Content uploaded by Massimo Faccoli
Author content
All content in this area was uploaded by Massimo Faccoli on Dec 08, 2014
Content may be subject to copyright.
Better today but worse tomorrow: how warm summers affect
breeding performance of a Scots pine pest
F. CHINELLATO1,*, A. BATTISTI1, V. FINOZZI2, M. FACCOLI1
1 Department of Agronomy, Food, Natural Resources, Animals and Environment, University of Padova,
Padova, Italy
2 Regional Forest Service, Belluno, Italy
Keywords: bark beetle, global warming, Ips acuminatus, Pinus sylvestris, popu-
lation dynamic.
S. – Recent climate change are known to affect many insect populations,
including bark beetles. In this paper we explore how warmer temperature may affect
the performance of southern European populations of the pine bark beetle Ips acumina-
tus. During a seven-year-long study (2007-2013) we analysed: (a) insect voltinism and
phenology, (b) annual trend of the mean population density, and (c) their correlations
with temperature. The mean number of adults per trap captured during the flying season
(May-August) showed a bivoltine phenological pattern with two flight periods, in May
after hibernation and in July, when a second generation begin. The breeding performance
of the first generation was positively correlated with temperature In the warmer years,
the amount of summer captures resulted higher than the spring ones, suggesting a posi-
tive breeding performance of the first generation and the beginning of a large second
generation. The population density was instead negatively correlated with temperature,
and insect populations decreased following warmer years with a negative effect on the
population trend. Results from this study suggest that warm spring-summer temperature
can produce a within-year increase of breeding performance and voltinism of I. acumi-
natus, with a higher reproductive success of the first generation and the beginning of
a large second one. In these cases there is, however, a between-years reduction of the
population density probably due to a high winter mortality of the overwintering imma-
ture instars coming from an incomplete second generation.
I. – Recent climate changes are known to affect many
insect populations, including bark beetles (Coleoptera: Curculionidae,
Scolytinae) (D et al., 2005, 2007; B et al., 2006; B
et al., 2006; L et al., 2006; J et al., 2007; R et al.,
2008; F, 2009). In the last decades, high summer temperature
associated with long periods of drought promoted a progressive for-
est decline especially in southern Europe and circum-Mediterranean
countries. Besides the direct effect on trees, warmer climatic conditions
may reduce insect developmental time (W and S,
Agrochimica, Vol. LVIII – Special Issue (2014) 133-145
* Corresponding author: chinellato.f@gmail.com
F. CHINELLATO ET AL.
134
1998), increase voltinism (C et al., 2012), and affect the dia-
pause mechanisms (G, 1985; B et al., 2007), resulting in an
increase of the infestation pressure on the host trees.
For many decades I. acuminatus (Gyllenhal), a polygamous bark
beetle attacking the upper part of stem and branches of Scots pine (Pinus
sylvestris L.) (C, 1962; B, 1968), has been considered
of minor importance (B, 1968), causing only sporadic damage
following infestations of other pine pests primary agents of tree mortal-
ity (C, 1962). Nevertheless, in recent years many outbreaks
have been reported in a number of Scots pine forests of central Europe
(M, 1995; S and W, 1997) and south-western
Alps (F and Z, 2001; Wermelinger et al., 2008). Large
infestations recently affected also the eastern part of the Italian Alps
(Dolomites, NE Italy) causing considerable economic (F et al.,
2011) and ecological damage (C et al., 2012, 2013). Besides
the reduction in timber quality of the infested trees, there are other
important non-timber concerns, such as soil protection, biodiversity
conservation and landscape quality of the Dolomite valleys (C
et al., 2008, 2012).
