The Distribution, Relative Abundance, and Seasonal Phenology of Ceratitis capitata, Ceratitis rosa, and Ceratitis cosyra (Diptera: Tephritidae) in South Africa Author(s): Marelize De Villiers, Aruna Manrakhan, Pia Addison, and Vaughan Hattingh Source: Environmental Entomology, 42(5):831-840. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN12289

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COMMUNITY AND ECOSYSTEM ECOLOGY

The Distribution, Relative Abundance, and Seasonal Phenology of Ceratitis capitata, Ceratitis rosa, and Ceratitis cosyra (Diptera: Tephritidae) in South Africa MARELIZE DE VILLIERS,1,2 ARUNA MANRAKHAN,3,4 PIA ADDISON,4

AND

VAUGHAN HATTINGH1

Environ. Entomol. 42(5): 831Ð840 (2013); DOI: http://dx.doi.org/10.1603/EN12289

ABSTRACT Ceratitis capitata (Wiedemann), Ceratitis rosa Karsch, and Ceratitis cosyra (Walker) are fruit ßy species (Diptera: Tephritidae) of economic importance in South Africa. These pests cause direct damage to a number of commercially produced fruit and are of phytosanitary concern. A study was conducted to determine the distribution, relative abundance, and seasonal occurrence of the three species in different climatic regions of South Africa. The relative abundance and seasonal phenology of C. capitata and C. rosa were also compared between production areas and home gardens in Stellenbosch, Western Cape. Yellow bucket traps baited with Biolure were used to trap the ßies over a 2-yr period in the different sampling areas. Different fruit types were sampled in Stellenbosch to determine fruit ßy infestation. C. capitata was found to have a widespread distribution in South Africa, whereas C. rosa were absent from or only present in low numbers in the drier regions. C. cosyra was restricted to the North East and East coast, following a similar pattern to the distribution of marula, Sclerocarrya birrea, an important wild host. Fruit in home gardens provided a breeding ground for C. capitata and C. rosa and a source for infestation of orchards when fruit started to mature, highlighting the need for an area-wide strategy for the control of fruit ßies. KEY WORDS Ceratitis, Mediterranean fruit ßy, Natal fruit ßy, marula fruit ßy, ecology

Fruit ßies belong to the family Tephritidae, which is one of the largest and most economically important in the order Diptera (White and ElsonÐHarris 1992). The larvae of most tephritid species develop in the seedbearing organs of plants, and ⬇35% breed in soft fruit including many commercial fruit types (White and ElsonÐHarris 1992). The family Tephritidae consists of many genera, including Ceratitis Mac Leay (Dacinae: Ceratitidina: Dacini)Ña predominantly Afrotropical group consisting of 88 species (White and ElsonÐ Harris 1992, De Meyer 2001). Within the Ceratitis group, the Mediterranean fruit ßy, Ceratitis capitata (Wiedemann), is the most notorious, having spread from Africa to most regions of the world (White and ElsonÐHarris 1992, De Meyer 2000, European and Mediterranean Plant Protection Organization [EPPO] 2012). South Africa currently hosts a total of 27 Ceratitis species, 17 of which are associated with commercially produced fruit and nut crops and the remaining are 1 Citrus Research International, Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Victoria St, Stellenbosch, 7600, South Africa. 2 Corresponding author, e-mail: [email protected]. 3 Citrus Research International, 2 Baker St, Nelspruit, 1200, South Africa. 4 Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Victoria St, Stellenbosch, 7600, South Africa.

