Larval Biology; Hawaiian Tree Snails

Larval Settlement and Metamorphosis
We take a very broad approach to studies of settlement and metamorphosis of marine invertebrate animals. Metamorphosis in larvae of many invertebrates depends on very specific external chemical signals. Our studies include investigation of the chemical nature of a small metabolite from prey coral that induces settlement and metamorphosis in the sea slug Phestilla sibogae and of a complex substance from bacterial films that induces metamorphosis in the small fouling worm Hydroides elegans. We have extensively investigated settlement-signal transduction mechanisms in these larvae, as well as the roles of de novo transcription events following induction. We are interested in the genetics of both bacteria and larval populations in determining settlement in larval H. elegans. The latter work has led us to a major interest on the composition of marine biofilms, and thus on the interactions between marine microorganisms and developing marine animals at the time of larval recruitment. Finally, together with a collaborator from the University of California, we are studying the responses of larvae of P. sibogae to encounters with the coral cue to investigate the question, “Can minute invertebrate larvae effectively utilize dissolved cues to achieve site-specific settlement in the turbulent flow that characterizes coral reefs and other wave-swept intertidal habitats?” This effort includes extensive field studies, research in very large and very small flumes, and extensive micro-videography of individual larvae in filaments of coral cue. Similar studies are also being conducted with several members of the biofouling community, including Hydroides elegans, the bryozoan Bugula neretina, the ascidian Phallusia nigra and a barnacle Balanus amphitrite.

Conservation and Evolutionary Biology of Hawaiian Tree Snails
Among the spectacular endemic evolutionary radiations for which Hawai'i is famous is that of the terrestrial and arboreal snails. These snails are famous for both their high rates of speciation and, more recently, their disastrously high extinction rates. We study, in the field and the laboratory, the demography and conservation biology of a single family of endemic Hawaiian snails, the Achatinellidae. These snails have suffered from habitat alteration and outright destruction and from introduced predators. The field studies provide models for determining demographic patterns and analyzing causes of mortality of terrestrial invertebrates in their natural habitat, and they reveal much about the mechanisms of evolution in these snails. Our captive propagation effort now includes five Achatinella species. Currently we are studying microsatellite DNA sequences to compare genetic identities of individual snails, analyze the degree of inbreeding in very small, remnant field populations, and devise breeding plans for captive-rearing.

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Other Professional Experience and Activities (Last 10 years):

Ballast-water Task Force, Hawaii Departments of Land and Natural Resources and Agriculture, 1997- 99.
Ad hoc committee on governance, Society for Integrative and Comparative Biology, 1999.
International Workshop on the Census of Marine Live, Heraklion, Crete, Nov. 2000.
Chair, Search Committee for Head of Department of Invertebrate Zoology, U.S. National Museum of Natural History, Smithsonian Institution, 2000.
Chair, Search Committee for Director, the Smithsonian Marine Station, Smithsonian Institution, U.S. National Museum of Natural History, 2001. Board of Editors, Pacific Science, 1984 - 2006.
Editorial Board, Invertebrate Biology, 1995 - 2006.
Department of Conservation, New Zealand, Endangered Landsnail Advisory Group, 2006 -.

Current:

Research Associate, Bernice P. Bishop Museum, 1983-.
Research Associate, Museum of Comparative Zoology, Harvard University, 1994 - .
Member, Mollusc Specialist Group, Species Survival Commission, International Union for The World Conservation Union, 1985 -.
Western Association of Marine Laboratories, Secretary-Treasurer, 1998 -.
Board of Directors, Pacific Institutes of Marine Science, 2002 - present.

Membership in Professional Societies:

American Association for the Advancement of Science; American Institute of Biological Sciences; American Malacological Society; American Microscopical Society; International Society on Invertebrate Reproduction and Development; Malacological Society of London; Sigma Xi; Society for Conservation Biology; Society for Integrative and Comparative Biology; Unitas Malacologica; Western Society of Naturalists.

Offices:

Conservation Council for Hawaii (affil. Nat. Wildlife Fed.), Oahu Chapter: President, 1981- 82.
Society of Sigma Xi, Hawaii Chapter: Councilor, 1989-90, President, 1991-92.
Western Society of Naturalists: President, 1993.
American Society of Zoologists, Division of Invertebrate Zoology: Chairman 1991 and 1992.
Society for Integrative & Comparative Biology (formerly American Society of Zoologists):
President, 1995 and 1996; Past-President, 1997, 1998.
Hawaii Academy of Sciences, President, 2004 - 2005.
Pacific Institutes of Marine Science (International), President, 2007 - 2009.

