ORIGINAL PAPER

In situ extinction of carabid beetles and community changesin a protected suburban forest during the past century:the ‘‘Bosco Farneto’’ near Trieste (Italy)

Pietro Brandmayr Æ Roberto Pizzolotto ÆGiorgio Colombetta Æ Tullia Zetto

Received: 13 June 2007 / Accepted: 18 March 2008 / Published online: 8 April 2008

� Springer Science+Business Media B.V. 2008

Abstract The carabid beetle species assemblages (14

sample sites) of a 238 ha urban oak forest in Trieste, Italy,

studied in 1983–84 with pitfall traps, were compared with

an historic list of 57 species hand collected by entomolo-

gists in the same forest before it was logged in 1944.Trap

data have been improved by hand collections to get a

species list as complete as the historic one. Multivariate

analysis was used to group the sites (14 plus the historic

list) into three assemblages of brooks, clearings and forests.

After the Second World War logging, the secondary eco-

logical succession resulted in a lower species number, with

a trend to a new equilibrium. Some important forest spe-

cialists, such as Laemostenus venustus, have been lost.

Human pressure and recolonisation by carabids are still

occurring. The in situ extinction of ground beetles near the

end of the last century reached values between 57 and 64%

of the species historically recorded. Consequently, urgent

restoration measures are required for waterside habitats,

forest and land management, to maintain small open areas

or clearings. The study of carabid species assemblages and

habitat affinities seems a useful tool for adaptive manage-

ment of forests affected by human activities, because

changes in carabid species number and type can be easily

related to human disturbance.

Keywords Biodiversity loss � Carabidae �Human disturbance � Land use change � Local extinction

Introduction

Carabid and tiger beetles are increasingly used as valid

biological indicators in an attempt to develop models of

biodiversity variation related to environmental degradation

(Thiele 1977; Stork 1990; Pearson and Cassola 1992; Des-

ender et al. 1994b; Niemela 1996; Brandmayr et al. 1996;

Luff 1996). The coleopteran family Carabidae is rich in

species and well-known, at least in some fundamental eco-

logical and behavioural traits (Lovei and Sunderland 1996).

Carabids and their species assemblages are frequently

used as environmental indicators or ecological indicators

(in the sense of McGeoch 1998). Several studies deal with

their indicator value in climate change (Ashworth 1996;

Gobbi et al. 2006), habitat fragmentation (De Vries 1994,

Spence et al. 1996; Davies and Margules 1998; Magura

et al. 2001; Niemela 2001; Lovei et al. 2006), or evaluate

the influence of stressing factors of management practices

in grasslands (Blake et al. 1996; Rushton et al. 1989), in

croplands (Pfiffner and Niggli 1996; Kromp 1999) and in

logging forests in temperate (Szyszko 1983) or boreal

zones (Niemela et al. 1993). Carabids can, together with

other taxa, be used as biodiversity indicators (Rainio and

Niemela 2003).

Nearly all the studies quoted here are contemporary or

short-time comparisons of sampling plots or sites; they are

snapshots of differences, during short periods of one or two

to three years. For carabids very few exceptions are known;

the best are perhaps the studies of Desender and Turin

(1989) and Desender et al. (1994a) of the decline of open

land species in the fauna of four western European coun-

tries. Nevertheless, exact numbers of species losses related

to specific habitats are very difficult to obtain, probably

because studies of such areas are rarely focused over an

entire century or many decades. Brandmayr and Algieri

P. Brandmayr � R. Pizzolotto (&) � T. Zetto

Dipartimento di Ecologia, Universita della Calabria,

87036 Rende, CS, Italy

e-mail: rotopito@unical.it

G. Colombetta

Via Elia 2, Trieste, Italy

123

J Insect Conserv (2009) 13:231–243

DOI 10.1007/s10841-008-9161-6

(2001) found that about 86% of the Italian populations of

the chlaeniine wetland ground beetle Epomis circum-

scriptus were extinct at the end of the twentieth century.

In the city of Trieste (Italy, Friuli-Venezia Giulia

Region), an old Mediterranean suburban forest, long-called

Farneto (or Boschetto) by Triestine citizens, was protected

for centuries because of its importance as a wood reserve

for the garrisons and for supplying natural resources (fungi,

bark, medicinal plants) to inhabitants, its vegetation and

biomass structure was left unchanged until 1943–44, when

the necessities of the Second World War forced the

inhabitants to exploit its extensive wood reserves. After

clear-cutting during the War, part of the hill slope was

artificially reforested, while some other parts recovered

mostly by natural regeneration.

The municipality of Trieste recently guaranteed the

protection of the forest against urbanisation. In 1996 the

Nature-2000 team of the Department of Biology of Trieste

University proposed the creation of a SCI (Site of Com-

munity Interest), and now the Farneto Forest is scheduled

as ‘‘Site of National Interest’’ in the frame of the parallel

protection Programme ‘‘Bioitaly’’, with the SIN-number:

IT3342014.

The Farneto wood area represents a type of synthesis in

space and time of these anthropization processes. In past

times the area was on the outskirts of Trieste, until it was

surrounded progressively by the city but without losing the

ecological function of a semi-natural area connecting the

more natural karstic plateau.

