UC Agriculture & Natural Resources California Agriculture

Title High temperature affects fruit populations in California’s Central Valley

Permalink https://escholarship.org/uc/item/79k8f30z

Journal California Agriculture, 65(1)

ISSN 0008-0845

Authors Johnson, Marshall W Wang, Xin-geng Nadel, Hannah et al.

Publication Date 2011

Peer reviewed

eScholarship.org Powered by the California Digital Library University of California REVIEW ARTICLE ▼

High temperature affects olive fruit fl y populations in California’s Central Valley

by Marshall W. Johnson, Xin-Geng Wang, Hannah Nadel, Susan B. Opp, Kris Lynn- Patterson, Judy Stewart-Leslie and Kent M. Daane Marshall W. Johnson W. Marshall

Olive fruit fl y commonly infests in California’s Central Valley. Field studies indicate that trap counts for olive fruit fl y adults in ­free sites decrease in mid­ and late sum­ mer and then rebound from Septem­ ber to November. Part of this decline is associated with heat stress that the fl ies experience in mid­July and Au­ gust. Studies have shown that adult fl ies will die within a few days if they cannot access adequate amounts of water and carbohydrates. Flight An adult female olive fruit fl y deposits an egg into olive fruit. ability is dramatically reduced when resources are unavailable. Olive fruit by pruning infested trees to facilitate McPhail traps (Johnson et al. 2006). fl y adults may use black scale hon­ greater air movement in the summer, The numbers of adults captured in the which results in signifi cant desiccation Central Valley decline during the eydew as a carbohydrate source to of fi rst-instar crawlers (Daane and Cal- hottest periods of July and August and help them survive hot periods. Heat tagirone 1989). increase in September as temperatures also affects the fl y’s reproduction and However, the establishment of ol- decrease (Rice et al. 2003; Yokoyama immature stages within olive fruit. ive fruit fl y ( oleae [Rossi]) et al. 2006) (fi g. 1). For most spe- (Diptera: ) forced many cies, a decline in trap counts suggests a Geographic information system (GIS) growers onto a weekly treatment re- reduction in adult densities in an area. maps may be useful for predicting gime that runs from mid-June through This is not initially the case with olive the risk of olive fruit fl y infestation. harvest (September to December), fruit fl y, whose behavior changes as using the spinosad product GF-120 daily temperatures rise. NF Naturalyte Fruit Fly Bait (Dow Avidov (1954) reported that below he discovery in 1998 and subsequent AgroSciences) (Johnson et al. 2006). This 62°F the adults are inactive. As tem- Tspread of the olive fruit fl y through- management proto- out the major olive-producing areas of col enables growers California dramatically affected the to deliver fruit with As temperatures surpass 84°F, adult fl ies become pest management activities practiced by near-zero infestation increasingly agitated and egg laying is halted, growers. Prior to its introduction, the levels to the table olive major pests targeted for con- processors. Olives des- and above 95°F they are motionless. trol in California olives were olive scale tined for oil pressing (Parlatoria oleae Colvée) (Hempitera: Di- may have signifi cant aspididae) and black scale ( oleae levels of infestation without an appre- peratures increase above the threshold [Olivier]) (Hempitera: ) (Daane ciable decline in quality, as long as the temperature, adult activity increases. et al. 2005). Olive scale is well managed time between harvest and pressing is Normal activity, fl ight and egg lay- with biological control due to the intro- minimal (Pereira et al. 2004; Torres-Villa ing occur between 73°F and 84°F. As duction and establishment of the para- et al. 2003). temperatures surpass 84°F, adult fl ies sitoids Aphytis paramaculicornis DeBach become increasingly agitated and egg Adult behavior and survival and Rosen, and Coccophagoides utilis laying is halted, and above 95°F they Doutt (Daane et al. 2005). Black scale is Olive fruit fl y adults may be moni- are motionless. Laboratory observa- mainly controlled in the Central Valley tored with fl at-panel sticky traps or tions (M.W. Johnson, unpublished) also