Although I. acuminatus has recently been listed among the most
damaging of European scolytids (G and E, 2004), pre-
cise information concerning biology, population dynamics and their
variations according with climate and climatic change are still largely
unknown (C et al., 2012). Along the southern Alps, where
this pest has recently caused extensive damage (W et al.,
2008; C et al., 2012, 2013), both I. acuminatus and Scots
pine occur at the southern edge of their natural distribution range and
in climatic conditions very different from those occurring in central and
northern Europe. As temperature is the primary driver of insect devel-
opment, climate change may modify flight behaviour, developmental
rate and voltinism of these population. Increases in temperature could
permit more rapid rates of development, with a possible increasing
of the number of generations per year or a higher breeding perform-
ance. In this respect the recent outbreaks of I. acuminatus recorded in
southern Europe are apparently indirectly correlated to pine decline
caused by high summer temperatures and drought, which have strongly
contributed to Scots pine mortality observed in the Alps in the last
decades (W et al., 2008). Unfortunately, no studies have
investigated how weather conditions and their variations may directly
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
135
affect the reproductive performance of I. acuminatus and the dynamics
of its populations.
In this paper we explore the possible relationships between climate
change and breeding performance of I. acuminatus populations infesting
Scots pine forests in an outbreak area of the north-eastern Italian Alps.
We hypothesize that warmer climatic conditions may positively affect
the reproduction of the southern European populations of I. acuminatus,
increasing the breeding performance of the first generation and allowing
the development of a second generation. With the aim of contributing
to a better understanding of the mechanisms driving the population
dynamic of a forest pest exposed to climate change, during a seven-year
long study (2007-2013) we analysed: (a) insect voltinism and phenol-
ogy, (b) annual trend of th population density, and (c) their correlations
with temperature and its variations in order to find a close relationships
between climate and insect breeding performance.
M M. – Study site. – The Scots pine forest we
used for our study extends over three municipalities of the Cadore Valley
(Borca, San Vito and Cortina) (46°40’N; 12°20’E), Province of Belluno,
North-Eastern Italian Alps. The forest (about 22.3 km2 in area) grows on
S-SW facing slopes, 1,000-1,600 m a.s.l. The stands are older than 100
years, with a mean density of about 300 trees per hectare, and show poor
growth because of limitation of nutrients and water (C et al.,
2012; 2013; F et al., 2012). The forest has natural regeneration and
no silvicultural management for timber production, although small phytos-
anitary clearcuts have been occasionally carried out to preserve the general
health of the forest, which is very important for soil protection against
erosion and avalanches (C et al., 2012; 2013; F et al.,
2012). Because of the increasing bark beetle infestations recorded in the
last decade, since 2007 the Regional Forest Service has applied a specific
sanitation felling programme in autumn of each year by cutting and remov-
ing all I. acuminatus infested trees from the valley (F et al., 2011).
Phenology and voltinism of the model species. – As reported by
C et al. (2012), in the study area I. acuminatus usually has two
distinct attack periods (i.e., generations). The first attack is conducted
in spring by adults of the parent generation (hereafter referred to as
“spring adults”) that in middle-end May emerge from the overwinter-
ing sites. They colonize suitable trees and in summer, approximately 8
F. CHINELLATO ET AL.
136
weeks later, the beetles of the offspring generation (hereafter referred
to as “summer adults”) emerge from the infested trees looking for new
suitable hosts where a second generation will develop in the latest part of
the summer. The two groups of insects (“spring” and “summer” adults)
are usually well separated along the seasons, indicating the end of one
generation and the beginning of the following (Figs. 1 and 2). In case
of short and cold spring or summers, at the end of the first generation
the “summer adults” stay under the bark and do not reproduce before
hibernation (i.e., following spring).
Population monitoring by pheromone-baited traps. – Between
2007 and 2013 the population of I. acuminatus occurring in the inves-
tigated forest was monitored by pheromone-baited traps (F et
al., 2012). In early spring, dry black 7-funnel traps (Witasek®) were set
up in recent clearcuts (less than 1 year old) located no closer than 30
m each other. The total number of traps set up annually slightly varied
among years. Traps were baited with species-specific pheromone lures
composed of Ipsenol, Ipdienol and (S)-(+)-cis-verbenol, supplied by the
Spanish chemical company SEDQ®-Sociedad Española de Desarrollos
Quìmìcos. Every year, traps were checked twice per month from May to
end of August. All pheromone dispensers were replaced once, in June,
Fig. 1. – Seasonal variation of Ips scuminatus adults (mean adults per trap) during the flight period in 2008
(May-August). The line above the curve shows the separation between spring (GSp) and summer genera-
tions (GSu).
