Analysis of testate amoeba and microarthropods from pollen samples John M. Logan Project Testate amoeba and microarthropods are potentially proxies for environmental information. Amoeba may be useful in reconstruction of past hydrology (Buttler et al., 1996) and sea-levels (Charman, 1998). Microarthropods may provide data about soil nutrients (Blair and Crossley, 1988) and ecosystem development (Schowalter, 2000). Can microarthropods and testate amoeba be recognized in pollen samples from the American southwest? Can they be readily classified and are they proxies for environmental information? Methodology A series of black and white photographs taken during pollen analysis of a series of pollen samples was examined for testate amoeba and microarthropods. Approximately 21 photographs were noted with testate amoeba or microarthropods. After the photographs were located they specimens in the photographs were identified. The primary key for the mites was Krantz (1975) and the primary keys for the amoeba were found in PDF form on E. A. D. Mitchell’s website. In each case the result of classification was to be genus and species. Literature about testate amoeba and mite ecology was searched for data concerning environments and habitats. The literature and other useful references for both testate amoeba and mites is included in a bibliography at the end of this report. Results Most of the testate amoeba could be identified to the genus and species level, although some of the identifications are tentative. Most of the mites could be identified to the super family or family level and many of these as well must be considered tentative. One specimen was identified to the genus and species level. Information on habitat/environment was difficult to obtain. There was some information on most of the specimens, but it was not extensive. The best information was obtained on some of the testate amoeba identified to genus and species and some of the mites at the family level. Discussion There appears to be considerable potential for identification and environmental proxy data using both mites and testate amoeba. Some of the specimens were more easily identified, but all of the specimens that were sufficiently complete could be identified. Based on this study it appears that amoeba will be easier to classify than mites and both will provide some environmental information if identification has high enough resolution – to the genus and species level. It will be most interesting to apply the methods of palynology to an assemblage looking for variation in counts and genera vertically through a soil column. It would also be interesting (and expensive) to determine if there was a change in the composition of the minerals in the amoeba tests. One could probably perform a statistical analysis of the composition of the mite genera to determine their potential impact on soil microbes and soil fertility. Ongoing Research I don’t consider this project done. I am continuing to collect and read literature resources. I am interested in identifying other testate amoeba and mite specimens. I have made a contact with Mitch Pavao-Zuckerman, who provided me with the name of a researcher, Sina Adl, who is analyzing soil decomposition and has done research in testate amoeba. I will contact them for sources that they may know about on testate amoeba. I intend to contact the arthropod repository at the University of Arizona for additional information and/or contacts about microarthropods. This project has potential if one has the perseverance to continue. Attachments There are two sections of attachments, one for testate amoeba and one for mites. They consist of a table of the taxonomy of the specimens found in the photograph search, the photographs