D. Jean Lodge

Global diversity and geography of soil fungi

Introduction The kingdom Fungi is one of the most diverse groups of organisms on Earth, and they are integral ecosystem agents that govern soil carbon cycling, plant nutrition, and pathology. Fungi are widely distributed in all terrestrial ecosystems, but the distribution of species, phyla, and functional groups has been poorly documented. On the basis of 365 global soil samples from natural ecosystems, we determined the main drivers and biogeographic patterns of fungal diversity and community composition. Direct and indirect effects of climatic and edaphic variables on plant and fungal richness. Line thickness corresponds to the relative strength of the relationships between the variables that affect species richness. Dashed lines indicate negative relationships. MAP, mean annual precipitation; Fire, time since last fire; Dist. equator, distance from the equator; Ca, soil calcium concentration; P, soil phosphorus concentration; pH, soil pH. Rationale We identified soil-inhabiting fungi using 454 Life Sciences (Branford, CN) pyrosequencing and through comparison against taxonomically and functionally annotated sequence databases. Multiple regression models were used to disentangle the roles of climatic, spatial, edaphic, and floristic parameters on fungal diversity and community composition. Structural equation models were used to determine the direct and indirect effects of climate on fungal diversity, soil chemistry, and vegetation. We also examined whether fungal biogeographic patterns matched paradigms derived from plants and animals—namely, that species’ latitudinal ranges increase toward the poles (Rapoport’s rule) and diversity increases toward the equator. Last, we sought group-specific global biogeographic links among major biogeographic regions and biomes using a network approach and area-based clustering. Results Metabarcoding analysis of global soils revealed fungal richness estimates approaching the number of species recorded to date. Distance from equator and mean annual precipitation had the strongest effects on richness of fungi, including most fungal taxonomic and functional groups. Diversity of most fungal groups peaked in tropical ecosystems, but ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal ecosystems, and many fungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus). Consistent with Rapoport’s rule, the geographic range of fungal taxa increased toward the poles. Fungal endemicity was particularly strong in tropical regions, but multiple fungal taxa had cosmopolitan distribution. Conclusions Climatic factors, followed by edaphic and spatial patterning, are the best predictors of soil fungal richness and community composition at the global scale. Richness of all fungi and functional groups is causally unrelated to plant diversity, with the exception of ectomycorrhizal root symbionts, suggesting that plant-soil feedbacks do not influence the diversity of soil fungi at the global scale. The plant-to-fungi richness ratio declined exponentially toward the poles, indicating that current predictions—assuming globally constant ratios—overestimate fungal richness by 1.5- to 2.5-fold. Fungi follow similar biogeographic patterns as plants and animals, with the exception of several major taxonomic and functional groups that run counter to overall patterns. Strong biogeographic links among distant continents reflect relatively efficient long-distance dispersal compared with macro-organisms. Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework. Global metagenomics detects hotspots of fungal diversity and macroecological patterns and indicates that plant and fungal diversity are uncoupled. [Also see Perspective by Wardle and Lindahl] Assessing fungal diversity worldwide Fungi are hyperdiverse but poorly known, despite their ecological and economic impacts. Tedersoo et al. collected nearly 15,000 topsoil samples from 365 sites worldwide and sequenced their genomes (see the Perspective by Wardle and Lindahl). Overall, they found a striking decline in fungal species richness with distance from the equator. For some specialist groups though, diversity depended more on the abundance of host plants than host diversity or geography. The findings reveal a huge gap between known and described species and the actual numbers of distinct fungi in the worlds soils. Science, this issue 10.1126/science.1256688; see also p. 1052

Responses of Tree Species to Hurricane Winds in Subtropical Wet Forest in Puerto Rico: Implications for Tropical Tree Life Histories

JESS K. ZIMMERMAN,* EDWIN M. EVERHAM III,t ROBERT B. WAIDE,* D. JEAN LODGE,*? CHARLOTTE M. TAYLOR,t** and NICHOLAS V. L. BROKAW? *Terrestrial Ecology Division, University of Puerto Rico, PO Box 363682, San Juan, PR 00936, tSUNY College of Environmental Science and Forestry, Syracuse, NY 13210, USA, IDepartment of Biology, University of Puerto Rico, Rio Piedras, PR 00931, ?Manomet Observatory, Box 1770, Manomet, MA 02345, USA