associated with wild hosts (Annecke and Moran 1982; Hancock 1984, 1989a,b; White and ElsonÐHarris 1992; Du Toit 1998; De Meyer 1998, 2001; De Meyer and Freidberg 2006; Carroll et al. 2006). The main Ceratitis pest species of economic importance in South Africa are C. capitata, Ceratitis rosa Karsch (Natal fruit ßy), and Ceratitis cosyra (Walker) (marula fruit ßy) (Annecke and Moran 1982). C. capitata and C. rosa are important pests of citrus, deciduous, and subtropical fruit, whereas C. cosyra is mostly a pest of subtropical fruit in South Africa (Annecke and Moran 1982). These three species cause direct damage to commercial fruit crops and are also of phytosanitary concern and may result in restrictions on international fruit trade (Barnes 2000, EPPO 2012). All three species are polyphagous, attacking various fruit types, more so for C. capitata and C. rosa than for C. cosyra (De Meyer et al. 2002, Belgian Biodiversity Information Facility 2010). C. capitata, C. rosa, and C. cosyra differ in their distribution patterns in South Africa (Du Toit 1998, De Meyer 2001), with C. capitata being more ubiquitous in its distribution within the country, C. rosa being more abundant in the northeastern and coastal regions, and C. cosyra being restricted to the northeastern part of the country. In South Africa, the three fruit ßy species are currently controlled mainly by the application of toxic baits as sprays or in bait stations (Barnes 2000). In addition, C. capitata is controlled through the Sterile

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Fig. 1. riod.

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Vol. 42, no. 5

Sampling areas (black dots) where Ceratitis species were monitored across South Africa over a 2-yr pe-

Insect Technique (SIT) in deciduous fruit growing areas in some parts of the Western Cape Province (Barnes and Venter 2008). Information on population ecology of pests is important for implementation of proper control strategies. Despite the importance of the Ceratitis pest species in South Africa, little quantitative information has to date been published on their relative abundances in different regions of the country and their spatial and temporal population dynamics. Moreover, little is known about the ecology of the Ceratitis species in different habitat types (cultivated and noncultivated areas) and host types within a cultivated area. In most fruit production areas in South Africa, fruit ßy control strategies are directed at farms or groups of farms, using a scheduled “calendar” program. Control using bait application usually starts 1Ð2 mo before harvest. Surrounding areas and nearby residential areas are usually not included in the fruit ßy management program. However, these marginal and residential areas in particular are breeding grounds or overwintering sites for local fruit ßy pests (Barnes 2008). Although general distribution patterns of C. capitata, C. rosa, and C. cosyra in South Africa were described by De Meyer (2001), these patterns were largely based on localities associated with collection of specimens and literature records rather than systematic sampling across the year and fruiting season. There were no published information on the relative abundance and seasonal occurrence of the three Ceratitis pests in different areas of South Africa, before the current study. Previous authors have demonstrated differences in the inßuence of temperature, relative humidity, and light intensity on the development, survival, and mating behavior of C. capitata and

C. rosa (Myburgh 1962, Duyck et al. 2006, Nyamukondiwa and Terblanche 2009, Nyamukondiwa et al. 2010), indicating that climate may inßuence their distribution and abundance. Therefore, the objective of this study was to determine the distribution, relative abundance, and seasonal occurrence of C. capitata, C. rosa, and C. cosyra in different climatic regions of South Africa. In addition, the relative abundance and temporal ßuctuations of C. capitata and C. rosa were compared between two habitat types (production areas and home gardens) and in fruit types, within commercial fruit production areas in a temperate climatic region. Materials and Methods Distribution, Relative Abundance, and Seasonal Phenologies of Ceratitis Pest Species in South Africa. To determine the distribution ranges, relative abundances, and seasonal phenology of the Ceratitis species across South Africa, 36 sampling areas representing different climatic regions of the country were used (Fig. 1). The Ko¨ ppenÐGeiger climate classiÞcation system (Kriticos et al. 2012) was used to deÞne the climate types (see Table 1). Because little information is available on the distribution of C. rosa on the West coast of the country, proportionally more sampling sites were chosen in this region (Fig. 1). In each of the sampling areas, three yellow bucket traps (Chempac [Pty] Ltd., Paarl, South Africa), each baited with three-component Biolure Fruit Fly (Chempac [Pty] Ltd., Paarl, South Africa) (consisting of ammonium acetate, putrescine, and trimethylamine), were used to monitor the fruit ßies, as this lure-trap combination is attractive to all three species targeted in the study

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Table 1. The relative abundance (mean number of C. capitata, C. rosa, and C. cosyra flies per trap per month), mean yearly minimum and maximum temperature, and mean yearly precipitation across different climatic regions of South Africa Climate type

