Attraction of Pollinators to Atemoya (Annona squamosa ×

Annona cherimola) in Puerto Rico Using Commercial Lures and

Food Attractants
Author(s): David A. Jenkins, Christian Millan-Hernandez, Andrew R. Cline,
Thomas C. McElrath, Brian Irish, and Ricardo Goenaga
Source: Journal of Economic Entomology, 108(4):1923-1929.
Published By: Entomological Society of America
URL: http://www.bioone.org/doi/full/10.1093/jee/tov136

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 HORTICULTURAL ENTOMOLOGY

Attraction of Pollinators to Atemoya (Annona

squamosa 3 Annona cherimola) in Puerto Rico Using
Commercial Lures and Food Attractants
DAVID A. JENKINS,1,2,4 CHRISTIAN MILLAN-HERNANDEZ,1 ANDREW R. CLINE,2
THOMAS C. MCELRATH,3 BRIAN IRISH,1 AND RICARDO GOENAGA1

J. Econ. Entomol. 108(4): 1923–1929 (2015); DOI: 10.1093/jee/tov136

ABSTRACT Atemoya is a hybrid between Annona squamosa L. and Annona cherimola Miller (Annona-
ceae) and has potential to be an important fruit crop in tropical and subtropical areas. A major impedi-
ment to fruit production is low fruit set due to inadequate pollinator visits, typically, by beetles in the
family Nitidulidae. We used Universal moth traps to monitor the attractiveness of two commercially
available Nitidulidae lures in combination with various food attractants, including raw bread dough, ap-
ple juice, and malta beverage, a soft drink by-product of the brewing process. The most commonly
trapped beetles were, in order of decreasing frequency, Carpophilus dimidiatus (F.), Brachypeplus muti-
latus Erichson, Urophorus humeralis (F.) (Coleoptera: Nitidulidae), and Europs fervidus Blatchley
(Coleoptera: Monotomidae). All traps, except the unbaited control traps, caught beetles. In a previous
study, we found that combining two commercial lures had a synergistic effect on the attraction of these
beetle species. In this study, the addition of food attractants increased the number of beetles trapped
compared with traps baited with only the commercial lures. Also, food attractants appear to be key in at-
tracting U. humeralis; only one U. humeralis individual of the 206 caught during the experiment was
trapped without a food attractant. The variation between the number of beetles caught in traps contain-
ing the same treatments was high and may explain the erratic results reported in other studies of pollina-
tion in Annona spp. The results are discussed with respect to the use of nitidulid lures and food
attractants to increase fruit set in atemoya and other Annonaceae.

