Research article

Temporal shifts in a Xylaria assemblage (Ascomycota,

Xylariaceae) resulting from management activities in a
protected cloud forest
Cambios temporales en un ensamblaje de Xylaria
(Ascomycota, Xylariaceae) como resultado de las
actividades de manejo en un bosque de niebla protegido
Santiago Chacón1 , Elsa Utrera-Barillas1 , Miguel A. García-Martínez2, 3, 4

Abstract:
Background and Aims: Tropical montane cloud forest (TMCF) is one of the most threatened ecosystems worldwide. Natural protected areas (NPAs)
have been established to prevent further loss of these forests in Mexico. To assess whether management activities temporally impact the biodiversity
of NPAs, the use of indicator groups, such as some groups of macromycetes, has been proposed. The aim of this study was to assess the temporal
shifts over the last 36 years in the alpha, beta, and gamma diversity of a Xylaria assemblage in a NPA of TMCF as a result of anthropogenic manage-
ment activities.
Methods: Collections were performed in a 31 ha NPA of TMCF in Xalapa, Veracruz, Mexico, during three 10 year and one six year sampling periods
(1980-2016), taking into account specimens deposited in the herbarium XAL and collections performed by the authors, mainly in the two latter
periods. Species number and abundance, compositional similarity, species turnover, and gamma diversity of assemblages were determined and
compared among the sampling periods.
Key results: Of 3480 individuals belonging to 30 Xylaria species, the most abundant species were X. scruposa, X. anisopleura, X. berteroi, X. cubensis,
X. feejeensis, X. albocinctoides, and X. arbuscula. The inventory completeness was 99.9%. Species richness varied from six (1990-1999) to 28 species
(2010-2016). Jaccard index separated two assemblage clusters. Gamma diversity was more influenced by beta diversity than alpha diversity.
Conclusions: Xylaria assemblages are a useful bioindicator group and monitoring them over time may provide information about the impacts of
management on TMCF ecosystems. Temporal dynamics of these assemblages partly depend on the historically implemented management in the NPA
of TMCF. Effective conservation outcomes for TMCF will only be achieved if current management strategies are maintained and integrated into the
long-term management framework of NPAs containing TMCF.
Key words: Ascomycetes, fungal diversity, temporal changes, urban ecosystems, urban forest.

Resumen:
Antecedentes y Objetivos: El bosque mesófilo de montaña (BMM) es uno de los ecosistemas más amenazados mundialmente. Las áreas naturales
protegidas (ANP) han sido establecidas para prevenir la pérdida de estos bosques en México. Para evaluar el impacto temporal de las actividades de
manejo de las ANP sobre la biodiversidad, se ha propuesto utilizar bioindicadores, como algunos grupos de macromicetos. El objetivo de este estudio
fue evaluar los cambios temporales, durante los últimos 36 años, en la diversidad alfa, beta y gama de un ensamblaje de Xylaria en un ANP de BMM
como un resultado de las actividades de manejo antropogénico.
Métodos: Las recolectas fueron realizadas en un ANP de 31 ha de BMM en Xalapa, Veracruz, México, durante tres periodos de muestreo de 10 años
y uno de seis (1980-2016), considerando ejemplares depositados en el herbario XAL y recolecciones realizadas por los autores principalmente en
los últimos dos períodos. La riqueza, abundancia, similitud, recambio y la diversidad gama de los ensambles fue determinada y comparada entre
periodos de muestreo.
Resultados clave: De 3480 individuos pertenecientes a 30 especies de Xylaria, las más abundantes fueron X. scruposa, X. anisopleura, X. berteroi, X.
cubensis, X. feejeensis, X. albocinctoides y X. arbuscula. La integración del inventario fue de 99.9%. La riqueza varió de seis (1990-1999) a 28 especies
(2010-2016). El índice de Jaccard separó dos agrupaciones. La diversidad gama estuvo más influenciada por la diversidad beta que por la alfa.
Conclusiones: Los ensamblajes de Xylaria son bioindicadores útiles y su monitoreo temporal puede proveer información del impacto del manejo del
BMM. La dinámica temporal de estos ensamblajes depende parcialmente del manejo implementado históricamente en el ANP de BMM. La conser-
vación eficiente del BMM dependerá del mantenimiento de las estrategias de manejo actuales y su integración a un plan de manejo a largo plazo del
ANP que contiene BMM.
Palabras clave: Ascomicetos, bosque urbano, cambios temporales, diversidad fúngica, ecosistemas urbanos.

