@ BioRisk

BioRisk 21: 11-18 (2023)
DOI: 10.3897/biorisk.21.108551

Short Communication

Biomonitoring with bryophytes in managed forested areas.
Three examples from the southern Italian Apennines

Carmine Colacino'®

1 Scuola di Scienze Agrarie, Forestali, Alimentari e Ambientali (SAFE), Universita degli Studi della Basilicata, Potenza, Italy
Corresponding author: Carmine Colacino (carmine.colacino@unibas. it)

OPEN Qaceess

Academic editor: Pavel Stoev
Received: 23 June 2023
Accepted: 28 September 2023
Published: 27 October 2023

Citation: Colacino C (2023)
Biomonitoring with bryophytes in
managed forested areas. Three
examples from the southern Italian
Apennines. BioRisk 21: 11-18. https://
doi.org/10.3897/biorisk.21.108551

Copyright: © Carmine Colacino.

This is an open access article distributed under
terms of the Creative Commons Attribution
License (Attribution 4.0 International -

CC BY 4.0).

Abstract

Three sites in the southern Italian Apennines were selected to assess correlation be-
tween forest structure and bryophyte flora. In two of the sites, the Index of Air Purity
(IAP)—based on cover data of epiphytic bryophytes—was evaluated. The results show
that bryophyte populations—and consequently |AP—are affected by forest structure and
development, and that studies including different sites require a precise assessment of
silvicultural characteristics to allow comparisons. Indicator values of mosses and liver-
worts were also taken into consideration in characterizing ecologically the three sites.

Key words: Bryophyte Flora, forest structure, IAP, indicator values, silviculture

Introduction

Bryophytes are a popular tool for the assessment of air quality in polluted urban
areas, showing, together with lichens, all the necessary characteristics for a good
bioindicator. They are sensible to polluting agents, stay in place in the area of
study, have wide distribution and a life cycle sufficiently long, and they can accu-
mulate pollutants in their body (Aleffi 1998; Govindapyari et al. 2010). De Sloover
proposed in 1964 an Index of Atmospheric Purity (IAP) to assess air pollution
and based on cover data of epiphytic lichens (De Sloover 1964; De Sloover and
LeBlanc 1968) and epiphytic bryophytes (LeBlanc and De Sloover 1970). The IAP
is extensively applied in cities and urban areas (e.g., Aleffi 1992; Dymytrova 2009;
Zechmeister and Hohenwallner 2006) to supplement static and mobile monitors
(for CO, CO,, SO,, O,, NO,), or satellite monitoring systems to assess particulate
matter pollution, ground-level ozone, carbon monoxide and other major contam-
inants in wider areas. The limit of these monitoring devices is that they do not
give information about the effects of air contaminants at the ecological level. The
aim of this study is to verify the use of the IAP method (selected because of its
widespread use and the possibility to have comparable results) in the assess-
ment of environmental pollution in managed forested environments. Cryptogam-
ic communities are conditioned by the developmental stage of the forest (Bark-
man 1958), and bryophytes, in particular, are important ecological components
of managed forests. Bryophyte flora and vegetation provide information on the
conditions of a forested area, its structure, ecology and climate at a given time

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

(Brunialti et al. 2010). To further characterize ecologically the areas under study,
and to evaluate the effectiveness of the Indicator Values of Mosses and Liver-
worts (Dill 1991), non-epiphytic bryophyte species have been considered. These
indicator values were originally developed for Central Europe, but they appear to
be usable also in internal mountain areas of southern Italy. The numerical values
of these ecological indicators (varying from 1 to 9) are: Light number (L), from
deep shade plants to full light plants. Temperature number (T), from cold to ex-
treme warm indicators (from alpine to lowland, or from the Arctic to the Mediterra-
nean zone). Continentality number (C), from euoceanic to eucontinental (from the
Atlantic coast to the interior of Eurasia). Moisture number (M), from great dryness
to permanently wet or sprayed, near waters or waterfalls, in water). Reaction num-
ber (R), from strong acid to base and lime indicators. The Median value is then
calculated. Chorological values were also considered, but are not presented here.