KEY WORDS Europs fervidus, Monotomidae, Nitidulidae, Annonaceae, pollinator

Atemoya, Annona squamosa L.  Annona cherimola
Miller (Annonaceae), is a hybrid between the sugar ap-
ple, A. squamosa, and the cherimoya, A. cherimola.
Production of atemoya and other Annona spp. is con-
strained by poor fruit set (Gazit et al. 1982, Morton
1987, Peña et al. 2002). Atemoya flowers, like other
members of the Annonaceae, have female and male
parts, but the stigma is receptive before pollen is re-
leased by the anthers (Morton 1987, Zomlefer 1994,
Nakasone and Paull 1998). Combined with limited pol-
linator visits, this floral ontogeny often results in unfer-
tilized carpels (Nadel and Peña 1994). Hand
pollination is practiced in many areas where atemoya
and other annonaceous crops are grown to increase
fruit set (Saavedra 1977, Escobar et al. 1986, Morton
1987, Melo et al. 2004), but it is labor-intensive and
expensive.
1
USDA-ARS-Tropical Agriculture Research Station, 2200 Ave.,
P.A. Campos, Ste. 201, Mayaguez 00680, Puerto Rico.
2
California Department of Food and Agriculture, Plant Health &
Pest Prevention Services, 3294 Meadowview Rd., Sacramento, CA
95832.
3
Department of Entomology, University of Georgia, 413 Biological
Sciences Bldg., Athens, GA 30602.
4
Corresponding author, e-mail: david.jenkins@ars.usda.gov.
Published by Oxford University Press on behalf of Entomological Society of America 2015.
This work is written by US Government employees and is in the public domain in the US.
Atemoya and the related cherimoya are successfully
pollinated in Israel by the nitidulid species Carpophilus
hemipterus (L.), Carpophilus mutilatus Erichson, Uro-
phorus humeralis (F.), and Epuraea luteola Erichson
(Gazit et al. 1982). Additional species of nitidulids are
important in pollinating atemoya in the United States
and Australia, including Carpophilus nepos Murray
[Carpophilus freemani Dobson], Carpophilus marginel-
lus Motschulsky, Carpophilus fumatus Boheman, Carpo-
philus maculatus Murray, Carpophilus pilosellus
Motschulsky, Carpophilus dimidiatus (F.), Lobiopa insu-
laris (Castelnau), and Colopterus posticus (Erichson)
(George et al. 1989, Nagel et al. 1989, Nadel and Peña
1994, Blanche and Cunningham 2005). Eight of the
above species (C. hemipterus, C. dimidiatus,
U. humeralis, L. insularis, and E. luteola) have all been
reported from Puerto Rico (Wolcott 1948, Jenkins et al.
2013) and a survey of atemoya flowers revealed that
C. dimidiatus and E. luteola are visitors to atemoya flow-
ers in Puerto Rico, along with Europs fervidus Blatchley
(Coleoptera: Monotomidae) and Loberus testaceus Reit-
ter (Coleoptera: Erotylidae) (Jenkins et al. 2013).
Nitidulid beetles often respond to aggregation pher-
omones of other nitidulid beetles that feed on similar
substrates. The aggregation pheromone of C. hemipte-
rus was found to be attractive to several other nitidulid
beetles, including C. mutilatus, Carpophilus lugubris
1924 JOURNAL OF ECONOMIC ENTOMOLOGY
Murray, Carpophilus obsoletus Erichson, U. humeralis
(Bartelt et al. 1992), and Carpophilus davidsoni (James
et al. 1994). Similarly, Carpophilus brachypterus (Say)
and C. hemipterus are mutually attracted to each
other’s aggregation pheromones (Williams et al. 1995).
In many cases, responses to pheromones of other spe-
cies can be explained by common pheromone compo-
nents (Williams et al. 1995), but pheromones may also
act as kairomones for nitidulid beetles (Bartelt et al.
1993).
Recent trials in Puerto Rico demonstrated that
commercially available lures for Nitidulidae attracted
three species of potential pollinators: C. dimidiatus,
Brachypeplus mutilatus Erichson, and a Europs
sp. (Jenkins et al. 2013), which we have since identified
as Eu. fervidus. This attraction increased with dose
(number of lures) and the combination of the two lures
attracted more beetles than would be expected if the
effect was additive. Food odors synergize the attractive-
ness of aggregation pheromones (Lin et al. 1992).
When combined with aggregation pheromone lures,
raw bread dough has been effective at attracting niti-
dulid beetles (James et al. 1997, Peña et al. 1999), as
has apple juice (James et al. 1998). Although we saw
substantial attraction of nitidulids to lures without food
attractants (Jenkins et al. 2013), we wanted to deter-
mine how the addition of food attractants would affect
the number of beetles trapped, as well as determine
the food attractant that was most effective in attracting
potential pollinators into atemoya orchards.
