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Microorganism species richness and diversity in elfin forest bryophytes

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Microorganism species richness and diversity in elfin forest bryophytes
Translated Title:
La riqueza del microorganismo de especies y la diversidad en briófitos del bosque enano ( )
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Miller, Andrew
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Bryophytes   ( lcsh )
Aquatic ecology   ( lcsh )
Briófitos
Ecología aquática
Tropical Ecology 2006
Ecología Tropical 2006
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Reports   ( lcsh )
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Abstract:
The elfin cloud forest in Monteverde, Costa Rica is an area with a species rich bryophyte community that harbors an unexplored community of microscopic organisms. I examined two morphospecies of bryophytes to compare their species richness of microorganisms living in the water the bryophyte holds. The factors that I examined that may affect microorganism’s species richness are pH and structural differences between the bryophyte morphospecies. Bryophyte water samples were collected, pH was measured, and protozoan species were counted and viewed under a compound microscope. Even though there were visible differences in structural complexity between moss morphospecies (longer shoot lengths and thicker patches) there were non-significant differences between the average species richness per sample (Mann-Whitney U test, U = 78.5; P = 0.16). I found a significantly higher diversity of microorganisms in one moss morphospecies (T-test, t-value = 3.62, P < 0.05). The moss morphospecies with shorter shoot lengths had one unique microorganism and higher average (but not significant) species richness per mL of water than the second morphospecies (T-test, t-value = -1.5; P = 0.14). This is due to one moss morphospecies holding much more soil and detritus in its samples and therefore microorganisms living in the attached soil were also counted.
Abstract:
El bosque nuboso enano en Monteverde, Costa Rica es un área con una comunidad de briofitas rica en especies, la cual es una comunidad inexplorada de organismos microscópicos. Examiné dos morfoespecies de briofitos. Los factores que examiné que pueden afectar la riqueza de especies de microorganismo es el PH y algunas diferencias estructurales entre las morfoespecies de briofitos.
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Microorganism species richness and diversity in elfin forest bryophytes Andrew Miller Department of Biology, University of Wisconsin-Madison ABSTRACT The elfin cloud forest in Monteverde, Costa Rica is an area with a species rich bryophyte community that harbors an unexplored community of microscopic organisms. I examined two morphospecies of bryophytes to compare thei r species richness of microorganisms livi ng in the water the bryophyte holds. The factors that I examined that may affect microorganisms species richness are pH and structural differences between the bryophyte morphospecies. Bryophyte water samples were collected, pH was measured, and protozoan species were counted and viewed under a compound microscope. Even though there were visible differences in structural comple xity between moss morphospecies (longer shoot lengths and thicker patches) there were non-significant differe nces between the average species richness per sample (Mann-Whitney U test, U = 78.5; P = 0.16). I found a significantly higher diversity of microorganisms in one moss morphospecies (T-test, t-value = 3.62, P < 0.05). The moss morphospecies with shorter shoot lengths had one unique microorganism and higher average (but not significant) species richness per mL of water than the second morphospecies (T-test, t-va lue = -1.5; P = 0.14). This is due to one moss morphospecies holding much more soil and detritus in its samples and therefore microorganisms living in the attached soil were also counted. RESUMEN El bosque nuboso enano en Monteverde, Costa Rica es un rea con una comunidad de briofitas rica en especies, lacual es una comunidad inexplorada de or ganismos microscpicos. Examin dos morfoespecies de briofitos y compare la riqueza de especies de micr oorganismos que viven en el agua acumulada en los briofitos. Los factores que examin que pueden afectar la riqueza de especi es de microorganismo es el pH y algunas diferencias estructurales entre las morphospecies de briofitos. Las muestras del agua de briofitos fueron reunidas, el pH fue medido, y la especie de protozoos contada y vista bajo un microscopio compuesto. Aunque hubieron diferencias visibles en la complejidad estructural entre morphospecies de musgo (como las longitudes ms largas delas hojas y parches ms gruesos) no hubo diferencias significativo entre la riqueza de las especies (MannWhitney U test, U = 78.5; P = 0.16). Encontr una diversidad apreciablemente ms alta de microorganis mos en una morfoespecie dounusgo (T-test, t-value = 3.62, P < 0.05). La morfoespecie con hojas de longitudes ms cortas tuvo mas morfoespecies por mililitro de agua que la segundo morfospecies (T-test, t-value = -1.5; P = 0.14). Esto se debe a que morfospecies de musgo tiene mucha ms tierra y detrito en sus muestras, por lo tanto los microorganismos que viven en la tierra colectada fueron contados tambin. INTRODUCTION 1

