d’Orbigny 1935

"On a global basis...the two great

destroyers of biodiversity are, first

habitat destruction and, second,

invasion by exotic species”

- E.O. Wilson

Invasive Ampullariidae

(Mollusca: Caenogastropoda)

Kenneth A. HayesHoward University, Department of Biology

Washington, DC

National Plant Diagnostic Network Malacology Workshop

UC Davis 16-18 June 2015

What are Apple Snails?

Freshwater snails in the family Ampullariidae

Afropomus SauleaLanistesPilaMarisaPomacea PomellaAsolene

117 23 12173 303

Felipponea

Berthold 1991; Bieler 1993;

Cowie & Thiengo 2003; Hayes et al. 2009, 2014

Invasion Biology• Introduced around the world

– Aquaculture and aquarium trade

– SE Asia, Spain, USA, Iran, Russia, Pacific

Islands, Africa, India

– Major pest of rice and other aquatic crops

– Major environmental pest

Disease Ecology and Public HealthAngiostrongylus cantonensis

Lv. et al. 2011

Photo: Camila Krug

Graeff-Teixeira et al 2009

Jaynee R. Kim, Kenneth A. Hayes, Norine W. Yeung and Robert H. Cowie

Norine W. Yeung, Kenneth A. Hayes, and Robert H. Cowie

A. cantonensis in rat brain

– Pila sp.

– Pila dolioides

– Pomacea sp.

– Pomacea canaliculata

– Pomacea lineata

– Pomacea cuprina

– Pomacea gigas

– Pomacea insularum

– Pomacea insularis

– Pomacea insularus

− Pomacea scalaris

− Pomacea bridgesii

− Pomacea diffusa

− Pomacea cuprina

− Pomacea haustrum

− Pomacea paludosa

− Ampullarius sp.

− Ampullarium canaliculata

− Ampullaria cuprina

− Ampullaria levior

− Ampullarium insularum

Invasive Apple Snails

Agricultural DamageNumber 1 Rice Pest in SE Asia Number 1 Taro Pest in Hawaii

Damage

• Alteration of ecosystems

– Near complete removal of aquatic vegetation

– Competition with native herbivores

– Consumption of native snails and invertebrates

• Trophic shifts

– Macrophyte dominated to phytoplankton dominated

• Declining biodiversity and ecosystem stability

Aditya & Raut 2002; Carlsson et al. 2004; Carlsson & Lacoursiere 2005; Wood et

al. 2005; Carlsson & Bronmark 2006

“The relationships of the numerous species described, remains,

however, in a state of hopeless confusion” Pain 1960

“The limits among species are exclusively based on personal

opinions that are seldom transmissible:

the species is in the eye of the expert” Cazzaniga 2002

Systematic Confusion

Phylogenetics

• 5 loci (2 mtDNA, 3 nDNA)

• >1500 snails• 51 New World species

• 13 Old World species

• >2500 Sequences

• Integrative taxonomy

– Molecules

– Morphology

– Ecology

– Biogeography

Hayes et al. 2009;

Hayes 2009

New World

Old World

Marisa cornuarietisAsolene spixiiPomacea diffusa

NOT bridgesii

Planorbella sp. Biompholaria sp.

Marisa cornuarietis

Pomacea canaliculata

Pomacea maculata

USA Rice Growing States

Figure 2. Present populations of the island apple snail, Pomacea insularum, and its occupiable

area.

Byers JE, McDowell WG, Dodd SR, Haynie RS, Pintor LM, et al. (2013) Climate and pH Predict the Potential Range of the Invasive

Apple Snail (Pomacea insularum) in the Southeastern United States. PLoS ONE 8(2): e56812. doi:10.1371/journal.pone.0056812

http://127.0.0.1:8081/plosone/article?id=info:doi/10.1371/journal.pone.0056812

Systematic Revision of Ampullariidae

Hayes et al. 2012

Pomacea maculata and P. canaliculata

≤ 2 mm ≥ 3 mm

L

Ct

Lung and Siphon

MarisaPomacea

Asolene

Gill

Lung

Hayes et al. 2012

ShortLong

Medium

Hayes et al. 2012

Hayes et al. 2012

P. canaliculataP. maculata

Reproductive Anatomy

Modified from Gamarra-Luques et al. 2006 and Ghesquiere, 2005

Reproductive Anatomy

P.

maculata

P.

canaliculata

Hayes et al. 2012

Reproductive Anatomy

S.A. Ghesquiere – applesnail.net Hayes et al. 2012

≤ 2 mm

Eggs

≥ 3 mm

Mean clutch size ~260 eggs Mean clutch size ~1600 eggs

P. canaliculataP. maculata

Hayes et al. 2012

Egg Morphology

Hayes et al. 2009, 2015

Oviposition Location

Copulatory apparatus

Penis & Sheath

Reproductive Anatomy

Hayes et al. 2009; Hayes 2009; Hayes et al. 2012

Gamarra-Luques et al. 2006

Ghesquiere

Pomacea canaliculata

Pomacea maculata

Rawlings, Hayes, Cowie & Collins, 2007

Cowie, Hayes, Tran & Levin, 2007.

Hayes, Joshi, Thiengo & Cowie, 2008

Tran, Hayes & Cowie, 2008. Malacologia

P. maculata

Molecular Systematics

In Reality

Hayes et al. In PrepPomacea paludosa

Silvana Thiengo

Aline Mattos

Sonia Barbosa dos Santos

Aline Schilithz

Monica Fernandez

Wellington Costa

Alfredo Castro-Vazquez

Ricardo San Martin

Fábio Faraco

Francisco Feitosa

Luiz Jorge Pinheiro

Jean-Pierre Pointier

Tim Rawlings

Tim Collins

Ravi Joshi

María Virginia De La Hoz

Francisco J. Borreo

André Favaretto Barbosa

Pablo Coelho

José & Suzana Almato

Maria E. Diupotex-Chong

Néstor Cazzaniga

Helena Fortunato

Dr. W. Lobato Paraense

Dr. Lygia Corrêa

Romi Burks

Roland Schultheiß

Christian Albrecht

Philippe Bouchet

John Slapcinsky

Acknowledgments

David Robinson

Suzete Gomes

Rob Cowie

Ellen Strong

Norine Yeung

Jaynee Kim

Gary Rosenberg

Bob Howells

Marty Meyer

Dick HoenischNational Plant Diagnostic Network

Smithsonian Tropical Research Institute

Thank You

Pomacea canaliculata