Biology of Protortonia navesi (: ), a New Pest in Brazil, with Notes on Its Behavior in the Field

CHARLES MARTINS DE OLIVEIRA,1,2 MARINA REGINA FRIZZAS,3 1 4 JOSEFINO DE FREITAS FIALHO, AND PENNY J. GULLAN

Embrapa Cerrados, Departamento de Entomologia, Rodovia BR 020, km 18, Caixa Postal 08223, Planaltina, DF, 73310-970, Brazil Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021

Ann. Entomol. Soc. Am. 101(4): 779Ð785 (2008) ABSTRACT Protortonia navesi Fonseca (Hemiptera: Monophlebidae) is a scale recently reported as a new cassava (Manihot esculenta Crantz) crop pest in central Brazil. The biology P. navesi was studied under controlled and Þeld conditions, and some aspects of its Þeld behavior were recorded. The laboratory experiments were carried out from August to December 2004 under controlled conditions (25 Ϯ 2ЊC, 70 Ϯ 23% RH, and a photoperiod of 12:12 [L:D] h), and the Þeld experiment from September 2003 to August 2004, at Planaltina, Federal District, Brazil. In the laboratory, P. navesi showed a 69.2-day cycle from oviposition to adult eclosion, going through three nymphal stages in 44.5 d, on average. The females reproduced by thelytokous parthenogenesis, with an average oviposition capacity of 239.6 eggs per female. No males were observed in this species. In the Þeld, P. navesi had a permanent underground population. However, from September to December 2004, the aerial parts of were colonized by part of this population, which was controlled by the predator Exoplectra sp. (). Individuals of P. navesi were observed to be active on cassava roots in the Þeld throughout the year, suggesting that this may have at least Þve generations per year in central Brazil.

RESUMO A cochonilha Protortonia navesi Fonseca (Hemiptera: Monophlebidae) foi relatada re- centemente como uma nova praga na cultura da mandioca no Brasil Central. No´s estudamos a biologia de P. navesi em condic¸o˜es controladas e observamos alguns aspectos do seu comportamento em campo. Os estudos foram conduzidos em laborato´rio (25 Ϯ 2ЊC; UR 70 Ϯ 23%; 12 h fotofase) de agosto a dezembro de 2004 e em campo de setembro de 2003 a agosto de 2004, em Planaltina, Distrito Federal, Brasil. Em laborato´rio P. navesi apresentou um ciclo (ovo-adulto) de 69,2 dias, passando por treˆs esta´dios ninfais com durac¸a˜o total de 44,5 dias. As feˆmeas se reproduziram por partenogeˆnese telõ´toca, sendo capazez de colocar em me´dia 239,6 ovos. Na˜o foram observados machos nesta espe´cie. Em campo, P. navesi apresentou uma populac¸a˜o subterraˆnea permanente. Entretanto, de setembro a dezembro, parte dessa populac¸a˜o colonizou a parte ae´rea das plantas, sendo controlada pelo predador Exoplectra sp. (Coccinellidae). No campo foram observadas fases ativas do inseto, em raõ´zes de plantas de mandioca, durante todo ano sugerindo que a cochonilha pode produzir pelo menos cinco gerac¸o˜es por ano.

