Aquatic Botany, 36 (1990) 255-262 255 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

A Study of the Vertical Zonation of Intertidal Fungi on Rhizophora apiculata at Kampong Kapok Mangrove , Brunei

KEVIN D. HYDE

Plant Pathology Branch, Department of Primary Industries, P.O. Box 1054, Mareeba, Qld. (Australia)

(Accepted for publication 29 September 1989)

ABSTRACT

Hyde, K.D., 1990. A study of the vertical zonation of intertidal fungi on Rhizophora apiculata at Kampong Kapok mangrove, Brunei. Aquat Bot., 36: 255-262.

Decayed samples of Rhizophora apiculata Blume were collected from various tidal levels in Kampong Kapok mangrove, Brunei and examined for higher marine fungi. Fifty-seven species were recorded; this represents the greatest number of intertidal fungi known from a single species of mangrove tree. Trichocladium cf. opacum (Corda) Hughes (17.75%) was most common, while Xylomyces sp. (13%), Cirrenalia pygmea Kohlm. (12.75%), Lulworthia sp. (12.75%), Lepto- sphaeria australiensis (Cribb & Cribb) Hughes (10.5%) and Thalassogena sphaerica Kohlm. & Volkm.-Kohlm. (8%) were also recorded frequently. The fungi were found to be vertically zonated; some were limited to the upper (e.g. Hypoxylon oceanicum Schatz, SavoryeUa lignicola Jones & Eaton) or lower (e.g. Antennospora quadricornuta (Cribb & Cribb) Johnson, Thalassogena sphaerica) levels, while only two (Cirrenalia pygmea and Lulworthia sp.) were present through- out the tidal range. The greatest number of species were collected from above mean tide (notably Level 3). Fungi with certain characteristics were also limited to vertical zones (e.g. those with carbonaceous walls only occurred above mean tide).

INTRODUCTION

Prop roots of mangrove trees (e.g. Rhizophora spp. ) may be submerged con- tinually, or periodically, depending on their topographic location. At the lower levels, underground roots may become exposed as a result of erosion, and so are continually submerged except during very low tide. At the upper levels, prop roots are only submerged for short periods during high tides, and a gra- dation of submergence/exposure times occurs between these two extremes. The prop roots in the intertidal zone may die or become damaged, and are colonized by intertidal fungi and other organisms (e.g. bacteria, marine borers).

Vertical zonation of marine organisms in mangrove stands (e.g. algae, mol-

0304-3770/90/$03.50 © 1990 Elsevier Science Publishers B.V.

256 K.D. HYDE

luscs) has long been recognized (Hutchings and Saenger, 1987). However, it has yet to be established if it occurs for marine fungi. Kohlmeyer (1969), Kohl- meyer and Kohlmeyer (1979) and Aleem (1980) found little evidence of ver- tical zonation, while Hyde and Jones (1988) observed that some fungi tended to occur consistently at certain levels (e.g. Aigialus grandis and Caryosporella rhizophorae at the mid-littoral level). Hyde and Jones (1988) also found that the greatest species diversity occurred at the mid-littoral level. However, the tidal ranges and the intertidal levels were not defined.

Studies using defined intertidal zones were carried out by Hyde (1988). He was able to show that with Rhizophora spp., some fungi were limited to specific intertidal zones (e.g. lower level: Humicola alopallonella and Trichocladium cf. opacum), while others were distributed throughout the tidal range (e.g. Cir- renalia pygmea and Halocyphina villosa). Hyde (1988) suggested that partic- ular fungi may be best adapted for growth and reproduction at a particular intertidal zone, and may therefore be sampled more frequently at that level. In this paper the results of a study of the intertidal fungi from a single host spe-

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ZONATION OF FUNGI ON RHIZOPHORA APICULATA 257

cies, Rhizophora apiculata Blume, are presented. Fungi were collected from four defined intertidal levels, and they provide new data on the vertical zona- tion of these fungi.

MATERIALS AND METHODS

Prop roots and exposed subterranean roots of Rhizophora apiculata were collected from the intertidal zone of Kampong Kapok mangrove, Brunei, dur- ing the period January to May 1987. A small frontal s tand on a steep eroded bank was selected, so that sampling at all levels was possible. Furthermore, at this site, physical factors (e.g. salinity, soil type) were less variable throughout the transect. Trees in the stands were mostly of R. apiculata, with a small number of Xylocarpus granatum Koenig. Selected samples were decayed, but still a t tached to the host tree. This ensured all were from R. apiculata and that the decay-causing organisms had developed at a specific vertical level. One hundred samples were collected from each of four tidal levels (illustrated in Fig. 1 and Table 1 ), and examined for the presence of intertidal fungi. Salini- ties and water temperatures were recorded throughout the study and were 16- 25%o and 27-31 ° C, respectively. Voucher slides of all the fungi collected in this s tudy were prepared and are held in the author 's herbarium.