LAND USE HISTORY, ENVIRONMENT, AND TREE COMPOSITION IN A TROPICAL FOREST

The effects of historical land use on tropical forest must be examined to understand present forest characteristics and to plan conservation strategies. We compared the effects of past land use, topography, soil type, and other environmental variables on tree species composition in a subtropical wet forest in the Luquillo Mountains, Puerto Rico. The study involved stems > 10 cm diameter measured at 130 cm above the ground, within the 16-ha Luquillo Forest Dynamics Plot (LFDP), and represents the forest at the time Hurricane Hugo struck in 1989. Topography in the plot is rugged, and soils are variable. Historical documents and local residents described past land uses such as clear-felling and selective logging followed by farming, fruit and coffee production, and timber stand im- provement in the forest area that now includes the LFDP. These uses ceased 40-60 yr before the study, but their impacts could be differentiated by percent canopy cover seen in aerial photographs from 1936. Using these photographs, we defined four historic cover classes within the LFDP. These ranged from cover class 1, the least tree-covered area in 1936, to cover class 4, with the least intensive historic land use (selective logging and timber stand improvement). In 1989, cover class 1 had the lowest stem density and pro- portion of large stems, whereas cover class 4 had the highest basal area, species richness, and number of rare and endemic species. Ordination of tree species composition (89 species, 13 167 stems) produced arrays that primarily corresponded to the four cover classes (i.e., historic land uses). The ordination arrays corresponded secondarily to soil characteristics and topography. Natural disturbances (hurricanes, landslides, and local treefalls) affected tree composition, but these effects did not correlate with the major patterns of species distributions on the plot. Thus, it appears that forest development and natural disturbance have not masked the effects of historical land use in this tropical forest, and that past land use was the major influence on the patterns of tree composition in the plot in 1989. The least disturbed stand harbors more rare and endemic species, and such stands should be protected.

ENDOPHYTIC FUNGI OF MANILKARA BIDENTATA LEAVES IN PUERTO RICO

Endophytic fungi were isolated from healthy leaves of Manilkara bidentata (Sapotaceae) collected in Puerto Rico. One leaf was collected from each of three trees. Four 5 X 20 mm panels were cut from each leaf, surface sterilized, cut into 50 1 X 2 mm pieces, and plated on malt agar. Petioles were cut into ten 1 mm segments. Fungi were isolated from 90%-95% of the leaf pieces and all of the pet- iole segments. Xylaria spp. were found in 73%-74% of the leaf pieces in two of the three leaves, but only 21% in the third leaf. Xylaria cf. multiplex, X. cf. ad- scendens, a member of the X. mellisii/X. arbuscula complex, and 20 other fungal species were isolated. Nineteen of the 22 species on leaf blades were found on at least two of the three leaves, but half of the 12 species in petioles were unique to one leaf. The 22 species islolated from leaf blades fit a lognormal dis- tribution. An estimated three to six species were not discovered, indicating that the 22 species found on leaf blades represented 79%-88% of the endophytic community.

Global diversity and distribution of macrofungi

Data on macrofungal diversity and distribution patterns were compiled for major geographical regions of the world. Macrofungi are defined here to include ascomycetes and basidiomycetes with large, easily observed spore-bearing structures that form above or below ground. Each coauthor either provided data on a particular taxonomic group of macrofungi or information on the macrofungi of a specific geographic area. We then employed a meta-analysis to investigate species overlaps between areas, levels of endemism, centers of diversity, and estimated percent of species known for each taxonomic group for each geographic area and for the combined macrofungal data set. Thus, the study provides both a meta-analysis of current data and a gap assessment to help identify research needs. In all, 21,679 names of macrofungi were compiled. The percentage of unique names for each region ranged from 37% for temperate Asia to 72% for Australasia. Approximately 35,000 macrofungal species were estimated to be “unknown” by the contributing authors. This would give an estimated total of 56,679 macrofungi. Our compiled species list does not include data from most of S.E. Europe, Africa, western Asia, or tropical eastern Asia. Even so, combining our list of names with the estimates from contributing authors is in line with our calculated estimate of between 53,000 and 110,000 macrofungal species derived using plant/macrofungal species ratio data. The estimates developed in this study are consistent with a hypothesis of high overall fungal species diversity.

Factors related to diversity of decomposer fungi in tropical forests

Recent studies suggest that host-preferences are common among certain groups of tropical fungal decomposers but rare in others, and sometimes occur where we least expect them. Host preferences among microfungi and ascomycetes that decompose leaf litter are common but usually involve differences in relative frequencies more than presence/absence, so their diversity may be loosely correlated with species richness of host trees. Strong host-specificity appears to be rare among wood decomposer fungi, whereas characteristics of their substrata and habitat are very important for this group. Anthropogenic disturbance predisposed a tropical forest to subsequent hurricane damage, and the resulting direct and indirect effects on host diversity and habitat heterogeneity were reflected in the decomposer fungal community more than sixty years after the original disturbance. While species richness of dictyostelid slime molds and functional diversity of their bacterial prey increased with disturbance, the more diverse microfungi and ascomycetes were apparently negatively affected by disturbance.

