Adaptations to host infection and larval parasitism in Unionoida

Abstract Freshwater mussel larval parasitism of fish is unique among bivalves. The relationship is primarily phoretic rather than nutritive; only the smallest glochidia and the haustorial larva grow substantially while on the host. Growth of the smallest larvae suggests a lower functional size limit of ∼150 μm for the juvenile stage. Most Ambleminae, the most diverse North American clade, infect host gills by attracting feeding fish. Many species of Pleurobemini and some Lampsilini release conglutinates of eggs and larvae that resemble host food items. Many Lampsilini and a few Quadrulini use mantle modifications to attract host fish to the female. The mantle of some Quadrulini forms a posterior chamber that holds glochidia for immediate release in response to host fish. In many Lampsilini, mantle flap lures and a protrusible marsupium promote attack by the host fish and direct extraction of glochidia from the marsupium by the host. Host extraction of glochidia from the brooding female might have favored the evolution of long-term brooding in Lampsilini because glochidia need not be released by the female to encounter the host. A remarkable derivative of the host extraction strategy evolved in Epioblasma, which catch fish between the valves and release glochidia directly to the trapped host before releasing it. Host specificity is a critical feature of the evolutionary diversification and conservation biology of Unionoida. As temporary parasites, mussels must primarily evade the innate immune responses of the host, rather than the adaptive (acquired) responses. Evolution of host specificity is associated with selective encounter of host taxa, either because of host attraction strategies or because of dominance of particular host species in the habitat. The intricate relationships between mussels and fish are easily disrupted and, thus, contribute to the imperilment of many mussel species, yet they also fascinate us and compel conservation efforts.

[1]  Constance L Rogers-Lowery,et al.  Encapsulation of Attached Ectoparasitic Glochidia Larvae of Freshwater Mussels by Epithelial Tissue on Fins of Naïve and Resistant Host Fish , 2006, The Biological Bulletin.

[2]  R. V. Dimock,et al.  ACQUIRED RESISTANCE OF BLUEGILL SUNFISH LEPOMIS MACROCHIRUS TO GLOCHIDIA LARVAE OF THE FRESHWATER MUSSEL UTTERBACKIA IMBECILLIS (BIVALVIA: UNIONIDAE) AFTER MULTIPLE INFECTIONS , 2003, The Journal of parasitology.

[3]  J. Welsh Photic Stimulation and Rhythmical Contractions of the Mantle Flaps of a Lamellibranch. , 1933, Proceedings of the National Academy of Sciences of the United States of America.

[4]  W. Haag,et al.  Mantle displays of freshwater mussels elicit attacks from fish , 1999 .

[5]  D. Lane,et al.  Byssus drifting and the drifting threads of the young post-larval mussel Mytilus edulis , 1985 .

[6]  D. Waller,et al.  Gill tissue reactions in walleye Stizostedion vitreum vitreum and common carp Cyprinus carpio to glochidia of the freshwater mussel Lampsilis radiata siliquoidea , 1989 .

[7]  G. Bauer The adaptive value of offspring size among freshwater mussels (Bivalvia, Unionoidea) , 1994 .

[8]  C. Titman,et al.  The dispersal of young post-larval bivalve molluscs by byssus threads , 1976, Nature.

[9]  W. Hoeh,et al.  Eurytopic Host Use by Two Congeneric Species of Freshwater Mussel (Pelecypoda: Unionidae: Anodonta) , 1982 .

[10]  C. Lydeard,et al.  Molecular systematics and evolution of reproductive traits of North American freshwater unionacean mussels (Mollusca: Bivalvia) as inferred from 16S rRNA gene sequences. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  Eric R. Pianka,et al.  On r- and K-Selection , 1970, The American Naturalist.

[12]  H. Hannibal ON ORTMANN'S "NOTES UPON THE FAMILIES AND GENERA OF THE NAJADES". , 1912, Science.

[13]  Y. Loya,et al.  Hydrodynamic impediments to settlement of marine propagules. and adhesive-filament solutions , 1994 .

