OCCURRENCE AND DIVERSITY OF MYXOMYCETES (PLASMODIAL SLIME MOLDS

Acta Manilana 60 (2012), pp. 57–65 Printed in the Philippines ISSN: 0065–1370

Occurrence and diversity of myxomycetes (plasmodial slime molds) in Mt. Palay-palay National Park, Cavite, Philippines Israel Rhey Corpuz1, Czarina Cherizze Martinez1, Kimberly Anne Petilla1, Jaela Nicole Baranda1, Anthony Buaya2, & Thomas Edison E. dela Cruz1,2* 1

Department of Biological Sciences, College of Science and 2Fungal Biodiversity and Systematics Group, Research Center for the Natural and Applied Sciences, University of Santo Tomas, España Boulevard, 1015 Manila, Philippines

Myxomycetes are fungus-like organisms that are widely distributed in different ecological niches. This study look into the occurrence and diversity of myxomycetes in Mt. Palaypalay National Park in Cavite Province, Philippines. A total of 228 moist chambers were prepared from aerial and ground leaf litter, and twigs. Thirty one species of myxomycetes belonging to 11 genera were collected from the field and moist chambers. These were identified as Arcyria cinerea, A. denudata, Collaria arcyrionema, Diderma effusum, D. hemisphericum, Didymium iridis, D. megalosporum, D. nigripes, D. squamulosum, Hemitrichia calyculata, H. serpula, Lamproderma scintillans, Perichaena pedata, Physarum bivalve, P. compressum, P. echinosporum, P. globuriferum, P. oblatum, P. roseum, P. viride, and Stemonitis fusca. Highest myxomycete yield was observed in aerial leaf litter. In terms of taxonomic diversity, twigs showed the highest diversity followed by ground and aerial leaf litter. Highest species diversity and richness were also observed in twigs while evenness was noted in ground leaf litter. Similarities of myxomycete assemblages were low between the three substrata. This research study is the first report of myxomycetes in Mt. Palay-palay National Park, Cavite, Philippines. Keywords: slime molds, lowland forest, species abundance, species distribution, taxonomy

INTRODUCTION About 985 species of myxomycetes (plasmodial slime molds) are recorded in temperate and tropical forests worldwide [1]. In the Philippines, Reynolds [2] in the early 80’s listed

*To whom correspondence should be addressed E-mail: [email protected]

107 species of myxomycetes, and recently, this number was updated to 124 species by studies of Moreno et al.[3], Dagamac et al. [4, 5], and Macabago et al.[6]. In ecological terms, myxomycetes play several important roles in the environment. As “microbial predators” in forest soil ecosystems, slime molds served as important saprotrophs involved in soil nutrient cycling and respiration [7, 8]. Economically, myxymoyctes are also reported as sources of secondary metabolites with antimicrobial, Acta Manilana • Volume 60 (2012)

Corpuz IR et al. ⏐ Acta Manilana 60 (2012)

antifungal, trypanocidal, and cytotoxic activities [9, 10, 11]. These merit a thorough study of these organisms, specifically on their taxonomy and ecology. Whereas most of the ecological studies on myxomycetes were directed towards the temperate region [12], there is also a need for ecological studies on myxomycetes in the tropics particularly in the less explored lowland and montane forests of the Philippines. Mt. Palay-palay National Park in Ternate, Cavite with its secondary growth lowland forest and patches of primary lowland forest is an ideal site to explore for myxomycetes. Logging activities and “slash-and-burn” farming (“kaingin”) practices also threatened the area, and thus necessitates further assessment of its biodiversity. This research study therefore aimed to assess the occurence, distribution, and diversity of myxomycetes (slime molds) within the dipterocarp forested areas of Mt. Palay-palay National Park. This is the first report of myxomycetes in Mt. Palay Palay National Park in the province of Cavite, Philippines.

