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BRIEF RESEARCH REPORT
published: 04 April 2022
doi: 10.3389/ffunb.2022.869689
Frontiers in Fungal Biology | www.frontiersin.org 1April 2022 | Volume 3 | Article 869689
Edited by:
Li-Wei Zhou,
Institute of Microbiology (CAS), China
Reviewed by:
Young Woon Lim,
Seoul National University, South Korea
Genevieve Gates,
University of Tasmania, Australia
Tom May,
Royal Botanic Gardens
Victoria, Australia
Gang Wu,
Kunming Institute of Botany
(CAS), China
*Correspondence:
Jeffery K. Stallman
jstallma@purdue.edu
Specialty section:
This article was submitted to
Fungal Genomics and Evolution,
a section of the journal
Frontiers in Fungal Biology
Received: 04 February 2022
Accepted: 09 March 2022
Published: 04 April 2022
Citation:
Stallman JK and Robinson K (2022)
Importance of Seasonal Variation in
Hawaiian Mushroom
(Agaricomycetes) Basidiomata
Production for Biodiversity Discovery
and Conservation.
Front. Fungal Biol. 3:869689.
doi: 10.3389/ffunb.2022.869689
Importance of Seasonal Variation in
Hawaiian Mushroom
(Agaricomycetes) Basidiomata
Production for Biodiversity Discovery
and Conservation
Jeffery K. Stallman 1
*and Kyra Robinson 2
1Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, United States, 2Department of Biology,
University of Hawaii at Hilo, Hilo, HI, United States
The Hawaiian Islands have a relatively well-known funga for a tropical location, yet
there are over 400 species of mushrooms (Agaricomycetes) in the archipelago that
remain to be documented. Importantly, the International Union for Conservation of Nature
(IUCN) recently evaluated six mushrooms endemic to the islands as threatened with
extinction. To improve detection of mushrooms for biodiversity discovery and better
monitor threatened species in the archipelago—where many localities lack strong annual
precipitation patterns associated with an obvious season for increased mushroom
basidiomata production—we examined the phenology of Hawaiian mushrooms. Monthly
richness was determined from a literature review and abundance from online data
repositories. Phenological patterns were separately explored for native species and
differing elevation and annual precipitation categories. Despite relatively consistent
monthly temperatures and areas with regular monthly rainfall, we found Hawaiian
mushrooms generally exhibit uneven temporal patterns in basidiomata production:
richness and abundance are generally highest in January and lowest from February
to April, then usually increase from May to July and remain at elevated levels through
December. This pattern does not occur when considering native species richness only,
nor when examining abundance data stratified by elevation and annual rainfall categories.
Increased monthly basidiomata abundance in low elevation (<1,000 m), dry (<1,000 mm
rainfall/year) locations on O‘ahu and low, mesic (1,000–2,500 mm rainfall/year) locations
on O‘ahu and Kaua‘i are positively correlated with increased monthly rainfall. Phenology
of macrofungal sporocarp production should potentially be included in species threat
assessments by the IUCN to increase detection via traditional surveying methods.
Keywords: endangered species, fungi, Hawai’i, Hygrophoraceae, Pacific
Stallman and Robinson Seasonality of Hawaiian Mushrooms
INTRODUCTION
Biodiversity discovery of the organisms occurring on earth is
ongoing. Lower estimates suggest hundreds of thousands of
species still lack formal scientific description (Costello et al.,
2012), while others estimate millions of undescribed species
within single taxa, such as Arthropoda (Stork, 2018). At the
same time, species on earth are facing numerous threats to
their existence as many argue earth’s biota has entered a
sixth mass extinction event, calling for renewed conservation
efforts (Ceballos et al., 2015). Fungi, often overlooked in this
conversation, have recently been recommended to be included
in global conservation goals along with plants and animals (Cao
et al., 2021; Gonçalves et al., 2021). They are one of the groups of
organisms with the most biodiversity yet to be discovered, with
around 135,000 species currently known (Hibbett et al., 2016) out
of an estimated 2.2–6.0 million (Taylor et al., 2014; Hawksworth
and Lücking, 2017).
