CSIRO PUBLISHING Australian Journal of Botany, 2019, 67, 617–629 https://doi.org/10.1071/BT19155

Australian corticolous myxomycetes: models of distribution and development

Peter Wellman

17 Warragamba Avenue, Duffy, ACT 2611, Australia. Email: [email protected]

Abstract. This paper presents an integrated model of the variation over a continental landmass of myxomycetes, a single-celled organism in the phylum Amoebozoa. Bark samples were collected on long traverses across Australia, and cultivated in Petri dishes by the moist chamber technique to obtain large assemblages of common species. The results of this survey and previous surveys are consistent with there being four major myxomycete assemblages: Tropical, Northern Arid, Southern Arid and Temperate. Where mapped, these species assemblage regions are consistent with the Australian phytogeographical regions. The myxomycetes differ between arid and non-arid areas; the arid areas have slightly higher productivity per wetting event, with members of the Physarales and Liceales relatively important and the Stemonitidales, Trichiales and Cribrariales less important. When the bark samples are placed in a moist culture there is a myxomycete growth cycle and then the population declines to resting phases. The population increase during a growth phase can be modelled by a linear plot of log(abundance) against species rank, where abundance is total harvested spore volume of a species. The population decline appears to be linear from two weeks after watering, declining to negligible activity 4 weeks after watering.

Additional keywords: biogeography, ecology, ecosystem dynamics.

Received 22 September 2019, accepted 17 December 2019, published online 10 February 2020

Introduction The result of all the previous worldwide work on Myxomycetes (plasmodial slime moulds) are phagotropic myxomycetes was summarised by Stephenson and Rojas eukaryotic single-celled organisms in the phylum (2017). Most of the work to date in natural habitats has been Amoebozoa. Their life cycle has two very different feeding in describing all species, finding which species are present in stages: a relatively small uninucleate phase; and a larger what substrates, and investigating which environmental multinucleate plasmodium. They feed when there is variables affect the presence of a species, with each paper moisture but otherwise survive in three types of dormant generally considering a single climatic area. Previous work on stages (microcysts, sclerotia and spores). Because of the Australian myxomycetes with this objective consists of Ing numerous types of dormant phases myxomycetes are and Spooner (1994), Mitchell (1995), McHugh et al.(2003), relatively successful in arid environments. Fruiting bodies Black et al.(2004), Jordan et al.(2006), Rosing et al.(2007), (containing the spores) are permanent structures, and are the Davison et al.(2008, 2017), Wrigley de Basanta et al.(2008), basis of the species identification. Myxomycetes are the McHugh et al.(2009), Stephenson and Shadwick (2009), only living organisms that have both a single celled phase Knight and Brims (2010), Lloyd (2014), and Wellman (2017). living as a true microorganism and can be identified from a In this paper and two previous papers (see Wellman 2015, permanent structure. They are easily cultivated in the 2016) myxomycetes have been studied in a different way. laboratory, so they are relatively easy to study. Taken together, the sampling covers the whole continent, and Myxomycetes are normally identified from their fruiting the studies concentrate on the local population of common bodies. The fruiting bodies can be obtained either from species rather than the rare species. To achieve these collecting fruiting bodies in the field after rain (which is objectives the procedure and emphasis differed somewhat difficult in central Australia), or from cultivating suitable from normal; rather than collection of spot samples in a substrates in the laboratory using the moist chamber culture compact area, samples were collected systematically in very technique (Stephenson and Stempen 1994; Novozhilov et al. long traverses (to 2000 km long) sampling all the Australian 2017; Wrigley de Basanta and Estrada-Torres 2017). Previous regions. The growth procedure was not optimised to find the overseas work had shown that dead bark off a live tree was maximum number of species but to study competing, large the most productive material for moist chamber culture multi-species populations. As a result of this different (e.g. Schnittler 2001), so this substrate was used in this study. approach, topics can studied that were not previously

Journal compilation CSIRO 2019 Open Access CC BY-NC-ND www.publish.csiro.au/journals/ajb 618 Australian Journal of Botany P. Wellman explored, such as modelling of the myxomycete growth sample the main rainfall variation, importantly crossing the and decay after wetting, the variation of productivity lowest annual rainfall area of Australia. A small study was and order dominance over a continent, and the evidence for made of the bark in trees in wet temperate rainforest in the myxomycete-geographical regions. The ecological conclusions north-east highlands of New South Wales. of this paper are consistent with previous international work, but In a previous paper (Wellman 2016), I showed that in the paper shows how these conclusions can be integrated on a Australia, myxomycete species assemblages along long continental scale. profiles appeared to be constant over long distances, and then The moist chamber technique simulates a rainfall event. there is a wide transition zone to another constant species However, the results from moist chamber cultivation are assemblage. I recognised four species assemblages: a tropical, unlikely to be replicated during actual normal rainfall northern dry, southern dry, and temperate. As the word ‘dry’ is events in the countryside because it is unusual in Australia inaccurate, this paper uses the names Tropical (Tr), Northern for bark to be damp continuously for 4 weeks. The moist Arid (NAr), Southern Arid (SAr), and Temperate (Te), for these chamber experiments are important because the results species assemblages. To prove this model for all Australia we determine the myxomycete productivity of the bark samples need to determine that: (1) species assembles are reasonably under standard conditions, and can be used to model constant within profiles; (2) transition zones are where they population dynamics. would be expected geographically; and (3) the four species The intention of this paper, and the earlier traverses assemblages are reasonably constant east–west across incorporated in this paper, is to sample the corticolous Australia. Also of interest is whether the myxomycete species myxomycetes over the main Australian landmass. Because the assemblage boundaries correlate with the phytogeographical main reason for changes in species is likely to be the change in the regions defined by the maxima in plant species turnover. The wetting events, the sampling was designed to determine the collected myxomycete traverses are positioned to have two change in species assemblages with changes in rainfall. The crossings of each of the three main phytogeographical region mean annual rainfall (Fig. 1) has a low of 200 mm/year in the boundaries (Fig. 2). central south of Australia, and a gradual then abrupt increase towards the coastline. The coastal areas with high rainfall occur along the northern margin of Australia, the east coast and in the Materials and methods south-west corner. Both the previous and new sampling was The method used in the previous long traverses (Wellman 2015, carried out predominantly on long traverses on tar-sealed roads, 2016), and the survey reported here, are similar and are described in the direction of the rainfall gradient (Fig. 1). There is a long below. The bark sampling was generally conducted during the north–south traverse across Western Australia with a gap in the winter, as the winter temperature is pleasant and, for most of middle, a traverse across the centre of Australia, and several Australia, rain in winter is unlikely. Most samples were short traverses in eastern Australia. Together the traverses collected at least a month after the last rainfall. In Western

Darwin

Darwin Northern Australian PR 1500 1500 Tropical SA (Tr)

B Cairns 1000 1000 C Cairns Northern Desert PR 600 Northern E Port Hedland Northern Arid SA (NAr) Territory Port Hedland 400 Alice Alice Springs Springs A 300 Eremaean PR Western Queensland D Southern Arid SA (SAr) 300 Australia South 300 Australia 400 400 A 200 G F I Perth Southwest Australia PR Perth New South Adelaide Wales Temperate SA Sydney 1000 Adelaide H (Te) Euronotian PR 600 Victoria Sydney Temperate SA Melbourne (Te)