EXPERIMENTAL Study site. Mt. Palay-palay National Park (N14°12" E120°35") is located between the provinces of Cavite and Batangas, and belongs to three municipalities: Ternate, Maragondon, and Nasugbu (Fig. 1) Climatological data from the Philippine Atmospheric, Geophysical, and Astronomical Service Administration (PAGASA) recorded an annual temperature range of 28.4–26.2°C, an annual rainfall rate of 965–4064 mm, and a relative humidity percentage of 71–85%. The national park is composed of approximately 4000 hectares of forest reserves with a forest cover composed of a mixture of molave (Vitex parvilora A. L. Juss) and other dipterocarp trees. Sample collection and moist chamber (MC) preparation. Aerial (16) and ground (30) leaf litter, and twigs (30) were collected in brown paper bags in five areas along the accessible trail within the forest area. The collected samples were air-dried for few days, and moist chambers (in triplicates per sample) were setup

Arcyria cinerea Arcyria denudata Diderma effusum Diderma hemisphericum Didymium nigripes Lamproderma scintillans Physarum globuliferum Stemonitis sp.1 Stemonitis sp.3 Arcyria cinerea Arcyria sp.1 Diderma effusum Physarum echinosporum Physarum sp.1

Didymium iridis Perichaena pedata Physarum bivalve Physarum sp.1

Arcyria sp.2 Diderma effusum Diderma hemisphericum Didymium squamulosum Physarum compressum Physarum echinosporum Physarum oblatum

Arcyria cinerea Collaria arcyrionema Diderma effusum Diderma hemisphericum Didymium squamulosum

Figure 1. Map of the study site Mt. Palay-palay National Park in Ternate, Cavite and the species of myxomycetes identified in the five collection sites along the trail (in black dots).

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Occurrence and diversity of myxomycetes

for each of the samples following the protocol of Stephenson and Stempen [13]. A total of 228 moist chambers were prepared and placed in a wooden cabinet under diffused light at room temperature for up to 8 weeks. All moist chambers were regularly observed at least twice a week for the presence of myxomycetes either as plasmodia or fruiting bodies. Field specimens of myxomycetes were also collected within the forested area and placed in plastic box container. Fruiting bodies of myxomycetes collected from the field or moist chambers were placed on herbarium boxes and labelled properly. All specimen vouchers were deposited at the Pure and Applied Microbiology Laboratory, Research Center for the Natural and Applied Sciences, University of Santo Tomas in Manila, Philippines. Characterization and identification of myxomycetes. Fruiting body and spore morphologies of collected myxomycetes were described under a stereomicroscope and a compound light microscope. Fruiting body descriptions included the shape, type, size, appearance, and color of fruiting bodies, and the presence or absence of lime (CaCO3) and capillitium. Spores from the fruiting bodies were initially mounted on slides with 15% potassium hydroxide (KOH). Spore morphologies examined include shape, texture, size, and spore color. Identification was done following comparison of all morphometric data with published literature, and electronic and web-based identification keys (http://slimemold.uark.edu/). Ecological analysis. Initially, the percent yield of myxomycetes for each substrate type and the study site was computed by dividing the number of moist chamber (MC) with plasmodia/ fruiting bodies by the total number of MC prepared as described in Dagamac et al. [14]. A species list of myxomycetes in the study site was also prepared from collections in the field and moist chambers. The taxonomic diversity (S/G ratio) for each substrate type was then

assessed through the number of species and its corresponding genera. A lower S/G ratio indicates a higher taxonomic diversity since a biota in which the species are divided among many genera is “intuitively” more diverse in a taxonomic sense than one in which most species belong to only a few genera [15]. To assess further species diversity in the study site, the relative abundance was also determined for all of the species recorded from the moist chamber as described by Dagamac et al. [14]. A moist chamber positive with fruiting bodies of a specific myxomycete species is considered here as one positive collection. Then, the relative abundances (RA) for each species of myxomycetes were categorized as: (1) Abundant (A) if RA is >10% of the total collections, (2) Common (C) if RA is >5% but <10% of the total collections, (3) Occasional (O) if RA is >3 but <5 of the total collections, and (4) Rare (R) if the myxomycetes recorded a RA of <3% of the total collections [16]. Species diversity using the Shannon Index (HS), species richness using the Gleason Index (HG), and species evenness using the Pielou’s (E) Index were then computed based on these relative abundance data as described in Dagamac et al. [14]. A modified t-test (VarH) was also used to evaluate the significance differences of values of the different diversity indices [17]. Community analysis of the myxomycete assemblages was done by comparing the species common to the different substrates using the coefficient of community (CC) index as previously described by Stephenson [18]. The CC values close to 1.0 indicates that both substrates have the same species of myxomycetes.

