Arthropod Fauna Associated to Soybean in Croatia

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Chapter 5
Arthropod Fauna Associated to Soybean in Croatia
Renata Bažok, Maja Čačija, Ana Gajger and
Tomislav Kos
Additional information is available at the end of the chapter
http://dx.doi.org/10.5772/54521
1. Introduction
The importance of soybean (Glycine max (L.) Merr.), as today’s world leading oil and protein
crop, is increasing in Croatia. As a plant species, soybean was registered for the first time in
Croatia in 1876. Soybean is relatively new field crop for Croatia. It was grown for the first
time in 1910 but, starting with 1970s it became important field crop [1]. In 1981, soybean was
cultivated on an area of 3.381 ha. Since that time the area cultivated by soybean has in‐
creased considerably, and productivity has also risen steadily. Figure 1 presents the trends
in soybean production in Croatia in the period 1993-2010 [2].
0
50,000
100,000
150,000
200,000
250,000
1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004* 2005 2006 2007 2008 2009 2010
harvested area-ha; total production t
Area harvested (ha) Total production (t)
*only agricultural enterprises without small farms are included
year
Figure 1. Harvested area and total production of soybean in Croatia, 1993-2010
© 2013 Bažok et al.; licensee InTech. This is an open access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.

Today’s the area on which soybean is cultivated in Croatia varies, depending on the year, from
30.000 to 50.000 ha. Croatian government statistics [2] show gains in average yielding ability,
from 2.160 to 3.000 kg/ha, between 1993 and 2010. Comparing to data from USA [3] on the aver‐
age yield between 2.197 and 2.896 kg/ha, soybean yields obtained in “regular” years in Croatia
are satisfactory. The exceptions in registered yield quantity were observed in extremely dry
and warm years 2000, 2003 and 2007 in which yield was between 1.380 and 1.900 kg/ha. There‐
fore, the main problem of soybean yielding stability is related to vulnerability of soybean pro‐
duction in extreme climatic conditions in which pest outbreaks influence yields negatively.
Global climate changes are often discussed by numerous scientists. Besides the increase of
global mean temperature [4], the incidence of the years in which extreme conditions are
present vs. “regular” years is increasing. This is proved by the fact that in the period from 2000
to 2009, three years with extremely dry and warm conditions were observed. Consequently, to
mitigate the negative consequences of pest outbreaks and improve profits soybean growers, in
these extreme years, attempt to control the pests which can reduce crop productivity.
Comparing to weeds and diseases, in “regular years” pests are of somewhat less importance
for soybean production in Croatia. In different agro-ecosystems, the arthropod fauna of soy‐
bean contains a great number of damaging species [5-8]. Soybean pests have not been inves‐
tigated completely in Croatia. It was reported [8] that in the region where Croatia belongs,
soybean crops are attacked by over 180 pests (150 insects and 30 species from other animal
classes) among which approximately 25 pest species are the most important.
Some investigations or observations on arthropod fauna of soybean were conducted in the
past on the territory of Croatia [9 - 13], and in neighboring countries [14 - 24]. Additionally,
some of the species were registered recently as the pests which could cause significant yield
damage on soybean [25 - 29].
The most comprehensive overview of the potential arthropod pests’ fauna of soybean in
Croatia is given by Maceljski [9]. This overview is a result of the literature review and au‐
thor’s long time work experience in entomology. On the other hand, investigations carried
out by other scientists in Croatia [10 - 13] and neighboring countries [6-8, 14-24] reported on
the presence or harmfulness of some additional species. In the Table 1 arthropod species
that are reported as soybean pests both, in Croatia and in neighboring countries are listed.
Besides arthropod species, nematodes are established as potential pests on soybeans in Cro‐
atia [11, 12] and in neighboring countries [19]. Jelić [12] established 43 species of phytopara‐
sitic nematodes on 18 localities distributed in east Croatia (region of Slavonia). Identified
species belonged to the genera Ditylenchus Filipjev, Meloidogyne Goeldi, Paratylenchus Mico‐
letzky, Pratylenchus Filipjev, Rotylenchus Filipjev, and Tylenchorhynchus Cobb. However sig‐
nificant damages caused by nematodes haven’t been recorded jet. Besides mentioned pests,
some authors [8, 30] reported that significant damage on soybean crops in Serbia could be
caused by other animal species as are Cricetus cricetus L., Microtus arvalis Pallas and Lepus
europaeus Pallas as well.
In regular farming practice in Croatia soybean seed is not treated with insecticides. Among
the arthorpod pests, mites (Tetranychus urticae Koch and Tetranychus atlanticus = T. turkestani
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Ugarov & Nikolskii) could be controlled by the use of acaricides if their populations reach
economic threshold (usually in warm and dry years). Other pest species are controlled only
occasionally if pest outbreaks occur.