RESULTS

Fifty-seven species of higher fungi were collected at Kampong Kapok man- grove from 400 intertidal mangrove samples (Table 2). Most common was Trichocladium cf. opacum (17.75% of samples), while Xylomyces sp. (13%),

TABLE 1

Details of collections

Level Range Notes

1 0.2-0.8 m

2 0.8-1.4 m

3 1.4-2.0 m

4 2.0-2.6 m

Continually submerged except for short periods during spring tides; constantly waterlogged

Mostly submerged. Exposed most days for varying times; samples were mostly waterlogged with rare superficial drying

Mostly exposed. Submerged most days for varying periods. Superficial drying of samples occurred during low tides

Submerged for periods during spring tides. Samples were superficially dry for long periods

Highest tide during 1987=2.7 m; lowest=0.1 m {from Anon, 1987). Temperature=27-32°C. Salinity = 16-25%o.

258 K.D. HYDE

TABLE2

Vertical distribution of intertidal fungi from prop roots and subterranean roots of Rhizophora apiculata from Kampong Kapok mangrove, Brunei 1. The figures show the percentage of occur- rence in the samples per tidal level

Fungi Level Taxonomic group

1 2 3 4

Swampomyces cf. armeniacus Kohlm. & Voklm. Phoma sp. Leptosphaeria sp. Trichocladium sp. Dictyosporiumpelagicum (Linder) Hughes Hypoxylon oceanicum Schatz Ascomycete sp. Savoryella lignicola Jones & Eaton Halosarpheia v iscosa (Schmidt) Shearer & Crane Dactylospora haliotrepha (Kohlm.) Hafellner 5 Trematosphaeria lignatilis Kohlm. 2 Acrocordiopsis patilii Borse & Hyde 2 Hypophleoda rhizospora Hyde & Jones 5 Marinosphaera mangrovei Hyde 4 Rhizophila marina Hyde & Jones 1 Cucullospora mangrovei Hyde & Jones 1 Massarina velatospora Hyde & Borse 2 Halosarpheia marina (Cribb & Cribb) Kohlm. 2 12 Hydronectria tethys Kohlm. & Kohlm. 3 Leptosphaeria cf. avicenniae, Kohlm. & Kohlm. 4 Halosarpheia ratnagiriensis Patil & Borse 7 Phialophorophoma cf. litoralis Linder 9 Aigialus grandis Kohlm. & Schatz 11 CaryosporeUa rhizophorae Kohim. 17 Leptosphaeria australiensis (Cribb & Cribb) Hughes 2 25 Phomopsis sp. 1 Halosarpheia fibrosa Kohlm. & Kohlm. 1 Belizeana tuberculata Kohlm. & Volkm. 1 Torpedospora radiata Meyers 1 Aigialus parvus Schatz & Kohlm. 1 Trichocladium achrasporum (Meyers & Moore ) Dixon 4 Passeriniella savoryeUopsis Hyde & Mouzouras 2 Trematosphaeria sp. 3 Didymosphaeria enalia Kohlm. 1 3 Aniptodera sp. 3 Lulworthia sp. ( spores 340-490 ~m) 2 7 1 Lulworthia grandispora Meyers 3 13 Ophiodeira monosemeia Kohlm. & Volkm.-Kohlm. 1 2 Bathyascus grandisporus Hyde 3 4 Humicola alopaUonella Meyers & Moore 2 2 Lignincola laevis H~ihnk 3 3

4 5

15 4 22 2 5

11 4 4

10 7 1 1 2 9 2 3 1 2 2 1

15

1 U

1 C 3 L 4 H

H

U U U U L L L

U U U U L

U U L U C L L L C U L U L H L L

4 L

U 1 U

U U U H U

ZONATION OF FUNGI ON RHIZOPHORA APICULATA

TABLE 2 (continued)

259

Fungi Level

1 2 3 4

Taxonomic group

Cirrenalia tropicalis Kohlm. 3 3 H Cirrenaliapygmea Kohlm. 4 19 27 1 H Aniptodera mangrovei Hyde 2 2 U Lulworthia sp. (spores 220-335/~m) 4 30 15 U Xylomyces sp. 13 30 9 H Cirrenalia pseudomacrocephala Kohlm. 5 5 4 H Manglicola guatemalensis Kohlm. & Kohlm. 1 L Periconia prolifica Anast. 7 1 2 B Halocyphina villosa Kohlm. & Kohlm. 18 6 U Thalassogena sphaerica Kohlm. & Volkm.-Kohlm. 44 14 H Trichocladium cf. opacum (Corda} Hughes 27 H Bactrodesmium linderi (Crane & Shearer} 1 H Palm & Stewart Lignincola tropica Kohlm. 1 U Lulworthia sp. (spores 150-170 ~m) 1 U Etheirophora blepharospora (Kohlm. & Kohlm. } 1 U

