Non-indigenous insect species in Israel and adjacent areas

15 Pages·2007·0.27 MB·English

BiolInvasions(2007)9:629–643
DOI10.1007/s10530-006-9064-y
ORIGINAL PAPER
Non-indigenous insect species in Israel and adjacent areas
Uri Roll Æ Tamar Dayan Æ Daniel Simberloff
Received:15November2005/Accepted:18October2006/Publishedonline:29November2006
(cid:1)SpringerScience+BusinessMediaB.V.2006
Abstract Non-indigenous species cause great regions. Absence of roads, settlements and pres-
damage worldwide. Non-indigenous insects are ence of nature reserves are negatively correlated
known as harmful in many regions, but few with occurrence of ENI species. Seventy-nine
comprehensive works have investigated non- species are categorized as pests that damage
indigenous insects as a group. We compiled a produce, merchandise, forestry, etc. Despite a
comprehensivedatabaseofestablishednon-indig- general dearth of knowledge on impacts of ENI
enous(ENI)insectsinIsraelandadjacentregions insects on natural systems, 42 species are known
to investigate how they arrived, their biological to feed on native plants, some of conservation
characteristics, and the attributes of areas they concern. Biological control agents are usually
invade. Of 218 species of ENI insects in this more limited in their distribution than other ENI
region,124arewidespread. Mostspeciescameas insects.Furtherresearch,legislation,andenforce-
stowaways, but 38 were brought intentionally for ment are required to minimize effects of these
biologicalcontrol.MostENIinsectsinthisregion species on agriculture and natural habitats.
are in the Coleoptera, Diptera, Hymenoptera,
Lepidoptera, and Homoptera. Species from var- Keywords Biogeographic origin (cid:1) Biological
iousordersdifferintheirtendencytobelocalized control (cid:1) Impact (cid:1) Insects (cid:1) Israel
or widespread, and in biogeographic origins. The
distribution of species among orders differs
between native and ENI insects. The Coastal Introduction
Plain houses the most ENI insect species and the
Negev and Judean deserts the fewest. Most ENI Invasion biology is a new science lacking uni-
insects spread from the Coastal Plain to other versal hypotheses and accepted truths (Mack
et al. 2000). Basic information on species occur-
rencesisdeficientinmanyregions,tosaynothing
U.Roll(&)(cid:1)T.Dayan
oftheirvariousattributesorimpacts(Macket al.
DepartmentofZoology,
2000). Nevertheless, non-indigenous species are
TelAvivUniversity,TelAviv69978,Israel
e-mail:[email protected] known to have tremendous economic and con-
servation impacts worldwide (Mack et al. 2000;
D.Simberloff
Mooney and Hobbs 2000).
DepartmentofEcologyandEvolutionaryBiology,
Variousaspectsofinvasionshavebeenstudied
UniversityofTennessee,Knoxville,
TN37996-1610,USA intensively in recent years. Most invasion
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630 BiolInvasions(2007)9:629–643
research is conducted on a few taxa, especially exception to this rule, as they are deliberately
plants, birds, and mammals. The class Insecta is importedandreleased(insomecasesrepeatedly).
the most diverse taxon, and insects significantly Consequently,mostknowledgeofnon-indigenous
affect ecological systems (Wilson 1992). How- insectsisofthosethateventuallybecomepestsof
ever, except for vectors of human disease and agriculture, forests, or human health, or those
pests of agriculture and forestry, insects are used for biological control.
usually under-represented in ecological research Non-indigenous insect research in Israel and
owing to lack of taxonomic knowledge and its adjacent areas has been largely anecdotal,
paucity of experts. The lacuna in non-indigenous concentrating on agricultural and forestry
insect research is most prominent with respect to pests—their localities, negative effects, and
their effects on local environments. means of control. Another area of research is
Comprehensive studies of non-indigenous spe- purposefully introduced biological control
ciesofaparticulartaxonoraspecificlocationare agents, usually imported to combat non-indige-
vital. Only broad knowledge of this phenomenon nous insects. For these species there is usually
will allow insight into the ecological mechanisms information on release points, success in estab-
thatunderliethearrivalandspreadofintroduced lishing populations, and effects on target species.
species and the great impact a minority of them In 1966 Bytinski–Salz tabulated all known non-
have. Such insight is crucial for sound manage- indigenous insect and mite species in Israel.
ment. Nevertheless, we cannot assume that gen- However, since this work no one has compiled
eralizationsfromaparticulartaxonomicgroupor data on ENI insects systematically in Israel and
a specific location hold for every region or taxon adjacent areas.