Description

BWh

Arid, desert, hot

BWk

Arid, desert, cold

BSh

Arid, steppe, hot

BSk

Arid, steppe, cold

Csa

Temperate, dry and hot summer

Csb

Temperate, dry and warm summer

Cwa

Temperate, dry winter, hot summer Temperate, dry winter, warm summer Temperate, without dry season, hot summer Temperate, without dry season, warm summer

Cwb Cfa Cfb

Relative abundance C. capitata

C. rosaa

C. cosyra

Tmin (⬚C)

Tmax (⬚C)

Rain (mm)

Northern Cape Northern Cape Western Cape Western Cape Northern Cape Limpopo Western Cape Northern Cape Eastern Cape Mpumalanga Mpumalanga Limpopo Limpopo Free State Northern Cape Free State Northern Cape Northern Cape Northern Cape North West Western Cape Western Cape Western Cape Western Cape Western Cape Western Cape Western Cape Western Cape Mpumalanga North West KwaZulu Natal Limpopo KwaZulu Natal Western Cape Eastern Cape

14.4 54.1 39.6 38.9 0.08 0.7 518.6 15.0 28.0 10.4 33.5 0.3 0.2 13.3 53.4 103.7 0.9 30.5 124.3 27.7 32.5 38.0 2.3 198.2 268.9 161.2 28.7 15.8 5.6 1.3 10.3 9.0 1.9 1.3 190.8

0 0 0.02 0 0 1.4 0.01 3.6 191.8 33.2 18.6 0.09 0.4 54.7 0.8 0.4 0 0.6 0 7.8 148.7 25.5 0.01 35.5 0.7 29.6 137.6 267.6 168.1 41.3 200.7 55.8 39.6 0 269.6

0 0 0 0 0 3.5 0 0.01 0 0.7 23.3 2.0 0.4 0 0 0 0 0 0 0.02 0 0 0 0 0 0 0 0 15.3 1.3 0.2 1.0 0.02 0 0

11.0 12.5 11.9 7.8 11.0 12.8 10.2 9.9 11.1 15.9 11.6 13.7 15.9 7.8 8.4 9.1 10.3 9.4 10.3 9.5 10.9 10.8 11.1 10.9 9.9 11.8 9.9 10.1 13.0 10.5 11.5 11.4 14.4 11.4 11.8

28.3 30.2 27.3 23.0 22.8 27.6 26.2 26.8 26.0 29.7 27.7 29.2 28.6 24.4 24.8 24.0 25.4 25.5 23.9 26.4 23.3 24.1 24.7 23.9 24.5 20.4 20.2 21.5 25.8 26.3 24.5 23.9 25.1 24.6 23.5

3.1 1.7 3.3 5.2 2.4 8.8 5.4 8.3 6.6 12.1 11.2 7.4 9.3 Ko¨ ppen 10.6 5.3 7.7 3.3 6.8 3.5 9.1 15.6 8.0 8.5 11.5 7.4 12.1 17.9 18.3 16.4 12.9 17.0 21.6 18.7 10.4 11.9

Western Cape

13.9

20.2

10.9

20.9

17.4

Location

Province

Keimoes Onseepkans Vanrhynsdorp Beaufort West Hondeklipbaai Baltimore Clanwilliam Jan Kempdorp Kirkwood Komatipoort Marble Hall Tom Burke Tshipise Bloemfontein Britstown Gariepdam Garies Olifantshoek Springbok Vryburg Paarl Piketberg Porterville Riebeek Kasteel Citrusdal Onrus River Somerset West Stellenbosch Nelspruit Rustenburg Pietermaritzburg Tzaneen Nkwalini Swellendam King WilliamÕs Town Knysna

0

a

Taken from De Villiers et al. (2013). The 10⬘ CliMond climate dataset was used for climate averages, and the Ko¨ ppenÐGeiger climate classiÞcation system (Kriticos et al. 2012) was used to deÞne the climate types. See Ko¨ ppen (1936) for a detailed description of the parameters.

