Attraction of Pollinators to Atemoya (Annona Squamosa 3 Annona Cherimola) in Puerto Rico Using Commercial Lures and Food Attractants

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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 3 1 1 THOMAS C. MCELRATH, BRIAN IRISH, AND RICARDO GOENAGA Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020

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, apple 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 mutilatus 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 attracting 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 containing the same treatments was high and may explain the erratic results reported in other studies of pollination 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 Atemoya and the related cherimoya are successfully Miller (Annonaceae), is a hybrid between the sugar ap- pollinated in Israel by the nitidulid species Carpophilus ple, A. squamosa, and the cherimoya, A. cherimola. hemipterus (L.), Carpophilus mutilatus Erichson, Uro- Production of atemoya and other Annona spp. is con- phorus humeralis (F.), and Epuraea luteola Erichson strained by poor fruit set (Gazit et al. 1982, Morton (Gazit et al. 1982). Additional species of nitidulids are 1987, Penã et al. 2002). Atemoya flowers, like other important in pollinating atemoya in the United States members of the Annonaceae, have female and male and Australia, including Carpophilus nepos Murray parts, but the stigma is receptive before pollen is re- [Carpophilus freemani Dobson], Carpophilus marginel- leased by the anthers (Morton 1987, Zomlefer 1994, lus Motschulsky, Carpophilus fumatus Boheman, Carpo- Nakasone and Paull 1998). Combined with limited pol- philus maculatus Murray, Carpophilus pilosellus linator visits, this floral ontogeny often results in unfer- Motschulsky, Carpophilus dimidiatus (F.), Lobiopa insu- tilized carpels (Nadel and Penã 1994). Hand laris (Castelnau), and Colopterus posticus (Erichson) pollination is practiced in many areas where atemoya (George et al. 1989, Nagel et al. 1989, Nadel and Penã and other annonaceous crops are grown to increase 1994, Blanche and Cunningham 2005). Eight of the fruit set (Saavedra 1977, Escobar et al. 1986, Morton above species (C. hemipterus, C. dimidiatus, 1987, Melo et al. 2004), but it is labor-intensive and U. humeralis, L. insularis,andE. luteola) have all been expensive. reported from Puerto Rico (Wolcott 1948, Jenkinsetal. 2013) and a survey of atemoya flowers revealed that C. dimidiatus and E. luteola are visitors to atemoya flowers in Puerto Rico, along with Europs fervidus Blatchley 1 USDA-ARS-Tropical Agriculture Research Station, 2200 Ave., (Coleoptera: Monotomidae) and Loberus testaceus Reit- P.A. Campos, Ste. 201, Mayaguez 00680, Puerto Rico. ter (Coleoptera: Erotylidae) (Jenkinsetal.2013). 2 California Department of Food and Agriculture, Plant Health & Nitidulid beetles often respond to aggregation pher- Pest Prevention Services, 3294 Meadowview Rd., Sacramento, CA omones of other nitidulid beetles that feed on similar 95832. 3 Department of Entomology, University of Georgia, 413 Biological substrates. The aggregation pheromone of C. hemipte- Sciences Bldg., Athens, GA 30602. rus was found to be attractive to several other nitidulid 4 Corresponding author, e-mail: [email protected]. beetles, including C. mutilatus, Carpophilus lugubris

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. 1924 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 108, no. 4

Murray, Carpophilus obsoletus Erichson, U. humeralis C. mutilatus,andC. freemani. We had 11 treatments (Bartelt et al. 1992), and Carpophilus davidsoni (James including unbaited controls: et al. 1994). Similarly, Carpophilus brachypterus (Say) A. dusky sap beetle lure þ apple juice and C. hemipterus are mutually attracted to each B. date and fig blend lure þ apple juice other’s aggregation pheromones (Williams et al. 1995). C. dusky sap beetle lure þ date and fig blend In many cases, responses to pheromones of other spe- lure þ apple juice cies can be explained by common pheromone compo- D. dusky sap beetle lure þ malta nents (Williams et al. 1995), but pheromones may also E. date and fig blend lure þ malta act as kairomones for nitidulid beetles (Bartelt et al. F. dusky sap beetle lure þ date and fig blend 1993). lure þ malta Recent trials in Puerto Rico demonstrated that