Kohlm. & Volkm.-Kohlm. Antennospora quadricornuta (Cribb & Cribb) 3 U

T.W. Johnson

Classification: B, basidiomycete; C, coelomycete; H, hyphomycete; L, loculoascomycete; U, uni- tunicate ascomycete. 1Fungi are ranked in order of their affinity towards the tidal levels: those at the top have affinities towards the higher level sampled (level 4 }, those at the bottom have affinities towards the lower level sampled (level 1 ). The middle ranked species have affinities for the mid-mangrove levels or occur at more than one level.

Cirrenalia pygmea (12 .75%), Lulworthia sp. ( spore range 220-335 ~ m ) (12 .25%), Leptosphaeria australiensis (10.5%) a n d Thalassogena sphaerica (8%) were also c o m m o n .

In Tab l e 2 the fungi are r a n k e d in o rder of t he i r a f f in i ty t owards t he t ida l levels: those a t the t op h a v e af f in i t ies t owa rds t he h igher t idal level (4) a n d t hose a t the b o t t o m have af f in i t ies t o w a r d s the lower t ida l level (1) . T h e mid- d l e - r a n k e d species e i the r have af f in i t ies for t he m i d - m a n g r o v e levels or oc- cu r red in m o r e t h a n one level. T h e t a x o n o m i c groups to which the fungi be long are also shown.

T h e n u m b e r of fungi r eco rded a t each level are: Leve l 1, 15 species; Leve l 2, 18 species; Leve l 3, 41 species; Leve l 4, 28 species. T h e g rea t e s t d ivers i ty oc- cu r red a t Leve l 3. T w e n t y - t h r e e species were conf ined to a single level, while a n o t h e r 25 occupied two ad j acen t levels. On ly seven species (Ci r rena l ia pseu-

260 K.D. HYDE

domacrocephala, Didymosphaeria enalia, Halocyphina viUosa, Halosarpheia marina, Leptosphaeria australiensis, Lulworthia sp. (spore range 220-335/~m), Xylomyces sp. ) occurred in three out of four levels. Cirrenaliapygmea and Lul- worthia sp. (spore range 340-490/~m) were distributed throughout the tidal range.

The intertidal zone examined and the distribution of fungi with certain char- acteristics (e.g. wall structure, type of spore release) are illustrated in Fig. 1. In the upper levels (3,4), all higher taxonomic groups were represented. The fungi present included those with immersed (e.g. Halosarpheia ratnagiriensis) and superficial (e.g. Caryosporella rhizophorae) ascocarps, those with coria- ceous (e.g. Savoryella lignicola) and carbonaceous (Aigialus grandis) walls, and those with active (e.g. Hypoxylon oceanicum) and passive spore release (e.g. Halosarpheia viscosa). Fungi with active spore release and with carbon- aceous walls were confined to the upper levels. Many species also had coloured (e.g. Rhizophila marina) rather than hyaline ascospores. Fungi with appen- daged ( Halosarpheia viscosa ), ornamented/sticky ( Caryosporella rhizophorae ) and smooth-walled (Hypoxylon oceanicum) ascospores were also present.

At the lower levels, all higher groups (except the coelomycetes) were rep- resented. Ascocarps were superficial (e.g. Manglicolaguatemalensis), but mostly immersed (e.g. Lignincola tropica); fruiting body walls were mostly coriaceous or membranous (e.g. Aniptodera mangrovei); spore release where known was passive (e.g. A ntennospora quadricornuta); and ascospores were mostly hya- line (e.g. Thalassogena sphaerica). Unitunicate ascomycetes and deuteromy- cetes were more common than loculoascomycetes. Fungi with appendaged (e.g. Antennospora quadricornuta ) , ornamented/sticky (e.g. Didymosphaeria ena- lia) and smooth-walled (e.g. Thalassogena sphaerica) ascospores were present.

DISCUSSION

Vertical zonation of intertidal fungi found in mangroves is evident, contrary to published reports (Kohlmeyer, 1969; Kohlmeyer and Kohlmeyer, 1979; Aleem, 1980). In this study on Rhizophora apiculata, most fungi were confined to one or two intertidal levels and occupied a relatively small vertical zone. Very few fungi were more widely distributed and only two were found through- out the tidal range. These results confirm those from a previous study on Rhi- zophora spp., in Brunei (Hyde, 1988), and observations in Malaysia (Jones and Tan, 1987) and the Philippines (Jones et al., 1988).

