Download Generalist Predators (Coleoptera: Carabidae, Staphylinidae

Generalist Predators (Coleoptera: Carabidae, Staphylinidae)
Associated with Millipede Populations in Sweet Potato and Carrot
Fields and Implications for Millipede Management
Author(s): Adam J. Brunke, Christine A. Bahlai, Mark K. Sears, and Rebecca H.
Hallett
Source: Environmental Entomology, 38(4):1106-1116. 2009.
Published By: Entomological Society of America
DOI: 10.1603/022.038.0418
URL: http://www.bioone.org/doi/full/10.1603/022.038.0418
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BIOLOGICAL CONTROLÑPARASITOIDS AND PREDATORS
Generalist Predators (Coleoptera: Carabidae, Staphylinidae) Associated
With Millipede Populations in Sweet Potato and Carrot Fields and
Implications for Millipede Management
ADAM J. BRUNKE, CHRISTINE A. BAHLAI, MARK K. SEARS,
AND
REBECCA H. HALLETT1
Department of Environmental Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Environ. Entomol. 38(4): 1106Ð1116 (2009)
ABSTRACT The predatory beetle assemblage of Ontario carrot and sweet potato Þelds was described and assessed to identify species of interest to the control of the emerging pest millipede
Cylindroiulus caeruleocinctus (Wood) (Diplopoda: Julidae). Pterostichus melanarius (Coleoptera:
Carabidae) was identiÞed as a dominant species, and seven other carabid species [Pterostichus
melanarius (Illiger), Harpalus pensylvanicus (DeGeer), Ophonus puncticeps (Stephens), H. erraticus
Say, Bembidion quadrimaculatum oppositum Say, Poecilus chalcites (Say), Scarites subterraneus Fabricius, and Pterostichus permundus (Say)] were identiÞed as common species on the basis of activity
density. Common species became more abundant as the growing season progressed. In laboratory
bioassays, P. melanarius preyed on millipedes regardless of prey size, whereas H. erraticus never
selected millipedes as prey. A signiÞcant positive spatiotemporal relationship was found between P.
melanarius and C. caeruleocinctus in sweet potato Þelds. P. melanarius was found to be a natural enemy
of C. caeruleocinctus, and other common carabid species warrant future study. The role of Staphylinidae in millipede control could not be elucidated, likely because of low trapping efÞciency. Tachinus
corticinus Gravenhorst, an introduced staphylinid from Europe, was newly recorded in Ontario,
extending its North American range considerably westward from the province of Quebec. The results
of this study are an important foundational step toward developing a successful integrated pest
management strategy for controlling millipede damage in crops.
KEY WORDS Cylindroiulus caeruleocinctus, Pterostichus melanarius, integrated pest management
Julid millipedes (Diplopoda: Julidae) are most typically known for their beneÞcial role as key decomposers of organic matter, contributing to soil health
(Coleman et al. 2004). Recently in Ontario, millipedes
have been implicated as the causal agents of root
damage to corn, Zea mays L., and several root crops
including ginseng, Panax ginseng C. A. Mey., sweet
potato, Ipomoea batatas L. Lam., and carrot, Daucus
carota L. (Allen and Filotas 2008a). Millipedes in the
family Odontopygidae are well known in African
countries as agricultural pests of sweet potato (Ebregt
et al. 2005). Carrot and sweet potato yield loss caused
by suspected millipede herbivory was recently addressed in Ontario, Canada (Allen and Filotas 2008a,b;
Sears et al., unpublished data). That study identiÞed
the common European millipede Cylindroiulus caeruleocinctus (Wood) (family Julidae) as the most abundant species in these agroecosystems and showed that
it is capable of causing damage to carrot and sweet
potatoes. The study concluded that this species has
potential to be a pest of these vegetables.
The natural predator complex within the carrot
agroecosystem in northeastern North America is rel1
Corresponding author, e-mail: [email protected].
atively well known (Baines et al. 1990, Boivin 1999).
The sweet potato agroecosystem in North America is
less studied, and research has been limited to studies
conducted in the southeastern United States (Chalfant et al. 1990). Sweet potato has been increasing in
acreage and importance in Ontario (OMAFRA 2008)
and the northeastern United States (USSPC 2008) in
recent years, and several pests have been recognized
(OMAFRA 2008). Information about the composition
of the arthropod community inhabiting the sweet potato agroecosystem in northeastern North America,
including natural enemies of pest species, is critical to
proper pest management.
There are currently no registered pesticides or integrated pest management (IPM) strategies in place
for millipede control in Ontario, and thus, there is a
need to understand millipede ecology, especially their
natural enemies. Cylindroiulus caeruleocinctus has a
well-armored body and possesses defensive benzoquinones (Jacobson 1966); consequently, millipedes are
widely known as unpalatable to many predators
(Baker 1985). North American predators that specialize on millipedes are not known to occur in eastern
agricultural Þelds, although they occur elsewhere as
the western carabid genus Promecognathus Chaudoir
0046-225X/09/1106Ð1116$04.00/0 䉷 2009 Entomological Society of America
August 2009
BRUNKE ET AL.: GENERALIST PREDATORS AND MILLIPEDE MANAGEMENT
(Arnett and Thomas 2001) and as the rare forest beetle
genus Phengodes Illiger (Arnett et al. 2002). Therefore,
it is the generalist guild of predators that is of interest
to millipede management and the focus of this study.