Material and methods

The study sites were analyzed by determining their flora (bryological and vas-
cular), climate, geology, pedology. Plots were established and silvicultural pa-
rameters calculated (tree-structure and developmental stage).

The IAP (sites A and B) was calculated according to the method presented by
LeBlanc and De Sloover (1970) as partially modified by Nimis (1990). In particu-
lar, (1) a 60 x 50 cm grid-divided into 20 units of 10 x 15 cm-was placed on the
trunk of each tree at a height (lower side) of 80-100 cm, in areas with the highest
bryophyte density; (2) The IAP was calculated based on the following formula:

n
IAP = 2, (Qixfi/10),
i=1
where f, is an index of frequency/cover varying from 1 to 5; Q. is the number of
species accompanying any other species in each relevée (a factor of resistance
to pollution).

The division by 10 is arbitrary and was indicated in the original formula by LeB-
lanc and De Sloover (1970) to obtain smaller numbers. These values are based
on the diversity of epiphytic bryophyte populations, on the resistance to pollution
of each species, on the phorophytes, and, in our case, on the forest structure and
stage of development. Values of IAP recorded in the literature in urban areas
vary according to the distance from the pollution source and the ecological con-
ditions of the site (Nimis 1999). Values may vary from close to zero (indicating
air pollution) up to values of 50 or more (indicating lack of air pollution).

The bryophyte vegetation was considered in three sites: (Site A) a managed
forested area with Quercus cerris L. (Turkey oak) prevalent, and Quercus pu-
bescens Willd. (Downey oak) sporadic, near an Oil hub; (Site B) a forested area
with Fagus sylvatica L. (Beech). The IAP was determined in both sites; (Site C) a
mountain area with a Fagus sylvatica-Abies alba Mill. (Beech-Silver fir) coenosis.
The Indicator Values of mosses and liverworts were calculated for all three sites.

Site A

The area of study is situated in a plain near the Oil Hub of Viggiano (Locality Ref-
esa, Province of Potenza, Basilicata) in the Valley of the river Agri at an altitude of

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 12

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

610-620 m, in the heart of the southern Apennines. The geology is complex, in the
area considered there is limestone, shale, flysch, and varicolored clay. The soil is
various—of alluvial origin under the plots. Climate is Mediterranean with dry sum-
mers and the rains occurring mainly from October to February (max. in November,
87.3 mm). Average annual temperature is 12.4 °C. Coldest month average 4.5 °C.
Warmer month average 21.6 °C. The De Martonne Aridity Index was calculated,
its value (24.3) indicating a sub-humid climate. Overall, a Mediterranean climate
of the sub-humid type. According to a recent vegetation classification of Italy this
area is included in the temperate region, meso-temperate zone, southern Apen-
nines, neutro-subacidophilous series of Turkey oak (Di Pietro et al. 2010).

Three plots were selected and the usual dendrometry parameters measured
(height, dbh, growth estimate, basal area, etc.). The wood is relatively young
and the prevalent species is Turkey oak, with the sporadic presence of Downey
oak. Sampling occurred in 2003 and then again in 2008. In the first plot the
management is simple coppice (low forest) with an average age of 13-14
years (in 2003, 18-19 in 2008). The second plot is inwards with older trees
(about 30 years, then 35) and represent an aged coppice in conversion into high
forest. The third plot is a coppice-with standards stand, with larger diameters
and more spaced trees.

Site B

Mount Paratiello is situated to the west of the town of Muro Lucano (Province of
Potenza, Basilicata), in the southern Apennines, in the basin of torrents-some
with a more or less continuous flow of water, others with seasonal regimes—
tributary to the river Sele. The altitudes vary from 500 to 1400 m. Prevalent
expositions N, NE, NW. Geologically young, the erosion has exposed limestone
from the Cretaceous. Soils belong to the southern brown earths. The climate is
Mediterranean with dry summers and rains occurring mainly from September
to March (max. in December, 163 mm). Average annual temperature is 14.3 °C.
Coldest month average 2.2 °C. Warmer month average 30.4 °C (data 2000-
2010). The Aridity Index of De Martonne is 46.8 indicating a humid climate.
According to a recent vegetation classification of Italy this area is included in
the temperate region, lower supra-temperate zone, southern Apennines, neu-
tro-basiphilous series of beech (Di Pietro et al. 2010).