(Simberloff 1991). Non-indigenous insects are This study is meant to fill this gap. We
known from many locations, and their economic compiled a database from many sources and
tollinsomeinstancesisveryhigh(Pimentelet al. analyzed it with respect to various species attri-
2005). A few have also been noted as having butes, then compared our results to those from
negativeeffectsonlocalspecies.Forexample,the other regions. We also investigated the particular
arrival of several species of non-indigenous ants histories ofthe introduction and establishment of
has severely affected native flora and fauna the species in order to identify patterns. Further,
(Williams 1994; Holway et al. 2002). Various we sought patterns in their spread and distribu-
works describe non-indigenous insects as a group tion over Israel and adjacent areas. We also
in the USA (Sailer 1983; Kim 1991; Vazquez and correlated occurrence of ENI insect species with
Simberloff2001),theNetherlands(VanLenteren environmental, geographical, and human spatial
et al.1987),Australia(New1994),Italy(Pelizzari data.
and Della Monta 1997), Japan (Kiritani 1998),
France (Martinez and Malausa 1999), Spain
(Perez Moreno 1999), and Great Britain (Smith Methods
et al. 2005). There is great need for further
research. To this end, we surveyed established We studied ENI insects of the state of Israel,
non-indigenous (ENI) species of insects in Israel Golan Heights, West Bank and Gaza Strip, an
and adjacent areas, focusing on arrival, establish- area of about 27,500 km2 (see also Yom-Tov
ment,spread,andeffectsincomparisontowhatis 1988). Zoological data collected over the years
known from other regions. were gathered from this entire region (although
Insects, like most other invertebrates, are thesamplingeffortisprobablybiased,withfewer
usually introduced unintentionally (Mack et al. surveys in the West Bank and Gaza). For almost
2000). Generally small and obscure, they slip 40 years these areas were ruled by Israel and
through inspections (if such exist) in produce, hence both agricultural pest control and conser-
ornamental plants, soil, packing material, wood, vation were practiced by the same authorities,
etc., and can go undetected for many years. and cargo and produce have been transported
Insects introduced for biological control are an extensively within this area.
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BiolInvasions(2007)9:629–643 631
We obtained data from three main sources. distribution (52 species). (VI) Established local-
First was personal contact with curators and ly—a species established in one or a few small
researchers at the National Entomological Col- locations (34 species). (VII) Established wide-
lections at Tel Aviv University. Data thus spread—a species established over a large area,
obtained were primarily on species found in even if locally uncommon (124 species). (VIII)
biodiversity surveys. Second was either personal Extinct—an introduced or even an established
communication with local experts or published speciesthatdisappearedinthisregion(7species).
works relating to agricultural pests or biological (IX) Possibly native—a new find in the local
controlagents.Thefinalsourcewaslistsofnewly entomofauna,possiblynative(seealsobelow)(95
discovered species in the Israeli entomofauna, species). (X) Unknown—lack of knowledge of
which included some foreign ones (see below). status, as well as taxonomic uncertainties (8
These sources were augmented by data on species). Unless otherwise stated, in all further
each species from elsewhere in the world. analysestheinsectsexaminedwerethosethatare
Thedatabaseisaccessibleat:http://www.campus- established or in the process of establishment.
teva.tau.ac.il/images/up/fl_3cae1577.pdf These were the insects from the spreading cate-
For each species we recorded systematic affin- gory and from the three different established
ity, various life-history attributes, food habits, categories (categories IV–VII), 218 species alto-
geographic range of native population, source gether. See the online database for the list of
region for this introduction, new geographic these 218 ENI insect species with their status
range in this region, history of spread in this categories.
