Distribution and ecology of the assemblages of myxomycetes associated with major vegetation types in Big Bend National Park, USA

fungal ecology 2 (2009) 168–183

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Distribution and ecology of the assemblages of myxomycetes associated with major vegetation types in Big Bend National Park, USA George G. NDIRITUa,b,*, Frederick W. SPIEGELa, Steven L. STEPHENSONa a

Department of Biological Sciences, Environmental Dynamics Program, University of Arkansas, Fayetteville, AR 72701, USA Centre for Biodiversity, National Museums of Kenya, 40658 00100 Nairobi, Kenya

b

article info

abstract

Article history:

The distribution and ecology of the assemblages of myxomycetes associated with four

Received 1 September 2008

different microhabitats were studied in Big Bend National Park in Texas. During Mar. 2005,

Revision received 1 January 2009

twelve plots (30  30 m) were established along an elevational gradient that extended from

Accepted 10 March 2009

564 to 1807 m. Samples of aerial bark from dead and living trees, aerial litter (dead but still

Published online 17 May 2009

attached plant parts), ground litter (fallen dead plant parts) and ground bark (fragments of

Corresponding editor: Lynne Boddy

fallen bark) were collected from these plots, which encompassed all of the major vegetation types found in the Park. Four hundred forty-seven moist chambers were prepared, and

Keywords:

95.8 % (428) produced some evidence (either fruit bodies or plasmodia) of myxomycetes. A

Biodiversity

total of 71 species were recorded, with ground litter yielding most (45 species). Aerial litter,

Deserts

aerial bark and ground bark yielded 44, 39 and 37 species, respectively. Species abundance

Environmental gradients

distribution measures (diversity, dominance and similarities) varied among the four

Microhabitats

microhabitats as well as among the major vegetation types. Canonical Correspondence

Slime molds

Analysis (CCA) showed that species distribution patterns were closely related to: (1) the

Vegetation types

major environmental-complex gradients associated with differences in elevation/ temperature/moisture conditions that occur from one locality to another; and (2) the different types of microhabitat. Published by Elsevier Ltd.

Introduction Myxomycetes (also called plasmodial slime molds or myxogastrids) are eukaryotic microorganisms that commonly occur in terrestrial ecosystems, where they feed primarily on bacteria, algae and fungi. Studies of myxomycetes have been ongoing for more than 350 y, but many of the more important ecosystems in the world have not been surveyed adequately for these organisms (Ing 1994; Spiegel et al. 2004). Although the taxonomy of myxomycetes at the species level, using a morphological species concept, is

good, our knowledge of their distribution and ecology is poor (Feest 1987; Stephenson & Stempen 1994; Spiegel et al. 2004). For example, recent data obtained during a global inventory for all three groups of slime molds (protostelids, dictyostelids and myxomycetes) suggest that similar species from different regions of the world tend to be characterized by distinct morphological differences and their micro- and macrohabitat distribution patterns can change spatially and temporally along certain biotic and abiotic gradients that are not yet well documented (Clark et al. 2003; http://slimemold.uark.edu/).

* Corresponding author. Department of Biological Sciences, Environmental Dynamics Program, University of Arkansas, SCEN 632, Fayetteville, Arkansas 72701, USA. Tel.: þ1 479 575 7393; Fax: þ1 479 575 4936. E-mail address: [email protected] (G.G. Ndiritu). 1754-5048/$ – see front matter Published by Elsevier Ltd. doi:10.1016/j.funeco.2009.03.002

Distribution and ecology of myxomycetes in Big Bend National Park, USA

Recent efforts to include some ecological aspects of myxomycetes in taxonomic studies have led to an increased understanding of the distribution and ecology of these organisms (Stephenson 1988; Schnittler et al. 2002; Novozhilov et al. 2006). At the local level, myxomycetes have been reported to show a non-random distribution such that the assemblages of species in different microhabitats within the same habitat may be more dissimilar than assemblages associated with similar microhabitats in different habitats. Some species of myxomycetes appear to be strongly associated with particular microhabitats (Stephenson 1989, 2003; Stephenson & Stempen 1994; Schnittler & Stephenson 2000). Although some predictions can be made relating to the presence or absence of various species with respect to some microhabitats, too few data are available to allow quantitative predictions (Ing 1994; Spiegel et al. 2004). Moreover, the ways in which abiotic (e.g. moisture content, pH, physical habitat characteristics) and biotic (e.g. the availability of food resources and possible intra- and interspecific competition for these resources) factors interact to influence the distribution and occurrence of myxomycetes are poorly understood (Stephenson 1989). Big Bend National Park, located in the Trans-Pecos region of west Texas, covers an area of approximately 3291 km2 (Fig 1). The park encompasses a diverse range of habitats, from expansive areas of Chihuahuan Desert shrubland and grassland interspersed with woodland in the Chisos Mountains to riparian and wetland areas along the Rio Grande River. Deep canyons are found at some places along the

169

river. Several taxonomic collections that have been carried out in the park show that the region is rich in myxomycete diversity. McGraw (1968) reported 33 species, whereas Tiffany & Knaphus (2001) in their week-long collecting trips over 10 y listed a total of 70 species. No ecological data exist for the park. Moreover, only a few ecological studies of myxomycetes have been carried out in arid lands of the world (Novozhilov & Schnittler 2008). The few available data indicate that species assemblages vary unpredictably from one region to another (Novozhilov et al. 2003; Kosheleva et al. 2008). In the present study, two sets of data, the first generated during a preliminary survey carried out in Big Bend National Park during Jan. 1998 and the second obtained during a more comprehensive study during spring 2005 were used to analyze species distribution patterns and the composition of the assemblages of species associated with particular types of microhabitats. More specifically, efforts were made to: (a) determine the extent to which assemblages of myxomycetes change across the park in response to changes in vegetation; (b) compare and contrast the assemblages of myxomycetes associated with four different kinds of microhabitat (aerial litter, aerial bark, ground litter and ground bark); (c) assess the relationships between myxomycete distribution patterns and various environmental factors (e.g. pH, elevation and substratum richness); (d) compare the data with those from arid lands of the world. As used herein, the term microhabitat refers to a limited portion of the total habitat (sensu Stephenson 1989).

Fig 1 – Map of the United States (upper right) showing the location of Big Bend National Park (black dot) in Texas. The study sites sampled (1–13) are located along an elevation gradient that extends from 564 m to 1807 m. The area within the dotted line mostly consists of woodlands and shrublands in the Chisos Mountains. Chihuahuan Desert covers most of the lowlying areas and was characterized by a sparse cover of vegetation consisting of scattered shrubs and low-growing plants. Riparian vegetation was common along the River Rio Grande.

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G.G. Ndiritu et al.

Materials and methods Study sites Big Bend National Park is situated on the border between the United States and Mexico, with the Rio Grande River representing the boundary between the two countries (Fig 1). A large portion of the park occurs within the Chihuahuan Desert and is characterized by less than 300 mm of rainfall annually. Temperatures during the fall and spring are usually warm (ranges from 3 to 27  C), winters are mild (2–18  C), and summers are hot (18–34  C), with the highest temperatures between May and Aug. Elevations in the park range from 305 m to over 2438 m. The area of the park considered in the present study encompasses two different ecoregion zones.

The first of these is the lowland desert zone, within which study sites 1 and 7–13 are located, and the second is the mountain zone, within which study sites 2–6 occur. The vegetation of the lowland desert zone (from 564 to 995 m) is dominated by shrubs (Larrea and Yucca) and members of the Asteraceae, Fabaceae and Cactaceae, interspersed with the grass Eragrostis (Table 1). Also found in the lowland zones are riparian vegetation types along the Rio Grande River. These consist of Phragmites, Cynodon, and Pennisetum along with some shrubs belonging to the genera Cupressus, Acacia and Tamarisk. The vegetation of the mountain zone (from 1421 to 1807 m) is dominated by shrubs and trees, usually members of the genera Pinus, Ilex, Quercus and Cupressus. Understory species include shrubs that belong to the Asteraceae, Fabaceae or Cactaceae, along with stipa grass.

