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Assessment of potential non-target effects of Tetrastichus julis, a biological control agent of the cereal leaf beetle, Oulema melanopus

Authors:

Abstract

The cereal leaf beetle, Oulema melanopus (L.) (Coleoptera: Chrysomelidae), is an emerging pest of cereal crops in the Prairie Provinces of Canada. In other regions with a history of this pest, it is managed primarily through biological control with the parasitoid Tetrastichus julis (Walker) (Hymenoptera: Eulophidae). In this paper we report a study conducted during the summers of 2007 and 2008 in Pullman, Washington (USA), and 2010 and 2012 in Lethbridge, Alberta (Canada) assessing potential non-target effects of T. julis. The chrysomelid species tested included the following native and introduced species of leaf beetles (Chrysomelidae): Cassida azurea Fabricius, Chrysolina quadrigemina (Suffrian), Crioceris duodecimpunctata (L.), Deloyala guttata (Olivier), Galerucella calmariensis (L.), Gastrophysa cyanea Melsheimer, Gastrophysa polygoni L., Jonthonota nigripes (Olivier), Lema daturaphila Kogan& Geode, Leptinotarsa decemlineata (Say), Lilioceris lilii (Scopoli), and Xanthogaleruca luteola (Mu¨ ller) (Coleoptera: Chrysomelidae). Tetrastichus julis did not parasitize any of these potential non-target species. Thus the occurrence and relocation of T. julis in the Prairie Provinces of Canada and northwestern USA poses a relatively low risk to biodiversity.
Assessment of potential non-target effects of Tetrastichus
julis, a biological control agent of the cereal leaf beetle,
Oulema melanopus
Vincent A. D. Hervet .He
´ctor A. Ca
´rcamo .Lloyd M. Dosdall .
Terry D. Miller .Swaroop V. Kher
Received: 18 June 2015 / Accepted: 1 February 2016
ÓInternational Organization for Biological Control (IOBC) 2016
Abstract The cereal leaf beetle, Oulema melanopus
(L.) (Coleoptera: Chrysomelidae), is an emerging pest
of cereal crops in the Prairie Provinces of Canada. In
other regions with a history of this pest, it is managed
primarily through biological control with the para-
sitoid Tetrastichus julis (Walker) (Hymenoptera:
Eulophidae). In this paper we report a study conducted
during the summers of 2007 and 2008 in Pullman,
Washington (USA), and 2010 and 2012 in Lethbridge,
Alberta (Canada) assessing potential non-target
effects of T. julis. The chrysomelid species tested
included the following native and introduced species
of leaf beetles (Chrysomelidae): Cassida azurea
Fabricius, Chrysolina quadrigemina (Suffrian), Crio-
ceris duodecimpunctata (L.), Deloyala guttata (Oli-
vier), Galerucella calmariensis (L.), Gastrophysa
cyanea Melsheimer, Gastrophysa polygoni L., Jon-
thonota nigripes (Olivier), Lema daturaphila Kogan &
Geode, Leptinotarsa decemlineata (Say), Lilioceris
lilii (Scopoli), and Xanthogaleruca luteola (Mu
¨ller)
(Coleoptera: Chrysomelidae). Tetrastichus julis did
not parasitize any of these potential non-target species.
Thus the occurrence and relocation of T. julis in the
Prairie Provinces of Canada and northwestern USA
poses a relatively low risk to biodiversity.
Lloyd M. Dosdall—deceased.
Handling editor: Dirk Babendreier.
V. A. D. Hervet (&)
Institut Polytechnique LaSalle Beauvais, 19 rue Pierre
Waguet, 60000 Beauvais, France
e-mail: vincent.hervet@yahoo.fr
Present Address:
V. A. D. Hervet
Department of Biological Sciences, University of Lethbridge,
4401 University Drive, Lethbridge, AB T1K 3M4, Canada
H. A. Ca
´rcamo
Agriculture and Agri-Food Canada, 5403 – 1st Ave. S.,
Lethbridge, AB T1J 4B1, Canada
e-mail: hector.carcamo@agr.gc.ca
L. M. Dosdall S. V. Kher
Department of Agricultural, Food & Nutritional Science,
University of Alberta, 114 Street 89 Ave. NW, Edmonton,
AB P6G 2M7, Canada
e-mail: swaroop.kher@gov.ab.ca
Present Address:
S. V. Kher
Alberta Agriculture and Rural Development, 7000, 113 St.
NW, Edmonton, AB T6H 5T6, Canada
T. D. Miller
Aggrobiotic, 1854 Lexington Ave., Moscow, ID 83843, USA
e-mail: aggrobiotic@gmail.com
123
BioControl
DOI 10.1007/s10526-016-9722-7
Keywords Biological control Non-target study
Chrysomelidae Oulema melanopus Parasitoid
Tetrastichus julis
Introduction
The cereal leaf beetle, Oulema melanopus (Linnaeus)
(Coleoptera: Chrysomelidae), is a pest of small grains
native to Eurasia and North Africa (Haynes and Gage
1981; Olfert et al. 2004). It was first reported in North
America in 1962 in Michigan where it damaged cereal
crops, especially oat, Avena sativa L., and wheat,
Triticum spp. (Poaceae) (Manson and Boyce 1968).
Despite quarantine measures O. melanopus extended
its range north to Ontario and to the western USA (Bai
et al. 2006; Manson and Boyce 1968). It has been
reported that movements of farm machinery, Christ-
mas trees, fruits and plants contributed to the spread of
the beetle throughout the North American continent
(Dobesberger 2002; Haynes and Gage 1981). The
geographic range of O. melanopus continues to
expand in North America (Dosdall et al. 2011; Kher
2013). Between 1964 to 1970, releases of European
parasitoids were conducted in northeastern USA to
mitigate O. melanopus damage (Dysart et al. 1973;
Philips et al. 2011). The wasps released included
Diaparsis carinifer (Thomson), Diaparsis temporalis
Horstmann, Lemophagus curtus Townes (Hy-
menoptera: Ichneumonidae), Anaphes flavipes (Fo
¨r-
ster) (Hymenoptera: Mymaridae), and Tetrastichus
julis (Walker) (Hymenoptera: Eulophidae) (Dysart
et al. 1973; Haynes and Gage 1981). In the USA
Midwest, T. julis displayed high rates of parasitism
(Gage 1974; Haynes and Gage 1981; Maltby et al.
1971; Stehr 1970).
Tetrastichus julis is a larval endoparasitoid of
Chrysomelidae in the subfamily Criocerinae. It has
been reported from Oulema melanopus,Oulema
gallaeciana Heyden, and Lema cyanella (L.) (=punc-
ticollis (Curtis)) (Coleoptera: Chrysomelidae) (Noyes
2011). It may also have been reared from Oulema
duftschmidi (Redtenbecher) (Coleoptera: Chrysomel-
idae) (Graham 1991), which is a sibling species of
O. melanopus (Bezde
ˇk and Baselga 2015; Lopatin and
Nesterova 2005), but there is no definite evidence of
this. Only one study (Winiarska 1973) reports rearing
T. julis from L. cyanella. Unlike O. melanopus and
O. gallaeciana, which are grass feeders, L. cyanella
feeds on thistles in the genera Carduus, Cirsium, and
Silybum (Asteraceae) (White 1996). Winiarska (1973)
reports that in most cases T. julis reared from
L. cyanella were significantly larger than those reared
from O. melanopus and O. gallaeciana. Given this size
difference, the lack of other reports on this host
association, and the difference of host’s food, we
conclude that the parasitoids reared from L. cyanella
may not have been T. julis. We consider the two cereal
leaf beetles O. melanous and O. gallaeciana (Jelokova
´
and Gallo 2008; Miczulski 1973,1987) to be the only
reliably reported hosts of T. julis.