[14]  W. Jansen Seasonal prevalence, intensity of infestation, and distribution of glochidia of Anodonta grandis simpsoniana Lea on yellow perch, Perca flavescens , 1991 .

[15]  Charles F. Rabeni,et al.  Sediment in Streams: Sources, Biological Effects, and Control , 1997 .

[16]  Brian T. Watson,et al.  Life history and population biology of the endangered tan riffleshell (Epioblasma florentina walkeri) (Bivalvia: Unionidae) , 2001, Journal of the North American Benthological Society.

[17]  J. E. Buhay,et al.  Molecular systematics of the North American freshwater bivalve genus Quadrula (Unionidae: Ambleminae) based on mitochondrial ND1 sequences. , 2003, Molecular phylogenetics and evolution.

[18]  HAAG'AND,et al.  Host fishes and infection strategies of freshwater mussels in large Mobile Basin streams , USA , 2003 .

[19]  J. Williams,et al.  Reproductive biology of four freshwater mussels (Bivalvia: Unionidae) endemic to eastern Gulf Coastal Plain drainages of Alabama, Florida, and Georgia , 2002 .

[20]  R. E. Call A study of the unionidae of Arkansas : with incidental reference to their distribution in the Mississippi Valley / by R. Ellsworth Call. , 1895 .

[21]  R. E. Millemann,et al.  Glochidiosis of salmonid fishes. IV. Humoral and tissue responses of coho and chinook salmon to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae). , 1978, The Journal of parasitology.

[22]  R. Blažek,et al.  Temporal and spatial distribution of glochidial larval stages of European unionid mussels (Mollusca: Unionidae) on host fishes. , 2006, Folia parasitologica.

[23]  G. Bauer,et al.  Ecology and Evolution of the Freshwater Mussels Unionoida , 2012, Ecological Studies.

[24]  K. Roe,et al.  Hamiota, a new genus of freshwater mussel (Bivalvia: Unionidae) from the Gulf of Mexico drainages of the southeastern United States , 2005 .

[25]  L. B. Arey A microscopical study of glochidial immunity , 1932 .

[26]  Jess W. Jones,et al.  A HOLISTIC APPROACH TO TAXONOMIC EVALUATION OF TWO CLOSELY RELATED ENDANGERED FRESHWATER MUSSEL SPECIES, THE OYSTER MUSSEL EPIOBLASMA CAPSAEFORMIS AND TAN RIFFLESHELL EPIOBLASMA FLORENTINA WALKERI (BIVALVIA: UNIONIDAE) , 2006 .

[27]  M. Ramos,et al.  Life-History Data on the Virtually Unknown Margaritifera auricularia , 2001 .

[28]  L. B. Arey THE FORMATION AND STRUCTURE OF THE GLOCHIDIAL CYST , 1932 .

[29]  Klaus Wächtler,et al.  Larval Types and Early Postlarval Biology in Naiads (Unionoida) , 2001 .

[30]  A. Martel,et al.  Distribution and density of glochidia of the freshwater mussel Anodonta kennerlyi on fish hosts in lakes of the temperate rain forest of Vancouver Island , 2005 .

[31]  B. Anson,et al.  Phases in the Parasitism of the Unionidae , 1922 .

[32]  Daniel L. Graf The Etherioidea revisited: a phylogenetic analysis of hyriid relationships (Mollusca: Bivalvia: Paleoheterodonta: Unionoida) , 2000 .

[33]  J. Endler Frequency-dependent predation, crypsis and aposematic coloration. , 1988, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  James D. Williams,et al.  Morphological variation in glochidia shells of six species of Elliptio from Gulf of Mexico and Atlantic Coast drainages in the southeastern United States , 2003 .

[35]  G. Watters The Evolution of the Unionacea in North America, and Its Implications for the Worldwide Fauna , 2001 .