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Honors:

Fellow, American Association for the Advancement of Science.
Matsuda Scholar, University of Hawaii, 1989-90.

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Invited Symposium and Seminar Lectures (Last 10 years):

1998. The Larval Biology Meetings, Melbourne, Australia. Jan. "Evidence that the anterior sensory organ of a gastropod larva contains the receptor for an external metamorphic signal."
1998. Duke University Marine Laboratory, invited seminar, Mar. 25, "Settlement signals: how inverte brate larvae detect and process them." Department of Zoology, Duke University, Durham, NC, March 26, "Insular evolution, invasions, and extinctions: case histories from Hawaiian tree snails."
1999. Society for Integrative and Comparative Biology, Past Presidential Address, January 1999. "To save a snail....", Denver, CO.
1999. 10th International Congress on Marine Biocorrosion and Biofouling, Keynote Address, Feb. 1999. Melbourne, Australia. "Macrofouling Processes: settlement processes in the ubiquitous fouler Hydroides elegans."
1999. Harvard University, Department of Organismic and Evolutionary Biology, seminar, Feb. 25, 1999. "Settlement Signals: How Invertebrate Larvae Detect and Process them."
1999. Marine Coatings Research Institute, Qingdao, China. Sept. 6-7, 1999. Three lectures on biofouling, anti-fouling technology, and marine models for biomedical research.
2000. University of California at San Diego. Department of Biology, invited seminar, March 2, 2000. "Insular evolution, invasions and extinctionscase histories from Hawaiian tree snails."
2000. Scripps Institution of Oceanography, La Jolla, CA, invited seminar, March 3, 2000. "Settlement Signals: how invertebrate larvae detect and process them."
2000. Invited symposium address, "Recruitment of an invertebrate larva in response to a dissolved cue in wave-driven flow." The Larval Biology Meetings, Santa Cruz, CA, June 24 - 28, 2000.
2000. Invited symposium address, "Larval behavior in response to a dissolved settlement cue aids recruitment on coral reefs." 9th International Coral Reef Symposium, Bali, Oct. 23, 2000.
2001. Invited symposium address: "Metamorphic competence as a major adaptive convergence in marine invertebrate larvae." Society for Integrative & Comparative Biology, symposium on: Ontogenetic Strategies of Invertebrates in Aquatic Environments, Jan. 4, 2001.
2001. Invited research seminar, "Factors influencing settlement of marine invertebrate larvae." Bodega Marine Laboratory, University of California at Davis, May 17, 2001.
2001. Invited Plenary Lecture, "The capacity to metamorphose, metamorphic induciton and mechanisms of response in (at least some) invertebrate larvae." 9th International Congress on Invertebrate Reproduction and Development. Rhodes University, Grahamstown, South Africa. July 17, 2001.
2001. Invited symposium address: "Contributions of ex situ propagation and molecular genetics to the conservation of Hawaiian tree snails." UCLA Biodiversity Conference 2001: Experimental Approaches to Conservation Biology. Los Angeles, CA. Sept. 11 - 14, 2001.
2001. Invited research seminar, "Factors Affecting the Settlement and Metamorphosis of Marine Invertebrate Larvae: Data from the Field and Lab." Oregon Institute of Marine Biology, University of Oregon, Oct. 5, 2001.
2002. Two invited symposium talks for the Opening Ceremony of the Coastal Marine Laboratory and Mini-Symposium on Frontier Research in Marine Sciences: "Research Activities at the Kewalo Marine Laboratory," and "Induction of Metamoprhosis in Invertebrate Larvae by Dissolved Environmental Cues: Does it Work in Turbulent Moving Water?" May 22 - 23, 2002.
2002. Invited research seminars, "Induction of Metamorphosis in Invertebrate Larvae by Dissolved Environmental Cues: does it work in turbulent moving water?" "Issues in Biofouling Research." The Tropical Marine Science Institute, National University of Singapore, May 29, 30, 2002.
2002. 5th International Larval Biology Meeting. Vigo, Spain. "Do settling larvae make mistakes?" Sept. 18, 2002.
2002. Invited lecture, Hawaii State Foundation on Culture and the Arts: "A scientist looks at art: dissection, sorting, and moralizing." October 19, 2002.