region and in the world, local dispersal methods, We were conservative about designating a
means of introduction, ecosystems invaded, year species as non-indigenous. If no evidence indi-
of first discovery in this region, known economic cated the species was introduced, we classified it
or environmental impact (in this region), known as‘‘possiblynative’’andanalyzeditnofurther.A
records of introduction elsewhere, and status in newly discovered species was considered intro-
this region. duced if its known native range is distant. Here,
We classified each species based on specific too, we used a strict approach as to what
knowledge of its status given in the original constitutes distant, taking into account the fact
reference. For species that lacked this informa- that Israel’s neighbors do not have comprehen-
tion, a combination of information about its sive accessible entomological information. An-
status was used for classification: its native other reason a newly discovered species could be
geographical range, when it was introduced, categorized as non-indigenous was knowledge of
whether it has been seen since, its current its spread and many encounters after initial
distribution, whether it has spread, and also discovery.
the nature of the data sources (an article dealing Spatial patterns of ENI insects were based on
with non-indigenous species as opposed to one distribution in the 19 different insect regions of
dealing with new species in the regional fauna). Israel and its adjacent areas, as published by
Many insects have synonyms, which made cross- Fishelson (1985), and were analyzed using
referencing more difficult, and some are unspec- ESRI—ArcViewGIS8.2software.Wecompared
ified. the basal occurrence layer of ENI insects (high-
The status categories were: (I) Introduced by lighting hotspots), to various data layers, includ-
humans—no additional data (58 species). (II) ing climatic data (mean annual temperature and
Introducedandknownnottohaveestablished(21 mean annual precipitation), vegetation types,
species). (III) Commensal—found only in dwell- intercityroadsandtheirmargins,layoutofhuman
ings or storage facilities (7 species). (IV) Spread- settlements, and occurrence of nature reserves
ing—a non-indigenous species expanding its and national parks. We also aimed to compare
range (8 species). (V) Established, whereabouts occurrence of ENI insect species to diversity
unknown—a species that is breeding unaided patternsof native insects. However,because data
for several generations but with unknown onthelatterarelacking,weusedtheonlyreadily
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632 BiolInvasions(2007)9:629–643
availablesurrogatefornativeanimalbiodiversity, Year of discovery of ENI insects
which is the relative occurrence of land verte-
brates in 30 · 30 km2 over this region (which We classified ENI species according to year (in
may represent general patterns of biodiversity, at some cases decade) of discovery in this region
least at large scales). The basal ENI species (for 33 species, this was unknown), lumping
region layer was given new sets of values for together species introduced prior to the 20th
temperature, precipitation etc. We then calcu- century. Of the 35 species in the latter category,
lated correlations between ENI species richness 31 belong to the ‘‘established widespread’’ cate-
and the various attributes. We checked for gory and only 4 to other ENI species categories
autocorrelation between various spatial corre- (see above). A higher proportion of species
lates. Later we conducted backwards stepwise introduced before the 20th century belong to
multiple regression between various spatial cor- the ‘‘established widespread’’ category when
relates and ENI species richness in the different compared to species introduced after the begin-
regions. ning of the 20th century (v2 = 14.7, P = 0.00012;
We also compared insect spatial patterns to Yates corrected v2 2*2 test).
the distribution of 34 recognized vegetation We compared intentional vs. unintentional
types of Israel (Zohary 1982). To estimate the introductions of insects during the first and
number of ENI insect species in the various second halves of the 20th century. A higher
vegetation types, we overlaid the map of the 34 proportion of species were intentionally intro-
vegetation types on the map of the 19 insect duced during the second half of the century than
regions, dividing Israel into a complete covering during the first half: 5 intentional out of 67
of smaller polygons, each consisting of part of introductions (7.5%) during the first half, as
an insect region and a vegetation type. The opposed to 27 out of 77 during the second half
number of species in each vegetation type was (35%) (v2 = 13.92, P = 0.00019; Yates corrected
calculated as the weighted average of the v2 2*2 test).
number of species in each component area. We looked at the trend in the number of
These vegetation types were later lumped and species discovered over the decades. However,
compared. theregressionbetweennumberofspecies discov-
In the vegetation type analysis and calculation ered and decade of discovery (1900–1999) was
of average vertebrate species in each insect zone, insignificant (r = 0.431; r2 = 0.186; P = 0.214).
we used a species–area relationship to estimate
species numbers in the different new polygons Taxonomy of ENI insects
created (using z = 0.26 in all calculations).