Materials and Methods
The experimental site, located at the USDA-ARS-
Tropical Agriculture Research Experiment Station in
Isabela, Puerto Rico, was an orchard containing 13 ate-
moya and other Annona hybrids planted in three blocks
with two trees of each variety in each block. Each block
was surrounded by a row of Annona squamosa L.
(Annonaceae). The orchard was planted in May 2001,
and the trees were 11 yr old at the time of the
experiments.
Fifty-five Universal moth traps (Great Lakes IPM,
Vestaburg, MI) were hung 1.5 to 2 m above the ground
from randomly selected trees throughout the orchard,
excluding trees on the borders and separated by at least
one tree without a trap between trees with traps. Each
trap was assigned a lure treatment and a food attractant
treatment. Lure treatments included 1) four dusky sap
beetle lures (Great Lakes IPM, Vestaburg, MI); 2) four
date plus fig blend lures (Great Lakes IPM, Vestaburg,
MI); 3) or four of both lures for a total of eight lures.
Food attractant treatments included 1) 2–3 cm3 raw
bread dough (all purpose flour, salt, water, and yeast),
2) 100% apple juice (Mott’s 100% Juice), or 3) malta
beverage (Malta India brand). One set of traps was as-
signed the combined lure treatment (see lure treatment
number 3 above), but no food attractant treatment.
The dusky sap beetle lure is specifically designed to at-
tract C. lugubris, whereas the date plus fig blend lure
is specifically designed to attract C. hemipterus,
Vol. 108, no. 4
C. mutilatus, and C. freemani. We had 11 treatments
including unbaited controls:
A. dusky sap beetle lure þ apple juice
B. date and fig blend lure þ apple juice
C. dusky sap beetle lure þ date and fig blend
lure þ apple juice
D. dusky sap beetle lure þ malta
E. date and fig blend lure þ malta
F. dusky sap beetle lure þ date and fig blend
lure þ malta
G. dusky sap beetle þ raw bread dough
H. date and fig blend lure þ raw bread dough
I. dusky sap beetle lure þ date and fig blend
lure þ raw bread dough
J. dusky sap beetle lure þ date and fig blend lure
K. unbaited controls
Each treatment was replicated five times and the ex-
periment was conducted on 8 November 2012, and re-
peated on 1 February 2013. Both repetitions were
conducted when no flowers were observed on trees
within the orchard to remove the effects of floral attrac-
tion. In both repetitions, the lures were suspended
above the trap. The raw bread dough was placed in a
30-ml plastic Solo cup hot-glued to the bottom of the
Universal trap. The apple juice and malta lures were
deployed in different manners in 2012 and 2013. In
2012, traps assigned to receive apple juice or malta re-
ceived 300 ml of the fluid directly into the bottom of
the trap with a few drops of detergent (a surfactant to
break the surface tension of the water, allowing the
beetles to sink). In the remaining treatments, 300 ml of
tap water was added to the bottom of the trap and a
few drops of detergent added. Because the malta and
apple juice obscured the beetles and made extracting
them difficult, in 2013, all traps used 300 ml of water
with detergent as the trap fluid and 20 ml of the apple
juice and malta were poured into a 30-ml Solo cup hot-
glued to the bottom of the trap.
Traps were left for 1 wk, after which all of the beetles
in each trap were placed in labeled plastic vials containing
70% EtOH and returned to the laboratory to be identi-
fied under the stereoscope. Beetles were stored in alcohol
and subsequently identified by A.R.C., an authority on
Nitidulidae, and cucujoid beetles in general, or T.C.M.,
an authority on Monotomidae beetles. Voucher speci-
mens were deposited in the California State Collection of
Arthropods (Nitidulidae) and in the University of Georgia
Collection of Arthropods (Monotomidae).
Statistical Analyses. The number of individuals of
each species was tallied for each treatment, and treat-
ments were ranked according the number of beetles
trapped for each year. Chi-square analyses were con-
ducted to test the null hypothesis that the frequency of
beetles was equal among treatments. When chi-square
analyses determined that the distributions of beetles
were not equal, we would remove the treatment(s) that
differed most from the remainder and repeat the analy-
ses on the remaining treatments until we had clustered
the treatments into groups that chi-square analyses
failed to reject the hypothesis that beetles were equally
distributed among the remaining treatments.
August 2015 JENKINS ET AL.: ATTRACTING NITIDULID POLLINATORS IN PUERTO RICO 1925

