongena were collected from October 1998 to September 1999 from the Cispata Bay area (includes the nearby sloughs and the area close to Amaya Beach) (Fig. 1).

        Each month from October 1998 to September 1999, snails were searched for in the field (as fishers do, with the foot), collected manually and measured. This sampling was part of a study regarding distribution, abundance and growth of the snail. Thus, a great number of individuals (over 100), representing the entire depth distribution, was sampled. For the study of the reproductive cycle the largest 30 females, but measuring at least 70 mm of shell height (females of that size were observed to lay eggs), were selected. Due to the fishery, in which the average size of capture is around 50 mm, with few individuals reaching 80 mm or more, large individuals are scarce in the field, so when ever possible, larger individuals were bought from fishers. To get the 30 females, collected individuals had to be sacrificed to verify sex. As the aim of the study was to know the time of reproduction of M. melongena in Cispata Bay, the analysis was concentrated on females, considering that only when they are mature, copulation can occur. As perhaps not all females, but probably all males, may reproduce each year (as described for other gastropods), this method may sub estimate the number of reproducing individuals within the population. But the general seasonal pattern will not be affected by this.

        The tissues of each measured individual (total shell height in mm), were removed, and the gonad separated from them. Each component was then weighed separately (drained wet) to the nearest 0.01 g. The gonads were fixed in Bouin's fluid and prepared using traditional histologic procedures to obtain thin sections (6 [micro]m) stained with Ehrlich's Haematoxylin and eosin. Three sections were taken from each embedding block, each 360 [micro]m apart to avoid including the same reproductive follicles in the different sections.

        Two methods were used to establish the reproductive cycle. The first included a macroscopic quantitative evaluation (gonad index = GI) and the second was based on microscopic qualitative evaluation (index of gonad maturity = IGM).

        The gonad index (GI) is represented by:

        GI = (weight of the gonad / total weight of tissues) x 100

        For the total weight of tissues all soft tissues of the animal, including head, foot with operculum, visceral mass, mantle, as well as the gonad, were included.

        The index of gonad maturity (IGM) characteristics were established for each stage of gonad development, as defined by Ramorino (1975):

        * Evacuated (I): walls of acini with a corrugated appearance and abundant phagocytes within them.

        * Maturing (II): internal walls of the acini with pedunculated and pyriform vitellogenous oocytes and the presence of a few phagocytes and large spaces between them.

        * Maximum maturity (III): the walls of the acini take on a polygonal form without spaces between them and the presence of abundant nutritive cells.

        IGM was calculated using the following equation:

        Where F = stage of gametic development (I-III), n = number of individuals in stage F and N = number of total individuals.

        Using the size frequencies obtained throughout one sampling year and the growth parameters calculated by Hernandez (2001), the FISAT program routine for recruitment patterns (Gayanilo & Pauly 1997) was used. This permits determination of the number of recruitment pulses per year and their intensities. For this study, recruitment was defined as the addition of new individuals into the benthic population.

        Mean size at first maturity

        Based on information reported by Rodriguez (1976) and Flores (1980), which describe that M. melongena copulates from December to June, the egg masses being most abundant in February and March, an intensive sampling was done between December 1998 and March 1999. Ten individuals were obtained for each 10 mm size class, beginning with 20 mm individuals. This number of individuals was decided, considering the possibility to really obtaining them in the field, or being able to buy them from fishers. The lower limit of 20 mm corresponds to the smallest individuals fishers include in their catch. Both males and females were identified, using histologic sections of the gonads. Individuals were rated as either immature (abundant connective tissue absence of, or very few acini), or mature (Stages I-III). The data for each sex were fitted to a logistic model using the CurveExpert 1.3 program (Copyright (c) 1995-1997 Daniel Hyams.) based on the equation:

        Where Y = Relative accumulated frequency (%), a = constant, b = slope, c = constant and x = total shell height.

        The mean size at first maturity was estimated at a level of 50% of the relative accumulated frequency (Zetina 1999).

        Sex ratio and Intersex individuals

        Through macroscopic and microscopic observations, individuals were identified as either males or females and thereby an estimate of the sex ratio was obtained. When sex determination between macroscopic and microscopic examination did not agree, individuals were classified as in the intersex phase based on criteria used by Reed (1993) and Zetina (1999). At the macroscopic level, masculinized females present an atrophied penis which was smaller than that of normal males. An ovary was observed at the microscopic level. The feminized male had a gonopore with no macroscopic differences from that of a normal female, and microscopically they have a testis.