The present research aims to appraise in a historical

perspective the effect of anthropogenic activities and

urbanization on the degradation of the carabid species

assemblages and their ability to recover. The Farneto rep-

resents a unique possibility for this purpose because the site

has been visited by entomologists since the year 1818,

when the naturalists Hoppe and Hornschuch collected a

new lebiine subspecies, Lebia fulvicollis thoracica. Later,

between 1890 and 1930, the forest was the preferred col-

lecting target of a very active group of Triestine

entomologists and the results for carabid beetles were

organized by Giuseppe Muller (1926) in a detailed topo-

graphic catalogue.

The following questions were focused on in detail. (1)

Are carabid species assemblages a valuable record of the

changes observed in a suburban forest during the past

century? (2) Are the species assemblages censused after the

secondary succession (1945–19804) similar to the ancient

ones, or has a new ‘‘equilibrium’’ been reached? (3) How

many carabid species have been lost (become locally

extinct) during the past century? (4) Does human distur-

bance still exist and what should be the policies against it?

(5) Is the study of the ‘‘in situ extinction’’ an useful

approach?

Materials and methods

Study area

The climate of the study area in the city of Trieste belongs

to the submediterranean type. The mean annual tempera-

ture of the Farneto is 1.5�C below the mean of the city

centre (14�C), and is estimated at around 12.5�C at a

medium altitude of 150 m. The precipitation is about

1,000 mm/year.

The Farneto (Figs. 1, 2) covers an area of 238 ha on a

sandstone hill slope (Eocene ‘‘Flysch’’), located at the

eastern periphery of the city. The area extends like a finger

from about the centre of the city (altitude 60 m, and no

more than 1.5 km from the Adriatic Sea) to the border of

the Karst plateau behind Trieste (240 m asl). Its length is

about three kilometres and its maximum width is 700 m.

The slope exposure is mainly N or NNE. The southern

border is marked by the edges of the Chiadino and Cac-

ciatore hills. Two small, more or less permanent streams

run from the hilltops towards the Torrente Grande, which

borders the northern edge of the forest.

The original vegetation was a mixed forest dominated

by Quercus petraea, with a dense Sesleria autumnalis herb

layer (Associazione Sportiva 1994; Poldini 1989). Before

clear-cut logging in 1944, all the layers of the forest

structure were entirely native, with a mean diameter of

major trees (mostly oaks) around 1–1.5 m. Other tree

species were Q. cerris, Castanea sativa, Acer campestre,

Carpinus betulus, Ostrya carpinifolia and, along the

streams, Salix alba and Populus alba. After 1945, in the

post-war period, the area was partly reforested with aus-

trian black pine (Pinus nigra) and with cypress (Cupressus

sempervirens and C. arizonica), but a large part of the

forest was invaded by Robinia pseudoacacia. In 1984 parts

of the forest area were still occupied by remnants of the

open land created after the Second World War, but about

70% of the surface had been reconquered by native trees,

especially oaks, Fraxinus ornus and Ostrya carpinifolia.

This recently cleared open land was frequently crossed by

burnt areas that had retarded the ecological succession.

Some very small patches of humid vegetation with

Phragmites australis were also present.

After 1975, probably due to climate change and conse-

quently milder winters, the understorey shows an

increasing expansion of evergreen bushes, mainly Laurus

nobilis; other native Mediterranean elements such as Rus-

cus aculeatus were always found in the forest.

As a result, about 95% of the original Farneto is now

covered by trees 25–50 years old. At the time of our

1983–84 investigation, artificial pine plantations or natu-

rally-regenerated coppice forest accounted for about 85%

of the entire surface of the Farneto, and trees of the

232 J Insect Conserv (2009) 13:231–243

123

allochtonous species Robinia pseudacacia comprised

more than the 20% of the forest canopy.In 1984, the area

was threatened by pollution of brooks and the main

stream, the ‘‘Torrente Grande’’, and by illegal land use,

e.g. abandoning waste and rubbish.

At the eastern boundary of the Farneto, the open land is

represented by a true old pasture. Open ground was man-

aged through sheep and cattle grazing until the 1950s, when

this type of land use began to decline strongly in the whole

Trieste Province. This old open land still exists despite

Fig. 1 The study area of the Farneto wood hill (13� 210 3000 Est, 45� 380 5000 North)

Fig. 2 The Farneto forest seen

from the edge of the Karst

Plateau near Trieste

J Insect Conserv (2009) 13:231–243 233

123

heavy urbanisation of the surroundings in the last 20 years.

This site was also used for the historical comparison.

The features of the sampling sites are described in

Table 1.

Sampling methods and data analysis

Ground beetles were captured using pitfall traps, plastic

vessels with a top diameter of 9 cm, filled with 200 ml of a

mixture of wine vinegar and 5–6% formalin. The traps had

a small hole near the top to prevent over-flowing after

heavy rain. A wire cross across the upper hole allowed

escape for small mammals.

Because the study area is relatively narrow, and the

different environments are fragmented, a maximum of

three traps (four at one site) for each sample site was used

to maintain homogeneous sampling conditions. In each site

the traps were buried at a distance of &15 m from each

other, and were emptied once a month for a year starting in

March 1983 and ending in February 1984.

In the Farneto area, 14 sampling sites were trapped

(Table 1), starting from the western end (sample site OB)

and finishing at the eastern end (sample site LM).

The data from sites sampled in the Farneto were com-

pared with the historical data derived from the research of

Muller (cf. 1926) over the whole area of the Farneto wood

from 1900, and with the data of his collection (conserved in

the Trieste City Natural History Museum). To this end, a

site (site ‘1940’, see Table 1) with Muller’s data was added.