(Grove´ and De Beer 2011). A 1 by 1 cm block of Dichlorvos (containing 2, 2 dichlorovinyl dimethyl phosphate [Chempac (Pty) Ltd., Paarl, South Africa] was placed in each trap to kill fruit ßies entering the trap. The traps were placed 1.5Ð2 m above ground in host plants of the three Ceratitis species, or in suitable shade trees in proximity to a host plant. At each site, the three traps were placed at least 150 m from one another. Traps were placed mostly in home gardens in towns where chemical sprays were not applied, but at some locations, traps had to be placed on farms, either in home gardens within farms or in orchards depending on presence of host trees, as suitable monitoring sites were unavailable in the town. All traps were rebaited and trap catches collected once a month over a 2-yr period, with one exception. Sampling at Tom Burke in the Limpopo Province continued for 11 mo, whereafter this site was substituted with a nearby site at Baltimore (Fig. 1), where sampling continued for one more year. Monitoring commenced between August and October 2006 at the majority of the sites. Exceptions were Paarl, Pietermaritzburg, Nk-

walini, Hondeklipbaai, and Baltimore, where monitoring commenced during November 2006, April 2007, June 2007, August 2007, and August 2008, respectively. Relative Abundance and Temporal Fluctuations of C. capitata and C. rosa in Different Habitat Types in the Western Cape Province. Adult fruit ßy trapping and fruit sampling were carried out from May 2006 to April 2008 in and within a radius of 10 km of Stellenbosch (Fig. 1) in the Western Cape Province of South Africa, where both C. capitata and C. rosa are known to occur. Fruit ßy populations were monitored in three selected deciduous fruit orchards and three selected home gardens. In all three selected orchards, fruit ßy control was carried out mainly by weekly groundbased sprays with either a mixture of protein hydrolysate and malathion or GF-120 during the deciduous fruiting season, between October and May. Proper sanitation practices were also followed in all three deciduous fruit orchards. There were no fruit left over on trees and no fruit lying on the ground after harvest. In home gardens, there was no chemical control of fruit ßies. Fruit lying on the ground around the host trees were regularly removed.

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Fig. 2. Relative abundance (mean number of ßies per trap per month) and seasonal phenology of C. capitata in South Africa. The climate types are shown in the phenology graphs (see Table 1 for descriptions).

Fruit ßy adult populations were monitored using the Multilure trap (Betterworld manufacturing, Fresno, CA) baited with Biolure Fruit Fly. A 1 by 1 cm block of Dichlorvos was placed in each trap to kill attracted ßies. Four traps were placed in each selected orchard. Traps were placed at least 200 m apart and distributed between different commercial fruit species and cultivars present within the orchard. These included Prunus persica (L.) variety nucipersica (nectarine), Prunus domestica L. (plum), Pyrus communis L. (pear), Malus domestica Borkh (apple), and Citrus reticulata Blanco (mandarin). One trap was placed in a host tree in each of three home gardens, except in one garden where a second trap was placed in July 2007. These host trees were Mangifera indica L. (mango), Dovyalis caffra (Hook f. & Harvey) Warburg (Kei-apple), and Prunus persica (L.) variety persica (peach). All traps were placed ⬇1.5 m above ground in the tree canopy. Traps were serviced fortnightly except during the winter period of 2007, between July and September, where they were serviced monthly. Lures and killer blocks were replaced every 6 Ð 8 wk. Ripe fruit in orchards and home gardens were collected from the tree or the ground every 2Ð 4 wk, depending on fruit availability. All fruit collections were placed in individual plastic bags and were transported to rearing facilities in Stellenbosch. Fruit were counted, weighed, and placed in plastic containers covered with gauze. Fruit were incubated over a