Table 1 – Study sites locations, percentage slope, rockiness and vegetation characteristics Site

Name

Forest (Group one) 2 Bear Station

3

Lost Mile East

4

Lost Mile West

5

Chisos Mountains #1

6

Chisos Mountains #2

Desert (Group two) 1 Mile 5 Bahada

8

Rio Grande Village (Hill)

11

Mile 15 Bahada

12, 13

Mile 10 Bahada

Riparian (Group three) 7 Rio Grande Village (River) 9

Rio Grande Village (Pond #1)

10

Rio Grande Village (Pond #2)

Latitude, Slope % Rock % Cover % longitude, elevation

29 180 13.1900 N, 103 150 54.7200 W, 1421 m. 29 160 24.700 N, 103 170 8.5900 W, 1772 m. 29 160 27.4300 N, 103 170 20.3400 W, 1757 m. 29 150 47.1400 N, 103 180 19.100 W, 1677 m. 29 150 13.5600 N, 103 180 29.1700 W, 1807 m.

Vegetation height. Dominant plants or groups of vegetation

10–20

80–90

40–60

1.5 m. Cupressus, Larrea, Yucca along with Asteraceae, Fabaceae, Cactaceae and Eragrostis.

50

>80

60–70

>5 m. Pinus, Larrea, Quercus, Cupressus, also Asteraceae, Fabaceae, Cactaceae, Yucca and stipa grass.

30–50

50

80–90

>1 m. stipa grass, also Pinus, Asteraceae, Fabaceae, Cactaceae, Cupressus, Ilex and Larrea.

50

50

60–70

>5 m. Pinus, Quercus, Ilex, Cupressus also Asteraceae, stipa grass, Fabaceae and Cactaceae.

50–60

50

70–80

>5 m. Pinus, Quercus, stipa grass, Cupressus, Asteraceae, Fabaceae and Cactaceae.

29 160 14.3600 N, 103 90 38.3300 W, 995 m. 29 100 36.5700 N, 102 570 11.6500 W, 572 m. 29 110 48.7600 N, 103 10 48.64 W, 629 m. 29 140 31.2400 N, 103 50 19.2500 W, 764 m.

10–20

80–90

40–60

1 m. Larrea, Yucca along with Asteraceae, Fabaceae, Cactaceae and Eragrostis.

20

80

20

<1 m. Larrea, Acacia, Argemone, Yucca and Eragrostis.

5–10

70–80

30–40

0.5–0.75 m. Asteraceae, Fabaceae along with Larrea, Acacia, Yucca and Eragrostis.

10–20

80–90

40–60

0.5–1 m. Asteraceae, Fabaceae along with Larrea, Acacia, Yucca and Eragrostis.

29 100 29.8600 N, 102 570 3.2500 W, 564 m. 29 100 46.3900 N, 102 570 12.5300 W, 569 m. 29 100 47.3300 N, 102 570 13.4800 W, 569 m.

<1

<1

70–80

>5 m. Cupressus, Acacia, Tamarisk, Phragmites, Cynodon and Pennisetum.

<1

<1

80–90

>2 m. Pure stand of Phragmites.

<1

<1

70–80

>2 m. Sporobolus and Cyperaceae.

Study sites are presented in the three groups suggested by Canonical Correspondence Analysis (CCA) using species and environmental data.

Distribution and ecology of myxomycetes in Big Bend National Park, USA

Sampling regimes and strategy Samples for incubation in moist chamber cultures were collected from approximately the same localities in the park during the winter of 1998 and spring 2005. In the more extensive 2005 study, samples from the four different types of microhabitats (both aerial and ground substrates) were obtained from twelve plots (each 30  30 m) established along an elevation gradient that extends from 564 to 1807 m. In addition, distinctions were made with respect to the type (i.e. pieces of bark, dead leaves, other types of plant debris, etc.) and origin (i.e. plant species) of the sample material. The number of plants and different substrata present in a particular study site determined just how many substratum samples were collected in each site (referred to throughout this paper as substratum richness). Some of the more common groups of plants from which samples were collected included: (1) members of the Poaceae (e.g. reed, bermuda, buffel, tufted and drop seed grass); (2) various shrubs, including members of the Zygophyllaceae (e.g. creosotebush), Fabaceae (e.g. acacia), Tamaricaceae (e.g. tamarisk) and Asteraceae; (3) members of the Agavaceae (e.g. yucca); (4) succulent plants belonging to the Cactaceae (e.g. cactus and prickly poppy) and (5) woody plants in the Cupressaceae (e.g. cedar), Pinaceae (e.g. pine), Fagaceae (e.g. oak), and Aquifoliaceae (e.g. holly). During sampling, general site characteristics (e.g. slope, rockiness and vegetation cover) were recorded, the elevation was determined, and the geographical coordinates obtained using a portable Garmin GPS 12, Garmin Olathe, KS, USA (Table 1).

Moist chamber cultures In the laboratory, the sample material was incubated in a total of 535 moist chambers consisting of Petri dishes (63.6 cm2 area) lined with moistened filter paper, as described by Stephenson & Stempen (1994). For each sample, four replicates were prepared. These were incubated under ambient light and at room temperature for ca. 120 d and checked for the presence of myxomycetes on five occasions (days 4–7, 20–24, 40–45, 70–75 and 110–120). For each moist chamber culture, the total number of sporocaps produced was quantified as described by Novozhilov et al. (2000), but the multiple occurrence of a particular species was considered as one record (e.g. Stephenson 1989). Values of pH were determined for each moist chamber 24 h after water had been added to the sample material, using a flat electrode PH meter (Orion Model 210A, Orion Research Inc., Beverly, MA, USA).

Taxonomy Specimens of myxomycetes were identified to morphospecies using standard monographs (e.g. Martin & Alexopoulos 1969) for the group. Nomenclature used follows Herna´ndez-Crespo & Lado (2005) and uncertain identifications are indicated by ‘‘cf.’’ (compare). Names of vascular plants are those given in the PLANT database (NRCS 2007). The relative abundance index of each species, which is an estimate of the proportion of a species in relation to the total number of records, was determined as suggested by Stephenson et al. (1993), where

171

A ¼ abundant (>3 % of all records), C ¼ common (1.5–3 %), O ¼ occasional (0.5–1.5 %) and R ¼ rare (<0.5 %).

Data analysis The completeness of the sampling effort for each microhabitat was assessed with incidence (ICE) and abundance (ACE) based coverage estimators and CHAO2 (Colwell 2006; http://viceroy. eeb.uconn.edu/EstimateS). The estimators use rare species recorded to describe the overall species richness (Chao et al. 2000). The use and success of these estimators are still under examination, and it has been suggested that their success depends upon the sample size, abundance and distribution pattern of the organisms under consideration (e.g. Chao et al. 2006), hence all three were used for comparison as recommended by Unterseher et al. (2008). The estimated value for the percentage of completeness for each microhabitat was determined by dividing the actual number of species recorded by the mean number of species expected as estimated by all the estimators. Species recorded were described using several species abundance distribution measures. Species commonness and rarity were analyzed using a species rank/abundance plot, which has the benefit of displaying contrasting patterns of species richness, such as differences in evenness and biomass, among different assemblages (Magurran 2004). A sample-based rarefaction curve was generated using Coleman’s ‘random placement’ method (Coleman et al. 1982). The curve has the advantage of being closely related to a species accumulation curve. Relative abundance data were used to determine species diversity, dominance and evenness using the Hill family of diversity indices (Hill 1973; Pielou 1975), where pi ¼ percentage (relative abundance) of species per site (assemblage); N0 ¼ total number of species present; P N1 ¼ exp[ pi ln( pi)] ¼ exp(H0 ) ¼ exponential Shannon index; P 21 N2 ¼ ( pi ) ¼ reciprocal of Simpson’s index; NINF ¼ ( pi)1 ¼ for the commonest species; and J0 ¼ ln(N1)/ln(N0) for evenness. Species composition similarity was assessed using Morisita’s index of similarity and Horn’s index of overlap (Towner 1999) for all pairwise combinations of the four microhabitats. Morisita’s index is based on the logic of the Simpson diversity index, whereas Horn’s index is based on the logic of the Shannon index. Both indices are based upon the species identity and their abundances, with values ranging from 0 to 1, with an increasing degree of similarity between the two communities being compared. Spearman rank correlation values were generated to investigate the degree of association among elevation, slope, pH, substrata richness, vegetation cover, rock cover, species abundances and biodiversity indices. These non-parametric analyses were performed using STATISTICA (StatSoft Inc. 2000). To examine patterns in the composition of species assemblages in relation to environmental attributes, Detrended Correspondence Analysis (DCA) and Canonical Correspondence Analysis (CCA) were carried out (ter Braak & Sˇmilauer 1999). Randomized 499 Monte-Carlo permutation tests were performed to determine which environmental variables exerted significant influences on myxomycete distribution at p < 0.05, using conditional automatic forwarding options (Lepsˇ & Sˇmilauer 2003). Also tested were the significances of the first ordinance axis and all four axes together. During analyses

