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The effect of twig diameter on emergence rates of the oak twig pruner (Coleoptera: Cerambycidae)

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Abstract

Oak twig pruner (Anelaphus parallelus (Newman); Coleoptera: Cerambycidae) larvae develop inside twigs pruned from host plants. Reasons for this behaviour are unknown and differential emergence due to twig diameter has not been explored. Twigs pruned from walnuts (Juglans nigra Linnaeus; Juglandaceae) (n=179) and oaks (Quercus Linnaeus; Fagaceae) (n=84) were collected in Pennsylvania, United States of America in 2010; 118 pruned oak twigs were collected in New York State, United States of America in 2012. Twigs from 2012 were dissected to determine rates of emergence and larval mortality; both samples were examined for parasitoids. As the diameter of oak twigs (range of 3–16 mm) increased, larval mortality increased and adult emergence decreased. Date of collection did not influence twig diameter nor emergence rates. Three new parasitoids were associated with the oak twig pruner: Atanycolus Förster (Hymenoptera: Braconidae), Eubazus denticulatus (Martin) (Hymenoptera: Braconidae), and a potentially new genus of wasp (Hymenoptera: Braconidae, Hormiinae near Pambolus Haliday). Parasitism rates were an order of magnitude greater among twigs that contained more than one larva or pupa (23.1%; n=26) compared to those that contained only one (2.3%; n=341).
The effect of twig diameter on emergence rates of
the oak twig pruner (Coleoptera: Cerambycidae)
William P. Brown,
1
Marion E. Zuefle, Jason J. Dombroskie
AbstractOak twig pruner (Anelaphus parallelus (Newman); Coleoptera: Cerambycidae) larvae
develop inside twigs pruned from host plants. Reasons for this behaviour are unknown and differential
emergence due to twig diameter has not been explored. Twigs pruned from walnuts (Juglans nigra
Linnaeus; Juglandaceae) (n=179) and oaks (Quercus Linnaeus; Fagaceae) (n=84) were collected in
Pennsylvania, United States of America in 2010; 118 pruned oak twigs were collected in New York State,
United States of America in 2012. Twigs from 2012 were dissected to determine rates of emergence and
larval mortality; both samples were examined for parasitoids. As the diameter of oak twigs (range
of 316 mm) increased, larval mortality increased and adult emergence decreased. Date of collection did
not inuence twig diameter nor emergence rates. Three new parasitoids were associated with the oak twig
pruner: Atanycolus Förster (Hymenoptera: Braconidae), Eubazus denticulatus (Martin) (Hymenoptera:
Braconidae), and a potentially new genus of wasp (Hymenoptera: Braconidae, Hormiinae near Pambolus
Haliday). Parasitism rates were an order of magnitude greater among twigs that contained more than one
larva or pupa (23.1%; n=26) compared to those that contained only one (2.3%; n=341).
Introduction
Oak twig pruners, Anelaphus parallelus
(Newman) (Coleoptera: Cerambycidae), oviposit
at the ends of branches of living oaks (Quercus
Linnaeus; Fagaceae), black walnuts (Juglans
nigra Linnaeus; Juglandaceae), and other trees
(Gosling 1978) from the eastern United States of
America to Canada and westward to Texas,
United States of America (Solomon and Payne
1986). Larvae feed on the woody portion of
the stem, overwinter in the twig in a dormant state,
and resume feeding in the centre of the twig
the following spring. Early in the second summer,
the larva will chew away the wood at the proximal
end of the twig until it reaches the bark, fall to the
ground within the distal portion of the twig when
it is dislodged from the tree by the elements,
and continue development inside the fallen twig
(Gosling 1978, 1981). Larvae in fallen twigs may
be depredated by vertebrates and arthropods,
including parasitoids (Gosling 1978). Evolutionary
explanations for pruning twigs are not resolved.
Here, we report emergence and parasitism
rates from pruned oak twigs collected in 2012 in
New York State, United States of America as well
as the effect of twig diameter on larval mortality
and adult emergence, which might aid under-
standing the evolutionary origins of pruning
behaviour. Additionally, parasitoids and com-
mensal arthropods collected from pruned oak and
black walnut twigs in Pennsylvania, United States
of America were documented and identied to
species, when possible.