1 Instituto de Ecología, A.C., Carretera antigua a Coa- Received: April 20, 2018. To cite as:
tepec 351, El Haya, 91070 Xalapa, Veracruz, México. Reviewed: June 19, 2018. Chacón, S., E. Utrera-Barillas and M. A. García-
2 Universidad Veracruzana, Facultad de Ciencias Bio- Accepted by Marie-Stéphanie Samain: July 25, 2018. Martínez. 2018(2019). Temporal shifts in a Xylaria
lógicas y Agropecuarias, Josefa Ortiz de Domínguez Online first: October 10, 2018. assemblage (Ascomycota, Xylariaceae) resulting from
s/n, Centro Peñuela, 94945 Amatlán de los Reyes, Publised: Acta Botanica Mexicana 126 (2019). management activities in a protected cloud forest.
Veracruz, México. Acta Botanica Mexicana 126: e1378. DOI: 10.21829/
3 Universidad Politécnica de Huatusco, Calle 9 Sur en- abm126.2019.1378
tre Av. 7 y 9 s/n, Centro, 94100 Huatusco, Veracruz, This is an open access article under the Cre-
México. ative Commons 4.0 Atribution-Non commer-
4 Author for correspondence: [email protected] cial License (CC BY-NC 4.0 International). e-ISSN: 2448-7589

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Chacón et al.: Temporal shifts of a Xylaria assemblage

Introduction Among the impressive biodiversity harbored by Mexi-

Tropical montane cloud forest (TMCF) is a physiognomical- can TMCFs, macrofungi form one of the most diverse groups
ly heterogeneous floristic group composed of species with (Guzmán et al., 2003; Gómez-Hernández et al., 2012). Some
diverse biogeographic affinities. It is characterized by the studies suggest that Ascomycota and/or Basidiomycota as-
persistent cloud cover that envelops its vegetation (Wil- semblages rapidly respond to natural and anthropogenic
liams-Linera, 2007). This vegetation type stands out for its disturbances and management regimes (Gómez-Hernán-
high levels of plant and fungal diversity (Gómez-Hernán- dez and Williams-Linera, 2011; McGregor-Fors et al., 2015).
dez et al., 2012). It occupies less than 1% of the national Among ascomycetes, the Xylariaceae family, composed of 85
territory (Challenger and Dirzo, 2009), yet contributes 10% genera worldwide, is large and relatively well known (Kirk et
of plant diversity and exhibits a high degree of endemicity al., 2008). Most are saprobic wood degraders and actively
(Rzedowski, 1993). However, in Mexico, TMCF is also one decay the wood of living or dead angiosperms, while others
of the most threatened ecosystems (Medel, 2013; Estra- are endophytic and symbiotically live within plant tissues.
da-Contreras et al., 2015). In fact, several endophytes are commonly associated with
One conservation strategy for countering the current numerous tropical plants and even associated with termite
loss of TMCF is the establishment of areas for preserving nests (Rogers, 2000; Rogers et al., 2005).
the biodiversity and ecosystem services provided by these The genus Xylaria Hill ex Schrank is characterized
forests (Toledo-Aceves et al., 2011). Natural protected ar- by stromata, usually, erect, cylindrical or clavate, some-
eas (NPAs) play a key role as reservoirs of the biodiversi- times subglobose, usually higher than wide, surrounded
ty associated with TMCF in human-dominated landscapes by perithecia containing ascospores; stipitate perithecia
(MacGregor-Fors et al., 2016). However, the conservation with hemispherical or umbilicate ostioles; cylindrical asci
value of NPAs may be spatially dependent on structural with amyloid apical rings, black, ascospores usually with a
(e.g., habitat loss) and/or landscape factors (e.g., surround- straight, oblique, or spiraling germ slit (San Martín and Rog-
ing land uses/covers) (Gove et al., 2005; Escobar et al., ers, 1995). This genus is one of the most diversified in the
2008). Until now, little is known about whether the man- family and contains about 300 species (Kirk et al., 2008). In
agement activities of NPAs temporally impact their biodi- Mexico, 105 species have been recorded (San Martin and
versity. Thus, long-term studies are necessary to under- Rogers, 1989; 1995), yet only 18 species are found in TMCF
stand the conservation value of NPAs under anthropogenic (Medel, 2013). Medel et al. (2008) recorded 45 species
management regimes. of Xylaria for Veracruz, of which 24 species have been re-
Biological communities associated with TMCF are ported for TMCF. Evaluating changes in the richness, abun-
highly dynamic in space and time as a result of seasonali- dance, or turnover of Xylaria assemblages can potentially
ty, habitat characteristics, and the degree of anthropogenic be used as a tool for establishing conservation priorities or
pressures (Gómez-Hernández and Williams-Linera, 2011; determining the impact of management activities on en-
García-Martínez et al., 2016; MacGregor-Fors et al., 2016). dangered ecosystems, including TMCF.
Particularly, in the present context, temporal shifts experi- This study integrates a historical Xylaria inventory
enced by biological communities (including those of TMCF) coming from a series of samples collected over the last 36
may be a cumulative consequence of historical changes in years in a natural protected area of tropical mountain cloud
anthropogenic management activities (Toledo-Aceves et forest and it is improved with an exhaustive review of ad-
al., 2011). In addition, temporal variation in diversity (i.e., ditional specimens available in the Fungi Collection of the
species richness and abundance) and compositional simi- herbarium XAL of the Instituto de Ecología, A.C. (INECOL) in
larity (i.e., presence/absence of species) of a particular spe- Xalapa, Veracruz, Mexico. The aim of this study was to as-
cies group depend on the response ability and the degree sess the temporal shifts over the last 36 years in the alpha,
of taxonomic resolution of the group as well as how the beta, and gamma diversity of a Xylaria assemblage in a NPA
community is defined (Rahel, 1990). of TMCF that has experienced several anthropogenic man-

