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Datasheet

Pomacea maculata

Summary

  • Last modified
  • 23 November 2017
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Pomacea maculata
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Mollusca
  •       Class: Gastropoda
  •         Subclass: Caenogastropoda
  • Summary of Invasiveness
  • P. maculata is a freshwater snail native to a wide geographical area in South America from the Rio de la Plata in Argentina and Uruguay to the Amazon in Brazil. It is commonly confused with any number of simila...

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Pictures

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PictureTitleCaptionCopyright
Pomacea maculata (island apple snail); laying a clutch of eggs in the early morning. Armand Bayou Nature Center, Houston, Texas. USA. August, 2008.
TitleSnail ovipositing
CaptionPomacea maculata (island apple snail); laying a clutch of eggs in the early morning. Armand Bayou Nature Center, Houston, Texas. USA. August, 2008.
Copyright©Romi L. Burks-2008
Pomacea maculata (island apple snail); laying a clutch of eggs in the early morning. Armand Bayou Nature Center, Houston, Texas. USA. August, 2008.
Snail ovipositingPomacea maculata (island apple snail); laying a clutch of eggs in the early morning. Armand Bayou Nature Center, Houston, Texas. USA. August, 2008.©Romi L. Burks-2008
Pomacea maculata (island apple snail); aperture view of large shell that has been cleaned and briefly bleached.  The lip of the shell prominently displays the characteristic orange color that helps distinguish this species.
TitleShell
CaptionPomacea maculata (island apple snail); aperture view of large shell that has been cleaned and briefly bleached. The lip of the shell prominently displays the characteristic orange color that helps distinguish this species.
Copyright©Amy E. Miller-2013
Pomacea maculata (island apple snail); aperture view of large shell that has been cleaned and briefly bleached.  The lip of the shell prominently displays the characteristic orange color that helps distinguish this species.
ShellPomacea maculata (island apple snail); aperture view of large shell that has been cleaned and briefly bleached. The lip of the shell prominently displays the characteristic orange color that helps distinguish this species.©Amy E. Miller-2013
Pomacea maculata (island apple snail); lateral view of seven  shells arranged by increasing size. The second and third shells represent early and late juveniles, respectively, as described in Burks et al. (2011).  (Note scale)
TitleShell size
CaptionPomacea maculata (island apple snail); lateral view of seven shells arranged by increasing size. The second and third shells represent early and late juveniles, respectively, as described in Burks et al. (2011). (Note scale)
Copyright©Amy E. Miller-2013
Pomacea maculata (island apple snail); lateral view of seven  shells arranged by increasing size. The second and third shells represent early and late juveniles, respectively, as described in Burks et al. (2011).  (Note scale)
Shell sizePomacea maculata (island apple snail); lateral view of seven shells arranged by increasing size. The second and third shells represent early and late juveniles, respectively, as described in Burks et al. (2011). (Note scale)©Amy E. Miller-2013
Pomacea maculata (island apple snail); the increasing thickness of opercula as the snail increases in age and size.
TitleOpercula size
CaptionPomacea maculata (island apple snail); the increasing thickness of opercula as the snail increases in age and size.
Copyright©Amy E. Miller-2013
Pomacea maculata (island apple snail); the increasing thickness of opercula as the snail increases in age and size.
Opercula sizePomacea maculata (island apple snail); the increasing thickness of opercula as the snail increases in age and size.©Amy E. Miller-2013
Pomacea maculata (island apple snail); mating pair. Punta Gorda, Uruguay.
TitleMating pair
CaptionPomacea maculata (island apple snail); mating pair. Punta Gorda, Uruguay.
Copyright©Romi L. Burks-2014
Pomacea maculata (island apple snail); mating pair. Punta Gorda, Uruguay.
Mating pairPomacea maculata (island apple snail); mating pair. Punta Gorda, Uruguay.©Romi L. Burks-2014
Pomacea maculata (island apple snail); recently dislodged male and female mating pair, with visible male organ extended. Houston, Texas, USA. September, 2011.
TitleMating pair
CaptionPomacea maculata (island apple snail); recently dislodged male and female mating pair, with visible male organ extended. Houston, Texas, USA. September, 2011.
Copyright©Romi L. Burks-2011
Pomacea maculata (island apple snail); recently dislodged male and female mating pair, with visible male organ extended. Houston, Texas, USA. September, 2011.
Mating pairPomacea maculata (island apple snail); recently dislodged male and female mating pair, with visible male organ extended. Houston, Texas, USA. September, 2011.©Romi L. Burks-2011
Pomacea maculata (island apple snail); numerous egg clutches laid on wild taro (Colocasia esculenta). August, 2008.
TitleEgg clutches
CaptionPomacea maculata (island apple snail); numerous egg clutches laid on wild taro (Colocasia esculenta). August, 2008.
Copyright©Romi L. Burks-2008
Pomacea maculata (island apple snail); numerous egg clutches laid on wild taro (Colocasia esculenta). August, 2008.
Egg clutchesPomacea maculata (island apple snail); numerous egg clutches laid on wild taro (Colocasia esculenta). August, 2008.©Romi L. Burks-2008
Pomacea maculata (island apple snail); newly collected, medium-sized specimens, laying pink egg clutches.
TitleOviposition
CaptionPomacea maculata (island apple snail); newly collected, medium-sized specimens, laying pink egg clutches.
Copyright©Romi L. Burks-2011
Pomacea maculata (island apple snail); newly collected, medium-sized specimens, laying pink egg clutches.
OvipositionPomacea maculata (island apple snail); newly collected, medium-sized specimens, laying pink egg clutches.©Romi L. Burks-2011
Pomacea maculata (island apple snail); egg clutches aligned in order based on developmental stage: (a) represents a recently laid set of eggs with a gelatinous nature as seen from a dorsal viewpoint.  (b) what clutches look like after they have approximately 2 days to fully dry and set.  (c) after one week, the pink eggs in the clutches transition to gray. (d) grey color eventually yields to white when the clutch will soon hatch. (e) shows small brown hatchlings ready to leave the clutch.
TitleEgg clutches
CaptionPomacea maculata (island apple snail); egg clutches aligned in order based on developmental stage: (a) represents a recently laid set of eggs with a gelatinous nature as seen from a dorsal viewpoint. (b) what clutches look like after they have approximately 2 days to fully dry and set. (c) after one week, the pink eggs in the clutches transition to gray. (d) grey color eventually yields to white when the clutch will soon hatch. (e) shows small brown hatchlings ready to leave the clutch.
Copyright©Amy E. Miller-2013
Pomacea maculata (island apple snail); egg clutches aligned in order based on developmental stage: (a) represents a recently laid set of eggs with a gelatinous nature as seen from a dorsal viewpoint.  (b) what clutches look like after they have approximately 2 days to fully dry and set.  (c) after one week, the pink eggs in the clutches transition to gray. (d) grey color eventually yields to white when the clutch will soon hatch. (e) shows small brown hatchlings ready to leave the clutch.
Egg clutchesPomacea maculata (island apple snail); egg clutches aligned in order based on developmental stage: (a) represents a recently laid set of eggs with a gelatinous nature as seen from a dorsal viewpoint. (b) what clutches look like after they have approximately 2 days to fully dry and set. (c) after one week, the pink eggs in the clutches transition to gray. (d) grey color eventually yields to white when the clutch will soon hatch. (e) shows small brown hatchlings ready to leave the clutch.©Amy E. Miller-2013
Pomacea maculata (island apple snail); the visual perspective of a tiny (ca.1mm) hatchling starting out on its own in a sea of pink egg-mass.
TitleHatchling
CaptionPomacea maculata (island apple snail); the visual perspective of a tiny (ca.1mm) hatchling starting out on its own in a sea of pink egg-mass.
Copyright©Romi L. Burks-2014
Pomacea maculata (island apple snail); the visual perspective of a tiny (ca.1mm) hatchling starting out on its own in a sea of pink egg-mass.
HatchlingPomacea maculata (island apple snail); the visual perspective of a tiny (ca.1mm) hatchling starting out on its own in a sea of pink egg-mass.©Romi L. Burks-2014
'Snail Busters' apple snail trap as deployed in shallow water
Title'Snail Busters' apple snail trap
Caption'Snail Busters' apple snail trap as deployed in shallow water
Copyright©Jess van Dyke
'Snail Busters' apple snail trap as deployed in shallow water
'Snail Busters' apple snail trap'Snail Busters' apple snail trap as deployed in shallow water©Jess van Dyke
Snail Busters apple snail trap as delivered for deployment to control apple snails.  The traps use bait to attract adults into the contraption.
Title'Snail Busters' apple snail trap
CaptionSnail Busters apple snail trap as delivered for deployment to control apple snails. The traps use bait to attract adults into the contraption.
Copyright©Jess van Dyke
Snail Busters apple snail trap as delivered for deployment to control apple snails.  The traps use bait to attract adults into the contraption.
'Snail Busters' apple snail trapSnail Busters apple snail trap as delivered for deployment to control apple snails. The traps use bait to attract adults into the contraption.©Jess van Dyke
Radular morphology of Pomacea maculata (a & c) and Pomacea canaliculata (b & d). c & d are rachidian teeth.  All scale bars = 100 µm.
TitleRadular morphology of Pomacea maculata and Pomacea canaliculata
CaptionRadular morphology of Pomacea maculata (a & c) and Pomacea canaliculata (b & d). c & d are rachidian teeth. All scale bars = 100 µm.
Copyright©Kenneth A. Hayes
Radular morphology of Pomacea maculata (a & c) and Pomacea canaliculata (b & d). c & d are rachidian teeth.  All scale bars = 100 µm.
Radular morphology of Pomacea maculata and Pomacea canaliculata Radular morphology of Pomacea maculata (a & c) and Pomacea canaliculata (b & d). c & d are rachidian teeth. All scale bars = 100 µm.©Kenneth A. Hayes
Pomacea maculata critical point-dried penial sheath, showing two glands on the dorsal surface. Key = Green: apical sheath gland; Orange: basal penis sheath gland; Blue: penis bulb and penis pouch; Purple: prostate. Reproduced from Hayes et al. (2012).
TitlePenial sheath; Pomacea maculata
CaptionPomacea maculata critical point-dried penial sheath, showing two glands on the dorsal surface. Key = Green: apical sheath gland; Orange: basal penis sheath gland; Blue: penis bulb and penis pouch; Purple: prostate. Reproduced from Hayes et al. (2012).
Copyright©Kenneth A. Hayes
Pomacea maculata critical point-dried penial sheath, showing two glands on the dorsal surface. Key = Green: apical sheath gland; Orange: basal penis sheath gland; Blue: penis bulb and penis pouch; Purple: prostate. Reproduced from Hayes et al. (2012).
Penial sheath; Pomacea maculata Pomacea maculata critical point-dried penial sheath, showing two glands on the dorsal surface. Key = Green: apical sheath gland; Orange: basal penis sheath gland; Blue: penis bulb and penis pouch; Purple: prostate. Reproduced from Hayes et al. (2012).©Kenneth A. Hayes