http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 29 suggest that adults seek and remain One might assume that acquisition groups of tested flew significantly near moisture sources as temperatures of adequate amounts of food and water shorter distances (≥ 42%) than the con- approach and surpass 95°F. would be easy for adults, trol (F6,252 = 62.7, P < 0.01). Additionally, Reduced adult fly activity can result which are strong flyers. Using a custom- individual flies that were denied food in lower trap counts in the field while designed flight mill, Wang et al. (2009b) and water from the time that they maximum daily temperatures remain reported that adults of both sexes held emerged as adults and were held at around 95°F to 99°F and the flies have for 7 days at 75°F (constant temperature) either 65°F at night and 95°F, or 100°F, access to adequate water and carbo- and provided with ample food (honey during the day for 1 to 2 days, flew sig- hydrate sources (Wang et al. 2009a). and hydrolyzed yeast) and water, were nificantly shorter distances (≥ 92%) than However, as the frequency at which able to fly uninterrupted for an average the flies provided no food and water for daily maximum temperatures equal or of 2,164.8 ± 228.8 yards during a mean 24 hours after having access to food and surpass 100°F increases, greater num- period of 1.54 ± 0.16 hours (fig. 3). water for 7 days (fig. 3). bers of adults will die due to heat stress, Nonetheless, heat stress and lack of In a worst-case scenario, an adult especially when they cannot access water and food can affect flight ability. fly that emerges in mid-August in the adequate quantities of water and food Olive fruit fly adults that were subject Central Valley may commonly experi- (Wang et al. 2009a, b) (fig. 2). Although to the same conditions as described ence maximum daily temperatures over adult females may ingest liquid from for 7 days and then to water only or no 100°F for 3 consecutive days (Lynn- punctures they make in olive fruit, this food and water in diurnal temperature Patterson 2006). Without food or water secretion does not provide the needed regimes (65°F at night; 95°F or 100°F immediately available, an adult will carbohydrates to help them survive during the day) for 24 hours before the only be able to fly an average of 16.4 heat-induced stress (Johnson and Nadel, flight test did not perform as well as ± 4.4 yards to locate these resources unpublished data). the control group (fig. 3). All stressed in a dry and unexplored landscape.

5 (A) 75°F, food and water a Sites 2,500 (B) 95°F, water, 24 hours Treated (C) 100°F, water, 24 hours 4 Untreated (D) 95°F, no resources, 24 hours (E) 100°F, no resources, 24 hours (F) 95°F, no resources 3 2,000 (G) 100°F, no resources

b 2 b 1,500

Mean total ies/trap/week 1

0 10 17 24 1 8 15 22 29 5 13 20 27 4 11 18 25 1 8 15 22 29 6 13 20 27 3 10 17 24 31 7 14 Mean distance (yards) 1,000 April May June July Aug Sept Oct Nov bc

c Fig. 1. Average olive fruit fly populations at nine untreated sites (e.g., urban, landscape and 500 abandoned commercial plantings) and five treated (with GF-120) commercial sites in Fresno and Tulare counties during the 2003 growing season (Johnson, Nadel and Stewart-Leslie, unpublished data). d d

Fig. 2. Mortality of 0 90 Treatment olive fruit fly adults c c subjected to 1 to 3 95°F, water 80 Fig. 3. Mean distances flown by olive fruit fly days exposure to 100°F, water adults exposed to various temperatures and 95°F and 100°F, in the 70 95°F, no resources resources. Flies (A-E) were preconditioned for absence of food and 100°F, no resources b 60 7 days at 75°F with ample food and water with and without b b prior to treatment. Treatments were: (A) access to water (Wang c 50 no treatment (control); (B) preconditioned et al. 2009b). Different at 95°F, then 24 hours of water only; (C) letters above columns 40 preconditioned at 100°F, then 24 hours of representing the same 30 water only; (D) preconditioned at 95°F, then 24

temperature/resource Adult mortality (%) hours with no resources; (E) preconditioned at treatment indicate 20 b a 100°F, then 24 hours with no resources; (F) no significant differences a preconditioning, held from 1 to 2 days at 95°F (P < 0.05; Tukey’s 10 a a with no resources; and (G) no preconditioning, HSD test) within the a held from 1 to 2 days at 100°F with no exposure duration. 0 1 2 3 resources (Wang et al. 2009b). Different letters Days of exposure above columns indicate significant differences (P < 0.05; Tukey’s HSD test).

30 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1 A B

(W) (W) (H) (H)

Experimental setup shows (A) the typical distribution of fi ve olive fruit fl y adults (circled) within an observation chamber, with cotton wicks and water (W) and honey (H) at a cool temperature (80°F) and 20% relative humidity, and (B) the congregation of olive fruit fl y adults (circled) around a water wick (W) when the temperature is hot (99.5°F) and 37% relative humidity.

2,000 A B a 95°F, water 1,500 a 100°F, water 95°F, no resources 100°F, no resources 1,200 ab 900 b a b 600 a ab b b 300 ab b C

0 Mean distance own uninterrupted (yards) 1 2 3 Days of exposure

Fig. 4. Mean distances fl own by olive fruit fl y adults subjected to 1 to 3 days exposure to D 95°F and 100°F, in the absence of food and with and without access to water (Wang et al. 2009b). Different letters above columns representing the same temperature/resource treatment indicate signifi cant differences P( < 0.05; Tukey’s HSD test) within the exposure duration.

