Fruit flies (Diptera: Tephritidae) and Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) associated with fruit of the family Myrtaceae Juss. In South Africa

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Fruit flies (Diptera: Tephritidae) and Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) associated with fruit of the family Myrtaceae Juss. In South Africa

T

Tertia Grové∗, Karen de Jager, Maria L. Theledi1 Agricultural Research Council-Tropical and Subtropical Crops, Private Bag X11208, Nelspruit, 1200, South Africa

A R T I C LE I N FO

A B S T R A C T

Keywords: Bactrocera dorsalis Ceratitis capitata Ceratitis cosyra Ceratitis rosa Ceratitis quilicii Thaumatotibia leucotreta Myrtaceae

Fruit from 12 plant species of the family Myrtaceae Juss. were sampled from 2010 to 2017 in the Mpumalanga and Limpopo provinces of South Africa to obtain information on the host utilization of the economically important fruit fly species (Diptera: Tephritidae) and the false codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae). Bactrocera dorsalis (Hendel) was reared from five plant species, and significantly more B. dorsalis/kg fruit were reared from Syzygium samarangense (Blume) Merr. & L.M.Perry (P < 0.0001). Four plant species were not previously recorded as hosts for B. dorsalis in South Africa. Ceratitis capitata (Wiedemann) was reared from six plant species and significantly more were reared from Eugenia uniflora L. (P < 0.0001). Ceratitis cosyra (Walker) was reared from five plant species and only a few samples were positive with relatively low infestation indices. Ceratitis rosa sensu lato Karsch was reared from nine Myrtaceae fruit types. One hundred percent of Acca sellowiana (O.Berg) Burret, Psidium cattleianum Afzel. ex Sabine, and S. samarangense samples were positive for Ceratitis rosa sensu lato Karsch. The mean infestation index for C. rosa s.l. differed significantly between the fruit types, and significantly more were reared from P. cattleianum (P < 0.0001). From 2016, distinction was made between males of C. rosa sensu stricto and Ceratitis quilicii De Meyer, Mwatawala and Virgilio. Males from both species were reared from A. sellowiana, Psidium guajava L. and Syzygium jambos (L.) Alston while only C. rosa s.s. was reared from P. cattleianum, Psidium friedrichsthalianum (O.Berg) Nied. and Syzygium cordatum Hochst. ex Krauss. No fruit flies were reared from Plinia cauliflora (Mart.) Kausel and Syzygium paniculatum Gaertn. Thaumatotibia leucotreta was reared from 11 Myrtaceae fruit types. Acca sellowiana, P. cauliflora, P. cattleianum, P. friedrichsthalianum, S. paniculatum and S. samarangense were not previously recorded as host plants for T. leucotreta. Fruit flies and T. leucotreta were reared from fruit sampled from the tree and from the ground highlighting the importance of sanitation as a method to suppress pest population levels. The presence of economically-important fruit flies and T. leucotreta in invasive plant species highlights the importance of controlling these plants as they can serve as a reservoir when cultivated fruit are not present. Myrtaceae plants commonly found in gardens were also identified as hosts and these plants could serve as a breeding place for fruit flies and T. leucotreta. These pests could move from home gardens to orchards when fruit start to mature.

1. Introduction The horticultural industry is a fast-growing industry in Africa, which contributes greatly to livelihoods by promoting food security, and increases foreign export earnings. Numerous types of insect pests have a negative impact on fruit and vegetable production in Africa, and fruit flies (Diptera: Tephritidae) are among the most economically-important (Badii et al., 2015a; Ekesi et al., 2016). Females puncture and lay eggs

in fruit and vegetables, and inflict direct damage due to feeding of the larvae. The economic impact includes direct yield losses, increased production costs due to suppression actions, and the use of insecticides which can negatively impact on the environment. Fruit flies are also a limiting factor in international trade of fresh agricultural commodities. In the tribe Dacini, Bactrocera Macquart and Ceratitis MacLeay are among the important pest genera of tephritid fruit flies occurring naturally in Africa (White, 2006). Species of the genus Bactrocera are

∗

Corresponding author. Agricultural Research Council-Tropical and Subtropical Crops, Private Bag X11208, Nelspruit, 1200, South Africa. E-mail address: [email protected] (T. Grové). 1 P.O. Box 1344, White River, 1240, South Africa. https://doi.org/10.1016/j.cropro.2018.10.008 Received 30 April 2018; Received in revised form 2 October 2018; Accepted 4 October 2018 0261-2194/ © 2018 Elsevier Ltd. All rights reserved.

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Table 1 Host plants of the family Myrtaceae for fruit fly species of economic importance in Africa. Plant species (Common name)

Fruit fly species

References

Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava)

Bactrocera dorsalis (Hendel) Ceratitis capitata (Wiedemann)

White and Elson-Harris, 1992; Liquido et al., 1991 De Meyer and White, 2004; White and Elson Harris, 1992; USDAAPHIS, 2017 Badii et al., 2015b De Meyer and White, 2004

Eugenia brasiliensis Lam. (Brazil cherry)

Eugenia Eugenia Eugenia Eugenia Eugenia Eugenia

involucrata DC. (Cherry of the Rio Grande) myrcianthes Nied. (Ubajai) palumbis Merr. pyriformis Cambess. (Uvaia) rosea DC. uniflora L. (Pitanga, Surinam cherry)

