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Pests and Diseases in Portuguese Forestry: Current and New Threats

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Abstract and Figures

An overview of pest and disease problems in the main types of Portuguese forest is presented. Native pine forests, mainly Pinus pinaster and Pinus pinea have been occasionally affected by native bark beetles, cone feeders, one defoliator (the pine processionary moth) and a few fungi. Thus far, problems with these native pests and pathogens, arise mostly during outbreaks or epizootic periods. In most cases they are associated with poor forest management, fires or drought stress. Nevertheless, some alien pests and pathogens have recently become reason for concern, namely the pinewood nematode and Fusarium circinatum. Mediterranean forests composed of evergreen oaks, namely Quercus suber and Quercus ilex, were in the past mainly affected by defoliators such as Lymantria dispar and Tortrix viridana. During the second half of the 20th century, oak decline increased and was attributed to drought stress, together with a complex interaction of biotic agents. Fungi in the genera Biscogniauxia and Diplodia, the Oomycete Phytophthora cinnamomi together with bark and wood borers, in particular Platypus cylindrus, were associated with the most serious cases. For more than a century the exotic Eucalyptus forest plantations were free from pests and pathogens. However, they are currently threatened by increasing numbers of pests and diseases mainly originating from Australia. Some of them cause severe damage and compromise productivity. For all these forest ecosystems, health problems are expected to be favoured by climate changes and new biological invasions, implying that efforts should be made to develop new control strategies to combat future threats.
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Chapter 5
Pests and Diseases in Portuguese
Forestry: Current and New Threats
Manuela Branco, Helena Bragança, Edmundo Sousa
and Alan JL Phillips
Abstract An overview of pest and disease problems in the main types of Por-
tuguese forest is presented. Native pine forests, mainly Pinus pinaster and Pinus
pinea have been occasionally affected by native bark beetles, cone feeders, one
defoliator (the pine processionary moth) and a few fungi. Thus far, problems with
these native pests and pathogens, arise mostly during outbreaks or epizootic
periods. In most cases they are associated with poor forest management, fires or
drought stress. Nevertheless, some alien pests and pathogens have recently become
reason for concern, namely the pinewood nematode and Fusarium circinatum.
Mediterranean forests composed of evergreen oaks, namely Quercus suber and
Quercus ilex, were in the past mainly affected by defoliators such as Lymantria
dispar and Tortrix viridana. During the second half of the 20th century, oak
decline increased and was attributed to drought stress, together with a complex
interaction of biotic agents. Fungi in the genera Biscogniauxia and Diplodia, the
Oomycete Phytophthora cinnamomi together with bark and wood borers, in par-
ticular Platypus cylindrus, were associated with the most serious cases. For more
than a century the exotic Eucalyptus forest plantations were free from pests and
pathogens. However, they are currently threatened by increasing numbers of pests
and diseases mainly originating from Australia. Some of them cause severe
damage and compromise productivity. For all these forest ecosystems, health
M. Branco (&)
Centre of Forestry Studies, Institute of Agronomy (ISA), University of Lisbon,
Tapada da Ajuda, 1349-017 Lisbon, Portugal
H. Bragança E. Sousa
National Institute of Agrarian and Veterinary Research, I.P.,
Quinta do Marquês, 2780-159 Oeiras, Portugal
A.J. Phillips
Department of Life Sciences, Faculty of Sciences and Technology,
New University of Lisbon, 2829-516 Caparica, Portugal
Springer International Publishing Switzerland 2014
F. Reboredo (ed.), Forest Context and Policies in Portugal, World Forests 19,
DOI 10.1007/978-3-319-08455-8_5
problems are expected to be favoured by climate changes and new biological
invasions, implying that efforts should be made to develop new control strategies
to combat future threats.
Keywords Alien pests Bark borers Wood borers Castanea Chestnut Cone
feeders Defoliators Eucalyptus Fungal pathogens Insect pest Nematode
Oak Pest management Pinus Quercus
5.1 Introduction
The relevance of forest pests and diseases in a particular region needs to be
considered in the light of the historical evolution and present situation of forest
land cover, forest management practices as well as the environmental changes and
disturbances that have occurred within historical times. Changes in forest struc-
ture, namely tree species composition, tree density, age structure and dimensions,
as well as changes in cultural practices and external disturbances affecting trees,
such as forest fires and drought stress, have conditioned the susceptibility of
Portuguese forests to pests and pathogens during the last century. Additionally, the
repeated introductions of alien pests and pathogens in recent decades have had
major impacts on forest health at the national level.
Considering land cover, larger areas of forest land with a specific tree species
might result in an increased occurrence of pests and diseases, possibly as a con-
sequence of the increase in the concentration of their food resources (Hambäck and
Englund 2005). The low diversity of forest species in Portugal, along with the
dominant occurrence of clonal stands, could favour the occurrence of large out-
breaks of forest pests and pathogens, at either spatial or temporal scales, whenever
disturbances occur. Nevertheless, the three dominant types of forest in Portugal,
maritime pine, eucalyptus and cork oak are quite distinctive in terms of land-
ownership structure as well as silvicultural practices. Forest management also
determines tree susceptibility, defined as the lack of resistance of the forest land to
specific hazards, as well as the time period of exposure to risk. For example, a low
rotation period, i.e. cultivation cycle in forestry between plantation and harvesting,
reduces the period that trees are exposed to wood borers (Jactel et al. 2009,2012).
Portuguese pine forests are mainly distributed through small landownership, fre-
quently slightly or moderately managed, with natural regeneration, and stands of
uneven age. On the other hand, Eucalyptus forests in Portugal are usually more
intensively managed, frequently even-aged with short rotation plantations of about
1,100–2,500 tree ha
. At the opposite extreme are cork oaks, which are kept at
low tree density of 80–150 tree ha
, most usually in agro-forestry systems
combining cork oak production with pastures and agriculture crops. Such differ-
ences also contribute to distinct sanitary problems and control measures among the
three types of forests, as described in the following sections.
118 M. Branco et al.
In the Mediterranean basin, climate change has caused not only an annual
increase in temperature, as observed globally, but also a higher frequency of
extreme climatic events and changes in the quantity and distribution of precipi-
tation. Specifically, higher extreme values between day and night, with maximum
temperatures increasing at higher rates than minimum temperatures (Regato 2008),
more frequent extremely hot summer days, with temperatures above 40 C, and a
tendency for a decrease in winter precipitation has been registered (Solomon et al.
2007; Petit et al. 2005). Climatic models predict intensification of these tendencies,
with a temperature increase for the Mediterranean basin of 2.5–3.5 C until 2050
(Palahi et al. 2008), and decrease of precipitation of up to 30–45 % (Proença and
Pereira 2010). All these changes may have implications on the incidence of forest
pests and pathogens. Direct effects on the biology, distribution and behavior of the
insects and pathogens are expected as well as indirect effects through the increased
susceptibility of the hosts.
Changes in the biology and distribution of some forest insects in response to
on-going climatic changes have already been observed during the last 30–50 years.
In the Northern Hemisphere, a dispersal of some insect species to northern lati-
tudes or to colder areas has been registered (Bale and Hayward 2010; Menéndez
2007). This dispersion pattern is not particularly affecting the Mediterranean
Basin, except in mountain areas. Nevertheless, the establishment of alien insect
species originating from subtropical and tropical climates may increase in the
Mediterranean basin due to more favorable climatic conditions. Changes will
occur in the insect’s developmental cycle, survival and reproduction. Higher mean
summer temperatures should diminish the time to complete the life cycle and
cause a greater number of generations each year, and increase their breeding
capacity (Menéndez 2007), while milder winter temperatures may decrease their
mortality (Ayres and Lombardero 2000; Logan et al. 2003). On the other hand,
extreme events of intense precipitation or extremely high temperatures may also
have a negative impact on insect pests by increasing their mortality (Moore and
Allard 2008; Robinet et al. 2013).
Although many insects can act as primary pests, attacking vigorous plants and
overcoming their defenses, many others colonize plants already weakened by other
agents that break their defensive barriers (Sousa et al. 2011). Climate disturbances
causing drought stress or the higher occurrence of forest fire may be particularly
favourable for this kind of pest or pathogen. Additionally, higher temperature may
favour fungi, viruses and nematodes frequently associated with insects. These
organisms, which are vectored by the insects, may subsequently weaken the host
trees and making them more vulnerable for the insect pest attack (Paine et al.
1997). Furthermore, there is an increasing risk associated with the introduction of
exotic species, either by the international trade of wood and forestry products, live
plants and other commodities, or by their natural migration, which may be
enhanced by climatic changes.
Forest products and services provided by the forest, such as wood biomass,
cork, seeds, timber or soil conservation, will determine the economic values that
are exposed to pests and diseases (Jactel et al. 2009). The three main types of forest
5 Pests and Diseases in Portuguese Forestry: Current and New 119
also provide different products, mainly small round-wood for multiple purposes
and pine nuts from pine forests, wood for the pulp industries from Eucalyptus, and
cork from the montado system, thus imposing different economic impacts caused
by pests and diseases.
This chapter focuses on the main pests and diseases, past and present, and new
threats in three main forest types in the country, pines, evergreen oaks and
eucalyptus. Other broadleaved trees will also be mentioned, in particular the
chestnut trees, considering the large area it covers and its economic value, espe-
cially in the northern regions of Portugal. Due to the specificity of most insects and
pathogens, the majority of them affect trees only within one family or even one
genus. Furthermore, most of the insect species that feed on conifers do not feed on
broadleaved trees. Eucalypts are so geographically and phylogenetically distant
from European tree species that they harbour completely distinct herbivores. Thus,
the different forest types are also quite separated according to the organisms that
cause major problems. For each forest type we present here information on its
present distribution and from historical times as an approach to understand the
incidence of pests and pathogens.
Insects and pathogens that attack young seedlings are frequently polyphagous,
and a few of them also affect the three main forest types. These are mainly a
problem in nurseries, which will not be considered here.