[36]  M. Barnhart,et al.  Effects of Temperature, pH, and CO2 on Transformation of the Glochidia of Anodonta suborbiculata on Fish Hosts and in Vitro , 1999, Journal of the North American Benthological Society.

[37]  C. Ingersoll,et al.  Laboratory Toxicity Testing with Freshwater Mussels , 2006 .

[38]  R. Neves,et al.  Reproductive Biology of Four Species of Freshwater Mussels (Molluscs: Unionidae) in the New River, Virginia and West Virginia , 1992 .

[39]  S. Norris Osteology of the southwestern darters, Ethostoma (Oligocephalus) (Teleostei, Percidae) - with comparison to other North American percid fishes , 2001 .

[40]  E. Howerth,et al.  Experimentally Induced Glochidiosis in Smallmouth Bass (Micropterus dolomieu) , 2006, Veterinary pathology.

[41]  H. Vicentini Unusual spurting behaviour of the freshwater mussel Unio crassus , 2005 .

[42]  Joong-Ki Park,et al.  Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments. , 2000, Molecular phylogenetics and evolution.

[43]  Daniel L. Graf,et al.  THE EVOLUTION OF BROODING CHARACTERS AMONG THE FRESHWATER PEARLY MUSSELS (BIVALVIA: UNIONOIDEA) OF NORTH AMERICA , 2000 .

[44]  Ron B. H. Wills,et al.  Effects of temperature. , 2007 .

[45]  R. Murphy,et al.  Population structure and mantle display polymorphisms in the wavy-rayed lampmussel, Lampsilis fasciola (Bivalvia: Unionidae) , 2007 .

[46]  L. Holland-Bartels,et al.  Reproductive Characteristics of a Population of the Washboard Mussel Megalonaias nervosa (Rafinesque 1820) in the Upper Mississippi River , 1993 .

[47]  J. Rhymer,et al.  Determination of fish host use by wild populations of rare freshwater mussels using a molecular identification key to identify glochidia , 2008, Journal of the North American Benthological Society.

[48]  Jess W Jones,et al.  Life History and Propagation of the Endangered Fanshell Pearlymussel, Cyprogenia stegaria Rafinesque (Bivalvia:Unionidae) , 2002, Journal of the North American Benthological Society.

[49]  F. J. Dwyer,et al.  Differential exposure, duration, and sensitivity of unionoidean bivalve life stages to environmental contaminants , 2008, Journal of the North American Benthological Society.

[50]  Larry J. Weber,et al.  Effects of substrate and hydrodynamic conditions on the formation of mussel beds in a large river , 2006, Journal of the North American Benthological Society.

[51]  A. Beaumont,et al.  Aspects of veliger larval growth and byssus drifting of the spat of Pecten maximus and Aequipecten (Chlamys) opercularis , 1992 .

[52]  E. Wood Some mechanisms involved in host recognition and attachment of the glochidium larva of Anodonta cygnea (Mollusca: Bivalvia) , 2009 .

[53]  C. Vogel,et al.  The parasitic stage of the freshwater pearl mussel (Margaritifera margaritifera L.). I: Host response to glochidiosis , 1987 .

[54]  A. Zale,et al.  Reproductive Biology of Four Freshwater Mussel Species (Mollusca: Unionidae) in Virginia , 1982, Freshwater Invertebrate Biology.

[55]  J. McNair,et al.  Silk filaments enhance the settlement of stream insect larvae , 2006, Oecologia.

[56]  A. McIvor,et al.  Gill evacuation and release of glochidia by Unio pictorum and Unio tumidus (Bivalvia: Unionidae) under thermal and hypoxic stress , 2003 .

[57]  R. Murphy,et al.  Evolution of active host-attraction strategies in the freshwater mussel tribe Lampsilini (Bivalvia: Unionidae). , 2006, Molecular phylogenetics and evolution.

[58]  A. Simons,et al.  Identification of a Fish Host of the Inflated Heelsplitter Potamilus inflatus( Bivalvia: Unionidae) with a Description of Its Glochidium , 1997 .