KEY WORDS Insecta, cassava root scale, Manihot esculenta, bioecology

The Protortonia Townsend (Hemiptera: Mono- species of the Cactaceae, , Rosa- phlebidae), proposed by Townsend in 1898 (Townsend ceae plus Salicaceae, Euphorbiaceae, and Fagaceae, and Cockerell 1898), includes seven species. Five species respectively (Reyne 1964, Fonseca 1979, Foldi 2006, have a Neotropical distribution: Protortonia cacti (L.), P. Williams and Gullan 2008). Two species, P. azteca crotonis Reyne, P. ecuadorensis Foldi, P. navesi Fon- (Ferris) and P. primitiva (Townsend), occur in Mex- seca, and P. quernea Williams & Gullan and feed on ico in the NeotropicalÐNeartic transition region on plants of Pinaceae and Urtiaceae, respectively 1 Embrapa Cerrados, Caixa Postal 08223, Planaltina/DF, 73310-970, (Townsend and Cockerell 1898, Ferris 1925, Williams Brazil. and Gullan 2008). 2 Corresponding author, e-mail: [email protected]. Scale are important pests worldwide on 3 Centro Universita´rio de Brasõ´lia (UniCEUB), SEPN 707/909, Asa many crops, because their constant sucking of sap Norte, Brasõ´lia/DF, 70790-075, Brazil. 4 Department of Entomology, University of California, 1 Shields reduces plant vigor and sometimes causes plant death Ave., Davis, CA 95616Ð8584. (Williams and Watson 1990, Foldi 2005). P. navesi, the

0013-8746/08/0779Ð0785$04.00/0 ᭧ 2008 Entomological Society of America 780 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 4 cassava (Manihot esculenta Crantz) root scale, was Þrst of nymphs eclosing per day reached an adequate level described in the late 1970s from specimens collected for the studies (Ͼ90 specimens of same age). on Manihot utilissima Pohl in the Federal District, Biological Studies. Fifteen days before the start of Brazil (Fonseca 1979). This insect is native to Brazil the life cycle study, 1-yr-old cassava stems (ÔPioneiraÕ) (Fonseca 1979), and it has recently been found on were planted in plastic pots (7 cm in diameter by 10 cassava crops in the Federal District and states of cm in height) Þlled with fertilized and sterilized soil. , , and Goia´s (Oliveira and Fialho The 10-cm-length cassava stems were placed into the 2006). soil at a depth of 5 cm. Pots were periodically irrigated Cassava represents an important source of energy with 0.2% Nipagin solution. Newly eclosed Þrst-instar for human nutrition (Cock 1982, Nassar 2006) and nymphs were then transferred, using a thin brush, on shows high-yielding potential even under low crop- to the cassava stems in the plastic pots (one nymph per ping technology (Cock 1982). In Brazil, this species is pot; total of 90 replications). widely cultivated mostly by small producers (Farias Nymphal Phase. After the transfer of nymphs to 1991, Bellotti et al. 1999) and often in areas where the cassava stems, the pots were kept in a growth chamber Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021 environment (climate and soil) is not favorable to (25 Ϯ 2ЊC, 70 Ϯ 23% RH, and a photoperiod of 12:12 other crop species (Henry and Gottret 1995, Bellotti [L:D] h), and the insects were monitored daily under et al. 1999). Cassava is a subsistence crop, especially in a50ϫ magniÞcation stereomicroscope (Stemi SV 6; the north and northeastern regions of Brazil. Quanti- Carl, Zeiss, Jena, Germany). The duration of each tative and qualitative injuries caused by P. navesi in instar was determined for each of the 90 insects by cassava have been reported in Brazil (Oliveira and recording the days that exuviae were detected on each Fialho 2005), but little is known about its life cycle and plant. Morphometric parameters (specimen length ecology. The purpose of this work was to study the and width) were measured daily by using an optical biology of P. navesi by means of laboratory and Þeld device attached to the stereomicroscope. The per- experiments. The speciÞc objectives were to study the centage of survival for each instar was calculated by life cycle and reproductive characteristics of P. navesi dividing the number of specimens that molted to the in the laboratory and some aspects its behavior in the next instar by the number of specimens of the previous Þeld. instar multiplied by 100. To evaluate the survival capacity of Þrst-instar nymphs without food, the