On the other hand, in the Palearctic there are five
sibling species in the Oulema melanopus group:
O. melanopus, O. duftschmidi, Oulema rufocyanea
(Suffrian), Oulema mauroi Bezde
ˇk & Baselga and
Oulema verae Bezde
ˇk & Baselga (Coleoptera:
Chrysomelidae) (Bezde
ˇk and Baselga 2015). The
taxonomic status of these species had remained
uncertain until now (Bezde
ˇk and Baselga 2015).
Therefore, previous reports of host associations of
O. melanopus with T. julis in the Palearctic may not
have been correct (Bouc
ˇek 1977; Domenichini 1966;
Graham 1991; Kostjukov 1978), especially in areas
where at least two of these sibling species occur
sympatrically. To confirm the identity of the
O. melanopus that we used in the present study, we
sent specimens used in the 2010 study to the Canadian
National Collection of Insects, Arachnids and Arthro-
pods (CNC), Ottawa, ON, Canada. The potential
occurrence of O. duftschmidi (the most similar species
to O. melanopus) in our sample was carefully inves-
tigated, and males’ flagella were examined. All
the males were confirmed to be O. melanopus.
Sequences of cytochrome c oxidase 1 (CO1) from
some of these specimens were placed in the Barcode of
Life Data Systems (BOLD) online (http://www.
boldsystems.org/) (CNCCB2392-11, CNCCB2393-
11, CNCCB2394-11, CNCCB2395-11, CNCCE1912-12).
Three other species have been reported as hosts for
T. julis:Lema lichenis Voet, Lema melanopa Lin-
naeus, and Cassida nebulosa Linnaeus (Coleoptera:
Chrysomelidae) (Noyes 2011). However, Lema liche-
nis is a synonym of Oulema gallaeciana,Oulema
melanopus was referred to as Lema melanopa in early
literature (Ninan et al. 1968), and Cassida nebulosa is
not actually a host of T. julis.TheC. nebulosa mistake
comes from a confusing paragraph on p. 235 of
V. A. D. Hervet et al.
123
Graham (1991). A careful reading of this paragraph
and p. 268 of this publication (Graham 1991) shows
that Tetrastichus clito (Walker) was misidentified as
T. julis by a previous author, and T. julis was never
actually reared from C. nebulosa.
Tetrastichus julis is considered an effective biolog-
ical control agent of O. melanopus in USA and Canada
(Ellis et al. 1988; Evans et al. 2006; Gage 1974;
Harcourt et al. 1984; Kher 2013; Logan et al. 1976;
Stehr 1970). Tetrastichus julis was first introduced in
Canada in 1976 in south-central Ontario (LeSage et al.
2007). It was also introduced in British Columbia in
2002 (Philip 2002). It was first reported in southern
Alberta in 2007 (Dosdall et al. 2011), when it was
reared from O. melanopus larvae. Tetrastichus julis
likely spread to Alberta from Montana where it has
been known since 1999 (Hammon and Peairs 2003).
This parasitoid is still being relocated to various
regions of North America where O. melanopus
appears without it (HC, unpublished data). Despite
the widespread and long history of using T. julis as a
biocontrol agent of O. melanopus, there is no
published record of its potential effects on non-target
Chrysomelidae. Therefore, our objective was to
determine if T. julis attacks selected non-target leaf
beetles that occur in the Prairie Provinces of Canada:
southern Alberta, Saskatchewan, and Manitoba, as
well as in Washington State (USA).
Materials and methods
Our approach to test the hypothesis that T. julis does
not attack a range of carefully selected potential non-
target leaf beetles relied on laboratory tests conducted
by two research groups (in Washington, USA, in 2007
and 2008, and in Lethbridge, Canada, in 2010 and
2012), and a field study done in the summer of 2012
near Lethbridge, Alberta.
Selection of potential non-target chrysomelid
species
Potential non-target chrysomelid species were
selected according to certain criteria. For the
2006–2008 studies these criteria were: (1) their
taxonomic relationship with the known hosts of
T. julis, and (2) their availability. For the 2010 and
2012 studies, potential non-target species were
selected using a methodology similar to the one
proposed by Kuhlmann et al. (2006). Species were
selected according to: (1) their taxonomic relationship
with the known hosts of T. julis, (2) their economic and
environmental significance (as native non-pest, inva-
sive or native pests, or biocontrol agents), (3) their
availability, and (4) in addition to the criteria proposed
by Kuhlmann et al. (2006) we also considered species
of Chrysomelidae that are parasitized by related
Tetrastichus species. For example, we chose Lilioceris
lilii (Scopoli) (Coleoptera: Chrysomelidae) because it
is attacked by Tetrastichus setifer Thomson (Hy-
menoptera: Eulophidae). Crioceris asparagi (L.)
(Coleoptera: Chrysomelidae) was not included in our
test, although it could be a potential host of T. julis.It
share a common parasitoid with T. julis (Noyes 2011)
and it has been reported from the Prairies Provinces of
Canada (Bousquet et al. 2013; LeSage 1991; Riley
et al. 2003). However, despite examination of over a
hundred asparagus plants, Asparagus officinalis L.
(Asparagaceae), in southern Alberta, examination of
museum material (CNC; Royal Saskatchewan
Museum (RSM), Regina, SK; Royal Alberta Museum
(RAM), Edmonton, AB; University of Alberta Strick-
land Museum (UASM), Edmonton, AB; and Agricul-
ture and Agri-Food Canada Lethbridge Research
Centre museum (AAFC-LRC), Lethbridge, AB,
Canada), and a literature research, we failed to confirm
the report of LeSage (LeSage 1991; LeSage et al.
2008) and we conclude that C. asparagi either doesn’t
occur or is not a common species in the Prairies
Provinces of Canada. Due to the relative lack of native
non-pest leaf beetles in the same subfamily (=Crio-
cerinae) of the known hosts of T. julis in the study area,
we also screened introduced weed biocontrol agents,
pest species, and various chrysomelid species fortu-
itously collected in the area (Table 1).
Source of insect material
Beetles were collected as adults either by hand or with
a sweep net in their natural environment. We inves-
tigated the following species during the 2006–2008
studies: Oulema melanopus (collected in Spokane
County, WA); Leptinotarsa decemlineata (Say)
(Coleoptera: Chrysomelidae) (Franklin County,
WA), which is a major pest of potatoes, Solanum
tuberosum (L.) (Solanaceae) worldwide; Xan-
thogaleruca luteola (Mu
¨ller) (Coleoptera:
Assessment of potential non-target effects of Tetrastichus julis
123
Table 1 Species selected to be tested with Tetrastichus julis, reasons for selecting them, and why some of them could not be tested
Selected species Reasons for selection Tested Comments
Cassida azurea Same genus as a ‘‘known host’
a
of T. julis.
Economic and environmental importance
(introduced for weed biocontrol)
Yes
Cassida rubuginosa Same genus as a ‘‘Known host’
a
of T. julis.