5.2 Pine Forests
The Maritime pine Pinus pinaster Aiton is the most important pine species in
Portugal in terms of area planted and economic value. At present the species
occupies over 714,000 ha, representing 23 % of the national forest area (ICNF
2013). Its main products are manufactured wood, pallets, boards, and resin, which
together represent about 306 million Euros of exports (Mendes et al. 2004).
Portuguese maritime pine forests were initially restricted to the coastline, north
of the Tagus River, but as early as the 13th century forestation of wide areas of
central Portugal was established (Fabião 1987). During the 20th century large
areas were planted with maritime pine, especially in mountain regions of the
Northeast and the Centre of Portugal where soils are poor. During the 1940s the
maritime pine area in the country reached about 1.3 million ha (Costa 1995).
The stone pine Pinus pinea L. is the second most common pine species, with
increasing importance in the Portuguese forestry sector, mainly for the production
of pine nuts. Since 2005 its area has increased by 54 %, and at present it covers
175,742 ha (ICNF 2013).
The continuous stands of maritime pine predisposes them to large-scale forest
fires and infestations by bark beetles. Severe bark beetles attacks, associated with
forest fires, drought periods or storms were occasionally reported (Neves 1964).
The pine defoliator, processionary moth Thaumetopoea pytiocampa Schiff., and
the pine shoot moth Rhyacionia buoliana Shiff., were also reported as causing
120 M. Branco et al.
considerable economic damage, particular to young stands of maritime pine (Cabral
et al. 1965). More recently, in 1999, the alien pine wood nematode (PWN), Bur-
saphelenchus xylophilus (Steiner et Buhrer) Nickle (Nematoda: Aphelenchoididae),
the causal agent of pine wilt disease, emerged as a major concern for the maritime
pine industry leading to research on the associated organisms (Sousa et al. 2002).
5.2.1 Bark and Wood Borers
Among bark and wood borers, four main species stand out, the pine weevil Pis-
sodes castaneus (DeG.), the six-toothed pine bark beetle Ips sexdentatus Boern.,
the mediterranean pine engraver Orthotomicus erosus (Woll.) (Fig. 5.1) and the
pine shoot beetle Tomicus piniperda (L.) (Ferreira and Ferreira 1990). More
recently, it was shown that the Mediterranean pine shoot beetle Tomicus destruens
(Boern.) was widely distributed in the country, whereas the sister species T. pin-
iperda was mostly present in the North of Portugal (Vasconcelos et al. 2006). The
two closely related species are morphologically indistinct and for this reason the
past attacks of T. destruens might have been assigned to T. piniperda due to
misidentification. Nevertheless, the two species differ in their biological cycle. The
flight period of T. destruens occurs in autumn while for T. piniperda it is in early
spring (Vasconcelos et al. 2005).
The five main bark beetles further diverge on their ecological niche, namely on
the preferred age of host trees and preferred parts of the tree trunk, which is related
to beetle size and its biology. For example, whereas I. sexdentatus attacks larger
trees, with breast-high diameter (dbh) from 20–40 cm (Ferreira and Ferreira 1990),
and the attacks occur mainly on the lower part of the tree trunk, extending to
ground level (Chararas 1962), O. erosus and Tomicus sp. attack smaller and
younger trees, and frequently the upper part of the trunk. All these species prefer
trees that have been weakened in some way or are under stress. However, the pine
weevil P. castaneus, may attack young healthy trees from 4–15 years old (Day
et al. 2004), although it occurs also under some kind of tree stress. Slightly burned
trees at the edges of forest fires, or smaller dominated trees are also preferred hosts
for P. castaneus. Differences in the number of generations and type of galleries
also distinguish these species. Both I. sexdentatus and O. erosus are polygamous
and produce from 2–5 generations per year, whereas the two Tomicus species are
monogamous and univoltine, although they can produce 2–4 sister-generations in
Portugal. Tomicus piniperda adults in particular are early flyers and can be found
in winter with air temperatures around 8 to 9 C (Ferreira and Ferreira 1990).
The bark beetles select the susceptible host by decoding their odors, mainly
volatile terpenes such as a-pinene. In Portugal, T. destruens was demonstrated to
have a preference for the maritime pine during the trunk feeding phase, which might
be governed by the volatiles released by this species (Vasconcelos et al. 2003). In fact,
the maritime pine presents a bouquet of volatiles distinguishable from other closely
related pine species, namely from P. pinea and Pinus sylvestris L. (Santos et al. 2006).
5 Pests and Diseases in Portuguese Forestry: Current and New 121
For the multivoltine species, I. sexdentatus,O. erosus and P. validirostris, the
ongoing climatic changes may favour a greater number of generations and thus
higher reproductive growth. Effectively, an extension of the O. erosus flight period
to an almost continuous year round, from February to December, as observed in
recent years in Portugal, corroborate a scenario of a greater number of generations
(Sousa, pers. observ).
Bark beetle damage usually results in tree mortality. For the two pine shoot
beetles, severe damage is also due to the attacks on yearly shoots during the
maturation feeding period, which is essential for the adult gonad development in
this species (Fernandez Fernandéz et al. 1999). During shoot feeding the beetles
show a preference for healthy and vigorous trees, in contrast with the trunk attack
(Branco et al. 2010). As a consequence of this feeding activity, the shoots dry out
and are easily broken. Bark beetles also play an important role as vectors of the
blue-stain fungi Ophiostoma and Leptographium, carrying the spores in special-
ized structures (mycangia) located near the mandibles and on the sides of the
pronotum and the elytra (Solheim and Långström 1991).
All the mentioned bark borer species are colonizers of burned trees, and in
Portugal they are closely associated with trees damaged by forest fires or drought
stress. Ips sexdentatus is especially highly attracted to recently burned trees, and
complete gallery systems and egg-layings can be found just 1 week after a forest
fire (Ferreira and Ferreira 1990). Inadequate cultural practices, such as leaving
dead trees or debris in the field will provide further resources for the bark beetles
to reproduce and promote outbreaks (Ferreira and Ferreira 1990).
Completely different is the pine moth Dioryctria sylvestrella Ratz. (Lepidop-
tera: Pyralidae), whose larvae also mine galleries under the bark of the trunk where
they feed on phloem, but which prefer vigorous trees (Jactel et al. 1996). The
larval feeding activity causes ring incision, usually at the insertion of the branches
and although seldom causes tree death, it may result in tree deformation and
reduced timber quality. Tree vigor as induced by fertilization, and pruning injuries
are known factors that favour attack by D. sylvestrella.
Fig. 5.1 Adult of
Orthotomicus erosus in the
bark crevices of a Pinus
pinaster tree (Photo
by E. Sousa)
122 M. Branco et al.
5.2.2 Pine Defoliators
The pine processionary moth Thaumetopoea pityocampa Schiff (Lepidoptera:
Notodontidae) is the most important defoliator of pines in Portugal, as in other
regions of the Mediterranean Basin. Larvae develop from September until
February/March feeding on pine needles. For other Mediterranean regions the
populations of pine processionary moth are known to have cyclical outbreaks, yet
no studies confirm such population dynamics for the Portuguese populations.
Uneven aged stands, traditionally originating from natural regeneration, and high
landscape heterogeneity due to the small property size, might limit or mask pine
processionary moth outbreaks in Portuguese pine forests. Nevertheless, intense
attacks above 50 and up to 100 % defoliation have been observed in young
plantations with significant negative impacts on tree growth (Barrento et al. 2008).
Additionally, defoliated trees are then predisposed to attack by pathogens and
other insects, namely bark and wood borers (Ferreira and Ferreira 1990). Both of
the two main native pines, P. pinaster and P. pinea can be severely infested, yet
the composition and reduced amount of volatiles released by P. pinea make it a
less attractive species for the pine processionary moth (Paiva et al. 2011). Nev-
ertheless, P. pinea is most favourable for larvae development and might be heavily
attacked. Young stands of both species, 12–25 years old, are particularly prone to
attack by the pine processionary moth. Some non-native pine species occasionally
used in forest plantations in Portugal, such as P. radiata and P. nigra, are also
severely defoliated by this insect. Besides the impacts caused to pine forests, the
species poses a major public health concern due to allergies caused by the larvae
urticating hairs (Gatto et al. 2009).
As a consequence of climate change, the pine processionary moth has been
colonizing new regions in Europe, at higher latitude and altitude (Robinet et al.
2013). This is not the case in Portugal, where the species is present throughout the
country wherever the host pines are found. Nevertheless, in Leiria National Pine
Forest, in Central Portugal, a unique population of the pine processionary moth,
exhibiting shifted phenology with larval development during the summer months,
was found in 1997 and is currently expanding (Fig. 5.2). This population displays
phenotypic and genetic differentiation from the sympatric founder population with
the typical phenology (Santos et al. 2013). The two populations are reproductively
isolated by time, thus a rare process of allochronic speciation is ongoing (Santos
et al. 2007,2011a). Research results indicate that the shifted population is highly
successful, exhibiting divergent adaptation to its phenology, such as higher tol-
erance of the larvae to extremely high temperatures (Santos et al. 2011b). Since
mature larvae of this shifted population are active during summer, coinciding with
human leisure activities in natural environments, it is causing major public health
The pine sawfly Neodiprion sertifer (Geoffroy) (Hymenoptera, Diprionidae) is a
second, minor defoliator of pines trees in Portugal, feeding on pine needles during
spring. The species occurs only sporadically and in restricted areas and therefore is
5 Pests and Diseases in Portuguese Forestry: Current and New 123
hardly considered a problem (Ferreira and Ferreira 1990). Nevertheless, N. sertifer
is considered a major defoliator of pines in Europe (Day and Leather 1997). Its
preference for the Scots pine P. sylvestris, which has minor representation in
Portugal, may explain its low densities in the country. In Portugal, N. sertifer was
observed in young P. pinaster plantations but not on P. pinea (Ferreira and
Ferreira 1990).