        Cispata Bay (Fig. 1) is located in the Department of Cordoba, on the Caribbean coast of Colombia, between 90[degrees]26' and 9[degrees]21'N and 57[degrees]54' and 75[degrees]45'W. The bay is located south of the Gulf of Morrosquillo. It has an irregular topography, is bordered by mangroves, and has estuarine waters with a mean depth of about 2 m. (Sanchez et al. 1997). Inland from the bay occur 12 sloughs which connect with it by channels (Fig. 1).

        The study area experiences four climatic seasons including, (a) the dry season from January through March, (b) transition to the rainy season from April through August, (c) the rainy season from September through November and (d) transition to the dry season in December. These seasons are affected by the Caribbean Current which flows from east to west and by the Darien Countercurrent, or Panama Current, which flows northward along the coast (Ramirez 1994). The tides are semidiurnal, with an amplitude of less than 1 m the annual mean temperature is 26.7[degrees]C and the annual precipitation is between 900 and 1200 mm (Patino & Flores 1993).

        A high proportion (>50%) of mature individuals (Stage III) were observed from January through September, except for the months of February, April, and June in which the proportion diminished (Fig. 2). Each peak of mature individuals was preceded and followed by maturing individuals (Stage II). Spawned individuals (Stage I) appeared almost throughout the year, with the exception of January and the period of August and September. Thus, spawning appears to occur between February and July, and then again in October, the month in which the greatest proportion of spent individuals appeared.

        The index of gonad maturity (IGM) increased from October to December, staying high for the rest of the year, but with smaller peaks in January, March, and August (Fig. 3). The gonad index (GI) showed March, June, and September as months with maximum gonad development (Fig. 4). Main reductions in the gonad index, suggesting spawning, were observed during October-November and March-April, and a smaller one in June (Fig. 4).

        The recruitment pattern, estimated using the growth parameters L[infinity] = 163 mm and K = 0.2 [y.sup.-1] estimated by Hernandez (2001), shows that individuals entered the population throughout the year with a maximum in March (Fig. 5). This coincided with the period of maximum maturity, according to the proportion of individuals in Stage III and highest IGM (Figs. 2 and 3). Recruitment throughout the year coincides with the observation that mature individuals occur for the entire year, existing no defined seasonal pattern of reproduction. A small peak was observed in March.

        Mean size at first maturity

        According to Figure 6a, 50% of males reached sexual maturity at 52 mm shell height such results fit the logistic model. It was thus estimated that all males were capable of reproduction at a size of 73 mm (Fig. 6a). Data for females also fitted the logistic model. Females became sexually mature shortly after the males at a shell height of 65 mm, with all females capable of reproduction at 77 mm (Fig. 6b). Spawned females 74-75 mm in height were identified in April.

        The sex ratio changed with age (Fig. 7). In the smallest size class (26.5 mm) females predominated, but only 8 individuals of that size class were examined. In the second analyzed size class (32.5 mm) males predominated and then tended to decline toward greater size classes (32.5-92.5 mm). In the greatest analyzed size class (98.5 mm) only females were found, but again, it was only a small sample (4 individuals) (Fig. 7).

        Few individuals (13) could be classified as in the intersex phase, representing only 4% of the 325 individual examined. Individuals with both male and female characteristics had both a gonopore and an incipient penis similar to normal males, although microscopic examination confirmed they were females (masculinized females) with normal developed ovaries. These individuals measured 40-70 mm in shell height (Table I). Microscopic observations confirmed that some individuals with a gonopore were males (feminized males), and these were 55 to 73 mm in shell height presenting a normal developed testis. All these individuals were classified as in the intersex phase.

        The coincidence between the major recruitment pulse and the maximum maturity, described by various methods (stages of maturity, IGM, GI) with also coincident results, suggest that the reproductive cycle described is reliable. While the peak of maturity occurs in the dry season, the presence of mature individuals throughout the year shows that variation between dry and rainy season seems to affect little, supporting a hypothesis of continuous reproduction and recruitment, a condition common in neotropical gastropods (Weber 1977). Rodriguez (1976) reported that in another area of the Caribbean, copulation by Melongena melongena occurred between December and July. These observations may have been biased by the methodology used by Rodriguez as they were based only on field observations where sampling days did not necessarily coincide with days when ovicapsules were present.

        Continuous spawning, beginning at early age, represents a favorable condition for M. melongena, which is subjected to an artisanal fishery. According to growth data (Hernandez 2001), M. melongena becomes sexually mature in its third year (at sizes between 52 and 65 mm). Nevertheless, the fishery is capturing individuals as small as 12 mm shell height, the main captures occurring from >40 mm, with an average size of 57 mm (Hernandez 2001). Thus, most of the fished snails have not reproduced prior to capture. This is a situations which needs to be revised and regulated to prevent overfishing of this resource, affecting recruitment and thus population renewal. That is unless the fishery is inefficient, and a great proportion of individuals of all sizes escape capture.