slightly moist 2 cm layer of sterilized sand. All fruit samples were kept at ambient temperatures, except during the colder months between June and August when fruit were moved to a heated room maintained at a temperature of ⬇26⬚C. Fruit samples were regularly examined for insect emergence. If adult insects were found, the fruit containers were opened inside a transparent Perspex cage (50 by 50 by 50 cm) to capture the live adults. Any emerged tephritid ßies were then transferred to transparent Perspex cages (12 by 12 by 4.5 cm) and provided with water, sugar, and enzymatic yeast hydrolysate separately. Four days after emergence, fruit ßies were killed by freezing, identiÞed, sexed, and counted. Representative ßies were pinned and kept in the insect collections at the Department of Conservation Ecology and Entomology, University of Stellenbosch. Data Analysis. For each site, the relative abundance of each Ceratitis species was determined by calculating the mean number of ßies caught per trap per month and combining data from the three traps at each sampling site, as well as combining data from all the months during which sampling was done into one value. This resulted in a single relative abundance value for each species at each location. A Pearson correlation was calculated between relative abundance and the mean yearly maximum and minimum temperature and the mean yearly precipitation, respectively. As actual weather data for all sites were not available over the sampling period, long-term averages

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Fig. 3. Relative abundance (mean number of ßies per trap per month) and seasonal phenology of C. rosa in South Africa (De Villiers et al. 2013). The climate types are shown in the phenology graphs (see Table 1 for descriptions).

were taken, using the 10⬘ CliMond climate dataset (Kriticos et al. 2012) of historical long-term monthly climate averages for minimum and maximum temperature and precipitation, centered on 1975. For each site, seasonal occurrence was expressed as the mean number of ßies per site, per month, over the 2 yr. For the temporal ßuctuations of C. capitata and C. rosa in orchards and home gardens, the mean number of ßies per trap per day (FTD) was calculated for each month and each habitat type (home gardens vs. orchards) and for each host type in orchards. Effects of habitat and host on population levels of each species were determined using nonparametric KruskalÐWallis test (XLSTAT Version 2012.4.02, Addinsoft), as FTD values were not normally distributed (ShapiroÐWilk test; P ⬍ 0.05). For determination of fruit infestation in different habitat types, the total number of ßies per species that emerged from each fruit type was determined and expressed as the number of ßies per kg of infested fruit. Relative abundance of C. capitata and C. rosa was determined for each habitat type and host type using a Relative Abundance Index (RAI) formula developed by Segura et al. (2006): RAI ⫽ Number of C. capitata/ (Number of C. capitata ⫹ Number of C. rosa). RAI ⫽ 1 indicates exclusive presence of C. capitata and RAI ⫽ 0 indicates exclusive presence of C. rosa. The RAI was calculated for sampled fruit and for traps in the two habitat types (home garden and orchard). For each sampled fruit kind, the index was based on the total

number of ßies of each species reared from the fruit, whereas for the traps it was based on the total number of ßies of each species captured in all the traps in a particular habitat. Results Distribution, Relative Abundance, and Seasonal Phenologies of Ceratitis Species. C. capitata was present at all sampling sites across South Africa, with abundance generally high in the drier BW and BS climates, as well as the temperate Cs and Cfb climates (Table 1; Fig. 2). The correlation between precipitation and relative abundance of C. capitata was ⫺0.2 (n ⫽ 36; P ⫽ 0.3). The correlation between relative abundance and minimum and maximum temperature was ⫺0.2 (P ⫽ 0.3) and ⫺0.1 (P ⫽ 0.5), respectively. C. rosa had a more restricted distribution, being absent from the arid desert climates (BWh and BWk), except for Vanrhynsdorp where two ßies were trapped over the 2-yr period (Table 1; Fig. 3). C. rosa was generally also scarce in the arid steppe climates (BSh and BSk). However, at 3 of 15 sites sampled in the arid steppe climate, viz. Bloemfontein, Kirkwood, and Komatipoort, C. rosa was the most abundant of the three species. In terms of relative abundance of C. rosa, there was a positive correlation between precipitation and relative abundance (r ⫽ 0.6; n ⫽ 36; P ⬍ 0.001). A gradient was observed along the West coast, with abundance being higher in the South (with temperate

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Fig. 4. Relative abundance (mean number of ßies per trap per month) and seasonal phenology of C. cosyra in South Africa. The climate types are shown in the phenology graphs (see Table 1 for descriptions).