Results treatments containing bread dough and date fig blend

lure and bread dough with both lures combined
In total, 783 beetles were trapped in the 2012 repeti-
attracted significantly more C. dimidiatus than the
tion and 1,470 beetles were trapped in the 2013 repeti-
other lure types assayed (Table 5).
tion. Beetles trapped included six species: C.
In the 2012 trial, B. mutilatus was most abundant in
dimidiatus, B. mutilatus, U. humeralis, Eu. fervidus, E.
the bread dough and date and fig blend lure (Table 6).
luteola, and L. insularis. C. dimidiatus was the most
In the 2013 trial, the treatment containing apple juice
abundant beetle both years (368 and 774 in 2012 and
and date and fig blend lure attracted the most B. muti-
2013, respectively), followed by B. mutilatus (242 and
latus (Table 6).
576 in 2012 and 2013, respectively), U. humeralis (148
In the 2012 trial, U. humeralis was most abundant in
and 60 in 2012 and 2013, respectively), and Eu. fervi-
treatments containing apple juice combined with the
dus (25 and 54 in 2012 and 2013, respectively). Four
dusky sap lure and apple juice combined with the date
E. luteola and two Lobiopa insularis were trapped, all
and fig blend lure (Table 7). In the 2013 trial, too few
in 2013.
U. humeralis were trapped to see any patterns (Table 7).
No beetles were caught in the control traps baited
This was the only beetle trapped in any amount that
with no food attractants or lures, while all other combina-
was not a nitidulid. Too few Eu. fervidus were trapped
tions did attract some beetles (Tables 1–4). The number
in 2012 to make meaningful conclusions, but bread
of beetles attracted to a specific lure varied greatly (Tables
dough in combination with any of the lure types
1–4). For each beetle species, some food attractant and
attracted numerically more beetles than other treat-
lure combinations attracted numerically more beetles
ments (Table 8).
than others, but these were not consistent between years.
C. dimidiatus was the most commonly trapped bee-
tle in both years of the study. In the 2012 trial, C. dimi-
Discussion
diatus was most commonly trapped in treatments
containing malta with both lures combined, bread In a previous experiment where only lures were
dough with the date and fig blend lure, and malta with used and no food attractants (Jenkins et al. 2013), the
the date and fig blend lure (Table 5). In the 2013 trial, combined lures were most attractive. However, when

Table 1. Mean number (SEM) of C. dimidiatus trapped in uni- Table 3. Mean number (SEM) of U. humeralis trapped in uni-
versal traps baited with various combinations of food attractants versal traps baited with various combinations of food attractants
and nitidulid lures in the two years (n ¼ 5) and nitidulid lures in the two years (n ¼ 5)

C. dimidiatus U. humeralis
Food attractant Lure 2012 2013 Food attractant Lure 2012 2013
Apple juice Dusky sap beetle 2.0 (0.9) 5.4 (2.5) Apple juice Dusky sap beetle 9.8 (6.3) 1.8 (0.7)
Date and fig blend 7.8 (3.9) 16.4 (3.6) Date and fig blend 7.2 (1.3) 0.2 (0.2)
Combined 6.8 (2.7) 8.8 (1.6) Combined 4.4 (1.2) 1.0 (0.8)
Malta Dusky sap beetle 0.6 (0.3) 1.4 (0.9) Malta Dusky sap beetle 1.2 (0.7) 0.0 (0.0)
Date and fig blend 12.4 (8.0) 6.0 (2.0) Date and fig blend 2.6 (0.8) 0.0 (0.0)
Combined 17.6 (12.3) 11.4 (2.8) Combined 2.6 (0.7) 1.4 (0.5)
Bread dough Dusky sap beetle 1.2 (0.4) 10.4 (4.1) Bread dough Dusky sap beetle 0.6 (0.6) 2.2 (1.0)
Date and fig blend 16.2 (8.8) 49.4 (7.6) Date and fig blend 0.6 (0.4) 3.0 (2.5)
Combined 5.4(1.8) 45.0 (14.5) Combined 0.6 (0.2) 1.8 (1.2)
None Combined (Treatment J) 1.2 (0.4) 0.2 (0.2) None Combined (Treatment J) 0.0 (0.0) 0.2 (0.2)
None 0.0 (0.0) 0.0 (0.0) None 0.0 (0.0) 0.0 (0.0)