Such a fl y would have an 84% chance of dying in the fi rst 24 hours, and of Fly fl ight is measured using (A) a custom-designed fl ight mill setup with computer; (B) an those that did survive only about 25% individual fl ight mill unit; (C) a beam that rotates during insect fl ight; and (D) a tethered fl y would be able to fl y (Wang et al. 2009b). fastened to a rotating beam. Additionally, when olive fruit fl y adults were held at 65°F at night and 95°F or commonly in late July and early August 2009a). Eggs are deposited just beneath 100°F during the day over a 3-day pe- in California (Burrack and Zalom 2008; the fruit epidermis and may be exposed riod with either water alone or no food Wang et al. 2009a). During periods of to high temperatures, depending on or water, those fl ies that survived one high maximum daily temperatures (3 where an individual fruit is located on day could fl y signifi cantly farther than consecutive days at 100°F or above in the tree (Wang et al. 2009a). those that survived 3 days (F2,407 = 18.7, July and August) (Lynn-Patterson 2006), Laboratory studies showed that adult P < 0.01) (fi g. 4). mated adult females may lay their eggs females held under different diurnal in developing olives prior to morning temperature regimes (65°F at night and Egg and larval survival temperatures reaching 95°F. No eggs are 75°F, 95°F or 100°F during the day) laid Reproductive dormancy in olive deposited during the night, even when similar numbers of eggs when the tem- fruit fl y subsides as greater numbers of temperatures are cool enough for nor- perature was 65°F and the experimental mature fruit appear within the orchard, mal activity (Avidov 1954; Wang et al. chamber was illuminated (F2,55 = 0.2,

http://californiaagriculture.ucanr.org • JANUARY–MARCH 2011 31 P = 0.852). However, under illumination in the same locality in mid- and late examination of temperature trends in and higher temperatures, females laid summer 2007 and 2008 showed that less olive-producing areas in the Central significantly fewer eggs at 95°F (about than 2% of offspring from eggs laid in Valley over 10 years (1992–2001) re- four per female) than at 75°F (about 12 olives completed development to the vealed that it was quite common for per female) (F1,38 = 8.4, P = 0.006), and adult stage (Wang et al. 2009a). temperatures to be greater than 100°F no eggs were laid at 100°F (Wang et al. for 3 consecutive days during mid-July Scale honeydew and heat stress 2009a). and August (fig. 6) (Lynn-Patterson Even after eggs are deposited within This information suggests that it 2006). On the California coast, these olive fruit, they are still susceptible is difficult for olive fruit fly adults to trends were rarely observed. Over to the high temperatures common in survive the high summer temperatures this time period, temperatures greater Central Valley orchards. Eggs within in the Central Valley. Water may com- than 100°F for 3 consecutive days were fruit held at 65°F (night) and 75°F (day) monly be found within or near most more common in the southern (San developed into first-instar larvae after orchards from a variety of sources, such Joaquin Valley) than the northern 6 days (Wang et al. 2009a). In contrast, as morning dew, creeks, ponds, irriga- (Sacramento Valley) Central Valley (see eggs within fruit subjected to 65°F tion water (ditches and canals), sprin- http://arcims.gis.uckac.edu/CIMIS). By (night) and 95°F (day) had a 49% mor- klers, drip tape and fan jets. However, September, most of the Central Valley tality rate, and of the first-instar larvae fly adults also need carbohydrates to rarely had 3 consecutive days greater that did develop, none became second survive heat stress. Honeydew (fresh than 100°F (fig. 6).; in 2003, olive fruit fly instars. When subjected to 65°F (night) or dry) produced by black scale is a surpassed one adult per trap per week and 100°F (day), no eggs hatched after common carbohydrate source in olive at the end of August and continued to 10 days exposure and all died. The over- orchards. Our laboratory tests have increase into November (fig. 1). all finding was that egg (F3,57 = 2472, P shown that fly adults provided with Growers and consultants may wish < 0.001) and first-instar (F3,57 = 2472, P < honey and water, or black scale honey- to use these maps to determine if they 0.001) mortality increased as exposure dew and water, survive temperatures of can temporarily halt insecticide treat- time increased (Wang et al. 2009a). 65°F (night) and 97.5°F (day) with mini- ments for olive fruit fly adults during Later field studies showed that maxi- mal mortality compared to adults only July and August. However, there are mum daily temperatures in olive trees provided honey alone, honeydew alone, many factors other than temperature in the Central Valley (Parlier) varied or no food and water over 5 days (F4, 36 that influence whether olive fruit fly depending on whether measurements = 189.9, P < 0.0001) (fig. 5) (M.W. Johnson will be a problem in a particular olive were taken within the canopy interior and H. Nadel, unpublished data). orchard. Olive fruit fly adults with ac- or the east or west perimeter. Mean The carbohydrate source alone did cess to adequate sources of water and temperatures recorded on the west not reduce the impact of heat on sur- carbohydrates can survive heat stress side of the tree canopy in August 2007 vival. Flies that had food resources in large numbers and will be able to fly were 108°F (and over 104°F for 26 days) (honeydew or pure honey) but no water long distances (more than 1,000 yards) compared to 101°F (and over 104°F for suffered mortality similar to those flies even when stressed. Growers who con- 13 days) on the east side, and 96°F (and without food or water. There was a sider halting their control programs, never over 104°F) within the canopy significant interaction between carbo- especially in the San Joaquin Valley, interior (F2,90 = 52.7, P < 0.001). All of hydrate source and days of exposure should take under consideration the ir- these temperatures are high enough to (F20, 180 = 33.3, P < 0.0001). These results rigation schedules and infestation levels impose some level of mortality on olive are similar to what we have observed in of black scale and other that fruit fly eggs and larvae. Field studies our laboratory and field studies on olive might produce honeydew within their fruit fly when 50% honey water was own and neighboring orchards. Also used as a carbohydrate source. These important is the proximity of irrigation findings are significant because they canals, creeks, ponds and rivers, as well 100 suggest that olive fruit fly adults could as abandoned orchards or untreated use black scale honeydew to help them olives trees used for landscaping, which 80 Honeydew only Honeydew and water survive periods of high temperature in can serve as an infestation source of 60 Honey only the Central Valley. The management olive fruit fly. Morning dew in the or- Honey and water No food of black scale populations via cultural chard may provide a moisture source 40 controls such as the pruning of interior for flies, and weedy undergrowth in the canopies may also contribute to the orchard or neighboring crops can afford 20 management of olive fruit fly adults. some relief from the heat. Olive fruit y survival (%) Perhaps the most useful informa- 0 Temperature maps and fly activity 1 2 3 4 5 tion that one can obtain from the GIS Days of exposure Geographic information systems maps is knowing when temperatures (GIS) enable the examination of temper- historically have dropped to low levels Fig. 5. Survival of olive fruit fly adults when ature trends over specific areas based held at 65°F (night) and 97.5°F (day) with that would be conducive to olive fruit access to various combinations of water, honey on defined criteria, such as temperature fly activity and survival in a particular and black scale honeydew, or no food or water. levels for specific time intervals. The area. As temperatures decline at the end