with identification and a summary of the ecological/environmental information at the end, and a bibliography. The testate amoeba section is first followed by the mite section. Amoeba classification (Ogden and Hedly, 1980) with tentatively identified specimens (highlighted in gray) from pollen samples. Subphylum: Sarcodina; Superclass: Rhizopodea; Class: Lobosia; Order: Arcellinida Superfamily Arcellacea Family Arcellidae Genus and species Arcella artocrea Family Centropyxidae Genus and species Centropyxis aculeata Centropyxis laevigata Family Plagiopyxidae Genus and species Plagiopyxis Bullinularia Family Trigonopyxidae Genus and species Trigonopyxis Cyclopyxis eurystoma Family Hyalospheniidae Genus and species Hyalosphenia Heleopera Lesquereeusia Nebela Quadrullela Leptochlamys Family Paraquadrulidae Genus and species Paraquadrula Family Difflugiidae Genus and species Difflugia Pontigulasia Cucurbitella Sexangularia Subphylum: Sarcodina; Superclass: Rhizopodea; Class: Lobosia; Order: Arcellinida Superfamily Cryptodifflugiacea Family Cryptodifflugiidae Genus and species Cryptodifflugia Dfflugiella Wailesella Family Phryganelidae Genus and species Phryganella arcopodia Phryganella nidulus Superfamily Gromiacea Family Gromiidae Genus and species Pseudodifflugia Family Amphitrematidae Genus and species Amphitrema Subphylum: Sarcodina; Superclass: Rhizopodea; Class: Filosia; Order: Gromida Superfamily Euglyphacea Family Euglyphidae Genus and species Euglypha Assulina Placocista Sphenoderia Tracheleuglypha Family Trinematiidae Genus and species Trinema Corythion Family Cyphoderiidae Genus and species Cyphoderia Campascus Family Paulinellidae Genus and species Paulinella 1. Phyrganella arcopodia (Mitchell 2003) or Phyrganella nidulus (Cash 1905). Arizona, site AZ V:16:246. 2. Arcella discoides. (Mitchell 2003). San Clemente, California. 3. Cyclopyxis eurystoma (Mitchell 2003). San Nicholas Island, California. 4. Centropyxis laevigata (?) (Mitchell 2003). Cash (1905, p. 137). San Clemente, California. 5. Arcella artocrea (Mitchell 2004). Cash (1905, p. 127-8). San Nicholas Island, California. 5. Arcella artocrea (Mitchell 2004). Cash (1905, p. 127-8). San Nicholas Island, California. 6. Centropyxis aculeata (?) (Mitchell 2003). San Nicholas Island, California. 7. Centropyxis aculeata (?) (Mitchell 2003). San Nicholas Island, California. 8. Centropyxis aculeata (?). (Mitchell 2003). Arizona, St. David Cienega. Ecological and behavioral information by specimen: 1. Phyrganella arcopodia (Mitchell 2003) or Phyrganella nidulus (Cash 1905). Both seem to fit the specimen, but Phyrganella nidulus seems to fit better. Cash and Mitchell describe both species from Spaghum moss. 2. Arcella discoides (Mitchell 2003). 3. Cyclopyxis eurystoma (Mitchell 2003). This may be incorrect Ogden and Hedley (1980) don’t list North America in the distribution of this species. 4. Arcella artocrea (Mitchell 2004). Cash (1905, p. 127-8) suggests that the species is rare. 5. Arcella artocrea (Mitchell 2004). 6. Centropyxis aculeata (?) (Mitchell 2003). Ogden and Hedley (1980) don’t list North America in the distribution list for the species. Cash (1905, p. 134) states they are found in ponds and ditches on wet moss and spaghum and is most common in swampy ground. 7. Centropyxis aculeata (?) (Mitchell 2003). 