Table 1 shows the number of native and ENI
species by order. Total numbers of species in this
region (indigenous and non-indigenous) were
Results taken from Friedberg (1997). The orders shown
arethosewithatleastoneENIspeciesoratleast
Theentiredatabaseincludes414species,ofwhich 100 total representatives.
218belongtocategorieslabeledENIspecies(see We compared proportions of ENI insects to
above). We divided these 218 species into two theproportionoftotalinsectsfromthesixlargest
groups according to their status, to facilitate a native orders (Coleoptera, Diptera, Heteroptera,
search for patterns. The first group included Homoptera, Hymenoptera and Lepidoptera),
categories IV, V, and VI, insects currently finding a significant difference (v2 = 568.3,
spreading, established locally, and/or established P = 1.4E-120; v2 goodness of fit test); different
with unknown whereabouts—altogether 94 spe- orders showed different patterns (Table 1).
cies. The second group included category VII, The insect orders with the most ENI represen-
ENI species established and widespread in this tatives (Coleoptera, Diptera, Homoptera, Hyme-
region—124 species. noptera, Lepidoptera, and Thysanoptera) were
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BiolInvasions(2007)9:629–643 633
Table1 Numberofspeciesoftotal(afterFreidberg1997)andENIinsectsinIsraelfromdifferentorders
Order Total ENI v2 P-value Tendency
Coleoptera 3,000 38 1.66 0.2
Dermaptera 14 4
Dictyoptera 50 6
Diptera 3,320 10 33.5 7.1E-9 FewerENI
Heteroptera 700 0 10.1 0.0015 NoENI
Homoptera 700 86 501.6 4.4E-111 MoreENI
Hymenoptera 3,000 51 0.21 0.65
Lepidoptera 2,300 15 11.9 0.0005 FewerENI
Mallophaga 225 0
Neuroptera 180 0
Orthoptera 220 0
Thysanoptera 100 8
Total 13,809 218 568.3
Chi-squaredvaluesrepresentcomparisonsofproportionsofnativeandENIinsectgroups(seetext).Thetendencycolumn
showsifthedifferentproportionsarisefromhigherorlowerthanexpectednumbersofENIspecies
divided into two groups according to their cate- Samaria, Jordan Valley, Central Coastal Plain,
gories: ‘‘established widespread’’ and all other Southern Coastal Plain, Judean foothills, Judean
ENI categories (see above). We found significant Mountains, Judean Desert, Dead Sea area,
differences among the proportions of insects of NorthernNegev,CentralNegev,SouthernNegev,
the above orders from the ‘‘established wide- Arava Valley, Golan Heights and Mount Her-
spread’’ category (v2 = 28.9, P = 2.33E-05; v2 mon. Figure 1 shows the number of ENI species
goodness of fit test). However, only two orders in each region.
showed significant differences when the two
status categories were compared to each other Spatial analysis
within order (Yates corrected v2 goodness of fit
test). A higher proportion of insects from There is no significant correlation between the
the Homoptera were ‘‘established widespread’’ number of ENI species in a region and its area
when compared to other groups (v2 = 15.7, (r = –0.175; r2 = 0.031; P = 0.474). We compared
P = 7.5E-05).IntheHymenopteratheproportion several spatial features to the number of ENI
of ‘‘established widespread’’ species was lower species in the 19 different regions (Table 2).