Order Suborder Family Species Literature
source
Croatia Neighboring
countries
Collembola Smynthuridae Sminthurus sp. Latreille 1802 21 +
Thysanoptera Thripidae Frankliniella intonsa (Trybom
1985)
21 +
Hemiptera Heteroptera Miridae Lygus sp. Hahn 1833 9 +
Lygus gemellatus (Heerrich-
Schaeffer 1835)
21 +
Lygus pratensis (Linneaus
1758)
24 +
Lygus rugulipennis Poppius
1911
8 +
Halticus apterus (Linnaeus
1758)
9 +
Apolygus lucorum (Meyer-
Dur 1843)
24 +
Pentatomidae Dolycoris bacarrum (Linnaeus
1758)
21, 24 +
Eurydema oleracea (Linnaeus
1758)
24 +
Nezara viridula (Linnaeus
1758)
9, 26 +
Piezodorus sp. Fieber 1861 9 +
Anthocoridae Anthocoris sp. Fallen 1814 9 +
Orius niger Woolf 1811 6 +
Nabidae Nabis (Nabis) ferus Linnaeus
1758
6, 9 + +
Nabis feroides Wagner 1967 6 +
Nabis pseudoferus Remane
1949
6 +
Homoptera Membracidae Sctictocephala bisonia Koop
& Yonke
9, 22, 24 + +
Cicadella viridis (Linnaeus
1758)
9 +
Aphididae Aphis craccivora Koch 1854 21 +
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Order Suborder Family Species Literature
source
Croatia Neighboring
countries
Diaspididae Lepidosaphes sp. Shimer
1898
21 +
Coleoptera Elateridae Agriotes ustulatus Schaller
1793
15
Agriotes sp. Eschscholtz 1829 15 +
Scarabaeidae Anomala sp. Schoenherr
1817
21 +
Anobiidae Stegobium paniceum
(Linnaeus 1758)
21 +
Cocinelidae Subcocinella
vigintiquatuorpunctata
(Linnaeus 1758)
9, 21 + +
Chrysomelidae Longitarsus sp. Berthold
1827
9 +
Phylotreta undulata
Kutschera 1860
9 +
Haltica oleracea Linnaeus
1758
9 +
Lathiridae Corticaria sp. Marsham 1802 9 +
Curculionidae Phyllobius sp. Germar 1824 9 +
Sitophillus sp. Schnherr, 1838 9 +
Lepidoptera Gracilariidae Phylonorycter insignitella
Zeller 1846
24 +
Pyralidae Etiella zinckenella (Treitschke
1832)
8, 9, 14, 21 + +
Crambidae Udea ferrugalis Hubner 1796 21 +
Tortricidae Olethreutes lacunana
Freeman 1941
21 +
Grapholita compositella
Fabricius 1775
24 +
Lymanthridae Orgya gonostigma L. 21 +
Geometridae Ascotis selenaria Dennis &
Schiffermuller 1775
21 +
Nymphalidae Vanessa cardui Linnaeus
1758
9, 20, 23,
24, 25, 27,
28, 29
+ +
Noctuidae Acronicta (Viminia) rumicis
(Linnaeus 1758)
21 +
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Order Suborder Family Species Literature
source
Croatia Neighboring
countries
Chloridea dipsacea L.
(Heliothis viriplaca (Hufnagel,
1766))
21 +
Phragmatobia fuliginosa
(Linnaeus 1758)
21 +
Autographa gamma
(Linnaeus 1758)
7, 8 +
Helicoverpa armigera
(Hubner 1808)
7, 8 +
Mamestra sp. Ochensheimer
1816
7, 8 +
Diptera Cecidomyidae Clinodiplosis trotteri =
Anabremia trotteri (Kieffer
1909)
21 +
Acarolestes tetranychorum
(Kiefer 1909)
21 +
Anthomyiidae Delia platura (Meigen 1826) 8 +
Agromyzidae Lyriomyza congesta (Becker
1903)
21 +
Prostigmata Tetranychidae Tetranychus urticae Koch
1836
7, 8, 9, 10,
12, 13, 16,
17, 19
+ +
Tetranicuhus atlanticus = T.
turkestani Ugarov & Nikolskii
1937
7, 8, 9, 10,
16, 17, 19,
24
+ +
Tetranychus tumidus Banks
1900
24 +
Table 1. Arthropod species established to damage soybean in Croatia and neighburing countries
In only one investigation which was carried out in Serbia [21] beneficial fauna on soybean
was recorded. Only three predatory species were established, Coccinella septempunctata L.
(Coleoptera: Coccinelidae), Chrysopa carnea Stephens (Neuroptera: Chrysopidae) and Acaro‐
lestes tetranychorum Kief. (Diptera: Cecidomyidae). There are no similar investigations con‐
ducted in Croatia but, out of all species listed [9] as potential members of entomofauna of
soybean, two species (Anthocoris sp. Fallen and Nabis (Nabis) ferus L.) are listed as potential
beneficial insects.
The subject of pest control is rarely discussed without the reference to the concept of inte‐
grated pest management (IPM). IPM is essentially a holistic approach to pest control that
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seeks to optimize the use of a combination of methods to manage whole spectrum of pests
within particular cropping system. IPM relies heavily on biological controls with a perspec‐
tive chemical input only as a last resort. For effective control, there needs to be an under‐
standing of a pest’s interaction with its environment. This is so called concept of “life
system” which was initially conceived by Clark et al. [31] to reinforce the idea that popula‐
tion cannot be considered apart from the ecosystem with which it interacts. The life system
consists of the pest population plus its “effective environment”. Most ecological pest man‐
agement concentrates on the agro-ecosystem, defined as “effective environment” at the crop
level [32]. Monitoring in insect pest management can be used to determine the geographical
distribution of pests, to assess the effectiveness of control measures, but in its widest sense
monitoring is the process of measuring the variables required for the development and use
of forecast to predict pest outbreaks [33]. Such forecasts are an important component of pest
management strategies because a warning of the timing and extent of pest attack can im‐
prove the efficiency of control measures. For successful pest control according to the princi‐
ples of IPM it is of great importance to have deep knowledge in harmful and beneficial
arthoropods in particular agro-ecological conditions.