[59]  G. Bauer,et al.  Glochidial Mortality in Freshwater Mussels , 2001 .

[60]  L. Atkins Corrigenda - Observations on the Glochidial Stage of the Freshwater Mussel Hyridella (Hyridella) drapeta (Iredale) (Mollusca : Pelecypoda) , 1979 .

[61]  P. Kat,et al.  PARASITISM AND THE UNIONACEA (BIVALVIA) , 1984 .

[62]  W. C. Curtis,et al.  Studies on the reproduction and artificial propagation of fresh-water mussels [by] George Lefevre and Winterton Conway Curtis] , 2011 .

[63]  M. Ramos,et al.  Glochidium metamorphosis in the endangered freshwater mussel Margaritifera auricularia (Spengler, 1793): A histological and scanning electron microscopy study , 2002, Journal of morphology.

[64]  Resmrch Stnfion,et al.  An extraordinary reproductive strategy in freshwater bivalves : prey mimicry to facilitate larval dispersal , 2004 .

[65]  A. Bonetto,et al.  Taxonomy and zoogeographic relationships of the South American naiades (Pelecypoda : Unionacea and Mutelacea) , 1963 .

[66]  W. I. Utterback The Naiades of Missouri , 2010 .

[67]  Michael J. Sanderson,et al.  Homoplasy. The Recurrence of Similarity in Evolution. , 1997 .

[68]  G. Watters Morphology of the Conglutinate of the Kidneyshell Freshwater Mussel, Ptychobranchus fasciolaris , 1999 .

[69]  D. Allen,et al.  Early Life-history and Conservation Status of Venustaconcha Ellipsiformis (Bivalvia, Unionidae) in Minnesota , 2007 .

[70]  R. Coker,et al.  A NOTE ON THE METAMORPHOSIS OF THE MUSSEL LAMPSILIS LÆVISSIMUS , 1911 .

[71]  M. Young,et al.  The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland. II: Laboratory studies , 1984 .

[72]  G. Fryer The developmental history of Mutela bourguignati (Ancey) Bourguignat (Mollusca: Bivalvia) , 1961, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[73]  Demorest Dawnport,et al.  NOTES ON THE RELATIONSHIP BETWEEN THE FRESHWATER MUSSEL ANODONTA IMPLICATA SAY AND THE ALEWIFE POMOLBUS PSEUDOHARENGUS (WILSON)1 , 1965 .

[74]  M. Mccollough,et al.  The Freshwater Mussels of Maine , 2000 .

[75]  W. H. Dall A Monograph of the Naiades of Pennsylvania , 1911 .

[76]  H. W. Clark,et al.  Natural History and Propagation of Fresh-Water Mussels , 2010 .

[77]  W. Haag,et al.  Effects of light and presence of fish on lure display and larval release behaviours in two species of freshwater mussels , 2000, Animal Behaviour.

[78]  J. E. Buhay,et al.  Phylogeny of North American amblemines (Bivalvia, Unionoida): prodigious polyphyly proves pervasive across genera , 2005 .

[79]  H. Dartnall,et al.  The distribution of glochidia of the Swan mussel, Anodonta cygnea (Mollusca) on the Three‐spined stickleback Gasterosteus aculeatus (Pisces) , 2009 .

[80]  E. Hartfield,et al.  OBSERVATIONS ON THE CONGLUTINATES OF PTYCHOBRANCHUS GREENI (CONRAD, 1834) (MOLLUSCA : BIVALVIA : UNIONOIDEA) , 1996 .

[81]  T. Haggerty,et al.  Reproductive phenology in Megalonaias nervosa (Bivalvia: Unionidae) in Wheeler Reservoir, Tennessee River, Alabama, USA , 2005, Hydrobiologia.

[82]  R. Neves,et al.  Life history of the Endangered Fine rayed Pigtoe Fusconaia cuneolus (Bivalvia, Unionidae) in the Clinch River, Virginia , 1993 .