Table 2. Mean number (SEM) of B. mutilatus trapped in uni- Table 4. Mean number (SEM) of Eu. fervidus trapped in univer-
versal traps baited with various combinations of food attractants sal traps baited with various combinations of food attractants and
and nitidulid lures in the two years (n ¼ 5) nitidulid lures in the two years (n ¼ 5)

Brachypeplus sp. Europs sp.

Food attractant Lure 2012 2013 Food attractant Lure 2012 2013
Apple juice Dusky sap beetle 4.2 (0.8) 15.0 (7.3) Apple juice Dusky sap beetle 0.4 (0.2) 0.2 (0.2)
Date and fig blend 2.6 (0.7) 20.6 (4.6) Date and fig blend 0.6 (0.4) 0.2 (0.2)
Combined 5.0 (0.9) 15.2 (10.2) Combined 0.0 (0.0) 0.6 (0.6)
Malta Dusky sap beetle 3.0 (1.0) 1.0 (0.3) Malta Dusky sap beetle 0.0 (0.0) 0.4 (0.2)
Date and fig blend 3.2 (0.5) 2.2 (1.0) Date and fig blend 0.8 (0.6) 1.0 (0.8)
Combined 4.8 (1.7) 15.6 (2.8) Combined 1.0 (1.0) 0.4 (0.4)
Bread dough Dusky sap beetle 4.0 (2.1) 9.0 (2.6) Bread dough Dusky sap beetle 0.4 (0.4) 2.4 (0.9)
Date and fig blend 7.6 (1.3) 12.8 (3.2) Date and fig blend 1.0 (0.4) 3.0 (1.3)
Combined 5.0 (2.8) 13.0 (4.8) Combined 0.8 (0.4) 2.6 (1.4)
None Combined (Treatment J) 3.0 (1.3) 3.6 (2.4) None Combined (Treatment J) 0.0 (0.0) 0.0 (0.0)
None 0.0 (0.0) 0.0 (0.0) None 0.0 (0.0) 0.0 (0.0)
1926 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 108, no. 4

Table 5. Total number of C. dimidiatus trapped in 11 treatments in the two years

Carpophilus dimidiatus
2012 2013
Treatment No. Treatment No.
a
Combined lures þ malta 88 Date and fig lure þ raw dough 247e
Date and fig lure þ raw dough 81 Combined lures þ raw dough 225
Date and fig lure þ malta 62 Date and fig lure þ apple juice 82f
Date and fig lure þ apple juice 39b Combined lures þ malta 57g
Combined lures þ apple juice 34 Dusky sap beetle lure þ raw dough 52
Combined lures þ raw dough 27 Combined lures þ apple juice 44
Dusky sap beetle lure þ apple juice 10c Date and fig lure þ malta 30h
Combined lures (Treatment J) 6 Dusky sap beetle lure þ apple juice 27
Dusky sap beetle lure þ raw dough 6 Dusky sap beetle lure þ malta 7i
Dusky sap beetle lure þ malta 3 Combined lures (Treatment J) 1
Unbaited controls 0d Unbaited controls 0
Treatments are ranked by their attractiveness and are grouped (alternating shaded and unshaded fields) within years according to similarity, as
determined by chi-square tests comparing observed values to the values we would expect if the beetles were distributed evenly among the treat-
ments. See text for explanation of treatments.
a 2
v value ¼ 4.701; df ¼ 2; P ¼ 0.09531.
b 2
v value ¼ 2.18; df ¼ 2; P ¼ 0.3362.
c 2
v value ¼ 3.96; df ¼ 3; P ¼ 0.2658.
d
When included with the group above, v2 value ¼ 11.2; df ¼ 4; P ¼ 0.02441.
e 2
v value ¼ 1.03; df ¼ 1; P ¼ 0.3112.
f
When included in the group above, v2 value ¼ 86.93; df ¼ 2; P < 2.2e-16; when included with the group below, v2 value ¼ 13.73; df ¼ 3;
P ¼ 0.0033.
g 2
v value ¼ 1.69; df ¼ 2; P ¼ 0.4304.
h 2
v value ¼ 0.16; df ¼ 1; P ¼ 0.6911.
I 2
v value ¼ 10.75; df ¼ 2; P ¼ 0.0046.