Economic and environmental importance
(introduced for weed biocontrol)
No We eventually decided to not look for this
species because larval stage of this
species (mid-August to end of May) do
not match with flight period of T. julis in
the study area (second half of June and
second half of July in southern Alberta,
VH personal observations). Flight
period of T. julis is two weeks earlier in
Utah (Evans et al. 2006)
Chrysolina hyperici or
C. quadrigemina
Economic and environmental importance
(introduced for weed biocontrol)
Yes Only C. quadrigemena was tested
Crioceris
duodecimpunctata
Same subfamily (Criocerinae) as known hosts of
T. julis. Parasitized by parasitoid in the same
genus as T. julis:T. crioceridis. Economic
importance (invasive pest)
Yes
Crioceris asparagi Same subfamily (Criocerinae) as known hosts of
T. julis. Share same parasitoid species with
known hosts of T. julis:Necremnus
leucarthros, and another parasitoid in the same
genus: T. coeruleus. Economically important
(invasive crop pest)
No We could not obtain this species
Deloyala guttata and
Jonthonota nigripes
Collected by chance in T. julis’ habitat. Same
tribe (Cassidini) as a ‘‘known host’
a
of T. julis.
Native non-pest
Yes Larvae of both species look similar. We
realized that the larvae were a mix of
both species only after the experiment
was over, when adults emerged
Any species in subfamily
Donaciinae
Close related subfamily to subfamily of known
hosts of T. julis (Criocerinae) (Go
´mez-Zurita
et al. 2008), native non-pest
No We could not find any
Galerucella calmariensis or
G. pusilla
Collected by chance in T. julis’ habitat.
Economic and environmental importance
(introduced for weed biocontrol)
Yes Only G. calmariensis was tested
Galerucella nymphaeae Share close related parasitoid with known hosts
of T. julis: aPediobius sp. Native non-pest
No We only collected two adults, which did
not lay eggs
Gastrophysa cyanea Collected by chance in T. julis habitat, native
non-pest, mainly considered weed biocontrol
agent
Yes
Gastrophysa polygoni Collected by chance in T. julis’ habitat. Invasive,
but mainly beneficial as biocontrol agent of
weeds. Adults have similar colorations as O.
melanopus
Yes
Lema daturaphila or
L. trivittata
Same subfamily (Criocerinae) as known hosts of
T. julis. Native, but economically important
(crop pest)
Yes Only L. daturaphila was tested
Leptinotarsa decemlineata Encountered by chance in T. julis’ habitat.
Economic importance (invasive crop pest)
Yes
Lilioceris lilii Same subfamily (Criocerinae) as known hosts of
T. julis. Parasitized by parasitoid in the same
genus as T. julis:T. setifer. Economic and
environmental importance (pest of ornamental
and native plants)
Yes
V. A. D. Hervet et al.
123
Chrysomelidae) (Thurston County, WA), an invasive
pest of elm trees, Ulmus spp. L. (Ulmaceae);
Chrysolina quadrigemina (Suffrian) (Coleoptera:
Chrysomelidae) (Whitman County, WA) has been
introduced in the North American continent as a
biological control agent against the St John’s wort,
Hypericum perforatum L. (Hypericaceae); Lema dat-
uraphila Kogan & Goeden (Coleoptera: Chrysomel-
idae) (Mesa County, CO), a native pest of potatoes,
tomatoes, Solanum lycopersicum L., and especially
tomatillos, Physalis philadelphica Lamarck (Solana-
ceae), in North America.
For the 2010 and 2012 studies, O. melanopus larvae
and adults were collected with sweep nets in grassy
ditches, a field of Bromus sp., and winter wheat fields,
Triticum spp. (Poaceae). Potential non-target species
studied were Lilioceris lilii (Scopoli) (Coleoptera:
Chrysomelidae) (Calgary, AB), which is an invasive
pest of ornamental and native lilies, Lilium spp. L.
(Liliaceae) in North America; Galerucella calmarien-
sis (Linnaeus) (Coleoptera: Chrysomelidae) (collected
near Ottawa, QC), which has been introduced for the
biological control of the invasive purple loosestrife,
Lythrum salicaria L. (Lythraceae), L. decemlineata
(collected near Vauxhall, AB); as well as all the
following species that have all been collected in
Lethbridge County, AB: Crioceris duodecimpunctata
(L.) (Coleoptera: Chrysomelidae), a native pest of
cultivated and ornamental asparagus; Gastrophysa
cyanea Melsheimer (Coleoptera: Chrysomelidae), a
native, rather beneficial insect that feeds on Polygo-
naceae; Gastrohhysa polygoni L. (Coleoptera:
Chrysomelidae) an adventive, but beneficial insect
that feeds on Polygonaceae (however considered a
minor pest when feeding on cultivated buckwheat,
Fagopyrun esculentum Moench); Cassida azurea
Fabricius (Coleoptera: Chrysomelidae), introduced
for the biological control of the bladder campion,
Silene vulgaris (Moench); Jonthonota nigripes (Oli-
vier) (Coleoptera: Chrysomelidae) and Deloyala gut-
tata (Olivier) (Coleoptera: Chrysomelidae), which are
two native insects that feed on Convolvulacea.
Laboratory conditions
During non-experimental periods, for the 2006-2008
studies the beetles and parasitoids were maintained in
a greenhouse in 60 960 960 cm BugDorm
TM
acrylic insect rearing tents at 35 % RH, 18–23 °C,
16:8 L:D cycle under metal halide lamps. For the 2010
and 2012 studies, the beetles were maintained in
BugDorm
TM
acrylic-mesh cages or in Plexiglas cages
ranging from 91.1 to 209.8 dm
3
. The chrysomelids
were maintained on live potted plants. The plants used
were those indicated in Tables 2,3and 4. Trials were
run in rearing rooms at 23 % RH, 12:12 L:D cycle
with fluorescent and incandescent lights, at 11–22 °C
(temperature was changed to either accelerate or slow
beetle development to synchronize it with that of the
parasitoid). Beetle larvae used in experiments were
reared from eggs obtained in the laboratory to ensure
that they were free of parasitoids. The only exceptions
were J. nigripes,D. guttata, and C. duodecimpunctata,
which were collected as larvae for practical reasons.
Two C. duodecimpunctata were parasitized by wild
parasitoids and were thus excluded from the results.
Tetrastichus julis were obtained by rearing field-
collected parasitized O. melanopus larvae until para-
sitoids emerged. Additional adult T. julis were
obtained directly from the field by sweeping winter
wheat and by using an open bucket baited with honey
and O. melanopus larvae on wheat plants. Parasitoids
Table 1 continued
Selected species Reasons for selection Tested Comments
Oulema palustris Same genus as known hosts of T. julis. Native
non pest
No Only a single specimen ever collected in
the prairie Provinces of Canada, in 1918
in Edmonton, AB. The species if
probably not common and we did not
find it
Xanthogaleruca luteola Encountered by chance in T. julis’ habitat.
Economic and environmental importance
(invasive tree pest)
Yes
a
We eventually discovered that the host record Cassida nebulosa was erroneous thus making it very unlikely that any Cassida sp.
could be a host of T. julis
Assessment of potential non-target effects of Tetrastichus julis
123
were overwintered in their host’s cocoons at 2.5 °C for
six months during the winter of 2006–2007,
2007–2008, and 2011–2012 to be used in the exper-
iments. For the 2006-2008 studies, parasitoids were
kept in a greenhouse in 60 960 960 cm Bug-
Dorm
TM
acrylic insect rearing tents at 35 % RH,
18–23 °C, 16:8 L:D cycle under metal halide lamps.