The main species in the plots is Fagus sylvatica (beech). The forest is quite
old and was exploited heavily in the past (1700-1860). Some studies (e.g,.,
Susmel 1957) concluded it should be managed to get an uneven-aged struc-
ture, but it has always been managed as an even-aged system. Two plots were
selected, at 1356 m, and at 1423 m. The main difference between the two plots
is the time of last cutting, more recent in the first one (trees with smaller diam-
eters). Another factor affecting the plots is the slope, steeper at 1424 m-at the
tree vegetational limit, and more subject to erosion.

Site C

The population of silver fir on the northern slopes of Mount Motola (Teggiano,
Province of Salerno, Campania) represents the most important relict association
of silver fir in Campania, where it is associated with the beech. It is included in

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 13

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

the National Park of Cilento and Vallo di Diano, one of the largest in Italy. The
habitat belongs to the group of Mediterranean deciduous forests: “Apennine
beech forests with Abies alba”. At lower altitudes (800 to 900 m) Corylus avellana
L. (Hazelnut) is found in areas previously cultivated. The slopes show a series of
terraces supported by stone-walls, eroded by flowing rainwaters. At around 1000
m sparse and isolated individuals of silver fir are found, mostly in hollows and in
areas of difficult access. The hazelnut stands still maintain the original density
of plantation and the stools feature a high number of shoots, which form a dense
and continuous cover not colonized by other species. This area (in the submon-
tane belt up to about an altitude of 800-900 m) belongs to the mixed forest of
mesophile and meso-xerophile broadleaf trees (e.g., Pignatti et al. 2004) made
up by maples (Acer campestre L., Acer opalus Mill. subsp. obtusatum (Waldst. &
Kit. ex Willd.) Gams, Acer lobelii Ten.), European hop hornbeam (Ostrya carpinifo-
lia Scop.), Chestnut (Castanea sativa Miller), Italian alder (A/nus cordata (Loisel.)
Desf.), Bigleaf linden (Tilia platyphyllos Scop.). Climate is cold-humid, Temperate
Oceanic, without noticeable temperature extremes. Rains are well distributed
during the year. Soils are well aerated brown earths, with an abundant litter layer
and good water retention. Geologically limestone prevails (Saracino et al. 2005;
Cipollaro and Colacino 2005). According to a recent vegetation classification of
Italy this area is included in the temperate region, lower supra-temperate zone,
southern Apennines, neutro-basiphilous series of beech (Filesi et al. 2010).

Results

The main silvicultural and bryological (Indicator Values) results are presented
for each of the areas considered. (Plots have a diameter of 20 m, and are locat-
ed at a distance of 60 m one from the other.)

P=Plot; TBA=Total Basal Area (m?); ABA=Average Basal Area (m?); AD Aver-
age Diameter (cm, min.-max). I[AP=Index of Air Purity (Sites A and B only).

Site A — Quercus cerris (Turkey oak)

Year 2003:

- P1: #trees 402 - TBA 1.873 - ABA 0.005 — AD 8 (03-21) - IAP=0.32
- P2: #trees 278 —- TBA 2.581 - ABA 0.009 — AD 11 (03-36) — IAP=0.43
- P3: #trees 143 - TBA 2.568 —- ABA 0.018 — AD 15 (06-31) — IAP=0.37

Year 2008:
- P1: #trees 422 - TBA 3.597 — ABA 0.008 — AD 10.5 (05-19.0) — IAP=1.10
- P2: #trees 243 - TBA 4.120 — ABA 0.023 — AD 14.5 (05-37.0) — IAP=0.80
- P3: #trees 167 — TBA 3.909 — ABA 0.018 — AD 17.0 (05-37.0) — IAP=0.70
- P4: #trees 364 — TBA 1.962 — ABA 0.005 — AD 8.0 (05-23.5) — IPA= NC

Indicator Values of mosses and liverworts:

- L=7 (Semi-light plants, in full indirect light, but also occurring in shade).
T = 4 (between moderate warm and cool). C = 5 (Intermediate, between

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 14

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

sub-Mediterranean and sub-boreal). M = 4 (places moderately fresh be-
coming dry for long periods). R = 6 (between moderate acid and weakly
acid to weakly basic indicator).