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Table 2 – Occurrence of myxomycetes in the four microhabitats, including a number of species recorded and sampling effort Species name

Acronym

AIc

Abundancea GL98

Arcyria cinerea A. denudata A. insignis A. pomiformis Badhamia melanospora B. paniceae Calomyxa metallicae Ceratiomyxa fruticulosa Clastoderma debaryanum Comatricha eleganse C. laxa C. mirabilis C. nigra C. pulchella C. tenerrimae Comatricha sp. Craterium aureum C. minutum C. microcarpae Cribraria violaceae Dictydiaethalium plumbeume Diderma cf. chondriodermae D. effusume Diderma sp. Didymium anellus D. difforme D. dubium D. iridis D. minuse D. nigripes D. ochroideum D. squamulosum Didymium sp. Echinostelium minutum E. colliculosume Hemitrichia minor var. minore Lamproderma scintillanse Licea belmontianae L. biforise L. kleistoboluse Paradiacheopsis solitariae Perichaena chrysosperma P. corticalis P. depressa P. pedata P. vermicularise Perichaena sp. Physarum aeneume P. albume P. bitectum P. bivalve P. cinereum P. compressum P. didermoides P. echinosporum P. flavicomume P. lakhanpaliie P. notabilee P. pusillum P. serpulae P. spectabilee P. straminipese

ARCcin ARCden ARCins ARCpom BADmel BADpan CALmet CERfru CLAdeb COMele COMlax COMmir COMnig COMpul COMten COMsp. CRAaur CRAmin CRImic CRIvio DICplu DIDEchr DIDEeff DIDEsp DIDane DIDdif DIDdub DIDiri DIDmin DIDnig DIDoch DIDsqu DIDsp ECHmin ECHcol HEMmin LAMsci LICbel. LICbif LICkle PARsol PERchr PERcor PERdep PERped PERver PERsp PHYaen PHYalb PHYbit PHYbiv PHYcin PHYcom PHYdid PHYech PHYfla PHYlak PHYnot PHYpus PHYser PHYspe PHYstr

A R O R A O R R R O C R O O R O R R R R R C R R A R R R C R C A R C R O O R R R O A O A R C R R R O A C C O O R R C A O R C

15 – – 2 1 – 3 – – – – – 2 20 – 33 – – – – – – – – 3 10 – – – – – – – – – – – – 100 – – 4 10 8 – – – – – 20 90 – – – – – – 2 71 – – –

GL 589 5 61 – 3087 580 – 100 10 – 216 – 12 470 1 – – – 30 – – 3 2 – 595 – – – 577 2 1006 1285 22 1660 – 805 155 – – – – 379 82 2335 – 142 67 – 262 168 472 1101 2858 20 100 18 – 661 1466 9 5 3225

AL 332 – 1 – 5758 181 – – – 2 59 – 5 11 – – – 35 – – – – – – 332 11 – 270 2545 80 690 1936 48 30 – – – – – – – 184 201 2553 23 111 2 2 5 93 195 796 726 250 43 – – 370 2957 – 55 281

Recordsb GB 937 1 – – 135 250 – 10 – 12 25 4 30 145 1 2 25 – – 20 2 – – – 56 – – – – – 35 – – 1220 100 – – – – 5 12 479 264 303 – – – 60 – – 55 575 74 – – – – 310 75 115 – –

AB 626 – – – 786 120 4 10 25 76 81 – 69 55 5 – – – – 30 – – – 3 222 – 2 – 35 – – 50 – 6150 – – 10 20 – 11 30 191 340 2593 – – – 80 – – 448 368 – 930 7 – 10 795 804 100 – –

GL

AL

GB

AB

26 1 5 – 24 4 – 1 1 – 6 – 2 6 1 – – – 1 – – 1 1 – 25 – – – 7 1 17 25 2 4 – 7 5 – – – – 24 4 44 – 9 1 – 3 5 8 8 18 1 1 2 – 10 18 2 1 12

8 – 1 – 43 3 – – – 1 5 – 1 1 – – – 1 – – – – – – 17 3 – 1 22 1 9 26 1 1 – – – – – – – 10 6 50 1 12 2 1 1 4 7 10 8 2 4 – – 6 28 – 2 8

24 1 – – 3 1 – 1 – 2 1 1 4 2 1 1 1 – – 1 1 – – – 4 – – – – – 2 – – 5 1 – – – – 1 1 21 2 8 – – – 1 – – 3 5 2 – – – – 4 2 6 – –

26 – – – 6 4 1 1 1 2 9 – 5 2 1 – – – – 2 – – – 1 5 – 1 – 1 – – 2 – 11 – – 1 1 – 3 6 14 4 31 – – – 1 – – 4 3 – 4 2 – 2 5 8 8 – –

Distribution and ecology of myxomycetes in Big Bend National Park, USA

173

Table 2 (continued) Species name

P. cf. viridee Physarum sp. A Physarum sp. B Stemonitis fusca S. herbaticae S. cf. mussooriensis S. splendens Trichia favoginea Willkommlangea reticulata Moisture chamber cultures Records made Species recorded Mean species per culture Species estimated ACE ICE CHAO2 % Sampling effortd

Acronym

PHYvir PHYspA PHYspB STEfus STEher STEmus STEspl TRIfav WILret

AIc

R R O O C R R R O

Abundancea

Recordsb

GL98

GL

AL

GB

AB

GL

AL

GB

AB

– – 1 – – – – – – 59 61 18 1  0.3

29 – 51 – 682 – – – 70 187 361 45 1.9  1.4

– 61 75 459 944 40 150 320 89 147 330 44 2.2  1.6

70 – 3 93 515 – – 120 5 53 127 37 2.6  1.6

– – – 300 220 – – 280 23 60 186 39 3.0  1.8

2 – 2 – 10 – – – 3

– 2 3 4 6 1 1 2 4

1 – 1 3 5 – – 1 1

– – – 2 2 – – 3 2

19 34 31 55

45 55 56 80

44 57 64 70

38 59 64 60

38 49 44 81

a Total number of sporocarps per species per microhabitat for all moist chamber cultures. b Number of records per microhabitat. Abbreviation: GL ¼ ground litter, GB ¼ ground bark, AB ¼ aerial bark and AL ¼ aerial litter. c Abundance index (AI) proportion of a species in relation to the total number of records made (Stephenson et al. 1993), where A ¼ abundant (>3 % of all records), C ¼ common (1.5–3 %), O ¼ occasional (0.5–1.5 %) and R ¼ rare (<0.5 %). d Sampling effort is the number of species recorded divided by the mean value of estimated species richness of incidence-based coverage estimator (ICE) and CHAO2. Abundance-based coverage estimator (ACE) underestimated richness and thus was not used to determine the percent sampling effort. e Signify new records for Big Bend National Park.

carried out with DCA and CCA, rare species of myxomycetes (i.e. those that were recorded from only a single site) were excluded (Table 2). Environmental variables used included pH, elevation, substrata richness, vegetation cover and rock cover. Slope, which was highly correlated with elevation, was not used in the CCA because it has been suggested that highly correlated variables tend to cause redundancy in the set of explanatory variables (Lepsˇ & Sˇmilauer 2003).

preliminary data set for ground litter in 1998 was only 55 % complete (Table 2). As such, the surveys carried out in spring 2005 for the four microhabitats would be considered adequate, whereas the preliminary sampling in 1998 was insufficient, (Fig 2 upper panel). Although the numbers of moist chamber cultures prepared from the four microhabitats were different, the species data compiled were considered sufficient to justify further comparison analyses.