RESULTS A checklist of myxomycetes in Mt. Palay-palay National Park, Cavite. A total of 31 species of myxomycetes belonging to 11 genera were collected from the field and the moist chambers. These were identified as Arcyria cinerea (Bull.) Pers., Arcyria denudata (L.) Wettst., Collaria

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arcyrionema (Rostaf.) Nann-Brem. Ex Ing, Diderma effusum (Schwein.) Morgan 1894, Diderma hemisphericum (Bull.) Hornem, Didymium iridis (Ditmar) Fries, Didymium megalosporum Berk, et M.A.Curtis, Didymium nigripes (Link) Fr, Didymium squamulosum (Alb et Schwein) Fr, Hemitrichia calyculata (Speg) M. L Farr, Hemitrichia serpula (Scop) Rostaf ex Lister, Lamproderma scintillans (Berk et Broome) Morgan, Perichaena pedata (Lister et G. Lister) Lister ex E. Jahn, Physarum bivalve Pers, Physarum compressum Alb, et Schwein, Physarum echinosporum Lister, Physarum globuriferum (Bull) Pers, Physarum oblatum T. Macbr, Physarum roseum Berk, et Broome, Physarum viride (Bull) Pers, and Stemonitis fusca Roth. A higher number of species was recorded in the moist chambers (20) than in the field collections (18). However, nine genera were reported from the field specimens while only eight genera were recorded from the moist chambers. Several of the collections could only be identified up to the genus level: Arcyria (two species), Comatrichia (one species), Cribraria (two species), Physarum (two species), and Stemonitis (three species). Our study is one of the most recent checklists of myxomycetes since the publication of the annotated list of Philippine myxomycetes by Reynolds in 1981 [2] and the first report of myxomycetes in Mt. Palay-palay National Park, Ternate, Cavite. Percent yield, occurrence, and diversity of myxomycetes. A total of 228 moist chambers were prepared from aerial and ground leaf litter,

and twigs. Myxomycetes were recorded from 55% of the prepared MC. However, only 19% yielded fruiting bodies while 41% had plasmodia. Among the three substrates, aerial litter yielded the highest number of myxomycetes (96%) followed by ground litter (53%) and twigs (32%). The taxonomic and species diversity was also determined for each of the substrate types (Table 1). Results showed that twigs had the most number of genera (7) followed by ground (5) and aerial (3) leaf litter. Twigs also had 11 species while both the aerial and ground leaf litter had five to six species only. Thus, the highest S/G value was recorded from the aerial leaf litter while the lowest S/G value was recorded from ground litter, and was the most taxonomically diverse (Table 1). The relative abundance of each species of myxomycetes was also assessed for the study site and each of the substrata (Table 2). Two species were recorded as abundant, two species were recorded as common, five species from three genera were recorded as occasionally occurring, and 11 species from seven genera were recorded as rare (Table 2). In terms of species abundance per substrate type, A. cinerea and Stemonitis sp.3 were abundantly recorded in twigs while D. effusum, Arcyria sp. 2, C. arcyrionema, D. nigripes, and Physarum sp.1 were recorded as abundant in ground leaf litter. Diderma effusum, D. hemisphaericum, D. squamulosum, P. compressum, and P. echinosporum were recorded as abundant in aerial litter. On the other hand, D. effusum, Arcyria sp.1, D. irridis,

Table 1. Species and taxonomic diversity of myxomycetes from the three different substrates collected in Mt. Palay-Palay National Park, Cavite. Substrates Aerial Leaf Litter Ground Leaf Litter Twigs

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No. of Genera 3 5 7

No. of Species 6 5 11

S/G Ratio 2.00 1.00 1.57

HS

HG

E

0.64 0.68 0.85

3.84 5.14 7.56

0.49 0.87 0.64


Table 2. Relative abundance (RA) of the different species of myxomycetes recorded per study site and substrate. Species Arcyria sp. 1 Arcyria sp. 2 Arcyria cinerea Arcyria denudata Collaria arcyrionema Diderma effusum Diderma hemisphericum Didymium iridis Didymium nigripes Didymium squamulosum Lamproderma scintillans Perichaena pedata Physarum bivalve Physarum compresum Physarum echinosporum Physarum globuriferum Physarum oblatum Physarum sp. 1 Stemonitis sp. 1 Stemonitis sp. 3