Generalist predatory beetles from the families Carabidae (ground beetles) and Staphylinidae (rove beetles) occur in many agroecosystems (Sunderland
2002) and include species that are known to accept
millipede prey in laboratory settings (Snider 1984,
Baker 1985). Baker (1985) worked with Australian
carabids not known from Ontario, whereas Snider
(1984) studied species typical of a Michigan forest.
Both of these studies concerned close relatives of
species known from agricultural Þelds. We hypothesized that one or more generalist predatory beetle
species have the potential to be important to the management of millipede (C. caeruleocinctus) populations
through natural predation in carrot and sweet potato
Þelds. The objectives of this study were therefore to
(1) examine the biodiversity of predatory beetle species and determine the common members of the generalist predatory beetle guild in carrot and sweet potato Þelds; (2) determine the temporal distributions of
these common species; (3) evaluate the ability of
select common beetles to consume millipedes as prey;
and (4) assess spatial and temporal associations between identiÞed millipede predators and C. caeruleocinctus.
Materials and Methods
Species Richness and Temporal Distributions of
Predatory Beetles. Three carrot (C, G, and P) and
three sweet potato Þelds (CSP, GSP, and LSP) in
southern Ontario were sampled every other week,
over 7 d, in the summer of 2007. Site G was located
near Glencoe (42⬚44⬘47⬙ N, 81⬚42⬘32⬙ W), and sites C
and P were located near Chatham (42⬚24⬘43⬙ N,
82⬚11⬘6⬙ W). Site LSP was near West Lorne (42⬚36⬘13⬙
N, 81⬚36⬘24⬙ W), and sites CSP and GSP were near
Blenheim (42⬚20⬘8⬙ N, 81⬚59⬘50⬙ W). The year previously, carrot sites C and G were planted to corn, and
site P was planted to tomatoes. Sweet potato sites were
planted in 2006 to tobacco (CSP), soybean (GSP), and
winter wheat (LSP). All sites were irrigated as needed
except for carrot site G, which was without a water
source.
Soil types were determined by hand texture analysis
to be very sandy loam for carrot sites P and C and
sandy loam for carrot site G. Soil types at the sweet
potato sites were sandy loam for sites LSP and CSP and
loam for site GSP. Dry organic matter contents of soils
for each site were as follows: G, 2.9 ⫾ 0.17%; C, 5.2 ⫾
0.96%; P, 26.8 ⫾ 1.45%; LSP, 3.5 ⫾ 0.1%; CSP, 3.17 ⫾
0.07%; and GSP, 2.37 ⫾ 0.09. Of the sites sampled,
insecticides were applied only at site G (broad-spectrum insecticide applied twice in June).
Carrot sites G and P were sampled from 23 May to
4 September and site C from 29 May to 4 September.
All sweet potato sites were sampled from 20 June to 31
August. Sampling was conducted in three transects
per Þeld, with each transect in carrot Þelds corre-
1107
sponding to rows that were 1, 15, and 30 m from a Þeld
edge and in sweet potato Þelds in rows at 1, 10, and
50 m from the edge. Ten sampling units each 5 m apart
were placed in each transect. Each sampling unit consisted of a central pitfall trap with a corn bait trap
placed in the row 1 m away from the pitfall trap and
a potato bait trap placed 1 m away in the opposite
direction. Bait traps consisted of a mesh bag (holes ⬇1
cm diameter) constructed of a 15-cm-long cylinder of
clear plastic netting (MasterNet, Mississauga, Ontario,
Canada), containing either a quarter of a potato or 62.5
ml of corn, and sealed at both ends. Bait traps were
placed under the soil surface. Plastic 237-ml polypropylene specimen containers of 8 cm diameter (VWR
International, Mississauga, Ontario, Canada) were
used as pitfall traps. Containers were quarter-Þlled
with propylene glycol, placed in the soil with the top
lip level with the soil surface, and protected from
weather with a plastic canopy. Canopies were constructed from the container lids held above the pitfall
trap with wire supports. To minimize impacts on natural populations, all traps were only in place for 1 wk
every other week. Bait traps were used to capture
millipedes; beetles found in these traps were ignored
because beetles often escaped during bait collection.
Pitfall traps were placed to capture both millipedes
and beetles. Additional pitfall traps were placed in the
edge habitat of each Þeld but were used only to
enhance the assemblage descriptions for each site
(see Appendix 1). Contents of traps were washed
with ethanol and sieved. Millipedes, carabids, and
staphylinids were counted and identiÞed to species
with some staphylinid exceptions: species of Neohypnus Coiffait and Saiz cannot be reliably distinguished
without dissection and so were treated together; most
species of Aleocharinae encountered were small (3
mm), difÞcult or impossible to separate, and were
therefore not considered in this study. The taxonomy
of Arnett and Thomas (2001) was adopted for this
study.
The number of individuals of each beetle species
collected from a pitfall trap was used to determine
their activity density (AD), an approximation of relative abundance. AD is a product of both true density
and the activity level of the individuals caught and is
therefore most useful for identifying common assemblage members (see Luff 2002). Millipedes caught
within a given sampling unit were combined into a
single AD value. As aleocharine rove beetles were
excluded, total AD for predatory beetles was determined for all non-aleocharine beetles collected in this
study. Species captured were ranked in decreasing
order by proportion of the total individuals caught.
“Common” beetle species were identiÞed by adding
species in ranked order until 95% or more of the total
catch was achieved (all Þelds combined) (Luff 2002).
Each common speciesÕ AD over the sampling period
was compiled into a table for nonstatistical comparisons with each other and C. caeruleocinctus.