        As M. melongena appears to be gonochoric, the observation of intersex individuals generates doubts. The presence of such individuals confirms the observations of Rodriguez (1976), which, in agreement with the present study, reported masculinized females as occurring at sizes between 40 to 62 mm in shell height. For comparison, both feminized males and masculinized females were found in Cispata Bay, at a shell height range of between 40 and 73 mm.

        The decrease in the number of males with increasing size suggests the occurrence of consecutive hermaphroditism. Dominance by females is however frequent in populations of gonochoric molluscs, and becomes accentuated with increasing age, eventually generated by differential mortality (Fretter & Graham 1962, Gibbs et al. 1987). It has been found in populations of Nucella lapillus, affected by imposex, that the males are more abundant than females, as the latter suffer heavy mortality (Gibbs & Bryan, 1986 and Gibbs et al. 1987). But the identification of intersex individuals also points to the occurrence of hermaphroditism. This may however, be due to other specific causes such as those cited by Reed (1993) who indicated that sexual alternation in Strombus gigas could be due to abnormalities in the sex chromosomes. Horiuguchi et al. (1994) established that in neogastropods the development of male sex organs in females (termed "imposex") was a broad-scale problem described for numerous species. Gibbs et al. (1987) established that the presence of masculinized females in Nassarius obsoletus and Nucella lapillus could be produced by exposure of these species to toxic compounds present in antifouling paints such as tributylene and TBT (tributyltin chloride). Exposure to these pollutants of females of these species destroys the oviduct, suppresses oogenesis, and results in the development of a testis. The females become unable to reproduce and the population declines as a result (Gibbs & Bryan 1986). According to Horiuguchi et al. (1994), the degree of imposex in Thais clavigera and T. bronni, as indicated by the length of the penis, provides a rough estimate of TBT levels in the environment.

        Event though, the change in sexual proportion with size and the existence of few intersex individuals suggests the occurrence of protandric hermaphroditism in M. melongena, the evidence is weak. If the occurrence of protandric hermaphtoditism is true, however, the fishery for M. melongena may be interfering seriously with reproduction, as the individuals are not allowed to reach the larger sizes. This needs to be further studied, following over time the same individuals., to determine if changes in sexual proportion with size and intersex individuals are really evidence of protandric hermaphroditism, or result from other causes.

        We are grateful to Hanne Cogolio and Jesus Cantillo for help in field sampling, and to the snail collectors, especially "Tanque". We are also thankful for logistical support provided by Luz Marina Arias, Chief of the INPA office in Cordoba, and to Evila Jarava Ossa for her collaboration. Further thanks are extended to the personnel of the Amaya Research Station, to Marisol Romero of the U.Catolica del Norte, Coquimbo, for guidance in the histological interpretation of M. melongena gonads and to Piedad Victoria for review and edition of the Spanish text of this MS. We add final thanks to Adriana Zetina, Cristian Aycaguer and C. D'Asaro for sending reprints of their research which were important to our preparation of this MS. Two anonymous reviewers are acknowledged for their comments, which helped to improve the manuscript.

        Abbott, R. T. (1974) American seashells. Van Nostraa. New York. 663 pp.

        Bowling, C. 1994. Habitat and size of the Florida crown conch (Melongena corona Gmelin) Why big snails hang out at bars. J. Exp. Mar. Biol. Ecol. 175:181-195.

        Castagna, M. & J. N. Kraeuter. 1994. Age, growth rate, sexual dimorphism and fecundity of knobbed whelk Busycon carica (Gmelin, 1791) in the western mid-Atlantic lagoon system, Virginia. Journal of Shellfish Research. 13(2):581-585.

        Clench, W. J. & R. D. Turner. 1956. The family Melongenidae in the western Atlantic. Johnsonia 3(35): 161-188.

        Cosel van. R. 1986. Moluscos de la region de la Cienaga Grande de Santa Marta (Costa Caribe colombiano) Ann. Inst. Inv. Mar. Punta de Betin (15-16):79-370

        Dalby, J. E. 1989. Predation of ascidians by Melongena corona (Neogasteropoda: Melongenidae) in the northern Gulf of Mexico. Bull. Mar. Sci. 45(3):708-712.

        D'Asaro, Ch. N. 1997. Gunnar Thorson's world-wide collection of prosobranch egg capsules: Melongenidae. Ophelia 46(2):83-125.

        Diaz, J. M. & M. Puyana 1994. Moluscos del Caribe colombiano. Un catalogo de ilustraciones. Colciencias. Fundacion Natura. Invemar. 291 pp. mas laminas.