Identity

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Preferred Scientific Name

  • Pomacea maculata Perry, 1810

Other Scientific Names

  • Ampullaria amazonica Reeve, 1856
  • Ampullaria castelnaudii Hupé, 1857
  • Ampullaria crosseana Hidalgo, 1871
  • Ampullaria georgii Williams, 1889
  • Ampullaria gigas Spix in Wagner, 1827
  • Ampullaria haustrum Reeve, 1856
  • Ampullaria immersa Reeve, 1856
  • Ampullaria insularum d’Orbigny, 1835
  • Ampullaria vermiformis Reeve, 1856
  • Pomacea amazonica (Reeve, 1856)
  • Pomacea castelnaudii (Hupé, 1857)
  • Pomacea gigas (Spix in Wagner, 1827)
  • Pomacea haustrum (Reeve, 1856)
  • Pomacea insularum (d’Orbigny, 1835)

International Common Names

  • English: Channeled apple snail; golden apple snail

Local Common Names

  • USA: Giant apple snail; island apple snail

Summary of Invasiveness

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P. maculata is a freshwater snail native to a wide geographical area in South America from the Rio de la Plata in Argentina and Uruguay to the Amazon in Brazil. It is commonly confused with any number of similar large apple snails, including the well-known invasive golden apple snail Pomacea canaliculata (listed among ‘100 of the world’s worst invasive species’). Both species have been introduced to South-East and East Asia, although for many years they were not distinguished and the Asian introductions were widely identified as “golden apple snails” and the name P. canaliculata was applied to them. Due to the confusion in species identification, the history of introduction of P. maculata remains somewhat uncertain as does its invasiveness and pest potential. Much of the literature is confounded, for example, the snails illustrated by Cowie (2002) as P. canaliculata are in fact P. maculata. The majority of invasive populations in Asia appear to be P. canaliculata, often not mixed with P. maculata (Hayes et al., 2008; Tran et al., 2008) and the pest potential of P. canaliculata in such cases is clear. However, much less has been written about the invasiveness and pest potential of ‘P. maculata’.

The following statement (from the CABI Invasive Species Compendium datasheet for P. canaliculata) may equally apply to P. maculata: “Once introduced to an area, it spreads rapidly through bodies of water such as canals and rivers and during floods. It feeds on aquatic plants and can devastate rice (in South-east Asia), taro (in Hawaii; although P. maculata is not in Hawaii) and other aquatic or semi-aquatic crops. It may out-compete native apple snails (Halwart, 1994a; Warren, 1997), prey on native fauna (Wood et al., 2005, 2006) and alter natural ecosystem function (Carlsson et al. 2004a). It is also an important vector of various parasites including the nematode Angiostrongyulus cantonensis, which causes human eosinophillic meningitis (Lv et al., 2011; Yang et al., 2013)”.

The two species are now distinguishable, although there still remain questions over much of the recently published research that has not clearly and correctly identified the species in question. Nonetheless, it seems that together, these two large-bodied freshwater snails have flourished in locations to which they have been introduced and become invasive because of their high fecundity, generalized feeding, wide abiotic tolerances and close associations with humans. Several sources list P. maculata as a pest species. In the USA transport of all ampullariids except Pomaceabridgesii’ (incorrect identification of P. diffusa) between states is restricted (Gaston, 2006).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Mollusca
  •             Class: Gastropoda
  •                 Subclass: Caenogastropoda
  •                     Order: Architaenioglossa
  •                         Unknown: Ampullarioidea
  •                             Family: Ampullariidae
  •                                 Genus: Pomacea
  •                                     Species: Pomacea maculata

Notes on Taxonomy and Nomenclature

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The higher classification of the Gastropoda of Bouchet and Rocroi (2005) places Pomacea in the informal group Architaenioglossa of clade Caenogastropoda. Hayes et al. (2012) revised the taxonomy of P. maculata and P. canaliculata, redescribing both species and clearly distinguishing them morphologically. Hayes et al. (2012) reviewed many similar species and synonymized a number of them with either P. maculata or P. canaliculata. Those species synonymized with P. maculata are listed as “Other scientific names” in the section on Identity in this P. maculata datasheet. All of them were described originally in the genus Ampullaria, which is now considered a junior synonym of Pila (Cowie, 1997; ICZN, 1999), a genus of African and Asian Ampullariidae (Cowie, 2015). Some of them have been used in combination with the genus name Pomacea, and so these are also listed in the Identity section. Various other scientific names (tabulated by Cowie et al., 2006) have been used for the introduced apple snails in Asia (i.e., undistinguished P. maculata and P. canaliculata) that place them in incorrect, invalid or mis-spelled genus names (e.g. AmpullariaLamarck, 1799, AmpullariusMontfort, 1810), that identify them as different species (e.g. cuprinaReeve, 1856, leviorSowerby, 1909, lineata Spix in Wagner, 1827), or mis-spell the genus or species names (e.g. Ampullarium, insularus, insularis). The name Pomacea insularum (anglicized in the USA as the “island applesnail”) was formerly used as the valid name of P. maculata but is now a junior objective synonym of P. maculata, following the designation of a single specimen as both the neotype of P. maculata and lectotype of P. insularum; the same specimen was also designated as the neotype of P. gigas, thereby making this also a junior objective synonym of P. maculata (Hayes et al., 2012).

Prior to the work of Cowie et al. (2006), Rawlings et al. (2007), Hayes et al. (2008, 2009b, 2012) and Tran et al. (2008), the difficulty of distinguishing P. canaliculata from P. maculata meant that not only were their true ranges in South America not understood but also that the correct identities of ampullariids in Asia and other locations to which they have been introduced were not known. Thus, much of the literature published prior to these clarifications, especially in Asia, either confounded data from these two species (e.g. Cowie, 2002) or may have presented data from one species that in fact were derived from the other.

This confusion has meant that the common name most widely used in Asia, ‘golden apple snail’, or GAS (Joshi and Sebastian, 2006), in fact refers to two species, P. canaliculata and P. maculata. The name golden apple snail has also been used for an entirely different species, P. dolioides (incorrectly identified as P. lineata), in Suriname (Wiryareja and Tjoe-Awie, 2006). Similarly, the name ‘channelled [‘channeled’ in the USA] apple snail’ (or ‘applesnail’), an anglicization of the specific epithet ‘canaliculata’, was originally applied to populations in the USA that were thought to be P. canaliculata, but turned out in fact to be P. maculata (Howells et al., 2006; Rawlings et al., 2007). In any case, a number of other species of Pomacea, including P. maculata, have deeply channelled shell sutures, the feature that is reflected by this name. Pomacea maculata was initially identified in the USA as P. insularum by Rawlings et al. (2007), and given the common name ‘island apple snail’ (‘insularum’ in Latin means ‘of islands’) by various agencies. However, when P. insularum was synonymized with P. maculata by Hayes et al. (2012), the common name ‘island apple snail’ became inappropriate. Subsequently, the common name ‘giant apple snail’ has been suggested for P. maculata, but this name suffers from the fact that many apple snail species are very large, as well as potentially fostering confusion with ‘GAS’ used to refer to ‘golden apple snails’ (traditionally P. canaliculata but now known to be a mixture of P. canaliculata and P. maculata) and the ‘giant African snail’ (Lissachatina fulica). A reference to P. maculata as 'giant Peruvian’ or ‘Inca' snails (Dillon, 2006) does not reflect the broad distribution of this species. Additional confusion has also arisen because some of these names have been used for more than one species of ampullariid; for instance, ‘golden snail’ and ‘mystery snail’ have been used primarily for orange/yellow varieties of both P. canaliculata and P. diffusa (the latter often misidentified as P. bridgesii), notably in the aquarium trade, in some cases without realizing that they are different species, or without being able to distinguish them, or simply misidentifying them (see Cowie et al., 2006). Consequently, the use of common names should be avoided to reduce confusion within this taxonomically difficult group (Hayes et al., 2009b).

The first relatively comprehensive molecular phylogeny of the genus Pomacea was published by Hayes et al. (2009b) and showed that P. maculata and P. canaliculata are not particularly closely related and are not sister taxa. Nonetheless, in areas of Asia where introduced populations of P. maculata and P. canaliculata overlap (i.e. Japan, Korea, Vietnam and the Philippines), Matsukura et al. (2013) found preliminary genetic evidence of hybrid individuals. It remains unclear whether hybridization occurred only in the introduced range, or in the native range prior to introduction of the two species (including hybrids) to Asia. In the laboratory F1 hybrid progeny have been produced (Matsukura et al., 2013) but survivorship and reproductive viability of F1 or F2 hybrids in the field has not been assessed. In general, P. maculata and P. canaliculata maintain distinct characteristics and separate identities.

Ampullariid taxonomy has until recently relied almost exclusively on shell morphology (conchology). However, it has been extremely confused because of the gross morphological similarity within major ampullariid groups accompanied by considerable intra-specific variation. Consequently, species boundaries have been very difficult to assess based solely on conchology. Nonetheless, P. maculata can be distinguished from P. canaliculata somewhat reliably as adults based on features of the shell, that of P. maculata usually having a yellowish to reddish-orange wash round the pallial region of the peristome (the edge of the shell aperture), with that of P. canaliculata being unpigmented, and more subtly in the greater angulation of the whorl shoulder in P. maculata (Hayes et al., 2012). Definitive identification, however, must rely on molecular characters, internal anatomy or reproductive characteristics to distinguish clearly between the two species. In particular, P. maculata can be distinguished from P. canaliculata on the basis of the position and number of glands on the penial sheath, P. canaliculata having two distinctive areas of glandular tissue in the apical penial sheath gland, and P. maculata lacking a medial sheath gland but possessing a basal sheath gland (Hayes et al., 2012, 2015). Hatchlings of the two species are readily distinguished. The number of eggs in a clutch is greater in P. maculata but the eggs are smaller; hence hatchlings of P. canaliculata are roughly twice as big as those of P. maculata (Hayes et al., 2012). The two species differ most clearly genetically, having no shared haplotypes and a mean genetic distance of 0.135 at cytochrome c oxidase subunit I (COI) (Hayes et al., 2012). Results from analysis of the nuclear marker EF1-α are more enigmatic, with a few individuals identified as one or the other species on the basis of COI having EF1-α sequences corresponding to the opposite species, indicating possible hybridization events, or incomplete lineage sorting at this locus (Hayes et al., 2012; Matsukura et al., 2013).

Description

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The most thorough description available for P. maculata is by Hayes et al. (2012), in which P. maculata and P. canaliculata are compared. The following brief description is modified primarily from that publication, with other citations indicated as appropriate.