5.2.3 Sap-Suckers
Several sap-suckers, mainly aphids and scale insects, feed on pine trees but usually
do not constitute a serious problem. In some particular conditions high densities may
occur, especially in spring, causing needle discoloration, reduced growth and
weakened trees. The aphid Cinara maritimae (Dufour) (Hemiptera: Lachinidae) is
one of the sap-suckers most commonly found during spring and summer in pine
forests where they feed on pine needles. Their populations usually have a rapid
growth with subsequent decline. High levels of parasitism by encyrtid wasps par-
tially accounts for the rapid decline. Pineus pini (Macquart) (Hemiptera: Adelgidae)
Fig. 5.2 Nest of the pine
processionary moth,
Thaumetopoea pityocampa
with summer larval
development population in
Leiria, Portugal. Nests are
loose with very little silk
(Photo by Helena Santos)
124 M. Branco et al.
may also occur at high densities, particularly in nurseries and young plantations. It
has been observed causing severe damage in young P. pinea plantations, which is
probably associated with fertilizer applications. Additionally, two armored scale
insects Leucaspis pini (Hartig) and Leucaspis pusilla (Loew) (Hemiptera: Diaspi-
didade) may be occasionally observed on pine needles, especially in young trees but
without causing significant damage.
The maritime pine bast scale, Matsucoccus feytaudi Ducasse is one of the best
known scale insects feeding on P. pinaster. The species is monophagous feeding
uniquely on P. pinaster.Matsucoccus is distributed worldwide, specialized on
pines, and several species are important pests, such as M. feytaudi in southeastern
Europe (Jactel et al. 1998). In Portugal the pine bast scale has an endemic steady
state, is found in almost all P. pinaster stands but in general at low densities with
no apparent damage. A co-evolutionary history of M. feytaudi and P. pinaster in
the Iberian Peninsula (Burban et al. 1999) may account for the low severity of this
insect pest on this region. Additionally, several insects preying on M. feytaudi in
its native range, known for its kairomonal attraction to the sex pheromone of
M. feytaudi may further account for the low population of M. feytaudi in this
country (Branco et al. 2006a,b,2011).
5.2.4 Seed and Cone Insects
The pine cone weevil Pissodes validirostris Sahlberg (Coleoptera: Curculionidae)
and the pine cone moth Dyorictria mendacella Staudinger (Lepidoptera: Pyrali-
dae) have long been known as important damaging agents of the cones and seeds
in Portugal. Both insect species can attack several pine species, in Portugal they
are found mainly on P. pinaster and P. pinea. The pine cone weevil is univoltine,
eggs are laid between the scales of the cones in April–May and the larvae burrow
tunnels in the cone during spring and summer. Pupation occurs within the cones
and adults emerge in August–September and thereafter feed on twigs. The cone
moth displays two cycles per year, with feeding activity in spring and autumn. To
pupate the larvae burrow into the soil.
All these agents can affect production of seeds and, consequently natural
regeneration, as well as the production of pine nuts by P. pinea. However, seed
production losses associated with the pest have not been estimated. The production
of P. pinea pine nuts was estimated to be about 2.1, 4.0 and 0.5 million Kg in
2009, 2010 and 2011, respectively. Variation between years can be due to either
biotic agents or the cycles of mast years, usually with two mast years of peak
production interspersed with 2 years of reduced production. However, more dis-
turbing is the decrease of the yield of pine nuts.cone
observed in the last years.
Effectively, data of two major manufacturing industries (Preparadora de Pinhões
Lda and António Pais Lda) show stability of the pine nut yield in the last 18 years,
varying between 3 and 4 %, but in the 2011–2012 campaign this value dropped
below 2.5 %, which was never observed previously. The recent introduction, in
5 Pests and Diseases in Portuguese Forestry: Current and New 125
2010, of the alien western conifer seed bug Leptoglossus occidentalis Heidemann
(Hemiptera: Coreidae) (Fig. 5.3) might be associated with this decline.
This invasive insect pest, native to North America, was accidentally introduced in
Italy in 1999 (Taylor et al. 2001), and spread rapidly to most of western and central
Europe (Rabitsch 2008; EPPO 2010). Both adults and nymphs feed on young seeds or
flowers, sucking the endosperm and cause abortion of the seeds (Bates and Borden
2005; Mitchell 2000). More than 40 species of conifers, mainly Pinus sp. and
Pseudotsuga menziesii are known hosts. In Portugal the western conifer seed bug was
detected in both maritime pine and stone pine stands (Sousa and Naves 2011; Grosso-
Silva 2010). This species is causing much apprehension among local seed producers
and industrialists who are concerned with its possible effects on pine nut production.
5.2.5 Pine Wilt Disease
In 1999 the causal agent of pine wilt disease B. xylophilus (PWN) was first detected
at Marateca, Setúbal. This detection led to the adoption of severe restrictions on the
movement of plants, woody material, products and by-products of host tree species.
In 2009, PWN was also detected in the Portuguese Island of Madeira.
PWN is endemic to North America where it coexists in equilibrium with native
pines. In contrast, its accidental spread to Japan, in the early twentieth century,
caused an abnormal mortality of endemic pine species (Mamiya 1984). PWN was
subsequently introduced into China, Korea and Taiwan. Molecular studies (RFLP)
carried out on Portuguese populations of PWN showed genetic similarities with
the East Asian populations (Metge and Burgermeister 2005). The adult nematode
is less than 1.5 mm in length and transmission to a healthy host tree occurs by the
feeding activity of the insect vector, which in Portugal is Monochamus gallo-
provincialis Olivier (Naves et al. 2007a) (Fig. 5.4). During oviposition in the tree
bark, secondary transmission of PWN can also occur, however to a lesser extent
than through feeding (Naves et al. 2007b).
Pine wilt disease PWD is a complex interaction amongst three distinct organ-
isms: the pine wood nematode, the insect vector and the tree host. In Portugal the
disease appears only in P. pinaster. The introduction of B. xylophilus disrupted a
long-term equilibrium between the native insect M. galloprovincialis and its local
host, P. pinaster. Although M. galloprovincialis adults feed on healthy shoots for
sexual maturation, for breeding, they are attracted only to stressed, dying or
recently dead trees (Sousa et al. 2001). The association with the PWN renders the
insect the ability to indirectly kill the trees via transmission of the nematode.
Inside the tree the nematode has very short generation cycles and high repro-
duction rates. About 20–30 days after infection, leaf transpiration ceases and partial
interruption in the sapwood obstructs sap ascent, causing discoloration and wilting
of leaves all over the crown. Needles turn yellow and then brown starting with the
younger ones, but remain attached to the tree for a long period of time (Mamiya
1984). Symptoms may be confused with attacks by other biotic agents, such as bark
126 M. Branco et al.
beetles. Laboratory morphological identification or molecular techniques is the
only way to confirm infection by the nematode (Penas et al. 2002; Hu et al. 2011).
Transmission of PWN occurs during summer with rapid development and tree
decay, thereafter. As the wood decays the nematodes shift to ‘dauer-larvae’’, a
resistant stage of development. In late spring, these nematodes aggregate around
the insect-vector pupal chambers. As soon as the callow adult is formed, the
nematodes transfer to the insect’s trachea or under the elytra, the antennae and legs
(Naves et al. 2006). The emergence of new adults from the trees in the following
year completes the cycle.
5.2.6 Diseases Caused by Fungi
Pine pitch canker, caused by Fusarium circinatum Nirenberg & O’Donnell, is
probably the most destructive disease causing severe damage on several species of
pine (Fig. 5.5). Fusarium circinatum can infect the vegetative and reproductive
Fig. 5.3 Egg mass, nymph and adult (right)ofLeptoglossus occidentalis. (Photos Teresa
Fig. 5.4 Adult of
galloprovincialis (Photo by P.
5 Pests and Diseases in Portuguese Forestry: Current and New 127
parts of the hosts of all ages. The first symptoms of pitch canker are usually wilting
and discolouration of needles. On adult trees the fungus causes needle blight,
dieback, resin flows from the infected areas on the shoots, branches, trunk and
cones (Wingfield et al. 2008). The capacity to infect and survive in cones (even
from healthy branches) greatly facilitates its spread into new areas. Severe
infections may cause crown dieback and death of the tree. On seedlings the
symptoms are damping-off and root rot. The disease is spread by wind and insect
vectors but long distance dispersal is connected with the movement of infected
plants or seeds.
Pine pitch canker was first reported on Pinus species in North Carolina, USA in
1946 (Hepting and Roth 1946). In Europe F. circinatum was first reported from
northern Spain in 1997 causing a severe root disease of nursery seedlings of exotic
P. radiata and P. pinaster (Landeras et al. 2005; Pérez-Sierra et al. 2007). Later it
was reported from Italy on P. halepensis and P. pinea (Carlucci et al. 2007). In
2007 dieback symptoms were observed on groups of Pinus radiata and P. pinaster
in a nursery located in the central region of Portugal and F. circinatum was
isolated from the plant tissues (Bragança et al. 2009a). So far the disease seems to
be absent from forests, and is restricted to a small number of nurseries.
To prevent the spread of this fungus in Portugal, surveys have been intensified
in nurseries, and plant and seed traders. Eradication measures have been taken,
including the destruction of all contaminated lots of plants, intensive surveillance
of infected sites and surrounding areas and restricted quarantine measures as
determined by legislation (Commission Decision 2007/433/EC). The Portuguese
Forest Authority (AFN) has conducted a survey throughout the country to control
and eradicate the fungus (Ribeiro et al. 2010). Training for inspectors and formal
presentations to develop extension education tools on pitch canker have been held
Fig. 5.5 Early symptoms of
pine pitch canker on Pinus
seedlings (Photo by Helena
128 M. Branco et al.
including sampling procedures, description of disease symptoms, and relevant
aspects of the biology of the fungus, management recommendations and economic
factors. Research work is ongoing with the aim of improving the detection method
and to formulate control measures (Ribeiro et al. 2010).