Table 6. Total number of B. mutilatus trapped in 11 treatments in the two years

Brachypeplus sp.
2012 2013
Treatment No. Treatment No.
a
Date and fig lure þ raw dough 38 Date and fig lure þ apple juice 103d
Combined lures þ apple juice 25b Combined lures þ malta 78e
Combined lures þ raw dough 25 Combined lures þ apple juice 76
Combined lures þ malta 24 Dusky sap beetle lure þ apple juice 75
Dusky sap beetle lure þ apple juice 21 Combined lures þ raw dough 65
Dusky sap beetle lure þ raw dough 20 Date and fig lure þ raw dough 64
Date and fig lure þ malta 16 Dusky sap beetle lure þ raw dough 45f
Dusky sap beetle lure þ malta 15 Combined lures (Treatment J) 18g
Combined lures (Treatment J) 15 Date and fig lure þ malta 11h
Date and fig lure þ apple juice 13 Dusky sap beetle lure þ malta 5
Unbaited controls 0c Unbaited controls 0i
Treatments are ranked by their attractiveness and are grouped (alternating shaded and un-shaded fields) within years according to similarity,
as determined by chi-square tests comparing observed values to the values we would expect if the beetles were distributed evenly among the
treatments. See text for explanation of treatments.
a
When included in the group below, v2 value ¼ 23.19; df ¼ 9; P ¼ 0.0058.
b 2
v value ¼ 9.21; df ¼ 8; P ¼ 0.3251.
c
When included in the group above, v2 value ¼ 29.56; df ¼ 9; P ¼ 0.0005.
d
When included in the group below, v2 value ¼ 12.95; df ¼ 5; P ¼ 0.0239.
e 2
v value ¼ 2.42; df ¼ 4; P ¼ 0.6592.
f
When included in the group above, v2 value ¼ 11.36; df ¼ 5; P ¼ 0.0447; when included in the group below, v2 value ¼ 11.57; df ¼ 1;
P ¼ 0.0007.
g
When included in the group above, v2 value ¼ 7.47; df ¼ 2; P ¼ 0.02387.
h 2
v value ¼ 2.25; df ¼ 1; P ¼ 0.1336; Treatment “I” also groups with treatment “B,” v2 value ¼ 1.69; df ¼ 2; P ¼ 0.1936.
i
When included with the group above, v2 value ¼ 11.38; df ¼ 2; P ¼ 0.0034.

food attractants were combined with lures, even single
lures, this combination attracted more beetles than the
combined lures without food attractants. This suggests
that food attractants used in combination with lures are
much more powerful attractants than lures alone and
may be important in drawing potential pollinators from
other attractants, such as rotten fruit. Treatments
baited only with lures and no food attractants did not
trap U. humeralis (Jenkins et al. 2013), but U. humera-
lis was commonly trapped during both trials of this
experiment when food attractants were combined with
lures (Tables 3 and 7).
The rankings of lure and food attractant combina-
tions by their ability to attract given species were not
August 2015 JENKINS ET AL.: ATTRACTING NITIDULID POLLINATORS IN PUERTO RICO 1927