than that of the other ENI status groups lumped Number of ENI species is negatively correlated
together (v2 = 138.4, P = 6.14E-32). with three measures of human land use: reserve
area, proportion of road-free area, and propor-
Insect distributions in this region tion of settlement-free area. These are positively
correlated with one another, significantly except
For 172 ENI species some information was for road-free area and reserve-free area, the
availableontheirlocaldistributioninthisregion. correlation of which approaches significance
However of these, 21 were referred to as being (P = 0.071). Number of ENI species is uncorre-
distributed ‘‘all over Israel,’’ and a further 28 as lated with all other variables (mean annual
being widely distributed, widespread, or informa- temperature, mean annual rainfall, and mean
tionabouttheirlocationwasinsufficientlyspecific number of land vertebrates in 30 x 30 km quad-
(i.e. from the north to the center of Israel). The rats in each region).
remaining 123 species had specific location data. We conducted a backwards stepwise multiple
For each of these, we noted the distribution regression, in which all spatial attributes were
according to the 19 insect regions of Fishelson compared to the number of ENI species in each
(1985): Upper Galilee, Lower Galilee, Northern region. Two variables remained significant, mean
Coastal Plain, Carmel Range, Yizrael Valley, annual rainfall (b = –0.46) and proportion of
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634 BiolInvasions(2007)9:629–643
road-free area (b = –1.0) (r = 0.827; r2 = 0.683;
P = 0.0001). The latter statistic is one of the
three negatively correlated with number of ENI
species.
Vegetation type and ENI insects
We estimated ENI insect richness in this area
(excluding the Golan Heights and Mt. Hermon)
as described above for the 34 vegetation zones
(Zohary 1982) (see internet database for the list
of zones and estimated ENI species numbers).
We lumped these vegetation types into six major
vegetation and soil types (see internet database
for the lumping principle). We then estimated
total average species number for these six types.
Figure 2 displays the average species number for
each of these six types and the total average. Of
the six major vegetation and soil types, Mediter-
ranean plains, coastal and internal sands, and
built-up areas had the greatest number of ENI
species, while Saharo-Sindian desert had very
few.
Fig.1 Number of ENI insect species in the different ENI insects’ spread in the region
regionsofIsraelanditsadjacentareas(classificationofthe
regionsbasedonFishelson1985)
Data on spread of 56 ENI insect species were
available. In some cases these data included
date independent variables plus number of ENI species,
Table2 Matrix of the correlations (upper triangle) and over the 19 regions (correlations significant at the 0.05
associated probabilities (lower triangle) among all candi- levelareunderlined)
Correlation r Num. of Average Average Average Reserve Road free Settlement
ENI vertebrates annual annual area area / total free area /
P- value species proportions temperature rainfall proportion area total
Num. of ENIspecies 0.218 -0.038 0.215 -0.583 -0.748 -0.684
Average vertebrates
proportions 0.370 -0.280 -0.008 -0.568 -0.133 -0.185
Average annual
temperature 0.877 0.245 -0.768 -0.059 0.296 0.312
Average annual
rainfall 0.377 0.974 1.24E-04 0.080 -0.647 -0.534
Reserve area
proportion 0.009 0.011 0.811 0.744 0.423 0.626
Road free area /
total area 2.34E-04 0.588 0.219 0.003 0.071 0.823
Settlement free area
/ total 1.24E-03 0.449 0.194 0.018 0.004 1.51E-05
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BiolInvasions(2007)9:629–643 635
Fig.2 Averagenumber Average established non-indigenous insects numbers in
ofENIspeciesindifferent
s the different vegetation zones of Israel and adjacentareas
vegetationzonesofIsrael. e
Dashedlineshowsthe ci 40
e
totalaveragespecies p
s
numberforthesezones of 30
r
e
b 20
m
u
n 10
e
g
ra 0
Ave Mediterraneanforest andmaquis Mediterraneanplains (batha) Saharo-sindian desert Built area Coastal andinternal sands Steppe &Irano-Turanianvegetation
Vegetation type zone
directions of spread and, in many, years of first throughtheWestBankandintoJordan(Ateyyat
sightings in various locations. These data were 2002).
grouped into several general spread patterns.