Species abundance

Results Survey completeness During this study 71 species of myxomycetes were recorded from the four major microhabitats in Big Bend National Park, and 29 of these were new records for the park (Table 2). During spring 2005, 45 species were recorded from ground litter, 44 from aerial litter, 38 from ground bark, and 39 from aerial bark. Only 19 species were recorded from ground litter samples in 1998. The number of species expected if the sampling effort was exhaustive indicates that results of ICE and CHAO2 species richness estimators were comparable and reasonable, whereas those of ACE were low, unrealistic and highly unlikely (Table 2, Fig 2 upper panel). Species richness estimated by ACE was therefore not used to determine the percentage sampling effort of each microhabitat. Values obtained by applying the ICE and CHAO2 species richness estimator to the data sets from 2005 suggest that our sampling effort was 81 % complete for aerial bark, 80 % for ground litter, 70 % for aerial litter and 60 % for ground bark. The limited

Comparison of species rank/abundance data for the four microhabitats suggests that an uneven absolute abundance of common species existed among the microhabitats (Fig 2 middle panel, Table 2). The ground bark microhabitat was characterized by low species abundance and aerial bark by moderate species abundance, whereas aerial litter and ground litter microhabitats had high species abundances. The most commonly recorded species on aerial litter were Badhamia melanospora (24.6 % of all sporocaps from this microhabitat), Physarum pusillum (12.9 %), Perichaena depressa (10.9 %), Didymium minus (10.8 %) and Didymium squamulosum (8.4 %); for ground litter B. melanospora (12.1 %), Physarum straminipes (12.7 %), Physarum compressum (11.2 %), P. depressa (9.5 %), Echinostelium minutum (6.5 %), P. pusillum (5.8 %), and D. squamulosum (5.0 %); for aerial bark E. minutum (38.6 %), P. depressa (16.3 %), Physarum didermoides (5.8 %), P. pusillum (5.1 %), B. melanospora (5.0 %), and Physarum notabile (5.0 %); and for ground bark E. minutum (19.9 %), Arcyria cinerea (15.3 %), Physarum cinereum (9.4 %), Stemonitis herbatica (8.4 %), Perichaena chrysosperma (7.8 %), P. notabile (5 %) and P. depressa

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G.G. Ndiritu et al.

70 GB-CHAO2 60

GL-CHAO2

AB-ICE

AL-ACE AB-CHAO2 GB-ACE AB-ACE

40

GL-ACE

30

GL98-ICE GL98-CHAO2

20

GL98-ACE

10

0 1

20

39

58

77

96

115 134 153 172 191 210

Number of cultures 4.5 GL AL

Abundance (Log10)

AB

GB

3.5

1

11

21

31

The rate at which new species were encountered was relatively high and displayed similar trends for all microhabitats sampled during the 2005 survey, but a lower rate was apparent for samples of ground litter collected in 1998 (Fig 2 lower panel). Comparisons of species composition among the four microhabitats, using Horn’s index of community overlap and Morisita’s index of similarity, showed various degrees of similarity (Fig 3). The degree of similarity was high for the pairwise comparisons of ground litter–aerial litter and ground bark–aerial bark; moderate for ground litter–ground bark and ground litter–aerial bark; and low for ground bark–aerial litter and aerial bark–aerial litter. Both of the two types of community similarity indices provided reasonable and informative results, with the values for Horn’s index being consistently higher than those for Morisita’s index.

Species diversity Diversity indices (N0, N1, N2, J0 ) calculated for the sets of data from the various microhabitats increased with increasing elevation and plant substratum richness (Fig 4). The values for the ground litter microhabitat were highest in study sites 1–6, 8 and 12; moderate in sites 7 and 11; and lowest in sites 9 and 10. For aerial litter, diversity indices were highest in sites 1, 2, 5, 6, 8 and 12; moderate in sites 3, 4, 7 and 11; and lowest in sites 9 and 10. High diversity indices occurred in sites 3, 5, 10 and 11 for aerial bark and sites 1, 3, 6 and 11 for ground litter. Substratum richness and availability were strongly related to plant diversity, both of which increased with elevation and moisture availability. Substratum richness was highest for high-elevation mountain study sites (3–6), moderate in midelevation sites (1, 2, 11 and 12) and riparian sites (7), and lowest in dry low-lying arid sites in the Chihuahuan Desert (sites 9

4.0

3.0 41

Species rank 50

AL

40

GL

AB 30

1.0

GB 0.8

20

Indices

Number of species

Community similarity

GL-ICE

50

Number of species

AL-CHAO2 AL-ICE

GB-ICE

(5.3 %). Most of the species with high abundances were widespread in the park. All of the other species encountered were considered common, occasional or rare (Table 2).

GL98 10

0.6 0.4 0.2

0 1

20

39

58

77

96

115

134

153

172

Number of cultures Fig 2 – Curves of incidence (ICE) based coverage, abundance (ACE) based coverage and CHAO2 estimators (upper panel), K dominance (middle panel) and sample-based rarefaction (lower panel) generated for the sets of data from the four microhabitats. Abbreviations: AL [ aerial litter, AB [ aerial bark, GB [ ground bark, GL [ ground litter and GL98 [ ground litter collected in 1998.

0.0 GLxAL

GBxAB

GLxGB

GLxAB

GBxAL

ABxAL

Microhabitats Fig 3 – Pairwise combinations of the data sets for the four different microhabitats, based on community similarity indices calculated using Horn’s index of community overlap (hatched bars) and Morisita’s index (stippled bars). Abbreviations: GL [ ground litter, AB [ ground bark, AL [ aerial litter and AB [ aerial bark.

Distribution and ecology of myxomycetes in Big Bend National Park, USA

175

AB

GB NINF

N1

J' 1.0

20

0.8

15

0.6

10

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5

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0

1 2 3

4

5

6

7 8 9 10

0.0

11 12

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1.0

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5

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J'

25

N0, N1, N2, NINF

N2

J'

N0, N1, N2, NINF

N0

0

1

2

3

4

5

6

Sites

0.8

15

0.6

10

0.4

5

0.2 2

3

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9 10 11 12

N0, N1, N2, NINF

20

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0.2

J'

1.0

J'

N0, N1, N2, NINF

0.0

9 10 11 12

GL

25

1

8

Sites

AL

0

7

0

1

2

3

4

5

6

Sites

7

8

9

10 11 12

0.0

Sites PE AB-pH

AL-pH

GB-pH

GL-pH

9

GB

AL

AB

15

10

8 1500 7 1000 6

Elevation (m)

Substrates diversity

GL

Microhabitats pH

SB 20

Elevation 2000

500 5

5

4

0 1

2

3

4

5

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7

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11

12

Sites

0 1

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3

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8

9

10 11 12

Sites

Fig 4 – Myxomycete species indices (N0 – species richness, N1 – Shannon diversity index and N2 – reciprocal of Simpson’s diversity index, NINF – species dominance, J0 – species evenness) on aerial bark (AB), aerial litter (AL), ground bark (GB) and ground litter (GL) microhabitats. Hill family indices (Hill 1973) have been used for ease of comparison of communities (Magurran 2004). The lower figures show substratum richness (SB), pH and elevation (PE) of the study sites. Note that the lines used to connect data series in figure PE are only for display and are not meant to show any particular trend.

and 10). Values of pH were relatively higher for ground litter than for the other microhabitats investigated (Fig 4 PE). Biodiversity indices for the various microhabitats correlated in several different ways with elevation, slope, pH, substratum richness, vegetation cover and rockiness (see Supplementary material). For both the ground litter and aerial litter microhabitats, diversity indices and abundances were significantly correlated (r  0.6, p ¼ 0.05) with elevation, slope, rockiness, pH and substratum richness. Conversely, for ground bark, the diversity index and abundance were significantly correlated (r  0.6, p ¼ 0.05) with elevation, pH and

substratum richness, whereas the corresponding values for the aerial bark microhabitat were significantly correlated (r  0.6, p ¼ 0.05) with pH and substratum richness. A statistically significantly association (r  0.6, p ¼ 0.05) existed between species diversity indices (N1, N0) and substratum richness for the aerial litter and ground litter microhabitats and between the aerial bark and ground bark microhabitats, as well as for the species diversity indices (N0, N1, J0 ) and abundance, substratum richness and pH. The associations noted for the ground litter versus aerial litter microhabitats and the ground bark versus aerial bark microhabitats were