Cs climates) and decreasing toward the North, as the climate becomes drier. Another gradient was observed in the eastern half of the country, with abundance being higher around the coast and northeastern boundaries (with temperate Cw and Cf climates) and decreasing toward the drier inland areas. The correlation between relative abundance and minimum and maximum temperature was ⬍0.1 (P ⫽ 0.8) and ⫺0.3 (P ⫽ 0.04), respectively. C. cosyra had the narrowest distribution, being restricted to the northeastern regions and the East coast (Table 1; Fig. 4). Here it occurred in the temperate Cw and Cf climates, as well as the drier BSh climate. The correlation between relative abundance and minimum temperature, maximum temperature, and precipitation was 0.2 (n ⫽ 36; P ⫽ 0.3, 0.2, and 0.3, respectively) in all cases. In the arid BW and BS climates, as well as the temperate Csb and Cwa climates, seasonal phenology of the three species was similar, with numbers of all three species generally increasing during late spring (September and October), reaching a peak in the hot summer months (January to March) and declining into the winter (June to August) (Figs. 2Ð 4). In the Csa climatic zone (Riebeek Kasteel), numbers peaked in April. In the Cwb (Pietermartizburg) and Cfa (Nkwalini) climatic regions, numbers generally peaked in the autumn and winter period. This pattern was also observed for C. rosa in Kirkwood (BS climate). Relative Abundance and Temporal Fluctuations of C. capitata and C. rosa in Habitat and Host Types.

Generally, populations of both C. capitata and C. rosa were signiÞcantly higher (P ⬍ 0.0001) in home gardens (C. capitata: 2.47 ⫾ 0.84 ßies per trap per day; C. rosa: 2.59 ⫾ 0.38 ßies per trap per day) compared with orchards (C. capitata: 0.77 ⫾ 0.18 ßies per trap per day; C. rosa: 0.54 ⫾ 0.07 ßies per trap per day). C. capitata and C. rosa were equally abundant in the home gardens, while in orchards, C. capitata was slightly more abundant than C. rosa (Table 2; Fig. 5). For both fruit ßy species, population ßuctuations differed between home gardens and commercial orchards, particularly with respect to the timing and intensity of the peak levels (Fig. 5). A peak in population levels occurred earlier in the year in the home gardens, between January and March, with numbers peaking in the commercial orchards between March and May. The peaks in population levels were higher for both C. capitata and C. rosa in the home gardens (C. capitata: 11.86 ⫾ 6.11 ßies per trap per day; C. rosa: 7.45 ⫾ 2.24 ßies per trap per day) compared with orchards (C. capitata: 2.59 ⫾ 1.35 ßies per trap per day; C. rosa: 1.36 ⫾ 0.37 ßies per trap per day). Fruit ßy populations, in particular C. rosa, were sustained in home gardens throughout the year (Fig. 5), although during the winter months (JuneÐAugust) population levels of both species were low. Hosts such as guava were available in home gardens during the winter period (Table 2) and were mainly infested by C. rosa. In the orchards during the winter months, no or few C. rosa ßies were captured (Fig. 5). C. capitata pop-

0.6

837

C. rosa

2 26 109 11 56 38 8 0 0 5 5 95 43 104 25 2 0 25 0 0 4 52 14 13 7 5 2 7 31 76 117 2 8 1

16.5 26.7 371.0 30.6 36.2 242.1 142.4 11.2 39.7 23.0 11.2 39.2 29.1 32.6 37.2 9.0 12.9

0.9 0.0 0.0 0.3 0.5 0.3 0.6 1.0 1.0 0.3 0.6 0.2 0.6 0.5 0.1 0.8 1.0

0.5

DE VILLIERS ET AL.: ECOLOGY OF Ceratitis PEST SPECIES

C. capitata

1.6 1.0 0.3 0.5 3.0 0.2 0.1 0.6 0.1 0.3 1.1 3.2 4.2 8.0 0.7 1.1 0.9

Fig. 5. Population ßuctuations of C. capitata and C. rosa over 12 mo in commercial orchards and home gardens in Stellenbosch.