[83]  M. E. Gordon,et al.  GAMETOGENETIC CYCLE, REPRODUCTIVE ANATOMY, AND LARVAL MORPHOLOGY OF POPENAIAS POPEII (UNIONOIDA) FROM THE BLACK RIVER, NEW MEXICO , 2003 .

[84]  F. J. Dwyer,et al.  Standard guide for conducting laboratory toxicity tests with freshwater mussels , 2006 .

[85]  Jess W. Jones,et al.  Life history and propagation of the endangered dromedary pearlymussel (Dromus dromas) (Bivalvia:Unionidae) , 2004, Journal of the North American Benthological Society.

[86]  M. Barnhart,et al.  Fish Hosts and Culture of Mussel Species of Special Concern: Annual Report for 2000 , 2000 .

[87]  W. Threlfall SEASONAL OCCURRENCE OF ANODONTA-CATARACTA SAY, 1817, GLOCHIDIA ON 3-SPINED STICKLEBACKS, GASTEROSTEUS-ACULEATUS LINNAEUS , 1986 .

[88]  W. C. Curtis,et al.  Reproduction and parasitism in the Unionidæ , 1910 .

[89]  J. B. Box,et al.  Reproductive Biology and Juvenile Recruitment of the Shinyrayed Pocketbook, Lampsilis subangulata (Bivalvia: Unionidae) in the Gulf Coastal Plain , 1999 .

[90]  W. Hoeh,et al.  A Phylogenetic Perspective on the Evolution of Morphological and Reproductive Characteristics in the Unionoida , 2001 .

[91]  R. Neves,et al.  Occurrence of glochidia in stream drift and on fishes of the upper north fork holston river virginia usa , 1988 .

[92]  R. V. Dimock,et al.  Ultrastructure of the mushroom body: digestion during metamorphosis of Utterbackia imbecillis (Bivalvia: Unionidae) , 2005 .

[93]  T. Iwakuma,et al.  Survival of Glochidial Larvae of the Freshwater Pearl Mussel, Margaritifera laevis (Bivalvia: Unionoida), at Different Temperatures: A Comparison Between Two Populations With and Without Recruitment , 2007, Zoological science.

[94]  E. Gisbert,et al.  The European sturgeon Acipenser sturio is a suitable host for the glochidia of the freshwater pearl mussel Margaritifera auricularia , 2007 .

[95]  M. Ramos,et al.  Description of the glochidium of Margaritifera auricularia (Spengler 1793) (Bivalvia, Unionoidea) , 1998 .

[96]  W. Haag,et al.  Host Fishes and Host-attracting Behavior of Lampsilis altilis and Villosa vibex (Bivalvia: Unionidae) , 1999 .

[97]  Floriano Papi,et al.  Monitore Zoologico Italiano , 1952 .

[98]  M. Barnhart,et al.  Persistence of host response against glochidia larvae in Micropterus salmoides. , 2006, Fish & shellfish immunology.

[99]  B. Morton,et al.  Site selection and attachment duration of Anodonta woodiana (Bivalvia: Unionacea) glochidia on fish hosts , 1984 .

[100]  F. R. Lillie The embryology of the unionidae. A study in cell‐lineage , 1895 .

[101]  G. Watters A Brief Look at Freshwater Mussel (Unionacea) Biology , 2006 .

[102]  J. Jokela,et al.  Reproductive tactics in Anodonta clams: parental host recognition , 1993, Animal Behaviour.

[103]  Wendell R. Haag,et al.  Role of ecological factors and reproductive strategies in structuring freshwater mussel communities , 1998 .

[104]  W. Haag,et al.  Host Fishes and Reproductive Biology of 6 Freshwater Mussel Species from the Mobile Basin, USA , 1997, Journal of the North American Benthological Society.

[105]  R. Parker,et al.  Ecology and Reproductive Strategy of a South Louisiana Freshwater Mussel, Glebula rotundata (Lamarck) (Unionidae:Lampsilini) , 1984, Freshwater Invertebrate Biology.