Since 2009, diseased seedlings and adult pine trees have been analyzed by the
Plant Disease Diagnostic service of Instituto Nacional de Investigação Agrária e
Veterinária (INIAV), as required by owners, governmental agencies and local
authorities and also within the scope of research projects. The most frequently
encountered pathogenic fungi on pine seedlings are Cylindrocarpon sp., Botrytis
cinerea Pers.: Fr., Lophodermium seditiosum Minter, Staley & Millar and Pes-
talotiopsis sp. On adult trees Pestalotiopsis sp. was the most common, but Do-
thistroma sp., L. seditiosum,Diplodia sapinea (Fr.) Fuckel and Thyriopsis
halepensis (Cooke) Theiss. & Syd. were also frequent (Bragança et al. 2012). In a
survey of the Botryosphaeriaceae associated with conifers in Portugal (Alves et al.
2013)D. sapinea was the most common fungus on Pinus species. Neofusicoccum
luteum,N. australe and N. parvum were also frequently isolated. Unfortunately,
there is no information about the prevalence, distribution or importance of any of
these pathogens and associated diseases in Portuguese forests.
5.3 Evergreen Oak Forests
Cork oak (Quercus suber L.) and holm oak (Quercus ilex L.) forests are very
specific, complex and delicately balanced ecosystems that exist naturally in the
Mediterranean Basin. In Portugal, the two species have great value for their eco-
nomic, social and ecological importance. Although, mortality in cork oak stands has
been recorded as far back as the late 19th to early 20th century (Câmara-Pestana
1898; Lopes-Pimentel 1946; Natividade 1950; Branquinho-d’Oliveira 1931;
Ramires 1898), during last 3 decades a global and continuous loss of vigour has
been recorded throughout its range in the Mediterranean basin. The decrease in
stand density, lack of regeneration and decrease in the quality of cork are major
causes for concern. Drought and high temperatures, impoverishment of soil fertility
due to agricultural practices, together with pests and diseases are implicated in cork
oak and holm oak decline (Cabral et al. 1993; Costa et al. 2010). Several symptoms
have been associated with outbreaks of the decline and mortality, namely thinning
of the canopy, dry and discoloured leaves, dry branch tips, cankers on the trunk and
branches with presence of fungi and insects and a continuous process of abnormal
and slow death.
According to Ferreira and Ferreira (1991) and Cabral and Ferreira (1999), over
92 insect species can cause damage to cork and holm oak stands, although few
impose significant economic loses. Most of the species are defoliators while others
colonize the trunk, cork and branches.
5 Pests and Diseases in Portuguese Forestry: Current and New 129
5.3.1 Bark and Wood Borers
The main problems with bark and wood borers on the evergreen oaks are caused
by the ambrosia beetle Platypus cylindrus Fab., two buprestids Coraebus undatus
Fab., Coraebus florentinus Hbst., and the ant Crematogaster scutellaris Olivier. Of
lesser importance is the longhorn beetle Cerambyx cerdo L.
The oak pinhole borer P. cylindrus (Fig. 5.6) was once regarded to be of
secondary importance as a pest of cork oak stands in Portugal and other Medi-
terranean countries (Seabra 1939; Neves 1950). However, since the 1980s its
numbers have increased in Portugal and attacks have been noticed in apparently
healthy trees, particularly recently debarked ones (Sousa 1992; Sousa and
Débouzie 2002). Platypus cylindrus feeds on ambrosia fungi (namely Raffaelea
spp.), which it introduces into the sapwood of the host trees along the galleries
bored by the adults. The fungus invades the tree and causes it to wilt and die.
Specialized organs (mycangia) located on the beetle prothorax, serve to transport
the fungus (Cassier et al. 1996). The temporal variability of egg laying allows the
coexistence in the galleries of P. cylindrus of different developmental stages.
Consequently, a long emergence period, from spring to autumn, which may
continue for a second generation during the spring of the following year, can be
observed (Sousa and Débouzie 1999,2002).
The time between the onset of the first symptoms to death can vary from
3–18 months, depending on the host vigor (Sousa and Inácio 2005). Host selection
depends mainly on stand and tree characteristics (health status and dimensions)
and cultural practices (debarking intensity and period) (Sousa and Débouzie 1993,
1999). High densities of attacks on the same tree corroborate the existence of
aggregation pheromones (Sousa and Inácio 2005).
Coraebus undatus (Coleoptera: Buprestidae) almost exclusively breeds on
cork-oak trees and is mainly a problem in the Mediterranean Basin (Soria and
Ocete 1990). The insect does not kill standing trees, but damages cork planks,
reducing the value of the cork. Awareness of the damage related to C. undatus
activity lead to its recent inclusion in the list of European xylophagous and
phloeophagous insects of living trees that cause damage and need a common
strategy for survey (Lieutier 2007). The females lay eggs individually or in small
groups in bark flaps and fissures of the trunk from June to July (Evans et al. 2004).
The hatched larvae perforate successive layers of the cork, penetrate into the bark
and construct large galleries around the trunk (Romanyk and Cadahía 1992). Upon
completion of development (2 years), the larvae make a chamber in the bark and
transform into pupae and then into adults that eventually exist through a hole, mate
and complete the cycle. In Portugal, the percentage of trees attacked by C. undatus
per stand varies from 0 % up to more than 50 %.
130 M. Branco et al.
5.3.2 Defoliators and Seed Eaters
Both evergreen and deciduous oaks harbour many species of defoliator insects.
Most species are not noticeable and cause no significant damage. However, a few
species have been considered a concern in Portugal, especially for Q. suber due to
the high levels of populations attained. Consequently, economic losses due to
acorn loss, lack of wood production, reduced cork growth and cork quality have
been reported (Cabral and Ferreira 1999). These impacts depend on the intensity of
defoliation and the time at which defoliation takes place. Ecological impacts are
also expected. In particular, being at the bottom of food webs, oak defoliators may
have significant cascade effects on higher trophic levels, namely as food sources
for birds (Pereira et al. 2014). Several oak defoliator species undergo outbreaks,
which can happen at regular intervals and last for several years. During outbreaks,
complete defoliation may occur. Among the species with cyclical outbreaks, the
gypsy moth Lymantria dispar L. (Lep., Lymantridae) (Fig. 5.7) is one of the best
known species in Portugal, especially for the damage it causes on Q. suber. Other
conspicuous Lepidoptera in oak forest are Euproctis chrysorrhoea L. (Lymantri-
dae) and Tortrix viridana L. (Tortricidae), which feeds on buds and young leaves
at budburst, and is the earliest species to appear in early spring. This species is
considered to be the most serious bud moth attacking evergreen oaks. In the past,
when acorns were most valuable for the production of pigs in the ‘‘montado’
system, a high negative correlation between acorn production, and therefore pig
production, and T. viridiana population outbreaks, was commonly established.
In more recent decades, outbreaks of the pine sawfly Periclista andrei Konow
Fig. 5.6 Platypus cylindrus
(Photo by E. Sousa)
5 Pests and Diseases in Portuguese Forestry: Current and New 131
(Hym., Diprionidae) also become very noticeable on cork oak trees (Ferreira and
Ferreira 1991; Pereira et al. 2014).
Two main groups of insects, Curculio elephas Gyll. (Coleoptera; Curculioni-
dae) (Fig. 5.8) and moths from the genus Cydia spp (Lepidoptera, Tortricidae)
mainly feed on acorns. Larvae of both species feed inside acorns excavating
galleries, starting at the base of the cupule while the acorns are still forming.
Although year and site variation on the percentage of infested acorns is high,
infestation levels are usually elevated, frequently exceeding 60 % (e.g. Branco
et al. 2002). The insect population densities and the available resources dictated by
acorn production determine the infestations rates. Thus, mast and non-mast years,
characteristic of acorn production on oak trees, contribute in large part to the inter-
annual variability. Larval feeding activity of these insects concentrates on the basal
carbohydrate-rich cotyledons and seldom causes direct damage to the tip embryo,
thus acorn predation seldom affects their ability to germinate (Branco et al. 2002).
Nevertheless, acorn weight losses and structural changes resulting from the insect
feeding activity cause reduced seedling growth and decreased post-emergence
survival (Branco et al. 2002). This may contribute to a reduction in natural
regeneration in cork oak open land together with other biotic factors.
5.3.3 Diseases Caused by Fungi
Soil-borne pathogens including Phytophthora spp, namely P. cinnamomi Rands
(Moreira et al. 1999; Moreira and Martins 2005) and Diplodia canker caused by
Diplodia corticola AJL Phillips, A Alves & Luque (Alves et al. 2004), have been
regarded as the principal primary pathogens causing oak mortality in Portugal.
Symptoms of both diseases are often similar and normally the disease occurs in
foci within large areas or stands.
Phytophthora cinnamomi infects the roots and reduces their capacity to absorb
water and nutrients. Foliage of affected trees withers and turns brown, and
Fig. 5.7 Larvae (left) and female egg laying (right)ofLymantria díspar (Photo by E. Sousa)
132 M. Branco et al.
bleeding cankers develop on the trunk (Fig. 5.9). For some time it was considered
to be the main pathogen responsible for cork and holm oak mortality in Portugal
(Brasier et al. 1993; Moreira et al. 2006). It is also frequently associated with
declining cork oaks in Sardinia (Scanu et al. 2013). The symptoms observed in the
aerial part of trees are similar to those caused by drought.
Pythium spiculum B. Paul and Pythium sterilum Belbahri and Lefort, also
Oomycetes, were recently reported on holm and cork oak trees, in Spain and
Portugal causing a root rot similar to that induced by P. cinnamomi (Jiménez et al.
2008; Serrano et al. 2012).
Several fungi that cause cankers and diebacks are also considered to be
important contributing factors (Luque et al. 2001). Oliva and Molinas (1986) and
Luque and Girbal (1989) reported a Diplodia species associated with diseased cork
oaks in northeastern Spain. Luque and Girbal (1989) noted that conidia of the
isolates they studied were larger than typical for D. mutila. Alves et al. (2004)
introduced the species D. corticola for the large-spored Diplodia associated with
oak trees.