Assessment of Predatory Ability. Two common
carabid beetle species, Pterostichus melanarius (Illiger) and Harpalus erraticus Say, were chosen for
1108
ENVIRONMENTAL ENTOMOLOGY
laboratory experiments based on availability of live
specimens. P. melanarius was collected at site P and H.
erraticus was collected at site LSP, with dry pitfall
traps. Traps had large reßective, aluminum pie-plate
canopies to reduce light stress and desiccation. Beetles
were collected from 31 August to 21 September placed
into individual containers with soil from their respective Þelds and transported to the University of Guelph.
On the same day of collection, beetles and soil were
transferred to individual square plastic 946-ml containers (Ziploc; SC Johnson, Brantford, Canada) that
were ventilated by addition of a 3 by 9-cm mesh strip
in the lid. Beetles were provided with a 7.5 by 8-cm
waxed cardboard refuge and a vial cap as a standing
water dish. Beetles were kept in a controlled environment room with a 15Ð23⬚C temperature cycle and 16:8
h L:D photoperiod to simulate natural conditions.
Containers were misted daily with water. Commercially bred mealworms, Tenebrio molitor L., and standing water were provided to beetles ad libitum.
Millipedes (C. caeruleocinctus) were hand-collected from site LSP on 31 August and 21 September
and placed into several opaque plastic, lidded containers with soil, leaf litter, and bakerÕs yeast. Containers were misted daily. A readily available and easily cultured prey item was sought for comparison that
lacked both the physical and chemical defenses of
millipedes. Cabbage looper, Trichoplusia ni Hübner
(Lepidoptera: Noctuidae), was selected for these reasons and because the larvae approximated the size and
shape of C. caeruleocinctus. Several cultures of secondinstar cabbage loopers were obtained from colonies at
the Southern Crop Protection and Food Research
Centre, Agriculture & Agri-Food Canada, London,
Ontario, Canada, and maintained on a modiÞed wheat
germÐ based diet under the same temperature and
lighting conditions as carabid beetles. Cabbage loopers were raised to the desired size range and used in
feeding experiments.
Experiment 1: Palatability and Size Effects. A
choice experiment was conducted using millipedes of
two different size categories to examine palatability
of millipedes to both carabid species and the effect of
prey size on predation. Millipedes were grouped into
“small” (mean length: 14.0 ⫾ 0.65 mm; mean width:
1.1 ⫾ 0.04 mm) or “large” (mean length: 24.9 ⫾ 0.60
mm; mean width: 1.92 ⫾ 0.08 mm) size categories,
which differed signiÞcantly from each other in length
(StudentÕs t-test: n ⫽ 10, t ⫽ 12.28, df ⫽ 18, P ⬍ 0.001)
and width (StudentÕs t-test: n ⫽ 10, t ⫽ 9.07, df ⫽ 14,
P ⬍ 0.001).
Beetles were starved for 2 d before each experiment. One large and one small millipede were randomly selected and randomly assigned to either the far
left or right corners of the choice arena. Arenas were
rectangular plastic containers (17 ⫻ 11 ⫻ 10 cm; Ziploc; SC Johnson) lined with soil. A staging vial was
attached at one end of the arena to hold beetles before
introduction into the arena. Trials were conducted
under red lighting to minimize the effects of light on
the beetles, as they are nocturnal (Luff 2002). Trials
were conducted until 10 responsive replicates were
Vol. 38, no. 4
acquired (i.e., a prey item was chosen), for each species. In each replicate, an individual beetle was selected without replacement, placed into the staging
vial and allowed to move into the arena at will. The
length of time from the beetle entering the arena until
a choice was made was recorded. A choice was deÞned
as sustained grasping of the prey item, and replicates
were recorded as “nonresponsive” if no choice was
made within 15 min. Beetle choices were analyzed for
deviation from randomness (1:1 choice ratio) with a ␹2
test, in Proc FREQ (SAS 9.1). Time until choice was
compared using a least signiÞcant difference test
(Proc GLM; SAS 9.1) between prey types and between beetles, with shorter times interpreted as stronger responses to prey items. Statistical signiÞcance was
taken at ␣ ⫽ 0.05.
Experiment 2: Effects of Physical and Chemical
Defense on Predation. A choice experiment using the
same methodology as above was conducted with millipedes and cabbage loopers and replicated 20 times
for each carabid species. Both beetle species were
included in this experiment, regardless of their previous acceptance or rejection of millipedes, to ensure
that the experimental setup did not adversely affect a
beetleÕs receptivity to prey. Because size was found to
have no effect (see Results), millipedes and loopers of
similar size were selected by visual approximation,
rather than by measurement. Data were analyzed as
above.
Spatiotemporal Associations Between Millipedes
and Predatory Beetles. Beetle species found to consume millipedes in laboratory assays were selected for
a study of their spatiotemporal co-occurrence with
millipede populations. Linear regression analyses
(Proc GLM; SAS 9.1) were conducted between beetle
AD and millipede AD by crop and by individual Þeld.
Beetle and millipede ADs from each sampling unit for
each sampling period were used as data points in these
analyses. Statistical signiÞcance was taken at ␣ ⫽ 0.05.
Results
Species Richness of Generalist Predatory Beetles.