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The purpose of this investigation is to examine the richness and composition of microscopic organisms harbored in two, struct urally different species of moss in cloud forest. Bryophyte mats are a home for an array of microscopic organisms including protozoa and amoebas; they are found in many places around the world with distinctive communities harbored within their mois ture (Heal 1962; Raven 1986). Many moss species grow in continuously wet environmen ts such as rain and cloud forests (Mauseth 1995). These habitats offer a lower risk of desiccation and more favorable and less physiologically stressful locati on for organisms rather than being exposed and without protection outside of the bryophyte mat (Allen 1994). Community composition and diversity of bryophyte microorganisms are primarily linked to moisture content of the moss (Booth and Zygmunt 2005) and secondarily related to pH (Charman and Warner 1992). Ot her local conditions that are determinants of community richness are latitude, available light, nutrients, and climate severity (Pocs 1983; Smith 1996). Moss species differ in their tolerance of moisture, which in turn may affect the communities of microorganisms that live in a different moss species (Charman and Warner 1992). Studies of species composition in moss environments are scarce, and therefore further research is needed (Mitchel et al. 2003). The amount and kind of habitat structure in an ecosystem is also an important factor of community structure (Downes et al 2000). In a previous study, sphagnum moss with uniform conditions (from a macroscopic point of view) was analyzed for testate amoebae. Even though the sphagnum moss s eemed to be uniform macroscopically, species differences in testate amoebae were due to variation in elevation and other local 2

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ecological differences (Mitchel et al. 2003). N early all records of microorganism species composition are determined by the fore me ntioned local conditions (Smith 1996). I studied species composition and divers ity of microorganisms that live in bryophytes by comparing two different morphos pecies of moss at the same location, which have the same local environmental cond itions. I addressed the question of whether different moss species, which have the same local conditions, house different microorganism communities. There is a major difference in moss stru cture and possibly pH in the two moss species being examined. These two differences will offer the variability that may change microorganism composition. Habitat structure generally has positive effects on biological communities; it was found that abundance and species richness were positively correlated to increased habitat complexit y, vegetation and patc h size (Fournier and Loreau 1999; Lipcius et al. 1998) Habitat structure promotes greater biomass, resources, and abundance and diversity of organisms (S tewart et al. 2003). Moss sample A has much longer shoot lengths and is more struct urally complex, offering more surface area for habitat use than moss B. Moss B is a very short, compact moss that is firmly attached to the soil or substrate below. This study hypot hesizes that there will be differences in microorganism composition between moss sa mples A and B due to differences in structural complexity. Moss A should have higher species richness because of its physical attributes. 3

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MATERIALS AND METHODS Sampling sites and methods Moss patches were collected in the elfin cloud forest of Monteverde, Costa Rica around 1760 m and designated as morphospecies A and mo rphospecies B. This site was chosen because of the high density of moss in a small area. All samples were taken within 25m of each other. Each morphospecies of mo ss was collected from twenty different sites ranging from tree trunks, stumps, and fallen logs. In some cases, the moss samples accumulated a thin layer of silt or dirt substrat e at the base. This occurred more often in morphospecies B than morphospecies A. Samples were collected from October to November 2006. An equal amount of moss was collected into a 300-cm3 container. On nonraining days an equal amount of water was a dded to each sample, ranging from 1 4 oz. The moss was collected and covered in the Tupperware dish, wate r was added, and the sample was shaken for ten seconds. The sample was immediately rung out by hand to extract the water into a labeled quart-sized zip-lock bag. Chemical and physical characteristics of the mosses Morphospecies A was a thicker, spongi er mat with much longer shoot lengths, causing it to hang off of the branch or substr ate. Morphospecies B was much shorter and denser, clinging onto the substrate more firml y. The latter usually held a darker green pigment. Aqueous extracts of the moss samp les were tested for pH with a digital pH meter. An average shoot length was found by measuring the lengths of six samples of each morphospecies (mm) with calipers. 4

