1Department of Biological Sciences, College of Science, University of Santo Tomas, España Blvd. 1015 Manila, Philippines
2Fungal Biodiversity, Ecogenomics and Systematics-metabolomics (FBeS) Group, Research Center for the Natural and Applied Sciences, University of Santo Tomas, España Blvd. 1015 Manila, Philippines
*Corresponding author: [email protected] Date Submitted: 15 July 2023
Date Accepted: 31 October 2023 Date Published: 19 December 2023 Introduction
Myxomycetes, also known as plasmodial slime molds, are amoeboid, eukaryotic organisms that exhibit fungus-like characteristics as they give rise to spore-producing fruiting bodies. The fruiting bodies or sporocarps are visible on decaying plant debris such as logs, twigs, and leaf litter on the ground. Moist chamber culture (MC) techniques can also be used to record the presence of myxomycetes from plant- based substrata (Schnittler et al. 2015), such as inflorescences (Schnittler & Stephenson 2002; Cavalcanti et al. 2015; Alves de Sá et al. 2022; Pecundo et al. 2023), bark of living trees (Takahashi et al. 2018; Policina & dela Cruz 2020), twigs (Cabutaje et al. 2021), leaf litter (Macabago et al. 2016; Buisan et al. 2020), and woody vines (Pecundo et al. 2021; dela Cruz et al. 2023).
Green areas in cityscapes have recently been gaining attention for biodiversity and urban ecology studies. Parsons et al. (2018) indicated that urbanized areas had notably higher relative abundance, species richness, and diversity including mammalian occurrence as compared to wild areas. It is suspected that urbanized areas provide ample food resources for these animals through direct feeding or unintentional feeding through wastes and ornamental
value and perceived health benefits for the building occupants. Leaf litter from plant communities in these gardens offer suitable microclimate conditions and substrates that can support growth and development of myxomycetes. Myxomycetes, also called slime molds, play a role in maintaining the soil microbiome, and can influence the microbial communities in these residential gardens. In this study, 204 ground leaf litter samples of ornamental woody shrubs and herbaceous flowering plants were collected from elevated gardens in eight low-to-high rise buildings for the preparation of moist chambers (MC).
A total of 14 species of myxomycetes belonging to nine genera were recorded and identified in this study: Arcyria cinerea, Collaria arcyrionema, Diachea leucopodia, Diderma effusum, Diderma hemisphaericum, Didymium nigripes, Didymium sp., Didymium squamulosum, Ophiotheca chrysosperma, Perichaena cf. corticalis, Perichaena depressa, Physarum album, Physarum cinereum, and Stemonitis cf. pallida. Overall MC productivity ranged from 43 to 45%. In terms of species abundance, Arcyria cinerea and Perichaena depressa were among the most recorded myxomycetes. The study provided evidence of roof- top gardens as suitable habitats for myxomycetes.
Keywords: Amoebozoa, cosmopolitan, leaf litter, ornamental plants, slime molds, species occurrence, urban areas
plantings for herbivores. In the study of Wang et al. (2020), species richness of woody trees and perennial herbs also increases with urbanization. This was attributed to the high demand and preference for woody trees by urban planners and governments to quickly create green spaces and to the more adaptive survival strategies of perennial herbs on highly disturbed urban environment. Flores et al. (2020) showed that urban parks in Metro Cebu had a significant diversity and abundance of native and exotic ornamental plants. The study documented a total of 100 plant species, 95% of which are described as exotic and 5% as native species. The increase in vegetation in urban cities can significantly alter the diversities of organisms that are dependent on these plant communities.
Theodorou et al. (2020) showed higher species richness and flower visitation rates in cities by pollinator bees. Mushroom species richness had been positively correlated with diverse trees in urbanized areas, and with their study even reporting the discovery of new records for the country (Cho et al.
2020). Changes in plant communities, even due to natural disturbances, were also thought to impact species richness and play a role in shaping the diversity of myxomycetes in an area (Macabago et al. 2017; Cabutaje et al. 2021). This is further supported by the study of Ing (1983) which stated that the available plant species in a specific area affects the presence of myxomycetes within the vicinity.
Myxomycetes have been reported from urban areas.