Trap data have been collected over a short time span,

while Muller’s data were collected over a long time span. It

is likely that the time factor made Muller’s data more

complete than trap data. This is why we improved our

(trap) data with data from hand collections, carried out

either before and after the 1983–84 monitoring (hand col-

lecting controls were carried out until 2005), and many

entomologists helped in giving a complete picture of the

Farneto’s ground beetle faunula (see acknowledgements).

In such a way we made the same work of Muller, but for

the period 1983–84, avoiding that differences in collecting

methods affect the species lists.

For the historical comparison only presence-absence

values have been used.

We have tried to define the loss of species diversity with

the term ‘in situ extinction’, meaning the rate of loss of

species (of a single higher taxon or more) that have become

locally extinct during a certain historical period. For the

Farneto wood, we assumed that human pressures and

impacts decrease from the centre of the city, and that the

catastrophic events of the Second World War may also

have gradually increased in intensity from the periphery to

the centre.

Table 1 Features of the sample sites in the Farneto study area. The percentage of vegetation cover is given for the canopy, safe for LM where

the herb layer cover is given

Sample

site

Altitude

(m asl)

Exposure Slope

(�)

Percentage

vegetation

cover

Traps Site description

OB 90 N 20 95 2 Ostrya-Quercus dense coppice

OBac 90 N 20 95 3 brook borders in the forest; tree layer enriched by Sambucusshrubs

VP 105 NNW 15 70 2 Ostrya-Quercus coppice

LC1 135 N 20 35 1 large clearing with sparse bushes of Fraxinus ornus, Ostryaand other spp

LC 158 NNW 10 25 3 clearing with sparse bushes and dense grass coverage

RB 80 NNE 20 95 2 forest site heavily intruded by Robinia, densely covered by

Hedera helix; 30 m far from an urbanized area

CF 145 NE 15 80 2 forest site near the ruines of a police barracks abandoned after

the II World War

BF 110 N 10 95 4 forest site, cool-humid, near the valley-bottom of the Farneto

stream

S 135 NNW 10 85 2 Quercus wood with Sesleria grass layer

AS 140 WNW 15 90 3 forest site on the bank of a polluted (unloading home waters)

brook

BC 160 W 20 80 2 wood with warm microclimate conditions

AP 185 W 25 90 3 forest site on the bank of a non polluted brook

PCr 210 NNE 25 90 3 pine plantation with Fraxinus ornus undergrowth

LM 240 NE 15 90 3 old pasture of about 6 hectares, invaded by Sesleria autumnalis

1940 – – – – – collections made by Muller in the Farneto area

234 J Insect Conserv (2009) 13:231–243

123

A species accumulation curve and richness estimation

after 50 randomizations were computed on trap data to give

an estimate of catching efficiency. The estimators were:

Shannon diversity index, Incidence-based Coverage Esti-

mator (ICE) and Coleman estimator (Colwell 2005). ‘ICE

is the sum of the probabilities of encounter for the species

observed, taking into account species present but not

observed’ (Colwell 2005). To compute ICE, a hypothetical

maximum number of species is estimated on the basis of a

threshold (defined by the researcher, i.e. in our case the

species captured only three times) corresponding to the

least frequent species. ICE gives the theoretical species

richness including species not discovered in any sample.

The Coleman estimator estimates species richness on the

basis of all species actually discovered (Colwell 2005).

Data were analysed by cluster analysis (correlation

coefficient and minimum variance, also known as Ward’s

distance), and principal components analysis (StatSoft Inc.

2001).

To evaluate the nature of the changes that have had the

most influence in modifying the carabid assemblages of the

Farneto, the habitat preference of all the 66 taxa found in

the Farneto was determined from the literature or from

interpretation of available datasets. Each of the 66 species

in Table 2 was assigned to one of the following main

ecological classes: forest, pastures (and meadows), river-

side (or wetlands), using the criterion of Thiele (1977), see

also Maelfait et al. (1994); Telfer and Eversham(1996),

and Cuesta et al. (2006), which takes into account the peak

of abundance. Data were ordered as follows: species

recorded before 1940, species collected during the study in

1983–84, new findings in pitfall traps in 1983–84 (probably

not found by other entomologists who were pure hand

collectors) and species found before but not recorded in

1983–84 (defined as: lost).

Results

Catching efficiency

A species accumulation curve and richness estimation after

50 randomizations of pitfall traps data are outlined in

Fig. 3. The observed species curve (S obs.) does not flatten

towards the value of 27 (i.e. the number of species captured

by pitfal traps), but it does not seem to be very steep there.

Perhaps, by visual estimation of the shape of the curve, it

could be hypothesized that the asymptote lies between 30

and 32. Figures predicted by the Coleman curve are very

similar to the observed ones. ICE predicts a higher species

number, but this estimator is also based on hypothetical

species, so it is not only bound to actual ecosystem con-

ditions. More interestingly is the fact that ICE flattens the

more sites are added, and so does the Shannon index,

suggesting that the number of observed species is near the

actual maximum.

The species assemblages 1983–84

In the 14 sites of the Farneto forest, a complex of 27

ground beetle taxa was collected in 35 pit-fall traps

(Table 2). Data collected by hand were also included,

reaching a total of 70 species (i.e. four species have been

added: Paranchus albipes, a riverside species; Trechus

subnotatus, a rare riverside dweller; Clivina collaris, riv-

erside; Laemostenus algerinus, forest dweller).

