Mapping environmental effects of agriculture with epiphytic lichens

© 2005 Science From Israel / LPPLtd., Jerusalem

Israel Journal of Plant Sciences Vol. 53 2005 pp. 115–124

*Author to whom correspondence should be addressed. E-mail:

Mapping environmental effects of agriculture with epiphytic lichens

SERENA RUISI,a LAURA ZUCCONI,a,* FRANCESCA FORNASIER,b LUCA PAOLI,c LUISA FRATI,c AND STEFANO LOPPIc

aDipartimento di Scienze Ambientali, Università di Viterbo, Largo dell’Università, 01100 Viterbo, Italy bARPA Lazio (Agenzia Regionale per la Protezione Ambientale), via G. Garibaldi 114, 2100 Rieti, Italy

cDipartimento di Scienze Ambientali “G. Sarfatti”, Università di Siena, via P.A. Mattioli 4, 53100 Siena, Italy

(Received 26 May 2004 and in revised form 11 July 2005)

ABSTRACT

The present paper reports the results of a study designed to check the feasibility of epiphytic lichens as biomonitors of the effects of agriculture in an area of central Italy without heavy industrialization and with an economy mainly based on agricul-ture. The exclusion of nitrophytic species (objectively selected using the on-line check-list of Italian lichens) from the calculation of the index of lichen diversity, which is supposed to reflect air quality, led to more realistic results. Conversely,the use of only nitrophytic species allowed us to map the eutrophication in the area, which resulted in lichens heavily affected by agricultural activities. Mapping using only strictly nitrophytic species showed two “hot spots” where ammonia emission from animal husbandry plays an important role. Two sites emerged as suffering at the same time from ammonia and NOX pollution. It is concluded that epiphytic lichens are an effective tool to detect and map the effects of agriculture also in Mediterranean countries, at least in areas without heavy industrialization, given the proper species selection.

Keywords: ammonia, biomonitoring, dust, Mediterranean basin, nitrogen

INTRODUCTION

Agricultural activities result in increased emissions and deposition of nitrogen compounds. In Europe, the NH3 emission from animal breeding is one of the main sources of atmospheric nitrogen (Lee and Longhurst, 1993; Fangmeier et al., 1994); with regard to total N (NO3, NOx, and N2O) emissions, agriculture is by far the largest source (Krupa, 2003). Besides the potential acidifying effect, N depositions have a fertilizing role on ecosystems, causing changes in vegetation and soil microflora and mi cro fauna in areas where critical loadsare exceeded (Rosén et al., 1992; Krupa, 2003), and significantly contributing to forest decline in Europe(Krupa, 2003).

Nitrogen, mainly deposited as ammonia, ammonium, and nitrate, may strongly influence lichen-dominatedecosystems (Crittenden et al., 1994; van Dobben et al., 2001). Ammonia and ammonium, as by-product, from animal manure have a high deposition rate. Ammonia

is emitted to a low altitude and thus deposited near the emission sources (Sutton and Fowler, 2002; Krupa, 2003). Ammonia, ammonium, and nitrate reach lichen thalli mainly as dry deposition, and lichens have an extraordinary capacity to capture nitrogen (Søcthing, 1995). Studies of ammonia uptake and loss by a range of lichen species have been carried out by Miller and Brown (1999).

In bioindication studies of air pollution by epiphytic lichens, the inclusion of nitrophytic species has been questioned, since relatively high values could be deter-mined by eutrophication (defined by Nixon (1995) asan increase in the rate of supply of organic matter in an ecosystem), more than by air quality (van Herk, 2001). In fact, eutrophication is not necessarily associated with a decrease in lichen diversity but with a change in species composition, where acidophytic lichens are