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Publications (Last 10 years):

Pechenik, J. A., M. G. Hadfield and L. S. Eyster. 1995. Assessing whether larvae of the opisthobranch gastropod Phestilla sibogae become responsive to three chemical cues at the same age. Journal of Experimental Marine Biology and Ecology 19:1-17.
Hadfield, M. G. 1995. Variability, plasticity and flexibility: multiple paths to reproductive success for benthic marine invertebrates (invited review). Prog. Nat. Determinisme Recruitment (France), Informations, 22: 2-7.
Hadfield, M. G. and M. F. Strathmann. 1996. Variability, Flexibility and Plasticity in Life Histories of Marine Invertebrates. Oceanologica Acta 19(3-4):323-334.
Kobayashi, S. R. and M. G. Hadfield. 1996. An experimental study of growth and reproduction in the Hawaiian tree snails, Achatinella mustelina and Partulina redfieldii (Achatinellinae). Pacific Science 50:339-354.
Woollacott, R. M. and M. G. Hadfield. 1996. Induction of metamorphosis in larvae of a sponge. Invertebrate Biology 115:257-262.
Walters, L. J., M. G. Hadfield and C. M. Smith. 1996. Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Marine Biology 126:383-393.
Walters, L. J., M. G. Hadfield and K. A. del Carmen. 1997. The importance of larval choice and hydrodynamics in creating aggregations of Hydroides elegans (Polychaeta: Serpulidae). Invertebrate Biology 116(2):102-114.
Pires, A., S. L. Coon and M. G. Hadfield. 1997. Catecholamines and dihydroxyphenylalanine in metamorphosing larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Journal of Comparative Physiology A 181:187-194.
Hadfield, M. G., M. F. Strathmann and R. R. Strathmann. 1997. Ciliary currents of non-feeding veligers in ancient clades of gastropods. Invertebrate Biology 116(4):313-321.
Todd, C. D., M. G. Hadfield and W. A. Sneddon. 1997. Juvenile mating and sperm storage in the tropical coralivorous nudibranch Phestilla sibogae. Invertebrate Biology 116(4):322-330.
Murphy, B. F. and M. G. Hadfield. 1997. Chemoreception in the nudibranch gastropod Phestilla sibogae. Comparative Biochemistry and Physiology 118A: 727-735.
Hadfield, M. G. 1998. The D. P. Wilson Lecture, Research on settlement and metamorphosis of marine invertebrate larvae: past, present and future. Biofouling 12(1-3): 9-29.
Carpizo-Ituarte, E. and M. G. Hadfield. 1998. Stimulation of metamorphosis in the polychaete Hydroides elegans Haswell (Serpulidae). Biological Bulletin 194:14-24.
Holm, E., B. Nedved, E. Carpizo-Ituarte and M. G. Hadfield. 1998. Metamorphic-signal transduction in Hydroides elegans Haswell (Polychaeta: Serpulidae) is not mediated by a G protein. Biological Bulletin 195:21-29.
Boudko, D. Y., M. Switzer-Dunlap and M. G. Hadfield. 1999. The cellular and subcellular structure of anterior sensory pathways in Phestilla sibogae (Gastropoda, Nudibranchia). Journal of Comparative Neurology 403: 39-53.
Unabia, C. and M. G. Hadfield. 1999. The role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Marine Biology 133:55-64.
Hadway, L. J. and M. G. Hadfield. 1999. Conservation status of tree snail species in the genus Partulina (Achatinellinae) on the island of Hawai`i: a modern and historical perspective. Pacific Science 53:1-14.
Hadfield, M. G., E. Meleshkevitch and D. Boudko. 2000. The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biological Bulletin 198(1):67-76.
Pires, A., R. P. Croll and M. G. Hadfield. 2000. Catecholamines modulate metamorphosis in the opisthobranch gastropod Phestilla sibogae. Biological Bulletin 198(3):319-331.
Holm, E. R., B. T. Nedved, N. Phillips, K. L. Deangeles, M. G. Hadfield and C. M. Smith. 2000. Temporal and spatial variation in the fouling of silicone coatings in Pearl Harbor, Hawaii. Biofouling 15:95-107.