Diplodia corticola can affect plants of different ages and disease symptoms
include chlorosis, dieback (Fig. 5.10), thinning of the crown, branch and trunk
cankers, bark cracks, and vascular necrosis. The bleeding cankers on the trunk and
the thinning of the crown are similar symptoms to those caused by P. cinnamomi.
Luque and Girbal (1989) reported that after cork removal Diplodia corticola
invades the exposed trunks and causes death and wilting of Q. suber in north-
eastern Spain. In Portugal this fungus was first reported in 1990 (Fonseca 1991)
under the name of Botryosphaeria stevensii Shoemaker, with Diplodia mutila (Fr.:
Fr.) Fr. anamorph.
Fig. 5.8 Cork oak acorns
consumed by Curculio
elephas (Photo by António
5 Pests and Diseases in Portuguese Forestry: Current and New 133
Fig. 5.9 Trunk canker
caused by Phytopthora
cinnamomi on cork oak
(Photo by Helena Bragança)
Fig. 5.10 Diplodia dieback
of cork oak caused by
Diplodia corticola (Photo by
Helena Bragança)
134 M. Branco et al.
Diplodia corticola produces the phytotoxin Diplopyrone, which causes wilting
of cork oak cuttings (Evidente et al. 2003). Inoculation experiments on 6-months
old cork oak seedlings showed that symptoms develop rapidly after inoculation
and mortality is 100 % within a few weeks (H. Bragança personal communica-
tion). In Portuguese cork oak stands, canopy symptoms caused by D. corticola are
frequently confused with symptoms caused by P. cinnamomi. In fact the two
pathogens often coexist. Linaldeddu et al. (2013) determined that D. corticola and
P. cinnamomi act together to cause a severe decline and mortality of Holme oaks
on Caprera island in Sardinia. Of the various Botryosphaeriaceae and Phytoph-
thora species associated with the disease, D. corticola proved to be the most
aggressive in their inoculation experiments.
Diplodia corticola seems to be widespread in Portugal. Over the last years the
Plant Disease Diagnostic service of INIAV has detected it in samples of diseased
seedlings and mature cork oak trees collected from different regions of country
(Bragança et al. 2013). Nevertheless, no national monitoring survey has been
established to determine the impact of the pathogen or its contribution to cork oak
Several other fungi have been associated with oak decline and mortality in
Portugal. These include charcoal disease caused by Biscogniauxia mediterranea
(de Not.) Kuntze (Santos 2003; Santos and Martins 1992; Henriques et al. 2012),
Armillaria root rot disease caused mainly by Armillaria mellea (Vahl) P. Kumm.
(Azevedo 1976; Bragança et al. 2004), diffuse canker caused by Coryneum
modonium (Sacc.) Griffon and Maubl. (Bragança et al. 2013), various species of
Cryphonectria (Branquinho-d’Oliveira 1931; Santos et al. 2005; Bragança et al.
2011) and several Ophiostomatoid fungi, such as Raffaelea spp. (Inácio et al. 2012).
Some of these fungi are widespread throughout Portugal. However, although they
are frequently associated with decline and mortality, there is little evidence to
regard them as primary pathogens. For example, B. mediterranea is normally found
on moribund trees that have been attacked by either P. cinnamomi or D. corticola.
Luque et al. (2008) tested various fungicides for activity against D. corticola
in vitro and in field applications. They showed that benomyl, carbendazim,
cyprodinil +fludioxonil, thiabendazol and thiophanate-methyl applications after
cork removal can protect trees from infection by D. corticola. However, at present
no cide treatments or other control measures have been approved.
5.4 Eucalyptus
The area planted with eucalyptus has increased from less than 50,000 ha in the
1950s to the present 812,000 ha, which represent the dominant forest type in
Portugal (ICNF 2013). As a consequence, the values at risk to damage by pests and
diseases has experienced an increasing trend in eucalyptus forests. Eucalyptus
globulus is the main species used for forest plantation but in urban parks, arboreta
and roadside trees, other species have been used, mainly E. camaldulensis.
5 Pests and Diseases in Portuguese Forestry: Current and New 135
5.4.1 Insect Pests
From the early forest plantations in the 1950s until the 1980s eucalyptus planta-
tions were extremely healthy. A scenario that would change after the introduction
of the eucalyptus longhorn beetle Phoracantha semipunctata Fab., which imposed
high tree mortality and productivity losses. This became aggravated thereafter with
an increasing trend of new pest arrivals originating from Australia as well as new
emerging diseases.
Ctenarytaina eucaliptii Maskell (Hemiptera: Psyllidae) was the first alien insect
pest detected in Eucalyptus stands in Portugal in the late 1970s (Azevedo and Figo
1979). This sap-sucker feeds on the buds of the juvenile leaves and is primarily a
problem in nurseries (Ferreira et al. 1994) although not usually in forest stands.
The psyllid was found to be predated by many native predators, anthocorids,
syrphids, coccinelids and chrysopids (Azevedo and Figo 1979), which together
might have partially accounted for its low impact.
The newly arrived P. semipunctata in the 1980s generated far more alarm. After
its first detection, the beetle spread quickly and in a few years it became the main
concern for the Portuguese eucalyptus plantations industries (Araújo et al. 1985).
As with many wood borers, it attacks preferably trees under physiological stress,
especially water stress, causing tree death (Caldeira et al. 2002). Consequently, in
the southern regions of the country, with drier Mediterranean climate, and partic-
ularly in sandy soils, changes in land use occurred through the replacement of
E. globulus by other tree species or non-forestry land uses. Forest management
practices, namely monitoring and sanitary cuts, further contributed to solve the
problem. Two decades later, in 2001, a congeneric wood borer P. recurva Newman,
arrived in the Iberian Peninsula (Valente and Ruiz 2002). Up to now, the distri-
bution of P. recurva seems to be more restricted to the southern areas and damage is
much less than is caused by P. semipunctata. Previous changes in land use and
forest management practices might also have contributed to the lower vulnerability
of the eucalyptus plantations to this new invasive species with a similar ecology.
The eucalyptus snout beetle, Gonipterus plantensis Marelli (formerly known as
G. scutellatus) has been the major cause of tree growth losses in the Centre and
North of Portugal since the late 20th centuary until the present (Fig. 5.11). Volume
production losses of up to 70 % are observed in the more affected areas, and an
increase trend of wood loss with elevation is found (Reis et al. 2012).
In the last decade, seven new invading pest species were found, namely three
sap-sucking psylids, Ctenraytaina spatulata Taylor, Glycaspis brimblecombei
Moore, Blastopsylla occidentalis Taylor (Valente et al. 2004; Valente and Hod-
kinson 2009; Pérez-Otero et al. 2011), one eriophyid mite, Rhombacus eucalypti
Ghosh & Chakrabarti (Ferreira et al. 2006), two eulophid gall wasps Leptocybe
invasa Fisher & La Salle and Ophelimus maskelli Ashmead (Fig. 5.12) (Branco
et al. 2006c,2009,2014), and a heteropteran Thaumastocoris peregrinus Car-
pintero & Dellapé (Garcia et al. 2013). All these insect pests originated from
Australia, but the pathway to the Iberian Peninsula was not thought to be a direct
136 M. Branco et al.
Fig. 5.11 Eucalyptus
globulus defoliation caused
by Gonipterus platensis
(Photo by Ana Raquel Reis)
Fig. 5.12 Eucalyptus
camaldulensis with galls of
Ophelimus maskellii (Photo
by Helena Santos)
5 Pests and Diseases in Portuguese Forestry: Current and New 137
one. North Africa and other Mediterranean neighbor regions, South Africa, and in
particular South America, due to its commercial wood exchange with Portugal, are
the most plausible routes for the introduction of the novel eucalypt pests in the
Iberian Peninsula.
Apart from a few polyphagous root feeding insects, namely cockchafer beetles
(Scarabaeidae), such as Melolontha papposa Illiger and Anoxia villosa Fabr.
(Ferreira et al. 1994), Eucalyptus in Portugal have not been affected by native
European insect pests. Two Mediterranean native termites, Reticulitermes lucifu-
gus Rossi and Kalotermes flavicolis Fabr. are frequently decomposers of the dead
wood with positive effects on stump decomposition (Cabral 1985). The large
phylogenetic distance of Eucalyptus from the Palearctic plant species might, to a
great extent, account for its resistance to native insect pests.
5.4.2 Diseases Caused by Fungi
For many years Eucalyptus forests in Portugal were regarded as almost free from
pathogens. Until recently, only Botryosphaeria spp. and Mycosphaerella spp. were
considered to be of importance (Branco et al. 2008). Nevertheless, some recent
studies have revealed that fungal diseases have a greater impact than was origi-
nally suspected.
Since the 1990s Mycosphaerella leaf disease (MLD) has been found causing
severe defoliation in young trees (Fig. 5.13). When Crous et al. (2007) showed that
Mycosphaerella is polyphyletic, they transferred many of the species associated
with MLD to Teratosphaeria. However, some species, even though phylogeneti-
cally they belong in Teratosphaeria, have not yet been formally transferred and
continue to be known by their name in Mycosphaerella.
The first report of Mycosphaerella on eucalypts outside of Australia was when
von Thümen described M. molleriana (T. molleriana) from Portugal (Crous and
Wingfield 1997). Since then a further eleven species have been recorded in Por-
tugal (Table 5.1). Of these, T. nubilosa is considered to be the most widespread
and the most aggressive (Silva et al. 2009,2012). Notably, T. cryptica has not yet
been recorded in Portugal, and this is considered to be one of the most aggressive
species. Normally these pathogens do not kill the trees, but they do affect the
normal growth of young plants resulting in reduced growth and lower tree volume,
thus having negative implications on the final output for the wood pulp industry.