Israel Journal of Plant Sciences 53 2005

116

replaced by nitrophytic ones; increases in the abundance of nitrophytic lichens, correlated with increases in N deposition and decreases in SO2 concentrations and/or S deposition (acidification), were reported in Finland(Poikolainen et al., 1998) and The Netherlands (van Dobben and Ter Braak, 1999). Long-distance transport of nitrogen air pollution strongly influences the occur-rence of acidophytic lichen species in Europe and consti-tutes a threat to natural populations that has so far been strongly underestimated (van Herk et al., 2003). The use of nitrophytic species could instead represent an effec-tive tool for mapping the effects of ammonia pollution, as has been proposed for The Netherlands (van Herk, 1999). However, nitrogen effects may be hampered by the dominating effect of dust when using such mapping techniques in areas with a warm and dry climate, such as the Mediterranean basin (Loppi and De Dominicis, 1996).

According to Loppi (2004), lichen bioindication of air pollution produces more realistic results by ex-cluding nitrophytic species in calculating any index of lichen diversity. Moreover, monitoring of ammonia pol-lution and nitrogen deposition is feasible using region-ally selected indicator species.

The present study was designed to check the feasi-bility of epiphytic lichens as biomonitors of the effects of agriculture in an area of central Italy without heavy industrialization and with an economy mainly based on agriculture.

MATERIALS AND METHODS

Study area

The study was carried out in the Municipality of Viterbo (Latium, central Italy), which extends over an area of 400 km2 with about 59,000 inhabitants (Fig. 1). Climate is sub-Mediterranean, with mean annual temperature of 14.3 °C and mean annual rainfall of 807 mm, con-centrated in autumn and winter, while summer is fairly dry; prevailing winds are from the NNE (Provincia di Viterbo, 2002). Land morphology is hilly, and woody areas are dominated by deciduous oaks. Agriculture is practiced extensively. Air pollution is substantially lim-ited to the urban area of Viterbo, with domestic heating and vehicle traffic as the main sources of pollutants(98% of the NO2 recorded values range between 0 and 90 µg m–3, and SO2 is practically negligible) (Provincia di Viterbo, 2002).

Sampling design

The study area was systematically divided following the network used for monitoring the effects of air pollu-tion in forest ecosystems (European net EU-UN/ECE).

Sixteen 1 × 1 km primary sampling units (PSUs) were selected at the intersection of a 6 × 6-km grid (Fig. 1). Two PSUs (1a and 1b) were located outside of the limits of the Viterbo Municipality, to monitor the NW portion of the survey area. Each PSU was divided into four sec-tors of 500 × 500 m, and each sector was divided into four subsectors of 250 × 250 m. Within each subsector, secondary sampling units (SSUs) were positioned, corre-sponding to circular areas with a radius of 125 m.

Sampling tactic

The three suitable trees closest to the center of the four SSUs nearest to the center of each PSU were sampled. If trees were not available in the SSU selected, other sub-sectors were sampled by shifting the SSUs, following the standard procedure reported by Asta et al. (2002).

Trees were deemed suitable if well lit, with girth >70 cm, with trunk nearly straight, not damaged, and without parts with >25% cover of bryophytes. Quercus pubescens Willd. was selected as phorophyte and where absent it was replaced by trees with similar bark prop-erties, such as Quercus cerris L., Tilia spp., and Casta-nea sativa Miller.

Lichen sampling

For each tree, an index of lichen diversity (ILD) was calculated as the sum of frequencies of epiphytic lichens in a sampling grid consisting of four 50 × 10-cm lad-ders, each divided into 5 10 × 10-cm quadrants. This

Fig. 1. Survey area. Limits of the Viterbo Municipality with the location of the 16 PSUs at the intersection points of a 6 × 6-km grid.

Ruisi et al. / Monitoring ammonia with lichens

117

grid was positioned on the trunk at the four cardinal sides, 1 m from the ground. The ILD values of the PSUs were taken as the arithmetic means of the ILD values measured for each tree. In the case of identification prob-lems during field sampling, specimens were collectedand identified later in the laboratory.