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 Chacón et al.: Temporal shifts of a Xylaria assemblage

agement activities. Specifically, we examined whether the 19°31'06"N and the meridians 96°56'05"W; 96°56'27"W in
richness and abundance of Xylaria species changed over the municipality of Xalapa, Veracruz, at an elevation rang-
time, in addition to temporal patterns in the compositional ing from 1250 to 1350 m a.s.l. (Fig. 1). This 31 ha sanctuary
similarity of the Xylaria assemblage. The implementation of has been under state protection since February 17th, 1977,
long-term ecological monitoring using Xylaria assemblages and currently belongs to the INECOL (Luna and García,
as a model group could provide novel insight into the im- 1998). The terrain of this forest has a slope of 52% and a
pacts of management and conservation strategies on NPAs soil compaction of 10 kg/m2. Ground cover is composed of
and TMCF, one of the most threatened tropical ecosystems leaf-litter (72%), grass (10%), and forbs and herbs (8%), and
worldwide. the remaining proportion is uncovered. Tree canopy cover
is 79%, and canopy height is 11 m (García-Martínez et al.,
Material and Methods 2016). A total of 97 tree species are present (Lorea Hernán-
Study area dez, pers. com.) at a density of 1140 individuals/ha (García-
This study was conducted in a fragment of tropical moun- Martínez et al., 2016).
tain cloud forest in the central mountainous region of the Significant events have occurred in the study area be-
state of Veracruz, Mexico (Fig. 1). The climate is humid tem- fore the considered sampling periods that have changed its
perate, and the average annual temperature is 18 °C. The land use/land cover or management. Before 1980, the en-
annual precipitation varies from 1500 to 2000 mm. A hot- tire area was a shaded coffee plantation with some planted
dry season spans from March to May, a warm-rainy season citrus trees, and a portion of it was modified to create a
from June to October, and a cold-dry season from Novem- vacational/recreational center. Additionally, nine hectares
ber to February. The soil is characterized as Andosol, with were dedicated to creating a botanical garden, and an ur-
a volcanic origin and loamy texture (Williams-Linera et al., ban park with impressive infrastructure was constructed
2002; 2015). throughout the remaining area (Luna and García, 1998).
The studied forest is called Santuario del Bosque de From 1980 to 1989 the urban park was abandoned, and
Niebla and is located between the parallels 19°30'37"N; restoration activities began. The area came to be composed

Figure 1: Location of a natural protected area of tropical montane cloud forest, Santuario del Bosque de Niebla, in central Veracruz, Mexico. The
location of the study area (white circle) within the state of Veracruz (dark gray polygon) is shown. The dashed lines indicate the rivers and/or streams.