Although recently receiving more recognition, the prior
exclusion of fungi from these discussions is likely because
the majority are microscopic and often undetectable,
except through microbial isolation (although many are not
culturable with current techniques) or molecular methods.
Despite this, some groups such as the class Agaricomycetes
(Basidiomycota) are predominantly composed of species that
form macroscopic reproductive structures and are considered
one of the best-known fungal groups (Kalichman et al.,
2020). Most Agaricomycetes basidiomata are recognized
as common macrofungi (agarics, boletes, puffballs, corals,
polypores, etc.), and therefore are a large proportion of the
basidiomata humans interact with for food, recreation, or
cultural activities.
Large amounts of data, including life history and phenology
information, are required to find mushrooms, evaluate their
conservation status, and continue to monitor populations.
Having these data provides higher chances of detecting these
cryptic organisms, which other than persistent, perennial species,
undergo most of their lifecycle as microscopic hyphae immersed
in a substrate. For groups such as the Agaricomycetes that form
macroscopic reproductive structures, timing of surveys is vital to
increase detection (Halme and Kotiaho, 2012).
In 2017 and 2019, the International Union for Conservation of
Nature (IUCN) evaluated six endemic Hawaiian Agaricomycetes
species and found that four were vulnerable and two endangered
(IUCN, 2021). Phenological data could help with monitoring
known populations of threatened species over time, such as
the endangered Hygrocybe noelokelani (Figure 1A), and assist in
planning surveys for finding new populations of these species.
Additionally, although the Hawaiian Islands likely have one
of the best-known tropical funga among Agaricomycetes, with
over 600 species known, an estimated 450 species in this group
remain to be documented from the islands (Mueller et al.,
2007). Formal descriptions and naming of documented species,
such as a Cystolepiota sp. from Hemmes and Desjardin (2002)
(Figure 1B), are needed in addition to exploration for unknown
species lacking any documentation. Therefore, phenological data
may help with continued biodiversity discovery in the Hawaiian
FIGURE 1 | Hygrocybe noelokelani, an endemic, endangered Hawaiian
mushroom species. Photograph by Amy Durham (A). Endemic, undescribed
Cystolepiota sp. sensu Hemmes and Desjardin (2002) (B).
Islands, where an estimated 80% of native Agaricomycotina
species are endemic (Mueller et al., 2007).
While patterns exist in other regions explaining when
“mushroom season”—i.e., when basidiomata are most diverse
and abundant—occurs, this is often anecdotal and based on
cultural practices or correlated with increased seasonal rainfall
or temperature (Arnolds and Jansen, 1992; Chacón and Guzmán,
1995). In the Hawaiian Islands, seasonal rainfall variation is low
in many areas, particularly wet (>2,500 mm/year) locations, and
there is no clear monsoon/dry season dichotomy as in other
tropical locations (Giambelluca et al., 2013). Temperatures are
above freezing year round except at very high elevations, and
Hawaiian cultural practices related to fungi, such as a season
for foraging mushrooms, have not been recorded (Hemmes and
Desjardin, 2002).
The phenology of Hawaiian Agaricomycetes has had limited
study. Hemmes and Desjardin (2002) stated that the best time
to find mushrooms is from July through January. Based on a
3-year study of the genera Pholiota (1 species), Hygrocybe (7
species), and Rhodocollybia (1 species) occurring in montane
forest environments, these authors found increased abundance
of basidiomata from July to December. Stallman (2019) found
the highest species richness was from May to January among
38 primarily non-native mushrooms in the family Agaricaceae.
Non-native mushrooms are common in disturbed habitats in
the Hawaiian Islands and usually associate with non-native
plant communities.
To help determine when surveys should occur by
conservationists, taxonomists, or community scientists for
monitoring known species and continued biodiversity discovery,
we investigated the best months of the year for increased
basidiomata richness and abundance by performing a literature
review and aggregating observation and collection data
available in online databases. We examined seasonality based
on average monthly temperature and rainfall separately for
Frontiers in Fungal Biology | www.frontiersin.org 2April 2022 | Volume 3 | Article 869689
Stallman and Robinson Seasonality of Hawaiian Mushrooms
native (indigenous) species only, and under different elevation
(lowland, montane, subalpine/alpine) and annual rainfall (dry,
mesic, wet) categories.