Ceratitis cosyra (Walker) Ceratitis quilicii De Meyer, Mwatawala and Virgilio B. dorsalis C. capitata C. capitata C. capitata B. dorsalis C. capitata Ceratitis anonae Graham B. dorsalis C. anonae C. capitata

Myrcianthes pungens (O.Berg) D.Legrand (Guabiju) Pimenta dioica (L.) Merr. (Allspice, Pimento) Plinia cauliflora (Mart.) Kausel (Jaboticaba) Psidium cattleianum Afzel. ex Sabine (Strawberry guava)

Ceratitis cosyra C. quilicii Ceratitis rosa sensu lato Karsch Trirhithrum coffeae Bezzi C. capitata B. dorsalis C. capitata B. dorsalis B. zonata C. anonae C. capitata

Psidium friedrichsthalianum (O. Berg) Nied. (Costa Rican guava) Psidium guajava L. (Common guava)

C. C. C. C. C. B.

cosyra quilicii rosa s.l. capitata quilicii dorsalis

Bactrocera mesomelas (Bezzi) Bactrocera zonata (Saunders) C. anonae C. capitata

Psidium guineense Sw. (Brazilian guava) Rhodomyrtus tomentosa (Aiton) Hassk. (Downy rose myrtle) Syzygium aqueum (Burm.f.) Alston (Watery rose-apple)

Syzygium aromaticum (L.) Merr. & L.M.Perry (Clove) Syzygium borneense (Miq.) Miq. Syzygium cordatum Hochst. ex Krauss (Water berry) Syzygium cumini (L.) Skeels (Java plum)

Syzygium formosanum (Hayata) Mori Syzygium grande (Wight) Walp. (Sea apple) Syzygium guineense (Willd.) DC. (Water pear)

C. cosyra Ceratitis fasciventris (Bezzi) Ceratitis punctata (Wiedemann) C. quilicii Ceratitis quinaria (Bezzi) Ceratitis rosa Karsch C. rosa s.l. Ceratitis stipula De Meyer and Freidberg Dacus ciliatus (Loew) Zeugodacus cucurbitae (Coquillett) C. capitata C. quilicii B. dorsalis B. dorsalis C. quilicii C. rosa s.l. B. dorsalis B. dorsalis C. capitata C. rosa s.l. B. dorsalis C. capitata C. C. C. B. B. C.

cosyra quilicii rosa s.l. dorsalis dorsalis rosa s.l.

Liquido et al., 1991 White and Elson-Harris, 1992; USDA-APHIS, 2017 USDA-APHIS, 2017 USDA-APHIS, 2017 Liquido et al., 1991 USDA-APHIS, 2017 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, et al., 1991; USDA-APHIS, 2017 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, 1992 De Meyer and White, 2004 De Meyer and White, 2004 White and Elson-Harris, 1992 De Meyer and White, 2004 USDA-APHIS, 2017 Liquido et al., 1991 White and Elson-Harris, 1992; USDA-APHIS, 2017 White and Elson-Harris, 1992; Liquido et al., 1991 Sookar and Deguine, 2016 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, APHIS, 2017 Mwatawala et al., 2009b De Meyer and White, 2004 White and Elson-Harris, 1992 De Meyer and White, 2004; USDA-APHIS, 2017 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, et al., 1991 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, APHIS, 2017 De Meyer and White, 2004; White and Elson-Harris, De Meyer and White, 2004 De Meyer and White, 2004 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, De Meyer and White, 2004 White and Elson-Harris, 1992 De Meyer and White, 2004 Isabirye et al., 2016a, b Allwood et al., 1999 USDA-APHIS, 2017 De Meyer and White, 2004 Liquido et al., 1991 White and Elson-Harris,1992; Liquido et al., 1991 De Meyer and White, 2004 White and Elson-Harris, 1992 Tsuruta et al., 1997 Liquido et al., 1991 Grové et al., 2017 Grové et al., 2017 Liquido et al., 1991 De Meyer and White, 2004; White and Elson-Harris, APHIS, 2017 Badii et al., 2015b De Meyer and White, 2004 White and Elson Harris, 1992 Liquido et al., 1991 Liquido et al., 1991 Grové et al., 2017

1992; Liquido

1992; USDA-

1992; Liquido

1992 1992; UDSA1992

1992

1992; USDA-

(continued on next page)

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Table 1 (continued) Plant species (Common name)

Fruit fly species

References

Syzygium jambos (L.) Alston (Jambos, Rose apple)

B. B. C. C. C. C. C. B. B.

C. quilicii Ceratitis rosa s.l. B. dorsalis

De Meyer and White, 2004; Liquido et al., 1991 De Meyer and White, 2004 Isabirye et al., 2016b White and Elson-Harris, 1992; USDA-APHIS, 2017 De Meyer and White, 2004 De Meyer and White, 2004 White and Elson-Harris, 1992 Liquido et al., 1991 De Meyer and White, 2004; White and Elson-Harris, 1992; Liquido et al., 1991 De Meyer and White, 2004 White and Elson-Harris, 1992 USDA-APHIS, 2017 De Meyer and White, 2004 White and Elson-Harris, 1992 Liquido et al., 1991

B. dorsalis

Liquido et al., 1991

C. B. B. C.

USDA-APHIS, 2017 White and Elson-Harris, 1992; Liquido et al., 1991 De Meyer and White, 2004 De Meyer and White, 2004; White and Elson-Harris, 1992; USDAAPHIS, 2017 De Meyer and White, 2004