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
137
two months from the beginning of the trial. All caught insects were
identified at species level and counted. Population monitoring was per-
formed by a team of foresters working for the Regional Forest Service,
in collaboration with entomologists of the University of Padova.
Weather monitoring. – Climatic data consisting of air temperature
and precipitations were collected daily from 1996 to 2013 from a weath-
er station installed within a field laboratory of the Padova University
in an experimental sites within the study area (San Vito di Cadore,
BL, 46°27’11’’ N, 12°12’47” E, 1,107 m a.s.l.). Air temperature was
recorded every 15 min. Elevation and slope facing of the weather station
were similar to those of the pheromone traps.
Data analyses. – The mean of the maximum daily temperatures
recorded from May to August, the months of I. acuminatus breeding,
was calculated for each of the last 18 years (1996-2013). The deviance
of the mean temperature of each year (∆Tx) was then calculated on the
mean temperature of the whole investigated period.
According to F and S (2006), the breeding perform-
ance of the first generation of I. acuminatus was assessed as percentage
variation (∆Gx) of summer (GSux) and spring (GSpx) adult captures, and
calculated year by year as follows:
Fig. 2. – Seasonal variation of Ips scuminatus adults (mean adults per trap) during the flight period in 2012
(May-August). The line above the curve shows the separation between spring (GSp) and summer genera-
tions (GSu).
F. CHINELLATO ET AL.
138
∆Gx = [(GSux - GSpx)/GSpx] * 100
Similarly, the annual variation (∆Y) of I. acuminatus population
passing from one year (Yx) to the following one (Y(x+1)) was calculated
as follow:
∆Yx = [(Y(x+1) - Yx)/Yx] * 100
To describe the possible relationship between air temperature and
population trend, the ∆Yx recorded year by year over a 7-year period
(2007-2013) was correlated to ∆Tx using a multiple regression. An R2
value, adjusted for the number of parameters (Z, 1999), was used
to assess the goodness-of-fit of all possible models. As some of the
analysed time-series showed autocorrelation among the available data,
the correlation was corrected by the autocorrelation function (ACF) of
Statistica per Windows (L et al., 2002). Significance of effects was
based on α = 0.05, and statistic analysis was performed in Statistica 3.1
for Windows (Statistica, Tulsa, OK).
R. – Species voltinism and population trend. – The mean
number of adults per trap captured during the flying season (May-
August) showed a bivoltine phenological pattern with two flight periods,
the first (GSp) composed by parent adults emerging in May after hiber-
nation, and the second (GSu) composed by offspring of the first genera-
tion emerging in July and beginning the second generation. This pattern
was observed in all the monitored years excepted for 2010, when only
parent beetles were trapped. On one hand, in the bivoltine years 2007-
2009 and 2011 the amount of spring captures (GSp) resulted higher
than the summer ones (GSu), with a negative breeding performance of
the first generation (∆Gx) respectively of -71.8, -78.9, -86.4 and -55.0%
(Fig. 3a). In 2012 and 2013 such ratio (∆G2012 and ∆G2013) was instead
reversed, with GSu much higher than GSp, and a positive performance
of the first generation (89.3 and 72.7% respectively), i.e. offspring adults
more than parent adults (Fig. 3a). For 2010, having a single generation,
we considered ∆G2010 equal to -100% (Fig. 3a). On the other hand, the
variation in performance between consecutive years (∆Yx) shows an
opposite pattern, with positive values in 2008-2010 and 2011 (87.6,
12.5, 63.6 and 23.3%, respectively), and negative only in 2012 and 2013
(-41.9 and -82.9% respectively) (Fig. 3b).