Excluding aleocharines, 7,380 individual beetles
(7,018 collected from Þeld and 362 collected from
edge habitat) were identiÞed to species. Approximately 12 aleocharine “morphospecies” (690 individuals) were found to inhabit carrot and sweet potato
Þelds. The number of aleocharine morphospecies in
carrot and sweet potato Þelds was similar. Fifty carabid and 25 staphylinid species were recorded and
identiÞed in total. The identiÞed carabid and
staphylinid species collected from pitfall traps are
summarized in Appendix 1. Higher carabid species
richness was found in carrot (24 ⫾ 1) than sweet
potato (20 ⫾ 2) Þelds. Tachinus corticinus Gravenhorst
(Staphylinidae) is newly recorded from Ontario. A
species native to Europe, it was known previously in
North America from Quebec, New Brunswick, Nova
Scotia, Prince Edward Island, and Vermont (Campbell
and Davies1991; Byers et al. 2000; Klimaszewski and
Majka 2008), and these southwestern Ontario speci-
August 2009
BRUNKE ET AL.: GENERALIST PREDATORS AND MILLIPEDE MANAGEMENT
1109
Table 1. Average activity densities of the millipede C. caeruleocinctus and the “common” species of carabid beetles collected in
southern Ontario carrot fields
Site
Species
G
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Ophonus puncticeps
Harpalus erraticus
Bembidion quadrimaculatum oppositum
Pterostichus permundus
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Ophonus puncticeps
Harpalus erraticus
Bembidion quadrimaculatum oppositum
Poecilus chalcites
Scarites subterraneus
Pterostichus permundus
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Ophonus puncticeps
Harpalus erraticus
Bembidion quadrimaculatum oppositum
Poecilus chalcites
Pterostichus permundus
C
P
Mean activity density by weeka
23 May
29 May
12 Jun.
26 Jun.
10 Jul.
24 Jul.
7 Aug.
21 Aug.
4 Sep.
4.27
0
0
0.03
0
0.63
0
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
15.83
0
0
0
0
4.93
1.17
0
1.48
0
0
0
0
0
0
4.40
0
0
0
0
0.23
0
0
0
2.30
0
0
0
0
0.52
0.30
0
0
0
0
0
0
0
0
5.30
0.27
0
0
0
0.20
0.07
0
0
3.31
9.45
0.03
0
0
0.52
2.31
0
0.07
0
0
0.03
0
0.10
0
0.40
0.40
0
0
0
0.50
0.33
0.03
0
0.37
49.59
0
0
0
0.93
0.85
0.04
0
0.03
0.31
0
0
0.03
0
0.23
0.07
3.40
0.03
0
0.33
0.17
0.03
0
1.03
34.76
0.28
0.03
0
0.48
0.24
0.38
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
Ñ
0.41
1.69
0.48
0
0
0.03
0
0
0.07
0.80
12.63
0.07
0.07
0
0.07
0.23
0
0
0
1.07
0.10
1.53
0
0
0
0
2.59
0.21
0.14
0.03
0.10
0
0
2.63
38.80
2.93
9.67
0.03
0.07
0.1
0.10
0
0
0.17
0.13
1.70
0
0
0.55
0
0.82
0.29
0.54
0
0.04
0
0
6.14
3.24
2.86
0.31
0.14
0
0
0
0
0.10
0.07
0.07
0.77
0
0.03
0.30
0.50
0.30
0.03
0.50
0
0.03
0.03
0
2.21
1.34
1.93
0.10
0.24
0
0.03
0
a
Mean activity density for C. caeruleocinctus is the mean for all sampling units (i.e., bait and pitfall trap units) in the Þeld. Mean activity
density for carabids is the mean for all pitfall traps in the Þeld. Dates represent the end of the sampling week.
Ñ, sampling did not occur on this date at this site.
mens (two male, two female) are the westernmost
known in North America. Vouchers of all species and
aleocharine morphospecies were deposited in the
University of Guelph Insect Collection.
Common Predatory Beetles and Their Temporal
Distributions. Eight carabid species comprised 95% of
the total individuals captured (total AD) and were
therefore identiÞed as dominant, P. melanarius
(65.5%), or common, Harpalus pensylvanicus (DeGeer) (8.8%), Ophonus puncticeps (Stephens) (4.7%),
H. erraticus (4.7%), Bembidion quadrimaculatum oppositum Say (4.5%), Poecilus chalcites (Say) (2.4%),
Scarites subterraneus Fabricius (2.1%), and Pterostichus permundus (Say) (1.2%). Species not included as
common each comprised ⬍1% total AD. No identiÞed
staphylinid species were found to be common members of the predatory beetle assemblage of carrot and
sweet potato Þelds (but see Discussion), although
some of the excluded aleocharine morphospecies
were quite abundant.
The temporal distributions of the above eight species and C. caeruleocinctus are described in Tables 1
and 2. At least one common species co-occurred with
millipedes at any given time in both crop types, except
for 29 May and 12 June at site G (Table 1). No millipedes or predatory beetles were found on 12 June at
site G (Table 1). In carrot Þelds, relatively few common species were present in early summer with a
greater number present later in the growing season
(Table 1). This trend was also observed in sweet potato Þelds but was less pronounced (Table 2). Pterostichus melanarius, H. pensylvanicus, B. q. oppositum,
and P. permundus were widespread species present in
all Þelds of both crop types. H. erraticus was only
absent from one Þeld (GSP), whereas S. subterraneus
was more typical of sweet potato Þelds (absent from
G and P), and O. puncticeps was more typical of carrot
Þelds (absent from CSP and LSP). P. chalcites was
present in one sweet potato and two carrot Þelds.