Among the species found 19 are forest dwellers, 14 are

forest specialists, which are more represented in the eastern

(and upper) side of the forest. The most common forest

specialist is Carabus catenulatus, a typical earthworm

predator, but snail predators are also widespread (Carabus

caelatus, coriaceus, especially in the larval stages). Five

forest species are endemics of south-eastern Europe, and

the rare hygrophilous Trechus subnotatus seems to have

survived the clear-cutting shock of 1944 in at least one

stand. The canopy predators Calosoma sycophanta and

C. inquisitor are both active in many places.

Stands VP, S, CF and RB were at the time degraded or still

partly open land, and this suggests that at least some forest

species recolonized the young succession stages from the

eastern, Karst-facing, side of the area. Figure 4 gives the

activity density of the three most important forest specialists

in order of distance from the city centre. At least two of them

(Abax ater and Carabus caelatus) show a possible coloni-

sation direction from east to west; a small population of the

first could have survived near the Botanical Garden, where

some older trees were left standing.

Data classification and ordination

The analysis of the urbanisation phenomenon (the sites of

the Farneto wood area) (Table 2), shows a pattern (Fig. 5)

where site ‘1940’ (based on Muller’s collections) is sepa-

rate from the other groups, probably because it has 39

species not found in the present investigation.

The species distribution in the Farneto wood allows

identification of three groups of sites: group A composed

mainly of sample sites along small brooks, including the

only true pasture of the Farneto wood area; group B

composed of samples from clearings, and the related group

C of the forest samples.

The historical-dynamic relationships of the carabid

beetles species groupings can be deduced partly from

ordination through principal components analysis of the

sites (Fig. 6), where the first two dimensions explain 62%

of the variation.

J Insect Conserv (2009) 13:231–243 235

123

Table 2 Carabid beetle presence in the Farneto study area. Species grouped according to habitat preference (F = forest, forest specialists in

bold, P = pasture, R = riverside). Nomenclature follows Vigna (1993). Sites ordered as in Fig. 5

1940 LM PCr BC AS AP Obac LC LC1 VP S CF RB BF OB

F Carabus coriaceus L. 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

F Carabus catenulatus Scopoli 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

F Harpalus atratus Latreille 1 1 1 1 1 1

F Carabus caelatus Fabr. 1 1 1 1 1 1 1

F Abax ater (Villers) 1 1 1 1 1 1 1 1 1 1

F Myas chalybaeus (Palliardi) 1 1 1 1

F Laemostenus algerinus (Gory) 1

F Calosoma sycophanta (L.) 1 1 1 1

F Steropus melas (Creutzer) 1 1 1 1 1 1 1 1

F Notiophilus rufipes Curtis 1 1 1 1

F Synuchus vivalis (Illiger) 1 1

F Leistus rufomarginatus (Duft.) 1 1 1 1 1

F Calosoma inquisitor (L.) 1 1

F Trechus quadristristus (Schrank) 1

F Molops ovipennis Chaudoir 1

F Laemostenus elongatus (Dej.) 1

F Laemostenus venustus (Dej.) 1

F Philorhizus quadrisignatus (Dej.) 1

F Anillus florentinus Dieck 1

P Calathus glabricollis Dej. 1 1

P Harpalus dimidiatus (Rossi) 1 1 1 1

P Harpalus rubripes (Duft.) 1 1 1

P Anchomenus dorsalis (Pontopp.) 1 1

P Brachinus crepitans (L.) 1 1

P Calathus cinctus Motsch. 1

P Harpalus sulphuripes Germar 1 1

P Harpalus distinguendus (Duft.) 1

P Amara aequestris (Duft.) 1

P Ophonus puncticeps Stephens 1 1

P Scybalicus oblongiusculus (Dej.) 1

P Poecilus koyi (Germar) 1 1

P Lebia cruxminor (L.) 1

P Poecilus cupreus (L.) 1

P Ophonus brevicollis (Serville) 1

P Lamprias fulvicollis (Fabr.) 1

P Amara anthobia Villa 1

P Callistus lunatus (Fabr.) 1

P Amara eurynota (Panzer) 1

P Olisthopus glabricollis (Germar) 1

P Microlestes fulvibasis (Reitt.) 1

P Bradycellus verbasci (Duft.) 1

P Ocydromus tetracolus (Say) 1

P Diachromus germanus (L.) 1

P Harpalus flavicornis Dej. 1

P Amara familiaris Duft. 1

P Harpalus anxius (Duft.) 1

P Lamprias cyanocephala (L.) 1

P Microlestes fissuralis (Reitt.) 1

236 J Insect Conserv (2009) 13:231–243

123

Table 2 continued

1940 LM PCr BC AS AP Obac LC LC1 VP S CF RB BF OB

R Platysma nigrita (Paykull) 1 1 1

R Chlaeniellus vestitus (Paykull) 1 1 1

R Chlaenius velutinus (Duft.) 1

R Anisodactylus binotatus (Fabr.) 1

R Stenolophus teutonus (Schrank) 1

R Acupalpus meridianus (L.) 1

R Elaphropus haemorrhoidalis (Ponza) 1

R Thalassophilus longicornis (Sturm) 1

R Acupalpus maculatus Schaum 1

R Paratachys bistriatus (Duft.) 1

R Dinodes decipiens (Dufour) 1

R Pseudolimnaeum inustum (Duval) 1

R Metallina properans (Stephens) 1

R Ocydromus decorus (Zenker) 1

R Ocydromus dalmatinum (Dej.) 1

R Nebria brevicollis Fabr. 1

R Badister bipustulatus Fabr. 1

R Paratachys fulvicollis Dej. 1

R Ocydromus genei (Kuster) 1

R Paranchus albipes (Fabr.) 1

R Trechus subnotatus Dej. 1

R Clivina collaris (Hrbst) 1

Species number 57 18 8 8 9 11 5 3 5 3 5 5 3 6 5

Fig. 3 Species accumulation

curve and richness estimation

after 50 randomizations

(Colwell, 1997) (S

obs. = observed species,

ICE = Incidence-based

Coverage Estimator,

Coleman = Coleman species

richness estimator,

Shannon = Shannon diversity

index)