Neofusicoccum spp. have been associated with cankers and die-back of Euca-
lyptus in tropical and temperate regions worldwide (Slippers et al. 2004; Iturritxa
et al. 2011; Rodas et al. 2009). Symptoms included dieback of shoots and branches
(Fig. 5.14), lesions and cankers on the stems (Fig. 5.15) usually with brown and
red exudates on stems and branches with copious exudation of kino. Botryosp-
haeria dothidea (Moug. Ex Fr.) Ces. & De Not. and Neofusicoccum ribis Grossenb
& Dugg. were previously thought to be common on Eucalyptus, but DNA
sequence comparisons have now shown that many of the early identifications were
138 M. Branco et al.
probably incorrect. Earlier reports of these fungi probably represent species such
as N. parvum and others (Slippers et al. 2004; Rodas et al. 2009). In Portugal
B. dothidea,N. eucalyptorum and N. parvum have been reported associated with
stands with severe diebacks and cankers. However, the extent and distribution of
the pathogens and disease are not known.
A recent nationwide monitoring program aimed at identifying pathogens in
commercial eucalypt forests with dieback and mortality revealed an extensive
range of pathogens in Eucalyptus globulus. These include Botryosphaeriaceae spp,
Phomopsis sp., Mycosphaerella and Teratosphaeria spp, B. mediterranea,
Cytospora spp., Pestalotiopsis spp., Phytophthora spp., Sporothrix spp., Phoma
sp., Harknessia sp., Cylindrocarpon sp. However, neither the contribution of these
fungi to the disease, nor their geographic distribution have been ascertained in
Fig. 5.13 Young plantation (left) severely defoliated by Mycosphaerella leaf disease, and close
up (right) of the leaf symptoms (Photos by Carlos Valente)
Table 5.1 Mycosphaerella
and Teratosphaeria species
associated with MLD in
Species Reference
Teratosphaeria molleriana von Thümen (1881)
T. africana Crous (1998)
Mycosphaerella. walkeri Crous (1998)
M. madeirae Crous et al. (2004)
M. communis Crous et al. (2006)
M. heimii Crous et al. (2006)
M. lateralis Crous et al. (2006)
M. marksii Crous et al. (2006)
T. nubilosa Crous et al. (2006)
T. parva Crous et al. (2006)
M. grandis Silva et al. (2009)
M. vespa Silva et al. (2009)
5 Pests and Diseases in Portuguese Forestry: Current and New 139
Fig. 5.14 Dieback of Eucalyptus globulus caused by a Neofusicoccum species (Photo by
E. Diogo and H. Bragança)
Fig. 5.15 Trunk canker
caused by a Neofusicoccum
species on Eucalyptus
globulus (Photo by E. Diogo
and H. Bragança)
140 M. Branco et al.
5.5 Chestnut
In the Portuguese mainland, the chestnut Castanea sativa (Mill.) occurs pre-
dominantly North of latitude 39, generally in zones between 400 and 1 000 m
above sea level with broader areas distributed in Trás-os-Montes e Alto Douro,
Beira Interior, and in Azores and Madeira Islands. Trás-os-Montes e Alto Douro is
the most important chestnut-growing region in Portugal with approximately 85 %
of the total area of chestnut in the country, followed by Beira Interior with ca. 9 %
in area and production (Ministério da Agricultura 2007). Provisional data from the
last forest inventory (ICNF 2013) provide an estimated total area of chestnut of
approximately 41,410 ha. The same inventory indicates an estimated area of
67,116 ha for deciduous oaks and 177,767 ha for other broadleaves.
5.5.1 Pests
Melolontha sp., affecting the roots of plants in nurseries, and the wood borers
Zeuzera pyrina L. and Xyleborus dispar F., on trunks of adult trees, have been
observed occasionally both on chestnut as well as on deciduous oaks. However,
the most important damage caused by insects on chestnut result from two fruit
feeders, the fruit moth Cydia splendana Hübner and the weevil C. elephas
Recently, major outbreaks causing up to 40 % yield loss, were assigned to
C. splendana in Madeira, Azores and Trás-os-Montes e Alto Douro (Bento et al.
2007; Faria et al. 2007).
Although not found in Portugal to date, the possible establishment of the Asian
chestnut gall wasp Dryocosmus kuriphilus Yasumatsu, responsible for the for-
mation of galls on new buds, is a concern for chestnut producers. The formation of
galls on new buds interrupts fruit formation and thus can reduce yield by up to
70 % (Grazioli and Santi 2008).
A study on the nematodes associated with chestnut revealed nine species of
phytoparasitic nematodes but no association with tree decline was found (Macara
Outbreaks of the beetle Altica quercetorum Fourd. (Coleoptera; Chysomelidae)
occasionally cause severe defoliation of up to 95 % on deciduous oaks, mainly
Q. robur,Q. faginea and Q. pyrenaica. Outbreaks occur at cyclical intervals, after
which beetle populations decline. Natural enemies and pathogens such as Beau-
veria bassiana (Mansilla and Mazoy 1993) may contribute to population decline
following the outbreaks.
5 Pests and Diseases in Portuguese Forestry: Current and New 141
5.5.2 Fungal Diseases
The reduction of the Portuguese chestnut area in the last 2 decades has been
attributed to socio-economic changes and the occurrence of two pathogenic
organisms namely Phytophthora spp., which cause ink disease, and the fungus
Cryphonectria parasitica (Murrill) Barr, which causes chestnut blight.
Cryphonectria parasitica is a wound pathogen that infects branches and stems.
The most common symptoms on European and American chestnuts are yellowing
and wilting of the foliage, dieback, trunk and branch cankers (Fig. 5.16) shoots
developing below the canker and the presence of the reproductive structures.
These structures (pycnidia and perithecia) are orange-brown stromata emerging
from branches or stem, with yellow tendrils of conidia extruding in wet weather.
The smooth bark of young branches becomes reddish and sunken while the fungus
proliferates in the cambium and in the bark tissue forming pale brown mycelial
fans (Heiniger and Rigling 1994).
In Portugal, C. parasitica was first reported by Câmara (1929). The initial
infection was probably successfully eradicated, because the disease was not seen
again until 1989 when two disease foci were found in the Northeast of the country
(Abreu 1992). After this finding the fungus spread rapidly and a recent nationwide
monitoring program established that chestnut blight has spread into most of the
chestnut growing areas of Portugal (Bragança et al. 2008).
References to the occurrence of ink disease caused by Phytophthora spp. in the
North of Portugal (Minho province) date from the 19th C (Abreu 1995; Martins
and Abreu 2007). Yet, only in 1942 the association of P. cinnamomi and
P. cambivora with diseased chestnut tissue was confirmed (Pimentel 1947).
Although P. cambivora has been isolated occasionally from chestnut tissues in the
past, P. cinnamomi is by far the most prevalent species in chestnut orchards and
nurseries in Northeastern Portugal (Martins et al. 1999; Fonseca et al. 2004). This
aggressive root pathogen is at present widely distributed throughout Portugal
where it occurs on other hosts including cork oaks.
Other diseases affecting chestnut trees include diffuse cankers caused by Mel-
anconis modonia Tul. & C. Tul. Since 1995, this pathogen has been recorded in
Portugal on senescent bark or chestnut weakened by biotic and abiotic factors,
causing significant losses (Abreu 1996; Abreu and Gomes 1989). Mycosphaerella
maculiformis (Pers.) Schröt was also reported by Abreu and Gomes (1989)
affecting adult chestnut trees in the northeast of Portugal.
5.6 Japanese Cedar
Cryptomeria japonica (LF) D. Don., commonly known as Japanese cedar, is an
exotic species in Portugal and the most important forestry species of Azores islands.
Like most situations observed in plantations with exotic tree species worldwide,
C. japonica in Azores has been mostly free from herbivores and pathogens.
142 M. Branco et al.
5.6.1 Pests and Diseases
The native fungus A. mellea causing root disease rot (Fig. 5.17) has been found in
Portugal for a long time threatening C. japonica with high incidence rates
(Bragança et al. 2004). Consequently, several studies aiming at improving the
knowledge on the pathogen distribution, incidence and host-pathogen interaction
have been done. A survey made in 2007 in S. Miguel Island revealed that the
disease is widespread but has a scattered distribution in C. japonica stands, being
detected on 57 % of the 65 sampled plots (Nóbrega et al. 2007).
From field observations and the results of inoculation tests Melo et al. (2004)
concluded that there are significant differences in susceptibility among C. japonica
varieties, mainly between the trees with rose heartwood (susceptible) and dark
brown (resistant) heartwood. On the strength of the ecological and economic
constraints to control Armillaria root rot in forestry stands, the most suitable
measures for efficient disease control appear to be the maintenance of nurseries
health status and the progressive replacement of the rose heartwood varieties with
the ones that have dark brown heartwood.
5.7 Measures to Control Existing Pests and Pathogens
Control measures undertaken in Portuguese forests, including chemical, biological,
genetic, cultural or legislative control, have diverged according to insect pest and
pathogens as well as forest tree species. Problems with native insect pests on
native tree species have been mostly occasional. These are frequently associated
with either cyclical population outbreaks, as characteristic of many forest defoli-
ators, or local disturbances such as fire or poor management strategies, predis-
posing trees to insect attacks. This is the case with bark and wood borers on pines
Fig. 5.16 Chestnut canker
caused by Cryphonectria
parasitica (Photo by Helena
5 Pests and Diseases in Portuguese Forestry: Current and New 143
for which control has been made mostly by silvicultural practices, such as sanitary
thinning and cleaning of debris, or forest management to enhance tree vigour.
Several natural enemies, namely parasitoids, predators (arthropods, birds and
mammals) and pathogens contribute to maintain the populations of native insects
at low levels in endemic situations (Ferreira and Ferreira 1991). In the case of
defoliator insect pests, such as T. pityocampa on pines, or L. dispar on cork oak,
the control of outbreaks has been sporadically done with Bacillus thuringiensis
(Bt), a bacterium producing a toxin, b-endotoxin, commonly used as a biological
pesticide (Cabral et al. 1965; Ferreira and Ferreira 1991). Alternatively, selective
insecticides acting as insect growth regulators (IGR), such as diflubenzuron have
been also used for these forest defoliator insect pests (Ferreira and Ferreira 1991).