nymphs hatched from eggs used for the incubation period determination (see Materials and Methods Oviposition and Incubation Period) were transferred The experiments were carried out in a laboratory at to plastic petri dishes (6 cm in diameter by 1.5 cm in the Department of Entomology at Embrapa Cerrados, height) with Þlter paper underlay, covered with plas- at Planaltina, Federal District, Brazil, and in the Þeld tic Þlm, and maintained in a growth chamber. Groups at the experiment station at Embrapa Cerrados (47Њ of 50 individuals with 10 replications were used, and 42Ј 58.7Љ W; 15Њ 36Ј 23.4Љ S; 1,032 m). specimen mortality was recorded daily. Laboratory. The life cycle experiments were carried Adult Phase. After eclosion, the adults were indi- out from August to December 2004 in a growth cham- vidually transferred to petri dishes (9 cm in diameter ber under controlled conditions: 25 Ϯ 2ЊC, 70 Ϯ 23% by 1.5 cm in height) containing sterilized soil with RH, and a photoperiod of 12:12 (L:D) h. similar Þeld humidity (Ϸ33%) and covered with cor- Collection and Egg Production of Adult Females. rugated Þlter paper as described previously. Dishes Fifty adult females of P. navesi were collected from an were then covered with perforated plastic Þlm and area of Ϸ5,000 m2 planted with several cultivars of kept in a growth chamber under the same conditions cassava. The insects were immediately transported to described above. Specimens were monitored daily to the laboratory in plastic containers together with soil record the preoviposition and oviposition periods, lon- from the Þeld. The specimens were individually sep- gevity, and morphometric parameters (length and arated in petri dishes (9 cm in diameter by 1.5 cm in width). The separation of adult females from their host height) containing sterilized soil and covered with plant should not affect their reproductive biology be- corrugated Þlter paper (8 by 5 cm). The petri dishes cause adults lack mouthparts and thus do not feed. were covered with perforated plastic Þlm for aeration, Oviposition and Incubation Period. The petri dishes kept in the growth chamber, and inspected daily for containing adult scales were observed daily under the presence of eggs. Each day, the eggs obtained were stereomicroscope, and the specimens were carefully transferred to plastic petri dishes (6 cm in diameter by manipulated with forceps and needles. Any eggs 1.5 cm in height) with a Þlter paper underlay and present were counted and transferred, by using a Þne covered with perforated plastic Þlm. For egg incuba- dampened brush, into plastic petri dishes (6 cm in tion, dishes were ßoated in a covered plastic container diameter by 1.5 cm in height) over a Þlter paper (30 cm wide ϫ 40 cm long ϫ 15 cm high) containing underlay. The procedure for egg incubation is de- sterilized water and put into the growth chamber. This scribed under Collection and Egg Production of Adult procedure maintained a high relative humidity (93Ð Females. Eggs were monitored daily, the number of 97%) in the container but avoided direct contact be- nymphs hatching per day per female was recorded, tween the eggs and the water to prevent fungal pro- and these nymphs were removed from dishes. To com- liferation. Eggs were observed daily until the number pare the oviposition capacity of adult females raised in July 2008 OLIVEIRA ET AL.: BIOLOGY OF P. navesi 781

.the laboratory with those from the Þeld, 50 reproduc- Table 1. Average duration ؎ SEM of life cycle stages of P navesi under laboratory conditions (25 ؎ 2°C, 70 ؎ 23% RH, and tive females were collected in the Þeld and maintained ͓ ͔ as described above to record their total egg output. a photoperiod of 12:12 L:D h) Field. During September 2003 to August 2004, Duration Interval variation Life cycle phase weekly evaluations were made of the occurrence and (d) (d) behavior of P. navesi in the Þeld in a 1-yr-old cassava Ϯ 2 Egg 24.7 0.3 19Ð27 crop area of Ϸ5,000 m , and containing several culti- Nymph 44.5 Ϯ 0.6 35Ð60 vars, located at the experiment station of Embrapa Adult (longevity) 26.8 Ϯ 0.8 12Ð36 Cerrados. Cycle (eggÐadult eclosion) 69.2 Ϯ 0.9 54Ð87 Ϯ Insect Distribution on Plants. In this study, insect Cycle (eggÐadult death) 96.0 1.7 66Ð123 distribution