1000 2000 Tasmania Fig. 2. Relationship of the myxomycete traverses (thick lines) to the Fig. 1. Distribution of corticolous myxomycete traverses A–I. Traverses A, phytogeographical regions of González-Orozco et al.(2014) (zig-zag D, G, H and I are newly reported in this paper. Traverse F was reported by dotted lines) and of Ebach et al.(2015) (thin continuous lines). The area Wellman (2015), traverses C and E by Wellman (2016) and B is site 10–12 of names referto themyxomycete speciesassociations (SA),and theEbachet al. Davison et al.(2017). Contours give the distribution of the annual average (2015) phytogeographical regions (PR). The extent of each myxomycete rainfall in mm/year (BOM 2017). transition zone is shown by a thin straight line. Australian corticolous myxomycetes Australian Journal of Botany 619

Australia there was unseasonal rain a week before sampling Comatricha ellae, and the similarity of the smaller fruiting both when the whole traverse was sampled in July and also bodies of these species to Paradiacheopsis fruiting bodies when the southern end was re-sampled in November. made separation of Paradiacheopsis fruiting bodies, and their The moist culture technique was used in this study. Most identification and counting, uncertain. people using the moist culture are mainly trying to obtain the range of species found at a site. Many of these studies used Results only one piece of material, or several related pieces, for each Supplementary Material File S1 lists the sample localities, and Petri dish. This study tried to obtain, for a large number of File S2 the species collected and for each record the locality samples, the range of common species and their relative and number of fruiting bodies. The surveys resulted in productivity. Because of this difference in survey objective, spreadsheets listing, for each species-record, the sample the field sampling and moist culture in this survey were number, species, and number of fruiting bodies (except for conducted slightly differently from most previous studies. Echinostelium). The average size of the fruiting body for each (1) At each ‘site’ dead-bark pieces were collected from 1–4 species was estimated, mainly using Poulain et al.(2011). trees of the same species, from a range of 1–2.4 m above the Using these sizes the spreadsheet was used to calculate the ground, from random positions around the tree(s), and from the total volume of spores for each species record, and the total available range of the bark textures. (2) Five Petri dishes were volume of spores for each sample. The errors of the spore cultivated from each site. Each Petri dish contained if possible volumes are substantial, but the paper is mainly using the a full range of the types of bark. If long strips of bark were logarithms of the volumes. Spore volumes have previously collected, then each strip was cut into pieces and one piece put been used as mentioned in Novozhilov et al.(2017). in each dish. (3) The bark samples in the Petri dishes were kept moist, and at weekly intervals the Petri dishes were inspected and the mature fruiting bodies harvested. Generally there were Species assemblages no further fruiting bodies after 4 weeks and the sample was The results of the new surveys along long profiles are dried out after ~6 weeks. Samples 860–1087 (of Wellman presented in the form of tables of occurrences (see 2015, 2016) were subject to another cycle of soaking and Tables S1–S4, available as Supplementary Material to this cultivation, but few additional fruiting bodies were obtained. paper). To save space in the tables, a sample is not shown if it The fruiting bodies from the five Petri dish were not kept contains only one common species, and a species is not shown separate. The few fruiting bodies on the base of the bark pieces if it has only one occurrence. Where the survey abuts a were only collected when the bark pieces had dried. The previously published survey, then the species distribution of estimates from the number of fruiting bodies for each the adjacent part of the previous survey is summarised in one species is based on counting or estimating the number of column. harvested fruiting bodies, a number supplemented, when Table S1 shows a 500 km long north-west-trending traverse much of the bark was covered by fruiting bodies, by an in north-east New South Wales between Yarrowitch and estimate of the number of fruiting bodies never harvested. Goodooga (Fig. 1, traverse G), collected July 2017, with This procedure aimed at getting a large diverse species samples numbers 1129–1172. The species are divided into assemblage, and getting a large number of fruiting bodies three groups: 14 species that occur along the whole survey line, so that their relative productivity can be better determined. 10 SAr species, and six Te species. The transition zone is The pH of the bark was measured for 56 samples in Western ~250 km wide with a midpoint ~29.6S, 149.2E, located near Australia, 55 in Northern Territory and Queensland, and 11 near Narribri. Canberra. The measurements were made to an accuracy of Table S2 shows a 450 km long north-west-trending ~0.1 pH unit, by measuring deep fluid in a narrow plastic cup traverse in south-east New South Wales between Canberra with an inexpensive pH instrument that was calibrated using and Lake Cargelligo (Fig. 1, traverse H), with sample numbers standard solutions. 1101–1111 collected October 2016, and 1254–1291 mainly The myxomycete fruiting bodies were identified using a collected June–July 2017. The species are divided into three wide range of sources, but mainly Ing (1999), Poulain et al. groups: twelve species that occur along the whole survey line, (2011) and Discover Life (2018). In order that the bulk of the five SAr species, and eight Te species. The transition zone is Australian myxomycete identifications were consistent, the ~200 km wide with a midpoint ~33.6S, 146.1E near West more difficult to identify species of the previous Wyalong, but it is poorly defined at its north-west margin. publications (Wellman 2015, 2016)werere-identified. Table S3 shows an 1100 km long south trending traverse in Identifications in some species groups were difficult. In Northern Territory and South Australia between Alice Springs Physarum/Badhamia this was because the capillitium and Woomera (Fig. 1, traverse D), with sample numbers structure was generally not clear and spore diameters of 1201–1251 collected June 2017. The species are divided into possible species were similar. Echinostelium minutum and three groups. Most of the species (13) occur throughout the Echinostelium arboreum could be identified, but reliable traverse and occur elsewhere in both the SAr and NAr identification of the other species of Echinostelium could assemblages. Three species should occur both in the NAr not be obtained because the material used for identification and SAr, but they only extend south to sample 1208. Three was dried (Whitney 1980). The separation and identification of species characteristic of the SAr occur on the southern end of most Paradiacheopsis species was not attempted because the traverse and only extend north to sample 1220, not as far many samples were dominated by Comatricha elegans or north as the likely transition zone. In this traverse the SAr/NAr 620 Australian Journal of Botany P. Wellman transition zone is very poorly defined in the north, but it is New South Wales (Wellman 2016) and the wetter part of likely to be over samples 1201–1208, just south of Alice temperate Victoria (Rosing et al. 2007). Column 16 (Te3) Springs, with a midpoint at 24.3S, 133.8E. reports a few samples from cool-temperate closed rainforest in Table S4 shows a 1300 km long, south-trending traverse in New South Wales, mainly Nothofagus bark (traverse I of Western Australia from near Port Hedland in the north to Perth Fig. 1). Columns 18–20 summarise the data for columns in the south (Fig. 1, traverse A). Sample numbers 1312–1420 1–16, giving the sum of the species records in each of the were collected July 2018, and 1450–1502 were collected four species assemblages expressed as parts per thousand. In November 2018. There is a 340 km gap in this traverse these four columns significant species occurrences are in bold. between24.5and27.6S. The data in this table are not These are generally species with abundances >10‰. shown in full because there are 89 samples along the For much of this table the interpretation is relatively simple. profile. The table has been drastically shortened by For instance, Licea kleistobolus is relatively common in all summarising the occurrences for the two transition zones. four species assemblages, and Cribraria confusa is present The expected extent of the species that should terminate at only in the tropical and temperate species assemblages. The a transition zone are shown by the underlining. The difficulty is in determining the significance of relative interpretation is the NAr/SAr transition zone is 16 samples abundance differences (such as Licea biforis in columns wide, between samples 1362 and 1340, or further south, giving 17–20), and in estimating the abundance (occurrence rate) a transition zone of 250+ km wide with a midpoint ~23.3S, of outliers for this organism spread by spores. 119.7E, near Newman. The SAr/Te transition zone is Species characteristic of all four species assemblages (Tr, interpreted to be 32 samples wide, between samples 1425 NAr, SAr, Te) are Arcyria cinerea, A. sp. H (Arcyria sp. of and 1454 or further north; that is 260 km wide and with a Davison et al. 2008), Calomyxa metallica, Comatricha elegans, midpoint at 30.2S, 116.7E near Mount Magnet town-ship. C. ellae, Licea biforis, and L. kleistobolus. Species characteristic The results from this traverse are puzzling, as the sample spore of the wetter species assemblages (Tr, Te) are Clasterderma volumes are high, but key species of NAr and Te do not debaryanum, Cribraria confusa, Cribraria minutissima, appear as frequently as expected. This may be due to the rain Cribraria violacea, and Echinostelium minutum. Species before the sampling. characteristic of the arid species assemblages (NAr, SAr) are Badhamiopsis ainoae, Didymium dubium, Mcbrideola oblonga, and Physarum decipiens. The Tr assemblage differs from the Te Discussion assemblage in having, or having in greater numbers, The analysis in this discussion section interprets the results Hemitrichia minor, Perichaena chrysosperma, Stemonitis of both the new and the previously published corticolous mussooriensis, Trichia erecta,andTrichia munda. The Te myxomycete work – the datasets shown in Fig. 1 and assemblage differs from the Tr assemblage in having, or additional spot sample data. A total of 300 long traverse having in greater numbers, Arcyria pomiformis,andTrichia samples were used. contorta. The NAr assemblage differs from the SAr Table 1 shows the occurrence of myxomycete species in assemblage in having, or having in greater numbers each of the four species assemblage areas using this new data, Macbrideola decapilata and Perchaena corticalis. The SAr and the previously published data. Not all species can be assemblage differs from the NAr assemblage in having, or shown because the table would be too large, so the contents having in greater numbers Dianema corticatum, Didymium of the table concentrate on the significant species found in the dubium, Enerthenema papillatum,andPhysarum long profile studies, and leaves out many species found in low crateriforme. There is a major change in the species numbers in the wetter areas. Columns 2–11, 13 and 14 show assemblage between the non-arid (Tr, Te) and arid (NAr, the data from the long traverses of Wellman (2015, 2016)and SAr) species assemblages, and only a minor change of this paper. The myxomycete records within the transition between the non-arid assemblages (Tr, Te), and between the zones are recorded as follows: if the species is present in both arid assemblages (NAr, SAr). species associations then a record in the transition zone is put Table 1 shows the consistency of the occurrence of a in the closest species association, if the record is found in only species within a species association over a continental area. one of the species associations then all the records within the Table 1 and the profilesofTablesS1–S4 demonstrate that transition zone are allocated to that species association. The species can occur outside their normal range as outliers. The other columns sample the wetter parts of the Tropical and distinction between normal range and outliers is important in Temperate Species Assemblages. Column 1 (Tr2) is a interpreting World maps of myxomycete record sites, such as composite sample of the wetter Tropical areas in the in Discover Life (2018). Kimberly, Darwin and Cairns areas: sites CB, CO, CT, EB, FI, MJ, WF of McHugh et al.(2003), sites 1–11, 13 of McHugh et al.(2009), and sites 10–12 of Davison et al. Tree bark acidity (pH) and characteristics (2017). Column 12 is a composite sample of the temperate Table 2 shows for each myxomycete species the range of areas of SW of Western Australia combining the records of the observed pH and the host trees, while Table 3 gives for the traverse (Table S4), of Jordan et al.(2006) from Banksia bark common tree genera the range of pH, and the type of bark. Each for two sites, and spot samples of sites 19, 23–25 and 28 of myxomycete species grows on a range of bark pH, and a range of McHugh et al.(2009). Column 15 (Te2) comprises spot bark texture. Examples of the preference differences between samples from the wetter part of temperate south-eastern related myxomycete species are as follows. Arcyria cinerea Australian corticolous myxomycetes Australian Journal of Botany 621