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Protozoan diversity An eyedropper was used to extract a sample for microscope analysis. A compound microscope was used to look at two slides from each aqueous sample, viewing at 5, 10, and 40 power. Per slide, five viewing areas were looked at, the four corners and the middle of the slide. Microorganisms pr esent were recorded as morphospecies and photographed. Microorganisms were unable to be identified taxonomically so they were assigned identification codes and describe d morphologically, as described in the appendix. Statistical analysis Samples were classified as being in either Tier 1 or Tier 2. Tier 1 is the 15 samples that were collected on days when I added and collected a constant amount of water. Tier 2 is defined as the 15 samples above plus five samples I collected on days when it was raining and no water was added a nd thus an inconsistent volume of water was collected. A Mann-Whitney U test was us ed to compare Tier 1 species richness and average pH differences between fifteen samp les of A and B. A T-test was used to compare Tier 2 species richness and average pH. Statistics were carried out using the computer program Statview. RESULTS Moss sample data The average moss shoot length of morphos pecies A was 52 mm (range 17 92 mm, n = 6). Morphospecies Bs average moss shoot le ngth was 8 mm (range 4 10 mm, n = 6). 5

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The average pH for morphospecies A was 5.3 (range 4.0 6.5, n = 18). Morphospecies Bs average pH was 5.6 (range 4.8 7.2, n = 18). Microorganism taxa There were eleven total morphospecies of microorganisms found between the moss samples A and B. The most common or ganism found in both A and B was Type 2 with 632 and 527 individuals, respectively. On ly one individual of Type 7 and 10 were found in moss A. Moss B had only one individu al of Type 3 and 10. The richness of protozoans in moss A was 10, and 11 in B. There were 10 microor ganism morphospecies that were found in common with both moss types while Type 11 was unique to moss B. A single tardigrade was found in moss sample A but was not included in the analysis, which focused on protozoans. Statistical results A Mann-Whitney U test was used for Tier 1 and a T-test was used for Tier 2. Average species richness was compared between moss A and B. No significant differences were found between protozoans of moss A and B in the Tier 1 analysis (U = 146.5, p = 0.159, n = 15) while the Tier 2 analysis showed a significant difference (tvalue = -2.213, p = 0.033, df = 38). Species richness per milliliter was measured for both moss types, showing moss A S/mL = 0.104 a nd moss B S/mL = 0.147. No significant relationship was found (t-val ue = -1.51, p = 0.13, df 38). A beta-diversity test was used to measure species turnover. BetaMoss A = 0.22 while BetaMoss B = 0.19 showing that Moss A has higher turnover, meaning there are more changes in community composition between moss samples. Moss A had significantly higher diversity than moss B (Shannon Weiner Index, H1 A = 2.40, H1 B = 2.06, t = 3.62, df 6

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= 19, p < 0.05). Average pH was compared a nd no significant relationship was found in both Tier 1 (U = 143.5, p = 0.093, n = 15) and Tier 2 (t-value = -1.21, p = 0.24, df = 38). DISCUSSION Microorganisms, including protozoans, are cr itically important in all ecosystems, including aquatic and terrestria l ones. Terrestrial microorga nisms make up a significant part of communities (Anderson 2006). These microorganisms are essential as they dissolve organic matter, consume bacteria, maintain major biogeochemical cycles, and recycle elements (Darbyshire 1994; Nee 2004; Spaulding 2005). But their invisibility means that the most basic aspects of their ecology are virtually unknown. In this study I investigated basic parameters of community richness and composition of protozoans that live in the water droplets suspended (precarious ly!) in two kinds of moss. This is my effort to fill a gap in our knowledge of so me of the least understood taxa on Earth. The mosses I investigated were strikingly different in structural complexity but were otherwise very similar, with identical average pH and from similar microsites in the Monteverde Cloud Forest. De spite the great difference in shape, the protozoan communities that they harbored were very similar in the kinds of species and the number of species they harbored. Although Tier 1 proved to have non-signi ficant differences in average species richness there was a difference in species ri chness per mL between the moss types. Moss B had about a third greater S/mL than moss A and moss B also had one species that was unique to it. This may be because when moss B was collected it often held onto much more ground substrate than moss A. I believe this allowed moss B samples to include microorganisms that were living in the moss as well as in the soil. This may have greatly 7

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skewed results as I intended to only view microorganism s living in the actual moss habitats. Moss A had a significantly higher diversit y (T-test, p < 0.05) even though it did not have higher species richness. I believe this may be because moss As structural complexity allows species to live togeth er with enough resources space, and possible niches that monodominance doesnt occur. Moss A had an average shoot length over six times as long as moss B. This same reas oning may contribute to moss A having higher turnover than moss B. The relationships between habitat comp lexity and community composition needs to be researched further to understand biologi cal patterns and to formulate strategies for maximizing diversity (Stewart et al. 2003). Protist communiti es show us that a small change in any one of multiple local factor s (climate, space, moisture, nutrition, or light availability) can alter a communitys speci es make-up. Negative changes in the invisibles habitat will be certainly felt in other ecosystems since these microorganisms help control and regulate vital and global processes. Repeating a similar study but looking at microorganisms living only in the bryophyte vegetation and being careful not to collect soil in the water samples would give more accurate findings. This would allow one to study solely the effect of habitat structure seeing as how pH had no significant differences at the study site. Research about the effects of structural complexity of moss and its impact of microorganism species richness needs to be further explore d. A better understanding of these factors will give a clearer picture to how local co nditions of bryophytes impact microorganism populations. 8