COMten

7AB

COMnig DCA Axis 2

AM

COMele CRIvio

PHYs pe STEfus 5AL 10AB

PHYsp

TRIfav 4AB

1GB

BADpan WILret PHYpus 11AB 2AL 2GL PHYech BADgra DIDane DIDdif 1GL COMlax PHYnot

CERfru

11GB 6AB

3GB

COMpul ECHmin DCA Axis1

PHYdid

12AL 12GL 1AB PERdep PERver 1AL 8GL 11GL 4AL PHYcin DIDoch 9GL 7AL 10AL 11AL7GL 6AL 9AL DIDmin DIDsqu PHYstr 6GL

5AB PHYvir

4GB

PERchr

3AL ARCcin 6GB

PHYaen

LICkle PA Rsol STEher

PHYbiv

PHYcom 8AL PERcor 10GL PHYbit ARCins 3GL

5GB

CLAdeb

DIDnig

PHYser

4GL

HEMmin

3AB 5GL

LAMsci

+3.0

PHYalb

AB

CCA Axis 2 9

AL

DIDdif

Riparian Riparian

PHYstr PHYpus

7

Cover

10

DIDmin

PHYcin

PER ver

DIDsqu PHYbit

6

PH 1 Ydid

CCA Axis 1 3

2

-1.5

Desert

WILret 12 COMlax DIDane PHYech DIDoch PHYnot PERcor

+3.5

+2.0 PHYser

Elevation

4

ARCcin STEher STEfus

PERchr

Forest

8

pH

Substrate richness

Desert Rocky

-2.0

GB

BADgra PERdep BADpan

11

PHYcom

Forest

PHYbiv

5

PHYspe

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9

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6

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3

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4

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BADgra

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PHYcin

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Cover

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BADgra BADpan ARCins Rocky

12

COMlax

+2.0

Fig 5 – Top, (AM) is a Detrended Correspondence Analysis (DCA) biplot for all common myxomycetes in Big Bend N.P. Below are Canonical Correspondence Aanalysis (CCA) triplots of the four microhabitats: aerial bark (AB), aerial litter (AL), ground bark (GB) and ground litter (GL). Variables that related significantly with myxomycetes are shown with bold arrows. More results relating to the eigen values of the axes, the variances explained and Monte-Carlo permutation tests are provided in Table 3. The last two letters in the site names in the DCA biplot refer to the particular microhabitat being considered, and full names of abbreviated species are given in Table 2. Circled are sites’ groups as suggested by species assemblages and environmental variables.

Distribution and ecology of myxomycetes in Big Bend National Park, USA

consistent with community similarity results obtained using Horn’s and Morisita’s indices.

Relationship between myxomycetes and environmental variables Analysis of the pooled set of myxomycete data (37 samples, 46 species) using Detrended Correspondence Analysis (DCA) revealed that the composition of species assemblages at particular localities (study sites) in Big Bend National Park was influenced by a combination of factors related to differences in microhabitat, substratum richness and elevation. The differences in microhabitat and elevation were probably most strongly associated with the first axis, which accounted for 15 % of the variation (Fig 5AM, Table 3). Study sites and species assemblages associated with bark substrata were located in the high-elevation areas of the park and were generally clustered toward the right side of the ordination. In contrast, a substantial percentage of the species commonly associated with the ground litter and aerial litter microhabitats were located on the left. The second axis accounted for 8 % of the variation and was possibly most closely related to differences in substratum richness and microhabitat. Meanwhile, DCA results did not order study sites into any explainable clusters and it was impossible to indirectly attribute the observed pattern to any of the measured environmental variables. In general, environmental factors such as site moisture conditions, slope, aspect, soils, vegetation cover (biomass) and diversity increased with elevation. However, how all these factors interacted at the microhabitat level to influence the assemblages of myxomycetes present was not clear from the DCA biplots. For this reason, further evaluation of the data using Canonical Correspondence Analysis (CCA) was carried out. Ordination analyses using CCA and data for the common species associated with ground litter (27 species), ground bark (14), aerial bark (20) and aerial litter (26) suggest significant species–environment relationships. Conditional automatic unrestricted Monte-Carlo permutation tests and randomizations indicated that myxomycetes were significantly ( p ¼ 0.05) influenced by elevation (for the ground litter microhabitat), elevation and rock cover (aerial litter microhabitat) and substratum richness and rock cover (aerial bark microhabitat)

177

(Table 3, Fig 5). For the aerial bark microhabitat, strong correlations were noted between the first axis and substratum richness and elevation (r ¼ 0.9), whereas the second axis was most closely related to rock cover (r ¼ 0.9). Moreover, both the aerial litter and ground litter microhabitats were markedly correlated with elevation (r ¼ 0.9) while the second axis was correlated, albeit less strongly, with rockiness and substratum richness (r ¼ 0.7). Myxomycetes associated with the ground bark microhabitats were not significantly influenced by any of the environmental factors determined; however, the first axis was highly correlated with elevation (r ¼ 0.8), rockiness (r ¼ 0.9), vegetation cover (r ¼ 0.9) and substratum richness (r ¼ 0.7). Overall, the CCA triplots ordered sites and species into three major groups in response to elevation, rockiness, substratum richness, and vegetation cover. For both the aerial bark and ground bark microhabitats, the first group consisted of sites 3– 6, which were positively correlated with elevation, substratum richness and vegetation cover (Fig 5AB & GB, Fig 6). Myxomycetes associated with this group included A. cinerea, E. minutum, Paradiacheopsis solitaria, P. chrysosperma, Physarum bivalve, Physarum serpula, S. herbatica, Stemonitis fusca var. nigripes and Trichia favoginea. The second group comprised sites 1 and 11, which are located in low- to mid-elevation areas of the Chihuahuan Desert characterized by a rocky land surface. Species associated with these sites were B. melanospora, Comatricha elegans and Didymium anellus. The third group consisted of those sites (7, 10) situated in the riparian zones, where the more commonly associated myxomycetes included Badhamia panicea, Comatricha nigra and D. squamulosum. Some species associated with either the ground bark or aerial bark microhabitats were not consistently associated with any of the three groups. They included Comatricha pulchella, Comatricha laxa, P. depressa, P. notabile, P. pusillum and Willkommlangea reticulata. The ordering of particular aerial litter and ground litter microhabitat sites and species seemed to mimic those of bark microhabitats. However, it appeared that myxomycetes from both types of litter microhabitats responded more predictably to environmental factors. As was the case for bark microhabitats, it was possible to identify the three groups of study sites, with their associated species and environmental variables (Fig 5AL and GL, Fig 6). The first group consists of sites 2–6 and was highly correlated with

Table 3 – Summary results of DCA and CCA (eigen values, variances and Monte-Carlo permutation tests), including F and p values of environmental factors that significantly influenced myxomycetes % Variancesa

Microhabitats

Axis 1

Axis 2

Ground litter Aerial litterb Ground barkb Aerial barkb

20 24 47 29

13 12 21 26

All microhabitatsc

15

b

(36) (44) (47) (36)

8

(24) (23) (21) (33)

Eigen, F, p values

Environmental factors

Axis 1

First four axes

Conditional effects F, p values

0.29, F1.5, p ¼ 0.004 0.32, F1.9, p ¼ 0.01 0.41, F0, p ¼ 1 0.4, F0.8, p ¼ 0.3

F1.4, p ¼ 0.02 F1.4, p ¼ 0.05 F0, p ¼ 1 1.1, F1.4, p ¼ 0.09

0.36

0.89

Elevation F2.3, p ¼ 0.002 Elevation F2.6, p ¼ 0.002; Rockiness F1.7, p ¼ 0.03 – Substrate richness F2.3, p ¼ 0.008; Rockiness F2.4, p ¼ 0.02 –

a Variances of species data and species–environment relation (in parentheses). b Signify results of CCA. c Those of DCA analyses.