The study was conducted to determine the harmful and beneficial arthropod fauna during
the soybean growing season, and based on their dynamic of occurrence and abundance to
identify the harmful and beneficial species of greater importance for soybean production in
Croatia.
2. Materials and methods
Research was conducted on experimental field located in Zagreb. The soybean variety Zlata
(BC Institute Zagreb, Croatia) was planted on April 27th 2010 on an experimental area of 162
m2. The average plant density was 630.000 plants/ha. Soybean variety Zlata belongs to the
maturity group “0” and according to the information given by producers [34] it has a
“good” tolerance to pests and diseases. In order to control weeds gyphosate (pre-sowing),
metribuzin, metholachlor and clomazone (in the phase of the first trifoliate - V1, according
to [35]) and bentazon (in the phase of the third trifoliate - V3) were applied.
Sweep net sampling consisted of making a set of 50 sweeps across three rows of soybeans
while walking down the row [36]. A 30 cm diameter sweep net was used. Sampling began
when soybeans were in the beginning of flowering (R1) on June 24th 2010 and continued
through September 9th 2010 when plants reached physiological maturity (R7). Weekly sam‐
pling was done on the same day each week in late morning. It was performed for 12 weeks.
At each sampling date four samples were collected.
Whole plant counts were conducted on 10 plants per each of four replicates. As it was pro‐
posed by Kogan and Pitre [36] randomly selected plants were initially scanned for large, of‐
ten fast moving species. After the initial scan, both sides of each leaf on the plant were
searched, as were petioles, axils and stems. Additionally, one leaf per plant was collected at
each whole plant count date to establish mite population by leaf inspection. Therefore, four
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samples each containing 10 leaves were transported to laboratory to be examined under the
stereomicroscope and all life stages of mites were counted [37]. Whole plant counts and leaf
collection began one week later than sweep net sampling i.e. on July 1st 2010 and continued
through September 9th 2010. It was performed for 11 weeks.
All collected insects were identified to the family or genus and species (if possible). For iden‐
tifying insects identification keys were used [38-42].
Based on the number of all individuals, cenological characteristics (dominance and frequen‐
cy) of the insect orders and families (where appropriate) were determined [43].
The dominance was calculated by Balogh formula:
D1= a1
∑ai
x100
Where: a1 = number of identified specimens of one species;
Σa1 = total number of all collected specimens.
The frequency was calculated by Balogh formula:
Ca1 =Ua1
∑Ui
x 100
Where: Ua1 = number of samples with identified species;
∑Ui = total number of samples.
3. Results and discussion
The total catch was 1357 specimens which belong to six orders: Thysanoptera, Hemiptera,
Coleoptera, Lepidoptera, Diptera and Prostigmata (Table 2).
Out of 1357 specimens, only 73 individuals (5.37%) belong to beneficial fauna (mostly preda‐
tors), while all other collected specimens are herbivorous and therefore potential pests on
soybean. All found beneficials belonged to predators and majority of them (70 individuals)
belong to Hemiptera what confirms the statement of Ketzschmar [44] that predaceous Hem‐
iptera are usually more abundant in soybean fields than all other insect predators combined.
In earlier investigations [21] conducted in Serbia no predaceous Hemiptera have been found
while more recent investigations in Serbia [6] and in Croatia [9] stated that they are present
in soybean crops. All predaceous Hemiptera feed on a wide range of hosts and may extend
this polyphagy to plant feeding to some extent [45]. Such plant feeding causes no damage to
row crops but almost certainly has survival value for the predators by maintaining popula‐
tions where prey are scarce or absent. Some of the species which belong to family Pentato‐
midae are also recognized as predators [45]. Since some of the individuals collected in our
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investigation were classified as family Pentatomidae but, were not identified to the species,
it is possible that some of them are predaceous as well.
ORDER FAMILY GENUS SPECIES TOTAL NUMBER OF INDIVIDUALS CAPTURED
BY
SWEEP NET WHOLE
PLANT
COUNTS
LEAF INSPECTION
Thysanoptera * 52 12
Hemiptera Miridae Halticus apterus 44 3
Lygus Hahn
1833
sp. 4
Nabidae Nabis ferus
Linnaeus
1758
55
Anthocoridae * 3 8
Pentatomidae * 12
Nezara viridula
Linnaeus
1758
472 181
Piezodorus sp. Fieber
1861
28
Membracidae Stictocephala bisonia Kopp
& Yonke
1977
2
Cicadellidae Cicadella viridis
Linnaeus
1758
3
Coleoptera Coccinelidae * 3
Chrysomelidae Phyllotreta undulata
Kutschera
1860
4
Haltica oleracea
Linnaeus
1758
7
Longitarsus
Berthold 1827
sp. 2 1
Latridiidae Corticaria
Marsham 1802
sp. 21
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ORDER FAMILY GENUS SPECIES TOTAL NUMBER OF INDIVIDUALS CAPTURED
BY
SWEEP NET WHOLE
PLANT
COUNTS
LEAF INSPECTION
Curculionidae * 1* 1* 1
Phyllobius
Germar 1824
sp. 5
Sitophillus
Schnherr, 1838
sp. 1
Lepidoptera * 2
Nymphalidae Vanessa cardui
Linnaeus
1758
7
Noctuidae 15
Diptera Nematocera * 1
* 16
Prostigmata Tetranychidae Tetranychus urticae Koch
1836
387
TOTAL 759 211 387
* Identification was not possible; Beneficial species are marked in grey;
Table 2. Arthropod species established during the soybean vegetation in 2010 by three different methods
Using the entomological net, 759 individuals were collected, whereas 211 individuals were
gathered by whole plant counts and 387 individuals by leaf inspection.