For the 2010 and 2012 studies the parasitoids were
kept in 0.21 m
3
acrylic BugDorm
TM
cages at 23 %
RH, 20 °C, 12:12 L:D cycle with fluorescent and
incandescent lights.
Assays
Below we provide details for each test, with the
numbers in parentheses corresponding with those
listed in Tables 2,3and 4. The tests presented below
have different designs because they were conducted
independently by three different main investigators.
Test # 1 and # 3 (2006–2008 assays) were conducted
by TM in a quarantine facility at Washington State
University, Pullman, WA. Test # 2 (2010 assays) was
conducted by VH, and tests # 4 and # 5 (2012 assays)
were conducted by HC, were both done at the
Lethbridge Research Centre of Agriculture and Agri-
Food Canada, Lethbridge, Alberta, Canada.
No-choice laboratory tests (tests # 1–2)
Test # 1 was conducted in June 2007. Assays were
conducted in 60 960 960 cm BugDorm
TM
acrylic
insect rearing tents, maintained in rearing rooms set at
20 °C, 50 % RH, 16:8 L:D cycle under 400 W metal
halide lamps. Host plants were grown in 10 cm
diameter pots in rearing cages. Naı
¨ve T. julis females
of the first generation, and about 2–3 day old, were
used in the experiment. Our observations showed that
it usually takes a few hours for female T. julis to start to
parasitize a host, thus we did not wait to witness
oviposition into hosts. Instead, we placed one T. julis
female with one potential host larva in a cage with
honey water as a food source for 48 h (=one replica-
tion). In this way, 25 female T. julis were exposed
individually to one larva of each of the four potential
host species (see Table 2), and another 25 female
T. julis (all chosen randomly from the same pool of
parasitoids) to O. melanopus larvae as a control. Host
larvae used were second to third instar of relatively
similar size. They were allowed to feed upon host
plant material in test cages before and during exposure
to T. julis.
After removal of the parasitoids and beetle larvae
from the test arenas, the beetle larvae remained on the
Table 2 Summary of results for the no-choice tests
Test
#
Test species (?host plants used to rear insects
during test)
Number of
replicates
N
a
% parasitized Total # T. julis
emerged
Replications
b
Larvae
1O. melanopus (Hordeum vulgare L.) (control) 25 25 100 100 (Not counted)
C. quadrigemina (Hypericum perforatum L.) 25 25 0 0 0
L. daturaphila (Physalis philadelphicus Lamarck) 25 25 0 0 0
L. decemlineata (Solanum tuberosum L.) 25 25 0 0 0
X. luteola (Ulmus pumila L.) 25 25 0 0 0
2O. melanopus (Triticum aestivum L.) (control) 24 54 46 39 88
C. duodecimpunctata (Asparagus officinalis L.) 8 18 0 0 0
G. calmariensis (Lythrum salicaria L.) 7 18 0 0 0
G. polygoni (Polygonum convolvulus L.) 4 7 0 0 0
L. decemlineata (Solanum tuberosum L.) 6 10 0 0 0
N is the total number of larvae tested per chrysomelid species. Results are in percent parasitized replications (=containers) and total
percent parasitized larvae for each chrysomelid species tested
a
Excluding individuals that died as larvae (for these we could not know what happened, but probable cause of death was either
diseases or maladapted laboratory conditions)
b
A positive ‘‘parasitized replication’’ is a container that contained at least one beetle larva parasitized with T. julis
V. A. D. Hervet et al.
123
host plant and were transferred to cages in the
greenhouse. After two weeks of feeding after expo-
sure to T. julis, the O. melanopus larvae were placed
into 7.4 ml vials with 75 % ethanol for storage until
dissection to allow us to observe the presence or
absence of parasitoid larvae. Because we did not have
experience finding parasitoid eggs within other
chrysomelid larvae and because we didn’t know if
T. julis eggs would be able to develop within other
chrysomelid species, the non-target chrysomelid
species were reared until pupation, which occurred
in the perlite substrate provided. Once the pupae had
been formed, the beetle’s pupal cells were sifted from
the substrate and placed individually in 7.4 ml vials
with 75 % ethanol until dissection.
Test # 2 was conducted during the summer of 2010
to test the ability of Tetrastichus julis to attack and
develop in non-target chrysomelid species collected in
southern Alberta. For each replication three chry-
somelid larvae (instars 2, 3, and 4) were confined
during 48 h with a naı
¨ve female T. julis (used in only
one replication), that was at least two days old and
mated, in a 460 ml white polyethylene container half
filled with fine, slightly moistened, vermiculite. A
piece of filter paper was placed on top of the
vermiculite. Small drops of honey and water as well
as plant foliage were placed in each container to feed
the parasitoids and beetle larvae. Small holes were
made on the lid of the containers. For each experi-
mental container with three larvae of a potential non-
target species (the experimental unit), a similar
container with three O. melanopus larvae was set up
simultaneously as control, using one female parasitoid
randomly chosen from the same cage. Chrysomelid
larvae exposed to T. julis were kept in their containers
until they completed development to adults or died.
Larvae that died were dissected right away to assess if
they contained parasitoids.
Choice tests (tests # 3–4)
Trials for test # 3 were conducted in June 2008 under
similar conditions as those for test # 1. Twenty-five
T. julis females were used for each non-target
chrysomelid species (Table 3). Individual female
wasps were introduced into testing arenas pairing a
larva of the three non-target species with one
O. melanopus larva. Potted host plants, each with
their respective test species of beetle were placed
together in testing cages. Similar to test # 1, host
Table 3 Summary of results for the choice tests
Test # Test species (?host plants used
to rear insects during test)
Number of
replicates
N
a
% parasitized Total # T. julis
emerged
Replications
b
Larvae
3O. melanopus (H. vulgare) (control) 25 25 92 92 (Not counted)
vs.
L. daturaphila (P. philadelphicus)25250 00
O. melanopus (H. vulgare) (control) 25 25 96 96 (Not counted)
vs.
L. decemlineata (S. tuberosum)2525000
O. melanopus (H. vulgare) (control) 25 25 100 100 (Not counted)
vs.
X. luteola (U. pumila) 0
4O. melanopus (Elymus repens (L.)) (control) 5 50 80 53 21
vs.
C. azurea (Silene vulgaris (Moench)) 5 38 0 0 0
N is the total number of larvae tested per chrysomelid species. Results are in percent parasitized replications (=containers for test # 3
and cages for test # 4) and total percent parasitized larvae for each chrysomelid species tested
a
Excluding individuals that died as larvae (for these we could not know what happened, but probable cause of death was either
diseases or maladapted laboratory conditions)
b
A positive ‘‘parasitized replication’’ is a container that contained at least one beetle larva parasitized with T. julis
Assessment of potential non-target effects of Tetrastichus julis
123
larvae used in testing were all second and third instar
and of relatively similar size, and allowed to feed upon
plant material in test cages 24 h before exposure to
T. julis. After wasp removal from the test cages,
O. melanopus larvae were allowed to feed for only two
weeks, while all other chrysomelid species were
reared until pupation. The O. melanopus larvae and
other species’ pupal cells were then placed in 7.4 ml
vials with 75 % ethanol until dissection.
Test # 4 was done on a patch of bladder campion,
Silene vulgaris (Moench) Garcke (Caryophyllaceae),
in the weed garden of the Agriculture and Agri-Food
Canada research centre near Lethbridge, Alberta,
Canada. Ten wire mesh cages (16 cm diameter,
30 cm tall) covered with a 0.20 mm acrylic mesh
were placed within the patch of bladder campion in
early July 2012. Each cage was placed in a location
that contained at least one bladder campion and five
tillers of quackgrass, Elymus repens (L.) (Poaceae).
