New findings on

Distachio Droblems- I------I- ---

Richard E. Rice 0 Jerry K. Uyemoto Joseph M. Ogawa 0 Wynette M. Pemberton Ailments commonly thought to be physiological have now been traced to feeding by several insect

Ermany years, darkening and collapse in sleeve cages were exposed to several within 48 hours after the bugs fed. As the of hull tissues and subsequent abortion species of true bugs. Examination of the affected area expanded, the typical ne- of immature pistachio fruits was thought fruits revealed symptomatic patterns of crotic epicarp lesion appeared on the to be a physiological disorder. However, damage by the different species. Control surface of the fruit. These immature in 1983 tests, epicarp lesion symptoms fruits without insects remained healthy. fruits shriveled and dropped from the were reproduced when apparently Our results indicated that fruits with cluster within a few days after at- healthy pistachio fruit clusters were ex- typical symptoms were abundant as early tack. It is noteworthy to mention that, posed to field-collected adult leaffooted as April and that blackening of newly before the onset of external symptoms, bugs, , for 48 hours formed fruits was also a form of epicarp tissue discoloration first developed in the in open-mesh cloth bags on the (see lesion. flesh and later extended into the shell California Agriculture, March-April We observed other fruit symptoms in and out to the skin. 1984). This discovery suggested that a the orchards, however, that were not Internal fruit symptoms from coreid number of related bugs might also be able associated with insects, such as panicle and pentatomid bug feeding were quite to produce epicarp lesion symptoms. and blight (necrotic spots of the distinctive; these symptoms changed as To find out, we broadened our re- epicarp), endocarp necrosis (internal the shell hardened. In immature fruits, a search emphasis in 1984, examining the browning of the flesh and shell), and white netting or web pattern appeared in chronology of the various symptoms stylar-end lesion. Following are descrip- the inner shell tissue within 24 hours from fruit set in April until harvest in tions of the pistachio fruit disorders, after feeding. This was sometimes ac- September and studying the effects of their incidence, and distribution in Cali- companied by partial collapse or depres- feeding by other species of true bugs fornia orchards during the 1984 cropping sion of the inner shell surface. Eventual- (Hemiptera). Epicarp lesion is common- season. ly, these fruits also developed external ly described as a sunken, discolored area lesions, and most of them dropped from with darker zones, which extends over a Insect-associated disorder the tree. large portion of the fruit surface; a dried The term “epicarp lesion” is restricted As the shell of the maturing nut began resin exudate is usually present within to fruit symptoms induced by sucking to harden, the amount of internal white the lesion boundary. The disorder has insects. In 1984, incidence of epicarp netting decreased. The white net pattern also been associated with necrotic spots lesion ranged from 4 to 49 percent in was sometimes still seen in fruits that on the epicarp (skin) or with internal severely affected orchards in the Sacra- had dropped from the tree but retained browning of the flesh and shell (meso- mento and San Joaquin valleys. some green color in the dried shell. As carp and endocarp layers). hardening progressed and shells began to We began the 1984 program on April Leaffooted bugs (Hemiptera: Coreidae) lose color, the white net symptoms dis- 21 with a visit to a pistachio orchard that Stinkbugs (Hemiptera: Pentatomidae) appeared and were sometimes replaced had fruit clusters with numerous black- Two species of leaffooted bugs, Lep- by only a small black internal spot on the ened small fruits (less than 4 mm diame- toglossus clypealis Heidemann and L. shell where bug feeding occurred. ter) and typical epicarp lesion symptoms occidentalis Heidemann, and at least At this time, major damage symptoms on larger fruits. The shells of affected four species of stinkbugs in the genera from leaffooted and stinkbug attack fruits showed signs of feeding damage Thyanta, Chlorochroa, and Acrosternum shifted from the shell to the kernel or suggesting involvement of an insect oth- produced similar external and internal nutmeat. As the kernel began to enlarge, er than the leaffooted bug. damage to pistachio fruits. External discolored spongy or punky areas ap- In subsequent feeding trials in the symptoms on fruits 6 to 8 mm in diame- peared. The damaged tissues in these field, the symptoms were reproduced ter were subepidermal “water-soaked or areas stopped growing, leading to sunken when previously healthy fruits enclosed dark stained areas at the point of feeding Text continued, p. 18

CALIFORNIA AGRICULTURE, JANUARY-FEBRUARY 1985 15 “Water-spotting” is an initial symptom of epicarp lesion on small pistachio fruits.