Adults

The adult shell is globose, thick, occasionally malleate (predominantly in Brazilian specimens) but generally smooth (sometimes with faint axial growth lines) and ~35 to >165 mm in shell height. The shell coils dextrally – that is, when viewed with the apex uppermost the aperture is on the right side of the shell. Fully grown females are larger than males and can achieve a weight of over 200 g (Kyle et al., 2009). The shell is yellowish brown or yellow–green to greenish brown or dark chestnut, sometimes with reddish to green–brown or dark brown spiral bands of variable number and thickness. The shell has five or six whorls on average, increasing rapidly in size, with a deep suture between the whorls. The shoulder of the whorls is angulate. The shell spire is generally low but variable. The aperture is large and generally ovoid, and the inside lip of the shell is pale yellow to reddish orange.

The operculum (the trap-door like structure attached to the upper part of the animal’s foot and used to close the shell aperture when the animal withdraws into the shell) is dark brown; it is horny (corneous) in texture and somewhat flexible, and is uniformly concave in females, but concave at the centre and becoming convex toward the margins in males.

The foot is oval with a squarish anterior edge. The tentacles are long and tapering, highly extensible and with large but short eye stalks at their outer bases. The snout is short, squarish and with lateral, anterior tips elaborated into long tapering labial palps. The neck is modified on the left into a long, extensible siphon. The mantle cavity is deep and broad, occupying a third to half of the body whorl. In males the penis sheath is visible just behind the mantle edge above the right tentacle. The lung occupies most of the left side of the mantle and the gill is situated in the mantle roof, anterior to the lung and just posterior to the base of the siphon.

Eggs and Hatchlings

The eggs are spherical, calcareous, deep pink-red to lighter orange-pink, becoming paler as the calcium hardens, and eventually whitish pink just before hatching. They are laid in densely packed clutches above water on emergent vegetation and other firm substrates (e.g. bridge pilings, rocks). The height of deposition above water varies from a few centimetres to ~2 metres. The number of eggs per clutch ranges from a few hundred to as many as ~4500, with an average of ~1500 (Barnes et al., 2008; Burks et al., 2010). Individual egg diameter is ~1.9 mm. The pink colour of the eggs of P. maculata comes from the carotenoproteins that probably play roles in protection against solar radiation, stabilizing and transporting antioxidant molecules and helping to protect embryos from desiccation and predators (Pasquevich et al., 2014), as they do in P. canaliculata (Dreon et al., 2013). The proteins of P. maculata and P. canaliculata do however differ in their spectral properties, which may be another character that would help to distinguish the two species (Pasquevich et al., 2014).

When the eggs hatch, the hatchlings drop from where the eggs were laid into the water below. The first whorl of one-day-old hatchlings is ~0.8 mm wide and the hatchling shell is 1.2 mm in height; the semi-translucent operculum is ~1.1 mm in width (Barnes et al., 2008; Horn et al., 2008; Hayes et al., 2012). At this stage, small, scattered patches of pigment make their shells appear spotted. A distinct yet small dark brown line extends vertically from the top to the mid-point of the operculum. 

Distribution

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Native Distribution

P. maculata has a wide native range in South America extending from the Rio de la Plata in Argentina and Uruguay, through Paraguay and northwards in Brazil through the Pantanal to north of Manaus in Amazonia, overlapping with the range of P. canaliculata in the south (Hayes et al., 2008, 2009a, b, 2012).

Non-native Distribution

The taxonomic confusion surrounding P. maculata and P. canaliculata and the assumption in much of the literature regarding South-East Asia that the widespread ‘golden apple snail’ was P. canaliculata, has meant that the history of introduction and spread, in particular of P. maculata, in the region is difficult to ascertain. Although it is clear that P. canaliculata was first introduced to the region (to Taiwan) in about 1979 or 1980, P. maculata has not been demonstrated rigorously as ever having been present in Taiwan (Hayes et al., 2008). Therefore, the date of its first introduction to the region is not known. No mixed species populations were reported by Hayes et al. (2008), from which it can be inferred that the introductions and spread of the two species have been separate, that is, people have not introduced or moved around mixed species propagules. However, mixed and possibly hybridizing populations have now been detected, e.g. in Japan (Matsukura et al., 2013). These populations probably became mixed through either deliberate human-mediated introductions or via natural spread of one species to localities already invaded by the other. Hayes et al. (2008) reported introduced P. maculata in the wild in Asia from Malaysia (Borneo), Cambodia, Singapore, South Korea, Thailand and Vietnam (the report of Taiwan in Table 1 of that paper is incorrect). For most countries in which Hayes et al. (2008) recorded P. maculata, there were no previous records, the exceptions being Cambodia and Thailand. Thus, the first records for most countries are in 2008, although it is likely that P. maculata was introduced widely much earlier than this, especially as it was already in Thailand by 1990 or perhaps even 1984 (Keawjam and Upatham, 1990) and was first detected, highly localized, in Cambodia in 1995 (Cowie, 1995).

In the USA, P. maculata has been recorded from Alabama, Georgia, Florida, Louisiana, Mississippi, possibly North Carolina, South Carolina and Texas. Most of the P. insularum screened by Rawlings et al. (2007) possess COI haplotypes that are a close match to haplotypes from the Río Uruguay near Buenos Aires, indicating a probable origin in this region. The species was established in Texas by 1989, in Florida by the mid to late 1990s and in Georgia by 2005 (Rawlings et al., 2007) and continues to spread (Byers et al., 2013). Climatic modelling indicates that it could expand further north in the USA (Byers et al., 2013).

History of Introduction and Spread

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Due to the confusion in species identification, it is impossible to determine exactly when P. maculata was initially introduced to Asia, much less into individual countries. The range reported incorporates speculation and anecdotal accounts about P. canaliculata as well. The introduction of P. maculata may have occurred in concert and perhaps unknowingly with P. canaliculata, although most populations investigated by Hayes et al. (2008) were of just one species, suggesting that most initial propagules were also not mixed. Nonetheless, much of the primary literature dealing supposedly with P. canaliculata, may have been (and probably still is) also dealing inadvertently with either P. maculata or a mixture of the two species.

The majority of references identify Argentina as the original source of the introduced Pomacea (e.g. Mochida, 1991) and molecular study confirms the area of the Uruguay and La Plata rivers around Buenos Aires as the most likely specific locality (Hayes et al., 2008). Introductions of Pomacea began around 1979 or 1980, initially to Taiwan (Mochida, 1991) (though this appears to have been only P. canaliculata). When the first introduction of P. maculata took place is not known. However, Mochida (1991) mapped the spread of Pomacea, and although he did not distinguish species it is apparent that there was already an awareness that at least two species were involved, i.e. P. canaliculata and P. maculata. With some exceptions (e.g. Thailand), the dates given by Mochida (1991) for introduction of Pomacea to particular countries can therefore be taken as the earliest date that P. maculata might have been introduced to those countries.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Cambodia 1995 Yes Cowie, 1995; Cowie, 2002; Hayes et al., 2008 Possibly introduced from Vietnam. Only provisionally identified as either P. canaliculata or P. maculata by Cowie (1995); misidentified as P. canaliculata by Cowie (2002); identity confirmed by Hayes et al. (2008)
Japan South East Asia 1981/later Aquaculture (pathway cause) Yes Matsukura et al., 2013; Mochida, 1991 Introduced from elsewhere in east or South-East Asia. Present in south-western Japan and the Ryukyu Islands
Korea, Republic of South East Asia 1986/later Aquaculture (pathway cause) Yes Hayes et al., 2008; Matsukura et al., 2013; Mochida, 1991 Introduced from elsewhere in east or South-East Asia. Possibly previously confused with P. canaliculata, which is also in South Korea
Malaysia South East Asia 1987/later Aquaculture (pathway cause) Yes Hayes et al., 2008; Mochida, 1991 Introduced from elsewhere in east or South-East Asia. Possibly previously confused with P. canaliculata
Philippines South East Asia 1982/later Aquaculture (pathway cause) Yes Matsukura et al., 2013; Mochida, 1991 Introduced from elsewhere in east or South-East Asia. Possibly previously confused with P. canaliculata
Singapore South East Asia 1990s Aquaculture (pathway cause) ,
Aquarium trade (pathway cause) ,
Pet trade (pathway cause)
Yes Matsukura et al., 2013; Ng et al., 2014 Introduced from elsewhere in east or South-East Asia. Possibly previously confused with P. canaliculata
Spain 2009 Aquarium trade (pathway cause) ,
Pet trade (pathway cause)
Yes Horgan et al., 2012; MMAMRM, Ministerio de Medio Ambiente y Medio Rural y Marino In drainage canals and rice cultivation areas
Thailand South East Asia 1984-1990 Aquaculture (pathway cause) Yes Hayes et al., 2008; Keawjam and Upatham, 1990 Introduced from elsewhere in east or South-East Asia. 1984 was the first record of Pomacea but this record could have been either P. maculata or P. canaliculata
USA 1989 Aquarium trade (pathway cause) ,
Pet trade (pathway cause)
Yes Byers et al., 2013; Rawlings et al., 2007 Established in Texas by 1989
Vietnam South East Asia 1980s Aquaculture (pathway cause) Yes Cuong, 2006; Hayes et al., 2008 Introduced from elsewhere in east or South-East Asia. Possibly previously confused with P. canaliculata, which is also in Vietnam

Risk of Introduction

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Risk of future introduction of P. maculata remains high because of two primary vectors: the aquaculture industry and the aquarium trade. In general, the former is the primary risk in Asia and the latter in other regions, though by no means exclusively. The primary mode of spread has probably been deliberate introduction to new areas by people who see it as a potential source of food, generally not distinguishing it from P. canaliculata. Although usually confined initially to aquaculture facilities, the snails either escape or are deliberately released into agricultural or natural wetlands. This has happened despite knowledge of the serious pest status of Pomacea spp. in areas already invaded. It has also been reported as having been introduced by the pet trade, perhaps more commonly than P. canaliculata, although the main ampullariid in the pet trade is P. diffusa. Once introduced, it is further possible that it spreads naturally by floating downstream, to a limited extent by crawling upstream, during flooding, and even attached to birds, as has been reported for P. canaliculata in Hawaii (Levin et al., 2006). People may also move it around accidentally; for instance, eggs can be transported on boats (EFSA Panel on Plant Health., 2012), and in Hawaii small juveniles (of P. canaliculata) could be inadvertently transported on taro parts used for propagation (Levin et al., 2006).

Aquaculture

The aquaculture industry first transported apple snails, both P. maculata and P. canaliculata, from South America to Asia as potential human food sources (Mochida, 1991; Naylor, 1996). P. canaliculata spread rapidly through much of Southeast Asia following its initial introduction to Taiwan. It may now have reached most areas in which it would be able to live within the region. P. maculata, however, has not been recorded so widely in Asia (in part no doubt because of misidentification as P. canaliculata) and may still be spreading. Modelling the distribution of P. canaliculata in China under global warming scenarios indicates that this species could spread north into areas that it has not yet invaded (Lv et al., 2011). Similar range expansions related to climate change could also occur elsewhere, for instance in Korea and Japan. P. maculata is less tolerant than P. canaliculata of cold temperature (Yoshida et al., 2014), which may restrict its northerly spread in Asia compared to P. canaliculata, yet still allow it to spread further north than its current distribution. Similarly, following the introduction of P. maculata to Spain, climate matching combined with two global warming scenarios identified areas in Europe that may be susceptible (EFSA Panel on Plant Health, 2012).