Data interpretation

To interpret the ILD values in terms of air pollution, a scale of environmental alteration was calculated follow-ing the suggestions of Loppi et al. (2002). Naturality for sub-acid barked trees in the study area was estimated by means of 10 samplings from the Monte Casoli Nature Reserve of Bomarzo (Viterbo), close to the study area. The resulting interpretative scale is reported in Table 1.

Following the suggestions of Loppi (2004), in a suc-cessive step, nitrophytic species were excluded from the calculation of the ILD. Nitrophytic species (Table 2) were selected using the “floristic query interface” ofthe on-line checklist of Italian lichens (Nimis, 2003), asking for the epiphytic species of Latium with an indicator value for eutrophication of 4 (rather high eutrophication) or 5 (very high eutrophication). Strictly nitrophytic species, i.e., those with an indicator value for eutrophication from 4 to 5 were Candelariella re-flexa, Phaeophyscia orbicularis, Physcia dubia, and Physconia grisea.

To interpret the additional ILD values calculated:

• without the frequency of nitrophytic species (ILDNN), thus using species with a eutrophication index value from 1 to 3;

• only with the frequency of nitrophytic species (ILDN) (species with a eutrophication index value corresponding to 4 and/or 5, without excluding those assuming also lower values), expected to reflect theeutrophication in the area;

• only with the frequency of strictly nitrophytic species (ILDSN) (species with a eutrophication index value corresponding to 4 and/or 5), expected to reflect am-monia deposition;

three different interpretative scales were calculated, with class width equal to the standard deviation of the data.

Mapping

Two-dimensional maps were drawn using the SURFER plotting program (Golden Software Inc., Golden, Colo-rado, USA), which transforms discrete data into a con-tinuous distributional model, using kriging (geostatic autocorrelation of the nearest randomly placed value to produce an estimate of minimum least-squares vari-ance) with a linear variogram model as an interpolation algorithm.

Table 1Interpretative scales of ILD values in terms of environmental alteration

Environmental ILD, ILDNN, excluding ILDN, with only ILDSN, with strictly alteration all species nitrophytic species nitrophytic species nitrophytic species

very high 0 0 >60 >15high 1–40 1–20 41–60 11–15moderate 41–80 21–40 21–40 6–10low 80–120 41–60 1–20 1–5negligible >120 >60 0 0

Table 2Nitrophytic epiphytic species of Latium—humid sub-mediterranean belt (according to Nimis, 2003). Species found in the

present survey are in boldAmandinea punctata Hyperphyscia adglutinata Physcia dimidiataCaloplaca cerina Lecanora chlarotera Physcia dubiaCaloplaca cerinella Lecanora hagenii Physcia stellarisCaloplaca cerinelloides Lecanora umbrina Physcia tenellaCaloplaca herbidella Lecidella elaeochroma Physcia vitiiCaloplaca obscurella Phaeophyscia cernohorskyi Physconia distortaCaloplaca pyracea Phaeophyscia chloantha Physconia enteroxanthaCaloplaca ulcerosa Phaeophyscia hirsuta Physconia griseaCandelaria concolor Phaeophyscia orbicularis Ramalina canariensisCandelariella reflexa Physcia adscendens Xanthoria fallaxDiploicia canescens Physcia aipolia Xanthoria parietinaDiplotomma alboatrum Physcia biziana


118

Tabl

e 3

Spec

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ound

in th

e st

udy

area

with

thei

r mea

n fr

eque

ncy

in e

ach

PSU

Spec

ies

Sam

plin

g si

tes (

PSU

)

1a

1b

1 2

3 4

5 6

7 8

9 10

11

12

13

14

Acro

cord

ia sp

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0.6

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dine

a pu

ncta

ta

(H

offm

.) C

oppi

ns &

Sch

eid.

–

0.5

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8 –

0.1

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apty

chia

cili

aris

(L.)

Kör

b.

1.9

– –

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thon

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a (P

ers.)