32 CALIFORNIA AGRICULTURE • VOLUME 65, NUMBER 1 July 15 Aug. 15 Sept. 15 Occurrences 0 1–2 3–5 6–8 9–10

Fig. 6. Mean temperature patterns in California over 10 years (1992–2001), showing number of years (occurrences) with maximum temperatures greater than or equal to 100°F for 3 consecutive days ending on July 15, Aug. 15 and Sept. 15 (Lynn-Patterson 2006). of August, olive fruit are increasing in be helpful. Given that olive fruit fl y size and maturing (Martin and Sibbett adults need carbohydrate sources to 2005). Olive fruit fl y adults prefer to lay survive heat stress, it may be best to M.W. Johnson is Cooperative Extension Specialist their eggs in the largest olives avail- continue treating with GF-120 in July and Entomologist, Department of Entomology, able (Neuenschwander et al. 1985). As and August. The adults are attracted UC Riverside; X.-G. Wang is Associate Specialist, fl ies return to normal activity in late to the sweet fruit fl y bait in the GF-120. Department of Environmental Science, Policy and summer, the olives remaining on the If stressed fl ies seek a carbohydrate Management, UC Berkeley; H. Nadel is Supervi- sory Entomologist, U.S. Department of Agricul- trees are at greater risk of infestation source in summer, it may be assumed ture and Health Inspection Service, than at anytime during the summer, that they would then seek out available Plant Protection and Quarantine program, Buz- and protecting the fruit then is of prime bait residues in GF-120. If this is true, zards Bay, MA; S.B. Opp is Associate Vice Presi- consideration. the GF-120 may be having a greater dent, Academic Programs and Graduate Studies, impact than realized. This needs to be California State University, East Bay; K. Lynn- Future directions determined. Also of importance is the Patterson is GIS Academic Coordinator, UC Kear- Research on the ecology and man- impact of summer heat either directly ney Agricultural Center, Parlier; J. Stewart-Leslie is Manager, Consolidated Central Valley Table Grape agement of olive fruit fl y is continuing. or indirectly on natural ene- Pest and Disease Control District, Exeter, CA; and A better understanding of the abili- mies that are now being released as part K.M. Daane is Cooperative Extension Specialist, ties of olive fruit fl y adults to disperse of a classical biological control program Department of Environmental Science, Policy and among orchards in the summer would for olive fruit fl y control (see page 21). Management, UC Berkeley.

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