In general, Pomacea were not well liked as a food in Asia and markets did not develop (e.g. Wada, 1997; Cheng and Kao, 2006; Preap, 2006; Wada, 2006; Yang et al., 2006; Yin et al., 2006), although in parts of southern China P. canaliculata became a popular delicacy, eaten raw (Cowie, 2013a; Yang et al., 2013), and is now widespread (Lv et al., 2011). However, once these aquaculture efforts generally failed, snails were released or escaped, leading to the spread of apple snails throughout much of Southeast Asia. Deliberate introduction for food may therefore now be rare. Nonetheless, the global need to replace expensive sources of protein (e.g. beef) with cheaper alternatives might facilitate a resurgence of apple snails in aquaculture, especially in areas that have other non-traditional meat sources. The distribution of P. maculata in the USA overlaps with regions that raise other large invertebrates (e.g. crayfish) for food (Byers et al., 2012). The availability of large snail populations in these areas might draw attention to their culinary potential and result in the creation of an aquaculture industry where one did not formerly exist.

Aquarium trade

In the aquarium trade, particularly in the USA, stores receive freshwater snails from multiple sources and no mechanisms exist to verify the identity of the snails (Karatayev et al., 2009). P. maculata in the southeastern USA was probably introduced via the aquarium trade (Karatayev et al., 2009; Martin et al., 2012). While larger adult snails of some species are relatively easily distinguished, small juvenile snails sold in the pet trade are much more difficult to distinguish, especially by a non-expert. The United States Department of Agriculture Plant Protection and Quarantine Division (USDA-APHIS-PPQ) restricts the possession of most members of the genus Pomacea and requires a permit for their use in research or interstate transport (USDA-APHIS, 2013). In addition, apple snails in general occur on a number of other invasive species watch lists (e.g. the Global Invasive Species Database of the IUCN Invasive Species Specialist Group). However, the algae-eating ‘spike-topped’ apple snail, Pomacea diffusa (formerly identified as the different species Pomacea bridgesii) is not perceived as a threat to agriculture and so P. diffusa remains freely available in the aquarium trade. Without any requirement or practice of inspection, small P. maculata may be mistaken for P. diffusa and unintentionally sold to the public. P. maculata does not perform well in an aquarium, however, and so pet owners will often release the illegally acquired snail ‘back’ into the environment without any awareness of the consequences. Very few educational efforts exist to prevent this common occurrence from happening again and again (Martin et al., 2012). Furthermore, the recent name changes (Hayes et al., 2012) complicate matters because permit restrictions may lag behind changes in scientific terminology.

P. maculata has been detected in the pet trade in Belgium (Hayes et al., 2008) and its presence in both Israel (Roll et al., 2008) and Spain (EFSA Panel on Plant Health, 2012) is thought to have been due to introductions via the aquarium trade. Other apple snails, notably P. diffusa, have been found in the trade in Australia, Hawaii, Florida and Iran (Hayes et al., 2008).

Habitat

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P. maculata occurs in shallow parts of slow-moving bodies of fresh water, close to riverbanks, at the edges of lakes and in ponds, in wetlands and irrigated wetland croplands and in drainage/irrigation ditches. It has been reported from estuaries (EFSA Panel on Plant Health, 2012) but its salinity tolerance probably prevents its extensive penetration into such brackish habitats (Ramakrishnan, 2007), although eggs remain viable when exposed to periodic inundations typical of a tidal regime and modest, albeit reduced, growth and survival occurs at moderate salinities (5 and 10‰) (Martin and Valentine, 2014). Byers et al. (2013) provided a model that predicted suitable habitat for P. maculata in the USA, based on climate modelling and the influence of pH. Their pH data were from the dissertation of Ramakrishnan (2007), which examined tolerance to environmental temperature (15.2-36.6°C), salinity (0-6.8‰) and pH (4.0-10.5). Ramakrishnan (2007) also showed that the maximum desiccation tolerance of P. maculata was loss of 58% of total corporeal plus extracorporeal water and that it is a moderate regulator of oxygen consumption when subjected to progressive hypoxia, maintaining a normal oxygen uptake rate down to a critical PO2 of 80-120 Torr depending on temperature, and suggested that P. maculata would be most successful in oxygenated, flowing-water (but only slow-flowing) habitats.

Habitat List

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CategoryHabitatPresenceStatus
Brackish
Estuaries Present, no further details
Freshwater
Irrigation channels Secondary/tolerated habitat Harmful (pest or invasive)
Irrigation channels Secondary/tolerated habitat Natural
Lakes Principal habitat Harmful (pest or invasive)
Lakes Principal habitat Natural
Ponds Principal habitat Harmful (pest or invasive)
Ponds Principal habitat Natural
Reservoirs Principal habitat Harmful (pest or invasive)
Reservoirs Principal habitat Natural
Rivers / streams Principal habitat Harmful (pest or invasive)
Rivers / streams Principal habitat Natural
Terrestrial-natural/semi-natural
Wetlands Principal habitat Harmful (pest or invasive)
Wetlands Principal habitat Natural

Hosts/Species Affected

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P. maculata can impact many plant species. It can directly affect two aquatic crops: taro (Colocasia esculenta) and rice (Oryza sativa), but probably others. It will feed on macroalgae, submerged plants or freely floating macrophytes with little structural defense (e.g. Ludwigia) and plants that occur on the margins of the riparian zone. It may also feed on some submerged or freely floating plants that have tough physical structures or chemical defence compounds. Based on field and other observations of the snails in the USA and on the architecture of the plants, C. esculenta, Pontederia lanceolata, Sagittaria spp., Eichhornia crassipes, Pistia stratoites, Alternanthera philoxeroides, Schoenoplectus californicus, Scirpus maritimus, Thalia dealbata and Typha latifolia could provide a suitable substrate for P. maculata females to lay egg clutches.

As in almost all studies undertaken on Pomacea in East and South-East Asia, especially prior to the rigorous distinction of P. canaliculata and P. maculata by Hayes et al. (2008, 2012), the identity of the species involved must be considered with caution. For example, a number of studies have been undertaken on consumption of plants by apple snails in Laos (Carlsson and Lacoursière, 2005; Carlsson and Brönmark, 2006) and Thailand (Carlsson et al., 2004a). They all identified the snails as P. canaliculata and for the studies in Laos there is no evidence that this was in error, and in fact P. maculata has not been recorded from Laos. Yet it is still possible that these snails could have been P. maculata. The study in Thailand, however, may well have been on P. maculata, as the size of the snails reported in this study exceeded the maximum dimension given by Hayes et al. (2012) in their detailed description of P. canaliculata but was within the range of size of P. maculata. In the study of Carlsson et al. (2004a), apple snails consumed water hyacinth (Eichhornia crassipes) at a rate of 1.01 g plant per g snail per day. In fact, no published study has suggested that P. maculata consumes substantial quantities of E. crassipes quickly. In Laos, apple snails (probably P. canaliculata) consumed all of the duckweed (Lemna minor) offered in just six days but took 21 days to eat the equivalent amount of water hyacinth, and by the end of 32 days had consumed only 20% of the morning glory (Ipomoea aquatica) (Carlsson and Lacoursière, 2005). The snails consumed duckweed in one piece but first attacked the roots and aerenchyma-filled bulbs of water hyacinth before consuming the leaves. For morning glory, they took longer to scrape at the hollow stems that later gave access to the leaves, Also in Laos, snails (probably P. canaliculata) in an enclosure study consumed greater amounts of Ludwigia adscendens and Salvinia cucullata than of I. aquatica (Carlsson and Brönmark, 2006).

In contrast to studies in South-East Asia, recent studies in North America in areas where no P. canaliculata are present, can generally be reliably interpreted as being based on P. maculata. In a growth/survival experiment, Burks et al. (2011) demonstrated that a 10 g P. maculata from non-native populations in Texas consumed approximately 3.5 g of live plant material per day with more Eurasian watermilfoil (Myriophyllum spicatum) consumed than wild taro (Colocasia esculenta) and more taro than water hyacinth. However, when P. maculata from Texas was fed 26 plant species in no-choice tests E. crassipes was the sixth most consumed (Burlakova et al., 2009). Gettys et al. (2008) measured consumption rates of six size classes of P. maculata when presented with seven submerged macrophytes simultaneously. Patterns of consumption did not differ among size classes or across a range of temperatures (20-35 °C). The snails preferred the macroalgae Najas guadalupensis and Chara sp., as well as the alien invasive submerged macrophyte Hydrilla verticillata and only after exhausting these resources did they turn to, but ate considerably less of, the submerged macrophytes Potamogeton illinoensis, Vallisneria americana and Myriophyllum aquaticum; they did not consume noticeable amounts of Egeria densa.

Boland et al. (2008) tested whether structure or chemistry of resources made a difference in consumption by juvenile and adult P. maculata. Overall, juveniles consumed more per capita than adults and P. maculata ate more Myriophyllum spicatum than E. crassipes, especially when presented as reconstituted resources with chemical extracts. In an experiment in which juvenile P. maculata received three resources simultaneously (Burks et al., 2011) they consumed more M. spicatum than C. esculenta and E. crassipes. Burlakova et al. (2009) tested feeding rates of adult P. maculata on 15 aquatic plants in non-choice experiments. Snail consumption ranged from 55 % to 96 % on a subset of plants (approximate rank order: Hymenocallis liriosme, Ceratophyllum demersum, Ruppia maritima, Colocasia esculenta, Eichhornia crassipes, Sagittaria lancifolia). P. maculata showed a lower range of consumption (between 10 % and 34 %) on a second subset of plants (Alternanthera philoxeroidesSagittaria graminea, Panicum hemitomon, Scirpus maritimus, Canna glauca, Pontederia cordataS. californicus,). Snails consumed less than 10 % of Spartina alterniflora, Thalia dealbata and Typha latifolia. In a similar study to that of Burlakova et al. (2009), Baker et al. (2010) assessed adult P. maculata consumption on a suite of aquatic plants and macroalgae, and reported per capita consumption (grams plant per gram snail per day) based on non-choice experiments. Consumption rates on three plants (Limnobium spongia, Chara sp., Panicum repens) exceeded 3 g/g/d, whereas snails consumed another five species at a rate of 2-3 g/g/d (H. verticillata, S. latifolia, C. demersum, N. guadalupensis and V. americana). Consumption of another three plants (Pontederia lanceolata, Sagittaria kurziana and Myriophyllum heterophyllum) was 1-2 g/g/d and snails showed minimal consumption (0.032 – 0.049 g/g/d) of E. densa, Alternanthera philoxeroides and E. crassipes. In this study, there was no measurable consumption by P. maculata of Nymphaea odorata, T. latifolia, P. illinoensis, M. aquaticum, C. esculenta, Hydrocotyle umbellata, Pistia stratiotes and S. lancifolia. Morrison and Hay (2010) assessed preferences and consumption rates of multiple species of apple snails with eight macrophytes native to Florida; all snails showed roughly similar patterns of preference throughout the choice experiment, with Utricularia sp. being the most preferred as well as most readily consumed by all species. Specifically, P. maculata also quickly consumed S. latifolia after eliminating the Utricularia. Similarly to other species, P. maculata showed intermediate preference for Bacopa caroliniana and N. odorata. No snails consumed Eleocharis cellulosa, P. cordata, P. hemitomon or Typha sp.