Several different sucking insects can in- duce external symptoms of epicarp lesion early in the season (blackened small fruit on center branch, above) as well as on In controlled field tests, epicarp lesion symp- more mature pistachios (left). toms were induced in pistachios within 48 hours after feeding by true bugs.

In immature fruits, a white netting or web As shells hardened, the white net symp- pattern appeared on the inner shell tissue toms were sometimes replaced by a small within 24 hours after insect feeding. black internal spot where bugs fed.

The leaflike development of the hind legs of adult Leptoglossus occidentalis gives the insect its common name, leaffooted bug.

Before external symptoms of epicarp lesion appeared, insect feeding caused the middle flesh layer to become discolored within 24 hours (photo at left).

As the nutshell hardens, damage from leaffooted bug and stinkbug attack shifts to the kernel, which becomes discolored, spongy, and punky. Tissues in areas of pistachio nut damaged Leaffooted bug feeding can cause exten- Protruding microscopic stylet sheath or by insect feeding stop growing, leading to sive late-season damage to kernels of nuts “spike” is a sign of feeding by leaffooted sunken and distorted nutmeats. that show no external symptoms. bugs and stinkbugs.

Several species of smaller bugs, such as Calocoris norvegicus (left) can cause external epicarp lesion symptoms similar to those of larger bugs, but internal damage differs. Lygus feeding caused pitting (above).