3.1. Sweep net sampling
Number of arthropod individuals collected by sweep net sampling was the highest among
the three methods applied. Using these methods, species belonging to 20 different systemat‐
ic categories were collected. The collected individuals belonged to five insect orders, Thysa‐
noptera, Hemiptera, Coleoptera, Lepidoptera and Diptera. The abundance of insect orders
established by sweep net sampling is shown in Figure 2.
Order Hemiptera was present in the sweep net sampling in the highest abundance (82.48%).
The same order was the most frequent. It was present in 87.5% of all samples obtained by
sweep net sampling. Order Coleoptera was present in 57.5% of all samples and was desig‐
nated as constant. Other orders (Thysanoptera, Lepidoptera and Diptera) were less frequent;
they were present in 30-37.5% of all samples. Investigations conducted in different agro-eco‐
systems showed that the sweep net sampling is the most effective method to collect different
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leaf feeding pests as are leafhoppers [46], lepidopterous larvae [46, 47], leaf feeding Coleop‐
tera [48] and phytophagous Pentatomidae [49] as well as predaceous Hemiptera [45].
3.2. Whole plant count
The lowest number of individuals was established by whole plant count method. The major‐
ity of established individuals belonged to order Hemiptera. Only few Thysanoptera and
Lepidoptera were established by this method. Some authors stated that this method is suita‐
ble for larvae of Lepidoptera [46, 47] and for phytophagous thryps [50]. There are no data on
any damage caused by any phytophagous thrips in Croatia while Vanessa cardui L. was re‐
corded in previous investigations as important pest.
3.3. Leaf sampling and inspection
The only species established by leaf inspection was T. urticae. It was proved that this method
is good for establishing population of phytophagous thrips [48], whiteflies [49] and mites
[35]. It is obviously that out of these three groups, only phytophagus mites were present in
experimental field.
3.4. Collected species: abundance and importance
Sampling arthropod populations is a cornerstone of basic research on agricultural ecosys‐
tems and the principal tool for building and implementing pest management programs. The
purpose of sampling is dual, it is a research method for defining the nature and dynamics of
communities in agricultural ecosystems and it is also a mean for providing pest manage‐
ment decision. The purpose of sampling in our investigation was to get deep knowledge on
pest and beneficial species present in soybean crop. Conducted investigation encompassed
three most common sampling methods for investigations of soybean arthropod fauna. The
6.85%
82.48%
5.67%
2.90%2.11%
Thysanoptera Hemiptera Coleoptera Lepidoptera Diptera
Figure 2. Abundance of insect orders collected by sweep net sampling of soybean crop, Zagreb, 2010
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need to encompass all three methods is confirmed later by the fact that species identified by
each particular method differ. By employed methods we were able to get all relevant data
on above ground arthropod fauna that could be found on soybean canopy. We did not aim
to collect information on underground soybean arthropods and ground predators in soy‐
bean fields. To collect this information we should use common methods for sampling soil
arthropods, soil samples and extraction [51] or pitfall trapping [48]. Some of earlier research‐
es on soybean arthropod fauna in the region collected information on underground soybean
arthropods but, no research did pay attention on ground predators in soybean field. No re‐
searches among all conducted [6-29] did pay attention to abundance and frequency of par‐
ticular orders, genus or species as well, so it is not possible to compare if there are some
discrepancies with the results of previous researches.
Individuals that belonged to the order Thysanoptera have been found by sweep net sam‐
pling in highest abundance than by whole plan counts, and they haven’t been found by leaf
inspection at all. In Serbia one phytophagous thrips species (Frankliniella intonsa Trybom) on
soybean has been identified [21]. Since in our investigation thrips were not established by
leaf sampling and inspection, it could be concluded that they did not feed and develop on
soybean. It might be that those species are predaceous because it is reported [52] that thrips
are natural enemies of different pests. Important predaceous genera of thrips are Aelothrips
Haliday, Franklinothrips Back, Scolothrips Hinds, Leptothrips Hood, Karnyothrips Watson and
Podothrips Hood. Within the genus Aeolothrips, the species Aeolothrips intermedius Bagnall is
distributed throughout western and eastern Europe [53], the middle East and India but now
it can be considered cosmopolitan [54]. Comparative tests by many authors [53, 55, 56] using
different types of prey (including various species of Thysanoptera), suggested that both the
larvae and the adult females are generic predators, even though they present marked diet‐
ary preferences. In Italy [57] A. intermedius was detected in association with various different
phytophagous Thysanoptera, which included T. tabaci but also frequently F. occidentalis on
many different plant species including legume species Medicago sativa L. Predaceous thyrips
belonging to the genus Aelothips are reported as important predators of T. urticae in soyben
crops in north-eastern Italy [58]. Franklinothrips sp. adults and larvae are generalist predators
and attack a wide variety of arthropod pests including two spotted spider mite (T. urticae)
[59]. Genus Scolothrips is counting six species in Europe [60], and one of them, Scolothrips
longicornis Priesner is a predator of T. urticae [61] and T. turkestani [62]. Both pest species are
registered as soybean pests in Croatia. Genus Leptothrips is not present in Europe [60]. Genus
Karnyothrips is counting three species in Europe [60]. Some species are reported as predators
of scale insects [63]. Genus Podothrips is known as grass-living genus. It counts only two spe‐
cies in Europe present only in Italy and Cyprus [60]. Since identification to the species was
not possible, we cannot state which species of Thysanoptera were present.