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Chacón et al.: Temporal shifts of a Xylaria assemblage

of a mosaic of habitats, including TMCF, secondary and ri- herbarium revision, we based the abundance on the in-
parian vegetation, as well as grasslands. The active resto- cidence of Xylaria species (i.e., the number of times that
ration of the TMCF was later halted. Between 1990 and a given species was collected during a sampling period).
1999 the area was converted to an ecological urban park We grouped all Xylaria records (species and abundance
dedicated to conserving, maintaining, and restoring native records) in four sampling periods according to the year
plant communities. The area contained relictual, disturbed, when specimens were collected: 1980-1989, 1990-1999,
and heterogeneous fragments of TMCF. Natural succession 2000-2009, and 2010-2016 (three periods of 10 years and
continued, and the area was devoted to scientific research one period of six).
(Luna and García, 1998). Since 2000, the area was charac- We calculated the inventory reliability for each sam-
terized as a young forest with a high canopy cover but low pling period using the coverage estimator, which is a less
canopy height (Gómez-Hernández and Williams-Linera, biased estimator of sample completeness than non-para-
2011). Recently, the area may be categorized as a young metric methods. The resulting value indicates the propor-
forest remnant that, by now, is relatively undisturbed or as tion of the statistical population that is represented by the
a secondary cloud forest undergoing maturation processes collected species (Chao and Jost, 2012) and is expressed by
(MacGregor-Fors et al., 2016). the following equation:

( fn [ (n-1)f
Collections and specimen revisions Ĉn = 1- 1
(n-1)f 1
([ *100
+ 2f
1 2
Most Xylaria stromata are restricted to the rainy part of
the year, so the study site was sampled between July and where n is the sum of all individuals of all species in a given
November from 2010 to 2016 following the sampling tech- sampling period, and f1 and f2 are singletons (species each
nique of Lodge et al. (2004). In every sampling event, the represented by only a single individual) and doubletons
sporocarps of Xylaria were counted and collected in thin (species each represented by exactly two individuals), res-
paper bags and each specimen was macro and micromor- pectively. Sample completeness (Ĉn) indicates the propor-
phologically described when fresh. Then, the specimens tion of the “total community” represented by the collected
were dried in an oven at 50-60 °C for 48 h (Lodge et al., species and enables the diversity of assemblages sampled
2004). To improve our Xylaria inventory, we also examined at the same coverage to be compared. When Ĉn≈100%,
all specimens of Xylaria collected in the same study area sampling is complete given the effort and utilized collection
and deposited between 1981 and 2010 in the Fungi Col- technique (Chao and Jost, 2012). Values of Ĉn were calcula-
lection of the herbarium XAL. All specimens collected and ted using the iNEXT package for R (Hsieh et al., 2016).
obtained during our explorations are available in XAL, and As mentioned, the comparison of richness among
these were determined at the species level by identifying sampling periods is only ecologically appropriate for those
their micro and macromorphological characters according periods with a similar level of inventory completeness.
to several keys and specialized literature (Dennis, 1956, Therefore, a comparison of our estimates of species rich-
1957; Rogers, 1983, 1984; Rogers and Callan, 1986; Rog- ness per sampling period could be biased because of differ-
ers et al., 1988, 2002; San Martín and Rogers, 1989; San ences in inventory completeness. In particular, species rich-
Martín, 1992; Medel et al., 2008; Hladki and Romero, 2010; ness is sensitive to variations in the number of singletons
Tapia et al., 2017). and doubletons (Chao and Jost, 2012). Thus, we estimated
the species richness for each sampling period using cover-
Data analysis age-based inter- and extrapolations in the iNEXT package
As Xylaria species have a cespitose and gregarious growth for R (Hsieh et al., 2016). We considered 99.99% complete-
form, two or more sporocarps of the same species grow- ness as a reliable estimator of richness for all sampling pe-
ing in a diameter of <50 cm or in a fairy ring were record- riods (Chao and Jost, 2012). To compare species richness
ed as one individual. For correcting the bias implicated in among sampling periods, we used 95% confidence intervals