Syzygium lineatum (DC.) Merr. & L.M.Perry Syzygium malaccense (L.) Merr. & L.M.Perry (Malay-apple)

dorsalis zonata anonae capitata fasciventris quilicii rosa s.l. dorsalis dorsalis

C. capitata

Syzygium megacarpum (Craib) Rathakr. & N.C.Nair (Giant lau lau) Syzygium nervosum A.Cunn. ex DC. (Daly River Satinash, Rai Jamun) Syzygium paniculatum Gaertn. (Magenta cherry) Syzygium samarangense (Blume) Merr. & L.M.Perry (Java apple, Wax Jumbo)

capitata dorsalis zonata capitata

C. quilicii

distinguished morphologically. Another significant pest to the horticulture industry in sub-Saharan Africa is the false codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) (Venette et al., 2003; Gilligan et al., 2011; Prinsloo and Uys, 2015). This moth species is a significant pest of fruit trees and field crops. Numerous cultivated crops and wild plants are listed as hosts (USDA-APHIS-PPQ-EDP, 2010), although this host list was subsequently greatly reduced when sources of reliable host data were unavailable (EPPO, 2013; Moore et al., 2015). In cultivated crops, damage is particularly severe on citrus, pomegranates and peppers. Females deposit eggs singly on fruit and developing larvae cause significant damage by feeding. Feeding can also result in premature ripening and fruit drop as well as secondary infection by fungi. Thaumatotibia leucotreta is regarded as a phytosanitary threat when host commodities are exported to countries where it is absent and can possibly become established. This species is often intercepted at ports-ofentry in North America and Europe (Gilligan et al., 2011). The vast majority of interceptions in North America are historically from John F. Kennedy International Airport in New York (Venette et al., 2003), thus with travellers rather than imported consignments of fruit. In this study, fruit of the myrtle family (Myrtaceae Juss.) within the order Myrtales, were collected. The Myrtaceae is an important angiosperm family containing trees and shrubs, frequently with conspicuous oil glands and edible fruit (Wilson, 2011; Mitra et al., 2012). Genera which are of particular interest for the production of edible fruit include: Acca, Eugenia, Psidium and Syzygium (Mitra et al., 2012). Various economically-important fruit fly species in Africa utilize Myrtaceae as host plants (De Meyer and White, 2004; Copeland et al., 2006; Mwatawala et al., 2009b; Goergen et al., 2011; José et al., 2013; Badii et al., 2015b; Isabirye et al., 2016a; Grové et al., 2017). Current known information on Myrtaceae hosts utilized by the important fruit fly species present in Africa is presented in Table 1. Information on the known Myrtaceae host plants for T. leucotreta is provided in Table 2. Botanical nomenclature follows The Plant List (2013). The first objective of the study was to obtain baseline information on the host profile, host preference and niche partitioning of the main pest fruit fly species. Currently, information on the host plant range of B. dorsalis in South Africa is still limited. The second objective was to obtain information on the host profile of T. leucotreta. Insufficient information exists on alternative host plants that T. leucotreta utilize when cultivated fruits are

predominantly of Indo-Australian origin (White, 2006). Bactrocera species are well documented as invaders. In Africa, 11 indigenous species are known. However, Asian Bactrocera species were introduced to Africa (De Meyer and Ekesi, 2016). Of those introduced species, the Oriental fruit fly, Bactrocera dorsalis (Hendel) is currently the most widespread on the African continent and poses a major threat to horticulture. In Africa, the first species of B. dorsalis were observed on the Kenyan coast in 2003 and was initially described as a new species, Bactrocera invadens Drew, Tsuruta and White (Drew et al., 2005). Bactrocera dorsalis was first detected in the Limpopo province of South Africa during 2010 (Manrakhan et al., 2011). Whereas eradication was initially successful, the pest was later declared present but subjected to official control in the Vhembe District Municipality in Limpopo during 2013 (Manrakhan et al., 2015). In Mpumalanga province, B. dorsalis was detected in specified areas in the Ehlanzeni District Municipality during 2012 (IPPC, 2012). Subsequently, B. dorsalis was declared present in specific district municipalities of Limpopo, Mpumalanga, North West, Gauteng and KwaZulu-Natal during 2015 (IPPC, 2015). The latest update on the distribution in South Africa was given in February 2018 (IPPC, 2018). Bactrocera dorsalis is known to be a highly polyphagous species and various host plants were reported in Africa (Mwatawala et al., 2006, 2009b; Rwomushana et al., 2008; Goergen et al., 2011; José et al., 2013; Badii et al., 2015b). In many African countries, B. dorsalis is now the dominant fruit fly species attacking cultivated crops (Ekesi et al., 2009; Mwatawala et al., 2009a; Massebo and Tefera, 2015). In South Africa, only a few host plants were reported (Grové et al., 2017; Theron et al., 2017). Ceratitis is predominantly an Afrotropical genus comprising 95 species found in sub-Saharan Africa and the islands of the western Indian Ocean (De Meyer et al., 2015, 2016). Species within the genus attack a wide range of indigenous fruit and cultivated crops (Copeland et al., 2002, 2006; De Meyer et al., 2002; De Meyer and White, 2004; Grové et al., 2017). In South Africa, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), the Marula fruit fly, Ceratitis cosyra (Walker) and Natal fruit fly, Ceratitis rosa sensu lato Karsch are three fruit fly pests of importance for the fruit industry (Prinsloo and Uys, 2015). Recently, C. rosa s.l. was split into two species, i.e. C. rosa and the Cape fruit fly, Ceratitis quilicii De Meyer, Mwatawala and Virgilio (De Meyer et al., 2015, 2016). The two species can be distinguished based on morphological characteristics in males only, while females cannot be 26