Table 1. Occurrence of species in the four Species Associations For the origin of columns 1–16 see the text. The numbers are the number of occurrence records. Columns 17–20 show for each species association the sum of the records, normalised to show records per thousand of the records in the table. Figures in bold indicate significant species for that species association. NAr, Northern Arid; SAr, Southern Arid; Te, Temperate; Tr, Tropical

1 234 5 678 9 1011121314151617181920 Species assemblage Tr2 Tr Tr NAr NAr NAr SAr SAr SAr SAr SAr Te Te Te Te2 Te3 Tr NAr SAr Te v wet NT Qld WA NT+SA Qld WA SA NW NSW Can Nar WA Can Nar spot v wet ‰‰‰‰ Traverse of Fig. 1 CEA C E AD F HGAHG I

Arcyria cinerea 21 6 6 6 7 4 5 2 7 2 7 5 8 5 13 99 57 32 61 Arcyria sp. H 21 2 21 4 1 1421 6 101116 Arcyria pomiformis 112 63 8 112 0033 Badhamia affinis 31 221 00610 Badhamia macrocarpa 1741 103172 Badhamia versicolor 3522 010 10 4 Badhamiopsis ainoae 2 7 3 3 10 8 1 4 2 6 44 32 4 Calomyxa metallica 6 3 8 474 112314418 18 50 37 53 Clasterderma debaryanum 82 12 13112330 10 1 14 Clasterderma pachypus 11 1 2 2 3 2 2 3 6107 8 Comatricha elegans 8 9 11 3 7 6 7 12 1 2 3 6 5 2 7 1 84 54 34 39 Comatricha ellae 1 6 4 13 3 13 16 16 7 14 4 9 1 21 67 72 53 Comatricha laxa 1 12 221 5 1 7324 12 7 12 31 Comatricha pulchella 2 1 13 1 16362 Cribraria confusa 14 10 5 3 2 13 10 87 0035 Cribraria minutissima 21213 1 8358 1 81 0147 Cribraria violacea 11 6 5 1 1 4 8 5 1 66 0135 Dianema corticatum 12 0 0 17 0 Didymium dubium 144111913113 4 030 79 8 Echinostelium sp. 7 6 7 7 5 25 24 3 3 9 12 11 7 39 64 88 59 Echinostelium arboreum 313 7 023 10 0 Echinostelium minutum 10 5 6 2 1 1 3 1 25 1 63 7159 Enerthenema papillatum 2 4 1 8 3 5 2 3 11 7 4 17 3 18 3 29 77 Hemitrichia minor 33 1 18 000 Licea biforis 6846910928418 60 41 24 Licea kleistobolus 3 1 10 10 6 9 23 17 12 1 9 23 9 6 5 42 84 85 84 Licea operculata 10 3 1 16 5 2 1 4 1 1 30 13 39 4 Licea pygmaea 1434442323 17 4 Licea scyphoides 331101 913 15 0 Macbrideola decapilata 2 3 4 1 12 1 6 23 1 24 Macbrideola martinii 11 1 3 4 33 0114 Macbrideola oblonga 6 7 3 6 11 16 4 10 2 4 0 54 65 12 Macbrideola scintillans 91 2 30 004 Paradiacheopsis fimbriata 211452 1113319 013 18 51 Perichaena chrysosperma 16 11 48 004 Perichaena corticalis 1274 3 44 00 Perichaena vermicularis 656426 322549 057 23 39 Physarum cratoriforme 3133875721191341 6 Physarum decipiens 1 9 7 7 11 16 20 4 13 1 3 77 88 2 Physarum leucophaeum 7 6 4 7 4 10 3 10 6 2 2 21 57 37 20 Physarum viride 2 4 0708 Stemonitis fusca 2 1 3 2 2 2 2 2 6 0 11 12 Stemonitis laxifolia 2 0700 Stemonitis mussooriensis 24 1 1 18 012 Trichia sp. 15 1 7 2 9 6 4 45 01437 Number of records 176 68 88 104 105 89 187 183 190 39 127 148 96 74 191 29 1000 1000 1000 1000 grows over the enormous pH range of 3.7–7.4, but is mainly with a range of bark textures and for each texture sample the restricted to soft and fibrous barks, while Arcyria sp. H and whole range of bark pH. Over much of Australia the existing A. pomiformis are both restricted to relatively acid bark but A. sp. native trees have a full range of pH, but what is missing is H likes soft bark and A. pomiformis likes hard bark. generally a full range of bark textures. This is in part because the Echinostelium arboreum differs from E. minutum in all trees and tall shrubs use bark hardness and texture to limit tree measured factors - species association, preferred pH, and bark damage during the wildfires, such fires being more frequent in the texture. The occurrence of myxomycete species on a tree bark is arid areas. Most of the tree genera collected had a relatively clearly determined by three factors: species association narrow range of bark pH and bark type. The exception is (climate), bark acidity and bark substrate properties such as Eucalyptus, which has been divided into four bark types hardness and texture. To sample all the potential species that (Table 3). The myxomycete species observed range of would inhabit a species-assemblage area one has to sample trees substrate pH found in this survey can be compared with those 622 Australian Journal of Botany P. Wellman