Endocarp necrosis (above) and stylar-end lesion In the initial phase of panicle and shoot (below) both involve darkening of the blossom blight disease, caused by Botryosphaefia end of the pistachio fruit. Neither disorder has fungus, small necrotic spots appear on the been associated with a living organism. fruit surface (above). As the season pro- gresses, the spots enlarge slightly, be- come darker, and coalesce (above right). Ultimately, blight of the rachis and shoot occurs (right). and distorted kernels. Black necrotic tis- affected; direct feeding in hull tissues by dence of endocarp necrosis averaged 1,4, sue often occurred extensively in these mirids was not observed, nor was hull 10, and 15 percent in these blocks of damaged areas as a result of feeding by tissue pitted. The hulls did develop typi- . In five other pistachio orchards in leaffooted bugs; it is not clear at present cal lesion symptoms as caused by the the San Joaquin Valley, the estimated whether the stinkbugs also cause this other bugs, and damaged fruits eventual- incidence of endocarp necrosis ranged symptom. In one orchard with a leaffoot- ly dropped from the nut clusters before from 0 to as high as 10 percent. Attempts ed bug infestation, nuts affected by dam- shell maturity. to associate microbes with this disorder age to the kernel were caiculated at 16.5 In contrast to mid- and late-season failed when tissue pieces of the necrotic percent. attack by the larger bugs, mirids are margins of the shells were placed on Another diagnostic feature is the apparently unable to penetrate harden- culture medium. presence of protruding stylet sheath ma- ing pistachio shells. Consequently, ker- Stylar-end lesion is the necrosis of the terial produced by leaffooted bugs and nel necrosis has not been observed with skin, flesh, and shell layers on the blos- stinkbugs during feeding. These micro- mirids, and potential crop loss from som end of the fruit. This condition scopic sheaths, or “stylet spikes,” were these bugs is usually over by late May or appeared in mid- to late May in Kern found on the outer hull surface, on the early June as shells mature. Exposed or and Kings counties. In these orchards, inner hull, on outer shell surfaces, inside prominent stylet sheaths were not seen symptomatic fruits were in tight clusters, the shell cavity, or sometimes on the in association with mirid feeding on pis- that is, where normal elongation of the nutmeat itself. Their presence indicated tachio fruits, but greater bleeding or res- rachis did not occur. Incidence of stylar- feeding activity by these bugs when there in exudate was present on hull surfaces. end lesion among individual trees in a were no other hull or shell symptoms, Most Lygus hesperus feeding sites (60 to Kern County orchard ranged from 8 to particularly after the shells were com- 70 percent) tended to occur on the upper 61 percent. Elsewhere, incidence of this pletely hard and uncolored. However, one-third, or shoulders, of a fruit, where- disorder was very low or nonexistent. stylet sheaths were not always found, as feeding by leaffooted bugs and stink- Conclusions even on nuts known to be damaged by bugs appeared to be more random. caged bugs. All of these fruit disorders either re- Both coreids and pentatomids are ca- Fungus-associated disorder duce yields or affect nut quality. There- pable of penetrating mature shells and Symptoms of panicle and shoot blight fore, crop management programs are causing internal necrosis to nutmeats up consisted initially of small dark spots on necessary for their control. to the time of harvest. After shells had the fruit surface, which appeared in A large complex of true bugs (Hemip- completely hardened, however, these June. Such spots were closely associated tera) causes external epicarp lesion and nuts did not show external lesion symp- with pores (stomates) present in the epi- internal shell and kernel necrosis on pis- toms, nor did they drop as readily from carp. Affected fruits occurred predomi- tachio nuts. Damage symptoms, which the tree. nately on the lower branches of trees in vary with the insect family and maturity orchards with a closed or nearly closed stage of the nuts, are diagnostic and can bugs (Herniptera: Miridae) canopy where high-angled sprinkler irri- be used to determine which type of insect Our 1984 study showed that, in addi- gation equipment was used. As the sea- was feeding on a particular nut. These tion to leaffooted bugs and stinkbugs, son progressed, the spots enlarged slight- findings should be helpful in developing several species of smaller plant bugs in ly, became darker, and coalesced. By management strategies for insect control the family Miridae caused epicarp lesion mid-July, a blight of the rachis (the in pistachio orchards. symptoms. These species included Lygus branched structure supporting pistachio Further studies of panicle and shoot hesperus Knight and Calocoris norvegi- fruits) and shoot occurred. blight disease are needed to verify its cus (Gmelin). Isolations from the necrotic spots on relation to and to deter- The initial external damage by these the fruit yielded the fungus Botryos- mine the environmental conditions re- bugs to small fruits was similar to that phaeria. This organism was also recov- quired for infection. One approach in caused by the larger bugs. Internal dam- ered from the blighted rachis and shoot, controlling the disease is to avoid irriga- age, however, was quite different and and preliminary results of pathogenicity tion equipment that discharges water could be used to differentiate between, tests verified it as a pathogen of pista- into the tree’s canopy. We did not ob- for example, Lygus and Leptoglossus at- chio (Pemberton, unpublished data). At serve this disease in orchards with low- tack on pistachios. Mirid feeding on im- present, this disease appears to be limit- angled sprinkler, flood, or drip irrigation mature fruits was characterized by com- ed to only a few orchards in the northern systems. plete destruction and liquefaction of Sacramento Valley, where crop losses Because the causes of endocarp necro- shell tissue at the feeding sites within were estimated at 10 to 40 percent. sis and stylar-end lesion are not known, four hours after attack. The dissolved control measures for these disorders are shell material was first green then light Physiological disorders not currently available. Finding the brown and was contained within the Because the remaining fruit disorders causes could prove difficult, because we epidermal membranes, or cuticle, on ei- have not been associated with living or- have no clues at this time. It is worth ther side of the shell. There was very ganisms, they have been classified as mentioning that fruit with endocarp ne- little white netting in the shell tissue. abiotic in nature. crosis did not develop stylar-end lesion. After ingestion of the partially digest- In endocarp necrosis, the blossom end Richard E. Rice is Entomologist, Department of Entomology, Uniuersity of California, Dauis, sta- ed shell by a feeding mirid, a distinct, of the shell darkens while the skin and tioned at Kearney Agricultural Center, Park; clearly defined cavity or crater was left in flesh layers remain unaffected. During Jerry K. Uyemoto is Post Graduate Research P& the shell. At first, the cavity was covered 1984, fruit with these symptoms first thologist, Joseph M. Ogawa is Professor, and Wynette M. Pemberton is a graduate student, by the interior cuticular membrane, but appeared in early June on a Butte Coun- Department of Plant Pathology, all with UC Dauis. this membrane ruptured within 24 to 48 ty farm. On that farm, we sampled four This research was supported in part by finan- cial assistance from the Pistachio Commission of hours and exposed the entire cavity. orchard blocks by collecting fruit clusters California. The cooperation of pistachio growers. Cavities were up to 2 to 2.5 mm in at random from a total of three trees per processors, farm aduisors, and other technical per- sonnel is gratefully appreciated. Several of the diameter and 1 mm deep with perpen- block and removed the hull tissues of 100 photographs were taken by Jack Kelly Clark, Visu- dicular walls. Only the shell tissue was fruits per tree to expose the shell. Inci- al Media, UC Dauis.

18 CALIFORNIA AGRICULTURE, JANUARY-FEBRUARY 1985