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Mycologia, 95(1), 2003, pp. 11-18.
© 2003 by The Mycological Society of America

Microhabitat distribution of protostelids in a Tropical Wet Forest in Costa Rica


Donna L. Moore 1

     Biology/Chemistry Division, Corning Community College, Corning, New York 14830

Steven L. Stephenson

     Department of Biology, Fairmont State College, Fairmont, West Virginia 26554

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

A microhabitat study of protostelids was carried out in a Tropical Wet Forest at the La Selva Biological Station in Costa Rica. Nine species were recorded from sterile wheat straws placed out and then re-collected over a period of six weeks from two different litter microhabitats in an area of primary forest. All nine species were present on straws placed in the aerial litter microhabitat, but only six species were present on straws placed in the forest floor litter microhabitat. Total colonies, percent of straws colonized, and mean number of species per straw increased significantly over time. One species (Schizoplasmodiopsis pseudoendospora) typical of temperate litter was the overwhelming dominant on the forest floor litter, while Echinostelium bisporum, a species rare in temperate litter microhabitats, was the single most abundant species in the aerial litter microhabitat. Both of these species had significantly increased frequencies over time. Two species abundant in temperate aerial litter microhabitats and one species abundant in temperate forest floor litter were rare at La Selva. Our data conform to those obtained in an earlier study carried out in tropical forests in the mountains of Puerto Rico and provide additional support towards developing a model of microhabitat distribution of protostelids in terrestrial ecosystems.

Key words: ecology, mycetozoans, protoctists, slime molds, tropics


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Protostelids are a group of unicellular slime molds with amoeboid trophic cells and simple fruiting bodies in their life cycles. Together with two other groups of slime molds, the myxomycetes and dictyostelids, they make up the taxonomic group Eumycetozoa (Olive 1975Citation, Spiegel et al 1995Citation). Slime molds are eukaryotic, phagotrophic bacteriovores that probably have an important role in the regulation of the populations of bacteria present in soils and other microhabitats (Feest 1987Citation). Information relating to the ecology of protostelids has increased tremendously in recent years due to the introduction of a standardized sampling technique developed by Moore and Spiegel (1995)Citation. The technique has been used in studies carried out in a number of different types of ecosystems, including boreal forests and tundra of Alaska, temperate forests and grasslands of Arkansas, and tropical forests of Puerto Rico. Data obtained from these studies suggest that in temperate climates species tend to be partitioned between the aerial litter and the forest floor litter microhabitats, being relatively more abundant in one microhabitat than in the other (Moore and Spiegel 2000aCitation, bCitation). However species of protostelids commonly associated with the aerial litter microhabitat in temperate regions were rarely encountered in tropical forests of Puerto Rico, whereas the species associated with forest floor litter in temperate regions were present and abundant in the aerial litter and the forest floor litter microhabitats of Puerto Rico (Moore and Spiegel 2000cCitation).

Species diversity and richness of protostelids have been reported to vary among ecosystems. Temperate habitats in Arkansas exhibit the greatest species diversity and richness reported to date (Moore and Spiegel 2000aCitation), with tropical forests [Subtropical Wet, Subtropical Rain, and Lower Montane Rain Forests sensu Holdridge (1967)Citation] in the mountains of Puerto Rico (Moore and Spiegel 2000cCitation) next, and boreal forests and tundra of Alaska (Moore et al 2000Citation) characterized by the lowest species diversity and richness. However, very preliminary research in Tropical Wet and Tropical Moist Forests (Holdridge 1967Citation) of Costa Rica (Moore and Stephenson 1998) suggested a higher species richness (17 species) than was found to exist in Puerto Rico (10 species). Whether these trends are the result of differences in latitude, vegetation, or particular microhabitats, or a combination of all these factors, is not yet known.

The purpose of the present study was (i) to obtain, using the sterile straw technique, additional quantitative data on protostelid occurrence and distribution in tropical forests, (ii) to determine whether species associated with the temperate aerial litter microhabitat are rare in Tropical Wet Forests of Costa Rica, as they appear to be in Puerto Rico, and (iii) to determine whether species associated with temperate forest floor litter microhabitat exhibit a preference for the same microhabitat in the tropics.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
The La Selva Biological Station is located in the Atlantic lowlands of northeastern Costa Rica, near the confluence of the Sarapiqui and Puerto Viejo rivers in the province of Heredia. The predominant vegetation is Tropical Wet Forest, with about 55% of the area of the station consisting of primary forest. Average annual precipitation is about 4000 mm, with peaks of more than 400 mm per month occurring both in June–July and November–December. The period with the least precipitation is February–April, and March is normally the driest month. The average monthly air temperature is 25.8 C, which differs little among months. Indeed, the diurnal range in air temperature (6–12 C) greatly exceeds the monthly change of <3 C (McDade et al 1994Citation).