on cassava plants was evaluated for 1 yr by examining 10 plants each week for the presence of scales on both the aerial parts and the roots. After obligatory parthenogenesis has been reported for examination of the foliage, each plant was uprooted to some other species of scale insects (Nur 1980, Botton Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021 record scale insects living underground. et al. 2000, Normark 2003, Foldi 2005) but not previ- Insect Movement in the Field and on Plants. The ously in Protortonia. Males are known in four other movement of scale insects in the experimental area species of Protortonia (Williams and Gullan 2008). was evaluated by weekly examination, from Septem- Schrader (1930) described the mating behavior of P. ber to December 2003, of 35 deÞned strips of soil (1 m near primitiva and also observed that virgin females in width by 10 m in length). Presence or absence of laid inviable eggs. In P. ecuadorensis, the adult male has specimens of P. navesi walking on soil within each strip been described, but the biology is unknown (Foldi was recorded. The strips were distributed parallel to 2006), whereas in two other Protortonia species only one of the borders of the Þeld, with Þve strips within the presence of males has been recorded (Williams the experimental area and 30 other parallel strips out- and Gullan 2008). side the experimental area. For the strips located Laboratory. On average, the duration of the life cycle within the experimental area, at least 15 plants were of P. navesi was 69.2 d from oviposition until adult eclo- examined for presence of scale specimens moving on sion and 96.0 d from oviposition until adult death (Table the aerial parts. Each week, some specimens were 1). In P. near primitiva, the female biological cycle (from collected for subsequent identiÞcation of the instar. fertilization of egg to adult eclosion) averaged 85 d at Natural Enemy Studies. The presence of natural en- Ϸ25ЊC (range, 18Ð38ЊC) (Schrader 1930), slightly longer emies was observed and recorded. During November than that found for P. navesi. Based on these data, P. 2003, predator occurrences, parasitoid occurrences, or navesi might have Þve generations per year at Planaltina both were evaluated on 10 cassava plants infested with in the Federal District, Brazil. P. navesi nymphs. The plants had their aerial parts The insect body shape of P. navesi did not alter protected with a voile bag (60 cm in width by 90 cm within the nymphal and adult phases, with a constant in length) attached to the plant stem, thereby con- length/width ratio of 1.8, except for the end of the Þrst Þning nymphs of P. navesi as well as any natural en- instar (2.0). The second-instar nymphs had the short- emies present. The bagging was conducted to allow est stadium (11.6 d) and less growth in size (42%). the development and emergence of potential natural Nymphal Phase. Both P. navesi and P. near primitiva enemies (predator and parasitoids), which could be have three female instars, but for P. navesi, the total preying on or parasitizing the P. navesi nymphs. After nymphal period was 44.5 d (Table 1), compared with 30 d, the cassava plants were cut and taken to the 56 d observed in P. near primitiva (Schrader 1930). laboratory for counting of scales and veriÞcation of the Just after eclosion, the nymphs stayed grouped to- presence of natural enemies. gether, but after 1Ð2 d they moved quickly searching Taxonomic Identification. Specimens of P. navesi for a feeding site. The newly eclosed Þrst-instar were identiÞed at the Department of Entomology, nymphs had a red body and long setae on the lateral University of California (Davis, CA). The Coleoptera margin, but no wax. As they developed, white wax tufts (Coccinellidae) were identiÞed by Dr. Lu´ cia Massutti occurred laterally along the body and in a longitudinal de Almeida at the Zoology Department of Federal line from head to abdomen. Their dark-colored legs University of Parana´ (Curitiba, Parana´, Brazil), and were visible from above, and proportionally to the the Hymenoptera (Formicidae) were identiÞed by body, they were longer than in the second- and third- Karen Schmidt at the Department of Zoology of Uni- instar nymphs. versity of Brasõ´lia (Brasõ´lia, Federal District, Brazil). The Þrst-instar nymphs measured 0.84 Ϯ 0.01 mm in The studied insect vouchers are stored as part of the length and 0.46 Ϯ 0.01 mm in width just after emer- Entomological Collection of Embrapa Cerrados at gence and 1.77 Ϯ 0.02 mm in length and 0.87 Ϯ 0.01 Planaltina (Federal District, Brazil). mm in width at the end of this instar. The length/width ratio was 1.8 just after eclosion and 2.0 at the end of this instar. The increase in size during this instar was Results and Discussion 111% in length and 89% in width. No males of P. navesi were found in nature or in our Approximately 1.8 d after the initial feeding, the laboratory cultures, suggesting that the females repro- Þrst-instar nymphs developed a transparent anal wax duce by thelytokous parthenogenesis. Facultative or tube through which the honeydew was eliminated. At 782 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 4

Table 2. Average duration (؎ SEM) of the instars of P. navesi ,and their percent survival under laboratory conditions (25 ؎ 2°C (RH, and a photoperiod of 12:12 ͓L:D͔ h 23% ؎ 70

Duration Interval variation Survival Specimen Instar (d) (d) (%) no. (n) First 16.4 Ϯ 0.2 15Ð21 92.2 83 Second 11.6 Ϯ 0.2 6Ð16 73.5 61 Third 16.5 Ϯ 0.3 14Ð23 70.5 43

Þrst, this very thin tube was straight and directed downward; later, it assumed a spiral or irregular form and extended to 3Ð4 times the insectÕs length. Because honeydew might be a substrate for microorganisms, Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021 the anal tube allows the insect to eliminate honeydew far from its body to avoid contamination with its own waste and prevent the proliferation of fungi and bac- teria (Gullan 1997, Gullan and Kosztarab 1997). The Þrst instar of P. navesi lasted 16.4 d, on average, and the survival index during this stage was 92.2% (Table 2). In P. near primitiva, the duration of the Þrst instar observed by Schrader (1930) was 20 d, whereas in a Steatococcus sp. (also Monophlebidae), the Þrst instar lasted 8Ð12 d (McFadyen and Marohasy 1990). First-instar nymphs maintained in petri dishes with- out food stayed grouped for Ϸ6Ð8 d; thereafter, they displayed rapid movement. They survived an average of 10.4 d, but some specimens lived for 14 d. Second- and third-instar nymphs of P. navesi looked similar to the recently emerged adults. Second- and third-instar nymphs were reddish brown, and their bodies were covered with a thin wax layer; they dif- fered slightly in size and appearance from adults, be- cause the latter had a more convex body and no Fig. 1. Adult female of P. navesi covered with the wax mouthparts. The nymphs showed low mobility, mov- secretion. ing only after molting to search for a new feeding site, frequently close to the previous site, a behavior similar legs are short proportionally to the body size, and they to that of P. near primitiva (Schrader 1930). are not visible from the dorsal aspect. Insects did not The average durations of the second and third in- feed during the adult instar, and soon after emergence stars of P. navesi were 11.6 and 16.5 d, respectively, they left the host plant. with survival indices in these two stages of 73.5 and Approximately 2.7 d after emergence the adults 70.5%, respectively (Table 2). In comparison, the sec- began to secrete white wax in tufts over the dorsal ond and third instars of P. near primitiva lasted 14 and abdominal region. Afterward, the wax secretion cov- 22 d and of Steatococcus sp. lasted 8Ð12 and 12Ð13 d, ered the whole body (Fig. 1). After Ϸ4 d, the wax tufts respectively (Schrader 1930, McFadyen and Maro- on the abdomen formed an ovisac into which the eggs hasy, 1990). The body of the second-instar nymphs of were laid. The adult longevity was 26.8 d, on average P. navesi was 2.36 Ϯ 0.06 mm in length and 1.28 Ϯ 0.03 (Table 1), similar to P. near primitiva in which females mm in width just after the molt and 3.36 Ϯ 0.04 mm in survived for 29 d (Schrader 1930). The preoviposition length by 1.82 Ϯ 0.03 mm in width at the end of this period was 4.2 d, on average; oviposition lasted an instar. The length/width ratio was 1.8 and hardly var- average of 10.7 d, and the daily number of eggs per ied during this instar, despite a 42% increase