From 19 June to 5 September 2010, we
collected 284 pruned twigs near the Borough of
Kutztown, Berks County, Pennsylvania. A total of
61 pruned twigs, mostly from red oaks (Quercus
rubra (Linnaeus)), were collected from Kutztown
Park. Twigs were also collected from black
walnuts (n=179) and oaks (n=23) along an
access road on the west side of Lake Ontelaunee,
W.P. Brown,
1
Division of Natural Sciences and Mathematics, Keuka College, Keuka Park, New York, 14478,
United States of America
M.E. Zuee, IPM Program Ofce, NYSAES, 630 W. North Street, Geneva, New York, 14456, United States of
America
J.J. Dombroskie, Department of Entomology, Comstock Hall, Cornell University, Ithaca, New York, 14850,
United States of America
1
Corresponding author (e-mail: wbrown@keuka.edu).
Subject Editor: Dylan Parry
doi:10.4039/tce.2016.25
Received 20 August 2015. Accepted 11 April 2016. First published online 16 June 2016.
Can. Entomol. 00:15 (2016) © 2016 Entomological Society of Canada
1
10 km southwest of Kutztown, from 20 June 2010
until 5 September 2010. The road was monitored
two to three times per week. In all, 13 other
pruned twigs were incidentally collected from
areas near Kutztown.
Beginning 15 June through 22 July 2012, 118
pruned oak twigs were collected from the Penn
Yan, Dresden, and Watkins Glen areas of
New York State. All three sites were monitored at
least twice a week for fallen twigs; the Dresden
site was monitored almost daily. For both
twig collections (2010 and 2012), we did not
estimate how many individual host trees produced
the collected twigs, nor were we able to determine
where, in the tree, the twig originated. Any leaves
were removed from collected twigs, diameter at
the proximal end was recorded to the nearest
0.1 mm with digital calipers, and longer twigs
were cut to a length of ~30 cm from the proximal
end and placed in nylon mesh bags on the day of
collection. The mesh bags were placed in plastic
bins and stored in a basement at 1220 °C for
~10 months. Twigs were dissected and examined
for larvae, pupae, adults, parasitoids, or their
remains, and commensal arthropods. Twigs that
had cerambycid beetles other than the oak twig
pruner emerge (see below) were removed from
analyses on effects of twig diameter on emer-
gence. Parasitoids collected in 2010 and 2012
were identied to species by J.J.D., manager of
the Insect Diagnostic Laboratory at Cornell
University (Ithaca, New York, United States of
America). Voucher specimens were deposited in
the Keuka College insect collection, Keuka Park,
New York, and the Cornell University insect
collection, Ithaca, New York.
The difference in twig diameter between oaks
and walnuts collected in 2010 was compared with
at-test. The effects of twig diameter and date of
collection on adult emergence and the incidence
of dead larvae from twigs collected during 2012
were examined with binomial logistic regression.
The difference in parasitism rates between twigs
that contained at least one known oak twig pruner
larva or pupa and those known to contain more
than one beetle larva or pupa, of any species, were
compared with a χ
2
test.
There was no difference in the average diameter
of twigs pruned from oaks (mean =9.3, SD =
3.0, range 4.619.4 mm) or walnuts (mean =9.6,
SD =1.9, range 5.418.3 mm) collected in
Pennsylvania during 2010 (t
272
=1.0, P=0.31).
The mean diameter of oak twigs pruned in
New York during 2012 was 8.5 mm (SD =3.0)
and ranged from 3.1 to 15.6 mm.
The overall emergence rate of oak twig pruner
beetles from oak twigs during 2012 was 44%. As
oak twig diameter increased, the likelihood of
emergence decreased (Wald χ
2
=5.0, df =1,
P=0.025; Hosmer and Lemeshow Goodness-of-
t: χ
2
=7.9, df =8, P=0.44; max-rescaled
R
2
=0.06; Fig. 1) and the likelihood of larval
mortality increased (Wald χ
2
=5.1, df =1, P=
0.024; Hosmer and Lemeshow goodness-of-t:
χ
2
=6.8, df =8, P=0.56; max-rescaled
R
2
=0.07; Fig. 1). The date of collection did not
inuence the likelihood of emergence (Wald χ
2
=
0.02, df =1, P=0.54), the likelihood of larval
mortality (Wald χ
2
=0.01, df =1, P=0.92), or
twig diameter (F(1,108) =0.72, P=0.40).
Two parasitoids emerged from 87 oak twigs
(2.3%) and eight parasitoids emerged from
187 walnut twigs (4.2%) collected during 2010.