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2. Materials and methods

commercial scale in South Africa (Van Wyk, 2005). Approximately 45 000 tonnes of common guava are produced in the country and the majority is used in processing. The P. guajava is listed as an invasive species (a. NEMBA – Category 2 for plantations in Eastern Cape, KwaZulu-Natal, Limpopo, Mpumalanga and North West; b. NEMBA – Category 3 elsewhere in the above listed provinces; c. not listed if used for human consumption). Syzygium cordatum Hochst. ex Krauss (Water berry) is indigenous to southern Africa and the fleshy fruit is edible (Van Wyk et al., 2012). Syzygium guineense (Willd.) DC. (Water pear) is found in many parts of Africa, both wild and domesticated, and the fruit is edible (Van Wyk et al., 2012). Syzygium jambos (L.) Alston (Jambos, Rose apple) is native to south-east Asia, and encountered in gardens in South Africa and is listed as an invasive species (NEMBA – Category 3). Syzygium paniculatum Gaertn. (Magenta cherry) is a rainforest tree native to New South Wales, Australia and is a popular ornamental plant, often planted in hedges. The plant is considered by Henderson (2001) as a potential transformer. Syzygium samarangense (Blume) Merr. & L.M.Perry is indigenous to Malaysia.

2.1. Plant species sampled

2.2. Fruit collection

Twelve different Myrtaceae plant species were sampled (Tables 3 and 5). Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava) is indigenous to southern Brazil, Paraguay, Uruguay and north-eastern Argentina (Van Wyk, 2005). Although not cultivated on a commercial scale in South Africa, it is a common garden plant. Eugenia uniflora L. (Pitanga, Surinam cherry) originates from Tropical America and is a common garden plant (Van Wyk, 2005). Eugenia uniflora is listed as a Category 1b invasive species according to the National Environmental Management: Biodiversity Act, 2004 (Act No. 10 of 2004), Alien and Invasive Species Lists, 2016 (RSA, 2016). Pimenta dioica (L.) Merr. (Allspice, Pimento) is indigenous to Central America and the West Indies (Van Wyk, 2005). Plinia cauliflora (Mart.) Kausel (Jaboticaba) is indigenous to southern Brazil, where it is a traditional food source. Psidium cattleianum Afzel. ex Sabine (Strawberry guava) originated in the lowlands of eastern Brazil but has been distributed to numerous parts of the world as a fruit tree and as an ornamental plant (Van Wyk, 2005). Psidium cattleianum is an invasive plant species (NEMBA – Category 1b). Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava) grows naturally in Colombia, throughout Central America and in southern Mexico (Van Wyk, 2005). Psidium guajava L. (Common guava) is indigenous to Central America and is cultivated on a

Fruit were collected from 2010 to 2017 in three district municipalities in Limpopo (Capricorn, Mopani and Vhembe) and two in Mpumalanga province (Ehlanzeni and Gert Sibande). Only one sample was collected in Gert Sibande District Municipality. Most of the fruit samples (123 out of 204 for fruit fly and 97 out of 154 for T. leucotreta) were harvested from trees growing on the experimental farm of the Agricultural Research Council-Tropical and Subtropical Crops, Nelspruit (Ehlanzeni District Municipality). Due to the fact that different fruit trees were grown in close proximity, high fruit fly and T. leucotreta numbers were present on the farm. Samples were taken from different plant species at random and therefore varied, with the aim of collecting 10 or more fruit per sample (Tables 3 and 5). Only five samples had less than 10 fruit. Mature ripe fruit were sampled in all instances. The months when fruit were mature and were sampled is presented in Table 6. Fruit samples harvested from the indigenous S. cordatum and S. guineense, and reported by Grové et al. (2017), were included in the data. Collected fruit were placed in paper or plastic bags and transported in cool boxes to facilities at Nelspruit and Tzaneen. The number of fruit in each sample was counted and weighed. Fruit were placed on chicken wire mesh in cylindrical plastic containers (5 l or 10 l) with sterilized sand placed at the bottom of the containers. Mesh-

Table 2 Host plants of the family Myrtaceae for Thaumatotibia leucotreta. Plant species (Common name)

References

Eugenia uniflora L. (Pitanga, Surinam cherry) Psidium guajava L. (Common guava)

Venette et al., 2003

Syzygium cordatum Hochst. ex Krauss (Water berry) Syzygium guineense (Willd.) DC. (Water pear) Syzygium jambos (L.) Alston (Jambos, Rose apple)

Schwartz, 1981; Venette et al., 2003; USDA-APHIS-PPQ-EDP, 2010 Schwartz, 1981; Venette et al., 2003; Brown et al., 2014 Brown et al., 2014 USDA-APHIS-PPQ-EDP, 2010

not present. This information is important in the management strategies for the containment of pests.