Individuals belonging to six families of the order Hemiptera were identified in our research.
Four families belong to the suborder Heteroptera (so called typical bugs) and two families
belong to the suborder Homoptera.
Family Miridae was presented by genus Lygus sp. Four individuals were captured. Identifi‐
cation to species was not possible. Species belonged to the genus Lygus were reported by
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different authors [6, 8, 21, 24] to feed on soybean crops in Bosnia and Herzegovina and Ser‐
bia as well as in Croatia [9] without causing serious damages. More numerous were individ‐
uals of Halticus apterus. This species is distributed through Mediterranean region [64]. It was
reported to feed on soybean only in Croatia [9]. Other research showed that it feeds on some
legume plants such as Medicago sativa L., Lotus corniculatus L. and Trifolium repens L. in Italy,
and also to be able to cause damages on onions and Gallium [64]. Since it was not reported
as serious pest of soybean anywhere, it should be monitored in the future but the probabili‐
ty for this species to become important pest of soybean is low.
Family Nabidae was represented with one species, N. ferus. The same species was previ‐
ously reported in Croatia [9] and in Serbia [6]. Additionally two other species of this ge‐
nus, N. feroides and N. pseudoferus, were reported in Serbia [6]. The density of N. ferus was
moderate, total of 55 individuals were captured. This species was reported as common
predator species in Ukraine [65]. Aphids are the principal prey insects for this species, but
numerous other families are acceptable, including other bugs [65]. Because of its possible
importance in soybean agro-ecosystems, the dynamic of the appearance of this species will
be further analyzed.
Eleven individuals belonging to family Anthocoridae were captured in our investigation.
Family Anthocoridae was previously reported in soybean in Croatia [9] and in Serbia [6].
This family is mentioned as one of the most important predaceous family of Heteroptera in
soybean crops [45]. Within the family Anthocoridae, members of the genus Orius occur as
predators in soybean fields all around the world [45]. The species Orius niger Woolf has been
found in soybean fields in Serbia [6]. In some areas, species of the genus Anthocoris Fallen
are probably also important predators in soybean [45]. Captured individuals were not iden‐
tified to the species so it is not possible to discuss which genus was the most abundant in
our investigations.
Among the established Hemiptera, family Pentatomidae was the most abundant. Altogeth‐
er 512 individuals were found in sweep-net samples and 181 individuals by whole plant
counts. The most abundant species was the southern green stink bug, Nezara viridula L. This
species was reported as present in Croatia [9]. Recently the serious damages caused by this
species were reported in Croatia [26]. It is not mentioned as serious pest in neighboring
countries, while it was mentioned as serious threat to soybeans in Italy [58, 66]. It was re‐
ported [49] as one of the most abundant phytophagous stink bugs on soybean worldwide
among of almost 40 species of stink bugs that have been found on soybean. Due to high
number of captured individuals and registered damages caused by this species, it might be
identified as one of the potential pests on soybean in Croatia. Therefore the dynamic of the
appearance will be further analyzed. Species belonging to phytophagous genus Piezodorus
were captured in lower number. Genus Piezodorus was reported as possible pest genus in
Croatia [9] and in Italy [58]. The importance of the species P. guildinii Westwood is increas‐
ing in USA as well as in Brazil. This species was observed for the first time in southern Loui‐
siana in 2000 and since 2002, it has been a significant pest of soybean [67]. At present,
Eustichus heros (F.) and P. guildinii are more widespread and occur in greater numbers than
N. viridula, and P. guildinii is principally responsible for the green bean syndrome observed
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in Brazilian soybean [68]. Genus Piezodorus is counting three species in Europe [60]. Twelve
individuals, members of family Pentatomidae remained unidentified. It is possible that
some of them are phytophagous. Also it is possible that some of them are predators because
species which belong to family Pentatomidae are also recognized as predators [45].
Two families each represented with one species from the suborder Homoptera have been
collected in low numbers. Stictocephala bisonia was reported to feed on soybean in Croatia
[9], Serbia [21] and Bosnia and Herzegovina [24]. The second identified species was Cicadella
viridis. This species was registered to feed on soybean in Croatia [9] but without significant
damage. Within the USA, potato leafhopper (Empoasca fabae Harris) is the most important
leafhopper species [69]. Even though aphids are recognized as a regular part of entomofau‐
na of soybean, we did not record them. Several species of aphids are known to attack soy‐
bean crops. The most important species in North America is Aphis gyicines Matsumura [70,
71]. This species is not registered in Europe [60]. Some other species of aphids that are mem‐
bers of the fauna of Europe [60] and Croatia [72, 73] successfully colonize and reproduce
parthenogenetically on soybean [71]: A. craccivora Koch, Aulacorthum solani (Kaltenbach) and
Aphys gossypii Glover.