Rincon-Marin et al. (2021) listed a total of 32 myxomycetes species in two urban centers in Costa Rica while Hosokawa et al. (2019) listed 23 species from the inner-city and semi- urban parks in Sydney, Australia. Similarly, the study of Stephenson and Novozhilov (2021) reported 26 species of myxomycetes from ornamental woody shrubs and herbaceous flowering plants in a residential area garden. The study reported the similar number of taxa as compared to much
Philippine Journal of Systematic Biology Online ISSN: 2508-0342 larger sampling area of inner-city and semi-urban parks by Hosokwa et al. (2019). Meanwhile, in the Philippines, the study of Macabago et al. (2010) reported 28 species of myxomycetes from La Mesa Ecopark, the remaining green area within the urban city of Metro Manila. It was the first attempt to document myxomycetes from substrata collected within the National Capital Region. Recently, Garcia et al.
(2022) recorded eight species from a low-rise condominium building using a spore baiting approach coupled with moist chamber culture technique. The study reported relatively few species using spore baiting as a means to record the presence of myxomycetes from airborne spores. Contrary to the expected outcomes, wind flow, a driver of spore dispersal, did not significantly vary the species richness between an open- spaced area with unobstructed wind and an enclosed area with limited wind flow.
In this paper, we identified myxomycetes recorded
from ground leaf litter collected in urban roof-top gardens.
As diversity of myxomycetes is strongly correlated with vegetation types as earlier pointed out by Alfaro et al. (2014), the present study hypothesized that the leaf litter in plant communities in elevated urban gardens supports the growth of myxomycetes and can influence its species richness.
Materials and Methods Sampling Sites
Eight residential buildings with elevated or roof-top gardens within four cities in Metro Manila were chosen as study sites based on their availability and accessibility (Fig. 1).
Five of these residential buildings are in Manila and Quezon City within the populous part of the metro while the remaining three residential buildings are in the eastern side (Marikina) and the southwestern side (Las Piñas) where human population is less dense and/or with proximity to natural habitats. Elevated Figure 1. (a) Map of the study areas (map generated from QGIS). Photos of selected roof-top gardens: LRB - (b) Sta. Cruz Apartment, (c) 1588 Apartment Building, HRB - (d) Celadon Park Tower 3, (e) Sun Residences Condominium Tower 1.
a
Park Tower 2 [Manila City, 14°37′13.63″N 120°59′09.61″E], (6) Sun Residences Condominium Tower 1 [Quezon City, 14°37′05.8″N 121°00′01.98″E], (7) Paseo Verde At Real Tower 1 [Las Piñas City, 14°28′21.74″N 120°58′39.58″E], and (8) Paseo Verde At Real Tower 2 [Las Piñas City, 14°28′24.57″N 120°58′39.57″E] (Fig. 1). An approval from the building administrators was secured prior to the collection of leaf litter substrata.
Substrate collection and moist chamber (MC) preparation Samples of ground leaf litter were collected and placed in paper bags and then air-dried for at least a week prior to the preparation of moist chambers. One sample of collected leaf litter represented by one paper bag was used to prepare one moist chamber. Based on the available samples, a total of 204 moist chambers, i.e., 37 MC from the three low-rise buildings and 167 from the five high-rise buildings, were prepared in this study following the protocol of Stephenson & Stempen (1994).
The number of samples/moist chambers for each sampling site is provided in Table 1. Briefly, the leaf litter samples were
microscope for morphological traits. Microscopic slides with water as mounting medium were prepared to observe spore characteristics. Identification follows the morphometric descriptions in Les Myxomycetes (Poulain et al., 2011).
Names follow the online nomenclature information system of Eumycetozoa (Lado 2005-2023).
Data Analysis
The computed percent yield or moist chamber productivity follows the protocol of Macabago et al. (2012).