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G.G. Ndiritu et al.

Desert (Group 2)

Forest (Group1) ARCcin, 21

Riparian (Group 3)

PERdep, 22

Others, 32

GL

Others, 35

DIDmin, 4 COMpul, 4

PERdep, 19

BADgra, 18

DIDsqu, 15

PHYcom, 4

PHYcin, 5 PERchr, 17

LAMsci, 5

ARCcin, 2

ARCins, 4

DIDane, 17

PERdep, 3

COMlax, 6

PHYbiv, 6

DIDoch, 3

PERchr, 7

DIDane, 6 BADgra, 6 PHYstr, 7

PHYpus, 8

PERver, 8

STEher, 8

HEMmin, 7

PHYnot, 9 PHYpus, 10

DIDsqu, 10

PHYcom, 2 Others, 2 DIDdif , 2

WILret, 4

PERdep, 21

Others, 27

AL

DIDsqu, 12

STEfus, 3

Others, 20

PHYech, 4 PERchr, 4

BADgra, 29

PHYcom, 5 PHYcin, 5

PHYpus, 13

PERdep, 24

PERver, 5

PERchr, 3

DIDm in, 4 STEher, 5

PERcor, 6 DIDsqu, 6

DIDmin, 6

DIDoch, 9

PERdep, 24 Others, 29

PERver, 5

WILret, 1

TRIfav, 3

PHYbiv, 5 ARCcin, 7

DIDsqu, 8

DIDm in, 12

PHYnot, 6

DIDane, 3 PHYstr, 4

AB

PERchr, 3

COMlax, 5

PHYnot, 2

DIDane, 5

PHYpus, 5

PHYnot, 3 ARCcin, 23

PHYcin, 3 LICkle, 3 PHYdid, 4 PHYbiv, 4

PERdep, 3 ARCcin, 3

PHYser, 8

PERcor, 4 COMlax, 5 PARsol, 6

COMlax, 1 BADpan, 2

COMlax, 3

PERdep, 4

BADgra, 3 BADgra, 2 COMnig , 3

STEfus, 2 Others, 10

Others, 11

GB

PHYcin, 3

ARCcin, 20

PHYbiv, 3 ECHmin, 3

PHYpus, 2

DIDane, 4

PHYcom, 2

PERchr, 4

PHYcin, 2

PERchr, 17 PERcor, 2 ECHmin, 2 DIDoch, 2 COMmir, 2

BADgra, 2 COMele, 2

Fig 6 – Species assemblages associated with the three major land ecological zones (forest, desert and riparian) as suggested by CCA triplots for the four different microhabitats represented by aerial bark (AB), aerial litter (AL), ground bark (GB) and ground litter (GL). The full names of abbreviated species are given in Table 2; the value given after the species name is the number of records from that particular microhabitat.

high-elevation areas. Also, species from ground microhabitats were more closely associated with vegetation cover and substratum richness than those from aerial litter. Characteristic species included C. pulchella, E. minutum, Hemitrichia minor var. minor, Lamproderma scintillans, P. bivalve, P. serpula, Physarum spectabile, Physarum viride, S. herbatica and S. fusca var. nigripes. The second group consisted of those sites (1, 8, 11, and 12) that were situated in the low- to mid-elevation

sections of the park and were mostly influenced by rockiness. Common myxomycetes associated with these areas were C. laxa, D. anellus, Didymium ochroideum, Perichaena vermicularis, Physarum echinosporum, P. notabile, and W. reticulata. Sites from riparian zones (7, 9, and 10) made up the third group, where only a few common species occurred. These were D. squamulosum, Didymium difforme and P. cinereum. In both microhabitats, some species were unpredictable in

Distribution and ecology of myxomycetes in Big Bend National Park, USA

their occurrence, including A. cinerea, B. melanospora, B. panicea, D. minus, Perichaena corticalis, P. depressa, P. chrysosperma, Physarum bitectum, P. cinereum, P. compressum, P. didermoides, P. pusillum and P. straminipes.

Discussion Survey completeness The overall strategy of this study was to carry out a rapid myxomycete biodiversity survey of habitats and major substrata on which they are known to occur in Big Bend National Park in the manner described by Schnittler et al. (2002), using the techniques outlined in Spiegel et al. (2004), and later to assess the completeness of the survey. The sampling of major habitats (both micro- and macro-) in Big Bend National Park yielded 71 species, 29 of which were new records for the park. Surprisingly, an earlier 10-y survey of myxomycetes in the park (Tiffany & Knaphus 2001), based on visits made only during early fall and using both field collections and laboratory cultures, yielded 70 species, while McGraw (1968) recorded only 33 species. It is obvious that past surveys missed many species, some of which we found to be common and widespread. This was attributed to their failure to consider all microhabitats and habitats. Tiffany & Knaphus (2001) apparently directed much of their collecting effort to habitats in the Chisos Mountains, where they recorded 64 species as opposed to only 17 species for the Chihuahuan Desert. During the present study, the mountains and riparian zones along the Rio Grande River in the low elevation deserts were found to be rich in species. Comparison of our species list with the one compiled by Tiffany & Knaphus (2001), which is based largely upon specimens collected in the field, reveals some similarities and thus supports the idea that the use of moisture chamber cultures is an important technique for surveying myxomycetes in temperate deserts. Our sampling effort was not exhaustive, and several groups of species were not recorded. Some of the species missed included (1) wood-inhabiting (lignicolous) myxomycetes that rarely grow in laboratory culture, (2) myxomycetes that are associated strongly with some seasons of the year, (3) dung-inhabiting (coprophilous) myxomycetes as those substrata were not collected in our study, and (4) small-sized corticolous myxomycetes that are sometimes difficult to see using the moisture chamber technique were also missed. The first three problems can be addressed with repeated surveys of all microhabitats known to support myxomycetes in all major seasons by using both field and laboratory methods. Conversely, the small-sized corticolous myxomycetes can be studied easily using methods similar to those used to isolate protosteloid amoebae (Spiegel et al. 2007). Our sampling effort and the number of species recovered were comparable to a number of studies carried out in other arid areas of the world that used relatively similar methods (see Table 4 for references, areas studied and species recorded).

Microhabitats and community structure The few studies that have attempted to compare myxomycetes from different microhabitats have found strong preferences for

179

particular substrata. In the present study, 45 species were recovered from ground litter microhabitats, 44 from aerial litter, 39 from aerial bark and 37 species from ground bark, clearly indicating that all of the microhabitats were important for myxomycetes and that these results were similar to those from eight ecological studies carried out in several other regions of the world (Table 4). For example, in temperate arid regions of the Lower Volga River in Russia there was comparable species richness on bark substrata (37 species) but lower species richness in wood (23), ground litter (22) and dung (22) (Novozhilov et al. 2006). In a tropical forest in Ecuador, Stephenson et al. (2004) found more species on litter (56 species), followed by wood (34), the bark of living trees (14), inflorescences of large herbaceous plants (14) and epiphyllic liverworts growing on the leaves of understory plants (10). It is noteworthy that aerial microhabitats were the most productive. In a similar study in Costa Rica, 45 species were recorded on litter compared with 25 species from bark (Schnittler & Stephenson 2000). Unlike the situation in tropical forests, Stephenson (1989) found more species associated with bark than ground litter in temperate forests, and he recorded just five species from dung. Of the 168 species of myxomycetes reported from the Great Smoky Mountains National Park (Stephenson et al. 2001; Snell & Keller 2003), more than half occurred on aerial bark microhabitats. Although the numbers of species recovered from the four microhabitats were comparable, species compositions of the assemblages were different. Species assemblages were more similar for ground litter/aerial litter and aerial bark/ground bark than for ground bark/aerial litter and aerial litter/aerial bark. This dissimilarity was attributed to the variation in environmental conditions that occurs at the microhabitat level, and to differences in the local abundance of particular species as well as their dispersal abilities. We predict that species with high local abundances are widespread and likely to inhabit more microhabitats, although their colonizing ability is to a certain degree determined by their dispersal ability and microenvironmental conditions. Some of the species that occurred in high abundances in one or two microhabitats and colonized others with some regularity included A. cinerea, B. melanospora, D. anellus, D. squamulosum, E. minutum, P. chrysosperma, P. depressa, P. bivalve, P. cinereum, P. notabile, P. pusillum and S. herbatica. Several authors have suggested that the types of microhabitats available and the features of those microhabitats are more important than climatic factors in determining the distribution of corticolous myxomycetes (Eliasson 1991). A study of unicellular eukaryotes (Heino & Soininen 2006) indicated that their regional occurrence was primarily a reflection of habitat availability and to a lesser extent niche breadth and maximum size. Novozhilov et al. (2006) observed that although corticolous species were abundant and widespread, they were more specialized than the members of other ecological groups of myxomycetes. Some general statements have been made on the pH, substratum and microhabitat requirements of myxomycetes (e.g. Stephenson 1989). For example, most members of Stemonitales appear to prefer more acidic conditions when compared to members of the Physarales and Trichiales, whereas members of the Echinosteliales seem to have an affinity for moderately acidic substrata. In contrast, members of the Liceales generally occur over wide pH ranges. In any case, the general differences in species assemblages between litter