in both female was 22.6 (Table 3). After the start of oviposi- length and width. The body of the third-instar nymphs tion, 74.2% of the total eggs per female were produced was 3.85 Ϯ 0.06 mm in length and 2.15 Ϯ 0.04 mm in during the Þve Þrst days (Fig. 2). In the biparental P. wide just after the molt and 6.69 Ϯ 0.08 mm in length near primitiva, females began oviposition 4Ð5 d after by 3.65 Ϯ 0.07 mm wide at the end of the third instar. copulation and laid a total of 16Ð65 eggs (n ϭ 3) The length/width ratio was 1.8, and it did not vary depending on body size (Schrader 1930). In an unre- during this instar, despite a 73% increase in length and lated scale insect, capensis Giard, that lives 70% in width. on the roots of grape vines in South Africa, females Adult Phase. Adult females have a reddish brown were reported to have, on average, a 9-d preoviposi- body, which is 7.92 Ϯ 0.12 mm in length and 4.37 Ϯ 0.08 tion period, an 11-d oviposition period, and a daily mm in width shortly after eclosion. The length/width production of 23 eggs, with 62% of egg production in ratio (1.8) was maintained as the adult matured. Its the four Þrst days (De Klerk et al. 1980). July 2008 OLIVEIRA ET AL.: BIOLOGY OF P. navesi 783

Table 3. Preoviposition and oviposition periods, average total early January 2004 until the end of this study (August egg number, and average daily egg number per adult female of P. 2004), no individuals of P. navesi were found on the navesi under laboratory conditions (25 ؎ 2°C, 70 ؎ 23% RH, and a photoperiod of 12:12 ͓L:D͔ h) aerial parts of cassava plants. On the aerial parts, nymphs were located initially on the basal stem, and Reproductive Interval Duration/no. later on the top parts of the plants. They were dis- characteristics variation tributed along the woody stems, and the Þrst-instar Preoviposition period (d) 4.2 Ϯ 0.1 2Ð6 nymphs were found speciÞcally near the insertion of Oviposition period (d) 10.7 Ϯ 0.5 4Ð15 the leaf petiole. However, no specimens were found Ϯ Avg. total egg no./female 239.6 13.9 120Ð427 feeding on leaf veins or blades. When the insects Avg. egg no./d/female 22.6 Ϯ 0.8 13Ð36 became adults, they left the host plant and moved to a secluded and dark place (the same behavior was observed in laboratory). Reproductive females were Oviposition and Incubation Period. P. navesi is ovip- found in soil Þssures, underneath stones, and under arous. Eggs of P. navesi had an elliptic shape (0.73 Ϯ Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021 soil clods or plant residues. In these places, the females 0.01 mm in length and 0.33 Ϯ 0.01 mm in width), a red color, and they were covered by a white powder. Each were found with the body covered by a white wax female produced almost 240 eggs on average (Table tufts, which in the Þnal portion of the abdomen, as well 3), and the incubation period lasted 24.7 d on average as in laboratory, formed an ovisac into which the eggs (Table 1). Reproductive females collected in the Þeld were laid. oviposited 244.3 eggs on average (data not shown), After planting, cassava plants go through Þve stages Ϸ very close to the number recorded in the laboratory. of development with a total duration of 1 yr (Alves In some other scale insects, relative humidity has 2002). The Þrst four phases (germination, formation of been shown to inßuence the percent eclosion and the root system, development of aerial parts, and forma- incubation period (Gonza´lez et al. 1969, De Klerk et tion of storage root) are of high growth with a duration al. 1980). The egg incubation procedure used in the of 10 mo. In the Þfth phase, known as dormancy, the present experiments (relative humidity between 93 plant loses leaves and stops its growth and only retains and 95% and P. navesi eggs isolated from wet surfaces) translocation of starch from the aerial parts to the was adequate, because the survival index for eggs was roots. This phase has a duration of 2 mo and occurs 92.5% (data not shown). In M. capensis, relative hu- mainly in regions with signiÞcant yearly variation in midity below 75.5% prevented nymphal eclosion, temperature and rainfall. After the dormancy phase, a whereas at 100% RH favored egg survival and eclosion, new cycle of growth begins primarily