Table 2. The substrate of myxomycete species Columns give the number of pH samples (N1) and the observed range of pH of the substrate bark, the total number of species records (N2), and the most common tree species substrates. Tree genera are Ac, Acacia; Ata, Atalaya; Bra, Brachychiton; Bur, Bursaria; Cal, Callitris; Cas, Casuarina; Cor, Corymbia; Eb, Eucalyptus ‘coolabah’ type; Ere, Eremophila; Ery, Erythrophleum; Ef, Eucalyptus fibrous bark; Ei, Eucalyptus ‘iron bark’ type; Em, Eucalyptus with fissured bark; Gei, Geijera; Gre, Grevillia; Hak, Hakea; Lys, Lysiphyllum; Myo, Myoporum; Owe, Owenia; San, Santalum; Sch, Schinus

Species N1 pH range N2 Tree genera and number of trees Arcyria cinerea 44 3.7–7.4 70 Eb 27, Cor7, Ef6, Ei3, Cal2, Bra2 Arcyria sp. H 10 3.9–5.2 20 Eb3, Cor3 Arcyria pomiformis 7 3.7–4.6 9 Ery2, Hak2, Ca2 Badhamia capsilifera 4 5.8–6.2 4 Badhamia macrocarpa 12 3.7–6.3 11 Ac3, Bur2, Cas2 Badhamia versicolor 6 6.1–6.8 11 Ac3,Ere2 Badhamiopsis ainoae 12 4.9–6.3 36 Ac20, Cal4, Cas4, Ata2 Calomyxa metallica 17 4.4–6.8 51 Ac18, Eb7, Cal6, Cas3, Bra2, Ei2, Ow2, San2 Clasterderma debaryanum 4 3.9–6.2 9 Eb5 Clasterderma pachypus 4 4.1–6.6 11 Ac3, Gre3 Comatricha elegans 51 3.1–6.7 76 Cor18, Eb11, Gre7, Ef7, Ac5, Cal3, Hak3 Comatricha ellae 46 4.3–6.7 109 Ac24, Eb20, Gre10, Hak10, Cal6, Cor6, Cas5 Comatricha laxa 7 4.2–6.7 22 Eb3, Hak3, Ac2, Ei2, Gre2 Comatricha pulchella 26–6.5 6 Eb3 Comatricha vineatilis 3 3.9–4.5 4 Cor4 Cribraria bicolor 1 6.9 3 Eb2 Cribraria confusa 21 3.7–5.2 20 Ef6, Cor4, Ery4 Cribraria minutissima 20 3.7–6.0 35 Cor8, Ef7, Eb2, Gre2 Cribraria violacea 17 4.0–7.4 23 Eb13 Dianema corticatum 12 Eb7, Ac3 Didymium dubium 10 4.6–6.4 64 Ac24, Eb15, San4, Cas3, Gre3, Bra2, Cal2, Gei2 Echinostelium arboreum 5 6.6–6.8 15 Eb7 Echinostelium minutum 14 3.8–6.1 16 Aca3, Cor2 Enerthenema papillatum 19 3.7–6.2 50 Eb10, Cor7, Ef5, Gre4, Hak4, Aca2, Bra2, Cal2, Ei2 Hemitrichia minor 3 4.1–5.8 3 Ac2 Licea biforis 24 4.2–7.0 54 Ac21, Cas6, Eb5, Ef3, Gre3, Lys3, San2 Licea kleistobolus 54 3.7–7.1 117 Ac34, Eb7, Ef5, Hak5, Cal5, Lys3, Cas3, Cor3 Licea operculata 30 4.1–6.6 45 Ac20, Gre4, Cas3, Ery3, Hak3 Licea pygmaea 7 4.5–7.1 20 Ac5, Eb5, Cas2 Licea scyphoides 4 4.0–6.9 22 Ac14, San2 Macbrideola decapilata 8 6.0–7.1 8 Eb4, Lys2 Macbrideola martinii 10 Eb4, Ei2 Macbrideola oblonga 14 4.8–6.9 65 Ac19, Eb11, Cal7, Cas3, San3 Paradiacheopsis fimbriata 17 3.6–5.5 32 Cor6, Gre5, Hak5, Ei3, Ac22, Cal2, San2 Perichaena chrysosperma 4 5.2–6.3 3 Perichaena corticalis 10 5.2–7.4 11 Eb6 Perichaena vermicularis 17 5.2–6.8 53 Eb24, Bra2, Ac2, Gei2 Physarum cratoriforme 2 6.2–7.1 36 Eb10, Ac6, Cal5, San4 Physarum decipiens 25 4.4–6.9 90 Ac33, Eb17, Cas6, Cal3, Gre3, Myo3 Physarum leucophaeum 20 5.0–6.9 54 Ac16, Eb11, Cal2, Gei2, Lys2, Sch2 Physarum viride 24–0–4.4 2 Ac2 Stemonitis fusca 2 6.0–6.3 14 Eb6, Cas4 Stemonitis laxifolia 2 6.8–6.9 2 Stemonitis mussooriensis 4 4.5–6.3 7 Ery2 found in overseas surveys witha differentclimate, differentmean records per sample decreases from 6.1 to 3.9, the mean substrate range and different bark textures (Schnittler 2001; volume of spores per sample decreases from 5.5 to 3.0 mm3, Novozhilov et al. 2006). The species in common between the and there is an associated decrease in the ratio of Physarales three surveys have a similar tolerance of pH when allowance is records to total records from 28 to 2%. The trends shown in made for the range of substrate pH available in a sampling area. Table 4 are true when using only the Western Australian samples, Table 4 shows that the bark acidity (pH) correlates with and when only using only the rest of the samples. changes in the productivity and species composition for each There appears to be a regional change in the average pH of sample. As the average productivity of the bark samples tree bark within Australia (Table 5). Using the traverse data, decreases from neutral (column with the range 6.0–7.3) to the median pH is 5.1–5.8 over most of Australia (arid or acidic (the range 3.1–3.9), the mean number of species temperate), while the median is lower for the tropical region, Australian corticolous myxomycetes Australian Journal of Botany 623