Half of these species (28) dispersed away from Original geographic range
the center of the Israeli coastal plain. These
species spread north and south along the Israeli An original geographic range was known for 132
coastal plain and in most cases also inwards ENI species. We divided these ranges into the
towardsboththeJudeanMountainsandnorthern mainbiogeographicregionsoftheworld(Wallace
valleys.EightspeciesreachedthewesternGalilee 1876), and, where data permitted, further into
either from overseas or from Lebanon, then sub-regions (European and circum-Mediterra-
spread from it—the northwestern tip of Israel—- nean distributions in the Palearctic region and
both east towards other parts of the north, and SouthAfricanoriginintheEthiopianregion).Six
south along the coastal plain. The other species species had a Paleotropical or simply Tropical
showed various other patterns of spread within range (Table 3). We compared the original geo-
Israel. Also noteworthy is the spread of three graphic ranges of ENI insects from different
parasitic wasp species from Israel’s coastal plain orders to those of all ENI insects (Table 3).
Table3 Native biogeographic ranges for all ENI insect species in this region for which native ranges are known, and
separatelyforthefivelargestorders
Nativegeographic Allspecies Coleoptera Diptera Homoptera Hymenoptera Lepidoptera
range
Tropical 4 2 0 1 0 1
Neotropical 12 1 1 7 0 1
Australian 9 4 0 2 3 0
Paleotropic 2 0 0 0 1 1
Oriental 31 5 0 11 10 3
Ethiopian 22 6 5 2 5 1
SouthAfrica 6 0 0 1 5 0
Nearctic 10 1 1 6 1 0
Palearctic 10 1 0 2 6 0
European 22 3 1 14 1 2
Circum-Mediterranean 4 2 0 2 0 0
Total 132 25 8 48 32 9
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636 BiolInvasions(2007)9:629–643
ENI insects from the three largest orders Feeding habits of ENI phytophagous insects
(Coleoptera, Homoptera and Hymenoptera) do
not arrive from the same biogeographic regions. For 42 ENI species data were available on their
There were significant differences between the feeding on native Israeli plants. These species
original geographic range proportions of insects havebeenfoundon56differentplantspecies(see
from these orders and those of all ENI species database for details), of which 19 (34%) are
(v2 = 20.1, P = 0.028; goodness of fit v2 test). To protectedbylaw.This proportionexceeds thatof
allow statistical procedures, we lumped some protected plant species out of all of the native
geographical regions (see internet database for Israeli species (269 species out of a total of
data used in this analysis and the lumped 2,138—Fragman et al. 1999) (v2 = 21.87,
biogeographical regions). Hymenopterans are P = 2.91E-6; Yates corrected 2*2 v2 test). How-
mostly of Oriental or Ethiopian origin, most ever, in a newly revised ‘‘red list’’ for Israeli
Homopterans come from the Palearctic or plants (Sapir et al. 2003, 2004), species are listed
Oriental regions, and beetles come from various according to various attributes of their rarity,
regions in the Old World. endemism etc. The proportion of plants that host
ENIinsectsandareontheredlistoutofallplants
used by ENI insects does not differ from that of
Means of introduction
total ‘‘red list species’’ out of all native Israeli
plants (6 of 56 plants used by ENI insects as
Thirty-eight of the 218 ENI species were im-
opposed to 370 of 2,138 for all native Israeli
portedintentionally(mostlyasnaturalenemiesof
plants; v2 = 1.30, P = 0.253; Yates corrected 2*2
pests). Of these, 34 are Hymenoptera (various
v2 test).
parasitic wasps), three are lady-beetles (Cocci-
Of plants hosting ENI species, the proportion
nellidae), and one is a parasitic fly. For the
of trees is an order of magnitude larger than that
majority of unintentional introductions the spe-
ofnativetreespeciesoutofallofregionalplants;
cific means of entry are unknown. Most probably
20 of the 56 species of plants used by ENI
theyhitchhikedonproduceorliveplants.Twelve
insects—35%—are trees, as opposed to 70 of
species were listed as imported with wood or
2,138—3.2% of wild trees out of all Israeli native
timber, and four species were presumably im-
plants (Waisel and Alon 1978, Fragman et al.
ported with stuffed animals for museum or
1999). Trees hosting ENI insects are also more
privatecollections. Seven ENI insects most likely
likely to be on the protected list than is expected
entered Israel from neighboring countries by
by chance for a plant used by ENI insects (15 of
range expansion.