J Insect Conserv (2009) 13:231–243 237

123

Along the first axis (Fig. 6), site ‘1940’ is the only site

with positive correlation. Site LM has the second highest

score, and the forest samples lie at the negative extremity. On

the basis of the position of sites LM and ‘1940’ vs. the other

sites, it is possible to interpret the first axis as the axis of the

variation between the historical and present situations.

Along the second axis, sites ‘1940’ and LM are at the

two extremities, while the forest sites of group C (Fig. 6)

are concentrated at the axis origin. In this case, the second

axis represents the variation associated with ecological

succession induced by deforestation.

According to the ecological meaning of the axes, as

explained before, the space defined by the principal com-

ponent analysis is therefore comprised of four quadrants

(Fig. 6): quadrant I, the sub-space of the historical natural

conditions, quadrant II, probably associated with historical

degradation of the environment (a reasonable hypothesis,

because no data are available), quadrant III, associated with

conditions of recovery from degradation, and quadrant IV,

associated with present conditions.

Bearing in mind that the meaning of quadrant II was

inferred by its relative position, an ideal historical track was

drawn on the quadrants of Fig. 6, to outline the relationships

between heavy anthropization and secondary ecological

succession.

Species survival and habitat affinity

Figure 7 shows the change of species on the basis of habitat

affinity. For each group, the habitat affinity is reported as

species number. The highest proportion of species surviving

in 1983 was forest species, whereas both pasture and

waterside components exhibited outstanding losses. Water

pollution is probably the cause of the disappearance of the

most hygrophilic or streamside carabids, which were

reduced from 22 to five species (23%). The pasture and

meadow components were also affected greatly by reduc-

tion: from 24 to 12 (50%). Forest dwellers survived the best:

14 of 15 (93%). It is likely that the new species recorded in

1983 were living in the old Farneto, so the correct reduction

is probably from 19 to 14 (74%). Thus, the lost species (39)

pertain mostly to the waterside (44%) and pasture dwellers

(44%), and minimally to the forest elements (12%). Fur-

thermore, no new waterside species were collected.

Discussion

The answers posed in the introduction follow as subchapters.

Carabid species assemblages are a valuable record

of the changes observed in a suburban forest during

the past century

In the ecological landscape of the Trieste city surroundings

where farming and forestry have modified the natural

conditions, characteristic groupings of carabid species have

developed, which can be distinguished from those of

environments less affected by human activity (Fig. 5).

Fig. 4 Annual Activity Density

(individuals/trap in the standard

period of 10 days. Ordinate). of

three abundant forest species in

the Farneto wood, ordered by

increasing distance from the

centre of Trieste (abscissa,

where the distance is between

brackets). The forest links to the

Karst plateau at its eastern

border through a pasture of

*6–7 hectares (Site LM, right

in the graph). For graphical

reasons the values for

C. caelatus have been weighted

by 10

238 J Insect Conserv (2009) 13:231–243

123

After 40 years of a partly human-managed secondary

succession, the ground beetle assemblages of the suburban

Farneto forest comprise 19 silvicolous species, with 11

more stenotopic elements well-known from thermophilous

woodlands (Quercetalia pubescentis) of the Triestine Karst.

Most species show a discontinuous distribution; forest

elements are continuous only in the eastern part of the area.

A new equilibrium has been reached by the species

assemblages

The 1983–84 sampled groupings are not associated closely

with (they are distant from) the historical situation (site

‘1940’). This is probably because the land use of the area is

shifting to a new equilibrium, as outlined in the space

defined by the first two dimensions of the principal com-

ponents analysis (Fig. 6). Structural degradation (caused by

the Second World War and city expansion) resulted in

dramatic changes in historical forest communities (as

outlined in Fig. 6) and, especially after the 1944 clear-

cutting, an expansion of species typical of lawns and pas-

tures (axis II of the principal components analysis).

This secondary ecological succession has probably been

accelerated by the existence of natural corridors (stream-

sides), which allowed species of the karstic open lands to

exist within the Farneto group A (Fig. 5). In fact, the

activity density pattern of some forest species in 1983–

1984 suggests ‘‘per pedes’’ recolonisation from the eastern

boundary of the area, i.e. from the more natural habitats of

the Triestine Karst.

The regeneration of the forest environments represents a

new situation of stability, due to the current moderate

anthropogenic influence (periodical cutting, tourism),

which prevents or at least retards the development of new

very old forests.

This new situation probably does not correspond to past

conditions (before 1940), as can be argued from the posi-

tion of site group C, at the negative extremity of the first

axis (the present vs past axis of Fig. 6) and near the origin

of the second axis (the ecological succession axis of

Fig. 6).

The distribution of carabid species according to their

presence or absence in several environments, framed in a

historical perspective, suggests that the impact of human

activities allowed the entry of species that induced per-

manent transformations (forced stages) in communities.

These forced stages are not far from natural conditions.