Table 3. Tree bark properties Table 5. The relationship between species association and bark pH For Eucalyptus, Eb is coolabah type bark, Ef is fibrous bark, Ei is ironbark, N is number of samples. The samples are from the four species assemblages and Em is mallee bark. N is number of samples (NAr, Northern Arid; SAr, Southern Arid; Te, Temperate; Tr, Tropical), the three transition zones, and for Tr3 from sites 10 and 12 of Davison et al. Tree genus Symbol N pH range Hardness Micro-texture (2017) Acacia Ac 23 5.1–6.4 Hard Massive Species assemblage N pH quartile boundary Callitris Cal 3 4.5–5.5 Hard Massive 25% 50% 75% Casuarina Cas 6 4.6–6.2 Hard Massive Corymbia Cor 14 3.7–4.6 (6.3) Soft Layered Tr3 23 4.1 4.6 6.0 Eremophila Ere 3 5.7–6.4 Soft Strips Tr 13 3.8 3.9 4.5 Erythrophleum Ery 2 4.2–4.5 Medium Strips Tr/NAr 20 4.2 5.8 6.2 Eucalyptus b Eb 13 (5.2) 6.0–7.2 Soft Woven NAr 25 4.6 5.2 6.1 Eucalyptus f Ef 7 3.7–4.4 Soft Fibrous NAr/SAr 11 4.5 5.7 6.7 Eucalyptus i Ei 2 4.2–4.9 Hard Resin bodies SAr 8 4.8 5.3 6.2 Eucalyptus m Em 10 4.3–6.0 Hard Strips SAr/Te 28 4.3 5.1 5.5 Grevillia Gre 5 3.9–5.5 Hard Holes Te 20 4.5 5.2 6.4 Hakea Hak 6 3.7–5.2 Medium Layered Lysiphyllum Lys 4 5.5–7.1 Hard Strips 8 (a)

3 Table 4. Influence of bark pH on sample productivity 4 The relation between bark pH and the number of records per sample, the mean mm total volume of spores produced, and the percentage of Physarales records in Average total spore volume per sample 0 the sample Tr3 Tr NAr SAr Te Te4 7 (b) pH range 3.1–3.9 4.0–4.9 5.0–5.9 6.0–7.3 Number of samples 15 40 34 36 Records/sample 3.9 5.2 5.6 6.1 5 Mean volume (mm3) 3 3.9 4.8 5.5 Physarales records (%) 2 8 29 28 Average number of species per sample 3 Tr3 Tr NAr SAr Te Te4 (c) 100 3.9 for the savanna forest (Tr sample), and 4.6 for two sites in Trichiales the wetter area (Tr3; sites 10 and 12 of Davison et al. 2017). Hence the influence of pH is at two scales, at a tree scale the Stemonitidales % Liceales myxomycete assemblage will vary with the pH of the individual tree bark, and at a regional scale the slight Cribrariales changes in the mean pH of tree bark may results in a slight Physarales Volume of spores regional change in myxomycete assemblage. 0 Tr NAr SAr Te (d) 100 Clastodermatales Changes in species assemblages across Australia Trichiales The information from the long traverses in Table 1 are consistent Echinosteliales with there being four species assemblages. In the area of each % Stemonitidales species assemblage the assemblage is largely independent of mean annual rainfall changes inland from the coast, and Cribrariales Liceales independent of east–west changes across Australia such as Physarales Number of records timing of rainfall (winter or summer). The non-arid/arid 0 Tr3 Tr Tr/NAr NAr NAr/SAr SAr SAr/Te Te Te4 boundary in the north is at ~650 mm mean annual rainfall, Species assemblage falling mainly during the summer. It is ~250 mm in the south- west with mainly winter rain, and ~500 mm in the south-east Fig. 3. Regional change in the mean myxomycete harvest. Errors shown with equal amounts of summer and winter rain. Hence, on a are standard deviations of the mean. continental scale, there is no point in plotting the various parameters against rainfall. To a first approximation samples, and Te4 is composed of the data of Rosing et al. the variation of myxomycetes within Australia can be (2007), Wellman (2016),andcolumn16ofTable1. However, summarisedbyplottingparameters against species assemblages. Tr3 and Te4 are not ideal samples because they have low sample The traverse data is used to compile samples of Tr, NAr, SAr, Te numbers, possibly biased sampling, and importantly are from and the transitions, the environments being mainly open forest, relatively wet open forest, rather than very wet closed rainforest woodland with grass or scrub understory, and scrubland with (which is thought to be the extreme environment). isolated trees. Tr3 and Te2 document the wetter areas; Tr3 is Fig. 3 show the change, over Australia, in the character of the composed of sites 10 and 12 of Davison et al.(2017)of24 mean corticolous myxomycete harvest. The variation in 624 Australian Journal of Botany P. Wellman productivity, shown by the total spore volume per sample (Fig. 3a) and by the number of species found at a site (Fig. 3b), is for a slight rise from Tr and Te to a high at the 30 NAr/SAr transition zone. For both parameters the values are thought to be much lower in areas of wet tall open forest, and 20 closed rainforest, but there is only poor data to support this in the Tr2 and Te2 values. The relative importance of the myxomycete orders 10 changes over Australia (expressed as a percentage of the Number of samples assemblage) can be based either on the total volume of spores 0 (Fig. 3c) or the number of records (Fig. 3d). With both methods −1.0 0.0 1.0 1.6 the Echinosteliales and Clastodermatales have about the 3 Log10 volume of spores (mm ) same importance in arid and non-arid areas, the Physarales 3 0.1 mm3 1 mm 10 mm3 and Liceales are more important in the arid areas, and the Trichiales, Cribraiales, and to a lesser extent the Fig. 4. Histogram of the myxomycete harvest of 170 samples. Stemonitidales, are more important in the non-arid areas. When measuring importance by the number of records, the orders have similar importance except for a constant low acid bark, and (notably) single trees that were not local, number of the Clastodermatales. When measuring being exotic or from another part of Australia. The low importance by the volume of spores, the Physarales volumes are thought to be due to bark with little food, or dominates the pattern of change. It is ~55% of the volume suitable myxomycete species not being available for one tree. in the arid area, and ~20% in the non-arid areas. The In Fig. 4 the volumes vary by 2.5 orders of magnitude. A mean Trichiales, Stemonitidales and Cribraiales together form of the raw values would be dominated by the larger values. In 40% of the volume in the arid areas and 60–80% of the this paper, each mean volume from many samples has been volume in the non-arid areas. The change from non-arid to calculated using the logarithm of the values so the long tail of arid characteristics is more gradual (in terms of region low values results in a mean that is much influenced by low subdivisions and distance) in the north than in the south. In values, hence the mean is significantly lower than the mode or the north the change is between Tr through Tr/NAr to NAr, median. whereas in the south the change is between SAr/Te to Te. Previous corticolous work, based on both the differences between local studies, and on larger regional studies Modelling the pattern of fruiting during a growing event (Novozhilov et al. 2017; Schnittler et al. 2017) have shown The moist chamber technique simulates a rainfall event, so the many of the correlations discussed above: decrease in abundance results of the growing experiments can be used to model and richness in very high rainfall areas, increasing species population dynamics. In the plant and animal kingdoms it is diversity with increasing pH values towards neutral, and the common to use abundance-rank plots to determine the higher proportion of Physarales in arid areas. This paper abundance relationship of species in a large population supplements these earlier papers as it shows how these (May 1976). Normally in these plots log(abundance) is variables change over a whole continent, and the difference shown on one axis, and the other axis is rank, plotted between expressing these changes as number of species, and linearly, with the highest rank with a value of 1. The expressing them using volume of spores. ecological importance of a species is dependent on the amount the species eats. With myxomycetes we can allow for the varying size of the fruiting body and the large range in Histogram of total spore volume the number of bodies by using total harvested fruiting body Fig. 4 is a histogram of the total spore volume using 170 volume of each species as a measure of species abundance. A samples. It illustrates the various influences on sample total site never has a large number of species, so the abundance-rank spore volume. To decrease the effects of regional variation in plot of a single site is very irregular and not useful by itself. mean volume, the data used to construct the histogram were However we have a large number of sites with the same from a single area (Western Australia), and it excluded data number of species, and rather than base an interpretation on from Tr and Te that Fig. 3a showed had lower mean volumes. a single site, we can base the interpretation on the mean path of The histogram plots volume on a logarithmic scale. The the log(abundance)-rank plots of all sites with the same (or histogram has a reasonably symmetrical high, with a mean similar) number of species. Fig. 5 shows a log(abundance)- of 4 mm3, a mode at 6 mm3, and one-half the amplitude at 2 rank plot both for sites with 11 or 12 species, and sites with six and 16 mm3. There is only a small tail on the high side, and a species. The plots have been simplified in that a few sites with very long tail on the low side. In this histogram the higher very different relationships have been omitted for simplicity, volumes (>20 mm3) are likely to be samples where one species and species points are not shown on the plot if their total has carried considerable mass from a previous feeding event volume is <0.001 mm3, because these fruiting bodies are small on the tree to the feeding event in the Petri dish. Lower and easy to overlook, so their abundance is likely to be greatly volumes (<1mm3) (12% of the samples) in part comprise underestimated, and so incorrect. In this paper samples were trees with corky or insufficiently-weathered bark, possibly plotted with a different number of species, hence the rank scale Australian corticolous myxomycetes Australian Journal of Botany 625 has been inverted, and species with the lowest rank have a the errors in the data fit will increase dramatically in samples value of 1. with few species. The log(abundance)-rank plots for samples with 11 or 12 Individual fruiting body of different species in this study species give tracks that are within a wide linear band for most of generally vary in radius from 0.03 mm for Echinostelium to ~1 their extent. The average relationship for samples with 11–12 mm, so their volumes range from 1.10À5 to ~0.5 mm2,andthe species is given by the thick linear dotted line. This line gives for number of fruiting body vary from 1 to 10 000, the higher the highest rank species a predicted mean total volume of ~7 numbers of fruiting body for species with the smallest fruiting mm3, and for the lowest rank species a predicted mean total body. The fruiting body volumes have a greater range than the volume of ~0.02 mm3. A similar pattern describes the log number of fruiting body, so species with a larger fruiting body (abundance)-rank plots of samples with six species, with the tend to have higher total volume, and species with smaller mean line with similar highest and lowest rank values. fruiting body tend to have low total volume. Two other effects For flowering plants and animals a linear relation between log may make a secondary contribution to the ranking: (1) if some (abundance) and rank is taken to be consistent with species species are much more efficient than others at growth and radiating into what is initially a vacant environment with producing fruiting bodies they would be higher rank species food, the species growth for each species being exponential. than their fruiting body volume would warrant. Conversely if In Fig. 5 the linearity of the mean relationship (dotted line) some species are relatively less efficient they would have a using a log(abundance) scale is consistent with each species lower rank than their fruiting body volume would warrant; having exponential growth. The volume of the highest rank (2) predominant effects are random factors. Before growth species is generally only slightly less than the sample total starts in the Petri dish there is, for each species, near random volume, and the ~7 mm3 volume value is nearly the same as the numbers of the three dormant phases (spores, microcysts and mode value of Fig. 4. The predicted volume for the lowest rank sclerotium), each with different times to complete the life species is ~0.02 mm3, which equates to one fruiting body with cycle and to develop mature fruiting bodies. So if there is no a diameter of ~0.35 mm. This value is reasonable as in this efficiency difference between species, the species position in model for the lowest rank species the number of fruiting bodies the ranking would be random, but with a mean dependent on should be one, and its predicted fruiting body diameter should fruiting body volume. The observational data of this survey is approximate the mean of the fruiting body diameter of the that for an area with a near constant species assemblage sample. More importantly, the mean relationships for 11–12 (within a species assemblage area or transition zone), a species in the sample should be the same as that for six species tree genera, or Eucalyptus type, has a range of dominant in the sample, except that there should be 10–11 equally myxomycete species and near dominant species, apparently spaced volumes in one and six in the other. The model at random. That is, the highest ranking species in each Petri predicts that for samples with n species, then the n spore dish are thought to be determined by random events not by a volumes will be equally spaced along the log scale, although few species having more efficient growth. Twelve samples have what appears to be a ‘swarm’ of relatively large number of large fruiting body of one species, this ‘swarm’ being of high total volume (>16 mm3), and larger