G. dusky sap beetle þ raw bread dough Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020 commercially available lures for Nitidulidae attracted H. date and fig blend lure þ raw bread dough three species of potential pollinators: C. dimidiatus, I. dusky sap beetle lure þ date and fig blend Brachypeplus mutilatus Erichson, and a Europs lure þ raw bread dough sp. (Jenkins et al. 2013), which we have since identified J. dusky sap beetle lure þ date and fig blend lure as Eu. fervidus. This attraction increased with dose K. unbaited controls (number of lures) and the combination of the two lures attracted more beetles than would be expected if the Each treatment was replicated five times and the ex- effect was additive. Food odors synergize the attractive- periment was conducted on 8 November 2012, and re- ness of aggregation pheromones (Lin et al. 1992). peated on 1 February 2013. Both repetitions were When combined with aggregation pheromone lures, conducted when no flowers were observed on trees raw bread dough has been effective at attracting niti- within the orchard to remove the effects of floral attrac- dulid beetles (Jamesetal.1997, Pen˜a et al. 1999), as tion. In both repetitions, the lures were suspended has apple juice (James et al. 1998). Although we saw above the trap. The raw bread dough was placed in a substantial attraction of nitidulids to lures without food 30-ml plastic Solo cup hot-glued to the bottom of the attractants (Jenkins et al. 2013), we wanted to deter- Universal trap. The apple juice and malta lures were mine how the addition of food attractants would affect deployed in different manners in 2012 and 2013. In the number of beetles trapped, as well as determine 2012, traps assigned to receive apple juice or malta re- the food attractant that was most effective in attracting ceived 300 ml of the fluid directly into the bottom of potential pollinators into atemoya orchards. 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 Materials and Methods few drops of detergent added. Because the malta and The experimental site, located at the USDA-ARS- apple juice obscured the beetles and made extracting Tropical Agriculture Research Experiment Station in them difficult, in 2013, all traps used 300 ml of water Isabela, Puerto Rico, was an orchard containing 13 ate- with detergent as the trap fluid and 20 ml of the apple moya and other Annona hybrids planted in three blocks juice and malta were poured into a 30-ml Solo cup hot- with two trees of each variety in each block. Each block glued to the bottom of the trap. was surrounded by a row of Annona squamosa L. Traps were left for 1 wk, after which all of the beetles (Annonaceae). The orchard was planted in May 2001, in each trap were placed in labeled plastic vials containing and the trees were 11 yr old at the time of the 70% EtOH and returned to the laboratory to be identi- experiments. fied under the stereoscope. Beetles were stored in alcohol Fifty-five Universal moth traps (Great Lakes IPM, and subsequently identified by A.R.C., an authority on Vestaburg, MI) were hung 1.5 to 2 m above the ground Nitidulidae, and cucujoid beetles in general, or T.C.M., from randomly selected trees throughout the orchard, an authority on Monotomidae beetles. Voucher speci- excluding trees on the borders and separated by at least mens were deposited in the California State Collection of one tree without a trap between trees with traps. Each Arthropods (Nitidulidae) and in the University of Georgia trap was assigned a lure treatment and a food attractant Collection of Arthropods (Monotomidae). treatment. Lure treatments included 1) four dusky sap Statistical Analyses. The number of individuals of beetle lures (Great Lakes IPM, Vestaburg, MI); 2) four each species was tallied for each treatment, and treat- date plus fig blend lures (Great Lakes IPM, Vestaburg, ments were ranked according the number of beetles MI); 3) or four of both lures for a total of eight lures. trapped for each year. Chi-square analyses were con- Food attractant treatments included 1) 2–3 cm3 raw ducted to test the null hypothesis that the frequency of bread dough (all purpose flour, salt, water, and yeast), beetles was equal among treatments. When chi-square 2) 100% apple juice (Mott’s 100% Juice), or 3) malta analyses determined that the distributions of beetles beverage (Malta India brand). One set of traps was as- were not equal, we would remove the treatment(s) that signed the combined lure treatment (see lure treatment differed most from the remainder and repeat the analy- number 3 above), but no food attractant treatment. ses on the remaining treatments until we had clustered The dusky sap beetle lure is specifically designed to at- the treatments into groups that chi-square analyses tract C. lugubris, whereas the date plus fig blend lure failed to reject the hypothesis that beetles were equally is specifically designed to attract C. hemipterus, 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 wasmostabundantin dimidiatus, B. mutilatus, U. humeralis, Eu. fervidus, E. the bread dough and date and fig blend lure (Table 6). luteola,andL. 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 and60in2012and2013,respectively),andEu. fervi- treatments containing apple juice combined with the dus (25 and 54 in 2012 and 2013, respectively). Four Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020 dusky sap lure and apple juice combined with the date E. luteola and two Lobiopa insularis were trapped, all andfigblendlure(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 tionsdidattractsomebeetles(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 beetle 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 universal 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. Combined lures þ malta 88a 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 c h