From the economic assessment of managing processionary moth in pine forests in
Portugal it was demonstrated that control measures with Bt were not profitable for
private forest owners considering wood losses, yet the control compensates in the
form of social profit by minimizing public health risks with urticating larvae
(Gatto et al. 2009).
Bark beetles and P. cylindrus are occasionally monitored using commercial
lures based on pheromones and kairomones. Some initial studies on the chemical
ecology of C. undatus are starting with the aim of developing an environmentally
friendly approach to control this pest (Fürstenau et al. 2012).
Special concern and control measures have been developed for the control of
alien pest species affecting native or exotic trees, of which one example is the
PWN. The PWN is included in Directive no. 2000/29/EC of 8 May 2000 con-
cerning protective measures against the introduction and spread of harmful
Fig. 5.17 Armillaria sp. on
the trunk of Cryptomeria
japonica (Photo by Helena
144 M. Branco et al.
organisms to plants or plant products in the EU. It is also referenced by the
European and Mediterranean Plant Protection Organization (EPPO) as a quaran-
tine organism (EPPO A2 list), regarding their high destructive potential. In Por-
tugal at the onset of the PWN detection in 1999, the stands affected by the disease
were confined to the continental region of the Setúbal peninsula. Despite the
actions taken to prevent the spread of PWN, new outbreaks were detected in spring
2008. For this reason, the entire mainland was declared a Restriction Zone (RZ)
with a security zone of 20 km wide along the Spanish border in 2011. All trees
with symptoms were felled outside the flight period of the vector, the infected
material was destroyed and the insect vector is monitored since the first detection
of the PWN. In the earlier years mainly a mixture of a-pinene, ethanol and cis-
verbenol was used as lures. Research on the chemical ecology of the beetle
allowed for the identification of an aggregation pheromone, which is now used in
commercial lures (Pajares et al. 2010). The control of the nematode is on course,
but so far no commercial product is authorized.
The control of fungi and oomycetes is also variable according to the organisms.
For the control of D. corticola on cork oak some studies with fungicides have
shown minor positive results, some of them however, are not allowed under
European regulation (Luque et al. 2008). Regarding oomycetes, namely Phy-
tophthora spp., the pathogens can survive for long periods in the soil and there are
no treatments to eradicate them. However some products that induce defense
mechanisms in plants (phosphites, potassium phosphonate) are currently used by
the forest owners in attempts to control the disease in infested sites. Good site
conditions and adequate management practices are considered factors that can
mitigate the effects of the disease. The presence of hypovirulent Cryphonectria
parasitica was detected in Portugal (Bragança et al. 2007) and offers the potential
for biological control of the disease, either naturally or after canker treatments.
Whether hypovirulence can establish itself in Portugal, however, remains to be
seen. The low vegetative compatibility-type diversity currently observed in Por-
tugal will favour hypovirus invasion of the C. parasitica populations. In contrast,
frequent sexual reproduction could pose a major obstacle to this type of control
(Bragança et al. 2007). An integrated approach involving the release of hypovir-
ulent isolates together with sanitation measures to remove cankers or dead wood
with perithecia may be the best practice to control chestnut blight in Portugal for
the time being (Bragança et al. 2009b).
Classical biological control seems to be one of the best strategies for controlling
Eucalyptus pests, as one of the known reasons for the success of these novel pests
is its release from their natural enemies. Several natural enemies have been
introduced, either unintentionally or intentionally and these have helped to control
eucalyptus insect pests in Portugal. Particular examples are Anaphes nitens Hubber
(Mymaridae), an egg parasitoid of Gonipterus spp., (Reis et al. 2012); Avetianella
longoi Siscaro an encyrtid egg parasitoid of Phoracantha spp. (Farrall et al. 1992);
Closterocerus chameleon Girault, a parasitoid of the gall wasp O. maskelii (Branco
et al. 2009,2014); Psyllaephagus bliteus Riek and P. pilosus Noyes, two encyrtids
5 Pests and Diseases in Portuguese Forestry: Current and New 145
used for the control of C. eucalypti and G. brimblecombei, respectively (Valente
et al. 2004; Dhari et al. 2014). In most cases the success achieved with the
biological control has been high, favoured by the high dispersion rates and rapid
establishment of the parasitoids. For example, the percentages of parasitism for
C. chameleon are higher than 50 % and up to 100 % (Branco et al. 2009,2014).
However, in some other cases the rates of parasitism are less expressive and not
enough to solve the problem, as with A. longoi (Valente and Branco 2008) and
with A. nitens, which is unable to control G. platensis in the northern areas of the
country (Reis et al. 2012). For the two wood borers of the genus Phoracantha
forest management practices, such as site selection and sanitary felling, and mass
trapping with trap logs help to keep the populations at low densities. Furthermore,
predation by native birds might contribute to the mortality of the larvae (Valente
and Branco 2008). For the eucalyptus snout beetle G. platensis chemical control
with insecticides, flufenoxuron and tiaclopride, has been applied in the Centre and
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... However, the mean stand infestation index (IP) value was very low with an IP = 0.17 ± 0.09, thereby revealing low C. undatus population levels. This agrees with Branco et al. [38] who reported that the percentage of trees attacked by C. undatus in cork oak forests in Portugal varies between 0% and 50%. ...
... Overall, all of the identified lipophilic compounds have been previously reported in cork extractives with small differences in composition: lipophilic extracts of corks from Q. suber from Bulgaria and Turkey [38] showed the dominance of triterpenoids with betulinic acid and friedelan-3-one as the main components. The inner cork compared to the complete cork had a lower proportion of alkanoic acids (6.8% vs. 14.2% in reproduction cork) and a higher proportion of triterpenes (77% vs. 50% in reproduction cork) [23,25,26,28]. ...
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The beetle Coraebus undatus, during its larval stage feeds, and excavates galleries on the cork-generating layer of Quercus suber L. trees, seriously affecting the cork quality with significant economic losses for the cork industry. This work compared the composition of the extracts present in the innermost cork layers (the belly) of cork planks from Q. suber trees with low and moderate C. undatus attack in one stand. The total extractives in the inner cork layer from trees with moderate and low C. undatus attacks were similar (on average 22% of the cork mass) with a high proportion of polar compounds (91% of the total extractives). The chemical composition of the inner cork lipophilic extractives was the same in trees infested and free of larvae, with triterpenes as the most abundant family accounting for 77% of all the compounds, predominantly friedeline. The hydrophilic extractives differed on the levels of phenolic compounds, with higher levels in the inner cork extracts of samples from trees with low attack (90.0 mg GAE g−1 vs. 59.0 mg GAE g−1 of inner cork mass) The potential toxic activity of phenolic compounds may have a role in decreasing the larval feeding.
... and Phellinus torulosa, which cause root rot and wood decay. Since the 1990s, a complex of fungal species native to Australia, commonly known as Mycosphaerella, has been causing leaf necrosis and severe defoliation, especially in young plantations (Branco et al. 2014). Fungi such as Botryosphaeria spp. ...
... List of invasive pests affecting Eucalyptus spp. in Europe(Branco et al. 2014; Hurley et al. 2016) a Countries appear by order of first records Countries abbreviations: ES-Spain; FR-France; IE-Ireland; IT-Italy; PT-Portugal; UK-United Kingdom ...
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Although native to Australia, Eucalyptus species are found throughout Europe. At present, they are located mainly in the Iberian Peninsula and Eucalyptus globulus is the most commonly planted species. Climate forecasts anticipate an expansion of Eucalyptus to other regions of Europe. The fast growth of E. globulus, together with its resprouting ability and wood properties, has promoted the use of this species in the Iberian Peninsula. The total volume of E. globulus harvested there was close to 14 million m3 in 2019. Eucalyptus species represent the main source of raw material for the pulp and paper industries and provide an important source of income to non-industrial owners. Being exotic fast-growing trees, their expansion has also been associated with negative environmental impacts. The species therefore poses a series of challenges, while also generating opportunities. The objectives of this review paper are: (1) to summarize the importance of Eucalyptus plantations in Europe; (2) to analyse the opportunities and challenges of this genus in present and future plantations in Europe; (3) to assess to what extent forest management, at both stand and landscape levels, can reduce negative impacts; (4) to make policy and management recommendations that may support the use of this genus in other European regions. These aims are accomplished based on a thorough literature review, particularly focused on research developed in the Iberian Peninsula.
... Pine wilt disease (PWD) is a devastating disease of pine trees caused by Bursaphelenchus xylophilus (pine wood nematode; PWN) Nickel (Aphelenchida: Parasitaphelenchidae). The PWN is native to North America and is now found in the USA, Canada, Mexico, China, Korea, Japan, Portugal and Spain [1][2][3][4]. Since the introduction of PWN into China in 1982, despite the adoption of various measures to prevent its spread, the occurrence of PWD has exceeded expectations. PWD has occurred in 666 county-level administrative regions of 19 provinces (autonomous regions and municipalities directly under the Central Government), with a total area of 1,114,600 hm 2 and 19,467,400 dead pine trees in 2019, which has resulted in severe direct economic losses and losses of ecological service value equal to hundreds of billions of yuan [5]. ...
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Determining the mechanisms of pine wilt disease (PWD) resistance in Pinus is a popular research topic, but information on volatile organic substances (VOS) and their role in PWD is lacking. Whether the difference in VOS among Pinus thunbergii parl. that have different levels of resistance with pine wood nematodes (PWNs) is the reason for the differing resistance needs to be studied. In this study, resistant P. thunbergii introduced from Japan and susceptible P. thunbergii native to China were used to investigate the effects of different lines inoculated with PWN. We determined the expression levels of the terpene synthesis-related genes geranylgeranyl diphosphate synthase (GGPPS), 3-hydroxy-3-methylglutaryl-coenzyme A reductase 1 (HMDH1), two kinds of alpha-farnesene synthase (PT) genes. The types and the relative percentage content of terpenoids in the pine needles were also determined by gas chromatography coupled with mass spectrometry (GC-MS). Results show that the growth, population size and migration of PWNs were significantly inhibited. The expression of terpene synthesis genes in the resistant P. thunbergii was higher than that in the susceptible one. The analysis of terpenoids revealed a total of 41 terpenoids, of which resistant P. thunbergii contained 39 and susceptible P. thunbergii only 28; 14 terpenoids were specific to resistant P. thunbergii, in which 8 of the terpenoids were constitutive terpenes and 6 were inducible terpenes. There were 3 terpenes unique to the susceptible P. thunbergii, and only 1 inducible terpene. Our results showed that the reduction in the expression of disease symptom and suppression of PWNs in resistant P. thunbergii was likely related to differences in the types and content of resistance-related substances in the trees. This study does not specifically connect elevated compounds in resistant P. thunbergii to resistance to PWN and assays should be conducted to establish direct effects of terpenoids on pinewood nematode activity and reproduction.