Out of four families of the order Coleoptera that were identified, one represents mainly pre‐
daceous species (family Coccinelidae). Some species of the family Coccinelidae are reported
as the members of arthropod fauna on soybean in Croatia and Serbia [9, 21]. Species Epilach‐
na varivestris Mulsant is known as a soybean pest in USA [48]. Three species of the phytoph‐
agous genus Epilachna are present in Europe, including Croatia [60] but only in Dalmatia
where soybean cultivation is not common. Individuals from the genus Corticaria, family La‐
tridiidae were the most numerous. Adults and larvae of this family feed on the conidia of
fungi and Myxomycetes [74]. All found species from the order Coleoptera were previously
listed as potential members of soybean fauna in Croatia [9] but, due to the low populations,
their potential to be significant pests or predators is not very high. We did not employ any
method for sampling soil dwelling insects or underground fauna. Therefore we did not col‐
lect the species which belong to families Elateridae and Scarabaeidae that are known as pol‐
yphagous soil pests that could cause damage on soybean crops [15, 21].
Only 22 individuals from order Lepidoptera were collected. Painted Lady (Vanessa cardui)
was the only identified species. Other specimens were classified into the family Noctuidae.
V. cardui was previously recorded to significantly damage soybean in Croatia [9, 25, 27, 29]
and in neighboring countries [20, 23]. The outbreak of this pest is periodical. Higher popula‐
tion could be expected in weedy soybean fields because females are attracted by pollen
sources and heavy plant density [25]. There are many of species from the family of Noctui‐
dae and from the other families, members of the order Lepidoptera which could cause the
damage but, until now, serious damage in Croatia was reported only by V. cardui. In USA,
the most important lepidopterous species are Anticarsia gemmatalis (Hubner), Pseudoplusia in‐
cludens (Walker), Trichoplusia ni (Hubner), Platypena scabra F., Heliothis zea Boddie, Heliothis
virescens (Fabricius) and Heliothis (=Helicoverpa) armigera (Hubner) [46, 47, 75]. Except T. ni
and H. armigera, other species are not distributed in Europe [60]. H. armigera is often men‐
tioned as one of the potentially very dangerous species. Because of its invasive nature this
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pest is currently placed on Annex I A II of Council Directive 2000/29/EC, indicating that it is
considered to be relevant for the entire EU and that phytosanitary measures are required
when it is found on any plants or plant products. Some countries made pest risk analyses
[76]. Damages caused by this species were reported on soybeans in Vojvodina Province of
Serbia and in Montenegro in the very warm summer of 2003 [77] when 85.3% of the soybean
pods were injured in August. H. armigera is a serious pest on outdoor crops in Portugal and
Spain, predominantly on tomato crops as well as on cottom and maize. It developed resist‐
ance to many groups of insecticides [78]. We did not find caterpillars of limabean pod borer
(Etiella zinckenella Treitschke) even though this species was reported as soybean pest in Cro‐
atia [9] and in neighboring countries [6, 14, 21]. In Southern Europe and in Central and
South America E. zinckenella is only damaging pod borer species in soybean.
Order Diptera was represented by 17 individuals that were not indentified to the species.
The pest species from the order Diptera reported in the literature are Delia platura Meigen [6,
58], Liriomyza congesta Becker and Clinodiplosis trotteri Kief. [21]. Larvae of D. platura could
cause damage on soybean seed during the emergence. Larvae of L. congesta are damaging
leaves [21] and larvae of C. trotteri are damaging plant stem [21]. Some of Diptera species in
soybean could be natural enemies, for example predaceous species Acarolestes tetranychorum
feed on mites [21].
We established one species from order Prostigmata (infraclass Acari). This was the species
T. urticae which was established only by leaf inspection. This species is the most important
pest of soybean in the whole region [6, 8-10, 13, 17, 19, 29]. The pest outbreaks are occurring
in dry and warm years in which farmers must apply control measures. Besides T. urticae,
soybean in Croatia [9] and neighboring countries [16, 17, 19] is often attacked by T. atlanticus
(= turkestani). Both species have similar thermal requirements but, T. atlanticus prefers ex‐
tremely dry conditions [9]. Some differences were established in their response to host plant
nutrient status [79]. The development of T. urticae is positively influenced by potassium con‐
tent in the plant host, while T. atlanticus is positively influenced by content of phosphorus.
According to the data obtained from Meteorological and Hydrological Service of Republic of
Croatia, somewhat lower temperatures and higher amount of rainfalls in July and August in
2010, comparing to the average were recorded. That could cause the absence of T. atlanticus
in experimental field and relatively low population of T. urticae.
The dominance indices of the insect orders established in total capture are shown in Figure 3.
In total catch the eudominant orders were Hemiptera (60.46%) and Acarina (28.6%), while
subdominant were orders Thysanoptera (4.73%), Coleoptera (3.33%), Lepidoptera (1.63%)
and Diptera (1.26%).
3.5. Most important phytophagous species
The significant feeding on soybean was established by two species, N. viridula and T. urticae.
Therefore we will further analyze their appearance with the respect of their life cycle and
possible damages that they can cause.
The dynamic of the appearance of N. viridula is shown in Figure 4.