In this study, the greatest diversity of intertidal fungi (41 species) occurred above mean tide level, at Level 3 (Table 2). Hyde (1988) also found that the greatest diversity of species occurred here (at middle level). Above the mean tidal level, samples are submerged daily for varying periods and dry superfi- cially during low tide. The tidal changes may cause abrupt fluctuations in the environmental conditions (i.e. pH, salinity, osmotic pressure, temperature, UV

ZONATION OF FUNGI ON RHIZOPHORA APICULATA 261

irradiation). As a result, a greater range of ecological habitats may be available, so accounting for the higher species diversity.

The most common fungi found at each level in this study differed from level to level with little overlap (when those fungi with a broad distribution, e.g. Leptosphaeria australiensis, are excluded). The results confirm, in part, those of Hyde (1988). No other data are available for comparison. There were only nine intertidal fungal species with a broad distribution.

Kohlmeyer (1986) noted that most of the ascomycetes found on intertidal parts of mangrove trees were characterized by carbonaceous ascocarps, thick- walled, bitunicate asci, and a well developed interascicular tissue. In this study, there were eight ascomycetes with the above characteristics (e.g. Caryosporella rhizophorae and Hypoxylon oceanicum), seven bitunicate ascomycetes with immersed or erumpent non-carbonaceous ascocarps (e.g. Leptosphaeria aus- traliensis and Massarina velatospora) or superficial soft-walled ascocarps (e.g. Manglicola guatemalensis), and 27 unitunicate ascomycetes (e.g. Cucullospora mangrovei and Halosarpheia ratnagiriensis). The role of the unitunicate as- comycetes is therefore great, particularly above the mean tidal levels (Levels 3,4) where 14 loculoascomycetes, 22 unitunicate ascomycetes and 11 deutero- mycetes were recorded. Savoryella lignicola was most common (on 22% of sam- ples) at Level 4, while at Level 3 Lulworthia species were common (13-15%). At Level 4, seven of the nine most frequently collected fungi were unitunicate ascomycetes, while at Level 3, five out of 12 were unitunicates.

Kohlmeyer (1986) also stated that members of the class ascomycetes with unitunicate, dissolving asci grow mostly below the loculoascomycetes in areas that never dry out and that bear other delicate marine organisms. In this study, the most common group below mean tide were the ascomycetes with unituni- cate, dissolving asci and the hyphomycetes. Only three loculoascomycetes (e.g. Manglicola guatemalensis and Leptosphaeria australiensis ) occurred here. Seven unitunicate ascomycetes with dissolving asci (e.g. Antennospora quadricor- nuta and Bathyascus grandisporus) and six unitunicate ascomycetes where the method of spore dispersal is unknown (e.g. Thalassogena sphaerica and Anip- todera mangrovei) were present.

The study confirms in part the observations of Kohlmeyer (1986), while the differences may be due to tidal range. Kohlmeyer (1986) states that in the tropics the tidal range is usually not more than 0.1-0.5 m, whereas in this study it was 2.6 m. A more defined pattern of distribution may result from a greater tidal range. Furthermore, extent of colonization may be involved. This study compares species identified on samples and does not take into account the extent of colonization of one or more species on a single sample. However, a correlation between frequent colonizers and those fungi with large numbers of fruiting bodies was noted.

The data presented in this paper highlight the intertidal fungi involved in the colonization of dead Rhizophora apiculata wood and illustrate the vertical

262 K.D. HYDE

zonation of these fungi. However, although wood samples were attached to the host tree, they had undergone sufficient decay to enable detachment by hand. The fungi recorded will therefore reflect the state of decay of the samples, and early colonizers (e.g. Capillataspora corticola Hyde, Didymosphaeria enalia ) may be absent or recorded in lower numbers than if weakly decayed wood were selected.

ACKNOWLEDGEMENTS

I am grateful to Professor E.B.G. Jones of Portsmouth Polytechnic for his continued support and to Dr. Renos Mouzouras for commenting on the manuscript.

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Hutchings, P. and Saenger, P., 1987. Ecology of Mangroves. University of Queensland Press, St. Lucia, 388 pp.

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237-250. Kohlmeyer, J., 1986. Ascocratera manglicola gen. et sp. nov. and key to the marine loculoasco-

mycetes on mangroves. Can. J. Bot., 64." 3036-3042. Kohlmeyer, J. and Kohlmeyer, E., 1979. Marine Mycology. The Higher Fungi. Academic Press,

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