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
139
Temperature variation. – On average, the last 10 years have been
the warmest of the last 18, with a general trend indicating a progressive
increase of the mean temperatures (Fig. 4). The years 2003, 2005, 2012
and 2013 have been the warmest of the study period. All the years in
which the I. acuminatus population was monitored (2007-2013) showed
a mean of the May-August daily maximum temperature higher than the
mean of the last 18 years (1996-2013) with the exception for the cool
Fig. 3. – a) Summer captures compared with spring captures of the same year (∆G), and b) total captures of
one year compared with those of the previous one (∆Y). ND, no data available.
F. CHINELLATO ET AL.
140
2008 (-0.95°C) and for 2010 on the mean (-0.002°C); 2012 and 2013
have been the warmest year with a positive deviation of +1.03 and
+1.04°C, respectively (Fig. 4).
Correlation performance vs. temperature. – The breeding perform-
ance of the first generation (∆Gx) was positively correlated with tem-
perature deviation (∆Tx) from the mean (R2 = 0.967; F = 43.3795; p =
0.0061) (Fig. 5). Performance of the first generation greatly increase
in warmer summers (Fig. 5). The population trend between two con-
secutive years (∆Yx) was instead negatively correlated with temperature
deviation (∆Tx) from the mean (R2 = 0.84; F = 21.76; p = 0.00956), and
insect populations decreased after warmer years (Fig. 6).
D. – Weather conditions can affect population growth,
distribution and voltinism of many forest insect species. In particular,
warm temperatures affect the distribution range and performance of
the pine processionary moth Thaumetopoea pityocampa (Lepidoptera:
Thaumetopoeidae) in southern Europe (B et al., 2005), winter
moth Operophtera brumata (Lepidoptera: Geometridae) in northern
Europe (H et al., 2007) and many species of bark beetles as the
mountain pine beetle Dendroctonus ponderosae in British Columbia
Fig. 4. – Deviation of May-August daily maximum temperatures from the mean calculated for the same
period in the last 18 years (1996-2013).
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
141
(L et al., 2003; C et al., 2004; K et al., 2008). Warm
temperatures can furthermore affect fauna composition, favouring more
aggressive against less aggressive species (C et al., 2013).
The main results from our study support these hypotheses also for I.
acuminatus. In the investigated area, spring-summer temperature of
the last years was generally warmer than in the past. This phenomenon
affected positively the breeding performance of I. acuminatus within the
same year, allowing the high reproduction of the first generation and the
beginning of the second, but negatively the population trend between
consecutive years, with a general decreasing of the population density
following particularly warm years.
Breeding performance of the first generation of I. acuminatus was
as much higher as the maximum temperature of the season was 0.5-
1°C warmer than the mean of the last 18 years. Warmer temperatures
provide optimal environmental conditions for larval development
resulting in a very high number of new adults quickly emerging in
early summer with the possibility, i.e. time, to begin a second gen-
eration in the same year. I. acuminatus has a large distribution area,
from southern Alps to Northern Europe (P, 1995). Because of
the short and cool summers of central and northern Europe, in most
Fig. 5. – Relationship between deviation of the May-August daily maximum temperatures from the mean
calculated for the same period in the last 18 years (1996-2013) (∆Tx), and variation between summer and
spring captures of the same year (∆Gx).
F. CHINELLATO ET AL.
142
European countries I. acuminatus is an univoltine species, produc-
ing only one generation per year and overwintering as adults in the
bark of the infested Scots pines (B, 1968). Spring and summer
temperature is thus a crucial factor in order to fully complete the
first generation. Adults generally emerge in spring with a mean air
temperature of about 18°C (B, 1968), although Alpine popula-
tions seem to be able to fly with lower temperature (C et
al., 2012). In this respect, an early spring emergence associated to
warmer temperature makes the breeding season longer, giving more
time to begin also a second generation. In addition, warmer spring
and summer reduce the mean developing time, passing from 8-9 to
6-7 weeks per generation (C et al., 2012), increasing voltin-
ism and reducing larval exposition to natural enemies, with a general
improvement of the breeding performance. Lastly, high temperatures
and associated droughts deeply stress host trees increasing the attack-
ing rate of I. acuminatus (W et al., 2008) and the number
of adults reproducing before winter (C et al., 2012). Effect
of high temperatures on bark beetle voltinism was studied in the same
area also for the most aggressive species in Europe, I. typographus
Fig. 6. – Relationship between deviation of the May-August daily maximum temperatures from the mean
calculated for the same period in the last 18 years (1996-2012) (∆Tx), and variation (∆Yx) between total
captures of one year (Y(x+1)) and the previous one (Yx). (F = 21.76; p < 0.01).