Soybean - Pest Resistance
126

0
20
40
60
80
100
120
140
160
180
24-Jun
1-Jul
8-Jul
15-Jul
22-Jul
29-Jul
4-Aug
11-Aug
18-Aug
26-Aug
2-Sep
9-Sep-12
phenophase: R1, R2 R3, R4, R6 R7, R8
Total number of individuals
sweep net whole plant inspection
Figure 4. The dynamic of the appearance of Nezara viridula (L.) on soybeans in Croatia in 2010 established by two
sampling methods
The southern green stink bug, N. viridula, is one of the most economically important soy‐
bean pests [80]. It has a worldwide distribution, occurring throughout the tropical and sub‐
tropical regions of Europa, Asia, Africa and America [49]. This pest is in constant expansion
as a consequence of the increased acreage for soybean production, particularly in South
America [80]. This pentatomid is highly polyphagous, attacking more than 145 species of
plants (including cultivated and uncultivated species) within 32 families [49]. Life cycle of
the southern green stink bug has been studied by number of authors in different parts of the
world [81-85]. The biology of this pest has not been studied in Croatia jet but, some data
were presented by different authors [26, 29]. From literature it is known [49] that southern
green stink bug, like most pentatomids, overwinters in the adult stage under different ob‐
jects that offer protection (litter, bark etc.). In the northern hemisphere [49] overwintering
4.73%
60.46%
3.33%
1.63%
1.26%
28.60%
Thysanoptera Hemiptera Coleoptera
Lepidoptera Diptera Prostigmata
Figure 3. The dominance indices of arthropod orders established in the total capture of arthropod species on soybean
in Croatia in 2010
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adults emerge in March and first generation develops on clover. The total developmental
time from eggs to adults lasts between 23 days [82] and 49 days [81]. In USA, it develops 3-5
generations per year, depending on the climate. The 3rd, 4th and 5th generations attack soy‐
bean. We found it on soybean when soybeans began to mature, in August and onward what
corresponds with the data presented by Todd and Herzog [49]. Probably the first two gener‐
ations developed on some other plants. Stink bugs feed primarily on the seeds of soybean.
Feeding results with puncture marks on the seed coat, deformation of the seed coats and re‐
duced seed weight and size. Adults live longer, approximately 30 to 50 days [81, 82] and
they cause more damage than nymphs [86]. Croatian authors [26] proposed economic
threshold of 1 bug/30 m of soybean row or 8-10 bugs/10 sweep nets what seems to be too
low. It is important to point out that the threshold depends on the period when insects oc‐
cur. Early infestation causes more damage than late infestation [86]. Late in the season high
infestation level of 2 bugs/m2 will not result with the damage [86]. In our investigation we
established infestation of 2 bugs/plant by whole plant count method and 4-5 bugs/10 sweep
nets without seeing any damage on the yield. The appearance of N. viridula was in literature
[26] connected with higher temperatures and drought, what was not the case in our investi‐
gation. Generally, in other countries the southern green stink bug is controlled with non-se‐
lective insecticides, which belong to carbamates, the organophosphate group, or the
cyclodiene group, such as endosulfan or to pyrethroids [80]. Some of the mentioned insecti‐
cides are banned in Croatia and others are not allowed for that purpose. In the case of pest
outbreak farmers do not have any available option to control this pest.
The second species which was recorded in high population density was T. urticae. The infes‐
tation with T. urticae started somewhat earlier that the attack of N. viridula. The dynamic of
the appearance of T. urticae is shown in Figure 5.
0
10
20
30
40
50
60
70
80
90
100
1-Jul 8-Jul 15-Jul 22-Jul 29-Jul 4-Aug 11-Aug 18-Aug 26-Aug 2-Sep 9-Sep
R3, R4, R6 R7, R8
Total number of individuals
leaf inspection
Figure 5. The dynamic of the appearance of Tetranychus urticae on soybeans in Croatia in 2010
Soybean - Pest Resistance
128

The maximal infestation of T. urticae was recorded on August 11th and it was 2.25 mites/leaf.
This infestation is considered as very weak to weak infestation [87]. After that date, the
number of mites significantly decreased without the use of acaricides. The reason of the de‐
crease of the population is the period in August in which strong rain occurred. Strong rain
probably caused washing up the spider mites from the leaves as it was mentioned by some
authors [29, 87]. T. urticae injure soybean by feeding on the green foliage and pods. By their
needle-like chelicerate mouthparts that are used to puncture individual plant tissue cells
and consume the entire cytoplasmic contents, they are leaving and empty irreversible dam‐
aged cell. The presence of numerous empty cells results in the yellow or brown spots on
mite-injured leaves. Extensive feeding by large numbers of mites causes the leaves to appear
yellow or brown [37]. Complete defoliation due to mite feeding can reduce pod set and seed
yield. Under the favorable conditions mites have very short developmental time, between
8-20 days [9]. That enables them to develop several generations in a very short time and to
increase population up to the economic threshold very fast. Therefore permanent monitor‐
ing of the pest population is needed. No acaricides are allowed for the control of T. urticae in
soybean crops at the moment in Croatia. Even though there are some mite resistant cultivars
in USA [88], they are not registered in Croatia.
3.6. Most important zoophagus species
Total of 73 predaceous species are collected in the investigation. Family Nabidae was repre‐
sented by one specius, N. ferus. Members of the family Nabidae are confirmed predators of
different kind of insects [89]. Most types of insect prey of nabids are plant-feeding species,
but nabids sometimes attack predaceous insects, including members of their own species.
The polyphagous feeding habits of the nabids make them less effective than species-specific
predators against specific prey species [89]. Altogether 55 individuals of N. ferus were count‐
ed. The dynamic of the appearance of N. ferus is shown in Figure 6.