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. 0.

8 0.

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121

RESULTS

During the present survey, 136 trees were sampled and 111 infrageneric taxa of epiphytic lichens were found (Table 3). The genera with the highest number of species were Physcia (8 species), Pertusaria (6), Phys-conia (6), Melanelia (6), Lecanora (5), and Phaeophys-cia (4). Physcia adscendens was the most common spe-cies, recorded within all PSUs with a high frequency.

Foliose species were dominant (72.4%), while crus-tose and fruticose ones accounted for 25.1% and 2.5%, respectively. Almost all species (99.6%) had green algae

different from Trentepohlia as photobiont, which have a photosynthetic optimum in very sunny situations. Of the lichens found, 65% reproduce asexually, mostly by soredia (62.2%), and 35% reproduced sexually.

The ILD map (Fig. 2a), which is supposed to reflectthe air quality of the area (Asta et al., 2002), evidenced a general picture of low to negligible environmental alteration.

The map of ILD values excluding nitrophytic species (Fig. 2b) showed a high environmental alteration SW of the town of Viterbo, i.e., in the direction of prevailing winds, and around station 3, where a dump is located.

Fig. 2. ILD maps of: (a) whole epiphytic species; (b) excluding nitrophytic species; (c) nitrophytic species; (d) strictly nitro-phytic species. Note that high values in maps a and b correspond to low pollution, while high values in maps c and d correspond to high pollution.


122

Although direct measurements of air pollutants in the area are not available, this new map seemed to better reflect the air pollution status in the area, evidencing ahigh environmental alteration around the main urban area. (It should be taken into account that following the sampling design, a station within the town of Viterbo was not sampled.)

The map of ILD values with only nitrophytic species (Fig. 2c), expected to reflect the eutrophication in thearea, showed that most of the municipality is subjected to high or very high enrichment of nutrients. This map seemed in line both with the agricultural activities carried out throughout the area and the consequent influence of dust from arable lands. It is important tonote that PSU 14, which is located in the Nature Reserve of Lake Vico, did not show eutrophication.

The map of ILD values with strictly nitrophytic species (Fig. 2d), supposed to reflect ammonia concen-trations in the air, showed two peaks, one around station 4, and the other in a belt encompassing stations 10 and 13. No direct atmospheric NH3 measurement was avail-able, but the area in the vicinity of these two peaks is heavily exploited for sheep, pig, and cattle breeding. However, as PSUs 10 and 11 are located SW of Viterbo in the direction of prevailing winds, a possible role of NOX or other nitrogen compounds should also be con-sidered.

DISCUSSION

Nutrient input can affect lichen vegetation either by direct application (e.g., farming), or indirectly through atmospheric deposition, especially close to emission sources. Both natural hypertrophication from grazing animals (wind-blown dust from excreta and urine) and artificial hypertrophication from application of fertiliz-ers lead to nutrient enrichment of neighboring habitats, and can affect the composition of lichen floras (Brown,1992). Benfield (1994) noted that the diversity of the ep-iphytic lichen flora fairly accurately reflects the intensityof farming in East Devon (UK); Ruoss (1999) reported a substantial nitrogen deposition in agricultural areas of Switzerland and a massive presence of nitrophytic lichen species in areas subject to intense agricultural activity, where their occurrence is related to farming. In Italy, Loppi and De Dominicis (1996) showed that the lichen vegetation is only slightly influenced by agri-culture, and factors determining a higher frequency of nitrophytic species in agricultural sites may include dust impregnation of bark and the drier microclimate of trees in these sites. In Greece, Pirintsos et al. (1998) found that grazing induces nitrophytic lichen flora, even if dustmay play an important role in promoting nitrophytic

species. In The Netherlands, van Herk (1999) showed that high levels of nitrogen compounds in the air can induce lichen communities dominated by nitrophytic species, and that the abundance of nitrophytic species on Quercus is closely dependent on NH3 concentra-tions. However, van Herk (2001) recognized that these features are governed by a high bark pH caused by the alkaline properties of NH3 rather than by increased nitrogen availability. A positive correlation between the abundance of nitrophytic species and the bark pH, as well as the atmospheric ammonia (which alkalizes bark), was also provided by van Dobben et al. (2001) in The Netherlands.