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ACKNOWLEDGEMENTS I would like to thank Karen Masters, Alan Masters, Cam Pennington, and Tom McFarland for advising and assisting me throughout my research process; I couldnt have done it without you. I would also like to thank the Estacion Biologica de Monteverde for the use their lab space and giving me access to the Elfin Cloud Forest. LITERATURE CITED Allen, B. 1994. Moss flora of Central America. Mi ssouri Botanical Garde n, Missouri. pp.1-3. Anderson, R.O. 2006. The Density and Diversity of Gymnamoebae Associated with Terrestrial Moss Communities (Bryophyta: Bryopsida) in a Northeastern U.S. Forest. Journal of Eukaryotic Microbiology. 53: 275-279. Booth, R. and J. Zygmunt. 2005. Biogeogr aphy and comparative ecology of testate amoebae inhabiting Sphagnum-dominated peatlands in the Great Lakes and Rocky Mountain regions of North Amer ica. Diversity & Distributions. 11 : 577. Charman, D and B. Warner. 1992. Relations hip between testate amoebae (Protozoa: Rhizopoda) and microenvironmental para meters on a forested peatland in Northeastern Ontario. Ca nadian Journal of Zoology. 70: 2474-2482. Darbyshire, J.F. 1994. Soil Protozoa. CA B International, Wallingford, UK. Downes, B.J., P.S. Lake, E.G. Schreiber, A. Glaister. 2000. Habitat structure, resources and diversity: the separate effects of surface roughness and macroalgae on stream invertebrates. Oecologia. 123: 569-581. Fournier, E., M. Loreau. 1999. Effects of newly planted hedges on ground-beetle diversity (Coleoptera, Carabidae) in an agricultural la ndscape. Ecography. 22: 8797. Heal, O.W. 1962. The abundance of microdistri bution of testate amoebae (Rhizopoda: Testacea) in sphagnum. Oikos. 13: 35-47 in Buttler, A., B, Warner, P. Grosvernier, Y. Matthey. 1996. Vertical pa tterns of testate amoebae (Protozoa: Rhizopoda) and peat-forming vegetation on cutover bogs in Juro, Switzerland. 9

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New Phytologist. 134: 371-382. Lipcius, R.N., D.B. Eggleston, D.L. Miller, T.C. Luhrs. 1998. The habitat-survival function for Caribbean spiny lobster: an inverted size effect and non-linearity in mixed algal and seagrass ha bitats. Freshwater Res. 49: 807-816. Mauseth, J.D. 1995. Botany: An Introduction to Plant Biology. University of Texas, Saunders College Publishing. pp.615-624. Mitchell, D. Borcard, A.J. Buttler, Grosvernie r, D. Gilbert, J.M. Gobat. 2003. Structure of Microbial Communities in Sphagnum Peatlands and Effect of Atmospheric Carbon Dioxide Enrichment. Microbial Ecology. 16: 187-199. Nee, S. 2004. More than meets the eye. Nature. 429: 804-805. Pocs, T. 1983. Tropical Forest Br yophytes. Bryophyte Ecology. pp.59-101. Raven, P.H. and G.B. Johnson. 1974. Biology of Plants. Mosby Collage Publishing. pp.146-148. Smith, H.G. 1996. Diversity of Antarctic terrestrial protozoa. Biodiversity and Conservation. 5: 1379-1394. Spaulding, J. 2005. Protist community diversity in relation to resources in bromeliads. CIEE Spring Tropical Biology and Cons ervations, pp 1-9. Unpublished. Stewart, T.W., T.L. Shumaker, T.A. Radzi o. 2003. Linear and nonlinear effects of habitat structure on composition and abundance in the macroinvertebrate community of a large river. The American Midland Naturalist. 149 : 293-305. 10

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0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 AB Moss MorphospeciesSpecies Richness Fig. 1. Mean protozoan species richness found in 20 samples of two moss species in the Elfin Cloud Forest, Monteverde, Costa Ri ca between October and November 2006. No significant difference in average protozoan community richness was found (U = 146.5, p-value = 0.159, n = 15). 11