2 2 1 1 7 2 1 1 1 8 2 6 6 4 4 3 1

38 21 18 17 322 6 62 11 NA 8 60 31 43 70 8 27 NA

ulations, however, were sustained in the orchards at low levels between June and August and declined thereafter to almost zero in September and October. In orchards, populations peaked earlier in the season (summer to autumn) in deciduous fruit orchards (nectarine, plum, and apple) and later (autumn to winter) in citrus orchards (Fig. 6). For both fruit ßy species, however, there were no signiÞcant differences in catches between different host types. C. capitata and C. rosa were able to infest similar host types, with few hosts being exclusively infested by one of the species (Table 2). In home gardens, only C. rosa adults were reared from infested guava and jambos while only C. capitata adults were reared from infested peach and strawberry tree berries. In orchards, only C. capitata adults were reared from infested wine grape berries (Table 2). The relative abundance of C. capitata and C. rosa in some hosts also varied between habitat types. For instance, citrus in orchards were mainly infested by C. capitata, whereas in home gardens, citrus was more abundantly infested with C. rosa. No fruit ßy infestation was recorded on dune myrtle (Eugenia capensis (Ecklon & Zeyher) Harvey & Sonder) and lemon (Citrus limon (L.) N. L. Burman), which were sampled from home gardens. In the study orchards in Stellenbosch, no fruit ßy infestation was recorded on apple. The study orchards were, however, subject to bait application for fruit ßy control. NA ⫽ not available.

Orchard

Fig Guava Jambos Kei-apple Loquat Mango Natal Plum Peach Strawberry tree Soft citrus (Easy Peeler) Kei-apple Nectarine Peach Pear Plum Soft citrus (Easy Peeler) Winegrape Ficus carica Psidium guajava Syzygium jambos Dovyalis caffra Eriobotrya japonica Mangifera indica Carissa macrocarpa Prunus persica var. persica Arbutus unedo Citrus reticulata Dovyalis caffra Prunus persica var. nusipersica Prunus persica var. persica Pyrus communis Prunus domestica Citrus reticulata Vitis vinifera Home garden

Common name ScientiÞc name

Jan. JulyÐAug. Feb. Feb. Sep.ÐNov. Jan.ÐFeb. Nov. Jan. May Mar. Jan., Mar. Oct.ÐDec. Oct.ÐJan. Jan.ÐMar. Jan.ÐFeb. Jul., Oct.ÐNov. Mar.

Total no. fruit units No. samples Months sampled Host Habitat type

Table 2.

C. capitata and C. rosa infestation of different fruit types in home gardens and orchards

Total wt of infested fruit (kg)

Total no. of adults emerged

Infestation level (ßies/kg fruit)

RAI in sampled fruit

RAI in traps

October 2013

Discussion C. capitata appears to be well adapted to all climates in South Africa. C. rosa, however, although being also widely distributed across South Africa, was absent in the generally drier regions. In fruit infestation studies conducted in Stellenbosch, where C. capitata and C. rosa coexisted, both species were found to infest a

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ENVIRONMENTAL ENTOMOLOGY

Fig. 6. Population ßuctuations of C. capitata and C. rosa over 12 mo in Þve commercial host fruit environments in Stellenbosch.

similar range of hosts, although host preferences differed between species, and similar hosts were used differently by the two species depending on habitats. These results indicate that for these two polyphagous species, host plant availability is not an important