Before placing the cages, all C. azurea adults and
larvae, and predatory arthropods were removed from
those areas.
In each cage, ten second to fourth instar O. melano-
pus larvae were placed onto the quackgrass and ten
C. azurea larvae were placed onto the bladder
campion. Four female T. julis previously exposed to
males were placed into five of these cages. The sides of
all cages were sprayed with a honey water solution to
feed the parasitoids. The remaining five cages without
T. julis served as controls. White paper towel covered
with a 2 cm layer of fine moist vermiculite was placed
on the ground of the cages to recover pupae. After
four days the chrysomelid larvae were brought to the
laboratory and individually reared as done for the
laboratory tests above.
Sequential choice test (test # 5)
For the 2012 trials, male and female parasitoids were
allowed at least 24 h to mate after their emergence and
females were kept 24 h alone prior to experiments.
Each replication consisted of one or two T. julis
females with three to ten potential non-target chry-
somelid larvae of a single species placed in a 240 ml
plastic container with the bottom lined with filter paper
and a corresponding control with O. melanopus larvae
(Table 4). A moist cotton ball, drops of honey, and
host plant foliage were placed in each container to feed
Table 4 Summary of results for the sequential choice test
Test # Test species (?host plants used to
rear insects during test)
Number of
replicates
N
a
% parasitized Total # T. julis
emerged
Replications
b
Larvae
5O. melanopus (Avena sativa L.) (control) 10 85 50 16 11
vs.
C. azurea (S. vulgaris)1099000
O. melanopus (A. sativa) (control) 5 19 20 5 6
vs.
G. cyanea (P. convolvulus) 5 19 0 0 0
O. melanopus (A. sativa) (control) 3 9 67 22 9
vs.
D. guttata mixed with J. nigripes
(*half and half) (P. convolvulus)
3150 00
O. melanopus (A. sativa) (control) 9 38 44 11 15
vs.
L. lilii (Lilium sp.) 9 52 0 0 0
N is the total number of larvae tested per chrysomelid species. Results are in percent parasitized replications (=containers) and total
percent parasitized larvae for each chrysomelid species tested
a
Excluding individuals that died as larvae (for these we could not know what happened, but probable cause of death was either
diseases or maladapted laboratory conditions)
b
A positive ‘‘parasitized replication’’ is a container that contained at least one beetle larva parasitized with T. julis
V. A. D. Hervet et al.
123
the parasitoids and the beetle larvae. Parasitoids were
left 24 h with either a potential non-target host or
O. melanopus larvae, then switched to the other
container for another 24 h. The order of exposure was
done randomly. This way the larvae of both control
and non-target test replications were exposed to the
same parasitoids. The chrysomelid larvae were reared
until death, parasitoid emergence, or metamorphosis
to adult.
Results
Tetrastichus julis did not parasitize any of the non-
target species during choice, no-choice, and sequential
choice tests (Tables 2,3,4). The chrysomelid larvae
that died during or shortly after exposure to T. julis
were excluded from the results as these were believed
to die from unknown factors other than parasitism by
T. julis. Although we rarely observed the action of the
adult T. julis parasitizing a chrysomelid larva, it was
only observed on O. melanopus larvae. Rearing of the
chrysomelidae and dissections revealed which larvae
were parasitized. For about 1/4 of the replications in
tests # 4 and # 5 the actual number of parasitized
O. melanopus larvae was not recorded, but only the
total number of T. julis recovered per container was
recorded. For these, we estimated the number of
parasitized O. melanopus larvae by using the average
number of T. julis per parasitized O. melanopus
larvae from the other replicates (n =51 parasitized
O. melanopus; mean =4.57 ±0.26 SE, min =1,
max =10 T. julis per larva).
For the no-choice tests (test # 1–2), seven potential
non-target species of Chrysomelidae were exposed to
Tetrastichus julis (Table 2). None of them produced
parasitoids whereas 100 % (test # 1) and 46 % (test
# 2) of the control replications contained parasitized
O. melanopus. For the choice tests (test # 3-4), five
species of potential non-target species of Chrysomel-
idae were tested (Table 3). None of them produced
parasitoids whereas between 80 % (test # 4) and
100 % (test # 3) of the control replications had
parasitized O. melanopus. In the sequential choice
test (test # 5), 5 potential non-target species of
Chrysomelidae were exposed to T. julis. None of
them produced parasitoids whereas 20 % to 67 %
of the control replications contained parasitized
O. melanopus.
Discussion
Results of our experiments show that T. julis did not
parasitize any of the Chrysomelidae exposed to it in
no-choice, choice, and sequential choice tests. Only
larvae of O. melanopus that we used as control were
parasitized. This shows that T. julis is unlikely to
parasitize any non-target species in the study area and
can be considered a safe biological control agent.
The only native species of Oulema in the study area
is Oulema (Hapsidolemoides)palustris (Blatchley)
(Coleoptera: Chrysomelidae). We found two speci-
mens of this species in the Strickland Museum of
the University of Alberta. The first specimen’s
labels indicated: ‘‘Minneapolis,/8.22.17 Minn./
F.C.Fletcher’’; ‘‘Swept ex./herbage in woods.’’ (col-
lection date must be 22 August 1917). The second
specimen’s label indicated: ‘‘Edmonton, Alta./
29.vi.1918/F.S. Carr’’. Both specimens were initially
identified as Lema brunnicollis Lacordaire. Specimens
were sent to the CNC where the identification was
corrected as Oulema palustris.Oulema palustris was
previously only documented in Que
´bec and Ontario in
Canada, and from 24 states in the eastern half of USA
(Riley et al. 2003; White 1993), making Minnesota its
new northeasternmost report in USA, and Alberta its
new westernmost report in Canada and on the
continent. Testing such a rare species remains a
challenge for this type of study, but given its host
plants (thistles) it is unlikely to be at risk from T. julis.
Another species in the subfamily Criocerinae, Lema
cyanella, is reported to occur in the Prairie Provinces
of Canada (Bousquet et al. 2013; Klimaszewski et al.
2010; Riley et al. 2003; Webster et al. 2012). Lema
cyanella was studied as a potential biological control
agent of Canada thistle, Cirsium arvense (L.) Scopoli
(Asteraceae) (McClay et al. 2001) in field cages in NB,
SK, and AB, and in an open field in AB, Canada,
during the 1980s and 1990s. Through a literature
review (Arnett Jr. et al. 2002; Finnamore 1984; Julien
and Griffiths 1998; Matsumura et al. 2011; Peschken
1984; White 1993,1996; Winston et al. 2014), from
personal communications with the authors of this
biological control program as well as with a CNC
taxonomist and a CNC technician (A.S. McClay, R.S.
Bourchier, H.B. Douglas, K. Savard), and because of
the absence of specimens from North America in
museums’ insect collections (CNC, RSM, RAM
UASM, AAFC-LRC, and the Smithsonian Institution
Assessment of potential non-target effects of Tetrastichus julis
123
National Museum of Natural History, Washington,
District of Columbia, USA), we conclude that Lema
cyanella does not occur in North America. Due to non-
target feeding of L. cyanella on native Cirsium spp. the
biocontrol program was discontinued and the beetle
eradicated. Lema daturaphila, Lema nigrovittata
(Gue
´rin-Me
´neville) and Lema trivittata Say (Coleop-
tera: Chrysomelidae) are three species that feed on
Solanaceae in the Nearctic. They are phylogenetically,
morphologically, and biologically very similar. In the
current study we found that L. daturaphila did not
appear to be a suitable host for T. julis. This suggests
that L. trilineata and L. nigrovittata are also not likely
to be suitable hosts.