        Flores, F. P. 1980. Aspectos biologicos y ecologicos de Melongena melongena y Melongena corona (Mollusca:Gasteropoda) en la laguna de Terminos Campeche. Mexico. Tesis de Grado. Universidad Nacional Autonoma de Mexico Mexico. 31 pp.

        Fretter, V. & A. Graham. 1962. The reproductive system 1 y 2. Their functional anatomy and ecology. In: British Prosobranch Molluscs. Printed for the Ray Society. London.

        Gallardo, C. S. 1989. Patrones de reproduccion y ciclo vital en moluscos marinos bentonicos, una aproximacion ecologico evolutiva. Medio Ambiente 10(2):25-35.

        Gayanilo, F. C., Jr. & D. Pauly (eds). 1997. FAO-ICLARM Stock Assesment Tools (FiSAT). Reference manual. FAO Computerized Information Series (Fisheries) No. 8. Rome, FAO. 262 pp.

        Gibbs, P. E. & G. W. Bryan. 1986. Reproductive failure in populations of the dog-whelk, Nucella lapillus. Caused by imposex induced by tributylin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 66:767-777.

        Gibbs, P. E., G. W. Bryan, P. L. Pascoe & G. R. Burt. 1987. The use of the dog--whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. Journal of the Marine Biological Association of the United Kingdom 67:507-523.

        Hathaway, R. & K. D. Woodburn. 1961. Studies on the crown conch Melongena corona Gmelin. Bulletin of Marine Sciences. Gulf and Caribbean. 11(1):45-65.

        Hawkins, F. 1973. Contribucion al estudio biologico de Anomalocardia brasiliana chipichipi en la Cienaga de Tesca. Bahia de Cartagena. Tesis de Grado U.J.T.L. Bogota.

        Hernandez, S. 2001. Evaluacion de la poblacion del Caracol Copey Melongena melongena (Linne, 1758) y su pesqueria en la Bahia Cispata, Caribe Colombiano. Tesis para optar al Grado de Magister, Facultad de Ciencias del Mar, Universidad Catolica del Norte, Coquimbo, Chile.

        Horiuguchi, T., H. Shiraishi, M. Shimizu & M. Morita. 1994. Imposex and organotin compounds in Thais clavigera and T, bronni in Japan. Journal of the Marine Biological Association of the United Kingdom 74: 651-669.

        Morton, B. 1986. Reproduction, juvenile growth, consumption and the effects of starvation upon of the South China Sea whelk Hemifusus tuba (Gmelin) (Prosobrancia: Melongenidae). Journal of Experimental Marine Biology and Ecology. 102:257-280.

        Patino, F. & F. Flores. 1993. Estudio ecologico del Golfo de Morrosquillo. Univ. Nacional. Colombia Fondo FEN., 109 pp.

        Ramirez, A. 1994. Introduccion a la biologia pesquera del Golfo de Morrosquillo y su relacion con los ecosistemas naturales. Informe Final Ecopetrol. Distrito Cano Limon-Covenas 155 pp.

        Ramorino, L. 1975. Ciclo reproductivo de Concholepas concholepas en la zona de Valparaiso. Revista de Biologia Marina, Valparaiso 13(2): 149-177.

        Reed, S. E. 1993. Gonadal comparison of masculinized females and androgynous males to normal males and females in Strombus gigas (Mesogastropoda: Strombidae). Journal of Shellfish Research 12(1):71-75.

        Rodriguez, H. 1976. Algunos aspectos de la biologia de Melongena melongena (Linne, 1758) (Gasteropoda:Prosobranchia) en la zona de Castillo Grande. Bahia de Cartagena. Tesis de Grado U.J.T.L. Bogota.

        Sanchez, H., R. Alvarez, F. Pinto, A. Soledad, J. C. Pino, F. Garcia & M. T. Acosta. 1997. Diagnostico y zonificacion preliminar de los manglares del Caribe de Colombia. Republica de Colombia. Ministerio del Medio Ambiente, Direccion General Forestal y de Vida Silvestre. Organizacion Internacional de Maderas Tropicales. Direccion de Proyectos de repoblacion y Ordenacion Forestal. Bogota. 511 pp.

        Villareal, G. 1989. Impacto de la depredacion por Melongena melongena (L) sobre la poblacion del ostion Crassostrea virginica (Gmelin) en la laguna de Tampamachoco. Veracruz. Cienc. Mar. 15(2):55-65.

        Weber, H. H. 1977. Gastropoda: prosobranchia In Giese A.C. and I.S. Pearse (eds): Reproduction of Marine Invertebrates Vol IV Molluscs: Gastropods and Cephalopods, Academic Press, New York, 83 pp.