RA per Study Site R R A O R A C R R O R R R O O R R O R C

RA per Substrate Aerial Ground Twigs Litter Litter – – O – A – – – A – – C – A – A A O A – – – – O – A – A – – – – O – – O C – – A – – A – – – – O – – O – A – – – O – – A

A = abundant (>10); C = common (5–10); O = occasional (3–5); R = rare (<3) a Relative Abundance = No. of collection of a specific species of myxomycetes / Total number of myxomycete collection  100 b RA was computed from data obtained from moist chambers only

L. scintillians, P. pedata, P. globuliferum, P. oblatum, and Stemonitis sp.1 were recorded as occasionally occurring in twigs. Only two myxomycetes species were recorded as common, namely A. denudata and P. bivalve, which were recorded in twigs and aerial leaf litter, respectively. To further assess its diversity, the species diversity, richness, and evenness were assessed using three diversity indices: Shannon (H S ), Gleason (H G ) and Pielou’s (P) Indices. Since it is not possible to quantify the population of different species of myxomycetes in the study site, the relative abundance data from the moist chamber were used to compute these. A moist chamber positive for a species of myxomycetes is also recorded here as one individual for that particular species. In this study, the species diversity was highest in twigs (H S = 0.85)

followed by ground leaf litter (HS = 0.68) while aerial leaf litter was recorded as the lowest (HS = 0.64) (Table 1). However, analysis with ttest showed no significant difference between the Hs values when the three substrates were compared. In contrast, twigs has the highest value of richness (H G = 7.56) followed by ground litter (HG = 5.14) and aerial litter was recorded as the lowest (HG = 3.84). On the other hand, ground litter (E = 0.87) showed the highest value of evenness, followed by twigs (E = 0.64), while aerial litter (E = 0.49) had the lowest evenness value. When the communities of the collected myxomycetes in the 3 substrates were compared, a CC value of 0.18 was computed between aerial litter and ground litter, 0.12 for aerial litter and twigs, and 0.13 for ground litter and twigs.

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DISCUSSION Mt. Palay-palay National Park is an important key biodiversity area in Luzon since it is the only established wildlife sanctuary in the province of Cavite and is covered by approximately 62.5% lowland dipterocarp forest [19]. Hence, it was assigned as a “very high” conservation priority level by the Philippines’ Department of Environment and Natural Resources. However, for conservation efforts to be successful, it is necessary that the biodiversity of the area is well studied including its microbiota. Myxomycetes or slime molds are one of the least explored organisms in the country mainly due to lack of skills and interest by researchers. However, these myxomycetes play an important role as secondary saprotrophs in forest ecosystems [8]. These slime molds maintained balance between bacterial and fungal decay in ecological terms since these are predators of bacteria [20]. Myxomycetes such as Fuligo septica may also be used as models to study the uptake and concentration of heavy metals, e.g. zinc [21, 22]. Hence, it is important to assess myxomycete biodiversity in Mt. Palay-palay as it remains underexplored, and thus provides us baseline information for the conservation initiatives for the protection and preservation of the national park. In the study, 31 species of myxomycetes belonging to 11 genera were recorded in Mt. Palay-palay National Park. The collected species belongs to the genera Arcyria, Collaria, Comatricha, Cribraria, Diderma, Didymium, Hemitrichia, Lamproderma, Perichaena, Physarum, and Stemonitis. More species were noted in moist chambers than in field collections. The use of moist chambers in assessing myxomycete diversity in the tropics, subantartic and temperate regions is well established. For

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example, Wrigley de Bassanta et al. [23] recorded 442 collections of myxomycetes from Patagonia and Tierra del Fuego in Argentina with 37% of the moist chambers positive for myxomycetes. Similarly, Tran et al. [24] reported that substrata collected during the rainy season had 42% positive for myxomycetes while substrata collected during the dry season had 72 % of the moist chambers with myxomycetes. In the Philippines, Macabago et al. [25] reported myxomycetes from 51% of the prepared MC. A lower percentage (23%) was reported by Dagamac et al. [14] in Mt. Arayat National Park. The result of the productivity obtained in the study was thus comparable to these papers. Similarly, this study and that of Macabago et al. [25] and Dagamac et al. [14] noted that highest productivity was recorded with aerial leaf litter. Aerial leaf litter served as good spore trap during spore dispersal, and hence, may explain its higher yield of myxomycetes. In the study of Schnittler et al. [26], myxomycete spores can easily be dispersed up to 1.8 km by even a slight breeze, and theoretically up to 500 km by a storm with a speed of 100 km/h. Kilgore et al. [27] also observe that herbaceous plant aerial structures were favourable microhabitat for myxomycetes as compared to ground litter. In contrast to the productivity, the highest S/G value was recorded from the aerial leaf litter and thus, the least taxonomically diverse (Table 1). Ground leaf litter had the lowest S/G value and the highest taxonomic diversity. Five species belonging to five genera were reported from ground leaf litter. Decaying leaf litter serve as a favourable habitat for microorganisms including myxomycetes [1, 28]. Ground litter harbour more microorganisms and traps moist which thus positively correlates to high species occurrence in ground litter as compared to other substrates [13, 18].