... Pragas e Doenças Associadas aos Eucaliptos 163 de eucaliptos, nomeadamente treze insetos e um ácaro (Figura 1). às doenças, apesar de o seu impacto económico não estar ainda bem determinado em Portugal, o conhecimento dos patogénios já detetados em associação com o eucalipto em todo o território continental permite sugerir que as principais doenças de origem biótica são causadas por fungos, dos quais se destacam os da família Botryosphaeriaceae (Neofusicoccum, Botryosphaeria e Diplodia), os géneros Teratosphaeria e Mycosphaerella e a espécie Quambalaria eucalypti(BARRADAS et al., 2016;BATISTA et al., 2020;BRAGANÇA et al., 2015;BRANCO 2007;BRANCO et al., 2014;SILVA et al., 2015).Figura 1 -Curva cumulativa do número de espécies de artrópodes australianos, fitófagos, associados aos eucaliptos em Portugal, com base no ano da sua primeira deteção. Os nomes científicos dos artrópodes estão assinalados no gráfico, sendo Rhombacus eucalypti um ácaro e as restantes espécies insetos Embora as principais pragas e doenças dos eucaliptos sejam originárias da Austrália, alguns insetos e fungos que ocorrem naturalmente nas áreas onde os eucaliptos foram introduzidos constituem também problemas relevantes(WINGFIELD et al., 2008;ALFENAS et al., 2009). ...
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O eucalipto tornou-se uma das espécies incontornáveis da floresta portuguesa. Nos últimos anos, a ocorrência de grandes incêndios tem vindo a aumentar (onde os ocorridos em junho e outubro de 2017 foram particularmente significativos), acentuando a polémica em torno do efeito das plantações de eucalipto na propagação do fogo. Do protagonismo socioeconómico, aumento de área plantada e relação com o fogo resultam discussões apaixonadas, mas nem sempre fundamentadas no conhecimento existente. A informação disponível permite esclarecer dúvidas e recentrar o problema nos fatores que têm realmente influência nos regimes de fogo: as dinâmicas demográficas e de uso do solo que ocorreram no último século e a necessidade de encarar a floresta para além da árvore, como um sistema complexo. É a estrutura dos povoamentos, mais do que as espécies, que condiciona a propagação dos incêndios. Embora o problema dos incêndios, grandes e pequenos, seja territorial e não apenas do sector florestal, a solução passa pela gestão do uso do solo e do espaço rural, incluindo a floresta. Ao nível do ordenamento do território, a diversificação da paisagem e a redução da área florestal nalgumas zonas, quebrando a continuidade da vegetação, são algumas das soluções possíveis. À escala da árvore e da propriedade, a gestão florestal é a única ferramenta que permite conviver com o fogo e minimizar os danos causados pelos incêndios. É possível fazer melhor com os recursos disponíveis, adequando as opções de gestão às condições locais, numa perspectiva integrada à escala da paisagem, que considera as suas múltiplas dimensões: social, ambiental e económica. Este artigo faz parte do Caderno Técnico da Silva Lusitana sobre Eucalipto em Portugal. Tem como ponto de partida a obra "O Eucaliptal em Portugal. Impactes Ambientais e Investigação Científica" publicada em 2007 e procura dar visibilidade a algum do conhecimento científico desenvolvido nos últimos 10-15 anos sobre plantações de eucalipto e o fogo.
... Habitat 9330: Quercus suber forests, EEC, 1992) and were also highly protected and supported in Portugal, through financial afforestation initiatives (Mendes and Silva Dias, 2002). However, these forests are threatened due to different causes, such as inadequate understorey and tree management , pests and diseases (Branco et al., 2014, Tiberi et al., 2016 or severe droughts (Acácio et al., 2017). This has been reflected in an overall decline from 28.0 to 26.5% of the tree crown cover between 1996 and 2005 (Paulo et al., 2016) and of ca. ...
Shrub encroachment is a global phenomenon occurring in a wide range of ecosystems, including in tree plantations, which is known to affect ecosystem functioning and productivity. Forest management in tree plantations (e.g. shrub clearing, tree thinning and pruning) often aims to increase wood and non-woody products yield while optimizing other ecosystems services such as carbon sequestration. However, little is known on the effect of shrub clearing on tree growth and tree water status in juvenile tree stands. Under climate change scenarios that predict increased frequency of extreme events such as droughts, management during the early stages of stand plantations may be crucial for its sustainability. This study aimed to explore the combined effect of shrub understorey removal and drought in two cork oak (Quercus suber L.) juvenile plantations, with similar stand age but distinct soil types and forest management, on tree water status, assessed through leaf water potential measurement, and on tree growth. The study was conducted during two consecutive years, including a drought year. Results revealed that the shrub understorey removal positively affected the physiological response of trees in both plantations but only affected tree growth (i.e. total height and leaf area) in the plantation with a higher tree density and shrub biomass. Shrub biomass and species composition most probably had a determinant effect on tree growth due to soil water competition. Our results emphasize the need for site-specific forest management during the early stages of cork oak plantation for maintaining its future sustainability and provision of ecosystem services.
... Climate conditions, such as more frequent and abundant rainfall with increasing temperatures and higher concentrations of water vapor, will lead to favorable conditions for the development of infectious diseases and the germination of spores, as well as the activity and spread of the zoospores and their reproduction [123][124][125][126][127][128][129][130][131][132][133][134]. Moreover, increased winter rainfall may stimulate diseases [135]. ...
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Pesticides are indispensable in agricultural production. They have been used by farmers to control weeds and insects, and their remarkable increases in agricultural products have been reported. The increase in the world’s population in the 20th century could not have been possible without a parallel increase in food production. About one-third of agricultural products are produced depending on the application of pesticides. Without the use of pesticides, there would be a 78% loss of fruit production, a 54% loss of vegetable production, and a 32% loss of cereal production. Therefore, pesticides play a critical role in reducing diseases and increasing crop yields worldwide. Thus, it is essential to discuss the agricultural development process; the historical perspective, types and specific uses of pesticides; and pesticide behavior, its contamination, and adverse effects on the natural environment. The review study indicates that agricultural development has a long history in many places around the world. The history of pesticide use can be divided into three periods of time. Pesticides are classified by different classification terms such as chemical classes, functional groups, modes of action, and toxicity. Pesticides are used to kill pests and control weeds using chemical ingredients; hence, they can also be toxic to other organisms, including birds, fish, beneficial insects, and non-target plants, as well as air, water, soil, and crops. Moreover, pesticide contamination moves away from the target plants, resulting in environmental pollution. Such chemical residues impact human health through environmental and food contamination. In addition, climate change-related factors also impact on pesticide application and result in increased pesticide usage and pesticide pollution. Therefore, this review will provide the scientific information necessary for pesticide application and management in the future.
... related to Phytophthora pathogens(Sánchez et al., 2002;Gómez- Aparicio et al., 2012;Branco et al., 2014) might compromise the survival of oak seedlings (Domínguez-Begines et al., 2020). Further research is necessary about fungal and insect damage as stress agent on seedlings, especially, the joint response with drought, which may affect water-stressed hosts (Jactel et al., 2012).F I G U R E 4 Predicted probability of (a) chlorophyll content, (b) flavonoid content, (c) anthocyanin content, and (d) nitrogen balance index (NBI) for different species (Q. ...
Question Worldwide, mixed oak woodlands regenerate poorly due to different anthropogenic impacts. Our question is whether spatial distribution (regeneration microsite) of oak recruits is determined by different biotic and abiotic stress agents and whether recruits of co‐occurring oak species may respond differently to each source of stress. Location Mediterranean California mixed oak woodlands. Methods We recorded the main regeneration microsites of four co‐occurring oak species (Quercus lobata, Q. douglasii, Q. kelloggii and Q. agrifolia) in 25 belt transects in a nature reserve and identified the main stress agent for each species and microsite. We also analyzed their response to stress through physiological parameters (chlorophyll, flavonol, anthocyanin and nitrogen). Results Q. agrifolia and Q. lobata seedlings mostly established under shrubs and trees, respectively. The other species did not have a prime regeneration microsite. Biotic stress occurred more frequently than abiotic (drought) stress for all species. Regarding biotic sources of stress, the deciduous Q. lobata, Q. douglasii and Q. kellogii showed high browsing damage; insect damage was light and occurred mostly in the evergreen Q. agrifolia whereas fungal damage was significantly lower in Q. douglasii. Physiologically, all oak species responded similarly to stress agents although Q. douglasii and Q. kelloggii showed higher chlorophyll content than Q. agrifolia and Q. lobata, which might be related to differences in resilience. Conclusions Deciduous oaks are particularly vulnerable to overgrazing whereas the evergreen Q. agrifolia seems more affected by fungal and insect damage. Management aimed at the co‐existence of deciduous and evergreen oaks should consider the enhancement of microsites that best ameliorate the impact of predicted stress agents but also the oak physiological responses (i.e. resilience) to each stress agent. We suggest keeping low ungulate densities and carefully consider the species selection in assisted regeneration projects depending on the predominant stress agent and microsite.
... It seems that, in the Balkan Peninsula, these species may be important [4,23,45]. In the Mediterranean area, their importance as pests decreases due to small numbers [16,24,30,[46][47][48]. ...