)

3 than a normal high volume total harvest. A log(abundance)- rank plot was made for samples containing these events

(mm 10 (Fig. 6). For all samples there is a bigger than expected 6 species volume change between the highest volume species and the

volume

s next, shown by the difference in slope of the thick lines and thin lines in Fig. 6. Hence this sample data is not consistent

10 Specie 1 with the linear log(abundance)-rank model. The data is

) consistent with there being an abnormal transfer of 3 myxomycete mass from the previous myxomycete feeding event on the tree bark to the event in the Petri dish for the species forming a swarm. The genera forming these ‘swarms’ 1 0.1 are Physarum (seven samples), Badhamia (three samples), Stemonitis (one sample) and Enerthenema (one sample). 11−12 species The number of fruiting bodies forming a ‘swarm’ ranged 1 Species volume (mm 3 from 300 to 1000. 0.1

Modelling the decrease in myxomycete activity at the end of a growing event 11 9 7 5 3 1 In this survey the harvest was greatest at the first and second Species rank (reverse scale) harvests, then decreased, and was negligible from harvest four

Fig. 5. Rank-log10(abundance) plots. The lower plot shows traces for onwards. Of interest is the shape of the rise and fall in fruiting samples with 11 or 12 species, and the upper plot shows traces for body numbers, and its possible variation between species. samples with six species. A dotted line gives the mean relationship of a plot. Samples 1312 to 1391 were investigated. For each species of 626 Australian Journal of Botany P. Wellman

1.5 g f e d 1.0 c b 10

)

3

0.5 a

Sporotheca harvest

1 exponential increase (normalized 2 weeks =1.0) 0 0 1 2 3 4 5 Growing time (weeks)

Species volume (mm Fig. 7. Decline of myxomycete activity after two weeks. Each line shows 0.1 the change in the number of fruit produced, averaged for 2–8 samples, and normalised to the collection at the end of week two after watering. Species abbreviations: a, Arcyria sp. H.; b, Physarum decipiens;c,Enerthenema papillatum;d,Perichaena vermicularis;e,Badhamiopsis ainoae;f, 11 9 7 5 3 1 Calomyxa metallica;g,Comatricha ellae or Comatricha elegans. Species rank (reverse scale)