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
143
(F and S, 2006; F, 2009). These studies shows
that the beginning of the second generation is directly relate to the
weather conditions occurring at the beginning of the season.
The population trend between consecutive years shows instead an
opposite response to temperature, with warmer spring and summer
affecting negatively the population density of the following year. As
previously reported, long and warm summers allow the complete devel-
opment of the first generation and elicit the beginning of the second
one. Time is however not enough for the full development also of the
second generation, which faces the winter usually as larvae or callow
adults in the phloem (C et al., 2012). While I. acuminatus
adults may survive winter temperature lower than -25°C in the bark of
the infested trees (B, 1968), younger instars are unsuitable to sur-
vive the long and cold alpine winter, resulting in a large insect mortality
and a population decrease in the following year. A similar mechanism
was described also in other bark beetle species living in the same
region, where bivoltine populations of I. typographus suffer a winter
mortality of about 50%, which becomes close to 100% considering only
larval instars (F, 2002).
Although weather conditions play a key role for insect development
and breeding performance of bark beetles, there are many other envi-
ronmental variables involved, and spring-summer temperature alone is
clearly not sufficient to propose a reliable model of population dynamic.
Beside temperature, also humidity and precipitation, quantity and qual-
ity of the host-trees, amount of natural enemies may affect directly or
indirectly beetle performance and reproduction. Spring and summer
temperature can be however considered among the most crucial factors
affecting I. acuminatus phenology and voltinism, and definitely popu-
lation dynamic (C et al., 2012). Warm summer temperature
can increase flight activity of the first generation offspring eliciting the
beginning of a second generation, but negatively affects the population
growth in the following year, especially if associated with a cold winter.
Warmer climatic conditions, hence, have only a quick short-time posi-
tive effect on the breeding performance of I. acuminatus, but they do not
improve the general population trend in a middle-long temporal scale.
In conclusion, data presented in this study suggest that warm spring-
summer temperature can produce a within-year increase of breeding
performance and voltinism of I. acuminatus, but a between-years reduc-
tion of the population density probably due to a high winter mortality of
F. CHINELLATO ET AL.
144
the overwintering immature instars coming from an incomplete second
generation. Further studies focused on this topic but carried out on larger
datasets, also concerning other species, could be very helpful to better
understand the effect of temperature on bark beetle populations, and
their impact on forest ecosystems.
A. – We thank the foresters of the Regional
Forest Service of the Belluno district for assistance in field work. We
also sincerely thank T. Anfodillo, F. Fontanella and R. Menardi of
the Centre of Studies of Alpine Environment “Lucio Susmel” of the
University of Padova in San Vito di Cadore for providing meteorologi-
cal data and helping in field data collection. Special thanks to A. Garside
for linguistic proofreading. The research was partially supported by the
Italian national project “2010 - CPDA104007: Study of the response
mechanisms to climatic change in model forest insects”.
REFERENCES
B A.: Ecological studies on bark beetles (Coleoptera: Scolytidae) associated with Scots pine (Pinus sylvestris
L.) in Norway with particular reference to the influence of temperature. Medd. Nor. Skogfor. 83, 441-602
(1968).
B A., S M., S A., R A., R C. and L A.: Expansion of geographical
range in the pine processionary moth caused by increased winter temperature. Ecol. Appl. 15, 2084-2094
(2005).
C A., T S.W., R J. and S L.: Effects of climate change on range expansion by the
mountain pine beetle in British Columbia. In: Mountain Pine Beetle Symposium: Challenges and Solutions
(Shore T.L., Rooks J.E. and Stone J.E., eds.). Natural Resources Canada, Canadian Forest Services, Pacific
Forest Centre, Victoria, Canada, pp. 223-232 (2004).