        Woodbury, B. D. 1986. The role of growth, predation and habitat selection, the population distribution of the crown conch Melongena corona. Journal of Experimental Marine Biology and Ecology 97:1-12.

        Zetina, A. I. 1999. Biologia reproductora del caracol "chivita" Melongena corona bispinosa (Philippi, 1844) (Mollusca Neogastropoda Melongenidae) de la Cienaga de Chuburna, Yucatan, Mexico. Tesis de Maestria en Ciencias, Centro de Investigaciones y de Estudios Avanzados del Instituto Politecnico Nacional Unidad Merida, Dpto Recursos del Mar, Mexico, 71 pp.


        Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.4996610.

        Published by the Royal Society. All rights reserved.

        References

        2015 Cellular chirality arising from the self-organization of the actin cytoskeleton . Nat. Cell Biol. 17, 445-457. (doi:10.1038/ncb3137) Crossref, PubMed, ISI, Google Scholar

        2016 Formin is associated with left–right asymmetry in the pond snail and the frog . Curr. Biol. 26, 654-660. (doi:10.1016/j.cub.2015.12.071) Crossref, PubMed, ISI, Google Scholar

        Vandenberg LN, Lemire JM, Levin M

        . 2013 It's never too early to get it right: a conserved role for the cytoskeleton in left–right asymmetry . Commun. Integr. Biol. 6, e27155. (doi:10.4161/cib.27155) Crossref, PubMed, Google Scholar

        . 2020 Flipping shells: unwinding LR asymmetry in mirror-image molluscs . Trends Genet. 36, 189-202. (doi:10.1016/j.tig.2019.12.003) Crossref, PubMed, ISI, Google Scholar

        Felix MA, Sternberg PW, Ley PD

        . 1996 Sinistral nematode population . Nature 381, 122. (doi:10.1038/381122a0) Crossref, ISI, Google Scholar

        . 2008 Nodal signalling is involved in left–right asymmetry in snails . Nature 405, 1007-1011. (doi:10.1038/nature07603) Google Scholar

        Hoso M, Kameda Y, Wu S-P, Asami T, Kato M, Hori M

        . 2010 A speciation gene for left–right reversal in snails results in anti-predator adaptation . Nat. Commun. 1, ncomms1133. (doi:10.1038/ncomms1133) Crossref, ISI, Google Scholar

        Schilthuizen M, Craze PG, Cabanban AS, Davison A, Stone J, Gittenberger E, Scott BJ

        . 2007 Sexual selection maintains whole-body chiral dimorphism in snails . J. Evol. Biol. 20, 1941-1949. (doi:10.1111/j.1420-9101.2007.01370.x) Crossref, PubMed, ISI, Google Scholar

        Richards PM, Morii Y, Kimura K, Hirano T, Chiba S, Davison A

        . 2017 Single-gene speciation: mating and gene flow between mirror-image snails . Evol. Lett. 1, 282-291. (doi:10.1002/evl3.31) Crossref, PubMed, ISI, Google Scholar

        Davison A, Chiba S, Barton NH, Clarke BC

        . 2005 Speciation and gene flow between snails of opposite chirality . PLoS Biol. 3, e282. (doi:10.1371/journal.pbio.0030282) Crossref, PubMed, ISI, Google Scholar

        . 2003 Single-gene speciation by left–right reversal. A land-snail species of polyphyletic origin results from chirality constraints on mating . Nature 425, 679. (doi:10.1038/425679a) Crossref, PubMed, ISI, Google Scholar

        . 1923 On the inheritance of sinistrality in Limnaea peregra . Proc. R. Soc. Lond. B 95, 207-213. (doi:10.1098/rspb.1923.0033) Link, Google Scholar

        . 1923 Inheritance of direction of coiling in Limnaea . Science 58, 269-270. (doi:10.1126/science.58.1501.269) Crossref, PubMed, Google Scholar

        . 2005 Sinistral snails and gentlemen scientists . Cell 123, 751-753. (doi:10.1016/j.cell.2005.11.015) Crossref, PubMed, ISI, Google Scholar

        . 2005 The convoluted evolution of snail chirality . Naturwissenschaften 92, 504-515. (doi:10.1007/s00114-05-0045-2) Crossref, PubMed, ISI, Google Scholar

        . 2019 The development of CRISPR for a mollusc establishes the formin Lsdia1 as the long-sought gene for snail dextral/sinistral coiling . Development 146, dev.175976. (doi:10.1242/dev.175976) Crossref, ISI, Google Scholar

        . 2020 Response to ‘Formin, an opinion’ . Development (Camb) 147, dev187435. (doi:10.1242/dev.187435) Crossref, PubMed, Google Scholar