Table 3 Number of samples of the different Myrtaceae plant species examined for the presence of fruit flies and the incidence and percentage positive samples for each fruit fly species. Plant species (Common name)

Exotic plant species Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava) Eugenia uniflora L. (Pitanga, Surinam cherry) Pimenta dioica (L.) Merr. (Allspice, Pimento) Plinia cauliflora (Mart.) Kausel (Jaboticaba) Psidium cattleianum Afzel. ex Sabine (Strawberry guava) Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava) Psidium guajava L. (Common guava) Syzygium jambos (L.) Alston (Jambos, Rose apple) Syzygium paniculatum Gaertn. (Magenta cherry) Syzygium samarangense (Blume) Merr. & L.M.Perry (Java apple, Wax jumbo) Indigenous plant species Syzygium cordatum Hochst. ex Krauss (Water berry) Syzygium guineense (Willd.) DC. (Water pear)

No. samples (tree, ground)

No. fruit

Fruit weight (kg)

No. positive samples (Percentage) Bactrocera dorsalis

Ceratitis capitata

Ceratitis cosyra

Ceratitis rosa s.l.

41 (20, 20)

1118

23.316

2 (4.9%)

0

4 (9.8%)

41 (100%)

17 (17, 1) 5 (5, 0) 15 (12, 3) 14 (8, 6)

1642 185 812 1391

6.303 0.087 4.709 4.640

0 0 0 7 (50.0%)

16 (94.1%) 1 (20.0%) 0 4 (28.6%)

0 0 0 2 (14.3%)

6 (35.3%) 0 0 14 (100%)

10 (4, 6)

126

3.698

0

0

3 (30.0%)

6 (60.0%)

18 (8, 10) 26 (24, 2) 13 (13, 0) 2 (1, 1)

502 1165 1364 49

31.611 2.989 3.045 1.104

9 (50.0%) 7 (26.9%) 0 2 (100%)

9 (50.0%) 4 (15.4%) 0 0

4 (22.2%) 1 (3.8%) 0 0

17 (94.4%) 25 (96.2%) 0 2 (100%)

22 (22, 0) 21 (21, 0)

4441 1723

8.890 5.689

0 0

7 (31.8%) 0

0 0

10 (45.5%) 4 (19.0%)

27

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fitted lids were placed on containers to ensure good ventilation. Samples were placed at room temperature for approximately 8 weeks and examined for fruit fly and moth emergence. In the beginning of the study, the samples were not examined for the presence of T. leucotreta but commenced in 2014 and continued until 2017 (Table 5). Before discarding samples, fruit and sand were examined for the presence of larvae, moth pupae, fruit fly puparia and adults. Fruit sampling and processing followed the methodology described by Copeland et al. (2002) and Copeland (2007).

indices for the different fruit types (F11, 203 = 7.58, P < 0.0001, LSD = 13.845). Significantly more B. dorsalis/kg fruit was reared from S. samarangense in comparison with the other plant species. Ceratitis capitata was reared from six different plant species and 94.1% of E. uniflora samples were positive. A significant difference in infestation indices was present for C. capitata for the different plant species and significantly more was reared from E. uniflora (F11, 203 = 20.42, P < 0.0001, LSD = 26.477). Ceratitis cosyra was reared from five plant species and only a few samples were positive. There was a significant difference in infestation indices of C. cosyra for the different fruit types and the highest number was reared from P. guajava (F11, 203 = 2.14, P = 0.0196, LSD = 4.916). Ceratitis rosa s.l. was present in nine fruit types. One hundred percent of A. sellowiana, P. cattleianum and S. samarangense samples were positive for C. rosa s.l. The infestation indices for C. rosa s.l. differed significantly between the 12 plant species (F11, 203 = 19.57, P < 0.0001, LSD = 75.399). Significantly more C. rosa s.l. was reared from P. cattleianum in comparison with the other plant species. Significant differences were present in the mean infestation indices of B. dorsalis, C. capitata, C. cosyra and C. rosa s.l. in A. sellowiana, E. uniflora, P. cattleianum, P. friedrichsthalianum, P. guavaja, S. jambos, S. samarangense and S. cordatum (Table 4.) All four fruit fly species were reared from P. guajava and S. jambos. Ceratitis spp. dominated over B. dorsalis in all the fruit types. Ceratitis capitata was the abundant species found in E. uniflora with a mean of > 100 C. capitata/kg fruit. Ceratitis capitata was the only species reared from P. dioica. In comparison to all the other fruit fly species, significantly more C. rosa s.l./kg fruit was found in A. sellowiana, P. cattleianum, P. friedrichsthalianum, S. jambos, and S. cordatum. In A. sellowiana, P. cattleianum and S. samarangense > 100 C. rosa s.l./kg fruit were reared. No fruit flies were reared from P. cauliflora and S. paniculatum. In samples processed during 2016/17, distinction was made between C. quilicii and C. rosa s.s. and both were identified. Both males of C. quilicii and C. rosa s.s. were reared from A. sellowiana, P. guajava and S. jambos, while only C. rosa s.s. was reared from P. cattleianum, P. friedrichsthalianum and S. cordatum (Table 7). Fruit flies were reared from fruit sampled from the tree and ground and there were no significant differences between the infestation indices (A. sellowiana F1, 39 = 2.13, P = 0.1523; P. cattleianum F1, 9 = 0.16, P = 0.6971; P. friedrichsthalianum F1, 13 = 0.01, P = 0.9252; P. guajava F1, 17 = 0.09, P = 0.7699). No B. dorsalis was reared from the fruit samples harvested from 2010 to 2013 and an increase in the mean infestation index for B. dorsalis was observed from 2014 to 2016 (Fig. 1).