Hurricane effects on soil organic matter dynamics and forest production in the Luquillo experimental forest, Puerto Rico : results of simulation modeling

The forests and soils at Luquillo Experimental Forest (LEF), Puerto Rico, are frequently disturbed by hurricanes occurring at various frequencies and intensities. We have derived a forest version of the Century soil organic matter model to examine the impact of hurricanes on soil nutrient availability and pool sizes, and forest productivity in the tabonuco forest at Luquillo. The model adequately predicted aboveground plant production, soil carbon, and soil nitrogen levels for forest conditions existing before Hurricane Hugo. Simulations of Hurricane Hugo and of an historical sequence of hurricanes indicated a complex pattern of recovery, especially for the first 10 yr after the hurricanes. After repeated hurricanes, forest biomass was reduced, while forest productivity was enhanced. Soil organic matter, and phosphorus and nitrogen mineralization stabilized at higher levels for the LEF than for hurricane-free tabonuco forest, and organic soil phosphorus was substantially increased by hurricanes. Results from these simulations should be regarded as hypotheses. At present there is insufficient data to validate the results of hurricane model simulations.

SHORT-TERM EFFECTS OF HURRICANE GILBERT ON TERRESTRIAL BIRD POPULATIONS ON JAMAICA

Four months after Hurricane Gilbert we resampled 10 habitats that were sam- pled previously in December 1987. Overall, we found no change in the total number of species nor in the mean number of individual birds detected. The mean number of individuals declined in three montane habitats (cloud forest, pine plantation, and coffee plantation), where structural damage to tree trunks and branches was often severe, and trees were still defoliated. In the mountains, higher proportions of nectarivores and fruit ! seedeaters declined than insectivores. We found increased mean numbers of individuals in two lowland sites (wet limestone forest and mangroves), where structural damage to trees was also severe, but where new foliage was present. Mean numbers of individuals did not change in five other lowland habitats, despite varying levels of vegetation damage. Populations of several species declined in some habitats and increased in others, a pattern consistent with interhabitat migration. Population declines in montane habitats were related to diet, suggesting that Hurricane Gilberts greatest stress on Jamaicas montane bird populations occurred after its passage rather than during its impact. Frequent hurricanes may contribute to some of the commonly observed characteristics of the Caribbean avifauna. Received 5 March 1991, accepted 10 July 1991. IN SOME tropical regions, hurricanes occur with sufficient frequency to be important fac- tors in determining the structure and species composition of biotic communities (e.g. Wads- worth and Englerth 1959, Odum 1970). For bird populations in particular, hurricanes can have both direct and indirect effects (for recent re- view, see J. Wiley, unpubl. manuscript). Direct hurricane effects include death from exposure to high winds and rain (Kennedy 1970). Indi- rect effects of hurricanes on bird populations include destruction of food supplies (or nesting, roosting, and foraging substrates) by the storms high winds (Jeggo and Taynton 1980). Further- more, storm-weakened birds may be at greater risk to predation, particularly in the absence of vegetative cover or roosting sites for protection (Engstrom and Evans 1990). Hurricanes can dis- rupt normal migration patterns and, in some instances, change the geographic distributions of species (Thurber 1980). Following hurri- canes, humans may kill weakened birds and accelerate the rate of habitat destruction

Distribution and dispersal of Xylaria endophytes in two tree species in Puerto Rico

Xylaria species are common endophytes in tropical plants. It is not known, however, whether transmission of Xylaria occurs horizontally or vertically, whether individual Xylaria strains have wide host ranges or are host-specific, or how they are dispersed. We compared frequency of Xylaria endophytes in leaves and seeds of two tree species in Puerto Rico, Casuarina equisetifolia (Australian pine) and Manilkara bidentata (ausubo). These trees were chosen because they differ markedly in morphology, habitat, distribution, and origin. In C. equisetifolia Xylaria was significantly more frequent in leaves than in seeds. Xylaria was isolated from seeds of trees in inland parks, but never from seeds of trees growing on beaches. This suggests that vertical transmission of Xylaria may be possible but is not necessary for infection. In M. bidentata, Xylaria was isolated from 97% of leaves but was never isolated from seeds, suggesting that transmission is entirely horizontal. Seedlings raised in a greenhouse far from other M. bidentata trees had a level of Xylaria infection as high as seedlings in the forest, suggesting that inocula can come from other sources and endophytic strains are not host-specific.

Three host-specific Xylaria species

Xylaria axifera is apparently related to X. comosa, and although it is restricted to the petioles of plants in the Araliaceae, it apparently does not invade its host until after the petioles have fallen. The de? scription of X. axifera is emended to account for this host specificity and to include distinctive characteris? tics not provided in the original description. Two new, closely related Xylaria species that are only found on litter from trees in the Meliaceae (X meliacearum on petioles and X guareae on branches) are also de? scribed.