through the indicating that normal egg development strongly de- translocation of starch from roots to aerial parts pends on high relative humidity values (De Klerk et al. (Ternes 2002; Alves 2002, 2006). Nymphs of P. navesi 1980). Schrader (1930) observed a 24-d incubation occurred on the aerial parts of plants (SeptemberÐ period in P. near primitiva, very similar to that ob- December) after the dormancy phase and during the served in P. navesi, and low total number of eggs laid start of a new cycle of growth. This season coincides by females of P. near primitiva (65 or fewer per fe- with periods of increased relative humidity, mainly male). due to the increase of rainfall, and temperature in the Field. Insect Distribution on Plants. Throughout the “Cerrado” (Dias 1992, Klink and Machado 2005). evaluated period (September 2003ÐAugust 2004) These observations suggest that the vegetative growth Ϸ93% of the plants had specimens of P. navesi on their of the cassava plant, with high translocation of starch roots, and on each of the evaluated dates at least eight from roots to aerial parts, and the increase of relative of the 10 plants had scales on roots. Nymphs of P. humidity and temperature, provide favorable condi- navesi occurred on the aerial parts of plants during the tions for part of the population of P. navesi to colonize middle of September 2003, a period during when cas- the aerial parts of the plants. sava plant sprouts were developing, and P. navesi were Insect Movement in Field and on Plants. One hun- found on the aerial parts until December 2003. By dred percent of the specimens of P. navesi found walk- ing on the soil over the crop area were the newly emerged Þrst-instar nymphs of P. navesi. Some indi- viduals were found up to 15 m distant from the border of the crop area, suggesting that their easy transit during this developmental stage was the main dissem- ination method within the crop after introduction of this species into a Þeld. On the plants, all specimens found walking, also were newly emerged Þrst-instar nymphs. Our data suggest that once nymphs colonized the host plant and settled at their feeding sites, they did not move until the molt to the subsequent instar. From the second instar to the adult, the specimens Fig. 2. Average percentage of eggs produced daily per showed low mobility and continuous feeding, because adult female of P. navesi under laboratory conditions (25 Ϯ no second- or third-instar nymphs were found actively 2ЊC, 70 Ϯ 23% RH, and a photoperiod of 12:12 [L:D] h). moving up in the soil or on plants. The formation of an 784 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 101, no. 4 anal tube by the Þrst-instar nymphs was observed in of plants (AugustÐSeptember), just before the begin- the Þeld as well as in the laboratory. ning of the rainy season in the Brazilian “Cerrado,” Natural Enemy Studies. In terms of possible natural which occurs in the period SeptemberÐOctober until enemies, the predatory larvae of Chrysopidae (Neu- MarchÐApril. During the period NovemberÐDecem- roptera) and Syrphidae (Diptera) were present, but ber, the population of P. navesi was reduced drastically during Þeld observations there was no evidence of by Exoplectra sp. However, this natural enemy only them feeding on P. navesi. Only coccinellids were attacks the scale population on the aerial parts of observed on 80% of Þeld-collected plants that were plants and does not access the underground scale maintained within voile bags for 30 d, with 14 indi- population, which restricts the potential use of this vidual adult beetles per plant, on average, and no P. predator to control the pest. navesi specimens or any other natural enemy (pred- Approximately 8,000 scale species have been regis- ator or parasitoid) were present. On the other 20% of tered and they occur in practically all habitats and the plants, no natural enemies were found, but the colonize all plant parts. The international trade of number of scale specimens per plant was 369, on plants facilitates their further dispersal around the Downloaded from https://academic.oup.com/aesa/article/101/4/779/8542 by guest on 01 October 2021 average (data not shown). The predator was identiÞed world and can lead to the introduction