Fig. 6. Rank-log10(abundance) plots for samples where one species has a analysing geographical regionalisation, gave maps for Africa large fruiting ‘swarm’. The slope given by the thick line (defined by the of a parameter ‘neighbourhood heterogeneity’. Bands of high species with the greatest volume and the species with the second greatest heterogeneity correspond with the transition zones. The bands volume) is much steeper than the slope defined by the remainder of the are generally 200–300 km wide, which is consistent with species. transition zone widths for Australian myxomycetes. The magnitude of myxomycete change over a species these samples the number of fruiting bodies was counted for each assemblage boundary can be expressed by the proportion of harvest, and if there were records for most weeks the sample- species that terminate at the transition zone. Estimates for the Tr/ species could be used. Species were selected that had records that NAr boundary are 80% in the Northern Territory and 80% in could be used derived from three or more samples. For each Queensland (Wellman 2016), for the NAr/SAr boundary it is species the total number of fruiting bodies for the selected 30% in the Northern Territory and ~43% in Western Australia, samples was added for each harvest. The results for each and at the SD/Te boundary it is 57% in north-east New South species were normalised to a value of 1.0 at harvest 2 Wales, 53% in south-east New South Wales and ~64% in (14 days). The graph of this data (Fig. 7) shows the mean Western Australia. These proportions have low accuracy but paths of the various species are relatively consistent after they show there is generally considerable species change at harvest 2, with an approximately linear decrease from species assemblage boundaries. harvest 2 to harvest 4 and an average of very few fruiting The restriction of certain myxomycete species to certain bark bodies for each species at harvest 4 and later. The simplest types, and the restriction of certain bark types to some explanation for this linear decrease is that the myxomycete phytogeographical regions makes it highly likely that at least numbers are limited by a linear decrease in food supply and in part myxomycete species associations are controlled by that this food supply affects the species equally. Prior to week phytogeographical regions. However, the partial independence two the trajectories of the species are different, consistent with of the myxomycete species association is suggested by species the exponential increase of each species starting at different that are characteristic of arid areas (Physarum decipiens, and times, and possibly increasing at a different rate. This overall Mabrideola oblonga). model is roughly consistent with the published ‘development Myxomycetes (a unicellular organism) appears to be time’ information, such as by Schnittler (2001). geographically distributed in such a way that different species It is unusual for bark in the countryside to be dry for long associations are found in distinct geographical regions. This periods then damp continuously for four weeks or longer. leads to question as which plant and animal groups are also in Hence moist chamber cultivation is unlikely to be replicate the similar (major) geographical regions, and how much the pattern of myxomycete growth and decrease in activity during boundaries agree. The difference in flora and fauna of the arid a rainfall event in the countryside. Figs 5 and 7 are important in and non-arid areas of Australia was recognised early (Tate 1889). that they are an indication of the controls on myxomycete It is a major feature of the phytogeographical and terrestrial growth and subsequent decrease in activity. zoogeographical regions (Kikkawa and Pearse 1969; Cogger and Heathwole 1981; Ebach et al. 2013, 2015; González-Orozco Biogeographical region boundaries et al. 2014). There is approximate agreement between the various In order to put the transition zone widths for myxomycete estimates of the arid/non-arid boundary position from plant, species assemblages in perspective, it is necessary to compare animal, myxomycete and arid ecology (Morton et al. 2011). A them with transition zone widths for other Australian boundary between a northern and southern arid areas was organisms. However no estimates of transition zone width recognised by Burbidge (1960). González-Orozco et al. and continuity have been published. Linder et al.(2012), in (2014) showed that this boundary was the major floral Australian corticolous myxomycetes Australian Journal of Botany 627 boundary in Australia. Computer analysis showed that a there is very little evidence for ‘past events’ controlling similar boundary is a reasonably important boundary for Australian corticolous myxomycete distribution. Random birds (Kikkawa and Pearse 1969) and for reptiles (Cogger distribution is not dominant as the level of outliers in and Heathwole 1981). The present paper shows that there is a Tables S1–S4 is low. Hence this study is consistent with similar boundary with myxomycetes. Hence, there seems to be environmental control (the Baas-Becking model of ubiquity) common first-order biogeographical regionalisation in being the overriding control of myxomycete distribution. Australia, and this includes myxomycetes (Fig. 2). In Myxomycetes may be a fairly obscure group of single cell Europe and Africa computer analyses of flowering plant organisms but models for their distribution and growth may be and animal distribution data have been used to determine if important in two contexts. First, single cell organisms there is a common biogeographical region. Common regions constitute a major proportion of life on Earth. In a paper on was found in subSaharan Africa with mammal, bird, the biomass distribution on Earth, Bar-On et al.(2018) amphibian, reptile, and vascular plants (Linder et al. 2012), estimated that of the total biomass of the Earth of 550 Gt but common regions were not found in Europe (Rueda et al. of carbon, of which 450 Gt C was plants, 70 Gt C was bacteria, 2010). 7 Gt C was archaea, and 4 Gt C was protists. In the soil biomass myxomycetes form a major component of soil Similarity of the Australian species assemblages to those protozoans (Stephenson et al. 2011). Modelling of these found in other continents other single cell organisms over the Earth is difficult except by molecular methods, while myxomycetes can be studied Three overseas corticolous surveys give species lists that easily using normal botanical methods. Second, continental- contain a large proportion of the species found commonly scale distribution modelling of spore bearing plants/fungi in Australia. McHugh (2009) reported a small survey from two (ferns, mosses, liverworts, lichen, fungi) is difficult in a areas in Paraguay: an arid area near Filadelfia (mean annual  mainly arid continent such as Australia. Distribution models rainfall 700 mm, 22 S), and from the higher rainfall area in  have not been proposed for these groups. However the effect of eastern Paraguay (1200–1800 mm, ~26 S). A high proportion spore distribution should be similar for myxomycetes and of the species in this survey are also found in the Australian spore bearing plants. arid and non-arid species associations. Novozhilov et al. There has been very little previous discussion of the relative (2003) reported on a survey in the Colorado Plateau of  abundance of myxomycete species within continental sized USA 30–38 S and a mean rainfall of 130–250 mm/year, but areas. It seems from this study that myxomycete distributions with a wide range in altitude and hence climate, and few tree are an interaction between three distribution models; species species. These Colorado species are very similar to the distribution density having step-like changes, gradients in Australian arid species (Wellman 2016). Pando and Lado density, and random distribution of ‘outliers’. Step-like (1990) and Wrigley de Basanta (1998)reportedonsurveys  changes are supported by the species association model of Spain 36–44 S and a mean rainfall of 400–1000 mm/year. (Table 1). Ing (1982) made maps of the distribution over The reported species are similar to SAr and Te species Britain, which are consistent with species having a limited assemblages in Australia (Wellman 2016). Wellman (2017) tolerance to the Atlantic weather causing the distribution of compared myxomyetes species assemblages field-collected on species to terminate at different distances to the north-west. wood in temperate climates in Australia, Patagonia, Spain and This gradient change is similar to the change across Tr and Te Britain and found that there were no major differences in the from the relatively arid short woodland to the wetter tall open species present or their relative abundance that could not be forest and closed-canopy rainforest. These two observations attributed to normal collecting variation. Hence the support gradients in distribution density. The possibility of a myxomycetes in Australia on bark and wood have a similar low density of ‘outliers’ is consistent with the existence of species assemblage to those elsewhere in areas with the same scattered odd species observations within the long profiles of climate. The major differences between Australian corticolous this paper (Tables S1–S3). myxomycetes and those overseas are that only in Australia is Using molecular techniques it has been found that marine the common Comatricha species C. ellae and C. elegans,one amoeba-eating bacteria have a mean value of gross growth common Australian species (Arcyria sp. H) has not been efficiency of 22% (Zubkov and Sleigh 1999) and 36% (Butler recognised elsewhere, and one rare species (Cribraria bicolor, and Rogerson 1996). The total volume of myxomycete spores Stephenson et al. 2018) has not been found outside Australia. grown from five Petri dishes of each sample is ~4 mm3 over most of Australia (Fig. 3), so the total volume of bacteria (and Other topics other minor food groups) eaten can be estimated very Martiny et al.(2006) using data from molecular methods approximately as 14 mm3 dry volume for the very artificial discussed controls on microorganism distribution. They rainfall event of a moist culture experiment. The total mass of concluded that the control is both the present environment and the bark sample in five Petri dishes is to 30 g, and the area of past events, but not random distribution over space. However, the weathered bark surface is generally ~70% of the areas of this is not supported by the present study. Control by present the dishes or 4500 mm2. It is thought that only the small environment is supported by the existence of the species thickness of the well weathered bark is hosting the associations, and by the observation that almost all important myxomycetes and their food, so that area is probably the species are found in similar environments overseas. The only critical parameter to convert the harvest to a landscape significant species not found overseas is Arcyria sp. H. Hence, value of corticolous myxomycete productivity. 628 Australian Journal of Botany P. Wellman