Dusky sap beetle lure þ apple juice 10 Date and fig lure þ malta 30 Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020 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 treatments. See text for explanation of treatments. a v2 value ¼ 4.701; df ¼ 2; P ¼ 0.09531. b v2 value ¼ 2.18; df ¼ 2; P ¼ 0.3362. c v2 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 v2 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 v2 value ¼ 1.69; df ¼ 2; P ¼ 0.4304. h v2 value ¼ 0.16; df ¼ 1; P ¼ 0.6911. I v2 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. Date and fig lure þ raw dough 38a 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 v2 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 v2 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 v2 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 baited only with lures and no food attractants did not lures, this combination attracted more beetles than the trap U. humeralis (Jenkins et al. 2013), but U. humera- combined lures without food attractants. This suggests lis was commonly trapped during both trials of this that food attractants used in combination with lures are experiment when food attractants were combined with much more powerful attractants than lures alone and lures (Tables 3 and 7). may be important in drawing potential pollinators from The rankings of lure and food attractant combina- other attractants, such as rotten fruit. Treatments 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. Dusky sap beetle lure þ apple juice 49a 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 e

Dusky sap beetle lure þ raw dough 3 Combined lures (Treatment J) 1 Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020 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 v2 value ¼ 1.98; df ¼ 1; P ¼ 0.1585. b v2 value ¼ 3.375; df ¼ 2; P ¼ 0.185. c v2 value ¼ 10.20; df ¼ 5; P ¼ 0.0698. d v2 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 v2 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 v2 value ¼ 0.35; df ¼ 2; P ¼ 0.8395. d v2 value ¼ 11.14; df ¼ 7; P ¼ 0.1325. consistent between years, suggesting that most lure and Rico and that this species responded, albeit weakly, to food attractant combinations will serve to bring poten- lures for nitidulids (Jenkins et al. 2013). The addition tial pollinators to the orchard. However, there are some of food attractants, particularly raw dough, increased important trends. Lures combinations containing date the numbers trapped, but the attraction was still weak and fig blend, either alone or in combination with (Tables 4 and 8). These beetles are likely responding to dusky sap beetle lures, attracted more C. dimidiatus yeasts present in the raw dough. However, the type of than lures containing only dusky sap beetle lure in both yeast present may not be the most preferred yeast for 2012 and 2013. This was also true for the B. mutilatus successful larval development and the yeast may not be that was trapped. When lures were tested without food in sufficient quantity. A recent study indicated that attractants (Jenkins et al. 2013), the date and fig lure although adults and larvae of the nitidulid species Bra- consistently attracted more beetles than the dusky sap chypeplus glaber LeConte may reside within the same beetle lure. This should be taken into consideration by microhabitat, i.e., the restricted confines of sabal palm atemoya growers in Puerto Rico that wish to adopt the inflorescence stalks, there was niche partitioning of the lure method to increase pollination. fungi–yeasts between the adult and larval life stages A previous survey determined that Eu. fervidus was (Cline et al. 2014). This phenomenon may be occurring the most common visitor to atemoya flowers in Puerto more broadly within other saprophagous lineages such 1928 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 108, no. 4 as Europs, but remains untested. Monotomids may or spatial variation, flight, and arresting behavior of these may not be closely related to Nitidulidae (Bousquet potential pollinators is needed. 2009), and their attraction to nitidulid lures may only be because of convergent food sources that give off similar chemical signals. Acknowledgments Except for U. humeralis, all beetles were more common in the 2013 experiment. This may be because of We thank Katherine Parys, Carey Minteer, and two anony- population fluctuations; most of these species utilize the mous reviewers for helpful comments that improved an earlier same or similar resources, i.e., rotten fruit, and so it is version of this manuscript. We also thank Zaid Abdo, Statistician for the USDA-ARS South Atlantic Area. This manuscript likely that populations would track resource availability. presents the results of research only; any mention of a propriet- The differences in populations could also be because of