20speciesoftreesasopposedto4of36forother
plants, v2 = 20.65, P = 5.52E-6; Yates corrected
Impact of ENI species 2*2 v2 test).
For the 71 species for which sufficient data
Seventy-nine of the 218 ENI species were were available (see database for details), we
described as ‘‘pests’’ in this region (by various classified the feeding habits of Israel’s phytoph-
sources) (see online database for details). These agousENIspeciesasmonophagous(twospecies),
are pests of agricultural produce, timber and oligophagous (feeding on 2–10 species from the
wood products, ornamental flowers and trees, same plant family; 19 species altogether), or
and stored food. Other species not categorized polyphagous (51 species altogether). We further
by the original sources as ‘‘pests’’ may inflict analyzed oligophagous and polyphagous insects
damage on commodities and agricultural pro- with respect to status, dividing them into two
duce. status groups, ‘‘established widespread’’ and all
We sought information regarding spread in other categories lumped together (see above).
other regions of the world of ENI species in this The oligophagous species’ proportions between
region. For 131 species we found such informa- thetwogroupsdidnotdifferfromthatofallENI
tion (listed in the database). species (v2 = 0.11, P = 0.74; Yates corrected 2*2
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BiolInvasions(2007)9:629–643 637
v2test),butpolyphagousspeciesdifferedfromall ‘‘introduced’’ (‘‘introduced butdid not establish’’
species in proportions in the different categories and ‘‘introduced with unknown fate’’).
(v2 = 13.78, P = 0.0002; Yates corrected 2*2 v2 Ofthe83speciesusedforthebiologicalcontrol
test).Polyphagousspeciestendedtobelongtothe agent analysis, 74 were imported intentionally
‘‘established widespread’’ category more than and 9 unintentionally. There was no significant
expected by chance. difference between the proportions introduced
Theproportionofpestspecies(seeabove)was intentionally and unintentionally in the ‘‘intro-
higher among polyphagous species than non-pest duced’’ and ‘‘established’’ categories (v2 = 0.001,
ENI species (32 of 79 pests are polyphagous, P = 0.97; Yates corrected 2*2 v2 test).
compared to 19 polyphagous species of 139 non- We divided the 43 species that established in
pests; v2 = 19.9, P = 8.3E-6; Yates corrected 2*2 Israelintotwogroups—‘‘establishedwidespread’’
v2test).Oligophagouspestsshowednosuchtrend and all the other status groups. Species used for
(11 of 79 pests are oligophagous, compared to 8 biologicalcontrolwerelesslikelytobelongtothe
oligophagous of 139 non-pests; v2 = 3.26, ‘‘establishedwidespread’’categorythantheother
P = 0.071; Yates corrected 2*2 v2 test). ENI species (v2 = 15.26, P = 9.35E-5; Yates cor-
rected 2*2 v2 test; see Table 4).
Biological control agents We tabulated biological control agents by
order. There were 20 beetles (Coleoptera), 1 fly
Ofthe414species listedinourdatabase,86were (Diptera), and 62 wasps (Hymenoptera). We
introduced as potential biological control agents. compared the proportion of beetles and wasps
Of these, 42 established populations and are that belong to the introduced and established
distributed among the various established cate- categories to the total proportions of biological
gories. Forty-one were introduced but are known controlagentsinthesecategories.Parasiticwasps
not to have established or their whereabouts are were more likely to establish and predaceous
unknown. Three more species are of unknown lady-beetles (Coccinellidae) less likely (v2 = 8.01,
status or are presumed native and were P = 0.0046; Yates corrected 2*2 v2 test).
withdrawn from further analyses (see Table 4).
We divided these species into two categories:
‘‘established’’ (all established categories) and Discussion
Insects are usually introduced unintentionally
(Simberloff 2003).Theyarefrequentlyinconspic-
Table4 Number of insect species that are potential bio- uous and overlooked by inspection measures (if
logical control agents, divided into the various status
these exist). Often many years can pass before
groups, with indication of intentional and unintentional
theyarediscovered.Thisneglectisalsoduetothe
introductions
fact that many regions lack extensive, ongoing
Statuscategories Intentional Unintentional Total
insectsurveysinthenaturalenvironment.Usually
Established an ENI species receives attention when it harms
Established, 27 1 28 human enterprises—agriculture, industry, for-
whereabouts estry, etc. Consequently, we have an incomplete
unknown
view of ENI insects.