Assessment of diversity and distribution of myxomycetes in Mt. Palay- Palay was also determined using relative abundance data from the moist chambers. Novozhilov et al. [29] noted that moist chambers were sufficient enough to reflect the diversity of species of myxomycetes in a particular habitat or study site. In the study, the abundant species included Arcyria cinerea and Diderma effusum (Table 2). A. cinerea was reported abundant only in twigs while D. effusum was abundant in both aerial and ground leaf litter.

demonstrated that woody substrates tend to be favourable for the majority of myxomycetes due to its high moisture content as also shown by the data on twigs in this study.

Five species were also reported abundant in both leaf litter substrate while only two species were abundant in twigs. The results are not surprising since species of Diderma and Arcyria were often found abundantly in the tropics. In Macabago et al. [25], A. cinerea was reported abundant in all substrates while D. effusum was abundant only in aerial leaf litter. Dagamac et al. [14] reported A. cinerea as abundant in all substrates, and in the two study sites and collection seasons in Mt. Arayat, though D. effusum was recorded as rare or occasionally occurring. A higher number of collections were also recorded for A. cinerea in Ecuador [30], Paraguay [31], Costa Rica [32], Canary Island of Spain [33], and Thailand [28].

Finally, when the communities of the collected myxomycetes in the three substrates were compared, low CC values were recorded for all combinations. This simply implies that the species present were different in each of the substrates. This is interesting given that the substrata were collected almost in proximity. In contrast, Dagamac et al. [14] reported a higher CC values between aerial and ground leaf litter. Of all species of myxomycetes recorded from the moist chambers, only D. effusum was found present in three substrates. This species of myxomycetes is known to be of cosmopolitan distribution.

Analysis of diversity indices showed that twigs had the highest diversity and richness (Table 1). Eleven species belonging to seven genera were reported from twigs. However, species were most evenly distributed in ground leaf litter. In spite of the higher productivity of aerial leaf litter, i.e. 46 of the 48 MC yielded myxomycetes, aerial leaf litter had the lowest taxonomic and species diversity (Table 1). Lowest species richness and evenness were also recorded for aerial leaf litter as compared to the two substrates. These differences can be accounted by several environmental factors such as texture, pH and moisture of the substrates, and the available food microorganisms present on the substrate [12, 34]. Ing [35] and Stephenson et al. [36]

The rates of decomposition of the substrates which can be correlated for the presence of microorganisms also have influence on myxomycete diversity [24, 26]. This was perhaps the case observed for the ground leaf litter in this study which yielded a high number of species as opposed to aerial leaf litter.

CONCLUSIONS A total of 31 myxomycetes species belonging to 11 genera were recorded from the field and moist chamber of aerial and ground leaf litter and twigs collected in Mt. Palay-palay National Park in Ternate Cavite, Philippines. A higher number of collections were noted in moist chamber. A higher number of species and species diversity of myxomycetes was also noted in twigs. Aerial leaf litter had the lowest taxonomic and species diversity, though its moist chamber yielded the most of number of MC positive for myxomycetes. Of all collected species, Arcyria cinerea and Diderma effusum were recorded the most abundant. This is the first report of mycomycetes in Mt. Palay-palay National Park.

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AKNOWLEDGMENT The authors would like to thank the Research Center for the Natural and Applied Sciences of the University of Santo Tomas Manila under the directorship of Christina Binag, Ph.D. for the laboratory, research facility, and research grant for this study.

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OCCURRENCE AND DIVERSITY OF MYXOMYCETES (PLASMODIAL SLIME MOLDS

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