        Davison A, McDowell GS, Holden JM, Johnson HF, Wade CM, Chiba S, Jackson DJ, Levin M, Blaxter ML

        . 2020 Formin, an opinion . Development 147, dev187427. (doi:10.1242/dev.187427) Crossref, PubMed, ISI, Google Scholar

        . 2019 Heterochirality results from reduction of maternal diaph expression in a terrestrial pulmonate snail . Zool. Lett. 5, 2. (doi:10.1186/s40851-018-0120-0) Crossref, PubMed, ISI, Google Scholar

        Davison A, Barton NH, Clarke B

        . 2009 The effect of coil phenotypes and genotypes on the fecundity and viability of Partula suturalis and Lymnaea stagnalis: implications for the evolution of sinistral snails . J. Evol. Biol. 22, 1624-1635. (doi:10.1111/j.1420-9101.2009.01770.x) Crossref, PubMed, ISI, Google Scholar

        . 2010 Maternal inheritance of racemism in the terrestrial snail Bradybaena similaris . J. Hered. 101, 11-19. (doi:10.1093/jhered/esp058) Crossref, PubMed, ISI, Google Scholar

        Utsuno H, Asami T, Van Dooren TJM, Gittenberger E

        . 2011 Internal selection against the evolution of left–right reversal . Evolution 65, 2399-2411. (doi:10.1111/j.1558-5646.2011.01293.x) Crossref, PubMed, ISI, Google Scholar

        Asami T, Cowie RH, Ohbayashi K

        . 1998 Evolution of mirror images by sexually asymmetric mating behavior in hermaphroditic snails . Am. Nat. 152, 225-236. (doi:10.1086/286163) Crossref, PubMed, ISI, Google Scholar

        Davison A, Frend HT, Moray C, Wheatley H, Searle LJ, Eichhorn MP

        . 2009 Mating behaviour in Lymnaea stagnalis pond snails is a maternally inherited, lateralised trait . Biol. Lett. 5, 20-22. (doi:10.1098/rsbl.2008.0528) Link, ISI, Google Scholar

        . 1979 Courtship of lands snails of the genus Partula . Malacologia 19, 129-146. ISI, Google Scholar

        . 1860 On the origin of species . Ann. Mag. Nat. Hist. VI, 152. (doi:10.1080/00222936008697297) Crossref, Google Scholar

        . 1920 Les Variations et leur Hérédité chez les Mollusques. Classe des Sciences, Collection in-8°. Série II. Bruxelles, Belgium : l'Académic Royale de Belgique . Crossref, Google Scholar

        . 2016 Snail chirality: the unwinding . Curr. Biol. 26, R215-R217. (doi:10.1016/j.cub.2016.02.008) Crossref, PubMed, ISI, Google Scholar

        Ward-Fear G, Pauly GB, Vendetti JE, Shine R

        . 2020 Authorship protocols must change to credit citizen scientists . Trends Ecol. Evol. 35, 187-190. (doi:10.1016/j.tree.2019.10.007) Crossref, PubMed, ISI, Google Scholar

        . 2018 Left–right asymmetry: myosin 1D at the center . Curr. Biol. 28, R567-R569. (doi:10.1016/j.cub.2018.03.019) Crossref, PubMed, ISI, Google Scholar

        . 2000 The inheritance of divergent mitochondria in the land snail, Cepaea nemoralis . J. Moll. Stud. 66, 143-147. (doi:10.1093/mollus/66.2.143) Crossref, ISI, Google Scholar

        . 1982 The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra . Roux Arch. Dev. Biol. 191, 69-83. (doi:10.1007/BF00848443) Crossref, Google Scholar

        . 1980 The genus Partula on Moorea: speciation in progress . Proc. R. Soc. Lond. B 211, 83-117. (doi:10.1098/rspb.1980.0159) Link, ISI, Google Scholar

        . 1952 Der erbgang der inversion bei Laciniaria biplicata MTG (Gastr Pulm) . Mitt. Hambg. Zool. Mus. Inst. 51, 3-61. Google Scholar

        . 1966 The inheritance of polymophic shell characters in Partula (Gastropoda) . Genetics 54, 1261-1277. PubMed, ISI, Google Scholar

        Kuroda R, Endo B, Abe M, Shimizu M

        . 2009 Chiral blastomere arrangement dictates zygotic left–right asymmetry pathway in snails . Nature 462, 790-794. (doi:10.1038/nature08597) Crossref, PubMed, ISI, Google Scholar

        Bantock CR, Noble K, Ratsey M

        . 1973 Sinistrality in Cepaea hortensis . Heredity 30, 397-398. (doi:10.1038/hdy.1973.48) Crossref, ISI, Google Scholar