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Chacón et al.: Temporal shifts of a Xylaria assemblage

in which significant differences were indicated by non-over- dant species was X. scruposa (Fr.) Berk. (903 individuals),
lapping confidence intervals (Cumming et al., 2007). followed by X. anisopleura (Mont.) Fr. (820), X. berteroi
To evaluate differences in species’ dominance and (Mont.) Cooke ex J.D. Rogers & Y.M. Ju (496), X. cubensis
rarity and in community evenness among sampling peri- (Mont.) Fr. (435), X. feejeensis (Berk.) Fr. (231), X. albocinc-
ods and, thus, to better interpret our results, Xylaria abun- toides Y.M. Ju, H.M. Hsieh & J.D. Rogers (153), and X. ar-
dance was represented by rank-abundance species curves buscula Sacc. (136). The 23 remaining species were repre-
or Whittaker plots (Magurran, 2004). We plotted the pro- sented by less than 80 individuals. The average sampling
portional abundance of each species, ordered from the completeness was 95.6%. Sampling completeness was
most to the least abundant, to show differences in species’ 90.2% in the sampling period of 1980-1989, 98% in 1990-
dominance and rarity and in assemblage evenness among 1999, 94.2% in 2000-2009, and 99.9% in 2010-2016. Con-
sampling periods. sidering all four decades, the sampling completeness was
To analyze beta diversity, we determined the com- 99.9%.
positional similarity among sampling periods using the Jac-
card index. This index has values ranging from 0 (minimal Alpha diversity
similarity) to 100 (maximum similarity) (Magurran, 2004). With respect to species abundance, 41 individuals were
It only takes into account shared species and presence/ recorded in the sampling period of 1980-1989, 47 in 1990-
absence of species between sites (Jost, 2006). The compo- 1999, 50 in 2000-2009, and 3341 in the final sampling pe-
sitional similarity among sampling periods was represent- riod (2010-2016) (Table 1). We observed that the assem-
ed by a cluster analysis using the Unweighted Pair Group blage structure changed across the four sampling periods.
Method with Arithmetic Mean (UPGMA) linkage technique. Considering proportional abundance, the general pattern
For the post hoc analysis, a similarity profile test (SIMPROF) observed indicated an increase in species dominance du-
was used as statistical test to compare similarity among as- ring the sampling period of 1990-1999 (Fig. 2). The domi-
semblages in the PRIMER software version 6.1.16 (Clarke nant species during the periods of 1980-1989, 1990-1999,
and Gorley, 2006). The SIMPROF test assumes that a real and 2000-2009 was X. berteroi, with a relative abundan-
clustering of assemblages will be evidenced by an excess ce of greater than 35%. With respect to observed species
of smaller and/or larger similarities than expected under richness (Fig. 3), nine species were recorded in the sam-
the null hypothesis that all assemblages are drawn from the pling period of 1980-1989, six in 1990-1999, nine in 2000-
same species assemblage (Clarke et al., 2008). 2009, and 28 in the final sampling period (2010-2016).
To quantify the contribution of each time period to Upon comparing estimated species richness, we observed
total diversity (i.e., gamma diversity), we calculated the av- that the number of species recorded in the final sampling
erage number of species absent from each site (beta diver- period (2010-2016) significantly differed from that of the
sity), which is defined as β=γ-α, where γ corresponds to the other sampling periods.
number of species recorded historically in the study area
(gamma diversity) and α to the average number of species Beta diversity
present in a given time period (alpha diversity) (Lande, The evaluation of compositional similarity using a clus-
1996). This approach allows for a direct comparison be- ter analysis and SIMPROF test based on the Jaccard index
tween alpha and beta diversities in terms of numbers (or showed the significant separation of two assemblage clus-
percentages) of species (Crist et al., 2003). ters at a similarity of 27% (π=4.65, p=0.002) (Fig. 4). The
Xylaria assemblage collected in the 2010-2016 sampling
Results period was significantly separated from the assemblages
The Xylaria inventory collected in the other periods. Regarding species turnover
In total, we historically recorded 3480 individuals belonging among sampling periods, 59% of total species were unique
to 30 species of the genus Xylaria (Table 1). The most abun- to a single sample period, and 14% were shared by all sam-

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Chacón et al.: Temporal shifts of a Xylaria assemblage

Table 1: Historical inventory of the Xylaria Hill ex Schrank assemblages recorded over the last 36 years (four sampling periods) in a natural protected
area of tropical montane cloud forest, Santuario del Bosque de Niebla, in central Veracruz, Mexico. *New records for Mexico, **New records for
Veracruz, ***Possible new species for science.