180

G.G. Ndiritu et al.

Table 4 – Occurrences and distribution of common myxomycetes in some temperate and tropical arid regions of the world Study area, altitude (m), localities, study period and country.

Sonoran Desert, Arizona, 910–1650, 3 plots. 4 mo, USA.1,2 Colorado Plateau, Colorado, 1400–2300, 1300 km transect, 2 wk, USA.2

Lower Volga River Basin, – 20–28, 220 sites, 1995–2004, Russia.3

State reserve, south – eastern Siberia, 500–1500, 8 mo (2003–2006), Russia.4

Mangyshlak Peninsula, Kazakhstan.5

Great Lake Basin, western Mongolia, 1088–3238, 98 sites in five vegetation types, Mongolia.6 Atacama Desert, 0–5000 m, 100 km transect (33 sites), 3 wk, Chile.7 Kajiado District, 600–2300, 15 sites, 1 wk, Kenya.8

Big Bend National Park, Texas, 560–1810, 12 sites 2 wk, USA.9

Surveys (FC, MC). Microhabitats (GL, GW, GB, AL, AB). Total species recorded (T). Species occurrences: abundant (A), common (C). FC, MC. T: 31 (FC: 25, MC: 8). A: BADmel, DIDere, PERcor, PHYstr. C: PROphl. FC, MC (GW, AB, GL, D). T: 93 (FC: 16, MC: 78). MC, A: ECHcol, LICpar, MACdec, PERqua, PERver, PHYdec. C: BADmel, COMlax, DIDdif, DIDdub, DIDmex, ECHcoe, ENEpap, LICden, LICnan, LICper, PHYleu, PHYnot. FC, MC (GW, AB, GL, D). T: 158 (FC: 105, MC: 44). A: ARCcin, BADspi, DIDdif, FULcin, PERcor, PERdep, PHYnot. C: COMlax, COMnig, DIDane, DIDsqu, DIDtra, PERchr, PERver, PHYcin, PHYdec. FC, MC (GW, AB, GL, D). T: 123 (FC: 76, MC: 65). A: ARCcin, CRIcan, DIDdif, ECHmin, HEMpar, LICtes, LYCepi, PARsol, PHYalb. C: COMnig, CRIvio, DIDsqu, FULsep, LICkle, LICope, LICpar, PARfim, PERver, STEaxi, TRIbot. FC, MC. T: 96. A: ECHcol, MACobl, PERver, PHYnot. C: ARCcin, ARCinc, COMnig, DIDane, DIDsqu, ECHarb, LICkle, PERcor, STEaxi, STEspl. MC (GW, AB, GL, D). T: 36. A: DIDane, DIDdif, ECHarb, ECHcol, PERdep, PERqua, PERver, PHYdec, PHYnot, C: ARCcin, BADapi, COMpul, DIDsqu, LICkle, PERchr, PHYdid. FC, MC (GW, GL, AB). T: 24. A: BADmel, DIDvac. C: COMlax, PERdep, PERver, PHYspe. MC (GL, GB, AL, AB). T: 37. A: ARCcin, COMlax, DIDane, PERchr, PERdep, PERver, PHYcin. PHYcom, PHYdid, PHYpus. C: COMten, MACobl, PHYser, PHYstr, STEfus. MC (GL, GB, AL, AB). T: 71. A: ARCcin, BADmel, DIDane, DIDsqu, PERchr, PERdep, PHYbiv, PHYpus. C: COMlax, DIDEchr, DIDmin, DIDoch, ECHmin, PERver, PHYcin, PHYcom, PHYnot, PHYstr, STEher.

Abbreviations of types of surveys – field collections (FC), moisture chambers (MC) and microhabitats considered – ground litter (GL), ground bark (GB), aerial litter (AL), aerial bark (AB) of living trees, ground wood (GW) and herbivore dung (D). Unless specified myxomycetes obtained during FC were obtained from GW. Most species presented above were obtained from GL, AB and D using moisture chamber technique. Full species names are: ARCcin, Arcyria cinerea; ARCinc, A. incarnata; BADapi, Badhamia apiculospora; BADmel, B. melanospora; BADspi, B. spinispora; COMlax, Comatricha laxa; COMnig, C. nigra; COMpul, C. pulchella; COMten, C. tenerrima; CRIcan, Cribraria cancellata; CRIvio, C. violacea; DIDEchr, Diderma chrondrioderma; DIDane, Didymium anellus; DIDdif, D. difforme; DIDdub, D. dubium; DIDere, D. eremophilum; DIDmex, D. mexicanum; DIDmin, D. minus; DIDoch, D. ochroideum; DIDsqu, D. squamulosum; DIDtra, D. trachysporum; DIDvac, D. vaccinum; ECHarb, Echinostelium arboreum; ECHcoe, E. coelocephalum; ECHcol, E. colliculosum; ECHmin, E. minutum; ENEpap, Enerthenema papillatum; FULcin, Fuligo cinerea; FULsep, F. septica; HEMpar, Hemitrichia pardina; LICden, Licea denudescens; LICkle, L. kleistobolus; LICnan, L. nannengae; LICope, L. operculata; LICpar, L. parasitica; LICper, L. perexigua; LICtes, L. testudinacea; LYCepi, Lycogala epidendrum; MACdec, Macbrideola declinata; MACobl, M. oblonga; PARfim, Paradiacheopsis fimbriata; PARsol, P. solitaria; PERchr, Perichaena chrysosperma; PERcor, P. corticalis; PERdep, P. depressa; PERqua, P. quadrata; PERver, P. vermicularis; PHYalb, Physarum album; PHYbiv, P. bivalve; PHYcin, P. cinereum; PHYcom, P. compressum; PHYdec, P. decipiens; PHYdid, P. didermoides; PHYleu, P. leucophaeum; PHYnot, P. notabile; PHYpus, P. pusillum; PHYser, P. serpula; PHYspe, P. spectabile; PHYstr, P. straminipes; PROphl, Protophysarum phloiogenum; STEaxi, Stemonitis axifera; STEfus, S. fusca; STEher, S. herbatica; STEspl, S. splendens; TRIbot, Trichia botrytis. Superscript numbers represent references: 1Blackwell & Gilbertson 1980, 1984; 2Novozhilov et al. 2003; 3Novozhilov et al. 2006; 4Kosheleva et al. 2008; 5Schnittler & Novozhilov 2000; 6Novozhilov & Schnittler 2008; 7Lado et al., 2007; 8Ndiritu unpubl. data; 9This study.