        . 2016 What determines direction of asymmetry: genes, environment or chance? Phil. Trans. R Soc. B. 371, 20150417. (doi:10.1098/rstb.2015.0417) Link, ISI, Google Scholar

        Wade CM, Hudelot C, Davison A, Mordan PB

        . 2008 Molecular phylogeny of the helicoid land snails (Pulmonata: Stylommatophora: Helicoidea) . J. Moll. Stud. 73, 411-415. (doi:10.1093/mollus/eym030) Crossref, ISI, Google Scholar

        . 1924 The coincident production of dextral and sinistral young in the land-gastropod Partula . Science 59, 558-559. (doi:10.1126/science.59.1538.558) Crossref, PubMed, Google Scholar

        . 1938 Sinistrality in Limnaea peregra (Mollusca, Pulmonata): the problem of mixed broods . J. Genet. 35, 447-525. (doi:10.1007/BF02982368) Crossref, Google Scholar

        . 1987 Adaptation and rules of form: chirality and shape in Partula suturalis . Evolution 41, 672-675. (doi:10.1111/j.1558-5646.1987.tb05839.x) Crossref, PubMed, ISI, Google Scholar

        . 2010 Disentangling true shape differences and experimenter bias: are dextral and sinistral snail shells exact mirror images? J. Zool. 282, 191-200. (doi:10.1111/j.1469-7998.2010.00729.x) Crossref, PubMed, ISI, Google Scholar

        Gould SJ, Young ND, Kasson B

        . 1985 The consequences of being different: sinistral coiling in Cerion . Evolution 39, 1364-1379. (doi:10.1111/j.1558-5646.1985.tb05701.x) Crossref, PubMed, ISI, Google Scholar

        Davison A, Constant N, Tanna H, Murray J, Clarke B

        . 2009 Coil and shape in Partula suturalis: the rules of form revisited . Heredity 103, 268-278. (doi:10.1038/hdy.2009.49) Crossref, PubMed, ISI, Google Scholar

        Sutcharit C, Asami T, Panha S

        . 2007 Evolution of whole-body enantiomorphy in the tree snail genus Amphidromus . J. Evol. Biol. 20, 661-672. (doi:10.1111/j.1420-9101.2006.01246.x) Crossref, PubMed, ISI, Google Scholar


        Formerly Benign

        Roughly 15 percent of animal species live a hermaphroditic lifestyle of some form, Michiels estimates. Many of them are sequential hermaphrodites, such as clown fish that spend their young adulthood as one gender and then switch to the other. Among the animals that are simultaneously male and female, Michiels distinguishes between hermaphrodites where partners make contact to achieve internal fertilization and those in which at least one of the partners releases a cloud of gametes, so the partners don’t themselves make physical contact. According to Michiels, the fertilizers without partner contact are less likely to careen into a violent conflict than are hermaphrodites with full-contact internal fertilization.

        For years, biologists didn’t think much about sexual conflict, even in species with separate sexes, says Nils Anthes, also of Tübingen. Mating seemed “benign,” as Anthes puts it. Both males and females have urges for offspring, so at first glance, producing youngsters should be a happy, family project.

        That rosy view began fading in 1948, when fruit fly researcher Angus John Bateman of England argued that males invest much less energy in producing offspring than females do. That investment gap suggested that the best reproductive strategy for one sex isn’t equally good for the other. Bateman argued that the average male would do well to mate as widely as possible, while a female should be particular about whose sperm she accepts. What could make better tinder for conflict between the sexes?

        In 1979, theorist Eric Charnov, now at the University of New Mexico in Albuquerque , proposed that these ideas could apply to simultaneous hermaphrodites. For example, conflicts could arise as individuals of those species sort out when to play each sexual role.

        For years, theorists assumed that tactics in the hermaphrodite gender war would be fairly consistent within an individual or even a species, says Anthes. However, in the July Animal Behaviour, Michiels, Anthes, and Annika Putz, offer what they call a new framework for thinking about hermaphrodites. It urges theorists to compare his and hers benefits under changeable, thus realistic, conditions. Strategies could vary, for example, with the characteristics of available partners. In another paper, Michiels and Anthes report that sea slugs donate more sperm to a partner that’s been isolated than to one that’s recently mated and so already carries plenty of sperm.