Species 1980-1989 1990-1999 2000-2009 2010-2016

1. Xylaria albocinctoides Y.M. Ju, H.M. Hsieh & J.D. Rogers * 0 0 1 152
2. Xylaria allantoidea (Berk.) Fr. 6 0 0 0
3. Xylaria anisopleura (Mont.) Fr. 3 0 3 814
4. Xylaria arbuscula Sacc. 0 0 0 136
5. Xylaria berteroi (Mont.) Cooke ex J.D. Rogers & Y.M. Ju 15 21 19 441
6. Xylaria cubensis (Mont.) Fr. 1851 10 18 0 407
7. Xylaria curta Fr. 3 3 9 63
8. Xylaria feejeensis (Berk.) Fr. 1851 1 2 12 216
9. Xylaria discolor (Berk. & Broome) Y.M. Ju, H.M. Hsieh, J.D. Rogers & Jaklitsch * 0 0 0 1
10. Xylaria grammica (Mont.) Mont. 0 0 1 5
11. Xylaria heliscus (Mont.) J.D. Rogers & Y.M. Ju 0 0 0 3
12. Xylaria hypoxylon (L.) Grev. 0 1 2 3
13. Xylaria ianthinovelutina (Mont.) Fr. 0 0 1 5
14. Xylaria liquidambaris J.D. Rogers, Y.M. Ju & F. San Martín 0 0 0 15
15. Xylaria longipes Nitschke 0 0 0 3
16. Xylaria microceras (Mont.) Berk. 0 0 0 3
17. Xylaria multiplex (Kunze) Fr. 1 0 0 65
18. Xylaria scruposa (Fr.) Fr. 1 2 3 897
19. Xylaria telfairii (Berk.) Sacc. 1 0 0 2
20. Xylaria xylarioides (Speg.) Hladki & A.I. Romero * 0 0 0 6
21. Xylaria sp. 1 0 0 0 6
22. Xylaria sp. 2 0 0 0 21
23. Xylaria sp. 3 *** 0 0 0 36
24. Xylaria sp. 4 ** 0 0 0 6
25. Xylaria sp. 5 ** 0 0 0 1
26. Xylaria sp. 6 *** 0 0 0 21
27. Xylaria sp. 7 ** 0 0 0 1
28. Xylaria sp. 8 0 0 0 6
29. Xylaria sp. 9 ** 0 0 0 3
30. Xylaria sp. 10 ** 0 0 0 3

plings (Fig. 5). During the 2010-2016 sampling period, 16 and beta diversity (β) to gamma diversity (γ), the observed
unique species were found; during the 1980-1989 period, mean alpha diversity accounted for 37% and beta diversity
only one unique species was found. During the other sam- for 63% (Fig. 6).
pling periods, no unique species were found.
Discussion
Gamma diversity This study provides the first historical inventory of Xylaria,
The gamma diversity (γ) (i.e., historically recorded diversity) mycobiota associated with a NPA of TMCF in Mexico (Fig. 1).
of the studied Xylaria assemblages was equal to 30 species. Previous studies of macrofungi, including Xylaria species,
The estimated alpha diversity (α) varied from six to 12 spe- have been carried out throughout the Americas, mainly
cies, with an estimated mean alpha of 10 species. Using an in Argentina, Colombia, Mexico, and the United States of
additive approach to evaluate the contribution of alpha (α) America (Lodge et al., 2008; Hladki and Romero, 2010;

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Chacón et al.: Temporal shifts of a Xylaria assemblage

Figure 2: Rank-abundance curves of the Xylaria Hill ex Schrank assemblage associated with a natural protected area of tropical montane cloud forest,
Santuario del Bosque de Niebla, in central Veracruz, Mexico. Only species with a relative abundance higher than 10% (above dashed line) in a given
sampling period are shown.