Table 7. Total number of U. humeralis trapped in 11 treatments in the two years

U. humeralis
2012 2013
Treatment No. Treatment No.
a
Dusky sap beetle lure þ apple juice 49 Date and fig lure þ raw dough 15d
Date and fig lure þ apple juice 36 Dusky sap beetle lure þ raw dough 11
Combined lures þ apple juice 22b Combined lures þ raw dough 9
Combined lures þ malta 13 Dusky sap beetle lure þ apple juice 9
Date and fig lure þ malta 13 Combined lures þ malta 7
Dusky sap beetle lure þ malta 6c Combined lures þ apple juice 5
Dusky sap beetle lure þ raw dough 3 Combined lures (Treatment J) 1e
Date and fig lure þ raw dough 3 Date and fig lure þ apple juice 1
Combined lures þ raw dough 3 Dusky sap beetle lure þ malta 0
Combined lures (Treatment J) 0 Date and fig lure þ malta 0
Unbaited controls 0 Unbaited controls 0
Treatments are ranked by their attractiveness and are grouped (alternating shaded and un-shaded fields) within years according to similarity,
as determined by chi-square tests comparing observed values to the values we would expect if the beetles were distributed evenly among the
treatments. See text for explanation of treatments.
a 2
v value ¼ 1.98; df ¼ 1; P ¼ 0.1585.
b 2
v value ¼ 3.375; df ¼ 2; P ¼ 0.185.
c 2
v value ¼ 10.20; df ¼ 5; P ¼ 0.0698.
d 2
v value ¼ 6.36; df ¼ 5; P ¼ 0.273.
e
When included in the group above, v2 value ¼ 52.76; df ¼ 10; P ¼ 8.26E-08.

Table 8. Total number of Eu. fervidus trapped in 11 treatments in the two years

Europs sp.
2012 2013
Treatment No. Treatment No.
Combined lures þ malta 5a Date and fig lure þ raw dough 15c
Date and fig lure þ raw dough 5 Combined lures þ raw dough 13
Combined lures þ raw dough 4 Dusky sap beetle lure þ raw dough 12
Date and fig lure þ malta 4 Date and fig lure þ malta 5d
Date and fig lure þ apple juice 3 Combined lures þ apple juice 3
Dusky sap beetle lure þ raw dough 2 Dusky sap beetle lure þ malta 2
Dusky sap beetle lure þ apple juice 2 Combined lures þ malta 2
Dusky sap beetle lure þ malta 0b Dusky sap beetle lure þ apple juice 1
Combined lures (Treatment J) 0 Date and fig lure þ apple juice 1
Combined lures þ apple juice 0 Combined lures (Treatment J) 0
Unbaited controls 0 Unbaited controls 0
Treatments are ranked by their attractiveness and are grouped (alternating shaded and un-shaded fields) within years according to similarity,
as determined by chi-square tests comparing observed values to the values we would expect if the beetles were distributed evenly among the
treatments. See text for explanation of treatments.
a 2
v value ¼ 2.72; df ¼ 6; P ¼ 0.8431.
b
When included in the group above, v2 value ¼ 18.56; df ¼ 10; P ¼ 0.0462.
c 2
v value ¼ 0.35; df ¼ 2; P ¼ 0.8395.
d 2
v value ¼ 11.14; df ¼ 7; P ¼ 0.1325.