We hypothesized, following Hemmes and Desjardin (2002)
and Stallman (2019), that Hawaiian Agaricomycetes species
would show seasonal patterns in richness in abundance: both
would increase in May, June, or July, and remain elevated
through January before declining in February, irrespective of
average monthly rainfall and temperature, native or non-native
origin, and annual rainfall and elevation categories.
METHODS
The Hawaiian Archipelago
The Hawaiian Islands are a tropical, oceanic archipelago
consisting of eight current high islands (Hawai‘i, Kaho‘olawe,
Kaua‘i, L¯
ana‘i, Maui, Moloka‘i, Ni‘ihau, and O‘ahu) in the
northern Pacific Ocean. The islands are isolated from the closest
land mass, North America, by more than 3,500 km, and have
high elevation and rainfall heterogeneity between and within
islands. For example, on Hawai‘i Island, average rainfall varies
from <300 mm/year in Kawaihae to >7,500 mm/year at the
Makahanaloa rain gauge, and average annual temperature varies
from 24◦C in Kawaihae at sea level to 4◦C on Maunakea at >
4,000 m. In this study, the islands of Ni‘ihau and Kaho‘olawe
were excluded from all analyses due to lack of environmental
data and historically few collections (e.g., one meeting our criteria
from Ni‘ihau; zero from Kaho‘olawe for online abundance data).
Additional information on the islands included in this study are
available in Supplementary Table 1.
Richness Analysis
For our richness analysis, we first determined all Agaricomycetes
species known to occur in the Hawaiian Islands based on
authoritative sources. We then tabulated which month(s)
basidiomata of each species were reported in, and additional
environmental and life history data from these same sources.
The species list of Hawaiian Agaricomycetes was tabulated
from an unpublished list of Hawaiian Agaricomycotina
compiled by Drs. Dennis Desjardin and Don Hemmes from
∼1992 to 2007 and used by Mueller et al. (2007) for their
analysis of Hawaiian and global macrofungal biodiversity. We
checked primary literature, field guides, aggregated checklists,
MyCoPortal.org, and GenBank to verify each species on this
list occurred in the Hawaiian Islands, and added species
documented since 2007, or those missing. To be included, a
reference needed to explicitly state the species occurred in the
islands; environmental sequencing studies were not considered.
Species documented with incontrovertible DNA evidence and
metadata were included, even if unpublished (e.g., Psilocybe
cyanescens). Mycobank (Crous et al., 2004) and IndexFungorum
(www.indexfungorum.org) were used to update fungal names
and primary literature was consulted in case of disagreement.
Names were compiled at the species level without consideration
for infraspecific variation (e.g., subspecies or varieties).
For species on the list, months in which basidiomata
were found, different islands they were found on, origin as
native (indigenous to the Hawaiian Islands; not inferred to
be established via human-mediated dispersal) or non-native
(inferred to be established via human-mediated dispersal), and
elevation and rainfall information were recorded. To determine
a species origin as non-native or native we followed statements
in the literature when available or inferred this information
from its association with solely native vegetation or habitats. We
used a conservative approach, not assigning species to native
origin in ambiguous situations in which the species occurs in
both native and non-native habitats, or mixed vegetation, unless
additional evidence existed. Rainfall and elevation information
for each island were compiled based on Hawaiian habitat zones
by elevation (lowland <1,000 m, montane 1,000–2,000 m, and
subalpine/alpine >2,000 m) and rainfall (wet >2,500 mm, mesic
1,000–2,500 mm, and dry <1,000 mm) similar to Gagné and
Cuddihy (1999) using the Rainfall Atlas of Hawai‘i (Giambelluca
et al., 2013) and web resources (https://www.freemaptools.com/
elevation-finder.htm) based on reported collection locations. We
used a liberal approach for environmental variables, allowing
values approximately between two elevation or rainfall categories
to be included in both as some location information is not
specific (e.g., “Honolulu” or “slopes of Mauna Kea”) and could
encompass multiple zones. Additionally, the Hawaiian Islands
are known for steep environmental gradients where rainfall can
quickly change. We note that temperature throughout the year
in the islands, like other tropical locations, is relatively stable and
the largest temperature swings generally come from daily cycles
as opposed to annual cycles (Hartshorn, 2013). As elevation
increases, average air temperatures decrease (Giambelluca et al.,
2014).