8. Centropyxis laevigata (?) (Mitchell 2003). Cash (1905, p. 137) states the species is found in spaghum. Amoeba Bibliography Anonymous 2001 Community Dynamics of Phytoplankton, Protoplankton and Bacterioplankton in Selected Wisconsin Lakes. Vol. 37, Blackwell Publishing Limited, Anonymous 1986 Control of Multicellular Development: Dictyostelium and Myxococcus. Annual Review of Genetics 20539-566. Anonymous 1984 Miscellanea. Vol. 47, no. 5, British Museum Natural History, London. Bahcall, O. 2005 Network analysis: Profiling epistasis. Nature Reviews Genetics 6(5):349-1. Booth, R.K., and J.R. Zygmunt 2005 Biogeography and comparative ecology of testate amoebae inhabiting Sphagnum-dominated peatlands in the Great Lakes and Rocky Mountain regions of North America. Diversity & Distributions 11(6):577-590. Booth, R.K. 2001 Ecology of testate amoebae (protozoa) in two Lake Superior coastal wetlands: Implications for paleoecology and environmental monitoring. Wetlands 21(4):564576. Buttler, Alexandre, Barry G. Warner, Phillipe Grosvernier, Yvan Matthey 1996 Vertical patterns of testate amoeba (Protozoa:Rhizopoda) and peat-forming vegetation on cutover bogs in the Jura, Switzerland. New Phytologist. 134 (2): 37182. Cash, James and John Hopkinson 1905 British Freshwater Rhizopoda and Heliozoa. Volume I, Part 1. The Ray Society, London, England. Cash, James and John Hopkinson 1905 British Freshwater Rhizopoda and Heliozoa. Volume II, Part II. The Ray Society, London, England. Charman, Dan J., Helen M. Roe, and W. Roland Gehrels 1998 The use of testate amoeba in studies of sea-level change: A case study from the Taf estuary, south Wales, UK. The Holocene. 8 (2): 209-218. Funamoto, S., C. Anjard, W. Nellen, and H. Ochiai 2003 cAMP-dependent protein kinase regulates Polysphondylium pallidum development. Differentiation 71(1):51-61. Hägele, S., R. Köhler, H. Merkert, M. Schleicher, J. Hacker, and M. Steinert 2000 Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cellular microbiology 2(2):165-171. Hauer, G., and A. Rogerson 2005 Remarkable Salinity Tolerance of Seven Species of Naked Amoebae (gymnamoebae). Hydrobiologia 549(1-3):33-42. Lamentowicz, M., and E.A.D. Mitchell 2005 The Ecology of Testate Amoebae (Protists) in Sphagnum in Northwestern Poland in Relation to Peatland Ecology. Microbial ecology 50(1):48-63. Matapurkar, A.K., and M.G. Watve 1997 Altruist cheater dynamics in Dictyostelium: Aggregated distribution gives stable oscillations. American Naturalist 150(6):790. Mauquoy, D., and K. Barber 1999 Evidence for climatic deteriorations associated with the decline of Sphagnum imbricatum Hornsch. ex Russ. in six ombrotrophic mires from northern England and the Scottish Borders. Holocene 9(4):423-437. Mitchell, E.A.D., A. Butter, P. Grosvernier, H. Rydin, C. Albinsson, A.L. Greenup, M.M.P.D. Heijmans, M.R. Hossbeek, and T. Sarrinen 2000 Relationships among testate amoebae (Protozoa), vegetation and water chemistry in five Sphagnum-dominated peatlands in Europe. New Phytologist 145(1):95-106. Mitchell, Edward A. D. 2003. The identification of Centropyxis, Cyclopyxis, Trigonopyxis and similar Phryganella species living in Sphagnum. Guide available on website as PDF. Mitchell, Edward A. D. 2004 http://wslar.epfl.ch/mitchell/edward/testate_amoebae.htm. Updated 4-24-04. Accessed 12-12-05. Muangphra, P. 1982 Some testate amoebae (Testcealobosea; Sarcodina; Protozoa) from mosses of Kansas. Ogden, C.G., and R.H. Hedley 1980 An atlas of freshwater testate amoebae. Oxford University Press for the British Museum Natural History, Oxford. Polne-Fuller, M., R. Trench, A. Gibor, University of California, Santa Barbara. Marine Science Institute, and United States. Office of Naval Research 1991 An amoeba/zoozanthellae consortium as a model system for animal/algal symbiosis. University of California, Santa Barbara, CA. Raederstorff, D., and M. Rohmer 1987 The action of the systemic fungicides tridemorph and fenpropimorph on sterol biosynthesis by the soil amoeba Acanthamoeba polyphaga. European Journal of Biochemistry 164(2):421-426. Schultz, D.A. 1999 Chemotaxis of the testate ameba -. Tuma, R., and W.A. Wells 2002 Neutrophils on the move. Journal of Cell