Four 5 x 5 m study plots were established along the Camino Circular Lejano Trail, which runs through an area of primary Tropical Wet Forest at La Selva. These plots were selected in areas where permanent plots had not been established by other researchers and served to sample the diversity across the forest type. Two of the plots were located near the 100 m marker, one 15 m directly north (10° 25' 35'' N, 84° 00' 09'' W) and the other 15 m south (10° 25' 33'' N, 84° 00' 09'' W) of the marker. Two other plots were located 225 m farther along the trail, with one plot 15 m directly north (10° 25' 31'' N, 84° 00' 14'' W) and the other 15 m directly south (10° 25' 30'' N, 84° 00' 15'' W) of the trail.

Each 5 x 5 m study plot was divided into nine 1.6 m2 subplots. For each plot, four subplots were randomly chosen. Eight sterile straws were placed in each of the two microhabitats (forest floor litter and aerial litter) within each subplot. Straws were prepared in the manner described by Moore and Spiegel (1995)Citation. The forest floor litter microhabitat was defined as the layer of twigs, leaves, and other plant debris extending over the soil surface. Straws placed in this microhabitat were anchored to the leaf litter/soil by a stainless steel straight pin. The aerial litter microhabitat was defined as the assemblage of dead, attached plant parts located above the forest floor in the same subplots. Straws placed in the aerial litter microhabitat were sewn onto pieces of sterile nylon fishing line by using a sterile sewing needle. These were then strung between the two closest trees or, in some cases, palms or ferns at approximately 1 m above the ground. For each collection, one straw per microhabitat per subplot was randomly selected, removed from the fishing line (aerial straws) or straight pin (ground straws) and placed into a sterilized test tube provided with a rubber stopper. All straws were placed into the field on 15 March 2000. The first collection was made 3 wk later, on 5 April 2000, and collections continued each wk thereafter for a total of 4 collections, these being made on wk 3, 4, 5, and 6. Straws were plated out as described in Moore and Spiegel (1995)Citation.

Observations of culture plates began approximately 5 d after samples were plated out and continued for 3 wk. Species were identified by fruiting body morphology and, if necessary, by characteristics of the amoebae. The number of colonies was counted for each species per straw. A colony was defined as a cluster of fruiting bodies that was continuous along the straw and separated by more than 2 mm from the next such cluster as viewed under x100 with a compound light microscope. A single colony was also assumed to be a clone. The total number of straws colonized, mean number of colonies, and mean number of species per straw were calculated for each treatment by time replicate. The total number of colonies of each species per treatment was also calculated. These frequency data were assumed to conform to a Poisson distribution and were transformed using a Poisson variance stabilizing transformation (Anscombe 1948Citation). Data were subjected to repeated measures ANOVA, using Systat statistical software (Wilkinson 1998Citation). In the model used, time and microhabitat were considered the main effects, and a time by treatment interaction term was included. Post-hoc comparisons among treatments were made only if the overall ANOVA model with repeated measures was significant (P < 0.05). Plots were treated as replicates in this study (Montgomery 1991Citation). In addition, Shannon-Weiner diversity indices were calculated by summarizing data by plot for all weeks, and an ANOVA was used to analyze microhabitat effects. The level of significance was set as P = 0.05. A post hoc test, least square means, was used to analyze the multiple comparisons across treatments (Hatcher and Stepanski 1994Citation).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Nine species of protostelids were recorded on straws and seven species were recorded from native substrates during the entire study (Table I). Seven of the nine species encountered on straws from the aerial microhabitat also were encountered from native substrates from this microhabitat. Four of the six species encountered on forest floor litter straws also were encountered on samples of forest floor litter substrates.


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  		TABLE I. Relative (%)1 and absolute abundance (in parentheses) of species on straws compared to presence (+) or abundance (-) of species on natural substrates by microhabitat

 
Schizoplasmodiopsis pseudoendospora was the most abundant species, representing 44% of the total number of all colonies (Table I). Echinostelium bisporum was the second most abundant species, representing 23% of the total, while the third most abundant species, Cavostelium apophysatum, made up 15% of total. The other species encountered were uncommon or rare and none comprised more than 7% of the total number of colonies.