Aside from the species already mentioned, there are
other species in the subfamily Criocerinae that occur
in the Nearctic. Some of them already share their range
with T. julis, i.e., Lema conjuncta Lacordaire,
L. melanofrons R. White, L. pubipes H. Clark,
L. solani Fabricius, Neolema cordata R. White,
N. jacobina (Linell), N. ovalis R. White, N. quadrigut-
tata R. White, N. sexpunctata (Olivier), Oulema
collaris (Say), O. cornuta (Fabricius), O. longipennis
(Linell), O. maculicollis (Lacordaire), O. sayi
(Crotch), O. simulans (Schaeffer), O. texana (Crotch)
(Coleoptera: Chrysomelidae). Other species occur
south of the known range of T. julis in USA, i.e.,
Lema balteata J. L. LeConte, L. confusa Chevrolat,
L. circumvittata H. Clark, L. maderensis R. White,
L. opulenta Harold, L. trabeata Lacordaire, Lilioceris
cheni Gressitt and Kimoto, Neolema dorsalis (Oli-
vier), N. ephippium (Lacordaire), N. gundlachiana
(Suffrian), Oulemaarizonae (Schaeffer), O. brunnicollis
(Lacordaire), O. concolor (J. L. LeConte), O. elongata
R. White, O. laticollis R. White, O. Margineimpressa
(Schaeffer), O. minuta R. White, O. variabilis R. White
(Coleoptera: Chrysomelidae).
Several factors suggest that both O. melanopus and
T. julis could eventually colonize the entire USA and
most of Canada. For example, in the Palearctic,
O. melanopus has been reported as far South as
Morocco, Iran, and Iraq (Bezde
ˇk and Baselga 2015)
(previous reports of O. melanopus at similar and more
southern latitudes are considered doubtful (Bezde
ˇk
and Baselga 2015)) and as far North as Finland
(Bezde
ˇk and Baselga 2015). In addition, it has already
been reported in high numbers in some southern states
of USA (Georgia and Alabama) (Buntin et al. 2004).
Tetrastichus julis has been reported as far south as
Madeira island (Graham 1991; Walker 1872) and as
far north as St. Petersburg (Kostjukov 1978). Because
development of T. julis’ has been shown to closely
match that of O. melanopus (Evans et al. 2006; Kher
2013) it is likely that T. julis will occur in the same
geographic range as O. melanopus. However, it is
unlikely that any North American Chrysomelidae
species will be at risk of T. julis attack because
O. melanopus and O. gallaeciana are the only reliable
known hosts of T. julis, and beside O. melanopus there
are no other species in the subgenus Oulema in the
Nearctic nor other Criocerinae that feed on Poaceae in
North America.
High host specificity and development synchrony
of Tetrastichus spp. on Criocerinae species has led to
their use in biological control programs in North
America. For example, Tetrastichus setifer has been
used against the lily leaf beetle, Lilioceris lilii
(Casagrande and Kenis 2004), Tetrastichus coeruleus
(Nees) (Hymenoptera: Eulophidae) has been used
against the common asparagus beetle, Crioceris
asparagi (Capinera and Lilly 1975a,b; Johansen
1957; Russell and Johnston 1912; van Alphen 1980),
and Tetrastichus crioceridis Graham (Hymenoptera:
Eulophidae) (Graham 1983) has been used against the
twelve-spotted asparagus beetle, Crioceris duodecim-
punctata (Hendrickson et al. 1991; van Alphen 1980).
These studies support the hypothesis that T. julis is
host specific and safe to other Chrysomelidae.
In a biological control context, high host specificity
is a desired character for a biological control agent
(Brodeur 2012). This is particularly important for
classical biological control programs as the introduced
species should not establish on native fauna and cause
a threat to the biodiversity in a region where it was
introduced (Brodeur 2012; Kuhlmann et al. 2006).
Environmental, economical, and ecological implica-
tions of host specificity determine the success of a
biocontrol agent and of the biological control program
(Brodeur 2012). In this context, the results of the
present investigation are relevant as they establish host
specificity of T. julis to O. melanopus and lack of non-
target effects in the study area. Prior studies have
discussed host specificity but there have not been any
systematic host range assessment studies for T. julis so
far. Reasons for successful establishment of T. julis in
North America include its host-tracking capacity, host
specificity, and high synchronization with the host
(Haynes and Gage 1981). Among these, high host
V. A. D. Hervet et al.
123
specificity for O. melanopus compared to other
introduced parasitoids may have provided relative
advantage to T. julis and resulted in consistent
performance and greater colonization of O. melanopus
infested areas in North America. Establishment of
Tetrastichus julis through targeted releases and relo-
cations can greatly contribute to sustainable manage-
ment of O. melanopus in western Canada and save the
farming industry significant expenses in pest control,
and avoid the negative impact of insecticides on local
fauna. In the current case of biological control of
O. melanopus with T. julis, the minor risk on non-
target species is outweighed by the benefits.
Acknowledgments For providing us with Chrysomelidae
specimens we thank Laurent LeSage, Ken Fry, Peter Mason,
Jacob Miall, Andrea Brauner, and Drusilla Pearson. For
technical support we thank Lacey Jones, Carolyn Herle, Tracy
Larson, Michaela Schmitke, Chelsea Durand, Stephanie
Behrens, and William van der Weide. For identification of
specimens we thank Laurent LeSage and Hume Douglas. For
other personal communications and checking museum
collections we thank Alec McClay, Rob Bourchier, Karine
Savard, Dave Larson, Cory Sheffield, Michael Gates, and Alex
Konstantinov. We thank Felix Sperling and Danny Shpeley for
sending specimens of O. palustris to the CNC. We thank Pat
Bouchard for CO1 barcodes of O. melanopus. We thank Karen
Mah for helping with the literature research. We thank Rose De
Clerck-Floate and Eva Pavlik for access to their plot of bladder
campion. This study was funded by Agriculture and Agri-Food
Canada—Ducks Unlimited (Developing Innovative Agri-
Products for Winter Wheat Initiatives), by the Washington
Wheat Commission, and by a grant awarded to LD by the
Alberta Crop Industry Development Fund. This is Lethbridge
Research Centre Scientific Contribution No. 387-15027.
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Vincent A. D. Hervet worked on this project as part of his
studies at the Institut Polytechnique LaSalle Beauvais, Beau-
vais, France. He is currently a doctoral student at the
University of Lethbridge, Lethbridge, AB, Canada, studying
the ecology of hymenopteran parasitoids of cutworms
(Noctuidae).
He
´ctor A. Ca
´rcamo is an Integrated Pest Management (IPM)
scientist who leads the IPM laboratory at the Lethbridge
Research Centre (Agriculture and Agri-Food Canada), Leth-
bridge, AB, Canada.
Lloyd M. Dosdall now deceased, was a professor in IPM at the
University of Alberta, Edmonton, AB, Canada.
Terry D. Miller is an agro-ecological consultant with Agro-
biotic specializing in IPM, natural enemy production and
habitat modification to enhance biological controls in organic
and conventional cropping systems. He works at the Northwest
Biological Control Insectary and Quarantine (NWBIQ) at the
Washington State University, Pullman, WA, USA.