Abundance Analysis
For our abundance analysis, we first obtained online observation
and/or collection records of Hawaiian fungi identified to the class
Agaricomycetes (whether to species, or a higher level), then used
their associated geospatial information to extract environmental
metadata. We searched for collections and/or observations of
Agaricomycetes species in the Hawaiian Islands through May
25, 2021 from iNaturalist.org, MushroomObserver.org, and
Mycoportal.org. Observation and collection data were cleaned
considering the shortcomings of fungal repository data outlined
in Hao et al. (2021): observations or collections that were
duplicates, lacked geospatial or temporal data, or fell outside
the Agaricomycetes were removed. To be included, associated
geospatial coordinates needed to fall on land within the Hawaiian
Islands. ESRI ArcGIS (version 10.7.1) was used to visualize
observations and collections throughout the Hawaiian Islands
and bin these into rainfall and elevation categories. Rainfall data
was again obtained from the Rainfall Atlas of Hawai‘i, elevation
data was obtained from the National Centers for Coastal
Ocean Science Observations (NCCOS, 2022), and temperature
data from the Climate of Hawai‘i (Giambelluca et al., 2014).
Observations and/or collections that matched species identified
as native from the list used for our richness analysis were also
indicated as native in our abundance analysis.
Because the habitat in the Hawaiian Islands is highly
heterogeneous, correlating increased basidiomata production
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Stallman and Robinson Seasonality of Hawaiian Mushrooms
with environmental variables across the entire archipelago, or
even a single island, is difficult. To better investigate whether
basidiomata production correlated with average monthly
elevation or rainfall, we subset our abundance data into
categories by elevation, annual rainfall, and island, as in our
richness analysis. Maui, Moloka‘i, and L¯
ana‘i were considered
as a single entity, Maui Nui, as is often done in biogeographical
studies due to the connectivity of these islands in the recent
past (Price and Elliott-Fisk, 2004). Bins with <200 data points
were excluded. This left wet, lowland habitats on Hawai‘i and
O‘ahu; mesic, lowland habitats on Hawai‘i, O‘ahu, and Kaua‘i;
and dry, lowland habitats on O‘ahu. Point interpolations were
performed in ArcGIS using default settings to determine where
the highest density of observations and collections occurred.
Average monthly rainfall and temperature from the interpolated
highest density region were then obtained from Giambelluca
et al. (2013, 2014).
Excluded Species and Analyses
For both our richness and abundance datasets, the following
species were excluded from our analyses as detection may occur
year-round due to long-lasting, persistent structures: species
characterized as polyporoid (e.g., Polyporales; Hymenochaetales
spp.), corticioid (e.g., Corticiaceae spp.), gelatinous (e.g.,
Auriculariales spp.), or species with otherwise persistent
basidiomata (e.g., Nidulariaceae).
We used chi-square tests to determine if Agaricomycetes
reproductive phenology varied by month throughout the entire
Hawaiian archipelago. The null hypothesis was that no significant
difference existed between months in richness or abundance
counts across all Agaricomycetes species, and native species only.
Pearson’s correlation coefficient tests were performed between
monthly basidiomata counts of richness and abundance in
binned environmental categories with ≥200 abundance data
points on Hawai‘i Island, Kaua‘i Island, and O‘ahu Island, and the
average monthly rainfall and temperature corresponding to the
densest location of their abundance. The null hypothesis was that
no significant correlation existed between months of increase in
basidiomata richness or abundance in a binned habitat (e.g., wet
and low elevation) on an island and the monthly temperature or
rainfall at the densest location of their abundance. Analyses were
conducted using R (R Core Team, 2021).