Site B — Fagus sylvatica (Beech)

- P1 1356 m: #trees 288 —- TBA 4.635 — ABA 0.016 — AD 14.5 (5-69) -
IAP=2.2

* P2 1423 m: #trees 152 - TBA 6.601 — ABA 0.043 — AD 23.0 (5-60) -
IAP=4.0

Indicator Values of mosses and liverworts:

* L=7 (Semi-light plants, in full indirect light, but also occurring in shade).
T = 3 (cool). C = 5 (Intermediate, between sub-Mediterranean and sub-bo-
real). M= 4 (places moderately fresh becoming dry for long periods). R = 6
(between moderate acid and weakly acid to weakly basic indicator).

Site C - Fagus sylvatica-Abies alba (Beech-Silver fir) coenosis

- P1900 m: #trees 438 - TBA 18,4 — ABA 0.042 — AD 23.1 (Beech)
- P1900 m: #trees 275 — TBA 18,5 — ABA 0.067 — AD 29.3 (Silver fir)
* Sporadic presence of Bigleaf linden, Hungarian maple and Chestnut:
TBA 3.75.
- P2 1100 m: #trees 703 — TBA 30.2 - ABA 0.043 - AD 23.4 5 (Beech)
- Sporadic presence of European hop hornbeam, Hungarian maple and
Italian alder. Silver fir (sub-canopy) TBA 2.5.

Indicator Values of mosses and liverworts:

- 700-900 m: L = 5 (semi shade plants), T = 5 (moderate warmth), C=5 (in-
termediate), M = 7 (moisture), R =7 (weakly acid to weakly basic).

- 1000-1300 m:L = 5 (as above), T = 4 (Sub-Oceanic), C = 5 (as above), M = 7
(as above), R = 6 (between moderate acid and weakly acid to weakly basic).

In this site the study has been focused on the bryophyte flora and the silvicul-
tural aspects, from lower to higher altitudes. No IAP was calculated.

Discussion

Site A — The silvicultural data show there has been, as expected, an increase
in the average diameters in the three plots after 5 years, which is reflected
also in the values of total and average basal areas. This increase in diameter
has affected the number of epiphytic bryophyte species recorded. Downey
oak was not considered in the measurements, being a much better phoro-
phyte. Plot 4 of 2008 was made up of very young plants with smaller diame-
ters, too small to have any significant epiphytic vegetation. [AP could not be
calculated (NC). Overall, TBA values appear low, indicating a forest in the first
stages of development. The Indicator values of mosses and liverworts—re-

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 15

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

flecting the general ecological conditions of the site-have not changed from
2003 to 2008, as expected.

Site B — Plot 1 was cut more recently than Plot 2, as indicated, altering the
number of epiphytes capable to attach and grow on the bark, and resulting in
different IAP values. These values, in both plots, are quite low, not much differ-
ent from those obtained in Site A which was exposed to pollution. This may be
due to the type of forest management applied, with younger trees prevailing, and
lacking the time to reach an equilibrium (as shown by low TBA values). The Indi-
cator values appear to be almost identical in the two plots. Plot 1 has the same
values, while Plot 2 diverges only for M = 3 (dryness); this is due to its position
near the tree line and the uppermost montane grassland (edge effect) exposing
to the sun the bryophytes from the inside, as it was shown by Hylander (2005).