2.3. Identification of insects and plant species Keys were used for the identification of fruit flies (De Meyer, 1998, 2000; De Meyer and Freidberg, 2006; White, 2006; Virgilio et al., 2014). Distinction between males from C. rosa sensu stricto and C. quilicii were carried out in 2016 and 2017. For the identification of T. leucotreta, the diagnostic characteristics for adults described by Rental (2013) were used. The head has dark chaetosemas and antennae with one row of scales per segment. Forewings have a distinct question-mark pattern along the termen, a semi-circle along the costal margin and a white discal spot situated between these two pattern elements. T. leucotreta is sexually dimorphic. Males can be easily distinguished by the distinctive scent gland on the hindwing and dense black tufts on the hind tibia. Plant identification was done by horticulturists at the Agricultural Research Council-Tropical and Subtropical Crops and by the South African National Biodiversity Institute. 2.4. Data analyses The incidence was determined for each fruit fly species reared from the 12 different fruit types. Incidence was defined as the number of infested or positive samples in comparison with the total number of samples per fruit species. The infestation index was calculated as the number of emerged adult flies per 1 kg of fruit (Cowley et al., 1992). These infestation indices were calculated for each fruit fly species in each fruit sample. The quantitative results for T. leucotreta are presented as number of moths per fruit in each fruit sample. By calculating these indices, samples with different weights and numbers could be compared. SAS® 9.4 was used for analyses of data (GLM Procedure). The infestation index of B. dorsalis in each of the 12 fruit types (source of variation) was subjected to ANOVA and comparisons of means were performed using LSD test (⍺ = 0.05). Likewise, the infestation indices for the other fruit fly species was analysed. The mean infestation indices for B. dorsalis, C. capitata, C. cosyra and C. rosa s.l. (source of variation) in each fruit type were subjected to ANOVA and means were separated using LSD test (⍺ = 0.05). The mean infestation index for fruit sampled from the ground and from the trees (source of variation) was subjected to ANOVA and comparison of means were performed with LSD test (⍺ = 0.05) for fruit types: A. sellowiana, P. cattleianum, P. friedrichsthalianum and P. guajava. The ANOVA on ranks was used to analyse the number of T. leucotreta per fruit in each of the fruit types (source of variation). For all ANOVA models, the replicates were the samples of fruit (generally 10 fruit or more) as indicated in Tables 3 and 5 Tukey's HSD test (⍺ = 0.05) was used to find means of T. leucotreta that are significantly different from each other.

3.2. Thaumatotibia leucotreta

3. Results

Thaumatotibia leucotreta was reared from the fruit of all plant species sampled except P. dioica (L.), from which only one sample was examined (Table 5). Thaumatotibia leucotreta were present in samples from the tree and from the ground. More than 70% of A. sellowiana and S. guineense samples were positive for T. leucotreta. The highest mean of T. leucotreta per fruit was found in A. sellowiana. The ANOVA on ranks was significant, which indicated that at least one sample stochastically dominates one other sample (F11, 153 = 4.26, P < 0.0001). The means of A. sellowiana and S. guineense were significantly different from E. uniflora, S. cordatum and S. jambos (Critical value of Studentized Range = 4.69994).

3.1. Fruit flies

4. Discussion

Bactrocera dorsalis, C. capitata, C. cosyra and C. rosa s.l. were reared from the sampled fruit. Table 3 shows the number and percentage positive samples for the four fruit fly species in each of the 12 fruit types. Table 4 shows the mean infestation index of each fruit fly species in the different Myrtaceae fruit. Bactrocera dorsalis was reared from five plant species and there was a significant difference in the mean infestation

Bactrocera dorsalis was reported for the first time in South Africa from A. sellowiana, P. cattleianum, S. jambos and S. samarangense. Acca sellowiana was also reported as a host in Ghana and Uganda (Badii et al., 2015b; Isabirye et al., 2016a). Eugenia uniflora was reported as a host in West Africa and in Uganda but no positive samples were found in this study (Goergen et al., 2011; Isabirye et al., 2016a). Psidium cattleianum 28

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Table 4 Mean infestation indices of fruit fly species reared from the different Myrtaceae plant species. Plant species (Common name)

Mean number of fruit flies/kg fruit (SD) Bactrocera dorsalis

Ceratitis capitata

Ceratitis cosyra

Ceratitis rosa s.l.

Exotic plant species Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava)

0.15 (0.69)

0

0.44 (1.66)

150.13 (108.74)

Eugenia uniflora L. (Pitanga, Surinam cherry)

0

111.42 (96.18)

0

4.71 (8.20)

Pimenta dioica (L.) Merr. (Allspice, Pimento)

0

21,92 (49.01)

0

0

Plinia cauliflora (Mart.) Kausel (Jaboticaba) Psidium cattleianum Afzel. ex Sabine (Strawberry guava)

0

0

0

0

20.59 (32.84)

4.13 (7.55)

1.64 (5.01)

296.85 (174.74)

Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava)

0

0

2.70 (5.10)

57.15 (71.85)

Psidium guajava L. (Common guava)

12.47 (40.88)

6.16 (9.00)

6.37 (16.97)

28.09 (25.81)

Syzygium jambos (L.) Alston (Jambos, Rose apple)

3.88 (8.17)

1.27 (3.63)

0.07 (0.35)

96.07 (117.24)

Syzygium paniculatum Gaertn. (Magenta cherry) Syzygium samarangense (Blume) Merr. & L.M.Perry (Java apple, Wax jumbo)

0 80.75 (7.42)

0 0

0 0

0 209.35 (105.15)

0

4.06 (8.35)

0

15.29 (34.73)

0

0

0

2.3 (6.58)

Indigenous plant species Syzygium cordatum Hochst. ex Krauss (Water berry)