        Methods

        The genetic material used for sequencing the genome of the hermaphroditic freshwater snail Biomphalaria glabrata was derived from three snails of the BB02 strain (shell diameter 8, 10 and 12 mm, respectively), established at the University of New Mexico, USA from a field isolate collected from Minas Gerais, Brazil, 2002 (ref. 8). Using a genome size estimate of 0.9–1 Gb (ref. 7), we sequenced fragments (450 bp read length 14.08 × coverage) and paired ends from 3 kb long inserts (8.12 × ) and 8 kb long inserts (2.82 × ) with reads generated on Roche 454 instrumentation, plus 0.06 × from bacterial artificial chromosome (BAC) ends 8 on the ABI3730xl. Reads were assembled using Newbler (v2.6) 51 . Paired end reads from a 300 bp insert library (53.42 × coverage) were collected using Illumina instrumentation and assembled de novo using SOAP (v1.0.5) 52 . The Newbler assembly was merged with the SOAP assembly using GAA 53 (see Supplementary Data 1 for accession numbers of sequence data sets). Redundant contigs in the merged assembly were collapsed and gaps between contigs were closed through iterative rounds of Illumina mate-pair read alignment and extension using custom scripts. We removed from the assembly all contaminating sequences, trimmed vectors (X), and ambiguous bases (N). Short contigs (≤200 bp) were removed prior to public release. In the creation of the linkage group AGP files, we identified all scaffolds (145 Mb total) that were uniquely placed in a single linkage group (Supplementary Note 2 Supplementary Data 2). Note that because of low marker density, scaffolds could not be ordered or oriented within linkage groups. The final draft assembly (NCBI: ASM45736v1) is comprised of 331,400 scaffolds with an N50 scaffold length of 48 kb and an N50 contig length of 7.3 kb. The assembly spans over 916 Mb (with a coverage of 98%, 899 Mb of sequence with ∼ 17 Mb of estimated gaps). The draft genome sequence of Biomphalaria glabrata was aligned with assemblies of Lottia and Aplysia (http://biology.unm.edu/biomphalaria-genome/synteny.html) and deposited in the DDBJ/EMBL/GenBank database (Accession Number APKA00000000.1). It includes the genomes of an unclassified mollicute (Supplementary Note 7 accession numbers CP013128). The genome assembly was also deposited in Vectorbase 54 (https://www.vectorbase.org/organisms/biomphalaria-glabrata). Computational annotation using Maker2 (ref. 9) yielded 14,423 predicted gene models, including 96.5% of the 458 sequences from the CEGMA core set of eukaryotic genes 55 . Total RNA was extracted from 12 different tissues/organs dissected from several individual adult BB02 B. glabrata snails (shell diameter 10–12 mm between 2 and 10 snails per sample to obtain sufficient amounts of RNA). RNA was reverse transcribed using random priming, no size selection was done. Illumina RNAseq (paired ends) was used to generate tissue-specific transcriptomes for albumen gland (AG) buccal mass (BUC) central nervous system (CNS) digestive gland/hepatopancreas (DG/HP) muscular part of the headfoot (FOOT) heart including amebocyte producing organ (HAPO) kidney (KID) mantle edge (MAN) ovotestis (OVO) salivary gland (SAL) stomach (STO) terminal genitalia (TRG), see Supplementary Data 1 for accession numbers of sequence data sets. RNAseq data were mapped to the genome assembly (Supplementary Note 3). No formal effort was made to use the RNA-data to systematically enhance the structural annotation. VectorBase did, however, make this RNAseq data available in WebApollo 56 such that the community could use these data to correct exon-intron junctions, UTRs, etc. through community annotation. All of these community-based updates have been incorporated and are available via the current VectorBase gene set. Repeat features were analyzed and masked (Supplementary Note 32 see Vectorbase Biomphalaria-glabrata-BB02_REPEATS.lib, Biomphalaria-glabrata-BB02_REPEATFEATURES_BglaB1.gff3.gz). Further methods and results are described in the Supplementary Information.

        Data availability

        The sequence data that support the findings of this study have been deposited in GenBank with the accession codes SRX005826, -27, -28 SRX008161, -2 SRX648260, -61, -62, -63, -64, -65, -66, -67, -68, -69, -70, -71 SRA480937 SRA480939 SRA480940 SRA480945 TI accessions2091872204-2092480271 2104228958-2104243968 2110153721-2118515136 2181062043-2181066224 2193113537-2193116528 2204642410-2204763511 2204820860-2204852286 2213009530-2213057324 2260448774-2260450167. Also see Supplementary Data 1. The assembly and related data are available from VectorBase, https://www.vectorbase.org/organisms/biomphalaria-glabrata. The Biomphalaria glabrata genome project has been deposited at DDBJ/EMBL/GenBank under the accession number APKA00000000.1


        Watch the video: Γιατί δεν πρέπει να μαζεύουμε σαλιγκάρια με τα πρωτοβρόχια. AlphaNews (January 2022).