RESULTS
Richness and Abundance Species Lists
Based on our literature review, we found 643 known
Agaricomycetes occur in the Hawaiian Islands
(Supplementary Table 2). Of the 643 species, 321 had
associated seasonality data and lacked long-lasting or persistent
reproductive structures to be included in our analysis. Of these,
33 species were considered native in our study and included in
the native-only richness analyses.
A C
B D
FIGURE 2 | Total species diversity (richness) across 12 months considering all Agaricomycetes included in this study (n=321) (A), and only native species (n=33)
(B). Total observations and collections aggregated from online resources (abundance) across 12 months considering all Agaricomycetes (n=3,285) (C), and only
native species (n=169) (D). In both datasets, species known to produce long-lasting, persistent basidiomata were excluded. Chi-square values and p-values are
indicated in each plot with the null hypothesis being that there is no difference in richness or abundance counts between months.
Frontiers in Fungal Biology | www.frontiersin.org 4April 2022 | Volume 3 | Article 869689
Stallman and Robinson Seasonality of Hawaiian Mushrooms
We downloaded 11,292 observations or collections
from iNaturalist.org, MushroomObserver.org, and
Mycoportal.org through May 25, 2021. After cleaning, we
found 3,285 unique observations or collections meeting
our study criteria (Supplementary Table 3). The 3,285
observations or collections contain 478 unique names,
although due to the high number of records identified
above the species level, the number of unique species
these records constitute is unknown. Of these, 169
observations and/or collections of 22 unique species
A
B
C
FIGURE 3 | Examination of abundance data with ≥200 observations and/or collections and richness data on an island within annual rainfall and elevation categories
by average monthly rainfall and temperature. Datapoints are color coded by annual rainfall and elevation categories. The closest climate station to the highest density
of data points for a given category that was used to determine average monthly rainfall and temperature is indicated. Histograms show abundance (black), richness
(gray), average monthly rainfall (blue) and temperature (yellow) for: Hawai‘i Island, lowland wet and lowland mesic habitats (A); Kaua‘i Island, lowland mesic habitats
(B); O‘ahu Island, lowland wet, mesic, and dry habitats (C). Pearson’s correlation coefficients between richness and abundance counts and average monthly rainfall or
temperature that were found to be significant (p<0.05) are indicated in histogram panels.
Frontiers in Fungal Biology | www.frontiersin.org 5April 2022 | Volume 3 | Article 869689
Stallman and Robinson Seasonality of Hawaiian Mushrooms
were considered native and included in the native-only
abundance analyses.
Seasonality Trends and Analyses
Overall Agaricomycetes richness shows a peak in January with
lower diversity from February to June. Richness increases in July
and continues at an elevated rate through December (Figure 2A).
A significant difference in richness between months was found
(X2=96.7, p<0.01, df =11). Native-only richness show that
February to April is a period of lower mushroom diversity with
June and October also having low diversity (Figure 2B). For
richness counts of native species only, the null hypothesis that
there is no difference in richness between the 12 months cannot
be rejected (X-squared =19.2, p=0.06, df =11).
Overall abundance data shows peaks in January, March, and
October to December (Figure 2C). A significant difference in
species abundance between months was found (X2=309.1, p<
0.01, df =11). Native-only abundance data show that January has
very high abundance, February to April have low abundance, and
May to December have a low baseline of consistent abundance
counts (Figure 2D). A significant difference in species abundance
between months was found considering native species only (X2=
140.3, p<0.01, df =11).
Richness data by rainfall and elevation categories generally
show a trend of high diversity in January, low diversity
from February to April, May, or June, then high diversity
for the remainder of the year with outliers being dry, and
subalpine/alpine locations that also having high diversity in
March (Supplementary Figure 1). Abundance data by rainfall
amount and elevation do not follow an obvious pattern, although
abundance is generally highest from October through March
(Supplementary Figure 2).
Pearson’s correlation coefficient tests show significant positive
correlations between basidiomata abundance and average
monthly rainfall in lowland, mesic environments on Kaua‘i
(r=0.88; p-value <0.01) and O‘ahu (r=0.66; p=0.02), and
lowland, dry environments on O‘ahu (r=0.83; p-value <0.01).