Using a similar approach, Morrison and Hay (2011) conducted paired feeding experiments that gave P. maculata the choice between plants found outside their native distribution (i.e. North America) and those found within their native range (i.e. South America); all snails preferred North American to South American plants.

Generally, the patterns of host plant consumption by P. maculata were similar among the above studies, although with a few exceptionsFor S. lancifolia and P. hemitomon, one study (Burlakova et al., 2009) showed low to moderate consumption while no consumption occurred in another (Baker et al., 2010). There were some differences in consumption between congeneric plant species. For example, in the study by Morrison and Hay (2010), snails did not consume P. cordata but in that of Baker et al. (2010) they ate a small amount of P. lanceolata. However, there was much greater variation in consumption tendencies for taro and water hyacinth, although none of the studies showed P. maculata having a strong preference for these resources. Given these discrepancies in feeding patterns and the wide diversity of plants consumed, P. maculata should not be used for biological control of invasive plants and more studies need to be conducted to fully understand the mechanisms underlying the preferences of P. maculata for these plant species.

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Alternanthera philoxeroides (alligator weed)AmaranthaceaeWild host
Bacopa carolinianaScrophulariaceaeMain
Canna glaucaCannaceaeWild host
Ceratophyllum demersum (coontail)CeratophyllaceaeWild host
Colocasia esculenta (taro)AraceaeMain
Egeria densa (leafy elodea)HydrocharitaceaeWild host
Eichhornia crassipes (water hyacinth)PontederiaceaeWild host
Hydrilla verticillata (hydrilla)HydrocharitaceaeWild host
Hymenocallis liriosmeLiliaceaeWild host
Ipomoea aquatica (swamp morning-glory)ConvolvulaceaeWild host
Lemna perpusilla (duckweed)LemnaceaeWild host
Limnobium spongiaHydrocharitaceaeWild host
Ludwigia adscendens (water primrose)OnagraceaeWild host
Ludwigia grandiflora (water primrose)OnagraceaeWild host
Ludwigia palustrisOnagraceaeWild host
Myriophyllum aquaticum (parrot's feather)HaloragidaceaeWild host
Myriophyllum heterophyllum (broadleaf watermilfoil)HaloragidaceaeWild host
Myriophyllum spicatum (spiked watermilfoil)HaloragidaceaeWild host
Najas guadalupensisNajadaceaeWild host
Nymphaea odorataNymphaeaceaeWild host
Panicum hemitomonPoaceaeWild host
Panicum repens (torpedo grass)PoaceaeWild host
Peltandra virginicaAraceaeWild host
Pistia stratiotes (water lettuce)AraceaeWild host
Pontederia cordataPontederiaceaeWild host
Potamogeton illinoensisPotamogetonaceaeWild host
Ruppia maritimaRuppiaceaeWild host
Sagittaria gramineaAlismataceaeWild host
Sagittaria kurzianaAlismataceaeWild host
Sagittaria lancifoliaAlismataceaeWild host
Sagittaria latifolia (broadleaf arrowhead)AlismataceaeWild host
Salvinia cucullataSalviniaceaeWild host
Schoenoplectus californicusCyperaceaeWild host
Scirpus maritimus (saltmarsh bulrush)CyperaceaeWild host
Spartina alterniflora (smooth cordgrass)PoaceaeWild host
Thalia dealbataMarantaceaeWild host
Typha latifolia (broadleaf cattail)TyphaceaeWild host
Utricularia (bladderwort)LentibulariaceaeWild host
Vallisneria americana (Vallisneria)HydrocharitaceaeWild host

Growth Stages

Top of page Flowering stage, Fruiting stage, Vegetative growing stage

List of Symptoms/Signs

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Growing point

  • external feeding

Leaves

  • external feeding

Stems

  • external feeding

Vegetative organs

  • external feeding

Whole plant

  • external feeding

Biology and Ecology

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Knowledge of the biology of ampullariids, essentially as of 1999 and which focussed on their role as agricultural pests, was reviewed by Cowie (2002). The multi-authored book edited by Joshi and Sebastian (2006) also brought together considerable knowledge, with a primary focus on agriculture in Asia. The large amount of research on basic ampullariid biology that has been undertaken since around the year 2000 has now been reviewed by Hayes et al. (2015) and, although much of the knowledge is based on P. canaliculata, that comprehensive review should nonetheless serve as a key resource.

Genetics

The molecular genetics of P. maculata has been less studied than that of P. canaliculata, although the two species, previously difficult to distinguish, can now be readily distinguished based on DNA markers; they are not sister species (Hayes et al., 2008, 2009b, 2012). Thus, the natural range of P. canaliculata was formerly thought to extend from temperate Argentina into northern Amazonia (Cazzaniga, 2002), the species having been confused with P. maculata. P. canaliculata is now known to have a more restricted southern distribution and P. maculata an extensive distribution overlapping in part with that of P. canaliculata but extending as far as Amazonia (Hayes et al., 2012). The entire genome of P. maculata has not been sequenced or examined comprehensively. In the study of Hayes et al. (2012) P. maculata and P. canaliculata did not share any mitochondrial DNA COI haplotypes, even in places where their ranges overlapped. However, sequences of a portion of a single nuclear marker (EF1-a) from a few individuals of both species found in sympatry indicated possible hybridization or incomplete lineage sorting at this locus (Hayes et al., 2013; Matsukura et al., 2013). However, no studies have examined the survivorship or viability of any possible hybrids between the two species. A molecular method using species-specific markers within the COI fragment has been used to differentiate P. maculata and P. canaliculata in Asian populations (Matsukura et al., 2008), but the method does not take into account the overall extent of variation in COI and may not distinguish the two species in other places. The method focuses on P. maculata and P. canaliculata and may not help in distinguishing them from other closely related species.

Reproductive Biology

P. maculata has separate sexes with female size typically exceeding male size. Fertilization occurs internally, followed by oviparous development. Barnes et al. (2008) described the reproductive behaviour and fecundity of P. maculata (referred to as P. insularum). Female and male snails copulate for several minutes, if not hours. The time needed for egg development is uncertain. The female crawls out of the water onto an emergent substrate and lays a clutch of pink eggs. Burks et al. (2010) noted that P. maculata in Texas laid a disproportional number of clutches on riparian vegetation, specifically taro (Colocasia esculenta). In laboratory experiments eggs were laid on natural substrates (i.e. plants and wood) in preference to artificial substrates (Kyle et al., 2011). Nonetheless, egg clutches are laid on all sorts of substrates that can support the weight of the female snail (emergent plants, rocks, bridge supports, etc.). Kyle et al. (2011) found no clear relationship between female size and clutch size.

In Texas, with a warm temperate climate, females tend to start laying clutches near the end of spring or start of summer and continue throughout summer and the warmer months of autumn. Seasonal patterns have not been studied in the native range of P. maculata. No study has yet documented the potential or limitations for reproduction in the species but anecdotal observations suggest that mature female snails can lay one clutch every 7-10 days, with clutch size ranging widely but averaging over a thousand eggs per clutch (Barnes et al., 2008; Burks et al., 2010). Their reproductive capacity certainly exceeds that reported for other Pomacea species (Cowie, 2002). Viable clutches usually take 10-14 days to hatch (Barnes et al., 2008; Horn et al., 2008). The colour of the eggs starts off as a vibrant pink and then fades to light pink, grey and then eventually white as the oxidative proteins break down and the clutches start to hatch. Eggs are laid noticeably above the water line, from a few centimetres but generally higher and up to ~2 metres. Immersion of the eggs, especially for extensive periods, reduces hatching success. Even without water stress, not all clutches hatch fully and some fail to hatch at all, perhaps indicating incomplete fertilization. However, given its success as an invasive alien species it is not surprising that the majority of clutches display high hatching success, often 70% or more (Barnes et al., 2008). Hatchlings (~1 mm in width) then fall into the water and attempt to adhere to some type of substrate. Hatchlings are likely to rely on detritus and algal-based resources for food, although they also readily consume lettuce in the laboratory. They may also use leftover egg material as an initial resource.

Growth

No study has adequately documented immediate hatchling growth rates although rapid growth has been observed in the first six weeks. Individual growth rates vary widely. From a shell height of ~10 mm, the snails reach ~20 mm over 6 weeks and achieve ~28 mm after a further 6 weeks. Age or size at first reproduction has not been studied in P. maculata but based on anecdotal evidence, juvenile P. maculata mature and can start producing very small egg clutches at 9-12 months old. Adult P. maculata can reach up to 165 mm in shell height and weigh over 200g (Kyle et al., 2009; Hayes et al., 2012).

Physiology and Phenology

Physiological studies on P. maculata were carried out by Ramakrishnan (2007). This appears to be the only broad study of the physiology of P. maculata. Among environmental factors, Ramakrishnan (2007) examined tolerance to salinity, pH and temperature. She also assessed desiccation tolerance and oxygen consumption, in particular when subject to progressive hypoxia.

In this study, at salinity levels of 0-6.8‰ survival was greater than 90% after a 28 day exposure. However, above a level of 6.8‰, survivorship declined rapidly, such that at 13.6‰ and above, 100% mortality occurring within 3-7 days. Snails were exposed to ph in the range of 2 to 12.5 for a period of 28 days. At ph 2-3, all snails were dead within 4-13 days. At ph 3.5, 20% survived the full 28 days, while at ph values of 5.5-9 all but 0-2 snails out of 15-20 survived. Above ph10, all snails died within 2 days (ph12.5) and 22 days (ph10.5). Both acute and chronic temperature tolerance was tested on snails acclimated prior to testing to a range of temperatures. The acute upper lethal limit was below 42°C. To assess chronic tolerance, snails were maintained at the experimental temperature for 28 days. Survivorship of individuals held at temperatures ≤36°C was high but declined progressively at temperatures of 37-41°C regardless of acclimation temperature; survival was greater for large snails. Regarding chronic low temperature tolerance, all snails died within the 28 day period at 2-15°C, while there was no mortality at 20°C.

Ramakrishnan (2007) assessed desiccation tolerance of three size classes of P. maculata at relative humidities (RH) from <5% to >95% and temperatures of 20, 25 and 30°C. Larger snails survived longer than smaller snails. At 30°C, under the most desiccating conditions <5% RH), all of the smallest size class were dead after 56 days, but under the most desiccating conditions (>95% RH), 100% mortality did not occur until day 189. At 20 and 25°C and >95% RH these small snails survived the duration of the experiment (308 days). The largest snails all survived 308 days at 75% and >95% RH, regardless of temperature, while at <5% all were dead at day 203 (20 and 25°C) and day 154 (30°C). At intermediate RH levels and for the intermediate sized snails, survivorship ranged within these extremes. During desiccation, water loss was greater at higher RH values and higher temperatures, and smaller snails lost proportionately more water than larger snails. The greatest water loss at day 161 was 63% at >95% RH and 30°C among the smallest snails. At death, snails had lost as much as 81% of their water content <5% RH, 30°C), although snail size did not influence this parameter.