Thacker, R. and M. G. Hadfield. 2000. Mitochondrial phylogeny of extant Hawaiian tree snails (Achatinellinae). Molecular Phylogenetics and Evolution 16:263-270.
Hadfield, M. G. 2000. Why and how marine invertebrate larvae metamorphose so fast. Seminars in Cell and Developmental Biology 11(6):437-443.
Leise, E. M. and M. G. Hadfield. 2000. An inducer of molluscan metamorphosis transforms activity patterns in a larval nervous system. Biological Bulletin 199:241-250.
Swain, G., A. C. Anil, R. E. Baier, F.-S. Chia, E. Cone, A. Cook. M. Hadfield, E. Haslbeck, E. Holm, C. Kavanagh, D. Kohrs, B. Kovach, C. Lee, L. Mazzella, A. E. Meyer, P.-Y. Qian, S. S. Sawant, M. Schultz, J. Sigurdsson, C. Smith, L. Soo, A. Terlizzi, A. Wagh, R. Zimmerman, and V. Zupo. 2000. Biofouling and barnacle adhesion data for fouling-release coatings subjected to static immersion at seven marine sites. Biofouling 16: 331-344
Hadfield, M. G. and V. J. Paul. 2001. Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In, "Marine Chemical Ecology," J. B. McClintock and W. Baker, eds. CRC Press pp. 431 - 461.
Hadfield, M. G. 2001. Hemichordata. In, "Atlas of Marine Invertebrate Larvae," C. M. Young, M. E. Rice and M. Sewell, eds. Academic Press. Pp. 553-564.
Hickman, C. S. and M. G. Hadfield. 2001. Larval muscle contraction fails to produce torsion in a trochoidean gastropod. Biological Bulletin 200:257-260.
Croll, R. P., D. Y. Boudko and M. G. Hadfield. 2001. Histochemical survey of transmitters in the central ganglia of the gastropod mollusc Phestilla sibogae. Cell and Tissue Research 305:417-432.
Hadfield, M. G., E. J. Carpizo-Ituarte, K. del Carmen and B. T. Nedved. 2001. Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. American Zoologist 41:1123-1131.
Holland, B. S. and M. G. Hadfield. 2002. Islands within an island: Phylogeography and conservation genetics of the endangered Hawaiian tree snail Achatinella mustelina. Molecular Ecology 11:365-376.
Zabin, C. and M. G. Hadfield. 2002. Do locals rule? Interactions between native intertidal animals and a Caribbean barnacle in Hawai`i. Pacific Science 56:235-236.
Hofmann, D. K. and M. G. Hadfield. 2002. Hermaphroditism, gonochorism, and asexual reproduction in Cassiopea sp. - an immigrant in the islands of Hawai`i. J. Invert. Reproduction & Development 41: 215-221.
Walters, L. J., C. M. Smith and M.G. Hadfield. 2002. Recruitment of sessile marine invertebrates on Hawaiian macrophytes: do pre-settlement or post-settlement processes keep plants free from fouling? Bull. Mar. Sci. (in press).
Carpizo-Ituarte, E. J. and M. G. Hadfield. 2003. Transcription and translation inhibitors permit metamorphosis up to radiole formation in the serpulid polychaete Hydroides elegans Haswell. Biol Bull 204:114-125.
Hadfield, M. G., B. S. Holland and K. J. Olival. 2003. Contributions of ex situ propagation and molecular genetics to conservation of Hawaiian tree snails. "Experimental Approaches to Conservation Biology," M. Gordon and S. Bartol, eds. University of California Press (in press).
Huang, S. and M. G. Hadfield. 2003. Composition and density of bacterial biofilms affect metamorphosis of the polychaete Hydroides elegans. Mar Ecol Prog Ser 260:161-172.
Holland, B. S. and M. G. Hadfield. 2004. Origin and diversification of endemic Hawaiian tree snails (Achatinellidae: Achatinellinae) based on molecular evidence. Molecular Phylogeny and Evolution 32:588-600.
Hadfield, M. G. and M. A. R. Koehl. 2004. Rapid behavioral responses of an invertebrate larva to dissolved settlement cue. Biol. Bull. 207:28-43.
Koehl, M. A. R. and M. G. Hadfield. 2004. Soluble settlement cue in slowly moving water within coral reefs induces larval adhesion to surfaces. J Mar Systems 49: 75-88.