of species to as Exoplectra sp. (Coccinellidae: Exoplectrinae), and foreign regions where they may become pests. For their larvae were found in the Þeld in early November, example, in 1973 an unknown scale insect was re- mostly around the Þeld borders. In general, this pred- corded on cassava in the Congo-Kinshasa and Congo- ator fed on the scales by biting around the middle of Brazzaville, Africa. After 13 yr, this species had spread their body margin. After that, the scales had their across 70% of the African cassava belt, causing direct integument disrupted, lost all their body liquids and losses of Ϸ80% (Herren and Neuenschwander 1991, died. By the end of December, adults of Exoplectra sp. Bellotti et al. 1999). This pest was identiÞed as a new were observed all over the planting area, and the scales species of mealybug, Phenacoccus manihoti Matile- had practically disappeared from the aerial parts of Ferrero, presumed to have come from the South plants. Schrader (1930) reported the occurrence of America. In its area of origin, this mealybug is a rare low population of predators (Coleoptera) and para- insect, but in Africa it spread rapidly over the entire sitoids (Hymenoptera) in P. near primitiva. cassava-growing area of the continent (Herren 1981, Ant species of the genera Camponotus Mayr and Herren and Neuenschwander 1991, Bellotti et al. Brachymyrmex Mayr were found associated with the 1999). cassava root scale, feeding on their honeydew. Many P. navesi is a high-risk pest for quarantine purposes of these ants had built their nests at the base of plants for the following reasons. It has a relatively short life and had constructed large galleries that might reduce cycle and very active Þrst-instar nymphs that can sur- rootÐsoil contact and decrease water and nutrient vive up to 2 wk without feeding. Natural enemies uptake by the plants. The nymphs of an unrelated scale cannot efÞciently control the population of this cas- insect, Eurhizococcus brasiliensis (Hempel), present in sava pest on roots of plants, and many weedy plant vineyards in Brazil, have been observed to be trans- species, mainly belonging to the Asteraceae [i.e., Ag- ported by ants of Linepithema Mayr and Nylanderia eratum conyzoides L., Bidens pilosa L., Emilia sonchi- Emery (Soria and Gallotti 1986, Hickel 1994). In P. folia (L.) DC, Tridax procumbens L., and Vernonia navesi, the transport by ants was not observed in the cognata Less.], are known to act as hosts for this scale Þeld, but it might be another viable mechanism for for at least four months in the absence of cassava plants scale dissemination. (Oliveira and Fontes 2008). Thus this scale species P. navesi has been reported recently as a new cas- presents a high dispersal risk, mainly due to the wide sava pest in Brazil (Federal District and states of Minas distribution of cassava propagation material (stems) to Gerais, Bahia, and Goia´s) (Oliveira and Fialho 2005, other regions of Brazil and even to foreign countries, Oliveira and Fialho 2006). The main types of damage where P. navesi should be considered a quarantine observed in infested cassava plants were lower cassava pest. stem sprouting potential, reduced growth, lower root production, and even plant death (Oliveira and Fialho 2005). Infested roots can have dark spots that depre- Acknowledgments ciate the productÕs commercial value. In addition to M. We thank the Embrapa Cerrados employees Jaˆnio Fon- esculenta and M. utilissima, P. navesi has been found on seca Silva, Sebastia˜o Batista da Silva, Joa˜o Gomes de Moura, roots of at least 15 weed species commonly found in and Paulo Bernardes de Castro for the helpful work on cassava planting areas (Oliveira and Fontes 2008). carrying out the experiments; Dra. Lu´ cia Massutti de These weedy plants probably serve as reservoirs that Almeida, who kindly identiÞed the Coccinellidae specimens; allow P. navesi to reinfest a newly planted cassava and Karen Schmidt, who kindly identiÞed the Formicidae crop. specimens. P.J.G. was supported by Hatch funding from the Fonseca (1979), who described P. navesi, reported California Agricultural Experiment Station. that plant stems (M. utilissima) were the insectÕs hab- itat. 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