Establishedlocally 2 0 2
Established 8 4 12
widespread Biases in the data
Introduced
Introducedunknown 20 4 24
Our database could be biased in several ways,
fate
Introduceddidnot 17 0 17 owing to information sources. All data on insect
established introductions since those of Bytinski-Salz (1966)
Possiblynative 1 have been compiled based on a great variety of
Unknown 2
sources. These differences could skew thedatain
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638 BiolInvasions(2007)9:629–643
several respects. Different taxonomic groups are Taxonomic affinity
represented differently among different publica-
tions. Temporal differences in the availability of There is taxonomic selectivity towards estab-
data are also possible; between the 1920 s and lishment of species belonging to particular
1967 the Golan Heights were inaccessible to orders (Table 1). There is a higher than
Israeliresearchersandbetween1948and1967the expected representation of Homoptera, mostly
West Bank and Gaza Strip were inaccessible. scale insect pests of agriculture, easily trans-
Another matter is that different sources ported with produce and difficult to detect.
emphasize different attributes of the various Established homopterans were also more wide-
species. In comparative analyses between spe- spread than other invaders. Other orders that
cies, insects from a particular source may be feature many ENI species were not over-
over- or under- represented simply because they represented when compared to the number of
have or lack a specific datum. Therefore, we species among all insects in the region. The
tried to have several sources of information for increase in the number of ENI species seen in
each species. This goal was not always satisfied; this region is gradual; the different orders do
obviously worldwide pests are discussed more not show sharp increases over the decades with
than insects found for the first time in a specific respect to each other (see also Sailer 1983,
location. Simberloff 1986).
Several of the Hymenoptera families estab-
Years of introduction lished in this region also had a higher than
expected rate of establishment in the USA
A few ENI species were introduced unintention- (Vazquez and Simberloff 2001). These families
ally prior to the twentieth century, some possibly of parasitic wasps are used worldwide as biolog-
in ancient times (Bytinski-Salz 1966). These ical control agents. Aphids of Aphididae (Ho-
include tramp ants, cockroaches, and parasites moptera) were also found to have a high rate of
and pollinators of plants. Species introduced successfulestablishmentintheUSA.Otherinsect
before the 20th century were more likely to be families from this order did not show such a
widespread in this region. This fact could result pattern in the USA. The Aphididae is the most
from unique attributes that enable these species species-rich family of ENI homopterans in this
to spread and establish in an anthropogenic region;manyofitsrepresentatives areworldwide
environment. Another possibility is that these agricultural pests.
species have simply had more time to spread and We compared different beetle families to
establish.Theycouldalsohavehadsufficienttime both native species numbers and the propensity
to evolve adaptations to enable their spread. We of these families to establish in the USA
do not see an increase in the number of ENI (Vazquez and Simberloff 2001). Several beetle
speciesdiscoveredinthisregionindecadesofthe families represented by many native species
20th century. have no or only a few ENI representatives in
Intentional introductions of insects, the this region. More ENI species are found in
majority of which were for biological control, families that are pests of produce or timber,
occurred mostly during the second half of the such as long-horn beetles (Cerambycidae), der-
20th century, although use of insects to combat mestid beetles (Dermestidae), branch and twig
each other in this region probably dates back at borers (Bostrichidae), and death-watch beetles
least to the Talmud period (70–500 AD) (Ku- (Anobiidae). Another family represented by
gler 1988). This increase could be attributed to several ENI species is the lady-beetles (Cocci-
intensification of agriculture in Israel, with the nellidae), imported as predators of insect pests.
use of various sophisticated methods. Also, Most of the above beetle families have also
growing concern about pesticides helped spur established in greater than expected propor-
increased interest in biological control (Ausher tions in the USA (Vazquez and Simberloff
1997). 2001).
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