Zardus, J. D. and M. G. Hadfield. 2004. Larval development and complemental males in Chelonibia testudinaria, a barnacle commensal with sea turtles. Journal of Crustacean Biology 24(3): 409-421.
Zardus, J. d. and M. G. Hadfield. 2005. Population history of the Atlantic barnacle Chthamalus proteus and the genetic origins of its introduction to the Pacific. Molecular Ecology 14: 3719-3733.
Buckland-Nicks, J. and M. G. Hadfield. 2005. Spermatogenesis in Serpulorbis (Mollusca: Vermetoidea) and its implications for phylogeny of gastropods. Journal of Invertebrate Reproduction and Development 48(1-3): 171 - 184.
Hadfield, M. G., A. Faucci and M. A. R. Koehl. 2006. Measuring recruitment of minute larvae in a complex field environment: the corallivorous nudibranch Phestilla sibogae (Bergh). Journal of Experimental Marine Biology and Ecology 338: 57 - 72.
Shikuma, N. J. and M. G. Hadfield 2006. Temporal variation of an initial marine biofilm community and effects on larval settlement and metamorphosis of the tubeworm Hydroides elegans. Biofilms 2(4): 231-238.
Bishop, C. D.., D. F. Erezyilmaz, T. Flatt, C. D. Georgiou, M. G. Hadfield, A. Heyland, J. Hodin, M. W. Jacobs, S. A. Maslakova, A. Pires, A. M. Reitzel, S. Santagata, K. Tanaka and J. H. Youson. 2006. What is metamorphosis? Integrative & Comparative Biology 46(6): 655 - 661.
Holland, B. S. and M. G. Hadfield. 2007. Molecular Systematics of the Endangered Oahu Tree Snail Achatinella mustelina (Mighels, 1845): Synonymization of Subspecies and Estimation of Gene Flow Between Chiral Morphs. Pacific Science 61: 53 - 66.
Faucci, A., R. J. Toonen and M. G. Hadfield. 2007. Host shift and speciation in a coral-feeding nudibranch. Proceeding of the Royal Society of London, B 274: 111 - 119.
Miles, C. M., M. G. Hadfield and M. L. Wayne. 2007. Heritibility for egg size in the serpulid polychaete Hydroides elegans. Marine Ecology Progress Series 340:155-162..
Zabin, C. J., J. Zardus, F. B. Pitombo, V. Fread and M. G. Hadfield. 2007. A tale of three seas: consistency of natural history traits in a Caribbean-Atlantic barnacle introduced to Hawaii. Biological Invasions 9(5): 523 - 544.
Koehl, M. A. R. K., Strother, J. A., M. A. Reidenbach, J. R. Koseff, and M. G. Hadfield. 2007. Individual-based model of larval transport to coral reefs in turbulent, wave-driven flow: Effects of behavioral responses to dissolved settlement cues. Marine Ecology Progress Series 335:1-18.
Pettengill, J. B., D. E. Wendt, M. D. Schug, and M. G. Hadfield. 2007. Biofouling likely serves as a major mode of dispersal for the polychaete tubeworm Hydroides elegans as inferred from microsatellite loci. Biofouling 23: 161 - 169.
Zardus, J. D, B. T. Nedved, C. Tran, Y. Huang and M. G. Hadfield. (2007) Microbial Biofilms Facilitate Adhesion in Biofouling Invertebrates. Biological Bulletin (in press).
Nedved, B. T. and M. G. Hadfield. (2008) Hydroides elegans (Annelida: Polychaeta): a model for biofouling research. Chapter in: Marine and Industrial Biofouling, R. Venkatesan, S.P. Murthy, K. Cooksey, H.C. Flemming, Eds. Springer, Berlin (in press).
Erickson, P. B. and M. G. Hadfield. (2008) Isolation and characterization of eight polymorphic microsatellite loci in the endangered Hawaiian tree snail Achatinella sowerbyana. Molecular Ecology Notes (in press).



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Popular-Science Publications (last 10 years):

Hadfield, M. G. 2001. From hatching to finding the right home for metamorphosis: How do invertebrate larvae do it? Science in Africa, Sept. 2001: 1 - 3.
Shikuma, N. and M. G. Hadfield (2005) Marine biofilms: a hidden reservoir for human microbial pathogens. Voice of the Pacific (PACON Newsletter). Fall 2005.

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