C C.: A biological study of the scolytids of coniferous trees. Encyclopedie Entomologique, Lechevalier,
Paris (1962).
C F., F M., M L. and B A.: Distribution of Norway spruce bark and wood-boring
beetles along Alpine elevational gradients. Agr. For. Entomol. 16, 111-118 (2014)
C F., F M. and B A.: Outbreak dynamics and natural enemies of the pine bark beetle Ips
acuminatus. Proceedings of the ICE 2008, XXIII International Congress of Entomology (Durban, South
Africa, 6-12 July 2008) (2008).
C F., B A., S L.M. and F M.: Life history traits promoting outbreaks of the
pine bark beetle Ips acuminatus (Coleoptera: Curculionidae, Scolytinae) in the south-eastern Alps. Eur. J.
For. Res. 131, 553-561 (2012).
C F., S M.L., B A. and F M.: Spatio-temporal dynamics of an Ips acuminatus
outbreak and implications for management. Agr. For. Entomol. 15, 23-42 (2013).
F M.: Winter mortality in sub-corticolous populations of Ips typographus (Coleoptera Scolytidae) and its
parasitoids in the South-eastern Alps. J. Pest Sci. 75, 62-68 (2002).
F M. and S F.: A practical method for predicting the short-time trend of bivoltine populations of
Ips typographus (L.) (Col., Scolytidae). J. Appl. Entomol. 130, 61-66 (2006).
F M.: Effect of weather on Ips typographus (Coleoptera: Curculionidae) phenology, voltinism and associ-
ated spruce mortality in the southeastern Alps. Environ. Entomol. 38, 307-316 (2009).
F M., F V. and G P.: Sanitation felling and helicopter harvesting of bark beetle infested trees
in alpine forests: an assessment of the economic costs. For. Prod. J. 61, 675-680 (2011).
F M., F V. and C F.: Effectiveness of different trapping protocols for outbreak manage-
ment of the engraver pine beetle Ips acuminatus (Curculionidae, Scolytinae). Int. J. Pest Man. 58, 267-273
(2012).
EFFECT OF WARM SUMMERS ON A SCOTS PINE PEST
145
F B. and Z R.: Ips acuminatus: experiences from an outbreak in Southern Switzerland. J. For. Sci.
47, 80 (2001).
G J.-C. and E H.F.: Damage and control of BAWBILT organism. In: Bark and Wood Boring Insects
in Living Trees in Europe, a Synthesis (Lieutier F., Day K.R., Battisti A., Grégoire J.-C. and Evans H.F.,
eds.). Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 135-180 (2004).
H S.B., J J.U., I R.A. and Y N.G.: Shifting altitudinal distribution of outbreak zones of winter
moth Operophtera brumata in sub-arctic birch forest: a response to recent climate warming? Ecography
30, 299-307 (2007).
K W.A., D C.C., S G., R G.J., N E.T., C A.L. et al.: Mountain pine
beetle and forest carbon feedback to climate change. Nature 452, 987-990 (2008).
L J.A., R J. and P J.A.: Assessing the impacts of global warming on forest pest dynamics.
Front. Ecol. Environ. 1, 130-137 (2003).
M Z.: Possibilities of control and protection against Ips acuminatus in the region of forest enterprise
Znojmo. Zpravy Lesnickeho Vyzkumu 40, 22-26 (1995).
P A.: Zentral- und westpaläarktische Borken- und Kernkäfer (Coleoptera: Scolytidae, Platypodidae). Pro
Entomologia. Naturhistorisches Museum Basel (1995).
S M. and W C.J.: Development and use of pheromone dispenser in forest protection against Ips
acuminatus. Zpravy Lesnickeho Vyzkumu 42, 23-25 (1997).
W B., R A., S M D. and D M.: Assessing the role of bark- and wood-
boring insects in the decline of Scots pine (Pinus sylvestris) in the Swiss Rhone valley. Ecol. Entomol. 33,
239-249 (2008).
Z J.H.: BiostatisticalAanalysis. Prentice Hall Press, Upper Saddle River, USA (1999).