Syzygium guineense (Willd.) DC. (Water pear)

F-value P LSD

F3, 163 = 77.93 P < 0.0001 LSD = 23.718 F3, 67 = 22.05 P < 0.0001 LSD = 33.072 F3, 19 = 1.00 P = 0.4182 LSD = 32.585 – F3, 39 = 36.78 P < 0.0001 LSD = 67.512 F3, 39 = 6.11 P = 0.0018 LSD = 32.666 F3, 71 = 2.82 P = 0.0451 LSD = 17.301 F3, 103 = 16.75 P < 0.0001 LSD = 32.351 – F3, 7 = 7.03 P = 0.0450 LSD = 146.330 F3, 87 = 3.60 P = 0.0168 LSD = 10.709 F3, 83 = 2.56 P = 0.0605 LSD = 2.021

invasion into the country (Henderson, 2001). Mature P. guajava fruit were available for a lengthy period in South Africa (Table 6). Syzygium jambos was reported as an important host plant for in West Africa (Goergen et al., 2011) and is an important host in spring and summer in South Africa (Table 6). Syzygium samarangense was found to be an important host for B. dorsalis in this study and mature fruit were present in February and March (Table 6). The infestation index of. B. dorsalis varied between different fruit types, which indicates a preference for some fruit types over others. Bactrocera dorsalis and Ceratitis spp. were found in the same host plants which displayed interspecific competition, but Ceratitis spp. appeared to be dominant. Although dominance of B. dorsalis was not observed during the study, this might change in future. Bactrocera dorsalis is known to be highly competitive and has a number of traits that are advantageous over indigenous Ceratitis spp. (Ekesi et al., 2009). The number of positive samples and the mean infestation index for B. dorsalis increased rapidly from 2014. Cerartitis capitata was especially found to be associated with E. uniflora. Mature fruit were found from October to December (Table 6). Ceratitis cosyra was reported for the first time from Psidium friedrichsthalianum and S. jambos. Only 11 (5.4%) samples were positive for C. cosyra and Myrtaceae fruit are probably not preferred hosts. In Swaziland, a low percentage of C. capitata and C. cosyra emerged from feral P. guajava in comparison with the high percentage of C. rosa s.l. (Magagula and Ntonifor, 2014). Ceratitis rosa s.l. was reared from 61.3% of samples and a high infestation index was found in some of the fruit types, therefore Myrtaceae plants seem to be important hosts. There was a continuous supply of mature Myrtaceae host fruit throughout the year for C. rosa s.I. (Table 6). Important hosts for C. rosa s.l. were A. sellowiana, P.

Fig. 1. Percentage positive samples and the mean infestation indices for Bactrocera dorsalis in Myrtaceae plants from 2010 to 2016.

was also reported as an important host plant in Tanzania (Mwatawala et al., 2009b). Acca sellowiana and P. cattleianum were especially important hosts from February to May in South Africa (Table 6). Psidium guajava was previously recorded as a host plant in South Africa (Theron et al., 2017). In Mozambique and Tanzania, P. guajava was reported as an important host with high infestation indices (Mwatawala et al., 2009b; José et al., 2013). In this study, one P. guajava sample had an infestation index of 175.0 B. dorsalis/kg fruit and this sample was the only one where dominance over Ceratitis spp. was observed. Feral P. guajava trees are widely distributed in parts of Limpopo and Mpumalanga, and these host plants probably contributed to the progressive 29

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Table 5 Number of samples of the different Myrtaceae plant species examined for the presence of Thaumatotibia leucotreta and the number and percentage positive samples and the mean number/fruit. Plant species (Common name)

Exotic plant species Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava) Eugenia uniflora L. (Pitanga, Surinam cherry) Pimenta dioica (L.) Merr. (Allspice, Pimento) Plinia cauliflora (Mart.) Kausel (Jaboticaba) Psidium cattleianum Afzel. ex Sabine (Strawberry guava) Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava) Psidium guajava L. (Common guava) Syzygium jambos (L.) Alston (Jambos, Rose apple) Syzygium paniculatum Gaertn. (Magenta cherry) Syzygium samarangense (Blume) Merr. & L.M.Perry (Java apple, Wax jumbo) Indigenous fruit species Syzygium cordatum Hochst. ex Krauss (Water berry) Syzygium guineense (Willd.) DC. (Water pear)

No. samples (tree, ground)

No. fruit

Fruit weight (kg)

Number of positive samples (Percentage)

Mean number of T. leucotreta/ fruit (SD)

38 (19, 19)

1047

21.207

28 (73.7%)

0.10 (0.16)

15 (14, 1) 1 (1, 0)

864 31

4.213 0.016

3 (20%) 0

0.01 (0.01) 0

12 (10, 2) 8 (3, 5)

667 414

3.628 1.658

7 (58.3%) 3 (37.5%)

0.01 (0.02) 0.04 (0.07)

10 (4, 6)

126

3.698

4 (40.0%)

0.02 (0.02)

17 (7, 10) 15 (15, 0)

445 416

27.087 8.822

10 (58.8%) 4 (26.7%)

0.06 (0.08) 0.01 (0.02)

5 (5, 0) 2 (1,1)

421 49

0.892 1.104

2 (40.0%) 1 (50.0%)

0.02 (0.03) 0.04 (0.05)

16 (16, 0) 15 (15, 0)

2260 969

4.721 2.987

7 (43.8%) 12 (80.0%)

0.01 (0.01) 0.08 (0.09)