Three parasitoids emerged from 118 oak twigs
collected during 2012 (2.5%). Collectively,
twig pruners were attacked by parasitoids in
Braconidae (Hymenoptera) (Atanycolus Förster,
Eubazus denticulatus Martin, Hormiinae near
Pambolus Haliday (a potentially new genus of
wasp), and an unidentied species; all are new
associations with the oak twig pruner), Cryptinae
(Hymenoptera: Ichneumonidae), and Tachinidae
(Diptera). Potential predators and commensal
insects observed included Caenochrysis doriae
(Gribodo) (Hymenoptera: Chrysididae), Trypoxylon
frigidum Smith (Hymenoptera: Crabronidae),
Pyticeroides laticornis (Say) (Coleoptera: Cleridae),
Magdalis Germar species (Coleoptera: Curculio-
nidae), Liopinus alpha (Say) (Coleoptera:
Cerambycidae), Molorchus bimaculatus Say
(Coleoptera: Cerambycidae), Anelaphus villosus
(Fabricius) (Coleoptera: Cerambycidae), Mastogenius
crenulatus Knull (Coleoptera: Buprestidae), and
other arthropods (Araneae, Nabidae (Hemiptera),
Forculidae (Dermaptera), and Formicidae
(Hymenoptera)).
Occasionally, more than one larva or adult beetle,
including co-inhabitants of different species, were
collected from pruned twigs. Live oak twig pruner
larvae were noted in twigs approximately a year
after collection and, in three cases, parasitoids
emerged from twigs that contained dead, intact
2 Can. Entomol. Vol. 00, 2016
© 2016 Entomological Society of Canada
larvae, indicating the presence of more than one
larva in those twigs (Table 1). A small percentage of
twigs were pruned at both ends, implying that
multiple oak twig pruner larvae inhabited the same
twig and completed sequential prunes. Considering
only twigs known to contain one oak twig pruner at
any stage of development during 2010 and 2012
(some twigs were empty when dissected), eight of
341 twigs (2.3%) were parasitised. Six of 26 twigs
(23.1%) that held more than one beetle of any
species were parasitised; this difference was
signicant (χ
2
=28.3, df =1, P<0.0001).
The lower rate of emergence in twigs of larger
diameter in this study was correlated with a
greater rate of larval mortality in such twigs.
Similarly, twig girdlers (Oncideres cingulata
(Say); Coleoptera: Cerambycidae) were more
likely to emerge from honey locust (Gleditsia
triacanthos Linnaeus; Fabaceae) twigs of smaller
diameter (Coppedge 2011) but this nding did not
hold for the three other tree species examined.
Larger twigs may provide more resources for
developing larvae of twig girdlers (Cramer 1998)
but no twig characteristic, of seven measured, was
Fig. 1. The probability of oak twig pruner (Anelaphus parallelus) emergence (A) and larval mortality (B) in
relationship to diameter of oak twigs in New York 2012 (n=118, note, some data points overlap).
Brown et al. 3
© 2016 Entomological Society of Canada
a strong predictor of the number of twig girdler
eggs laid or hatched (Cramer 1998).
Forcella (1982) found that the twig girdler
(O. cingulata) chewed only through phloem
tissues, which prevented nutrients from passing
the girdling point. Because twigs were girdled
when nutrients were being removed from leaves
(September), timing of girdling resulted in
optimal nutrient value of twigs (Forcella 1982).
Nutrient reserves in twigs pruned by the oak twig
pruner were not examined, but twigs are pruned
by this species during July and August and fall to
the ground rather immediately (Gosling 1978),
precluding the buildup of nutrients. Alternate
reasons, therefore, may better explain pruning
behaviour in this species.
If larger twigs provide more resources for
larvae and support for female preference of large
twigs is not universal (Cramer 1998; Coppedge
2011; Paro et al. 2014) a possible explanation
for reduced emergence from larger twigs is that
they are better defended by the host plant (Palo
et al. 1992). Girdling branches may help to over-
come plant chemical defences (Paro et al. 2014),
including moisture levels and water potential
(Hanks et al. 1999). The time required to com-
plete a girdle is another likely cost associated with
using larger twigs (Paro et al. 2014), and larvae or
adults might be pinched by twig or branch
movements as the depth of the girdle increases
(W.P.B., personal observation).
While the above considerations could not be
addressed in this observational study, which
included unnatural storage conditions and hapha-
zard twig collection, the occurrence of multiple
larvae in some twigs - including larvae of other
species - suggest a complicated ecology. Gosling
(1978) collected cerambycids other than oak twig
pruners from pruned twigs, but did not provide
further details. Co-inhabitants of more than one
species were also observed in other studies
(Hovore and Penrose 1982; Lemes et al. 2015).
Interspecic competition for food or space within
girdled twigs has been suggested or demonstrated
many times (Linsley 1959; Rogers 1977; Hanks
et al. 1993; Dodds et al. 2001; Lemes et al. 2015).
Intraspecic competition and cannibalism as a
function of increased density has also been
observed (Powell 1982; Akbulut et al. 2004).