Swaroop V. Kher currently works at Alberta Agriculture and
Rural Development, Edmonton, AB, Canada. He was a part of
the project investigating sustainable management options for
the management of the cereal leaf beetle in western Canada as
part of his doctoral thesis at the University of Alberta.
Assessment of potential non-target effects of Tetrastichus julis
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... In 2014, 235 CLB larvae were reared from subsets of 10 random individuals from each field, and only T. julis (n = 457) emerged. Thus parasitism assessed by dissections of CLB larvae was attributed to this species as observed in previous studies from this region (Kher et al. 2014;Hervet et al. 2016). ...
... Because the impact of T. julis on CLB larval abundance happens the following year (i.e., parasitism does not decrease CLB abundance until the next generation), we hypothesize that this negative association is due to landscape-scale carryover effects Table 1 (model 9) for statistical details of T. julis on CLB populations from previous years. The success of this parasitoid has been linked to its high specificity to CLB (Hervet et al. 2016), and high dispersal ability which resulted in no colonization lag between newly and previously planted wheat fields in disturbed agricultural landscapes (Evans et al. 2015). We conclude that CLB parasitism by T. julis has strong negative effects on CLB abundance in agricultural landscapes in southern Alberta. ...
... The contrasting findings between Grab et al. (2018) and this study may be due to the parasitoid host specificity. While T. julis only attacks CLB (Hervet et al. 2016), P. digoneutis can attack several species of Lygus and therefore has a wider range of accepted hosts (Mason et al. 2011), which enables this species to exploit resources and alternative hosts from semi-natural habitats. The presence of CLB in high numbers in cereal fields (particularly in 2014) might have reduced T. julis searching time and increased parasitism (Stiling 1987). ...
Article
Full-text available
ContextLandscape complexity affects herbivores in agroecosystems, but consequences on pest control services are variable. Carryover effects of landscape composition in previous years on herbivore control may be important, but have been seldom assessed. Understanding landscape complexity effects at different temporal and spatial scales is important to improve sustainable pest control services.Objectives We examined the effect of agricultural landscape complexity (e.g., the percentage of semi-natural habitats) on cereal leaf beetle (CLB), Oulema melanopus L., and its parasitism by Tetrastichus julis (Walker).Methods From 2014 to 2015, we assessed CLB abundance and parasitism in 54 fields along a gradient of landscape complexity (2–70% of semi-natural habitats) in southern Alberta. We used generalized linear models to test the effects of percentage of crops and semi-natural habitats, and landscape and crop diversity on CLB abundance and parasitism at 0.5, 1, 1.5 and 2 km spatial scales.ResultsCLB abundance decreased with higher crop diversity at the 0.5 km scale and increased with CLB host crops in the current and previous years at multiple scales, supporting the resource concentration hypothesis. CLB parasitism increased with CLB abundance and in landscapes with increased canola and alfalfa during a year of low CLB abundance. CLB abundance had contrasting associations with semi-natural habitats: positive with woodlands and negative with pastures.Conclusions Our study suggests that crop diversity reduces the abundance of this specialist pest in agricultural landscapes likely by a dual effect of reducing host crop area and increasing habitats with resources for parasitoids.
... Tetrastichus julis, a multivoltine gregarious larval endo-parasitoid from Europe was introduced in Michigan in 1967. Tetrastichus julis has high host specificity and only attacks CLB (Hervet et al., 2016). By 1972, the establishment of T. julis was confirmed in 18 counties of Michigan, showing the expansion of its range to new CLB infested areas (Logan et al., 1976). ...
... Because the impact of T. julis on CLB larval abundance happens the following year (i.e., parasitism does not decrease CLB abundance until the next generation), I hypothesize that this negative association is due to landscape-scale carryover effects of T. julis on CLB populations from previous years. The success of this parasitoid has been linked to its high specificity to CLB (Hervet et al., 2016), and high dispersal ability which resulted in no colonization lag between newly and previously planted wheat fields in disturbed agricultural landscapes (Evans et al., 2015). I conclude that CLB parasitism by T. ...
... The contrasting findings between Grab et al. (2018) and this study may be due to the parasitoid host specificity. While T. julis only attack CLB (Hervet et al., 2016), P. digoneutis can attack several species of Lygus and therefore have a wider range of accepted hosts (Mason et al., 2011), which enable the species to exploit resources and alternative hosts from semi-natural habitats. The presence of CLB in high numbers in cereal fields might have reduced T. julis searching time and increase parasitism (Stiling, 1987). ...
Thesis
Full-text available
In recent years, the cereal leaf beetle (CLB) Oulema melanopus (Coleoptera: Chrysomelidae), an important pest of wheat, barley, and oat throughout the world, has become a serious pest of cereal crops in Western Canada. Following CLB invasion, Tetrastichus julis (Hymenoptera: Eulophidae), the most efficient larval parasitoid of CLB, was introduced into the Canadian Prairies. I investigated the effect of landscape complexity, ranging from high (semi-natural habitats > 50%) to low (semi-natural habitats < 30%) on the abundance of CLB and its parasitism in southern Alberta. Cereal leaf beetle abundance and the parasitism rate of T. julis responded positively to the proportion of CLB major hosts (wheat and barley) in the current and previous years at various spatial scales (0.5 to 2 km). Landscape diversity was negatively associated with CLB abundance. Cereal leaf beetle parasitism increased when there was a higher proportion of canola and alfalfa in the landscape. Cereal leaf beetle parasitism also positively responded to CLB abundance in cereal fields, indicating a density-dependent response. Overall, I concluded that diversification of crops and semi-natural habitats in the surrounding landscape are an important factor to reduce CLB numbers in the Canadian Prairies. Laboratory and field predation trials revealed for the first time the contribution of various predators to CLB control. Several species of Hippodamia (Coleoptera: Coccinellidae), carabids (Coleoptera: Carabidae) and nabid bugs (Hemiptera: Nabidae) were among the best predators of CLB immature stages under laboratory conditions, that also included Coccinella septempunctata (Coleoptera: Coccinellidae) and Staphylinidae. I found an average 24.5% of predation on sentinel eggs in wheat fields in 24 h trials. I developed a set of species-specific primers to detect CLB DNA in the gut content of generalist predators, which confirmed that Nabis americoferus and several Hippodamia species are the most promising predators of CLB in wheat. Nabis americoferus was the most abundant predator in the Lethbridge area and had 0.35 proportion positives for CLB DNA. Altogether, the predation studies highlight the importance of predators in CLB control, which has been neglected to date but can have important roles in sustainable pest management programs for CLB in cereal crops.
... We further examine olfactory cues involved in the host-finding behaviour of the principal parasitoid of the beetle, Tetrastichus julis (Hymenoptera: Eulophidae), which is a highly host-specific larval endoparasitoid of O. melanopus (Hervet et al. 2016). T. julis is a successful classical biological control agent that has contributed to management of O. melanopus in North America (Gage and Haynes 1975;Harcourt et al. 1977;Haynes and Gage 1981;Philips et al. 2011); its success is attributed to its gregariousness, host specificity, high synchronization with the host and capacity to track its host as the geographic range of the host expands (Haynes and Gage 1981;Evans et al. 2006;Kher et al. 2011;Philips et al. 2011). ...