Ramakrishnan (2007) also measured metabolic O2 consumption (VO2), in particular under progressive hypoxia to assess tolerance of P. maculata to hypoxic conditions. VO2 increased with body size and temperature, but P. maculata, especially juveniles, was not found to be an especially good oxygen regulator under hypoxic conditions in comparison with other freshwater snail species, perhaps reflecting its association with lotic (flowing water) habitats. This aspect of their biology warrants further study, especially in comparison with P. canaliculata, as it may be important in the ability of P. maculata to invade agricultural wetlands.

Longevity

Anecdotal estimates suggest P. maculata can live for up to 8 years.

Activity Patterns and Physiology

The activity patterns of P. maculata are probably similar to those of P. canaliculata but no studies have addressed these aspects of behaviour in P. maculata. However, experimental evidence (Ramakrishnan, 2007) indicates that P. maculata can survive long periods (i.e. months) without access to water and in the field will do this under minimal water conditions by burrowing into muddy substrates and closing the shell tightly with the operculum. They easily survive brief periods out of water using their lung rather than their gill, for instance during egg laying.

Population Size and Density

Burlakova et al. (2010) best described the invasive populations of P. maculata in a study conducted in southeastern Texas. In permanent habitats, such as ponds and lakes, they observed low densities (fewer than two snails per square meter), stable populations, and the same size structure through the year. Although low in comparison to ephemeral systems, higher snail densities occurred around the macrophyte-dominated zone versus the open water zone. They also noted rarely seeing juveniles despite high egg production. This pattern occurs in other lake systems.

In contrast, ephemeral agricultural habitats contained extremely high densities (>130 snails per square meter), and furthermore, snail size and numbers varied through time, both peaking in autumn. The differences were attributed to the survivorship of hatchlings and young juvenile snails, as the peak in population followed the mating season. Kyle et al. (2009) discussed the increasing proportion of juveniles observed in their study from 2006 to 2008. They suggested that introduced P. maculata populations continue to grow in the aquatic ecosystems of southeast Houston, and the same may be happening in the other parts of the southeastern USA to which P. maculata has been introduced (Byers et al., 2013).

Nutrition

Most ampullariids are generalist herbivores. Adult and juvenile P. maculata both consume aquatic macrophytes. Although some specific preferences may exist when offered different suites of plants, P. maculata can be considered a generalist herbivore that feeds on diverse aquatic plants (see the section on Hosts/Species Affected). P. maculata (and P. canaliculata) seem particularly voracious and generalist compared to other Pomacea species (Morrison and Hay, 2011).

Environmental Requirements

The most northern latitude at which P. maculata populations occur is the Ebro River delta in Spain (EFSA Panel on Plant Health, 2012; Horgan et al., 2012; Andre and Lopez, 2013), where it has been introduced. The southernmost latitude at which it occurs appears to be near Buenos Aires, Argentina (Hayes et al., 2012; Byers et al., 2013). Buenos Aires is one the coldest areas in the native range of the species, with average temperatures of 4-6 °C in the coldest months. In Houston, Texas, USA, where many populations of introduced P. maculata exist, temperatures can reach highs of 33 °C. Populations of P. maculata in Charleston, South Carolina, USA, probably experience the coldest temperatures in the introduced range, although climatic modelling indicates suitability of areas a little further north (Byers et al., 2013).

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Preferred Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Af - Tropical rainforest climate Preferred > 60mm precipitation per month
Am - Tropical monsoon climate Preferred Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer Tolerated < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
C - Temperate/Mesothermal climate Tolerated Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
Cf - Warm temperate climate, wet all year Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
40.8000 31.6036

Air Temperature

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Parameter Lower limit Upper limit
Absolute minimum temperature (ºC) 6 4
Mean annual temperature (ºC) 36.6 15.23
Mean maximum temperature of hottest month (ºC) 33.88 24.44
Mean minimum temperature of coldest month (ºC) 16 7

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Aramus guarauna Predator Adult/Juvenile not specific Perera and Walls, 1996; Peterson, 1980
Lepomis microlophus Predator Juvenile not specific Martin et al., 2012
Rostrhamus sociabilis Predator Adult/Juvenile not specific Perera and Walls, 1996; Peterson, 1980
Solenopsis geminata Predator Egg not specific Way et al., 1998; Yusa, 2001
Trachemys scripta elegans Predator Egg/Juvenile

Notes on Natural Enemies

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The best known natural enemies of apple snails in general are vertebrates. Throughout much of their natural range in South America, snail kites (Rhostramus sociabilis) and limpkins (Aramus guarauna) are major predators of various apple snail species, which are their almost exclusive food (Peterson, 1980; Perera and Walls, 1996). The ranges of both these species overlap with that of P. maculata and they are probably significant predators of this species. In parts of South America, large piles of apple snail shells can accumulate under the favorite perches of snail kites (R.H. Cowie, personal observations).

Apple snails, perhaps including P. maculata, are a major component of the diet of caiman lizards (Dracaena spp.) in South America (Perera and Walls, 1996). In the USA, the redear sunfish (Lepomis microlophus) was used as a biological control agent for P. maculata in a pond in Alabama although eradication was unsuccessful (Martin et al., 2012).

The bright pink eggs of P. maculata are generally thought of as being unpalatable to predators, as are those of P. canaliculata (Dreon et al., 2010). However, eggs and small juveniles of P. canaliculata (and perhaps therefore of P. maculata) are eaten by fire ants, Solenopsis geminata, in Asia, and these have been suggested as possible biocontrol agents (Way et al., 1998; Yusa, 2001), though introduction of such a major invasive pest would probably be inappropriate. A hemipteran and two orthopterans also eat the eggs of P. canaliculata (Yusa, 2006), and therefore also perhaps of P. maculata. Nonetheless, the extent of predation on P. maculata eggs by different species remains unclear. Red-eared slider turtles (Trachemys scripta elegans) may prey on eggs or hatchlings but ongoing research demonstrates limited consumption (R Burks, South Western University, Texas, USA, unpublished). By all field accounts, little damage occurs to the egg clutches. However, in one laboratory study, Horn et al. (2008) found that P. maculata adults readily consumed P. maculata eggs.

Means of Movement and Dispersal

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Active, short term dispersal does not necessarily translate into long term, long distance dispersal. P. maculata may spread naturally in the same ways as are thought to be the case for P. canaliculata, that is predominantly by floating downstream, although crawling upstream is also possible, unless the flow rate is too great (Ranamukhaarachchi and Wikramasinghe, 2006). However, the rapid spread of P. maculata within Asia following introduction has been predominantly human mediated.

Natural Dispersal

In both their native and introduced ranges P. maculata inhabit rivers with slow moving currents as well as isolated water bodies, such as lakes. In their non-native range, they often occur in canal or irrigation systems associated with wetland agriculture. Natural dispersal by floating downstream on the water current or during flooding (Martin et al., 2012) could result in expansion both within aquatic systems as well as (in the case of flooding) to other water bodies otherwise unconnected.

Vector Transmission

Snail kites (Rostrhamus sociabilis) are possible biological vectors. They prey on the snails, but if having picked up the snail they drop it some distance away (Cattau et al., 2010) this may lead to local expansion of the distribution. In Florida, the native snail, Pomacea paludosa, was the exclusive food of the kites until the introduction of P. maculata. The shells of P. paludosa are smaller, thinner and with a smaller aperture, making them easier to handle than P. maculata, which are then more likely to be dropped.

Intentional Introduction

The primary pathways of intentional introduction by people have been the aquaculture industry and the aquarium trade (Cowie, 2002; Cowie and Hayes, 2012). The former has probably been the main source of the invasion of P. maculata in Asia, while its presence in the continental USA is probably attributable to the latter.

As much of the literature on invasive apple snails in Asia has not distinguished P. maculata from P. canaliculata and because the latter seems more widespread in the region, it is difficult to draw inferences specifically regarding P. maculata. Nontheless, it can be assumed that P. maculata was introduced for the same reasons as was P. canaliculata, even if it was not distinguished from the latter. The impetus to introduce the snails was their perceived potential to provide an alternate, cheaper human food source as well as a gourmet product for export. The expansion of this enterprise probably resulted in the introduction of P. maculata to several countries. These intentional introductions eventually gave way to accidental introductions as these aquaculture projects failed, the markets having been over-estimated. Abandonment of the snail farms allowed the snails to escape and become major agricultural pests, as frequently reported for P. canaliculata (e.g. Naylor, 1996; Teo, 2004). The distribution of P. maculata in Asia now broadly overlaps that of P. canaliculata (Hayes et al., 2008, 2012).

The pet and aquarium trade present another source of both intentional and accidental introduction and this is probably the main if not only pathway of introduction of P. maculata to the USA (Karatayev et al., 2009; Martin et al., 2012). Either or both P. maculata and P. canaliculata were imported to Thailand by the aquarium trade but probably also for food (Keawjam and Upatham, 1990). In the USA the Department of Agriculture and other regulators now include P. maculata on watch or prohibited lists, but a different species of apple snail, P. diffusa (formerly P. bridgesii), that grazes algae on aquarium tanks remains available to the public through commercial pet stores. However, trade practice incorporates the collection and sale of young, immature snails that are much more difficult (or even impossible for a non-expert) to identify than are adults. Misidentification could then lead to customers buying a macrophyte-eating snail (P. maculata) instead of an algae-feeding snail (P. diffusa) and then, when the snail does not perform the desired function (i.e. cleaning the aquarium walls rather than eating the aquarium plants), owners dispose of the snails in local waterways (Martin et al., 2012).