Correlations between abundance of basidiomata and average
monthly rainfall or temperature in lowland, wet environments
on Hawai‘i Island and O‘ahu, and lowland, mesic environments
on Hawai‘i Island were not significant. Correlations between
species richness and average monthly rainfall or temperature in
either elevation or annual rainfall category were not significant
(Figure 3;Supplementary Table 4).
DISCUSSION
Trends in Seasonality and Environmental
Correlates
Despite a warm climate and areas with consistent year-round
rainfall, we found Hawaiian mushrooms generally exhibit
seasonality patterns in richness and abundance, except in
native-only species richness where we could not reject our
null hypothesis (Figure 2). Our results incorporating greater
taxonomic breadth agree with the prior findings of Stallman
(2019) for richness in the family Agaricaceae, which is primarily
represented by non-native species in the islands. Comparing
our results of native abundance data to that of Hemmes and
Desjardin (2002), we found the month of January to be by
far the most abundant, which was one of their least abundant.
Additionally, we found native-only basidiomata production is
as abundant from May–June as July–December, but May and
June showed low abundance in their dataset. These differences
could be due to overall low detection of native species, uneven
collecting efforts in different locations, or species selection. For
example, Hemmes and Desjardin (2002) found Rhodocollybia
laulaha to be the most abundant native species in their study, but
its origin is now uncertain after it was found in the American
tropics Keirle et al. (2010). Its origin was assigned as unknown in
this study, and therefore not included in our native-only analysis.
Our hypothesis that abundance and richness of mushroom
species would not correlate to monthly average rainfall or
temperature is supported when considering species richness and
elevation, but not for all instances when considering abundance
and rainfall. In lowland, dry and mesic environments on
O‘ahu, and lowland mesic environments on Kaua‘i, basidiomata
abundance is correlated to increased rainfall. Rainfall as a limiting
factor to increased abundance in areas lacking consistently
high year-round precipitation is intuitive, and follows anecdotal
observations and prior studies (e.g., Chacón and Guzmán, 1995).
In wet areas with the highest concentration of observations
and collections on Hawai‘i and O‘ahu, monthly rainfall is a
minimum of 200–300 mm, and increasing rainfall above this
baseline does not lead to increased monthly abundance or
richness (Figures 3A,C). Increased rainfall in lowland mesic
areas on Hawai‘i Island is not positively correlated with increased
abundance in basidiomata production despite O‘ahu and Kaua‘i
FIGURE 4 | Monthly counts of 87 collections or observations of the six
Hawaiian Agaricomycetes species found to be threatened by the IUCN:
Callistosporium vinosobrunneum,Humidicutis pakelo,Humidicutis peleae,
Humidicutis poilena,Hygrocybe lamalama,Hygrocybe noelokelani. Data from
MyCoPortal.org, iNaturalist.org, and MushroomObserver.org.
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Stallman and Robinson Seasonality of Hawaiian Mushrooms
seeing increased production during wetter months in mesic
locations (and O‘ahu in lowland dry areas). The reason for this
is unclear, but Hawai‘i is a large island (10,430 Km2) and by only
examining rainfall at the location interpolated to have the highest
number of mesic observations and/or collections, accuracy may
be lower than for the smaller islands of Kaua‘i (1,456 Km2) and
O‘ahu (1,545 Km2) (Supplementary Table 1).
Limitations
Several limitations exist in our study. First, our data incorporates
several broad categories. Temporally we examined monthly
instead of weekly; elevation by 1,000 m, and rainfall by 1,000–
1,500 mm. Additionally, we have not considered how seasonality
of Agaricomycetes may differ between substrates (e.g., wood or
soil) or ecological roles (e.g., saprotroph or symbiotroph), which
have been important explanatory variables in a Japanese oak
forest (Sato et al., 2012) and across Europe (Andrew et al., 2018).
Second, the majority of Hawaiian Agaricomycetes lack a
DNA barcode sequence to help verify species identity and allow
quick biogeographical comparisons with other sequence data
in GenBank. Our understanding of which species are native
may change as more data become available. Additionally, in
our abundance analysis, collections and/or observations not
identified to the specific level were deemed non-native, although
a small portion of these may constitute native species.