All straws collected during this entire study yielded a total of 188 colonies (Table II). Of the 128 individual straws collected, 69 straws (59%) were colonized by at least one protostelid. The mean number of colonies present on a particular straw was 1.47, while the mean number of species present per straw was less than one. A Shannon-Weiner diversity index value calculated for the entire data set was 1.57.


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  		TABLE II. Summary of colonization

 
Eighty-two colonies representing six species were present on the forest floor straws, and nine species, and 106 colonies were present on the aerial litter straws (Table I). Sixty-one percent of straws collected from the aerial litter microhabitat were colonized, while the corresponding figure for straws collected from the forest floor was 58% (Table II). The mean number of colonies was 1.66 for the aerial straws and 1.28 for the litter straws. Shannon-Weiner diversity indices were 1.68 for the aerial litter microhabitat and 0.98 for the forest floor litter microhabitat, with the aerial microhabitat exhibiting suggestively higher diversity (Table III, P = 0.055). In the repeated measures ANOVA, percent of straws colonized, mean number of both colonies and species per straw changed significantly over time (Table III, P < 0.05). For all three variables, colonization was statistically higher for weeks 4, 5, and 6 when compared to week 3 (Figs. 1, 2).


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  		TABLE III. ANOVA table for post-hoc tests

 


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  		FIG. 1. Mean number of Schizoplasmodiopsis pseudoendospora by week (± SE; P = 0.006).

 


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  		FIG. 2. Mean number of colonies of Echinostelium bisporum by microhabitat (± SE; P = 0.02). {diamondsuit}, aerial; {blacksquare}, litter.

 
In post-hoc comparisons, the two most abundant species were found to have statistically significant interactions or main effects using repeated measures ANOVAS (Table III). Schizoplasmodiopsis pseudoendospora was significantly more abundant on the forest floor than in the aerial litter microhabitat (Table I, P = 0.0001). Colonies of S. pseudoendospora also increased significantly between week 3 and week 4 (Fig. 1, P = 0.006) but not between weeks 4, 5 and 6. A significant time by microhabitat interaction for E. bisporum resulted from significantly greater numbers of colonies in the aerial litter microhabitat than in the litter microhabitat for all times except for week 3 (Fig. 2, P = 0.02).

The number of additional species collected each week was higher for the aerial than the forest floor microhabitat during weeks 3, 4, and 5 (Fig. 3a). Species numbers reached a plateau during weeks 5 and 6 in the aerial litter microhabitat, but an increase continued for week 6 in the ground litter microhabitat (Fig. 3b).



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  		 FIG. 3. Time until first appearance of species. A. Aerial microhabitat. B. Litter microhabitat. Ca = C. apophysatum, Eb = E. bisporum, Eo = E. oligospora, Ng = N. gracile, No = N. ovatum, Pa = P. arachisporum, Pm = P. mycophaga, Sp = S. pseudoendospora, Sv = S. vulgare

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The primary Lowland Tropical Wet Forest at La Selva, located on the Central American mainland, was characterized by higher species diversity, although similar species richness, and higher overall straw colonization than the Tropical and Subtropical Wet Forests in the mountains of Puerto Rico, an island in the Caribbean (Moore and Spiegel 2000cCitation). The straw technique successfully sampled species in the aerial and forest floor litter microhabitats, collecting two more species than controls. The present study yielded fewer species (9) than a previous study in Costa Rica (Stephenson and Moore 1998Citation) in which 17 species were isolated from samples of native litter. Schizoplasmodiopsis pseudoendospora, a species associated with the forest floor litter in temperate regions, is also more frequent in the same microhabitat at La Selva. Echinostelium bisporum, a species rarely encountered in temperate habitats and not recorded from Puerto Rico, was more abundant in the aerial litter than on the forest floor. Soliformovum irregularis and Protostelium mycophaga, two common inhabitants of the aerial litter microhabitat in temperate regions, appear to be rare at La Selva, as was also the case in Puerto Rico (Moore and Spiegel 2000cCitation). Similarly, Nematostelium gracile, a common forest floor species in temperate habitats, also was rare at La Selva. The aerial litter microhabitat in the forest at La Selva exhibited higher species richness and diversity than the forest floor litter microhabitat, another pattern that conforms to the data obtained in Puerto Rico. Comparisons of the time until first appearance of protostelids in aerial and forest floor litter microhabitats also suggest quicker colonization of species onto straws in the aerial litter microhabitat, another pattern that conforms to the Puerto Rican data. Longer study periods may be needed to adequately sample rare or seasonal species.