Assessment of Predatory Ability
Experiment. 1: Palatability and Size Effects. Millipedes were consumed by P. melanarius, but no size
preference was observed (␹2 ⫽ 1.6, n ⫽ 10, df ⫽ 1, P ⫽
0.21). Time for P. melanarius to make a choice ranged
from 22 to 580 s but did not differ between prey size
categories (F ⫽ 3.86, n ⫽ 10, df ⫽ 1, P ⫽ 0.08). Twelve
replicates of P. melanarius were classiÞed as nonresponsive and excluded from analyses; all nonresponsive beetles were observed to circle the perimeter of
the assay arena in an agitated manner without regard
to prey items. No millipedes were preyed on by H.
erraticus. Although two individuals of H. erraticus
were observed grasping millipedes in their mandibles
after trials had ended, they promptly released the
millipedes and appeared to wipe their mandibles and
maxillary palpi together and against the substrate. This
behavior was not observed in P. melanarius.
Experiment 2: Effects of Physical and Chemical
Defense on Predation. When given the choice between a millipede and a cabbage looper, P. melanarius
chose loopers (87.5%) signiÞcantly more often than
millipedes (12.5%; ␹2 ⫽ 9.0, n ⫽ 16, df ⫽ 1, P ⫽ 0.003).
Four replicates were classiÞed as “nonresponders.” H.
erraticus always chose loopers. The two beetle species
1110
ENVIRONMENTAL ENTOMOLOGY
Vol. 38, no. 4
Table 2. Average activity densities of C. caeruleocinctus and the dominant species of carabid beetles collected in southern Ontario
sweet potato fields
Site
Species
LSP
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Harpalus erraticus
Bembidion quadrimaculatum oppositum
Scarites subterraneus
Pterostichus permundus
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Ophonus puncticeps
Bembidion quadrimaculatum oppositum
Poecilus chalcites
Scarites subterraneus
Pterostichus permundus
Cylindroiulus caeruleocinctus
Pterostichus melanarius
Harpalus pensylvanicus
Bembidion quadrimaculatum oppositum
Scarites subterraneus
Pterostichus permundus
GSP
CSP
Mean activity density by weeka
20 Jun.
3 Jul.
17 Jul.
31 Jul.
14 Aug.
28 Aug.
35.77
0.97
0
0
0.07
0
0
2.87
0.43
0
0
0.03
0
0.47
0.73
1.60
0.07
0.03
0.60
3.30
0
6.23
0.37
0
0
0
0
0
2.03
0.10
0.03
0.03
0.03
0
0.33
1.03
0.63
0.07
0.07
0.23
0.20
0
6.53
0.40
0.50
0
0
0
0
0.18
0.07
0
0
0
0
0.29
0.29
0.10
0
0
0
0.17
0
18.73
0.23
0.73
0.20
0.03
0
0.03
3.20
0.07
0
0
0
0
0
0
2.27
0
0
0.07
0.07
0
80.47
2.66
0.47
2.57
0.03
0
0
14.10
0.07
0.03
0
0.03
0.03
0
0.03
1.47
0.07
0
0.07
0.03
0
69.47
2.70
0.23
2.10
0
0.03
0.03
14.13
0.43
0
0
0.07
0
0.03
0.07
6.53
0.50
0.03
0.07
0.13
0.07
a
Mean activity density for C. caeruleocinctus is the mean for all sampling units (i.e., bait and pitfall trap units) in the Þeld. Mean activity
density for carabids is the mean for all pitfall traps in the Þeld. Dates represent the end of the sampling week.
did not differ in the time taken to choose a prey item
(F ⫽ 2.18, n ⫽ 27, df ⫽ 1, P ⫽ 0.15). Time until choice
did not differ in P. melanarius between those that
chose loopers and those that chose millipedes (F ⫽ 0.0,
n ⫽ 16, df ⫽ 1, P ⫽ 0.98).
Spatiotemporal Associations Between Millipedes
and Predatory Beetles. Pterostichus melanarius and C.
caeruleocinctus were not found to be spatiotemporally
associated in southern Ontario carrot Þelds (R2 ⫽
0.0061, P ⫽ 0.07; Fig. 1A). However, a signiÞcant positive spatiotemporal relationship was found between
P. melanarius and C. caeruleocinctus in southern Ontario sweet potato Þelds (R2 ⫽ 0.2593, P ⬍ 0.001; Fig.
1B). Spatiotemporal associations were found in each
of the individual sweet potato Þelds; LSP (R2 ⫽ 0.1791,
P ⬍ 0.001; Fig. 2A), GSP (R2 ⫽ 0.079, P ⬍ 0.001; Fig.
2B), and CSP (R2 ⫽ 0.3209, P ⬍ 0.001; Fig. 2C).
Discussion
Predaceous Beetle Assemblages in Ontario Carrot
and Sweet Potato Fields. Our carabid assemblage descriptions are derived from one season of data and as
such cannot be considered complete in both composition and proportional abundance because of the
strong annual variability in agroecosystems (Scott and
Anderson 2003). However, while abundances will
vary, the status of some species as common is reasonably stable and predictable from year to year because
most of the assemblage variability is caused by uncommon species (Scott and Anderson 2003). Both
carrot and sweet potato Þelds were found to be less
species rich in Carabidae (24 ⫾ 1 and 20 ⫾ 2 species,
respectively) compared with the average value for
agroecosystems in North America (30 ⫾ 2 species)
(Luff 2002). Low carabid richness relative to this av-
erage has been reported in carrot agroecosystems in
the Netherlands and Quebec and was attributed to
lack of early season crop cover, preventing long-term
moist microhabitats (Booij and Noorlander 1992;
Boivin and Hance 2002). This explanation Þts with our
result that a greater number of common carabid species were found later in the season than earlier. However, species richness in this study may also have been
limited by the low rainfall experienced in southern
Ontario in 2007, as evidenced by declines in arthropod
activity density at some sites in June and July. Between-row cultivation in both crops tends to decrease
as the plant canopies close, and this early season disturbance may have played a role in determining richness and abundance patterns (Thorbek and Bilde
2004). The broad- spectrum insecticide applications
made at site G may have accounted for the absence of
millipedes and predatory beetles in our traps on 12
June, because nontarget effects of sprays are often
substantial (Huusela-Veistola 1996). Differences in
edge habitat were not quantitatively measured but
may also account for some of the differences observed
between Þelds (Dauber et al. 2005).