Therefore, it is reasonable to say that the capacity to re-

establish the natural conditions of this suburban forest is

not jeopardized greatly if the soil structure and ecological

landscape are not altered greatly over a long period.

The species richness of the new Farneto is very different

from that of the historical forest. After 1945 streams and

brooks were increasingly polluted, while the land use

changed and grazing ceased or decreased greatly in the

countryside around Trieste. Grazing is a high impact

activity, which generated a new habitat (the open land) and

a new species diversity at least for carabid assemblages in

the countryside around Trieste. Analysis of the habitat

affinity of the 70 ground beetle species involved in this

process suggests that the most considerable changes in

species composition are due to water pollution and the end

of grazing.

Carabid species become locally extinct

due to anthropogenic disturbance

Near the end of the twentieth century, 39 species of the 61

recorded by Triestine entomologists are locally extinct, in

other words the ‘‘in situ’’ extinction rate of carabid beetles

in this protected area could be estimated in about 64%.

Taking into account that some 8 species collected in our pit

Fig. 5 Classification of the Farneto sample sites, based on correlation

and minimum variance distance

J Insect Conserv (2009) 13:231–243 239

123

Fig. 6 Ordination of the

Farneto sample sites after

principal component analysis.

The circular line depicts an

ideal historical track based on

actual (continuous) and

hypothesised (dashed) data.

Correspondence between

number and sample site as

follows: 31=OB, 32=Obac,

33=VP, 34=LC1, 35=LC,

36=RB, 37=CF, 38=BF, 39=S,

40=AS, 41=BC, 42=AP,

43=PCr, 44=LM, 45=1940

Fig. 7 Changes in species

composition in the Farneto

study area

240 J Insect Conserv (2009) 13:231–243

123

fall traps may have escaped the hand collecting of previous

entomologists (especially Molops ovipennis, Myas cha-

lybaeus and Carabus caelatus, which are difficult to catch

without traps), a theoretical minimum of extinction may be

39/(61 + 8), approximately 57%. In both cases, more than

half of the carabid species of the Farneto forest disappeared

in the second part of the past century, and this alarming fact

makes theories about species diversity in disturbance gra-

dients oversimplified. It is well-known that the ‘‘stepping

stones of global extinctions are local extinctions’’ (Lovei

2001), and at least four or five of the vanished species (e.g.

Chlaenius velutinus, Pseudolimnaeum inustum) have today

(2006) only one live population in the whole Trieste

Province (personal communications, see acknowledge-

ments). The ultimate cause of extinction of most taxa

(90%) in the United States is habitat destruction or deg-

radation (Wilcove et al. 1998).

Human disturbance is still affecting the study area

Human disturbance in the forest continues and both forest

and open land species seem to avoid the urbanized borders

of the Farneto (Fig. 4). Consequently, in our opinion, the

following measures could stop local species extinction and

favour the original species richness: (1) restoration of

surface water quality and of waterside habitats for inver-

tebrates and vertebrates (the only amphibian surviving in

the forest is the fire salamander Salamandra salamandra);

(2) high-trunk (old-growth) oriented management, at least

in the core area of the forest, and soil restoration especially

through log decay; (3) maintenance of some clearings and

open tracks by horse grazing and/or by mowing.

Some of the forest specialists of the area need conser-

vation measures. Despite appearing less affected by

changes and having the ability to recolonize the original

habitat, some more sensitive species seem locally extinct,

e.g. Procerus gigas, the largest carabid of Europe (which

had a small live population until 1975 in the Botanical

Garden), Anillus florentinus (a deep soil dwelling bem-

bidiine species, highly affected by soil dryness),

Laemostenus venustus (a dendrophilic species connected to

very old chestnut and oak trees, see Pizzolotto et al. 1991),

and others of less importance. The sphodrine carabid L.

venustus is surely extinct in the whole Province of Trieste

and further investigations could clarify if L. venustus may

be considered a dendrophilic indicator of Mediterranean

forests, today well preserved in southern Italy.

Because secondary ecological succession is still going

on, it seems merely theoretical to predict whether the

maximum species number will be equal to, less than or

above the recorded 70. It is reasonable, however, to predict

that after several patches of the original landscape (oak

woods) have re-established, Farneto wood will reach

maximum species diversity, if human disturbance is kept at

a moderate level (tourism, recreation, small clearings).

‘In situ extinction’ as a tool for monitoring the natural

species turnover

The study of the in situ extinction, accompained by the

natural species turnover, is a useful approach for checking

the efficiency of conservation policies in protected areas, or

for evaluating new areas for the status of protection sites.

Species listings remain the most important attribute for site

evaluation (Usher 1986); moreover methods should be

quantitative, including relative abundances (Samways

1995). Many well-known National Natural Reserves, such

as the Monks Wood Reserve in Cambridgeshire, provide

excellent examples of species losses due to the cessation of

traditional management (e.g. butterfly species extinctions

in Peterken 1991). Monitoring carabid species disappear-

ance and/or recolonisation as in the Farneto could be an

optimal way of monitoring to check recovery after clear-

cutting.

The in situ extinction approach is not dependent on the

boundary span of the study area, when a historical census

of reliable biological indicators, such as carabids, has been

carried out, over at least a twenty-year time period. In this

sense, its application ranges from the rehabilitation moni-

toring of contaminated sites to the effects of climate

change on alpine environments, for example.

Conclusion

Further research is needed to elucidate the biological fea-

tures of carabid species (see Pizzolotto 1994) and

parameters of carabid species assemblages (see Penev

1996), to allow comparisons within different areas at large

scales (Dennis and Ruggiero 1996) and develop sound

management practices for suburban forests (the adaptive

management of Hillborn et al. 1995).