Our nding of a rate of parasitism an order of
magnitude greater in twigs holding more than one
Table 1. Descriptions of twig contents that contained more than one individual, live larva, or pupa.
Individual 1 Individual 2 Individual 3 Twig species Cases
Anelaphus parallelus Anelaphus parallelus Red oak 2
Anelaphus parallelus Anelaphus villosus Red oak 1
Anelaphus parallelus Mastogenis crenulatus Liopinus alpha Red oak 1
Anelaphus parallelus Molorchus bimaculatus Black walnut 1
Anelaphus parallelus Anelaphus parallelus (pupa) Black walnut, red oak 14
Anelaphus parallelus Anelaphus parallelus (pupa) Magdalis species Black walnut 1
Anelaphus parallelus Anelaphus parallelus (larva) Red oak 2
Braconidae Anelaphus parallelus (larva) Black walnut 2
Tachinidae Anelaphus parallelus (larva) Red oak 1
Anelaphus parallelus (larva) Molorchus bimaculatus Black walnut 1
Anelaphus parallelus (larva) Magdalis species Black walnut 2
Anelaphus parallelus (live larvae) Red oak 9
Anelaphus parallelus (three live larvae) Red oak 1
Anelaphus parallelus (live pupa) Red oak 1
Note: Individuals listed are adults unless otherwise indicated. Data are from 284 twigs collected in Pennsylvania in 2010 and 118 twigs collected in central New York State in 2012.
4 Can. Entomol. Vol. 00, 2016
© 2016 Entomological Society of Canada
larva or pupa is strongly suggestive of another
general benet of reducing larval density. Twig
pruning behaviours might reduce costs of inter-
specic competition (Gosling 1978), intraspecic
competition, and parasitism while securing
adequate food resources, creating enemy-free or
enemy-reduced space (Jeffries and Lawton 1984).
Acknowledgements
The authors thank Monika Zuee for making the
mesh storage bags and Brutus Brown, Matt Brown,
and Jennie Heckscher for helping to collect pruned
twigs. The editors and two anonymous reviewers
helped improve the quality of this work.
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Brown et al. 5
© 2016 Entomological Society of Canada
... There is a large literature on this topic (see recent review by Dussourd 2017), but few studies examined the costs and benefits of developing in twigs that remained in the canopy or fell to the ground as a result of girdling. Non-exclusive, and sometimes contradictory, hypothesized benefits of developing in twigs on the ground include increased moisture levels (Packard 1890, Linsley 1959, reduced moisture levels (Clarkson 1885), reduced competition from conspecifics or other stem borers (Gosling 1978, Brown et al. 2016, and reduced exposure to parasitoids and predators (Brown et al. 2016). Larvae in girdled branches that fall to the ground in autumn, like those produced by some species of Oncideres, may also benefit from being covered with leaves (Linsley 1959, but see Sanborn 1911. ...
... There is a large literature on this topic (see recent review by Dussourd 2017), but few studies examined the costs and benefits of developing in twigs that remained in the canopy or fell to the ground as a result of girdling. Non-exclusive, and sometimes contradictory, hypothesized benefits of developing in twigs on the ground include increased moisture levels (Packard 1890, Linsley 1959, reduced moisture levels (Clarkson 1885), reduced competition from conspecifics or other stem borers (Gosling 1978, Brown et al. 2016, and reduced exposure to parasitoids and predators (Brown et al. 2016). Larvae in girdled branches that fall to the ground in autumn, like those produced by some species of Oncideres, may also benefit from being covered with leaves (Linsley 1959, but see Sanborn 1911. ...
... Larvae inside of pruned or girdled twigs may be attacked by predators, including birds, mammals, and arthropods, as well as parasitic Hymenoptera and Diptera (Sanborn 1911, Polk and Ueckert 1973, Gosling 1978, Brown et al. 2016. The negative effects of predators and parasitoids were usually not assessed, or not distinguished, from the other effects of experimental treatments in the three experiments described earlier (Sanborn 1911, Polk and Ueckert 1973, Gosling 1978, confounding these potential selective factors of pruning and girdling behaviors with environmental variables and twig placement. ...
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... Anelaphus parallelus individuals were collected as larvae in 2010, 2012, 2014, 2016, and 2018 in fallen twigs pruned from living oaks and walnuts in southeastern Pennsylvania and central New York (Brown et al. 2016;Brown and Dombroskie 2019). The appearance of the pruned twig is diagnostic, preventing potential confusion with Anelaphus villosus (Fabricius) (Gosling 1978(Gosling , 1981. ...
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