Low species richness of Staphylinidae was an artifact of two characteristics of this study. First, pitfall
traps do not adequately sample staphylinid assemblages and can underestimate their abundance (Lang
2000). Halsall and Wratten (1988) found a pitfall trap
bias against Tachyporus Gravenhorst, a rove beetle
genus that was found in most Þelds surveyed (Appendix 1). Alternative trapping methods, such as suction
sampling (Holland et al. 2004) or coverboards (Davalos and Blossey 2006) are needed to sample staphylinids and carabids more accurately. Second, aleocharine
species were excluded from analyses in this study, and
this subfamily is the most speciose of the rove beetles
August 2009
BRUNKE ET AL.: GENERALIST PREDATORS AND MILLIPEDE MANAGEMENT
1111
100
90
A
80
70
60
50
y = 0.4506x + 7.7139
R² = 0.0061
p = 0.07
P. melanarius Activity Density
40
30
20
10
0
0
5
10
15
20
25
30
35
12
B
10
y = 0.0195x + 0.2245
R² = 0.2593
p < 0.0001
8
6
4
2
0
0
50
100
150
200
250
300
350
400
C. caeruleocinctus Activity Density
Fig. 1. Activity density of P. melanarius in relation to the activity density of C. caeruleocinctus in southern Ontario carrot
Þelds (A) and sweet potato Þelds (B). Activity density of P. melanarius was measured using pitfall traps, whereas that of C.
caeruleocinctus was measured using corn and potato bait traps as well as pitfall traps.
(Arnett and Thomas 2001). Aleocharine morphospecies found in Þelds may consist of many true species.
This subfamily was the dominant group of Staphylinidae in this study, consistent with results in New Zealand from the only other study to evaluate the rove
beetle assemblage of carrots in detail (Sivasubramaniam et al. 1997). It is unlikely that this group of small
beetles (most 3 mm) preys on adult or subadult C.
caeruleocinctus, but the role of aleocharines in millipede egg predation could be signiÞcant as some species are known to be important in dipteran egg mortality (Andersen et al. 1983).
Common Species in Carrot and Sweet Potato
Fields. The eight species identiÞed as common in this
study were all carabids and are typical of agroecosystems and of northeastern North American synanthropic habitats in general (Boivin and Hance 2002,
Cardenas and Buddle 2008). Indeed, four of the eight
common species were found in every Þeld. P. melanarius is frequently the dominant carabid in synanthropic ecosystems in both North America and in its
native Europe (Cardenas and Buddle 2008).
Predatory Ability of Two Common Carabids. Pterostichus melanarius consumed millipedes in situations
with and without the option of alternative prey. This
is the Þrst known record of P. melanarius consuming
millipede prey. This species does not seem to be
limited by the physical or chemical defenses of millipedes. P. melanarius was also observed to consume
millipedes in the Þeld, and it is possible that millipedes
are accepted more readily in nature than in our experiments. Although soft-bodied prey (cabbage loopers) were chosen more often than millipedes, this
response is expected in a generalist predator, where
the tendency to minimize handling effort is well
known (Sunderland 2002). Native Pterostichus species
have been found to readily accept millipedes in the
families Julidae and Polydesmidae (Snider 1984). Both
larval and adult stages of those Pterostichus spp. survived on a diet solely of julid prey, and viable offspring
were produced (Snider 1984). It seems likely that P.
melanarius can do the same, particularly because C.
caeruleocinctus is also a native European species.
Snider (1984) showed that many Pterostichus spp. can
consume large numbers of millipedes per day. P. melanarius was never observed to consume large quantities
of C. caeruleocinctus, but predation in our studies was
less than that observed by Snider (1984), likely because of less favorable conditions, especially lower
humidity, in captivity.
1112
ENVIRONMENTAL ENTOMOLOGY
Vol. 38, no. 4
12
A
10
y = 0.0162x + 0.6374
R² = 0.1791
p < 0.0001
8
6
4
2
0
0
50
100
150
200
250
300
350
400
P. melanarius Activity Density
4.5
4
B
3.5
3
2.5
y = 0.0138x + 0.1119
R² = 0.079
p = 0.0001
2
1.5
1
0.5
0
0
10
20
30
40
50
60
70
80
90
3.5
3
C
2.5
y = 0.0402x + 0.0324
R² = 0.3209
p < 0.0001
2
1.5
1
0.5
0
0
10
20
30
40
50
60
C. caeruleocinctus Activity Density
Fig. 2. Activity density of P. melanarius in relation to the activity density of C. caeruleocinctus in southern Ontario sweet
potato Þelds: (A) site LSP, (B) site GSP, and (C) site CSP. Activity density of P. melanarius was measured using pitfall traps,
whereas that of C. caeruleocinctus was measured using corn and potato bait traps as well as pitfall traps.
Cylindroiulus caeruleocinctus was unpalatable to H.
erraticus in laboratory feeding experiments, and it
seems that this species is not a millipede predator.