and bark substrata were significant and probably had more to do with overall microenvironmental conditions and other factors than simply differences in pH. Productivity (number of fruitings) of the more common species of myxomycetes varied considerably among different microhabitats. As a general observation, fruitings were largest in ground litter and aerial litter microhabitats, moderate for aerial bark and lowest in the ground bark microhabitat. B. melanospora was the single most abundant species in both the aerial litter and ground litter microhabitats, whereas E. minutum and P. notabile were the most abundant in the aerial bark and ground bark microhabitats. P. depressa was found abundantly in all of the microhabitats. This is in general agreement with studies in other parts of the world, where E. minutum was reported as one

of the most abundant species on bark in temperate forests (Stephenson 1989; Snell & Keller 2003). B. melanospora and P. straminipes were abundant on ground litter of members of the Agavaceae and Cactaceae in the Sonoran Desert of Arizona (Blackwell & Gilbertson 1980), whereas P. depressa, P. vermicularis and P. corticalis were frequent on the litter of desert plants in the Sonoran Desert of Arizona (Evenson 1961). Novozhilov et al. (2006) reported P. notabile as the most common species in an arid region in Asia. In contrast, the most frequently occurring species in the present study were not the same as those reported for arid areas of the Colarado Plateau (Novozhilov et al. 2003), where the most abundant species were Echinostelium colliculosum, Licea kleistobolus, Licea parasitica, Perichaena quadrata, P. vermicularis and Physarum decipiens. Similar differences in

Distribution and ecology of myxomycetes in Big Bend National Park, USA

species assemblages among arid regions have also been reported (Kosheleva et al. 2008; Novozhilov & Schnittler 2008). About 30 % (19 of the 64 species) known to occur commonly and abundantly in arid lands of the world were recorded in Big Bend National Park (Table 4), with Diderma chrondrioderma, D. ochroideum, P. bivalve, P. compressum and S. herbatica being reported for the first time as common species. Our hypothesis that higher levels of vegetation diversity would be accompanied by higher levels of myxomycete diversity was supported by the results of this study, in which species diversity indices were significantly correlated with vegetation cover and substratum richness. Riparian zones along the Rio Grande River in the Chihuahuan Desert, and forests and woodlands in the Chisos Mountains were especially species rich, implying that the availability of a diverse range of substrata in those habitats was a major factor determining species occurrence. Snell & Keller (2003) reported that species richness among different trees was comparable but that different tree species supported unique assemblages of myxomycetes, whereas Stephenson (1989) found that species richness and composition varied among tree species. Moderately acidic barks of trees such as Quercus and Cupressus had high species richness, whereas Pinus (with highly acidic bark) was poor in corticolous species (Stephenson 1989; Snell & Keller 2003).

Relationship between myxomycetes and environmental gradients There appear to be several environmental-complex gradients (sensu Whittaker 1972) that correspond to site-to-site differences in elevation/temperature/moisture conditions and the types of microhabitats associated with myxomycetes. Elevation, which positively influenced the myxomycetes associated with litter microhabitats, was also interpreted as a moisture gradient, whereas rockiness was perceived as being correlated with temperature. Substratum richness, which influenced aerial bark species, was interpreted to represent a combination of the intrinsic features (pH, texture and water holding capacity) of bark as a substrate. For instance, there was a strong correlation between bark pH and the distribution of some species. Species that display a high affinity for bark have been reported to make up a unique ecological assemblage, with a particular species characterized by narrow niche breadth (Novozhilov et al. 2006). In the present study, species consistently associated with bark included C. pulchella, E. minutum, P. bivalve, P. serpula, S. fusca var. nigripes and T. favoginea. Members of a second assemblage of species associated with the bark microhabitats included A. cinerea, P. solitaria, P. chrysosperma, P. serpula and S. herbatica, were more influenced by temperature and moisture conditions. The relationships between myxomycetes and environmental factors in the park were consistent with other findings. For example, the growth of P. straminipes appeared to be significantly inhibited by higher temperatures (>20  C), whereas the growth of B. melanospora and P. corticalis was least affected by high temperatures (Blackwell & Gilbertson 1984; Clark et al. 2003). In a Neotropical forest, Ogata et al. 1996 found significant correlations of species diversity and abundance with precipitation and temperature, while in another tropical forest, species assemblages from litter, wood and inflorescences

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were strongly influenced by pH (Stephenson et al. 2004). Similarly, Evenson (1961) recorded more species (52) in wet forests at high elevations compared to seven and 14 species in grasslands and desert shrubs, respectively, in Arizona. Unlike in bark, the distribution of species in aerial litter and ground litter microhabitats was more related to moisture conditions and temperature and to a lesser extent the pH of the substrate. Species that thrived well in cooler and wetter zones were C. pulchella, E. minutum, H. minor var. minor, L. scintillans, P. bivalve, P. serpula, P. spectabile, P. straminipes, P. viride, S. herbatica and S. fusca var. nigripes. Myxomycetes associated with rocky and arid areas included C. laxa, D. anellus, D. ochroideum, P. vermicularis, P. echinosporum, P. notabile and W. reticulata. A distinct assemblage of myxomycetes was made up by species that were widespread and occurred across the park, apparently not greatly influenced by any of the environmental factors considered in the present study. Examples included A. cinerea, B. melanospora, B. panicea, D. minus, D. squamulosum, P. corticalis, P. depressa, P. chrysosperma, P. bitectum, P. cinereum, P. compressum, P. didermoides, P. pusillum, and S. herbatica.

Conclusions The present study showed that desert landscapes and particularly their most favorable life-supporting habitats (e.g. riparian and mountain vegetation) can be exceedingly rich in myxomycetes. By considering all of the more important microhabitats, there were 29 new records for Big Bend National Park. Of the 71 species recorded in the park, eight (11 %) were abundant and ten (14 %) were common. Correlations were noted between species diversity and abundance of myxomycetes and elevation, slope, substratum richness, vegetation cover and rockiness. However, the assemblages of species associated with bark and litter were compositionally distinct. Litter-inhabiting species appeared to be more generalists, whereas bark-inhabiting species were more specialists. For the bark microhabitat, certain substratum characteristics (e.g. pH, texture and water holding capacity type) were suspected to be important in determining species assemblages, whereas environmental factors such as moisture conditions, temperature, and humidity were more important factors for assemblages associated with litter microhabitats. The surprisingly widespread distribution and overall abundance of some species in this temperate arid region during spring are intriguing and probably warrants further investigations. D. chrondrioderma, D. ochroideum, P. bivalve and S. herbatica had not been reported previously as occurring commonly in arid areas. Tiffany & Knaphus (2001) apparently did not encounter B. melanospora during their 10-y fall survey in the park, although in the present study the species was exceedingly abundant on decaying Opuntia pads in arid areas. Future studies might seek to elucidate the mechanisms or processes responsible for these patterns. For example, to what extent does season influence the composition of the assemblages of myxomycetes found in Big Bend National Park? The park is located in a subtropical-temperate transitional zone with relatively warm and cold conditions characteristic of different portions of the year. In theory, these conditions might allow the co-occurrence of both temperate and tropical

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species assemblages. The substantial number of species recorded in the Chihuahuan Desert challenges the notion that arid areas are poor in myxomycetes. It is possible that diversity ‘‘hot spots’’ for myxomycetes in the more favorable riparian and mountain habitats play a role of maintaining and/or reintroducing particular species throughout the region. In other eukaryotic microorganisms, the persistence of local populations and their abundance have been suggested to be important in determining regional occurrences (Soininen & Heino 2005). Another aspect that warrants investigation is how species assemblages change with an increase in distance from these diversity hot spots. Lastly, the predictable occurrences of a significant percent of globally abundant species in their suitable habitats/microhabitats offer an unique opportunity to test the two distribution models that have been proposed for eukaryotic microorganismsdubiquity (Finlay 2002) and moderate endemicity (Foissner 2006).

Acknowledgments This study was supported in part by a grant (DEB0316284) from the National Science Foundation, with logistical support supplied by Dr. Kimberly Smith of Biological Sciences at the University of Arkansas. The United States Department of the Interior through the National Park Service provided the study and collection permit (BIBE2005SCI0028). We wish to thank David Mitchell and Carlos Lado for their help with the identification of some species as well as Adam W. Rollins who read and many useful comments on the draft manuscript. Richard Stauffacher provided labels for specimens and organized species lists for uploading onto the Global Biodiversity Information Facility (GBIF) website.

Appendix. Supplementary material Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.funeco.2009.03.002.

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