Third, our abundance data aggregated from MyCoPortal.org,
iNaturalist.org, and MushroomObserver.org may hold
biases such as focus on or near population centers, and
increased documentation of conspicuous (large, colorful) over
inconspicuous species (Gonçalves et al., 2021). Non-native
mushrooms often occur near population centers and may have
additional water inputs from irrigation. While we believe that
most Hawaiian Agaricomycetes collections in herbaria have been
digitized (at SFSU, BISH, and ARIZ), some collections at these
locations and other herbaria may not be digitized, representing
an untapped data source in our abundance analysis that was not
captured via MyCoPortal.org searches.
Finally, our data is biased toward the recent past: only 14% of
collections or observations in our abundance analysis occurred
before 1990, and 29% were before 2000. As climate change
has been shown to change macrofungal reproductive phenology
(Andrew et al., 2018), some signal in seasonality patterns may be
lost due to changes over time in a changing climate. With our
data’s strong bias toward the present, we are likely seeing less of
this effect.
Conservation Implications
The six Hawaiian fungi that have so far been assessed
for the IUCN Red List and were found to be threatened
are the endangered Hygrocybe noelokelani and Hy. pakelo
(Vellinga, 2017b, 2019d), and the vulnerable Callistosporium
vinosobrunneum,Humidicutis peleae,Humidicutis poilena, and
Hy. lamalama (Vellinga, 2017a, 2019a,b,c). Regarding richness
of these species, some show strong seasonality (or rareness in
general) with C. vinosobrunneum only being found November to
January and Hu. poilena only in November, while other species,
such as Hu. peleae, occur throughout much of the year. These
threatened species are most abundant in January, November,
and December (Figure 4). Although current funds are not
allocated to Agaricomycetes conservation by the state or federal
government, understanding seasonal basidiomata production
could help managers plan field efforts to monitor these species
or find additional populations, as is done for imperiled Hawaiian
plants (e.g., Kawelo et al., 2012). Although morphological
identification of fungi is not always possible (Taylor et al.,
2006) or may require experts or DNA data, some threatened
species in the Hawaiian Islands such as Hy. noelokelani are easily
recognizable without molecular identification (Vellinga, 2017b).
Molecular tools can also be used to monitor populations
of threatened fungi (Gordon and Norman, 2015). The first
barrier to detection of threatened Hawaiian fungal species
via these methods is generating reference sequences for the
threatened species; currently none have an associated DNA
barcode (Schoch et al., 2012). Additionally, substrate would
need to be carefully considered as many threatened Hawaiian
species form basidiomata on mosses, making it unclear if high
throughput sequencing of soil would lead to detection if nearby
populations were present.
We note that all threatened Hawaiian Agaricomycetes
species are most often found in montane, wet, and mesic
habitats which are dominated by the native ‘¯
ohi‘a tree
(Metrosideros polymorpha). ‘ ¯
Ohi‘a are being killed by the
introduced pathogens Ceratocystis lukuohia and C. huliohia,
together known as Rapid ‘ ¯
Ohi‘a Death (ROD). The disease
has killed over one million trees in the islands (ROD
working group, personal communication) and will likely have
a detrimental impact on associated native plant communities
(Fortini et al., 2019). While direct evidence of native fungal
population declines from this disease is lacking, monitoring
of threatened fungi is needed to determine demographic and
distribution changes as Hawaiian forests change due to the effects
of ROD.
CONCLUSION
A diverse, abundant number of mushrooms occur throughout
the year in the Hawaiian Islands, but richness and abundance
are generally highest in January. If general surveys for
Agaricomycetes are to be completed and cannot be done year-
round, the period from July to January can be recommended
for overall elevated richness and abundance, including elevated
abundance of native species. Despite this recommendation,
richness of native species does not exhibit a strong seasonality
pattern as they are found relatively evenly throughout the year,
albeit in low abundance.
More selective approaches can be employed for surveys
depending on location. In particular, surveys in lowland,
dry and mesic environments where increased basidiomata
abundance is correlated with increased monthly rainfall
(at least on the islands of O‘ahu and Kaua‘i) should be
planned accordingly.