Article
Behavioural responses to the host-associated olfactory cues have not been completely understood for the cereal leaf beetle, Oulema melanopus, and its principal parasitoid, Tetrastichus julis. We, therefore, investigated the role of olfactory cues in the host-finding behaviour of these species using olfactory bioassays. Behavioural responses of O. melanopus to odours emanating from intact host plants (wheat, oat, barley) vs. a clean-air control were tested using multichoice and two-choice bioassays. For T. julis, responses of naïve and experienced adult female wasps to odours associated with the faecal coat of O. melanopus larvae were measured under multichoice and two-choice conditions. Our results indicate that olfactory cues are involved in the host-finding behaviour of both O. melanopus and T. julis. Olfactory responses of O. melanopus were influenced by the sex of the beetle and the physiological stage of adults (reproductively active vs. in reproductive diapause). Females respond to olfactory cues in greater proportions than males, and reproductively active, overwintered adults show greater responsiveness than teneral adults in reproductive diapause. Behavioural responses to cues emanating from different crop species were different in multichoice bioassays but not in two-choice bioassays. Further, we report for the first time that the olfactory cues associated with the faecal coat of O. melanopus evoke host-finding behaviour of its parasitoid, T. julis. Naïve female wasps are more likely to use these cues to locate the potential host than experienced females. The results of this investigation provide insights into host finding by both the species and the nature of behavioural response brought about by olfactory stimuli, and the results can help to design strategies to improve parasitoid activity by enhancing the crop environment to generate cues for host finding and to manage O. melanopus populations.
Article
Full-text available
Five species of the Oulema melanopus group are recognized in the western Palaearctic Region: O. melanopus (Linnaeus, 1758), O. rufocyanea (Suffrian, 1847), O. duftschmidi (Redtenbacher, 1874), O. mauroi sp. nov. (northern Italy), and O. verae sp. nov. (Spain and Portugal). The two new species are described and illustrated. The nomenclature of the group is discussed in detail. Oulema rufocyanea is proved to be a validly described species different to O. duftschmidi. To fi x the nomenclatural stability of the whole group and avoid subsequent misintepretations, neotypes are designated for Crioceris melanopoda O. F. Müller, 1776; Crioceris hordei Geoffroy, 1785; and Lema cyanella var. atrata Waltl, 1835 (all conspecifi c with O. melanopus). The primary type specimens or their photographs were examined if they exist. The spelling Oulema melanopus is fixed as correct and explained. Variation in the cytochrome c oxidase (cox1) gene across specimens of all the species has been analysed. All species in the group had extremely similar haplotypes, with interspecifi c sequence similarities between 90.5–99.5 %, compared to intraspecifi c sequence similarities between 91.6–100 %. As a result, the phylogenetic relationships among species in the group were not well resolved based on cox1 sequences.
Article
Full-text available
All 8237 species-group taxa of Coleoptera known to occur in Canada and Alaska are recorded by province/territory or state, along with their author(s) and year of publication, in a classification framework. Only presence of taxa in each Canadian province or territory and Alaska is noted. Labrador is considered a distinct geographical entity. Adventive and Holarctic species-group taxa are indicated. References to pertinent identification keys are given under the corresponding supraspecific taxa in the data archive.
Chapter
This book summarizes the biological control programmes in Canada since 1981. The book includes three chapters on the relationships of invasive species, pesticides and taxonomy to biological control, and contains sections on insects and mites (55 chapters, including crop pests, forest pests, public health pests and livestock pests), weeds (25 chapters), and pathogens (19 chapters). Some emphasis is given on pathogens and nematodes either as targets for control or as biological control agents acting directly as hyperparasites or pathogens, or indirectly as antagonists competing successfully for the same resources as the target pest. Appendices provide details of noteworthy publications on biological control from 1981-2000 and Canadian suppliers of biological control organisms .
Chapter
Pronotum broader than head; shape subquadrate, excavated in front for reception of head, angles borders strongly margined laterally; surface smooth or punctate; pleural region broad; prosternum broad in front of coxae with intercoxal process broad; procoxal cavities closed behind. Mesosternum subquadrate to transversely subrectangular; mesepimeron not reaching coxae; mesocoxal cavities closed behind. Metasternum somewhat wider than long in most. Legs with trochantins hidden; procoxae flat, globular, separate; mesocoxae globular separate; metacoxae triangular, separate; trochanters triangular, inter-stitial; femora weakly swollen; tibiae flattened, carinate, apically enlarged and with small apical spurs; tarsal formula 5-5-5, fourth tarsomere small in many, first three tarsomeres more or less broad and pubescent beneath; claws simple. Scutellum subcordate to pentagonal. Elytra entire, apically rounded; striae punctate, or surface smooth; intervals sparsely punctulate, a few smooth or confusedly punctate with large black impressions or small punctures; epipleural fold well developed. Wing has a dark, medial fleck (shagreened oval spot) near distal edge; two closed cells occur, an elongate wedge cell and a triangular radial cell; five veins nearly reach the hind edge of the wing; folding pattern with median area normal; anal lobe sessile.
Article
Fourteen parasitic species of Chalcidoidea and Ichneumonidae were associated with Oulema melanopus and O. gallaeciana, Tetrastichus julis, Diaparsis carinifer and Lemophagus curtus as obligatory larval parasites of both hosts, and Eupteromalus micropterus as a single obligatory parasite of pupal cells of O. gallaeciana. Peak larval parasitism densities, parasitism percentages and host relations are discussed. Fungal infections of pupal cells of O. gallaeciana are recorded. -from Author
Article
Cereal leaf beetles are serious animal pests of crops in many areas of western and eastern Slovakia. Research was carried out in these areas in order to receive knowledge on occurrence of natural enemies of Oulema gallaeciana. We were detecting particular species of parasitoids parasitising Oulema gallaeciana and their spreading in particular area. The results showed that dominant parasitoid was Necremnus leucarthros. Other parasitoids with bigger proportion on parasitisation were Pteromalus vibulenus and Diplazon spp. with parasitisation up to 30%. In respect of significant parasitisation of Oulema gallaeciana by parasitoid Necremnus leucarthros, it would be appropriate to use this species for biological control of cereal leaf beetle.
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Increases in international trade combined with the undeniable effects of global warming have led, and continue to lead, to significant changes in species composition on the planet. Comprehensive species checklists represent valuable tools to assess biodiversity patterns and monitor distributional changes over time. Here we report the distribution for all 8238 species-group taxa of Coleoptera known to occur in Canada and Alaska. From west to east, the number of species-group taxa are 1448 (Alaska), 1041 (Yukon Territory), 1115 (Northern Territory), 123 (Nunavut), 3932 (British Columbia), 2863 (Alberta), 2353 (Saskatchewan), 2679 (Manitoba), 4513 (Ontario), 4127 (Quebec), 2704 (New Brunswick), 2286 (Nova Scotia), 899 (Prince Edward Island), 501 (Labrador) and 1099 (Newfoundland). We document the presence of 393 Holarctic and 629 established adventive species-group taxa. The five most diverse families in the region are Staphylinidae (1682 species), Carabidae (989 species), Curculionidae (823 species), Chrysomelidae (598 species) and Elateridae (386 species). The valid scientific name, including author names and year of publication, is given for each species-group taxon. The classification follows current knowledge about the relationships of beetles down to the rank of subfamily. Tribes, subtribes, genera, subgenera and species-group taxa are listed alphabetically. References to pertinent identification keys are given under the corresponding supraspecific taxa. The first edition of the Checklist of beetles of Canada and Alaska was published in 1991. Based on our results, we have added over 800 species to the fauna of the region over the last 20 years, 20% of which are adventive species.