Biology 156(2):226. Velho, L.F.M., L.M. Bini, and F.A. Lansac-Tôha 2004 Testate Amoeba (Rhizopoda) Diversity in Plankton of the Upper Paraná River floodplain, Brazil. Hydrobiologia 523(1-3):103-111. Mites classification (Krantz, 1975) with tentatively identified specimens (highlighted in gray) from pollen samples. Phyllum: Arthropoda; Subphyllum: Chelicerata; Class: Archnida; Order: Acari Order: Parasitiformes Suborder Mesostigmata Super Cohort Monogynaspida Cohort Uropodina Super Family Trachytoidea Family Trachytidae Genus and species Caminella peraphora Cohort Gamasina Super Family Parasitoidea Family Zerconidae Order: Trombidiformes Suborder Prostigmata Super Family Hydrachnoidea Family Hydrachnidae Super Family Hygrobatoidea Family Hygrobatidae Family Bdellidae 1. Caminella peraphora (?) Krantz (1978, p. 75). Arizona, site AZ AA:12:753. 2. Zerconidae. (Krantz, 1978, p. 83-8). California, site CA-RIV-1492. 3. Superfamily Hydrachnoidea, adult (?) dorsal (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). Aztlan 1245. 4. Superfamily Hydrachnoidea, adult (?) ventral (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). Statistical Research 351. 5. Superfamily Hydrachnoidea, adult (?) dorsal (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). Statistical Research 351. 6. Superfamily Hydrachnoidea, adult (?) dorsal (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). California, site CA-RIV-1492. 7. Superfamily Hydrachnoidea, adult (?) ventral (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). Statistical Research 351. 8. Hygrobatoidea (?) (Krantz, 1978, p. 174-82). Arizona, site AZ BB:14:598. 9. Superfamily Hydrachnoidea, nymph (?) (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). San Clemente, California. 10. Superfamily Hydrachnoidea, nymph (?) (Krantz, 1978, p. 174-82). Family Hydrachinae (?) (Cook, 1974). San Clemente, California 11. Unidentified. Arizona, site AZ BB:9:173. Arizona, site AZ BB:9:173. 12. Unidentified. Statistical Research 165. 13. Unidentified. San Nicholas Island. Ecological and behavioral information by specimen: 1. Caminella peraphora (?) Krantz (1978, p. 75). “Caminella peraphora (Trachytidae) is virtually semi-aquatic in habitat, being found only in wet moss anchored in streams.” AZ AA:12 753. 2. Zerconidae. (Krantz, 1978, p. 83-8). None of the specimens Krantz (1978), Urhan (1998) or Urhan (2002) illustrated fit the specimen in the photograph. The specimen doesn’t appear to correspond with Zercon (spp.). Zercon species all have setae labeled J1 and J2 posterior on the anterior double or more in length of the other setae. The posterior anterior setae on the photograph specimen are all equal in length. Krantz (1978, p. 71) notes that the Zerconidae are parasites. The Zerconidae (Urhan 2002, p. 2127) live in humus and litter from a variety of habitats – woodlands, grasslands, and heathlands and also live among mosses and lichens. He states they are oliphagous predators (feeding on the same family, but potentially different genera), not parasites. 3. Hydrachnoidea (?) (Krantz, 1978, p. 174-82). The gnathosoma matches, but there are many other features that don’t, like the dorsal and anal shield on the photograph specimen, lacking in the illustrated specimen. The specimen in the photograph has no setae, but the specimen in the illustration has them. Specimens 3-7appear to be the same super family. Specimens 6 and 7 may be nymphs. Cook (1974, p. 33) includes only one family – Hydrachnidae. The female lays eggs in intercellular air spaces of plants. The nymphs are parasites of aquatic Hemiptera and Coleoptera exclusively, remaining attached to the host for relatively long periods of time (Cook, 1974, p. 34). They don’t leave the pond during the nymph and nymphochrysalis stages. During the nymph an adult stages they live in temporary ponds. They leave the pond when it dries out, living in permanent water during the winter or dry season (Cook, 1974, p. 33-4). 