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0 0.02 0.04 0.06 0.08 0.1 0.12 0.14 0.16 0.18 AB Moss MorphospeciesS/mL Fig. 2. The average protozoan community species richness per milliliter of water in bryophyte morphospecies A and B in the El fin Cloud Forest, Mont everde, Costa Rica between October and November 2006. No significant difference in species richness per mL between moss morphospecies was f ound (t-value = -1.51, p = 0.13, df = 38). 12

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4.8 4.9 5 5.1 5.2 5.3 5.4 5.5 5.6 5.7 5.8 AB Moss MorphospeciespH Fig. 3. Average pH of water extracted fr om bryophyte morphospecies A and B in the Elfin Cloud Forest, Monteverde, Costa Ri ca during October and November 2006. No significant difference between pH levels of moss morphospecies was found (U = 146.5, p-value = 0.093, n = 15). 13

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APPENDIX Microorganism morphospecies classified by a ssigned type and physical description as viewed from compound microscope at 5x, 10x, and 40x. Microorganisms were found in water extracted from two bryophyte morphospeci es in the elfin cloud forest, Monteverde, Costa Rica during October and November 2006. Microorganism morphospecies Description Type 1: In moss A and B Nematode eas ily visible at 5x and 10x. Long, thin shape, moves by lashing or gliding Type 2 : In moss A and B Vibrating irregular shapes small brown specks at 40x. Pillbox, kidney, oval, and irre gular shaped that squirm or vibrate with little or no forward movement. Type 3 : In moss A and B Motile smooth pillbox to oval shape with constant gray color, glides throug h substrate efficiently but slowly. No obvious vacuoles or organelles. Type 4 : In moss A and B Motile smooth pillbox to oval shape with constant green color, glides through substrate efficiently but slowly. No obvious vacuoles or organelles. Type 5 : In moss A and B Simple, soft chubby looking rounded cylinder visible at 10x. Tapered anterior e nd with spinning propellerlike cap at mouth. Gradual movement with periodic bulging. Visible organelles sometimes present at 40x. Type 6 : In moss A and B Bright green cells with rigid smooth shell, small vacuoles or organelles visible, single apical aperture sometimes visible. Very efficient and fast gliders visible at 10x. Type 7 : In moss A and B Body encased within layer of hollow spheres or plates, exterior looks very lumpy. Slight slink movement, slower than M6. Vacuole or large organelle visible in posterior end Type 8 : In moss A and B Visible at 40x, smooth cylinder wiggles rigidly to move periodically, light brown in color Type 9 : In moss A and B Visible at 10 x, looks like a slug. Two antennae visible at the anterior end. Elon gates to move slowly. Type 10 : In moss A and B Small worm so metimes visible at 10x, but need 40x to identify. Body is segmented in to small linked spheres, looks like body is made of connected bubbles. Type 11 : In moss B only Visible at 10x, barrel shaped with long thin strands extending from four or more appendages. More thin strands or antennae extending from the anterior. Exterior has a visible she ll and large plates, spastic movements by kicking legs. 14

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The elfin cloud forest in Monteverde, Costa Rica is an area with a species rich bryophyte community that harbors an unexplored community of microscopic organisms. I examined two morphospecies of bryophytes to compare their species richness of microorganisms living in the water the bryophyte holds. The factors that I examined that may affect microorganisms species richness are pH and structural differences between the bryophyte morphospecies. Bryophyte water samples were collected, pH was measured, and protozoan species were counted and viewed under a compound microscope. Even though there were visible differences in structural complexity between moss morphospecies (longer shoot lengths and thicker patches) there were non-significant differences between the average species richness per sample (Mann-Whitney U test, U = 78.5; P = 0.16). I found a significantly higher diversity of microorganisms in one moss morphospecies (T-test, t-value = 3.62, P < 0.05). The moss morphospecies with shorter shoot lengths had one unique microorganism and higher average (but not significant) species richness per mL of water than the second morphospecies (T-test, t-value = -1.5; P = 0.14). This is due to one moss morphospecies holding much more soil and detritus in its samples and therefore microorganisms living in the attached soil were also counted.
El bosque nuboso enano en Monteverde, Costa Rica es un rea con una comunidad de briofitas rica en especies, la cual es una comunidad inexplorada de organismos microscpicos. Examin dos morfoespecies de briofitos. Los factores que examin que pueden afectar la riqueza de especies de microorganismo es el PH y algunas diferencias estructurales entre las morfoespecies de briofitos.
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