Bark pH is an important parameter in determining natural variations in epiphytic lichen communities (Barkman, 1958). Dust could be responsible for high bark pH values, and thus nitrophytic species could be promoted by dust itself and not by nitrogen (Loppi and De Dominicis, 1996; van Herk, 2001). It is well known that in the Mediterranean area dust can play an important role since alkaline dust contamination raises bark pH and causes bark hypertrophication, explaining the pres-ence of Xanthorion vegetation on normally acid-barked trees (Gilbert, 1976). Moreover, dust impregnation, independent of dust chemistry, also makes the bark drier (Loppi and Pirintsos, 2000), and since nitrophytic species are also xerophytic, such interactions should be taken into account. Furthermore, also synergistic effects of light must be considered since most nitrophytic spe-cies are also photophytic, and a higher light influx leadsto drier conditions (Loppi and De Dominicis, 1996).

According to the results of the present study, nitro-phytic lichen species can be used profitably to monitorthe effects of farming activities and ammonia pollu-tion. The whole survey area, as expected in an area mainly occupied by arable land, was heavily affected by agricultural activities, with two “hot spots” where ammonia emission from animal husbandry also plays an important role.

It is noteworthy that PSUs 10 and 13 seem to suffer at the same time from ammonia and NOX pollution, as evidenced by the maps of ILD values without nitro-phytic species (Fig. 2b) and with strictly nitrophytic species (Fig. 2d). In field monitoring studies it is verydifficult to separate the effects of many inter-correlatedvariables, and discrimination between the effects of two or more pollutants or between the effects of pollution and those of other environmental changes is open to some controversy (van Dobben and Ter Braak, 1998; van Herk, 2001).

Comparison of the maps of ILD values (Fig. 2a) and ILD values without nitrophytic species (Fig. 2b) highlights in the latter the presence of two areas of


123

environmental alteration, effectively corresponding to sites with anthropogenic influence, not disclosed bythe former. Although Asta et al. (2002) suggested the use of the sum of frequencies of all lichen species as a measure of environmental alteration, this method, at least under certain circumstances, does not really reflecta situation of alteration. In fact, the presence of nitrogen compounds and/or dust or other factors stimulating the growth of nitrophytic species, has a “fertilizing” effect rather than depleting one on lichen vegetation. Conse-quently, in some cases, as for PSUs 10 and 13, the sum of two or more pollutants does not cause a marked im-poverishment in lichen communities, but could have an opposite effect. Thus, at least for the study area, the map of ILD values using all species simply reflects the diver-sity of epiphytic lichens on trunks of isolated deciduous oaks, with a biological value on its own, but without any clear relationship with atmospheric pollution.

CONCLUSIONS

As bioindication is largely a matter of data interpre-tation (Loppi et al., 2002), this does not mean that the effects of individual pollutants could not be detected, but it means that great care must be taken in the interpre-tation of the results. In this context, when monitoring the diversity of epiphytic lichens, the interpretation of the results could consist of several maps, each based on different groups of species, and each interpreted in a different way.

According to the results of the present survey, epi-phytic lichens are an effective tool to detect and map the effects of agriculture also in Mediterranean countries, at least in areas without heavy industrialization, given a proper species selection.

The problem of an objective criterion for the se-lection of indicator species can be overcome by using on-line databases, such as that of Nimis (2003), which are becoming increasingly widespread.

ACKNOWLEDGMENT

This research was funded by the University of Tuscia in Viterbo.

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Documents

Mapping environmental effects of agriculture with epiphytic lichens