Conclusions after this exponential growth is a linear decrease in harvested The regional variation of myxomycetes across Australia can be spore volume from the end of week two to negligible harvest at determined by sampling long traverses across the continent the end of week four. This model is consistent with a linear along the rainfall gradient. For each substrate sample we can decrease in the amount of food available. obtain relatively large populations of the stronger, common fl myxomycetes by collecting bark samples that are large and Con ict of interest diverse in texture, and by cultivating more Petri dishes for each The author declares that there are no conflicts of interest. sample. With these changes in procedure a continent-wide ecological study of a unicellular organism (myxomycetes) is Acknowledgements achievable over a relatively short period. I wish to thank the Australian National Herbarium for the use of fi Along myxomycete long-traverses we nd four distinct laboratory facilities, and two anonymous reviewers for very helpful species associations (Tropical, Northern Arid, Southern Arid suggestions. I received help and encouragement from Christine Cargill, and Temperate). In the arid and semiarid areas the myxomycete Judith Curnow and Heino Lepp of the Cryptogam Herbarium at the species associations do not change much within the species Australian National Herbarium, Steve Stephenson of University of association either north–south with amount of rainfall, or Arkansas, and (during field work) from Mike Morriss of Canberra. east–west with the proportion of rainfall falling in summer The collections are in the Australian National Herbarium (CANB). fi relative to winter. In the non-arid areas there is a strong change The research did not receive any speci c funding. in species from the inland, dryer forests of short woodland to References wetter forests (taller denser forest and closed rainforest), but this change is poorly defined with available data. The transition Bar-On YM, Philips R, Milo R (2018) The biomass distribution on Earth. zones between these species associations have a width of Proceedings of the National Academy of Sciences of the United States of – 200–400 km, which is about one-half the width of many of America 115, 6506 6511. doi:10.1073/pnas.1711842115 the geographical regions, so between one-half and one-third of Black DR, Stephenson SL, Pearce CA (2004) Myxomycetes associated with the aerial litter microhabitiat in tropical forests of northern Queensland, the Australian area is within a transition zone. Across a – – Australia. Systematics and Geography of Plants 74, 129 132. transition zone the species associations change by 30 80%. BOM Bureau of Meteorology (2017) Average annual rainfall map The four species assemblages can be distinguished by key for Australia. Product code IDCJCM004. Available at http://www. common species, the species being previously known to occur bom.gov.au/jsp/ncc/climate_averages/rainfall/index.jsp [Verified 22 in this climatic zone overseas. The regions defined by the four January 2020]. myxomycete species associations correspond with the major Burbidge N (1960) The phytogeography of the Australian region. Australian flowering-plant based phytogeographical regions. This is Journal of Botany 8,75–211. doi:10.1071/BT9600075 thought to be partly due by all bark types are not present in Butler H, Rogerson A (1996) Growth potential, production efficiency and all the phytogeographical regions. annual production of marine benthic naked amoebae (gymnamoebae) The average productivity of the myxomycete population, is inhabiting sediments of the Clyde Sea area, Scotland. Aquatic Microbial Ecology 10, 123–129. doi:10.3354/ame010123 relatively high and uniform over arid Australia, but it is lower Cogger HG, Heathwole H (1981) The Australian reptiles: origins, in the open forest non-arid areas, and is likely to be much lower biogeography, distribution patterns and island evolution. In in wet tall open-forests and closed rainforests. The change in ‘Ecological biogeography of Australia’. (Ed. A Keast) pp. 1303–1373. composition of the myxomycetes can be expressed using the (Dr W Junk: The Hague, The Netherlands) proportion of the myxomycete orders. The Echinosteliales and Davison EM, Davison PJN, Brims MH (2008) Moist chamber and field Clastodermatales have about the same importance in arid collections of myxomycetes from the northern Simpson Desert, and non-arid areas. The Physarales and Liceales are more Australia. Australasian Mycologist 27, 129–135. important in the arid areas. The Trichiales, Cribraiales, and to a Davison EM, Davison PJN, Barrett MD, Barrett RL, McMullan-Fisher SJM lesser extent Stemonitidales, are more important in the non- (2017) Additions to the myxomycota of summer rainfall regions of – arid areas. When measuring importance by the volume of tropical Australia. Nova Hedwigia 104,47 64. doi:10.1127/nova_hedwigia/2015/0287 spores, the Physarales dominates the pattern of change, it is Discover Life (2018) Discoverlife. Available at https://www.discoverlife. ~55% of the volume in the arid area, and ~20% in the non-arid org/ [Accessed January 2020]. areas. The myxomycete species clearly have preferred climatic Ebach MC, Gill AC, Kwan A, Ahyong ST, Murphy DJ, Cassis G (2013) area (species associations), bark preferences of pH, hardness Towards an Australian bioregionalisation atlas: a provisional area and texture. The pH of the bark is important, effecting the taxonomy of Australia’s biogeographical regions. Zootaxa 3619(3), number of records per sample, the total volume of spores 315–342. doi:10.11646/zootaxa.3619.3.4 produced, and the proportion of the Physarales. Ebach MC, Murphy DJ, González-Orozco CE, Miller JT (2015) A revised For most biological groups the population dynamics during area taxonomy of phytogeographical regions within the Australian – growth are determined by a single large population. With bioregionalisation atlas. Phytotaxa 208, 261 277. myxomycetes cultivation we have a large number of doi:10.11646/phytotaxa.208.4.2 González-Orozco CE, Ebach MC, Laffan S, Thornhill AH, Knerr NJ, individual growth experiments, which together can be used to Schmidt-Lebuhn AN, Cargill CC, Clements M, Nagalingum NS, infer the average population dynamics after a watering event. Mishler BD, Miller JT (2014) Quantifying phytogeographical Each growing phase can be modelled by a linear log(abundance)- regions of Australia using geospatial turnover in species rank plot. This model is consistent with the species growing composition. PLoS One 9(3), e92558. exponentially in an initially vacant space. The population decline doi:10.1371/journal.pone.0092558 Australian corticolous myxomycetes Australian Journal of Botany 629

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