The earlier study of protostelids in Costa Rica (Stephenson and Moore 1998Citation) yielded several more species than this study. That study encompassed several different tropical forests from across the entire country and was the first of its kind for protostelids in Costa Rica. Also in the earlier study, samples of naturally occurring litter were analyzed for the presence or absence of species, a crude quantitative measurement. In the present study, emphasis was placed on colonization of straws so that colony counts could be made. The straw technique lends itself to more accurate quantitative data, unlike the sampling of naturally occurring litter. Further research in Costa Rica should focus on the sampling of various forest types by using the straw technique.

This research certainly begs the question as to whether classical trends associated with island biogeography hold true for protostelids (MacArthur and Wilson 1963Citation, 1967Citation). Certainly the lower species richness and diversity associated with protostelids from Puerto Rico (an island) compared to Costa Rica (on the mainland) would support this theory. Since quantitative data using the straw technique have not been applied to any other tropical island or mainland, it is not yet possible to determine whether the trends in protostelid distribution are following the theory of island biogeography.

Comparison of data on protostelids obtained from the research in Costa Rica with data from Puerto Rico suggests that different types of tropical forests may not be as similar as one might imagine. Although mean annual rainfall is similar between the Puerto Rican sites (350–400 cm) and the Costa Rican site (400 cm), mean annual temperatures are higher (ca 3 C) for the Costa Rican site. Consequently, potential evapotranspiration (PET) is lower for the Costa Rican site (i.e., at higher temperatures and rainfall, humidity is highest and PET is lowest). This translates into more humidity and less moisture in the soil. Protostelid diversity and overall colonization on sterile straws were both higher for the primary Tropical Wet Forest in Costa Rica when compared to the Subtropical Wet Forests in the mountains of Puerto Rico. There is preliminary evidence that species richness is higher in dry and mesic forests than rainforests of Puerto Rico, as well as Hawaii (Spiegel pers comm). It has been suggested that constant high levels of precipitation may inhibit colonization of substrates by protostelids (Spiegel pers comm), and this may have been a factor for the forests sampled in Puerto Rico. It may, however, be that PET is higher for the Puerto Rican sites and that the soil/ground layers were more saturated. If such is the case, the Lowland Tropical Wet Forest at La Selva may provide relatively more moderate environmental moisture conditions, which in turn would be more conducive to protostelid colonization of those substrates potentially available to them. Interestingly, results obtained from microhabitat studies of myxomycetes carried out in tropical forests at several localities in Puerto Rico and Costa Rica indicate that members of this other group of slime molds are often more abundant and diverse in aerial microhabitats located above the ground than in microhabitats associated with the forest floor, their usual microhabitats in temperate and boreal forests (Stephenson et al 1998Citation). Myxomycetes appear to be organisms adapted to highly fluctuating conditions of environmental moisture, but continuously high moisture levels apparently do not favor their growth and development, thus leading to their apparent displacement from the forest floor (relatively moist) to aerial (relatively drier) microhabitats (Stephenson et al 2001Citation). Obviously, greater sampling in tropical climates will enable a better understanding of biogeography of protostelids.

As quantitative data accumulate, the differential occurrence of protostelids among microhabitats tells us more about their ecology than meets the eye. In temperate habitats, the forest floor litter microhabitat is distinct from the aerial litter microhabitat. The forest floor litter microhabitat is protected from drastically changing humidity, unlike the aerial litter microhabitat. In temperate regions, we see a group of species preferring the aerial or the forest floor litter microhabitat. In boreal and tundra forests, the forest floor microhabitat is much more like the aerial litter microhabitat; plants are often stunted and a leaf litter layer characteristic of temperate habitats is often lacking. Results from preliminary research hint to a "dropping" of temperate aerial litter species into ground litter in Alaska, although ground litter species still prefer this microhabitat. Compared to temperate forests, the aerial litter microhabitat is much more similar to the ground litter microhabitat in tropical forests. Our data seem to indicate that ground litter species "move" up into the aerial litter microhabitat, often being equally abundant in both microhabitats. Aerial litter species, however, were found to be rare in both microhabitats in tropical montane forests in Puerto Rico. The results of the present study support this hypothesis. Seasonal data from temperate habitats in Arkansas (Moore and Spiegel 2000bCitation) and data along an elevation gradient in Puerto Rico (Moore and Spiegel 2000cCitation) lend credibility to this working hypothesis of microhabitat distribution patterns in various ecosystems.