Site C — This forest is characterized by silver firs. Beeches become more fre-
quent in the higher parts of the submontane belt, as compared to other broad-
leaf trees (Plot 1). In this belt, the presence of all diametrical classes of silver
firs in reproductive age has been recorded (an abundant production of cones
was observed during Fall 2002). Silver firs here are taller than beeches, and
their canopy is directly exposed to sun rays. Their spatial distribution varies
from isolated plants within a stand of beeches, to pure populations with an
extension of even a few thousand square meters exhibiting the micro-environ-
mental conditions of pure silver fir forests. At higher altitudes (Plot 2) beeches
become the dominant trees and silver firs almost disappear (even though old
big stumps and rotting logs are still visible). Silver firs are still relatively abun-
dant in the sub-canopy layers as individuals of about 1-4 m of height in a “wait-
ing” phase, many with the vegetative apex damaged by grazing or by contact
with branches of higher trees. The Indicator values show that bryophytes of
xeric or Mediterranean environments prevail at lower elevations, while at higher
elevations, at the tree line, species with a sub-Oceanic (and sub-Mediterranean)
ecology prevail, as expected given the different ecological conditions previous-
ly indicated.

Conclusions

The values of IAP obtained in this study need consideration, and an explana-
tion. These values are lower in Site A, near a source of pollution, and higher in
site B, with no apparent pollution source, as expected. The IAP values in site B,
however, are much lower than those normally obtained in unpolluted urban ar-
eas. This may be related to the silvicultural management systems applied, with
frequent cutting of trees and resulting low TBAs, altering adversely bryophyte
diversity because of their vulnerability to microclimatic changes (Perhans et
al. 2009). Further study is required to compare IAP values from forest sites to
those obtained in urban areas; the determination of correction factors (possi-
bly based on TBA values, and phorophyte selection) is necessary. A preliminary
strategy—limited to forested areas, would be to consider stands at the same
stage of development and with comparable management systems, better if
aged (Hébrard 1989). The effectiveness of the Indicator values for mosses and
liverworts for the areas considered was verified both spatially (sites A, B, and
C) and temporally (site A).

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 16

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

Acknowledgments

| thank colleagues and students who assisted me in the field in some of the
studies reported here. Among them, | thank in particular, Enza Evangelista, Car-
mine D’Avella, and Filippo Verova.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

Financial support from my Department (SAFE) is kindly acknowledged.

Author contributions

The author solely contributed to this work.

Author ORCIDs
Carmine Colacino © https://orcid.org/0000-0002-2675-8835

Data availability

All of the data that support the findings of this study are available in the main text or
Supplementary Information.

References

Aleffi M (1992) Flora briologica e qualita dell’aria nella citta di Jesi (Marche — Italia cen-
trale). Archivio Botanico Italiano 67: 128-140.

Aleffi M (1998) Bioindicatori a livello di organismi vegetali: le Briofite. In: Sartori F (Ed.)
Bioindicatori ambientali, 102-112.

Barkman JJ (1958) Phytosociology and Ecology of Cryptogamic Epiphytes. Van Gor-
cum, Assen, 628 pp.

Brunialti G, Frati L, Aleffi M, Marignani M, Rosati L, Burrascano S, Ravera S (2010) Li-
chens and bryophytes as indicators of old-growth features in Mediterranean forests.
Plant Biosystems 144(1): 221-233. https://doi.org/10.1080/11263500903560959

Cipollaro S, Colacino C (2005) Bryoflora of the beech-silver fir coenosis of Mount Motola
(National Park of Cilento & Vallo di Diano) — Teggiano (Salerno, S-Italy). Flora Medi-
terranea 15: 385-396.

De Sloover J (1964) Végétaux épiphytes et pollution de l’air. Rev. Questions scientifiques
25:°531-5611..

De Sloover J, LeBlanc F (1968) Mapping of atmospheric pollution on the basis of lichen
sensitivity. In: Misra R, Gopal B (Eds) Proceedings of the Symposium in Recent Ad-
vances in Tropical Ecology. Banaras Hindu Univ., Varanasi, 42-56.