Nabis ferus is a common, widespread species in the Palearctic region [89]. It was reported as
predatory species on Trialeurodes vaporariorum Westwood [90], Oulema melanopus L. [91], Si‐
tobion avenae F. [92] and other aphid species [65], N. viridula [93] and leafhoppers in all stages
[89]. Species N. ferus overwinters in the adult stage [65]. Adults emerge from the soil and
migrate to field of various crops in April and May according to the weather. They mate, lay
eggs and the nymphs appear between late May and June and are present until July [65].
There is a second generation with nymphs in July-August and adults in August-October.
The dynamic of the appearance of N. ferus in experimental field corresponds with the data
on life cycle of this species [65]. In mid-late July we collected adults of the first generation
and nymphs were collected in August. Kereši [94] stated that zoophagous Nabis species de‐
velop one generation per year in soybeans. She mentioned adult appearance at the end of
July and maximal larval appearance at the end of August. It remains unknown in which
crop species is developing the first generation. Due to its preference to prey aphids which
are abundant in wheat fields, it could be that the first generation is developing in wheat
fields. The experimental field in our investigation was surrounded by wheat fields what
could influence high population of N. ferus.
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129

0
2
4
6
8
10
12
14
16
18
20
24-Jun 1-Jul 8-Jul 15-Jul 22-Jul 29-Jul 4-Aug 11-Aug18-Aug26-Aug 2-Sep 9-Sep
phenophase: R1, R2 R3, R4, R6 R7, R8
Total number of individuals
sweep net
Figure 6. The dynamic of the appearance of Nabis ferus on soybeans in Croatia in 2010
4. Conclusions
Literature reports that soybean crops in the region where Croatia belongs (Croatia, Hun‐
gary, Serbia, Romania, Bulgaria and Bosnia and Herzegovina) are attacked by over 180 pests
(150 insects and 30 species from other animal classes). However, by literature review from
Croatia, Serbia and Bosnia and Herzegovina we established that 52 species (or genus) of ar‐
thropods are reported to be associated with soybean crops. Out of these 52 species, seven
species are zoophagous, 44 species are phytophagous and one species is myceliophagous.
Additionally, we have found data on 43 species of phytoparasitic nematodes that can be
find in soybean fields but without causing significant damages and literature also reports on
three species of rodents that could cause significant damage on soybean fields.
In our investigations the number of established species was lower than the number obtained
by literature review. Total of 1357 individuals were collected and classified into the five or‐
ders from the class of Insects and one order from the class of Arachnida (infraclass Acari).
1232 individuals were classified in 15 species or genus, 58 individuals were classified into
the six families while 67 individuals were classified into the orders. Phytophagous arthro‐
pods were more abundant than zoophagous. The ratio between phytophagous and zoopha‐
gous specimens was 94.63% : 5.37%.
Based on the results of the literature review and of the research conducted, it could be con‐
cluded that significance of the arthropod pest fauna connected with soybean has changed
over the time. Nowadays, soybean production in Croatia could be endangered by four phy‐
tophagous arthropod species: N. viridula L., V. cardui L., T. urticae and T. turkestani.
N. viridula is attacking soybean pods and seed causing the loss in yield quantity and quality.
The early infestation is very dangerous. The population of this pest has been increasing in
the past few years. This could be connected with the increase of soybean cultivation area.
Obtained results indicate that the increase in pest population has occurred recently and that
Soybean - Pest Resistance
130

one existing species became significant pest of soybean. The life cycle of this pest as well as
other issues related to sampling procedure, economic threshold and control possibilities
have not been studied jet in Croatian agro-ecological conditions. In the future, investigations
should be carried out with the aim to collect more data on this pest and to be able to imple‐
ment IPM principles in its control.
V. cardui is causing defoliation of the soybean plants. As periodical pest it appears from time to
time in certain areas causing significant damage. Sampling procedure for this pest is establish‐
ed but, research should be conducted in order to determine economic threshold and the effica‐
cy of environmentally acceptable insecticides (B.t.k., spinosad, neem, IGRs, avermectins).
Phytophagous mites, T. urticae and T. turkestani as soybean pests are well known to Croatian
farmers. Due to their feeding on soybean leaves they are causing defoliation. Their infestation
is related to the climatic condition. In warm and dry years these pests cause more severe dam‐
age than in “normal” years. Sampling procedure for these pests is established but, due to the
lack of registered acaricides, their control is not possible. The future research should be fo‐
cused on finding appropriate ecologically acceptable acaricide for the control of this pest.
The critical period for the infestation by all four species is from flowering through maturity
in which period all four pests should be monitored and sampled on a regularly basis in or‐
der to ensure the proper information about the need for control measure.
Some other pests that were found in our investigation are capable of becoming key pests if
environmental conditions and population of their natural control agents are disrupted by
unnecessary application of insecticides. One of these species belongs to Piezodorus sp. which
is world widely recognized as very important soybean pest. Thus the future systematic and
intensive study of the arthropod fauna associated with soybean in Croatia has to be contin‐
ued. It will allow us to monitor the changes in the pest population and to prepare strategies
for the control of the new pests that could arise over the time.
The main zoophagous species found on soybeans was Nabis ferus. The role of this species in
soybean ecosystems, including its varying feeding strategies, needs much additional attention.
Acknowledgements
We thank Prof. Hrvoje Šarčević for providing us adequate experimental field conditions.
Author details
Renata Bažok, Maja Čačija, Ana Gajger and Tomislav Kos
*Address all correspondence to: rbazok@agr.hr
University of Zagreb, Faculty of Agriculture, Zagreb, Croatia
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