As a general remark, it seems more useful to recognize

and reconstruct the causes of disturbance, and relate them

to species assemblages and habitat preference, rather than

solely to the number of species. Carabid beetle studies are a

valid help toward this aim, because changes of carabid

species number and type can be related to human distur-

bance (Niemela et al. 2002; Venn et al. 2003; Ishitani et al.

2003). Furthermore we found that such disturbance can

lead to local species extinction, which could be a serious

biodiversity impoverishment when involving endemic

species.

Acknowledgements The authors are very indebted to several Tri-

estine entomologists, who generously helped with advice and opened

J Insect Conserv (2009) 13:231–243 241

123

their own collections. The late Mr. Carlo Posarini donated the only

specimen of Laemostenus algerinus captured in Trieste after World

War II, and helped in monitoring Procerus gigas for two decades

(1965–1985). Detailed information about the insect diversity of the

Farneto forest was obtained by Dr. Giuseppe Muller’s latest pupils,

Dr. Bruno Millo and Dr. Tiziano De Monte, and by our unforgettable

friend Dr. Guido Calligaris. The Museum of Natural History of the

city of Trieste allowed careful examinations of the two main collec-

tions and of ‘‘inserenda’’.

References

Ashworth AC (1996) The response of arctic carabids (Coleoptera) to

climate change based on the fossil record of the Quaternary

Period. Ann Zool Fenn 33:125–131

Associazione Sportiva del Corpo Forestale (1994) Il bosco Farneto -

Storia, natura e sentieri del ‘‘Boschetto’’ di Trieste. Spring,

Trieste

Blake S, Foster GN, Fischer GEJ, Ligertwood GL (1996) Effects of

management practices on the ground beetle faunas of newly

established wildflower meadows in southern Scotland. Ann Zool

Fenn 33:139–147

Brandmayr P, Algieri MC (2001) Habitat affinities of chlaeniine

species (Coleoptera, Carabidae) in Calabria and the status of

Epomis circumscriptus, evaluated by the ‘‘Cronogeonemie’’

software. In: Brandmayr P, Loevei G, Zetto T, Casale A, Vigna

A (eds) Natural history and applied ecology of Carabid Beetles.

Pensoft, Sofia

Brandmayr P, Cagnin M, Mingozzi A, Pizzolotto R (1996) Map of

zoocoenoses and evaluation for the Menta river dam in

Aspromonte (Calabria, Italy). Z Okol Natur 5:15–28

Colwell RK (2005) EstimateS: Statistical estimation of species

richness and shared species from samples. Version 7.5. User’s

Guide and application published at: http://purl.oclc.org/estimates

Cuesta D, Taboada A, Calvo L, Salgado JM (2006) A preliminary

investigation of ground beetle (Coleoptera: Carabidae) assem-

blages and vegetation community structure in Calluna vulgarisheatlands in NW Spain. Entomol Fenn 11:241–252

Davies KF, Margules CR (1998) Effects of habitat fragmentation on

carabid beetles: experimental evidence. J Animal Ecol 67:460–

471

De Vries HH (1994) Size of habitat and presence of ground beetle

species. In: Desender K, Dufrene M, Loreau M, Luff ML,

Maelfait J-P (eds) Carabid Beetles, ecology and evolution.

Kluwer Academic Publishers, Dordrecht

Dennis JG, Ruggiero MA (1996) Biodiversity inventory: building an

inventory at scales from local to global. In: Szaro RC, Johnston

DW (eds) Biodiversity in managed landscapes: theory and

practice. Oxford University Press, New York

Desender K, Turin H (1989) Loss of habitats and changes in the

composition of the ground and tiger beetle fauna in four west

European countries since 1950 (Coleoptera: Carabidae, Cicin-

delidae). Biol Conserv 48:277–294

Desender K, Dufrene M, Maelfait JP (1994a) Long-term dynamics of

carabid beetles in Belgium: a preliminary analysis on the

influence of changing climate and land use by means of a

database covering more than a century. In: Desender K, Dufrene

M, Loreau M, Luff ML, Maelfait J-P (eds) Carabid Beetles,

ecology and evolution. Kluwer Academic Publishers, Dordrecht

Desender K, Dufrene M, Loreau M, Luff ML, Maelfait J-P (eds)

(1994b) Carabid Beetles, ecology and evolution. Kluwer Aca-

demic Publishers, Dordrecht

Gobbi M, De Bernardi F, Pelfini M, Rossaro B, Brandmayr P (2006)

Epigean Arthropod Succession along a 154-year Glacier

Foreland Chronosequence in the Forni Valley (Central Italian

Alps). Arct Antarct Alp Res 38:357–362

Hillborn R, Walters CJ, Ludwig D (1995) Sustainable exploitation of

renewable resources. Annu Rev Ecol Syst 26:45–67

Ishitani M, Kotze DJ, Niemela J (2003) Changes in carabid beetle

assemblages across an urban-rural gradient in Japan. Ecography

26:481–489

Kromp B (1999) Carabid beetles in sustainable agriculture: a review

on pest control efficacy, cultivation impacts and enhancement.