Di Pietro R, Fascetti S, Filibeck G, Blasi C (2010) Le serie di vegetazione della regione
Basilicata. In: Blasi C (Ed.) La Vegetazione d'Italia. Palombi, Roma, 375-389.

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 17

Carmine Colacino: Biomonitoring with bryophytes in southern Italian Apennines

Dill R (1991) Indicator Values of Mosses and Liverworts. In: Ellenberg H, Weber E, Diull
R, Werner W, Pauliben D (Eds) Indicator Values of Plants in Central Europe. Goltze,
Gottingen, 175-214.

Dymytrova L (2009) Epiphytic lichens and bryophytes as indicators of air pollution in
Kyiv city (Ukraine). Folia Cryptogamica Estonica 46: 33-44.

Filesi L, Rosati L, Paura B, Cutini M, Strumia S, Blasi C (2010) Le serie di vegetazione della
regione Campania. In: Blasi C (Ed.) La Vegetazione d'Italia. Palombi, Roma, 351-373.

Govindapyari H, Leleeka M, Nivedita M, Uniyal PL (2010) Bryophytes: Indicators and
monitoring agents of pollution. NeBio 1: 35-41.

Hébrard JP (1989) Etude comparée de la végétation bryophytique des troncs de chéne
vert et de chéne pubescent (Peuplement agés) dans la forét domaniale de La Gardi-
ole de Rians (Var, France). Cryptogamie. Bryologie, Lichenologie 10: 253-266.

Hylander K (2005) Aspect modifies the magnitude of edge effects on bryophyte growth
in boreal forest. Journal of Applied Ecology 42(3): 518-525. https://doi.org/10.1111/
j.1365-2664.2005.01033.x

LeBlanc F, De Sloover J (1970) Relation between industrialization and the distribution
and growth of epiphytic lichens and mosses in Montreal. Canadian Journal of Botany
48(8): 1485-1496. https://doi.org/10.1139/b70-224

Nimis PL (1990) Air quality indicators and indices: the use of plants as bioindicators
for monitoring air pollution. In: Colombo AG, Premazzi G (Eds) Proc. Workshop Indi-
cators and Indices for Environmental Impact Assessment and Risk Analysis. Ispra
(Italy), May 1990, JRC (Ispra), 93-126.

Nimis PL (1999) Linee-guida per la bioindicazione degli effetti dell’inquinamento tramite
la biodiversita dei licheni epifiti. In: Piccini C, Salvati S (Eds) Atti Workshop Biomonit-
oraggio Qualita dell’Aria sul Territorio Nazionale. ANPA Atti 2: 267-277.

Perhans K, Appelgren F, Jonsson F, Nordin U, Sd6derstr6ém B, Gustafsson L (2009) Re-
tention patches as potential refugia for bryophytes and lichens in managed forest
landscapes. Biological Conservation 142(5): 1125-1133. https://doi.org/10.1016/j.
biocon.2008.12.033

Pignatti G, Terzuolo PG, Varese P Semerari P Lombardi VN (2004) Criteri per la definizione
di tipi forestali nei boschi dell’Appennino meridionale. Forest@ 1: 112-127. https://
doi.org/10.3832/efor0229-0010112

Saracino A, Colacino C, Esposito L, Curcio B, Cipollaro S (2005) II consorzio faggio-abete
bianco del Monte Motola di Teggiano (SA): Aspetti selvicolturali e primo contributo
alla brioflora. S.I.S.E.F. Atti 4: 165-171.

Susmel L (1957) Premesse storico-climatiche e bio-ecologiche alla selvicoltura della
foresta montana appenninica. Annali Accademia economico-agraria dei Georgofili
4: 3-42.

Zechmeister HG, Hohenwallner D (2006) A comparison of biomonitoring methods for
the estimation of atmospheric pollutants in an industrial town in Austria. Environ-
mental Monitoring and Assessment 117(1-3): 245-259. hhttps://doi.org/10.1007/
$10661-006-0991-y

BioRisk 21: 11-18 (2023), DOI: 10.3897/biorisk.21.108551 18