4. See listing for specimen 3. 5. See listing for specimen 3. 6. See listing for specimen 3. 7. See listing for specimen 3. 8. Hygrobatoidea (?) (Krantz, 1978, p. 174-82). The specimen keys to this superfamily, but it has features not visible in the illustrated specimens. Cook (1974, p. 151) notes that the larval stage of this super family is adapted for swimming with the second, third and sometimes first coxa fused. 9. See listing for specimen 3. Nymph (?). 10. See listing for specimen 3. Nymph (?). 11. Unidentified. 12. Unidentified. 13. Unidentified. Chelicera (?). Mite Bibliography André, H.M., X. Ducarme, and P. Lebrun 2002 Soil biodiversity: myth, reality or conning? Oikos 96(1):3-24. Blair, John M. and D. A. Crossley 1988. Litter decomposition, nitrogen dynamics and litter microarthropods in a southern Applachian hardwood forest 8 years following clearcutting. Journal of Applied Ecology. 25: 683-98. Cole, L., S.M. Buckland, and R.D. Bardgett 2005 Relating microarthropod community structure and diversity to soil fertility manipulations in temperate grassland. Soil Biology & Biochemistry 37(9):17071717. Coleman, D., S. Fu, P. Hendrix, and D. Crossley Jr 2002 Soil foodwebs in agroecosystems: impacts of herbivory and tillage management. European Journal of Soil Biology 38(1):21. Cook, David R 1974 Water mite genera and subgenera. Memoirs of the American Entomological Institute. Number 21. Ann Arbor, Michigan. Cortet, J., D. Gillon, R. Joffre, J. Ourcival, and N. Poinsot-Balaguer 2002 Effects of pesticides on organic matter recycling and microarthropods in a maize field: use and discussion of the litterbag methodology. European Journal of Soil Biology 38(3/4):261. Cowgill, S.E., R.D. Bardgett, D.T. Kiezebrink, and H.J. Atkinson 2002 The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere. Journal of Applied Ecology 39(6):915-923. Crossley, J.,D.A., C. Gist, and J. Proctor Charles W. 1975 Summer Biomass of Soil Microarthropods of the Pawnee National Grassland, Colorado. American Midland Naturalist 93(2):491. Culik, M.P., J.L. de Souza, and J.A. Ventura 2002 Biodiversity of Collembola in tropical agricultural environments of Espırito Santo, Brazil. Applied Soil Ecology 21(1):49. Heneghan, L., and D.C. Coleman 1999 Soil microarthropod contributions to decomposition dynamics: Tropicaltemperate comparisons of a.. Ecology 80(6):1873. Heneghan, L., and T. Bolger 1996 Effects of components of 'acid rain' on the contribution of soil microarthropods to ecosystem function. Journal of Applied Ecology 33(6):1329-1344. J. Romeis, M. Battini, and F. Bigler 2003 Transgenic wheat with enhanced fungal resistance causes no effects on Folsomia candida (Collembola: Isotomidae). Pedobiologia 47(2):141. Kampichler, C., and V. Geissen 2005 Temporal predictability of soil microarthropod communities in temperate forests. Pedobiologia 49(1):41-50. Kampichler, C., J. Rolschewski, D.P. Donnelly, and L. Boddy 2004 Collembolan grazing affects the growth strategy of the cord-forming fungus Hypholoma fasciculare. Soil Biology & Biochemistry 36(4):591. Kaneko, N., and E.F. Salamanca 1999 Mixed leaf litter effects on decomposition rates and soil microarthropod communities in an oak–pine stand in Japan. Ecological Research 14(2):131-138. Kautz, T., F. Ellmer, C. López-fando, E. Leedu, and W. Köhn 2002 EINFLUSS LANGJÄHRIG DIFFERENZIERTER ORGANISCHMINERALISCHER N-&Duml;NGUNG AUF BODENMIKROARTHROPODEN IN BERLIN (D) -- MADRID (E)--TARTU (EST). Archives of Agronomy & Soil Science 48(5):513. Krantz, G. W. 1975 A manual of Acarology. Oregon