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limiting factor determining their distribution. The results suggest that abiotic factors, such as temperature, humidity, and rainfall, are more important in inßuencing abundance and distribution of these pests. Nyamukondiwa and Terblanche (2009) found that C. capitata had a greater heat tolerance than C. rosa. Moreover, a model based on temperature tolerances of C. capitata and C. rosa showed that time to extinction was greater for C. capitata than for C. rosa in habitats where temperatures dropped below 10⬚C (Nyamukondiwa et al. 2010). C. capitata may also be better adapted to arid climates, and Duyck et al. (2006) showed that the pupae of C. capitata were less sensitive to desiccation than C. rosa. In the current study, we found C. rosa abundance to be positively correlated with precipitation, with higher abundance in areas with higher rainfall. The distribution of C. cosyra, however, appears to be more related to host plants than climate, following a similar pattern in distribution to that of marula, an important wild host of the species, which occurs in the northeastern part of the country, over the entire Limpopo province and parts of the North West, Gauteng, Mpumalanga, and KwaZulu Natal provinces (Venter and Venter 2007). The distribution of marula included all sites at which C. cosyra was present, with the exception of Vryburg. However, at the latter, only one specimen of C. cosyra was found during the 2-yr sampling period. C. cosyra was found to have a more restricted host range compared with C. capitata and C. rosa (De Meyer et al. 2002, Copeland et al. 2006). As C. cosyra has similar developmental thresholds to C. capitata and C. rosa (Grout and Stoltz 2007), its more restricted distribution is unlikely to be a result of climate. With regard to temporal ßuctuations or phenology of the three fruit ßy species in areas where they occurred, it is likely that host availability was more inßuential than climate, as there were many instances where similar phenological patterns were observed in different climatic regions, for example, the pattern for C. capitata in Keimoes (BWh climate), Bloemfontein (BSk climate), and Stellenbosch (Csb climate) were similar, yet the three areas fall into different climatic regions (Fig. 2). In most areas, fruit ßy population peaks were observed between early summer and autumn, generally declining toward the winter period (June to August). However, in the citrus production areas of the KwaZulu Natal and Eastern Cape provinces, the peaks shifted more toward the autumn and winter period, with ßies occurring in large numbers throughout the cold winter months. This may possibly be because of the availability of ripening citrus fruit produced in the area. The ßuctuating within-season population levels of C. capitata and C. rosa found in this study, in different habitats and different hosts within an area, is indicative of movement and dispersal of fruit ßies in response to host fruit availability. Myburgh (1964) studied the population ßuctuations of C. capitata in some areas of Western Cape and also found similar C. capitata phenology in dedicuous orchards and in home

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DE VILLIERS ET AL.: ECOLOGY OF Ceratitis PEST SPECIES

gardens. Myburgh (1964) also highlighted the importance of mixed fruit gardens for harboring C. capitata populations during winter. Tropical fruit ßies are known to be strong ßyers engaging in dispersal activities as a result of unavailability of hosts in an area, increases in air temperature, and foraging behavior of adults (Bateman 1972). C. capitata is known to disperse over both short and long distances (up to 9.5 km) (Meats and Smallridge 2007), and high infestations and adult population levels in home gardens would possibly lead to high egg pressure and consequent invasion of orchards during fruit ripening. Similar results were found by Israely et al. (1997) where a continuous ßow of C. capitata was reported from home gardens into commercial orchards, and from host to host within orchards, at varying times of fruit maturation. In studies conducted in northern Greece, distribution of C. capitata was also found to be patchy in mixed deciduous fruit orchards, with aggregation of females being closely related to phenology of the host tree and sequential availability of ripe or semiripe fruit (Papadopoulos et al. 2003). Results obtained in this study have shown that climate is an important determining factor in the distribution of C. capitata and C. rosa, with C. cosyra more dependent on the availability of host plants. This is probably because of the more restricted host range of C. cosyra compared with the other two species. Availability of host plants is probably an important factor determining the seasonal phenology of all three species. Home gardens are important breeding grounds and refuges for both C. capitata and C. rosa because of availability of a wide range of fruit throughout the year, which, with a lack of control measures, enables populations of both species to reach high levels. This highlights the need for an area-wide approach (Hendrichs et al. 2007) in the management of mobile, polyphagous, and multivoltine pest species such as C. capitata and C. rosa, with a variety of control strategies targeted in different habitats and hosts in line with host fruit availability. Acknowledgments We acknowledge the technical support from Juanita Liebenberg (Hortgro Science). We thank Noel Williams, Nonto Mfeka, and monitors across South Africa for trap servicing. This research was funded by Citrus Research International (CRI), Hortgro Science, the Technology and Human Resources for Industry Programme (THRIP), and the National Research Foundation (NRF).

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