Accidental Introduction

Eggs or hatchlings can be accidentally introduced to new locations as P. maculata females will lay clutches on any hard surface, including boats (EFSA Panel on Plant Health, 2012). If the clutch stays out of the water, it can develop over a period of two weeks or so and then hatch into a different body of water on the next boat trip, perhaps after the boat has travelled great distances on a trailer, as reported for zebra mussels by Britton and McMahon (2005). It is possible that snails (especially small juveniles or hatchlings) or their eggs may also be transported on wetland plants or propagules used for outplanting, as suggested for P. canaliculata (Cowie, 2002; Levin et al., 2006).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
AquaculturePossible food source Yes Yes
Crop productionMay have been introduced accidentally with other species Yes Mochida, 1991; Teo, 2004
Escape from confinement or garden escapeAfter snail farms were abandoned in SE Asia, snails dispersed Yes
Flooding and other natural disastersSnails or hatchlings could be moved via water flows Yes Yes Martin et al., 2012
FoodSome ethnicities might culture snails or collect locally Yes Yes
HitchhikerSnails eggs could be transported on the outside of boats Yes EFSA Panel on Plant Health, 2012
Intentional releaseTied to aquarium trade Yes Yes Karatayev et al., 2009; Martin et al., 2012
Interconnected waterwaysAs the snails are aquatic they can easily move between water bodies Yes Yes
Live food or feed tradeSome cultures may either rear snails or collect from local areas Yes
Pet tradeFrequency has never been quantified, but taxonomic confusion suggests it is not rare Yes Yes Karatayev et al., 2009; Martin et al., 2012
ResearchUnlikely to result in an establishment of an invasive population Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stockHatchlings, juveniles, adults Yes Yes
BaitJuveniles, adults (if used as bait) Yes Yes
Floating vegetation and debrisHatchlings, juveniles, adults Yes
Host and vector organismsJuveniles and adults Yes Yes
Pets and aquarium speciesJuveniles and adults Yes Yes
Plants or parts of plantsEggs, hatchlings Yes Yes
Ship hull foulingEggs, hatchlings Yes Yes
Ship structures above the water lineEggs, hatchlings Yes Yes
WaterHatchlings, juveniles and adults Yes Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Seedlings/Micropropagated plants eggs Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches eggs Yes Pest or symptoms usually visible to the naked eye
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Leaves
Roots
True seeds (inc. grain)
Wood

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Colocasia esculentaBurks et al., 2011. Other
Rostrhamus sociabilisCattau et al., 2010. OtherUSA

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Economic/livelihood Negative
Environment (generally) Negative
Human health Negative

Economic Impact

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No details of economic impacts exist for P. maculata because of past confusion between it and P. canaliculata. Estimates suggest that invasion of P. canaliculata into agricultural rice fields in Asia has resulted in millions of dollars worth of damage and loss (see CABI Invasive Species Compendium datasheet for P. canaliculata). P. maculata probably accounts for some proportion of the total amount; however, it remains difficult to determine whether or not past studies were based on P. maculataP. canaliculata or a mixture of the two species.

Environmental Impact

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Impact on Habitats

The snails’ herbivory is the main factor affecting habitats and the increasing spread of P. maculata populations, such as their invasion of the Florida Everglades, causes concern. Whilst quantitative consumption data remain uncollected from the field, various laboratory studies indicate that P. maculata acts as a generalist herbivore, and quickly consumes available resources. When given the opportunity, it can indiscriminately eliminate aquatic macrophytes by consuming them at a relatively rapid rate. On a small scale, the effects may not provoke action, but populations with higher densities would magnify this pattern and increase the ecological impact. In a study of P. canaliculata (the identification is probably correct), Laos Carlsson et al. (2004a) found that apple snail herbivory contributed to a shift in alternative stable states of a lake from a clear to a turbid condition. However, no studies on how P. maculata might alter ecosystem processes, particularly nutrient cycling, have been conducted. Nonetheless P. maculata may also be able to cause such an impact, which might be expected given the larger size of the species relative to P. canaliculata and other invertebrates.

Impact on Biodiversity

P. maculata may impact biodiversity through a number of different mechanisms including competition with native species and as a predator of native invertebrates, as studies have reported for P. canaliculata (see CABI Invasive Species Compendium datasheet for P. canaliculata). In an experiment testing the effects of density on Pomacea paludosa juveniles, Conner et al. (2008) found that one adult P. maculata had the equivalent impact of three to four P. paludosa on the native juveniles’ growth rates and survival. Their results imply that P. maculata range expansion could have a direct negative impact on P. paludosa populations, especially considering that juvenile survival may be particularly important for increasing population densities (Burlakova et al., 2009). This could negatively affect the snail kite (Rostrhamus sociabilis), an already declining bird species, which is locally endangered and usually feeds on P. paludosa. Although the snail kite can feed on P. maculata as an alternative, it often uses more energy trying to extract P. maculata from their shells and may use more resources flying back to suitable feeding perches (Cattau et al., 2010). Furthermore, such feeding attempts may prove unsuccessful. However, efforts have been made to facilitate consumption of P. maculata by the kites, for example managers have installed perches close to the water body where the birds can extract the snails rather than spending energy taking them back to a more distant location (Pias et al., 2012).

Social Impact

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Along with many other snail species, P. maculata can serve as an intermediate host for the parasitic nematode, Angiostrongylus cantonensis (rat lungworm) (Cowie, 2013b; Kim et al., 2014). Humans become infected when they ingest raw snails that are carrying infectious worm larvae. The larvae enter the person’s bloodstream and eventually end up in the brain, where after moving around for some time, they die. The neurological damage and immune reaction, the latter caused especially by the dead worms, cause eosinophilic meningitis. Patients suffer extreme ill effects and may die as a result of infection (Cowie, 2013b). Teem et al. (2013) reported infected P. maculata in Louisiana but the full extent of the distribution of infected P. maculata across the south eastern USA is not known. In Asia A. cantonensis is widespread in P. canaliculata (Lv et al., 2011), but as yet there has been no report of it in P. maculata. In the native range of P. maculata in South America the extent of the parasite’s distribution remains uncertain (Thiengo et al., 2013).

Risk and Impact Factors

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Uses

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Economic Value

A large market did not develop in Asia for introduced apple snails, primarily P. canaliculata but probably also including P. maculata. With the global need to find alternate protein sources, the culinary industries of various countries might explore further the use of apple snails as a local delicacy or ethnic cuisine. However, there is a risk of further spread of the snails, and consequent negative impacts, associated with such efforts.

Social Benefit

For professional researchers, because of the anatomical, physiological and behavioural adaptations of apple snails, the group in general provides a powerful model for addressing a number of ecological and evolutionary questions (Hayes et al., 2009b). Similarly, as an invasive species, P. maculata and other congeneric invasive species (primarily P. canaliculata but also P. diffusa) offer opportunities for addressing interesting questions of rapid evolution and adaptation (e.g. Hayes et al., 2009b; Matsukkura et al., 2013). Sometimes intentionally but frequently accidentally (due to taxonomic confusion and difficulty of identification), vendors might sell P. maculata as an aquarium snail for cleaning algae off aquarium walls. However, due to the snails’ preference for macrophytes over algae as a food resource, this species has limited application in the aquarium trade. The snail could be incorporated into educational displays in aquariums that teach about wetland ecosystems and some school teachers may use the large shells for art projects.

Environmental Services

Apple snails, though not P. maculata specifically, have been suggested for control of weeds in wetland rice (e.g. Wada, 2006). Another invasive apple snail, Marisa cornuarietis, has been suggested as a biocontrol agent for invasive weeds. While some people might see this as an environmental service, apple snails such as P. maculata that feed relatively indiscriminately on a wide range of macrophytes will have negative impacts on native and desirable vegetation and the animals associated with them (Robins, 1971; Simberloff and Stiling 1996; Cowie, 2002).

Uses List

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Animal feed, fodder, forage

  • Bait/attractant

General

  • Botanical garden/zoo
  • Pet/aquarium trade
  • Research model

Human food and beverage

  • Meat/fat/offal/blood/bone (whole, cut, fresh, frozen, canned, cured, processed or smoked)

Materials

  • Shell

Detection and Inspection

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Given their dark colouration, adult P. maculata may blend into their benthic sediments and be difficult to see. In contrast, the bright pink egg clutches cannot be missed in the landscape. These egg clutches provide a warning sign of a reproducing population (Burks et al., 2010; Kyle et al., 2011). Egg clutches are laid on emergent aquatic vegetation (Kyle et al., 2011) or on other hard surfaces above the water line, such as rocks, logs and various structures such as bridge supports, docks or quays, retaining walls, culverts, etc.). Newly laid clutches have a deeper pink colour and a noticeable gelatinous nature before they dry out and develop. These egg masses are very noticeable and can even be seen from a moving vehicle. When removing nuisance vegetation (e.g. taro in some parts of the USA), environmental managers should carefully inspect stems and leaves for the presence of clutches or hatchlings. Similarly, small watercraft (e.g. canoes, kayaks, paddle or fishing boats) that are moved between water bodies should be inspected for egg clutches.

In the native habitat, mounds of shells often indicate the presence of snail kites. In places to which they have been introduced, empty shells may occur along the margins of invaded habitat. Adult snails tend to occur near shore, in relatively shallow water (1 m deep) and within close proximity to stands of submerged macrophytes. Female snails may be found close to newly laid clutches. 

Similarities to Other Species/Conditions

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Species of Pomacea can be easily distinguished from those in other ampullariid genera (see figure 2 of Hayes et al., 2009b). Species in the Old World genus Pila, which also bear large, round, generally brownish or greenish dextrally coiling shells, have a brittle and calcified as opposed to a corneous and somewhat flexible operculum. Species of Lanistes, an African genus, appear to coil sinistrally, with the aperture to the left of the shell when viewed with the apex uppermost. The other Old World genera (AfropomusForbesopomusSaulea) include only a small number of species and are not likely to be encountered.

Among New World genera, the three species of Marisa are readily distinguished from species of Pomacea as they are planispirally coiled (the coils are almost flat) and are thus known commonly as giant ramshorn snails. Species of Asolene are generally small < 2 cm shell height) and usually yellow with brown bands. Felipponea species are small, and unlikely to be encountered. The genus Pomella is now treated as a synonym of Pomacea (Hayes et al., 2012); the animals bear very large round shells with a relatively enormous aperture compared to other Pomacea species.

Although the shells of many Pomacea species may be extremely variable, the shells of some species are sufficiently characteristic that they are readily distinguished from P. maculata. For example, the whorls of P. scalarisP. bridgesii and P. diffusa have a distinctive stair-like appearance, with the steps more sharply prominent in P. scalaris; the shell of P. papyracea is fragile and horny, with an almost black periostracum; and the shell of P. urceus is thick, solid, and black, with distinctive transverse ridges. Nevertheless, rather few Pomacea species can be identified definitively on the basis of the shell alone, and other morphological and molecular characters must be investigated to assist in correct identification. Also, the juveniles of many species are essentially indistinguishable morphologically.

The species with which P. maculata is most likely to be confused is P. canaliculata. The two species are extremely similar, and differences in size and subtle qualitative differences in shell shape fall within the range of individual variation, making them very difficult to distinguish morphologically (Hayes et al., 2012). However, they can be distinguished using both morphological and molecular characters, as described by Hayes et al. (2012)P. maculata generally has a thicker shell with a more distinctive angulate shoulder; the inner apertural lip is characteristically yellow to reddish-orange, which was also noted in the original descriptions of P. insularum and P. gigas, which are now treated as synonyms of P. maculata. Differences in shell morphology are most notable in newly hatched juveniles. The number of eggs laid per clutch is substantially higher in P. maculata (average ~1500) and the individuals eggs are much smaller, so that P. canaliculata hatchlings are nearly twice as large (shell width) as those of P. maculata. The operculum of P. maculata is also much thicker and more inflexible than that of P. canaliculata, creating a much less effective seal.