The frequency of moist chambers positive for myxomycetes was determined and divided by the total number of prepared MC. A moist chamber culture with occurrence of plasmodia or fruiting bodies was recorded as one positive collection in this study. In case both plasmodia and fruiting bodies were observed in a single moist chamber, it is counted as positive for fruiting bodies. For the construction of the species accumulation curves (SAC), an input file in tab-delimited format comprising the abundance data for each type of sampling sites was subjected using the scripts for iNEXT
Low Rise Buildingsa High Rise Buildingsb
Species S1 S2 S3 Total S4 S5 S6 S7 S8 Total
Arcyria cinerea (Bull.) Pers. 0 1 1 2 4 2 9 2 0 17
Collaria arcyrionema (Rostaf.) Nann.-Bremek. ex Lado 0 0 0 0 0 0 3 0 0 3
Diachea leucopodia (Bull.) Rostaf. 0 0 0 0 0 0 2 0 0 2
Diderma effusum (Schwein.) Morgan 0 0 0 0 1 0 2 0 0 3
Diderma hemisphaericum (Bull.) Hornem 0 0 0 0 1 0 0 0 1 2
Didymium nigripes (Link) Fr. 1 1 0 2 0 0 0 2 1 3
Didymium sp. 0 0 0 0 0 0 3 0 0 3
Didymium squamolosum Alb. & Schwein 0 0 0 0 1 1 2 3 1 8
Ophiotheca chrysosperma Curr. 0 0 0 0 0 1 0 0 0 1
Perichaena cf. corticalis (Batsch) Rostaf. 0 0 0 0 0 1 1 0 1 3
Perichaena depressa Lib. 4 0 0 4 6 2 6 0 1 15
Physarum album (Bull.) Chevall. 1 0 0 1 0 0 2 1 0 3
Physarum cinereum (Batsch) Pers. 0 0 0 0 0 0 1 0 0 1
Stemonitis cf. pallida Wingate 0 1 0 1 0 0 0 1 0 1
No. of MC prepared 11 8 18 37 38 20 67 20 22 167
% MC productivity 82 11 28 45 45 35 48 60 32 43
No. of species 3 3 1 5 5 5 10 5 5 14
No. of genera 3 3 1 5 4 4 7 4 3 9
Taxonomic Diversity Index (TDI) 1 1 1 1 1.25 1.25 1.43 1.25 1.67 1.56
Table 1. Species occurrence, moist chamber productivity, and taxonomic diversity index (TDI) of myxomycetes in elevated urban residential gardens.
a Sampling localities: Low-rise Buildings - (S1) Sta. Cruz Apartment, (S2) Bennt Apartment Bldg. and (S3) 1588 Apartment Building.
b Sampling localities: High-rise Buildings - (S4) Celadon Park Tower 3, (S5) Celadon Park Tower 2, (S6) Sun Residences Condominium Tower 1, (S7) Paseo Verde At Real Tower 1, and (8) Paseo Verde At Real Tower 2.
Philippine Journal of Systematic Biology Online ISSN: 2508-0342 v.2.0.20 (Chao et al. 2014; Hsieh et al. 2016) in R v.4.1.2.
iNEXT is designed to plot a sample completeness curve depicting how sample coverage varies with their sample size.
The sample completeness curve provides a bridge between the size- and coverage-based Rarefaction/Extrapolation (R/E) sampling curves. We also use the Paleontological Statistics Software (PAST) v.4.11 (Hammer et al., 2001) to compute the percentage exhaustiveness by dividing the actual number of recorded species by the 95% upper confidence interval as estimated by the Chao 1 estimator, a nonparametric method for estimating target species richness. Then, the number of species and genera for each study site were recorded. The ratio of species and genera were utilized for the determination of the taxonomic diversity index (TDI).
Results
Moist chamber productivity
This study recorded an overall 45% moist chamber (MC) productivity from the 204 prepared moist chambers, of which 58 moist chambers yielded fruiting bodies while 33 moist chambers yielded only plasmodia. The plasmodia did not further develop into identifiable fruiting bodies, and hence, the species richness observed in this study is an underestimation of the true number of myxomycetes in the collecting localities.
Between the two building types, the high-rise residential buildings (n = 5, 45% MC productivity, number of positive MC = 75, total number of prepared MC = 167) yielded a slightly higher percent MC productivity than the low-rise residential building (n = 3, 43% MC productivity, number of positive MC = 16, total number of prepared MC=37) despite a greater difference in the collected samples and prepared moist chambers. Based on Chao1 estimator, the overall sampling effort was 76% exhaustive, indicating a possibility of obtaining more species of myxomycetes in the study areas with further sampling (Fig. 2). The rarefaction curve of the SAC also showed that better sampling effort is apparent on substrates collected from high-rise than low rise building types. Moreover, the richness of species in high-rise building was higher than the low-rise buildings.
Species occurrence and taxonomic diversity
Fourteen species and nine genera of myxomycetes were recorded in the study. These were identified as follows:
Arcyria cinerea, Collaria arcyrionema, Diachea leucopodia, Diderma effusum, Diderma hemisphaericum, Didymium nigripes, Didymium sp., Didymium squamulosum, Ophiotheca chrysosperma, Perichaena cf. corticalis, Perichaena depressa, Physarum album, Physarum cinereum, and Figure 2. (a) Percent yield of moist chambers positive for myxomycetes from the eight urban gardens (n = MC positive for myxomycetes/total number of prepared moist chambers). (b) Species accumulation curve between samples collected in low- (blue line) and high-rise (orange line) buildings and for pooled data (pink line).
a
b
Stemonitis cf. pallida (Fig. 3). These myxomycetes belonged to the taxonomic Order Trichiales with bright-colored spores (4 species) and to the taxonomic orders Physarales (7 species) and Stemonitales (3 species), both are described as having dark-colored spores with members of Physarales known for the presence of lime in the peridium, stalk and/or capillitium of their fruiting bodies. Between the two residential building types, a higher number of species was recorded in high-rise building gardens (number of species = 14, TDI = 1.56) than in low-rise building gardens (number of species = 5, TDI = 1), however, the latter was more taxonomically diverse than the former. Expectedly, the number of moist chambers (LRB = 37, HRB = 167) influenced the species richness and TDI (Table 1).