The ability of conservationists and community scientists
to identify some of these fungi in the field and the temporal
Frontiers in Fungal Biology | www.frontiersin.org 7April 2022 | Volume 3 | Article 869689
Stallman and Robinson Seasonality of Hawaiian Mushrooms
variability among species suggests that including seasonality
data on macroscopic fungi in IUCN evaluations may be
useful to increase detections. This information could be
added to the existing ‘Habitat and Ecology’ field. Data
generated by mycologists and community scientists can
be useful in determining the full ranges of threatened
species and the phenology of their basidiomata production,
particularly in organisms recognizable to the species level
by macromorphology. Being able to record the absence of
species (i.e., negative records) in online community science
platforms would also be useful in gathering range data on
threatened species. Collecting baseline seasonality and range
data will allow for future comparisons with a changing
climate, and generating reference DNA barcodes for threatened
species allows for potential monitoring and new population
discovery via environmental DNA studies and comparisons with
online databases.
DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included
in the article/Supplementary Material, further inquiries can be
directed to the corresponding author.
AUTHOR CONTRIBUTIONS
JS conceived of the study, completed the research, analyzed
the data, and wrote the manuscript. KR completed the
research, analyzed the data, and wrote the manuscript.
Both authors contributed to the article and approved the
submitted version.
FUNDING
This article was funded in part by Purdue University Libraries
Open Access Publishing Fund.
ACKNOWLEDGMENTS
We thank Drs. Don Hemmes and Dennis Desjardin for sharing
their list of Hawaiian Agaricomycotina species. We thank
Amy Durham and Benjamin Lillibridge for preliminary data
collection. We thank Drs. Matthew Knope and Mary Catherine
Aime and her laboratory group at Purdue University for useful
discussions surrounding manuscript content. Finally, we thank
Dr. Danny Haelewaters for providing feedback on a draft of
the manuscript.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/ffunb.
2022.869689/full#supplementary-material
Supplementary Table 1 | Location, size, maximum elevation, age, and average
minimum and maximum annual rainfall and temperature on the six Hawaiian
Islands considered in this study.
Supplementary Table 2 | List of 643 Agaricomycetes species occurring in the
Hawaiian Islands tabulated from sources outlined in methods used in our richness
analysis. Origin, association with native or non-native vegetation, annual elevation
and temperature categories, island(s) of occurrence, month(s) basidiomata have
been documented, and a non-exhaustive list of references are included.
Supplementary Table 3 | List of 3,285 observations and collections of
Agaricomycetes species from the Hawaiian Islands in online repositories
downloaded from MyCoPortal.org, iNaturalist.org, and MushroomObserver.org as
of May 25, 2021 (and curated as indicated in methods) used in our abundance
analysis. Scientific name, month documented, database downloaded from with
unique identifier, location, year of observation, and annual elevation and
precipitation categories are included.
Supplementary Table 4 | Correlation coefficients between species richness and
abundance counts in annual rainfall and elevation categories on an island with
average monthly rainfall or temperature at the densest location of those
observations and/or collections. Correlations were only performed in annual
rainfall and elevation categories on a single island with ≥200 observations and/or
collections in our abundance dataset.
Supplementary Figure 1 | Total Agaricomycetes species diversity (richness) in
the Hawaiian Islands over different annual rainfall (wet ≥2,500 mm/year, mesic
1,000–2,500 mm/year, dry <1,000 mm/year) and elevation (lowland <1,000 m,
montane 1,000–2,000 m, subalpine and alpine >3,000 m) categories, excluding
species with persistent reproductive structures (n = 321).
Supplementary Figure 2 | Total Agaricomycetes abundance in the Hawaiian
Islands over different annual rainfall (wet ≥2,500 mm/year, mesic 1,000–2,500
mm/year, dry <1,000 mm/year) and elevation (lowland <1,000 m, montane
1,000–2,000 m, subalpine and alpine >3,000 m) categories based on curated
observation and collection data from MyCoPortal.org, iNaturalist.org, and
MushroomObserver.org (n =3,285).
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Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
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