Cabbage loopers were eaten readily, and both H. erraticus and P. melanarius took the same time to choose
a prey item, eliminating the possibility that laboratory
conditions prevented feeding behavior in H. erraticus.
It is unlikely that H. erraticus was deterred by the
physical defenses of C. caeruleocinctus, because it belongs to a genus of primarily omnivorous beetles that
have mandibles useful for the cracking of seeds (Ingerson-Mahar 2002). Given that individuals attempt-
August 2009
BRUNKE ET AL.: GENERALIST PREDATORS AND MILLIPEDE MANAGEMENT
ing to feed on millipedes promptly rejected them and
exhibited wiping behavior, it seems likely that H. erraticus was deterred by the defensive secretions of C.
caeruleocinctus.
Spatiotemporal Co-occurrence of P. melanarius
With C. caeruleocinctus. A signiÞcant relationship between the ADs of P. melanarius and C. caeruleocinctus
indicates that that these two species indeed co-exist
both spatially and temporally in sweet potato Þelds.
The amount of variation explained by millipede activity density was relatively low (r2 ⫽ 0.259), but this
is to be expected with generalist predators that are
typically not tightly linked to any one prey species. An
improved linear model might be achieved by using a
trapping method such as fenced pitfalls, which provide
a greater measure of true carabid density and do not
overestimate densities of large species as unfenced
pitfalls do (Mommertz et al. 1996). No relationship
was found between the ADs of these species in carrot
Þelds, which may be because of a greater abundance
of alternative prey or a lower abundance of millipedes
in carrot Þelds relative to P. melanarius. In sweet potato Þelds, millipede ADs were consistently much
greater than that of their co-occurring common carabids, whereas this was not seen in the carrot Þelds
studied (Tables 1 and 2). At high densities, C. caeruleocinctus may become an important prey species for
P. melanarius, and this may be mediated by the tendency of C. caeruleocinctus to form large, local aggregations in carrot and sweet potato Þelds (Sears et al.,
unpublished data).
Other Natural Enemies of C. caeruleocinctus. The
predatory potential of the other six common predatory
beetles remains to be evaluated directly. B. q. oppositum is almost certainly too small to prey on any millipede life stages, except eggs and Þrst instars. This
species is known to eat the eggs of pest Diptera (Sunderland 2002) and may also feed on C. caeruleocinctus
eggs. H. pensylvanicus and O. puncticeps are omnivorous, consuming a variety of prey from seeds to arthropods (Arnett and Thomas 2001; Honek et al.
2007). Snider (1984) tested the palatability of millipedes to one H. pensylvanicus individual, which refused this prey. P. chalcites is known as a primary
generalist insectivore (Sunderland 2002), but its status
as a millipede predator is unknown. The genus Poecilus
is closely related to Pterostichus, sometimes placed
within it (Downie and Arnett 1996), and may share
some of its biology. P. permundus overlaps the size
range of P. melanarius (unpublished data) and is likely
to follow the trend of its congeners in consuming
subadult and adult millipedes. S. subterraneus is known
to consume a wide range of large arthropod prey
(Sunderland 2002), and Baker (1985) reported millipede predation in the congener S. cyclops.
The generalist assemblage was examined for species
that were common, accepted millipede prey, and coexisted with millipedes. P. melanarius exhibited all of
these characteristics, and it is concluded that this species is a natural predator of C. caeruleocinctus in Ontario sweet potato and carrot Þelds and may play an
important role in millipede population regulation.
1113
This is the Þrst study to examine the predatory beetle
assemblage of these crops in Ontario, and the Þrst
study to address the natural control of C. caeruleocinctus in North American vegetable crops. The effect
of millipede density on millipede mortality by natural
predation is unknown and may be an important aspect
of future IPM strategies for C. caeruleocinctus.
Acknowledgments
We thank L. OÕKeefe and T. Marowa for their role in the
intensive Þeldwork of this project, and A. Verhallen (Ontario
Ministry of Agriculture, Food and Rural Affairs [OMAFRA])
for soil textural analyses. Drs. J. Allen and M. Filotas
(OMAFRA) provided logistical support and background
knowledge of carrot and sweet potato production in Ontario.
We thank the participating vegetable growers who volunteered Þelds for study and L. Verdon (AAFC) for provision
of cabbage loopers. This project was supported by the Canada-Ontario Research and Development Program and the
Fresh Vegetable Growers of Ontario through funding to
M.K.S. and R.H.H. and by a Natural Sciences and Engineering
Research Council Undergraduate Summer Research Assistantship to A.J.B.