Figure 3: Comparison of species richness estimates for a rarefied and extrapolated sample with a size up to double the reference sample. Differences
are considered to be statistically significant when the 95% confidence intervals (C.I.) do not overlap; for overlapping intervals, no differences are
assumed (α=0.05).

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 Chacón et al.: Temporal shifts of a Xylaria assemblage

Figure 4: Dendrograms of the hierarchical clustering of Xylaria Hill ex Schrank assemblages recorded in four sampling periods based on the Jaccard
similarity index. The dendrograms display as continuous lines the divisions for which the SIMPROF test rejects the null hypothesis (assemblages in these
groups have no further structure to explore); the groups of assemblages not separated by the SIMPROF test (at p<0.05) are indicated by dashed lines.

Figure 5: Percentage of total species (n=30) that occur in a natural protected area of tropical montane cloud forest, Santuario del Bosque de Niebla,
in central Veracruz, Mexico, during a given sampling period.

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Chacón et al.: Temporal shifts of a Xylaria assemblage

Figure 6: Contribution of the alpha and beta diversity of Xylaria Hill ex Schrank species recorded in four sampling periods to historical gamma
diversity. The gray bars represent alpha diversity per sampling period, the white bars beta diversity, and the dotted line mean alpha diversity. All
diversities are expressed as a percentage of total recorded species (n=30).

Gómez-Hernández and Williams-Linera, 2011; Soto-Medi- morphospecies may be new species because they are sup-
na and Bolaños-Rojas, 2013; MacGregor-Fors et al., 2015, ported by parsimony phylogenetic analysis of morpholog-
2016; Tapia et al., 2017; Ávalos-Lázaro et al., 2018). Such ical characters (Chacón Zapata, com. pers.). These results
studies vary widely in sampling efforts, collection methods, demonstrate that the NPA of TMCF serves as an important
objectives, and levels of identification, making meaningful refuge for Xylaria diversity and likely for other Ascomycota
comparisons difficult. However, these studies also report species, some of which appear to restrict their distributions
that TMCF maintains a high level of Ascomycota-Xylaria- to this type of vegetation (Tapia et al., 2017).
ceae diversity, which differs in composition and structure The historically recorded number of Xylaria species
among sites within a same region. in the NPA of TMCF is significantly high compared to the
The total number of species and/or morphospecies findings of other studies carried out in the region (Chacón
collected in this study represents nearly 29% of all Xylar- and Medel, 1993; Medel et al., 2008; Medel, 2013). Al-
ia species reported for Mexico (San Martín and Rogers, though a large proportion of species was present in each
1989) and 65% of all Xylaria species recorded for the state sampling period, not all of them were recorded in each
of Veracruz (Medel et al., 2008) (Table 1). In addition, the period (completeness deficits <10%) (Fig. 3). This result
inventory presented in this study increased with 59% the suggests that a consistently longer sampling period over
current number of Xylaria species reported for TMCF by several seasons would be necessary to record most species
Medel (2013). Ten percent of the collected species are present in this NPA. Some studies have reported the signif-
new records for Mexico and the state of Veracruz (Tapia icance of sampling macrofungi, including Xylaria, over peri-
et al., 2017), while six percent are new locality records in ods of several years to record the majority of species pres-
the state of Veracruz. Furthermore, two of the collected ent at a site (Gómez-Hernández and Williams-Linera, 2011;

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Chacón et al.: Temporal shifts of a Xylaria assemblage