Table 6 Months when fruit of the different Myrtaceae plant species beared mature fruit and were sampled. Plant species (Common name) Exotic plant species Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava) Eugenia uniflora L. (Pitanga, Surinam cherry) Pimenta dioica (L.) Merr. (Allspice, Pimento) Plinia cauliflora (Mart.) Kausel (Jaboticaba) Psidium cattleianum Afzel. ex Sabine (Strawberry guava) Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava) Psidium guajava L. (Common guava) Syzygium jambos (L.) Alston (Jambos, Rose apple) Syzygium paniculatum Gaertn. (Magenta cherry) Syzygium samarangense (Blume) Merr. & L.M.Perry (Java apple, Wax jumbo) Indigenous plant species Syzygium cordatum Hochst. ex Krauss (Water berry) Syzygium guineense (Willd.) DC. (Water pear)

Jan

Feb

Mar

Apr

May

X

X

X

X

X

X

X X

X X

X

X

X

Jun

X X

X X

Aug

Sep

Oct

Nov

Dec

X

X

X

X

X

X

X

X X

X X

X

X X

X

X X

X

X X

Jul

X

X

X

X X

confirmed in this study (Table 2). Acca sellowiana, P. cattleianum and S. guineense were identified as important hosts which can provide a reservoir when cultivated host fruit crops are not available (Table 6). The presence of fruit flies and T. leucotreta in fruit sampled from the ground stress the importance of sanitation as a method of control. Invasive plant species served as hosts for economically-important fruit fly species and T. leucotreta, therefore it is important to control these plants, especially in the vicinity of orchards. These plants can serve as reservoirs for pests when cultivated crops are not available. Invasive plant species can also provide pathways for range expansion and this is especially important for B. dorsalis, which is a newly-introduced species and with a limited distribution. Myrtaceae host plants growing in home gardens – often without any suppression methods – could enable fruit flies and T. leucotreta to reach high population levels. This places an emphasis on the importance of integrated area-wide management approaches which aim at addressing the total pest population within a delimited area, and not only fractions of the population.

cattleianum, P. friedrichsthalianum, S. jambos and S. samarangense, with more than 50% positive samples and with high infestation indices. A high infestation index of C. rosa s.l. was also reported from S. jambos in home gardens in the Western Cape province (De Villiers et al., 2013). Different Ceratitis spp. co-occurred in the same fruit types, which demonstrated interspecific competition. The closely-related species, C. quilicii and C. rosa s.s., were reared from the same host plants (Table 7). Psidium friedrichsthalianum was previously recorded as a host plant for C. quilicii, although not found in this study (Table 1). Although in only a few samples differentiation was made between the two species, results indicated that C. rosa s.s. dominated at lower altitudes such as Nelspruit (677 m), while at higher altitudes such as Ermelo (1667 m), C. quilicii was found. Mwatawala et al. (2015) found in Tanzania that C. rosa s.s. was predominant at lower altitudes while C. quilicii was predominant at higher altitudes. Acca sellowiana, P. cauliflora, P. cattleianum, P. friedrichsthalianum, S. paniculatum and S. samarangense were not previously recorded host plants for T. leucotreta, and this study confirmed the polyphagous nature of this species. Previously recorded Myrtaceae host plants were 30

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Table 7 Number of Ceratitis quilicii and Ceratitis rosa s.s. reared from the different Myrtaceae plant species during 2016/17. Plant species (Common name)

Exotic plant species Acca sellowiana (O.Berg) Burret (Feijoa, Pineapple guava)

Psidium cattleianum Afzel. ex Sabine (Strawberry guava) Psidium friedrichsthalianum (O.Berg) Nied. (Costa Rican guava) Psidium guajava L. (Common guava)

Syzygium jambos (L.) Alston (Jambos, Rose apple)

Indigenous plant species Syzygium cordatum Hochst. ex Krauss (Water berry)

Sample no.

Locality

District municipality

No. Ceratitis quilicii males/kg fruit

No. Ceratitis rosa s.s. males/kg fruit

No. Ceratitis. quilicii & Ceratitis rosa females/kg fruit

1 2 3 4 5 6 1

Ermelo Nelspruit Nelspruit Nelspruit Nelspruit Nelspruit Nelspruit

Gert Sibande Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni

31.6 0 0 0 0 0 0

0 11.5 3.7 59.7 37.2 83.9 213.5

26.3 34.4 9.9 42.6 43.7 86.8 236.0

1

Nelspruit

Ehlanzeni

0

4.9

2.5

1 2 3 4 1 2 3 4 5 6 7 8 9

Mganduzweni Bushbuckridge Tzaneen Tzaneen Nelspruit Nelspruit Nelspruit Nelspruit Nelspruit Nelspruit Hazyview Nelspruit Hazyview

Ehlanzeni Ehlanzeni Mopani Mopani Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni

35.0 0 1.8 0 0 0 1.7 5.2 0 0 27.7 0 3.8

0 10.2 7.4 2.6 14.8 8.3 27.0 41.4 28.0 242.1 0 137.0 0

53.8 16.3 9.2 2.6 5.9 30.3 40.5 60.8 31.5 259.6 25.2 201.3 0

1 2 3 4

Nelspruit Nelspruit Nelspruit Nelspruit

Ehlanzeni Ehlanzeni Ehlanzeni Ehlanzeni

0 0 0 0

8.1 1.8 33.0 7.3

0 2.9 26.4 14.6

Acknowledgements

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