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BRUNKE ET AL.: GENERALIST PREDATORS AND MILLIPEDE MANAGEMENT
1115
Appendix 1. Predatory beetle species collected in pitfall traps placed in field (F) and edge (E) habitats of carrot and sweet potato fields,
in southern Ontario
Carrot
Species list
Carabidae
Cicindelinae: Cicindelini
Cicindela
Harpalinae: Chlaeniini
Chlaenius
Cyclosomini
Tetragonoderus
Harpalini
Acupalpus
Anisodactylus
Bradycellus
Dicheirotrichus
Harpalus
Ophonus
Stenolophus
Lebiini
Microlestes
Licinini
Diplocheila
Platynini
Agonum
Calathus
Pterostichini
Poecilus
Pterostichus
Cyclotrachelus
Zabrini
Amara
Scaritinae: Clivinini
Clivina
Scaritini
Scarites
Trechinae: Bembidiini
Bembidion
Elaphropus
Trechini
Trechus
G
Sweet potato
C
P
LSP
GSP
CSP
F
E
F
E
F
E
F
E
F
E
F
E
punctulata
repanda
X
X
/
/
X
X
/
/
X
/
X
/
X
/
X
/
X
/
X
/
X
/
/
/
emarginatusa
nemoralis
pusillus
/
/
/
/
X
/
/
/
/
/
/
/
X
/
X
/
/
/
/
X
/
/
X
/
/
/
/
/
/
/
/
X
/
/
/
X
fasciatus
X
/
X
/
/
/
/
/
/
/
/
/
partiarius
rusticusa
santaecrucis
rupestrisa
tantillus
cognatus
affinis
caliginosusa
compar
eraticus
fulvilabris
indianus
longicollisa
pennsylvanicus
somnulentrus
puncticeps
comma
ochropezus
X
X
X
/
/
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
X
/
/
/
/
/
/
/
X
X
X
X
/
X
/
X
X
/
X
/
/
/
X
/
/
/
X
/
X
/
/
X
X
/
X
X
X
X
X
X
/
X
X
/
/
X
/
X
X
/
X
/
X
/
X
/
/
/
X
/
X
X
/
/
/
X
/
X
X
X
/
/
X
/
X
/
/
/
X
/
X
/
/
X
/
/
X
X
/
/
/
X
X
/
X
/
X
/
/
X
X
/
/
/
X
/
/
/
/
X
/
/
X
/
/
/
/
X
/
X
X
/
/
/
/
/
/
/
/
/
/
/
X
/
/
X
/
/
/
X
/
/
/
X
/
/
X
/
/
/
/
/
/
/
/
/
X
/
/
/
/
brevilobus
X
/
X
X
X
/
/
/
X
/
/
/
obtusa
/
/
/
X
/
/
/
/
/
/
/
/
cupripennea
muelleri
nutans
placidum
opacula
/
/
/
/
/
/
/
/
/
X
/
/
/
X
/
/
/
/
/
/
/
X
/
X
/
/
/
/
/
/
X
X
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
X
/
/
/
/
/
/
/
chalcites
lucublandus
melanarius
permundus
sodalis
/
X
X
X
/
/
/
X
X
X
X
/
X
X
/
/
/
X
/
/
X
/
X
X
/
/
/
X
X
/
/
X
X
X
X
/
X
X
X
X
X
X
X
X
X
/
/
/
/
X
/
/
X
X
/
/
/
X
/
/
avida
cupreolata
familiaris
musculus
rubricaa
/
X
X
X
/
/
X
/
/
X
/
/
X
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
X
X
X
X
/
/
X
/
/
/
/
X
/
X
/
/
/
/
/
/
/
/
/
X
/
/
/
/
/
/
impressefrons
/
/
X
/
X
/
/
/
/
/
X
/
subterraneus
/
/
X
/
/
/
X
/
X
X
X
X
affinea
nitidum
obtusum
quadrimaculatum
oppositum
anceps
xanthopusa
X
X
/
/
/
/
/
/
X
/
/
/
/
/
X
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
X
/
/
/
/
X
X
/
/
/
/
X
X
X
/
/
/
X
X
/
/
/
/
X
X
/
X
/
/
X
X
/
X
/
/
quadristriatus
/
/
X
/
X
X
/
/
/
/
X
/
Continued on following page
1116
Appendix 1.
ENVIRONMENTAL ENTOMOLOGY
Vol. 38, no. 4
Continued
Carrot
Species list
Staphylinidae
Paederinae: Paederini
Lobrathium
Scopaeus
Oxytelinae: Oxytelini
Anotylus
Thinobiini
Carpelimus
Staphylininae: Staphylinini
Belonuchus
Erichsonius
Neobisnius
Philonthus
Tasgius
Xantholinini
Neohypnus
Stenistoderus
Steninae
Stenus
Tachyporinae: Mycetoporini
Bryoporus
Mycetoporus
Tachyporini
Tachinus
Tachyporus
G
Sweet potato
C
P
LSP
GSP
CSP
F
E
F
E
F
E
F
E
F
E
F
E
collare
dimidiatuma
quadriceps
/
/
/
/
/
/
X
X
/
/
/
/
X
/
X
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
brevicepsa
insignitus
/
/
/
/
/
/
/
/
/
/
/
/
X
X
/
/
/
/
/
/
/
/
/
/
obesusa
/
/
X
/
/
/
/
/
/
/
/
/
rufipennis
nanus
sobrinus
carbonarius
caucasicus
concinnusa
janusa
ater
/
X
X
/
X
/
X
/
X
/
/
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
X
/
/
/
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
/
/
X
/
X
/
X
/
/
/
/
/
/
/
X
spp.b
rubripennisa
X
/
/
/
X
X
/
/
X
/
/
/
X
/
/
/
/
/
/
/
X
/
/
/
pubescensa
stygicusa
/
/
/
/
/
/
/
/
/
X
/
/
/
/
X
/
/
/
/
/
/
/
/
/
rufescens
consors
/
/
/
/
/
X
/
/
X
X
/
/
X
X
/
/
/
X
X
/
/
/
/
/
corticinusc
dispara
maculocollis
nitidulus
/
/
/
X
X
/
/
/
/
/
/
X
/
/
/
/
/
X
X
/
/
/
/
/
X
/
X
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
X
/
/
/
/
Edge traps were excluded from the main study because of variable edge habitat and asynchrony of the two trap collection schedules.
a
Species represented by one specimen.
b
Species included obscurus and melanops.
c
Newly recorded for Ontario.
X, present; /, absent.