Discussion
Ground leaf litter is a favorable substrate for myxomycetes. For instance, a higher MC productivity was noted in ground leaf litter than twigs in Anda Island, Pangasinan (Kuhn et al. 2013) and in Caramoan Islands (Macabago et al.
2020). In other studies, the TDI reflected a higher taxonomic diversity for ground leaf litter, e.g., in Cheng et al. (2013) with Figure 3. Representative species of roof-top garden myxomycetes:
(a) Stemonitis cf. pallida, (b) Collaria arcyrionema, (c) Diachea leucopodia, (d) Diderma effusum, (e) Diderma hemisphaericum, (f) Didymium nigripes, (g) Didymium sp., (h) Didymium squamulosum, (i) Ophiotheca chrysosperma, (j) Perichaena cf. corticalis, (k) Physarum album, (l) Physarum cinereum, (m) Perichaena depressa, and (n) Arcyria cinerea.
(Table 1), which is two species more than that reported by Garcia et al. (2022). Their study sites were an apartment complex and a condominium, and they utilized spore baiting techniques in addition to moist chamber culture method to account for airborne myxomycetes. Although, spore baits used in two urban centers in Costa Rica by Rincon-Marin et al. (2021) recorded a higher number of species in contrast to the results of Garcia et al. (2022), we did not use this strategy to record the myxomycetes in elevated gardens. This was primarily because of the lack of approval from building administrators to set up baits which will require longer exposure period and attract attention of the building occupants who may see these hanging spore baits as “eyesores”. In this study, we opted to collect fallen ground leaf litter readily available in the garden area. We did not account for the duration of the stay of leaf litter on the ground prior to collection. This would be a good future research topic, that is, to investigate the effects of garden management on the occurrence and community composition of myxomycetes.
Arcyria cinerea and Perichaena depressa are among the most recorded species in urban ground leaf litter. The two species were also abundant in previous studies. Arcyria cinerea was reported as abundant in a wide array of substrata, including twigs and barks (Macabago et al. 2010; Cheng et al. 2013), grassland litter (Carascal et al. 2017), dead inflorescences of herbaceous plants (Pecundo et al. 2017; dela Cruz et al. 2021), and coconut inflorescences (Cabutaje et al.
2021). As expected, cosmopolitan species like A. cinerea were also recorded as abundant in lowland montane forests (Alfaro et al. 2015), karst forests (Pecundo et al. 2021), coastal and inland forests (Macabago et al. 2016; Cabutaje et al. 2021). So, the abundance of A. cinerea in our urban garden leaf litter was not surprising. Similarly, Perichaena depressa is abundant in dried grass litter (Carascal et al. 2017) while Cavalcanti et al. (2015) demonstrated the occurrence of P. depressa in urban areas. Perichaena depressa was also present in leaf litter collected from ornamental shrubs in a residential garden (Stephenson & Novozhilov, 2021).
Roof-top gardens are an integral part of many low- and high-rise buildings in urban areas due to their aesthetic design, perceived health benefits, and environmental concerns, e.g., reducing trapped heat or cooling effect. However, how these urban roof-top or elevated gardens influence the assemblages and community composition of myxomycetes remains understudied. In our study, we reported the presence of myxomycetes in elevated gardens in residential buildings within a highly urbanized metropolis. While the elevations of the gardens did not vary greatly (i.e., 20–30 m high) between the two building types (low-rise vs high-rise building), our
Philippine Journal of Systematic Biology Online ISSN: 2508-0342 study showed that myxomycete spores could reach high vertical elevations and colonize leaf litter substrates present in artificial, man-made gardens where plant debris could serve as substrates for myxomycete colonization.
Acknowledgements
The authors express their gratitude to the Property Management Administration Office of these condominiums (Celadon Park, SMDC Sun Residences, and Paseo Verde at Real) and owners of the sampled residential buildings in Manila and Marikina cities for the collection of leaf litter.
This study is supported by a scholarship and thesis grant provided to one of the authors by the Department of Science and Technology – Science Education Institute.
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