Agric Ecosyst Environ 74:187–228

Lovei G (2001) Extinctions, modern examples of. In: Encyclopedia of

Biodiversity, 2. Academic Press

Lovei G, Sunderland KD (1996) Ecology and behavior of ground

beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256

Lovei G, Magura T, Tothmeresz B, Kodobocz V (2006) The influence

of matrix and edges on species richness patterns of ground

beetles (Coleoptera: Carabidae) in habitat islands. Glob Ecol

Biogeogr 15:283–289

Luff ML (1996) Use of carabids as environmental indicators in

grasslands and cereals. Ann Zool Fenn 35:185–195

Maelfait J-P, Desender K, Dufrene M (1994) Carabid beetles and

nature conservation research in Belgium: a review. In: Desender

k, Dufrene M, Loreau M, Luff ML,Maelfait J-P (eds) Carabid

Beetles, ecology and evolution. Kluwer Academic Publisher,

Dordrecht, The Netherlands

Magura T, Kodobocz V, Tothmeresz B (2001) Effects of habitat

fragmentation on carabids in forest patches. J Biogeogr 28:129–

138

McGeoch MA (1998) The selection, testing, and application of

terrestrial insects as bioindicators. Biol Rev 73:181–201

Muller G (1926) I Coleotteri della Venezia Giulia. Catalogo ragionato

- Parte I: Adephaga. Mosettigs, Trieste

Niemela J (1996) From systematics to conservation - carabidologists

do it all. Ann Zool Fenn 33:1–4

Niemela J (2001) Carabid beetles (Coleoptera: Carabidae) and habitat

fragmentation: a review. Eur J Entomol 98:127–132

Niemela J, Langor D, Spence JR (1993) Effects of Clear-Cut

Harvesting on Boreal Ground-Beetle Assemblages (Coleoptera:

Carabidae) in Western Canada. Conserv Biol 7:551–561

Niemela J. Kotze D J, Venn S, Penev L, Stoyanov I, Spence J, Hartley

D, de Oca EM (2002) Carabid beetle assemblages (Coleoptera,

Carabidae) across urban-rural gradients: an international com-

parison. Landsc Ecol 17:387–401

Pearson DL, Cassola F (1992) World-wide species richness patterns

of tiger beetles (Coleoptera: Cicindelidae): indicator taxon for

biodiversity and conservation studies. Conserv Biol 6:376–391

Penev L (1996) Large scale variation in carabid assemblages, with

special reference to local fauna concept. Ann Zool Fenn 33:49–64

Peterken GF (1991) Ecological issues in the management of

woodland nature reserves. In: Spellerberg BS, Goldsmith FB,

Morris MG (eds) The scientific management of temperate

communities for conservation. Blackwell Scientific Puclications,

Oxford

Pfiffner L, Niggli U (1996) Effects of bio-dynamic, organic and

conventional farming on ground beetles (Col. Carabidae) and

other epigaeic arthropods in winter wheat. Biol Agric Hortic

12:353–364

Pizzolotto R (1994) Soil arthropods for faunal indices in assessing

changes in natural value resulting from human disturbance. In:

Boyle T, Boyle CEB (eds) Biodiversity, temperate ecosystems

and global change. Sprtinger Verlag, Berlin, Heidelberg, New

York

Pizzolotto R, Mingozzi A, Cagnin M, Tripepi S, Aloise G, Barbieri A,

Scalzo A, Brandmayr P (1991) Effetti della ceduazione periodica

del castagneto sulle comunita di Coleotteri Carabidi, rettili,

uccelli e micromammiferi terricoli. S.IT.E. Atti 12:449–453

242 J Insect Conserv (2009) 13:231–243

123

Poldini L (1989) La vegetazione del Carso isontino e triestino. Lint

Publisher, Trieste

Rainio J, Niemela J (2003) Ground beetles (Coleoptera: Carabidae) as

bioindicators. Biodivers Conserv 12:487–506

Rushton SP, Luff ML, Eyre MD (1989) Effect of pasture improve-

ment and management on the ground beetle and spider

communitites of upland grasslands. J Appl Ecol 26:489–503

Samways MJ (1995) Insect conservation biology. conservation

biology series. Chapman & Hall, London

Spence JR, Langor DW, Niemela J, Carcamo HA, Currie CC (1996)

Northern forestry and ground beetles: the case for concern about

old-growth species. Ann Zool Fenn 33:173–184

StatSoft (2001) STATISTICA (data analysis software system),

version 6. www.statsoft.com

Stork NE (ed) (1990) The role of Ground Beetles in Ecological and

Environmental Studies. Intercept, Andover-Hampshire

Szyszko J (1983) State of Carabidae (Col.) fauna in fresh pine forest

and tentative valorisation of this environment. SGGW-AG

Monographs No. 28. Warsaw Agricultural University Press,

Warsaw, Poland

Telfer MG, Eversham BC (1996) Ecology and conservation of

heatland Carabidae in eastern England. Ann Zool Fenn 33:133–

138

Thiele HU (1977) Carabid Beetles in their environments. Springer,

Berlin, Heidelberg, New York

Usher MB (1986) Wildlife conservation evaluation: attributes, criteria

and values. In: Usher MB (ed) Wildlife conservation evaluation.

Chapman & Hall, London

Venn SJ, Kotze DJ, Niemela J (2003) Urbanization effects on carabid

diversity in boreal forests. Eur J Entomol 100:73–80

Vigna A (1993) Coleoptera Archostemata, Adephaga 1 (Carabidae).

Checklist delle specie della fauna italiana. Calderini, Bologna

Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998)

Quantifying threats to imperiled species in the United States.

Bioscience 48:607–615

J Insect Conserv (2009) 13:231–243 243

123