At least two species, P. mycophaga and N. ovatum, are highly abundant in temperate habitats but rare in the tropics. It may be that these are temperate species or that some aspect of the abiotic environment of the tropics limits their growth and/or dispersal. They certainly are present, but in low abundance. Another species, N. gracile, seems to be more abundant in Puerto Rico than either Arkansas or La Selva. In Arkansas, it is more abundant in the forest floor litter microhabitat and in Puerto Rico it is present in both microhabitats but exhibits a shift in microhabitat preference, from forest floor litter to aerial litter, as elevation increases (from a Tabonuco Forest to Palo Colorado Forest). Again, there appears to be something about the microhabitat that determines its abundance; whether this factor is abiotic or biotic requires further investigation. Two species, E. bisporum and C. apophysatum, are more abundant in La Selva than any other habitats examined with the straw technique. If they were truly tropical species, one would expect them to be equally abundant in Puerto Rico. At least for E. bisporum, there is another possible explanation, since this species appears to exhibit an occasional localized population explosion. Best and Spiegel (1984)Citation found that it was particularly abundant on old fruits and peduncles of Geum canadensis, a temperate member of the family Rosaceae. It may be that E. bisporum has a rather specific substrate preference and therefore occurs in localized populations. More intensive sampling in all habitats may find that this species is more common than once thought. It seems likely that C. apophysatum is a truly tropical species. Recent research in mesic forests of Puerto Rico and Hawaii corroborates this hypothesis (Spiegel pers comm). As further research is completed, we will have a better idea of what governs the population distribution of protostelids.

In summary, assemblages of protostelids associated with a primary Tropical Wet Forest at the La Selva Biological Station in Costa Rica exhibit lower overall colonization, species richness, and diversity than those of temperate habitats but higher species diversity and colonization than those reported for tropical montane forests of Puerto Rico. The body of information obtained in the present study, the first to use the sterile straw technique of Moore and Spiegel (1995)Citation to assess protostelid colonization in tropical forests of Costa Rica, represents a contribution towards the goal of developing a more complete understanding of the distribution and ecology of protostelids in terrestrial ecosystems. Moreover, the results we obtained provide a basis from which further studies can be launched.


   ACKNOWLEDGMENTS
 
This study was supported in part by a grant (DEB-9705464) from the National Science Foundation (to SLS). The assistance of Randy Darrah in setting up the study plots is gratefully acknowledged.


   FOOTNOTES
 
1 Corresponding author, moore_d{at}corning-cc.edu Back

Accepted for publication June 13, 2002.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Anscombe FJ., 1948 The transformation of poisson, binomial, and negative-binomial data. Biometrika 35:246-254[Free Full Text]

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Feest A., 1987 The quantitative ecology of soil mycetozoa. Progr Protistol 2:331-361

Hatcher L, Stepanski EJ., 1994 A step-by-step approach to using the SAS system for univariate and multivariate statistics. Cary, North Carolina: SAS Institute Inc. 552 p

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———, ———. 1967 The theory of island biogeography. Monographs in population biology I. Princeton: Princeton University Press. 218 p

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———, Stephenson SL, Laursen GL, Woodgate WA., 2000 Protostelids from boreal forest and tundra ecosystems in Alaska. Mycologia 92:390-393

Olive LS., 1975 The mycetozoans. New York: Academic Press. 293 p

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Stephenson SL, Estrada-Torres A, Schnittler M, Lado C, Wrigley de Basanta D, Ogata N., 2001 Distribution and ecology of myxomycetes in the forests of Yucatán. In: Gómez-Pompa A, Allen M, Fedick S, Jimenez J, eds. Lowland Maya Area: three millennia at the human-wildland interface. New York: Haworth Press (In press)

Stephenson SL, Landolt JC, Moore DL., 1998 Protostelids, dictyostelids, and myxomycetes in the litter microhabitat of the Luquillo Experimental Forest, Puerto Rico. Mycol Res 103:209-214

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