[106]  T. Newton,et al.  Thermal Criteria for Early Life Stage Development of the Winged Mapleleaf Mussel (Quadrula Fragosa) , 2007 .

[107]  James D. Williams,et al.  Evaluation of conservation status, distribution, and reproductive characteristics of an endemic Gulf Coast freshwater mussel, Lampsilis australis (Bivalvia: Unionidae) , 2002, Biodiversity & Conservation.

[108]  M. Ramos,et al.  Identification of the river blenny, Salaria fluviatilis, as a host to the glochidia of Margaritifera auricularia , 2001 .

[109]  W. Haag,et al.  Using morphometrics to identify glochidia from a diverse freshwater mussel community , 2005, Journal of the North American Benthological Society.

[110]  G. Vermeij,et al.  Molecular Systematics and Phylogeography of Mollusks , 2003 .

[111]  A. Gaunt,et al.  Mechanics of glochidial attachment (Mollusca: Bivalvia: Unionidae) , 1988, Journal of morphology.

[112]  M. Barnhart,et al.  CROSS-RESISTANCE OF LARGEMOUTH BASS TO GLOCHIDIA OF UNIONID MUSSELS , 2005, The Journal of parasitology.

[113]  Max R. Matteson Life History of Elliptio complanatus (Dillwyn, 1817) * , 1948 .

[114]  C. Saylor,et al.  Fish Hosts for Four Species of Freshwater Mussels (Pelecypoda: Unionidae) in the Upper Tennessee River Drainage , 1995 .

[115]  J. Serb,et al.  Congruence and Conflict Between Molecular and Reproductive Characters When Assessing Biological Diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)1 , 2008 .

[116]  J. Serb Discovery Of Genetically Distinct Sympatric Lineages in the Freshwater Mussel Cyprogenia Aberti (Bivalvia: Unionidae) , 2006 .

[117]  M. Glaubrecht,et al.  Novel reproductive modes in freshwater clams: brooding and larval morphology in Southeast Asian taxa of Corbicula (Mollusca, Bivalvia, Corbiculidae) , 2003 .

[118]  R. Neves,et al.  Reproductive Cycle and Fish Hosts of the Rabbit's Foot Mussel, Quadrula cylindrica strigillata (Mollusca: Unionidae) in the Upper Tennessee River Drainage1 , 1986 .

[119]  C. Lydeard,et al.  Molecular systematics of the freshwater mussel genus Potamilu (Bivalvia: Unionidae) , 1998 .

[120]  K. Walker,et al.  Freshwater Mussels (Hyriidae) of Australasia , 2001 .

[121]  K. Cuffey,et al.  Factors controlling the age structure of Margaritifera falcata in 2 northern California streams , 2006, Journal of the North American Benthological Society.

[122]  G. Watters THE KINETIC CONGLUTINATE OF THE CREEPER FRESHWATER MUSSEL, STROPHITUS UNDULATUS (SAY, 1817). , 2002, The Journal of molluscan studies.

[123]  L. B. Arey An experimental study on glochidia and the factors underlying encystment , 1921 .

[124]  Megan L. Schwartz,et al.  Ultrastructural evidence for nutritional exchange between brooding unionid mussels and their glochidia larvae , 2001 .

[125]  Daniel L. Graf,et al.  Palaeoheterodont diversity (Mollusca: Trigonioida + Unionoida): what we know and what we wish we knew about freshwater mussel evolution , 2006 .

[126]  J. Farris,et al.  Freshwater Bivalve Ecotoxicology , 2006 .

[127]  W. Haag,et al.  Variation in fecundity and other reproductive traits in freshwater mussels , 2003 .

[128]  Daniel L. Graf,et al.  REVIEW OF THE SYSTEMATICS AND GLOBAL DIVERSITY OF FRESHWATER MUSSEL SPECIES (BIVALVIA: UNIONOIDA) , 2007 .

[129]  R. Prezant,et al.  Flotation of the Bivalve Corbicula fluminea as a Means of Dispersal , 1984, Science.