consistent between years, suggesting that most lure and
food attractant combinations will serve to bring poten-
tial pollinators to the orchard. However, there are some
important trends. Lures combinations containing date
and fig blend, either alone or in combination with
dusky sap beetle lures, attracted more C. dimidiatus
than lures containing only dusky sap beetle lure in both
2012 and 2013. This was also true for the B. mutilatus
that was trapped. When lures were tested without food
attractants (Jenkins et al. 2013), the date and fig lure
consistently attracted more beetles than the dusky sap
beetle lure. This should be taken into consideration by
atemoya growers in Puerto Rico that wish to adopt the
lure method to increase pollination.
A previous survey determined that Eu. fervidus was
the most common visitor to atemoya flowers in Puerto
Rico and that this species responded, albeit weakly, to
lures for nitidulids (Jenkins et al. 2013). The addition
of food attractants, particularly raw dough, increased
the numbers trapped, but the attraction was still weak
(Tables 4 and 8). These beetles are likely responding to
yeasts present in the raw dough. However, the type of
yeast present may not be the most preferred yeast for
successful larval development and the yeast may not be
in sufficient quantity. A recent study indicated that
although adults and larvae of the nitidulid species Bra-
chypeplus glaber LeConte may reside within the same
microhabitat, i.e., the restricted confines of sabal palm
inflorescence stalks, there was niche partitioning of the
fungi–yeasts between the adult and larval life stages
(Cline et al. 2014). This phenomenon may be occurring
more broadly within other saprophagous lineages such
1928 JOURNAL OF ECONOMIC ENTOMOLOGY
as Europs, but remains untested. Monotomids may or
may not be closely related to Nitidulidae (Bousquet
2009), and their attraction to nitidulid lures may only
be because of convergent food sources that give off
similar chemical signals.
Except for U. humeralis, all beetles were more com-
mon in the 2013 experiment. This may be because of
population fluctuations; most of these species utilize the
same or similar resources, i.e., rotten fruit, and so it is
likely that populations would track resource availability.
The differences in populations could also be because of
different baiting methods. In 2012, the treatments con-
taining apple juice or malta used these as trap fluid,
whereas in 2013, a much smaller amount (20 ml vs.
300 ml) of the liquid food attractants was used. We dis-
count the possibility that the dark trap fluid in the first
experiments (apple juice and malta) did not allow us to
find all of the beetles; a strainer was used to remove all
solids and we are confident that all beetles in the trap
fluid were counted. There was considerable fungal and
bacterial growth in the apple juice and malta treatments
when they were used as trap fluids and this may have
influenced the number of beetles trapped.
Although previous work (Jenkins et al. 2013) demon-
strated that commercial nitidulid lures attracted poten-
tial pollinators, especially when combined, this work
demonstrates that the addition of food lures, including
bread dough, apple juice, or malta, are more attractive
than the lures alone. The addition a food attractant also
attracts an additional species in Puerto Rico; only one
U. humeralis of 206 individuals trapped was caught in a
trap that did not have a food attractant. This additional
species may also be, albeit to a lesser extent, valuable
as a pollinator in this system.
Finally, the wide variation in number of beetles
trapped within a treatment is informative. Although
there were not enough replicates to test for block effects
within treatments, more C. dimidiatus were trapped in
the western-most section of the orchard (mean of
10.25 6 2.6 SEM in 2012) than in the other two section
(means of 4.06 6 4.1 SEM and 2.4 6 2.4 SEM in 2012
for sections 2 and 3, respectively). The first section is
downwind from the other two sections and there is a
consistent wind from the east–northeast at the site. The
beetles may be orienting to the attractant volatiles, arriv-
ing in the orchard, but not moving further in, despite
the presence of additional attractants in those other
areas. If so, this will have consequences for lure or
attractant deployment to increase fruit set and should be
explored further. A concentration gradient, i.e., more
attractants or lures used further upwind, may help to
offset the skewed distribution of potential pollinators
arriving in an orchard. Thus, deployment of attractants
must take into account local physiographic conditions
such as prevailing winds and landscape formations
(deep valleys, etc., where volatiles may persist or
become more concentrated) and adjusted accordingly.
In summary, the addition of food attractants to com-
mercially available nitidulid lures attracted a variety of
potential pollinators to an atemoya orchard in Puerto
Rico. The high variability within trap catch suggests
that further study on the orientation, temporal and
Vol. 108, no. 4
spatial variation, flight, and arresting behavior of these
potential pollinators is needed.
Acknowledgments
We thank Katherine Parys, Carey Minteer, and two anony-
mous reviewers for helpful comments that improved an earlier
version of this manuscript. We also thank Zaid Abdo, Statistician
for the USDA-ARS South Atlantic Area. This manuscript
presents the results of research only; any mention of a propriet-
ary product does not constitute endorsement by the USDA.
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