MacGregor-Fors et al., 2015, 2016;). Specifically, upon eval- of land use/land cover types) (see Study Area, section at
uating the species diversity of Xylaria during 36 years in a Material and Methods). In fact, we consider that changes
NPA of TMCF, we observed deficits of 9% (1980-1989), 5% in the Xylaria assemblages (i.e., gains in diversity and com-
(2000-2009), 2% (1990-1999), and <0.1% (2010-2016) in positional shifts) are likely related to changes in land use/
the inventory completeness of the different sampling peri- land cover or management of the study area (see Study
ods. These results indicate the difficulty of determining the Area section at Material and Methods). Given that such
number of years of collection that are required to represent changes impact habitat structure or microenvironmental
the majority of Xylaria species in a given habitat. This im- conditions, they may limit or, in this case, favor the ability
plication was previously shown for other macrofungal as- of Xylaria species to colonize or increase their abundance
semblages associated with TMCF fragments in the region inside the TMCF.
near the studied NPA (Gómez-Hernández and Williams-Lin- The human impacts resulting from the management
era, 2011). Given the current scarcity of knowledge of the of the NPA have been historically significant (see Study Area
mycobiota of TMCF and the findings of the present study, section in Material and Methods). Recently, since 2010, a
our results significantly contribute to the data on Xylaria maturation or regeneration process has likely been occur-
assemblages for Mexico and the state of Veracruz. Thus, ring in the protected TMCF, which is supported by sever-
the alpha diversity of Xylaria assemblages can potentially al studies carried out in the area. For example, the same
be used as an indicator parameter of conservation degree NPA was found to harbor an impressive array of macrofungi
of the TMCF (Figs. 2, 3). assemblages that are shaped by resources and conditions
In the comparison of compositional similarity, we at the habitat level (Gómez-Hernández and Williams-Lin-
found two significant clusters or effective communities, sen- era, 2011; MacGregor-Fors et al., 2016). Likely, the natu-
su Jost (2006), of Xylaria assemblages (Fig. 4). This result ral succession and the associated subsequent changes in
indicates that the composition of Xylaria assemblages dif- substrate availability and microclimate, in the studied NPA,
ferentiated over time. This pattern of differentiation in com- may be currently responsible for improving the quality of
position may be explained by species turnover between time habitats available to Xylaria assemblages (see Study Area
periods, which may be related to the relatively high fraction section at Material and Methods).
of species that are specific to each time period and the low In conclusion, this study highlights the value of using
fraction of numerically dominant species (Fig. 5). This result Xylaria assemblages as a bioindicator group and as a means
is consistent with other studies that have investigated the of monitoring the effectiveness of conservation strategies
beta diversity of macrofungal assemblages in the region (Gó- and the impact of management activities over time. Over-
mez-Hernández and Williams-Linera, 2011; MacGregor-Fors all, our results suggest that the temporal dynamics of the
et al., 2015, 2016). Therefore, temporal shifts in species assemblages partly depend on the conservation and man-
turnover suggest that the compositional similarity of Xylaria agement strategies that have been historically implement-
assemblages, and likely of other macrofungi, may be highly ed in the studied NPA. The historical and structural hetero-
dynamic because of the addition and disappearance of new geneity recorded in the NPA may have induced shifts in the
and existing species, respectively, over time. alpha and beta diversity of Xylaria assemblages, which, in
Although the sampling efforts were not identical in turn, may have also influenced the ecological and ecosys-
each sampling period, we estimated a reliable inventory tem processes of the TMCF. Therefore, the present NPA is
over time, reinforcing the verity of the observed changes in demonstrated to be an important habitat for Xylaria, an
the Xylaria assemblages at the study area during the last 36 environmentally sensitive group of macrofungi. Effective
years. The alpha and beta diversity of Xylaria assemblages conservation outcomes for TMCF will only be achieved if
are undoubtedly influenced by local factors (e.g., human current management strategies are maintained and inte-
activity, management of NPA, and natural forest regenera- grated into the long-term management framework of NPAs
tion) and landscape effects (e.g., composition and structure containing TMCF.

Acta Botanica Mexicana 126: e1378 | 2019 | 10.21829/abm126.2019.1378 10

Chacón et al.: Temporal shifts of a Xylaria assemblage

Author contributions Chacón, S. and R. Medel. 1993. Los hongos (principalmente ma-
SC and EUB carried out field and laboratory work. SC, EUB, cromicetos) registrados en el bosque mesófilo de montaña
and MAGM analyzed and interpreted the results. SC, EUB, de México. In: Marmolejo, G. J. and F. Garza-Ocañas. Contri-
and MAGM wrote the manuscript. All authors read and ap- buciones micológicas en homenaje al Biólogo José Castillo
proved the final manuscript. Tovar por su labor en pro de la micología mexicana. Reporte
Científico No. especial 13. Facultad de Ciencias Forestales,
Funding Universidad Autónoma de Nuevo León. Linares, México. Pp.
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30861 (Diagnóstico para la conservación de la diversidad Vol. II: Estado de conservación y tendencias de cambio. Cd.
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