ary product does not constitute endorsement by the USDA. Downloaded from https://academic.oup.com/jee/article-abstract/108/4/1923/2380007 by guest on 23 July 2020 different baiting methods. In 2012, the treatments containing apple juice or malta used these as trap fluid, whereas in 2013, a much smaller amount (20 ml vs. References Cited 300 ml) of the liquid food attractants was used. We dis- Bartelt, R. J., P. F. Dowd, R. S. Vetter, H. H. Shorey, and T. count the possibility that the dark trap fluid in the first C. Baker. 1992. Responses of Carpophilus hemipterus experiments (apple juice and malta) did not allow us to (Coleoptera: Nitidulidae) and other sap beetles to the phero- find all of the beetles; a strainer was used to remove all mone of C. hemipterus and host-related coattractants in Cali- solids and we are confident that all beetles in the trap fornia field tests. Environ. Entomol. 21: 1143–1153. fluid were counted. There was considerable fungal and Bartelt,R.J.,K.L.Seaton,andP.F.Dowd.1993.Aggrega- bacterial growth in the apple juice and malta treatments tion pheromone of Carpophilus antiquus (Coleoptera: Niti- dulidae) and kairomonal use of C. lugubris pheromone by C. when they were used as trap fluids and this may have antiquus. J. Chem. Ecol. 19: 2203–2216. influenced the number of beetles trapped. Blanche, R. and S. A. Cunningham. 2005. Rain forest pro- Although previous work (Jenkins et al. 2013)demon- vides pollinating beetles for Atemoya crops. J. Econ. Ento- strated that commercial nitidulid lures attracted poten- mol. 98: 1193–1201. tial pollinators, especially when combined, this work Bousquet, Y. 2009. Monotomidae Laporte, 1840 (786 p), In R. demonstrates that the addition of food lures, including G. Beutel, J. F. Lawrence, R.A.B. Leschen (eds.), Handbook bread dough, apple juice, or malta, are more attractive of zoology, Part 29/Vol/ 2: Morphology and systematics (Ela- than the lures alone. The addition a food attractant also teroidea, Bostrichiformia, Cucujiformia partim). Walter de attracts an additional species in Puerto Rico; only one Gruyter, Berlin, Boston. Cline, A. R., P. E. Skelley, S. A. Kinnee, S. Rooney-Latham, U. humeralis of 206 individuals trapped was caught in a and P. Audisio. 2014. Multi-trophic interactions between a trap that did not have a food attractant. This additional sap beetle, Sabal palm, scale insect, fungi, and yeast, as well species may also be, albeit to a lesser extent, valuable as discovery of a compound with antifungal properties. PLoS as a pollinator in this system. ONE 9: 1–12. Finally, the wide variation in number of beetles Escobar,T.W.,R.D.Zareter,andS.A.Bastida.1986.Flo- trapped within a treatment is informative. Although ral biology of artificial pollination of soursop Annona muricata there were not enough replicates to test for block effects in Canca valley of Colombia. Acta Agron. 36: 7–20. within treatments, more C. dimidiatus were trapped in Gazit, S., I. Galon, and H. Podoler. 1982. The role of nitidulid the western-most section of the orchard (mean of beetles in natural pollination of annona in Israel. J. Am. Soc. 6 Hort. Sci. 107: 849–852. 10.25 2.6 SEM in 2012) than in the other two section George,A.P.,R.J.Nissen,D.A.Ironside,andP.Anderson. (means of 4.06 6 4.1 SEM and 2.4 6 2.4 SEM in 2012 1989. Effects of nitidulid on pollination and fruit set of for sections 2 and 3, respectively). The first section is Annona spp. hybrids. Sci. Hortic. 39: 289–299. downwind from the other two sections and there is a James,D.G.,R.J.Bartelt,andR.J.Faulder.1994.Attrac- consistent wind from the east–northeast at the site. The tion of Carpophilus spp. (Coleoptera: Nitidulidae) to syn- beetles may be orienting to the attractant volatiles, arriv- thetic aggregation pheromones and host-related coattractants ing in the orchard, but not moving further in, despite in Australian stone fruit orchards: beetle phenology and pher- the presence of additional attractants in those other omone dose studies. J. Chem. Ecol. 20: 2805–2819. areas. If so, this will have consequences for lure or James, D. G., R. J. Faulder, B. Vogele, R. J. Bartelt, and C. J. Moore. 1997. Phenology of Carpophilus spp. (Coleoptera: attractant deployment to increase fruit set and should be Nitidulidae) in stone fruit orchards as determined by phero- explored further. A concentration gradient, i.e., more mone trapping: implications for prediction of crop damage. attractants or lures used further upwind, may help to Aust. J. Entomol. 36:165–173. offset the skewed distribution of potential pollinators James,D.G.,C.J.Moore,R.J.Faulder,andB.Vogele. arriving in an orchard. Thus, deployment of attractants 1998. An improved coattractant for pheromone trapping of must take into account local physiographic conditions Carpophilus spp. (Coleoptera: Nitidulidae). Aust. J. Entomol. such as prevailing winds and landscape formations 37: 357–361. (deep valleys, etc., where volatiles may persist or Jenkins, D.A., A.R. Cline, B. Irish, and R. Goenaga. 2013. become more concentrated) and adjusted accordingly. Attraction of pollinators to atemoya (Magnoliales: Annona- ceae) in Puerto Rico: a synergistic approach using multiple In summary, the addition of food attractants to com- nitidulid lures. J. Econ. Entomol. 106: 305-310. mercially available nitidulid lures attracted a variety of Lin,H.,P.L.Phelan,andR.J.Bartelt.1992.Synergism be- potential pollinators to an atemoya orchard in Puerto tween synthetic food odors and the aggregation pheromone Rico. The high variability within trap catch suggests for attracting Carpophilus lugubris in the field (Coleoptera: that further study on the orientation, temporal and Nitidulidae). Environ. Entomol. 21: 156–159. August 2015 JENKINS ET AL.: ATTRACTING NITIDULID POLLINATORS IN PUERTO RICO 1929

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