State University Press, Corvallis, Oregon. Leinaas, H.P., S.J. Coulson, R.A. Ims, and G. Sovik 2000 Experimental manipulation of the winter surface ice layer: the effects on a high Arctic soil microarthropod community. Ecography 23(3):299. Lindberg, N., J.B. Engtsson, and T. Persson 2002 Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. Journal of Applied Ecology 39(6):924-936. Lisa Cole, Karsten M. Dromph, Vincent Boaglio, and Richard D. Bardgett 2004 Effect of density and species richness of soil mesofauna on nutrient mineralisation and plant growth. Biology & Fertility of Soils 39(5):337-343. Maraun, M., J. Salamon, K. Schneider, M. Schaefer, and S. Scheu 2003 Oribatid mite and collembolan diversity, density and community structure in a moder beech forest (Fagus sylvatica): effects of mechanical perturbations. Soil Biology & Biochemistry 35(10):1387. Minor, M.A., T.A. Volk, and R.A. Norton 2004 Effects of site preparation techniques on communities of soil mites (Acari: Oribatida, Acari: Gamasida) under short-rotation forestry plantings in New York, USA. Applied Soil Ecology 25(3):181. Parisi, V., C. Menta, C. Gardi, C. Jacomini, and E. Mozzanica 2005 Microarthropod communities as a tool to assess soil quality and biodiversity: a new approach in Italy. Agriculture, Ecosystems & Environment 105(1/2):323-333. Pregitzer, K.S., D.R. Zak, M.F. Allen, J.N. Klironomos, M.C. Rillig, and M. Kubiske 1997 Soil fungal-arthropod responses to Populus tremuloides grown under enriched atmospheric CO2 under field conditions. Global Change Biology 3(6):473. Salminen, J., C.A.M. Van Gestel, and J. Oksanen 2001 Pollution-Induced Community Tolerance and Functional Redundancy in a Decomposer Food Web in Metal-Stressed Soil. Environmental Toxicology & Chemistry 20(10):2287-2295. Schneider, K., and M. Maraun 2005 Feeding preferences among dark pigmented fungal taxa (“Dematiacea”) indicate limited trophic niche differentiation of oribatid mites (Oribatida, Acari). Pedobiologia 49(1):61-67. Schneider, K., S. Migge, R.A. Norton, S. Scheu, R. Langel, A. Reineking, and M. Maraun 2004 Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biology & Biochemistry 36(11):1769-1774. Schowalter, T. D. 2000 Insects as regulators of ecosystem development, in Invertebrates as webmasters in ecosystems, p. 99-114. D. C. Coleman and P. F. Hendrix, eds. CABI Publishing, New York, N.Y. Sjursen, H., and M. Holmstrup 2004 Direct measurement of ammonium excretion in soil microarthropods. Functional Ecology 18(4):612-615. Sjursen, H., A. Michelsen, and S. Jonasson 2005 Effects of long-term soil warming and fertilisation on microarthropod abundances in three sub-arctic ecosystems. Applied Soil Ecology 30(3):148-161. Thimm, T., A. Hoffmann, H. Borkott, J.C. Munch, and C.C. Tebbe 1998 The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but.. Applied & Environmental Microbiology 64(7):2660. Tsiafouli, M.A., A.S. Kallimanis, E. Katana, G.P. Stamou, and S.P. Sgardelis 2005 Responses of soil microarthropods to experimental short-term manipulations of soil moisture. Applied Soil Ecology 29(1):17-26. Urhan, R. 2002 New zerconid mites (Acari: Gamasida: Zerconidae) from Turkey. Journal of Natural History 36(17):2127-2138. Urhan, R. 1998 Some new species of the family Zerconidae (Acari: Mesostigmata) from Turkey. Journal of Natural History 32(4):533. Vtorov, I.P. 1993 Feral pig removal: Effects on soil microarthropods in a Hawaiian rain forest. Journal of Wildlife Management 57(4):875. Wanner, M., and W. Dunger 2002 Primary immigration and succession of soil organisms on reclaimed opencast coal mining areas in eastern Germany. European Journal of Soil Biology 38(2):137. http://protist.i.hosei.ac.jp/ http://wslar.epfl.ch/mitchell/edward/testate_amoebae.htm