The most readily apparent anatomical differences are in the male penis sheath (Hayes et al., 2012). Both species possess two glands on the dorsal surface of the penis sheath. However, the apical gland of P. maculata is distinguished from that of P. canaliculata by lacking a rugose central glandular surface bordered by smoother glandular tissue. Nonetheless, the development of the two types of tissue varies with maturity and they may appear undifferentiated in younger individuals. Other species of Pomacea possess, in addition to an apical gland, both a medial and basal gland. And although both P. maculata and P. canaliculata possess two dorsal penis sheath glands, P. maculata lacks the medial gland, whereas P. canaliculata lacks the basal gland. Position and number of penial sheath glands for a number of ampullariid species have been tabulated by Hayes et al. (2015).

The two species are readily differentiated by DNA sequences (Rawlings et al., 2007; Matsukura et al., 2008; Hayes et al., 2008, 2009a, 2012).

Both P. maculata and P. canaliculata, as well as several other species that exhibit similar shell morphology, lay pink clutches above the water’s surface that are readily distinguished from those of a number of other species with similar shell morphology but that lay bright green eggs. The number of eggs laid per clutch is substantially higher in P. maculata (average ~1500) than in P. canaliculata (average <300) and the individual eggs are much smaller (Hayes et al., 2012). Egg size is a reliable way to distinguish the two species, although it may not be so useful when other pink egg laying species are also present.

The other Pomacea species most likely to be encountered is P. diffusa. In the past, this species has been misidentified as P. bridgesii, which is generally larger. P. diffusa is the most common ampullariid in the aquarium pet trade (Perera and Walls, 1996). It can be distinguished from P. maculata by its more square-shouldered whorls, as indicated above, and the fact that the suture (the junction between successive whorls) is not deeply channelled. Nonetheless, distinguishing these species (at least when the much larger P. maculata are juvenile) on the basis of these shell characteristics is not easy and requires considerable experience, especially given the variability in shell shape within these species. Shell colour, the pattern of darker bands running spirally around the shell and the colour of the animal inside should not be considered diagnostic of species of Pomacea, and cannot be used to distinguish P. diffusa from P. maculata, especially as there are many colour varieties of P. diffusa that have been specially bred for the aquarium trade.

P. paludosa is the only native North American species of Pomacea, occurring in southeastern USA and Cuba. Although its shell is coloured similarly to that of P. maculata, adults are smaller than those of P. maculata and the suture between successive whorls is not deeply channelled, making it fairly readily distinguished, at least as adults, from P. maculata.

Other species that may be confused with P. maculata are P. lineata and P. dolioides. Both have brown shells, often with spiral bands; they are much smaller than P. maculata as adults and the shells are usually thinner. They tend to have more prominent shell spires, though this character is variable in all three species, and the sutures between their whorls are not deeply channellized.

Prevention and Control

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Most of the literature on management of apple snail pests undoubtedly refers to P. canaliculata, which is the most widespread introduced species of Pomacea in Asia. However, because of the past confusion regarding the identities of the species introduced to Asia, some of the information purportedly relating to P. canaliculata may relate to either or both P. canaliculata and P. maculata. The Invasive Species Compendium datasheet for P. canaliculata should be accessed for much information regarding prevention and control related to P. canaliculata, as the same information is mostly pertinent also to P. maculata. Much of the following information is additional information specific to the USA and to P. maculata.

Prevention

As for any invasive species, early detection, prompt eradication and strong regulation of transport are the best defenses against introduction and establishment of P. maculata as an alien invasive species. The first sign of an infestation is usually the presence of pink eggs, which are highly visible above the water line. A concerted effort must then be made (perhaps involving volunteers) to remove and destroy as many egg clutches as possible and perhaps to focus efforts on collecting female snails as they deposit clutches, typically around dawn. Additional educational materials should also be distributed to alert community members to new infestations, which should be reported promptly to the authorities (Martin et al., 2012). Raising public awareness is not only important to prevent the further spread of Pomacea species in Asia and elsewhere (e.g. USA, Europe), but also to warn people in regions in which parasites such as Angiostrongylus cantonensis occur of the dangers of infection.

In the USA, the US Department of Agriculture through its Plant Protection and Quarantine program prohibits interstate transport of P. maculata without a permit. Along with P. canaliculata, pro-active states (i.e. Texas, Florida, South Carolina) have put P. maculata on a list of prohibited species. Other states where snails have invaded (i.e. Alabama, Louisiana, Mississippi, Georgia) should be encouraged to adopt similar measures. Communication of the potential negative impacts of P. maculata on human health (as a vector of Angiostrongylus cantonensis) and agriculture (as a consumer of rice and other wetland crops) has recently raised public awareness, but only to a limited extent. In terms of education, a number of non-profit organizations as well as state and federal agencies have produced factsheets about the species but these vary substantially in their accuracy; see Dyke (2013) for current reliable information. In areas where snails have invaded, ecologists and resource managers should conduct routine surveys for the presence of pink egg clutches along lake or pond margins or riparian zones of streams and rivers.

Eradication

Eradication may be possible for small, established P. maculata populations restricted to isolated bodies of water. For example, biologists in Mobile, Alabama, reported anecdotal eradication of a population of snails found in a small neighbourhood lake; constant surveillance of the pond and destruction of clutches were reported as the key mechanisms for the eradication success (Martin et al., 2012).

Control

Cultural Control and Sanitary Measures

Numerous cultural control measures have been implemented for P. canaliculata (see the Invasive Species Compendium datasheet for P. canaliculata) and are probably also applicable to P. maculata.

In addition, and this applies to both P. maculata and P. canaliculata, and indeed to any snail or slug species, to guard against infection by the nematode parasite Angiostrongylus cantonensis, raw snails should never be consumed (Cowie, 2013a). Educational efforts should advise small children not to play with snails. Yeung et al. (2013) recommended carefully washing all produce for human consumption that might be contaminated.

Physical/Mechanical Control

In a few cases in the USA, managers have tried hand removal of snails and eggs as a strategy to reduce population size and growth. Although a useful control method for an early detected, small invasion of P. maculata, hand removal of adults is time consuming and some snails can still go undetected making the control treatment ineffective (Martin et al., 2012). Egg clutches on the other hand can be easily observed. Clutches should be physically destroyed by crushing.

In Florida, initial control efforts in Wellman’s Pond focused on hand collection of snails but this proved extremely time consuming and ineffective. Subsequent efforts were more successful and the use of snail traps facilitated the removal of four tons of P. maculata from the pond between April and July 2008. The removal of P. maculata allowed for the persistence of important aquatic vegetation.

One effort to detect and capture snails involves traps (Martin et al., 2012; Dyke, 2013). The donut-shaped black plastic trap sits on top of the sediment, held in place by a PVC pipe. Baited with a proprietary blend of food resources, the trap attracts snails, which enter, but the shape of the trap makes it more difficult for them to exit. The basic model does not have a grate to keep snails inside indefinitely. This requires the user to check the trap often (i.e. daily) to remove snails. Depending on the density of the population and the availability of resources, traps may be deployed for longer periods with the added security of a grate.

Biological Control

The only published example of biological control of P. maculata in the USA is in Langan Pond in Mobile, Alabama, where 14,000 native redear sunfish (Lepomis microlophus) were released to control P. maculata hatchlings (Martin et al,. 2012)Although eradication of the species was unsuccessful, the outcomes of this effort suggested that a diversity of fishes might help control the enormous numbers of small snail hatchlings produced by P. maculata. A few studies have been done in Asia on the use of fish to control P. canaliculata (see the Invasive Species Compendium datasheet for P. canaliculata).

Chemical Control

No species-specific pesticide exists for P. maculata and traditional molluscides may fail because of the ability of the snails to close the operculum for long periods of time. In the USA, use of chelated copper (e.g. Cutrine, Komeen, KTK-Tea, Captain) or copper sulfate represents the most widely used method of chemical control for P. maculata. As one example, in Florida, the St. John’s Water Management District (SJFMD) in cooperation with the Florida Fish and Wildlife Conservation Commission (FWCC) applied copper sulfate to Newnans’ Lake in 2007. Heavy snail mortality occurred but eggs were still found the following year. The Department of Natural Resources in South Carolina also used copper sulfate to kill snails in a small pond. They estimated the cost of application at $2.50/lb [$5.50/kg]. Martin et al. (2012) described a case study of repeated copper sulfate application to Langan Pond and Three Mile Creek in Mobile, Alabama. Overall, they applied four tons of copper sulfate in an attempt to prevent the snail invasion from reaching the Mobile-Tensaw Delta. In this case, high snail mortality occurred (50-75%) but some large, adult snails still persisted. Snails survived by filling their shells with air and floating away from the pesticide application. This may have indirectly contributed to the spread of P. maculata. Overall, application of copper sulfate is one of the most expensive control measures. Furthermore, few studies have investigated the indirect impacts of the pesticide on ecosystems. In addition to poisoning the snails themselves, all other invertebrates in the ecosystem, desirable or not, native or introduced, will be killed. An alternative chemical control measure might include herbicides that reduce weedy, emergent vegetation on which the snails lay egg clutches (Burks et al., 2010).

Monitoring and Surveillance

Continued surveillance for pink clutches on any number of hard substrates should be implemented (Burks et al., 2010; Kyle et al., 2011). In the USA, efforts should pay special attention to stands of other invasive plants, notably wild taro (C. esculenta), with which P. maculata is frequently associated.

Gaps in Knowledge/Research Needs

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There is much less knowledge of the general biology P. maculata than for the more well-known P. canaliculata (Hayes et al., 2015). Further research especially on its genetics, reproductive biology and physiological tolerances are required. The effectiveness of different control strategies and the potential for “invasional meltdown” (Simberloff and Von Holle, 1999) with other exotic species such as taro (Colocasia esculenta) also warrants further investigation. Furthermore, research to measure the proportion of snails infected by Angiostongylus or other parasites and assess the risk to human health is needed.

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Yusa Y, 2006. Predators of the introduced apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae): their effectiveness and utilization in biological control. In: Global advances in ecology and management of golden apple snails [ed. by Joshi, R. C.\Sebastian, L. S.]. Los Baños, Philippines: Philippine Rice Research Institute (PhilRice), 345-361.

Links to Websites

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WebsiteURLComment
Research profile of Dr. Kenneth Hayeshttps://www.researchgate.net/profile/Kenneth_Hayes/
Snail Bustershttp://snailbusters.wordpress.com
The Cowie Lab at the University of Hawaiihttp://www.hawaii.edu/cowielab/
The Pomacea Projecthttp://www.pomaceaproject.org

Contributors

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18/05/2015 Reviewed by:

Rob Cowie, University of Hawaii, USA 

22/07/13 Original text by:

Romi L. Burks, Department of Biology, Southwestern University, 1001 East University Avenue, Georgetown, TX 78626, USA 

Amy E. Miller, Animal Behaviour Program, Southwestern University, 1001 East University Avenue, Georgetown, TX 78626, USA 

Alexandria L. Hill, Department of Biology, Southwestern University, 1001 East University Avenue, Georgetown, TX 78626, USA