Ceratitis rosa (Natal fruit fly)

Pictures

Picture	Title	Caption	Copyright
Title Adult Caption Copyright ©Georg Goergen/IITA Insect Museum, Cotonou, Benin	Adult		©Georg Goergen/IITA Insect Museum, Cotonou, Benin

Identity

Preferred Scientific Name

• Ceratitis rosa Karsch

Preferred Common Name

• Natal fruit fly

Other Scientific Names

• Pterandrus rosa (Karsch)

International Common Names

• Spanish: mosca de la fruta de Natal
• French: mouche des fruits de Natal

EPPO code

• CERTRO (Ceratitis rosa)

Summary of Invasiveness

C. rosa is a polyphagous African species. Its known distribution is mainly southern and eastern Africa. It has been introduced to the Mascarene Islands: Mauritius and Réunion. It is considered to be a major pest of a number of commercial fruits, including fruits that are grown in subtropical or more temperate environments. It has similar environmental requirements to Ceratitis capitata except that it can withstand less dry conditions, but it is probably more suited to wetter and/or colder conditions. It should be considered as a potential invasive species in other parts of Africa, outside its current range, and in other parts of the world. The most likely pathway of dispersal and introduction is as larvae in infested fruits with commercial shipments or in the luggage of travellers. C. rosa is of quarantine significance for EPPO, JUNAC and OIRSA.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Diptera
•                         Family: Tephritidae
•                             Genus: Ceratitis
•                                 Species: Ceratitis rosa

Notes on Taxonomy and Nomenclature

C. rosa belongs to subgenus Pterandrus and may alternatively be cited as Ceratitis (Pterandrus) rosa Karsch. Earlier this species comprised fasciventris, but De Meyer (2001) considered both taxa as separate species.

C. rosa belongs to a species complex (Barr et al., 2006), comprising Ceratitis fasciventris, Ceratitis anonae and C. rosa. Male specimens can be readily differentiated by sexual secondary characters of the legs (De Meyer and Freidberg, 2006), but females are difficult to differentiate. Molecular separation also remains difficult or impossible (Barr et al., 2006), although microsatellite polymorphism between C. fasciventris and C. rosa is as comparable as that between these taxa and Ceratitis capitata (Baliraine et al., 2004).

Description

C. rosa, like other Ceratitis spp., has banded wings, and a swollen scutellum which is marked yellow and black. The pattern of grey flecks in the basal wing cells distinguishes Ceratitis spp. from most other genera of tephritids.

Larvae

The larvae of C. rosa have been illustrated by Orian and Moutia (1960). The third instar larvae have been described in detail and illustrated by Carroll (1998).

Adults (after De Meyer and Freidberg, 2006)

Male head: antenna yellow. First flagellomere two to three times as long as pedicel. Arista with short to moderately long rays; ventral rays shorter and sparser than dorsal rays, especially basally. Frons yellow; with short scattered setulae distinctly darker than frons. Frontal setae well-developed. Face yellowish-white. Genal seta and setulae dark, well-developed.

Thorax: postpronotal lobe yellowish-white, without spot, although sometimes darker yellow around postpronotal seta. Scutal pattern: ground colour greyish-brown with orange tinge; with streaks and darker markings but without distinct spots except prescutellar white markings separate, usually with paler area in between. Scapular setae dark. Scutellum yellowish-white, basally usually with two separate dark spots, sometimes less distinct; apically with three separate black spots, extending to basal 0.33. Anepisternum on ventral half darker yellowish-brown; setulae pale.

Legs: yellow except where otherwise noted; setation mainly pale. Foreleg: femur without bushy feathering posteriorly, only dispersed rows of long black setulae posterodorsally, posteroventrally shorter and pale; ventral setae black. Midleg: femur with few dispersed pale setulae ventrally; tibia moderately broadened; anteriorly black with conspicuous silvery shine when viewed from certain angle on distal 0.66 to 0.75 (black colour sometimes inconspicuous in teneral specimens but silvery shine is always present) with black feathering dorsally along distal 0.75 and ventrally along distal 0.66, occasionally to distal 0.75. Hindleg: femur at apical 0.25 with longer setulae dorsally and ventrally.

Wing: bands yellowish-brown. Interruption between marginal and discal bands near vein R₁ clear and complete; cubital band free; medial band absent; crossvein R-M opposite middle of discal cell. Apex of vein R₁ distal to level of crossvein R-M. Crossvein DM-Cu oblique anterobasally.

Abdomen: mostly yellow. Tergites 2 and 4 with pale-grey band on posterior half, anterior margin sometimes with narrowly brownish colour, especially laterally. Tergite 3 with posterior half patchily brownish colour, anterior half yellowish-brown, both parts not clearly demarcated; sometimes more complete brown. Tergite 5 with basal half brownish, sometimes divided medially into two spots.

Female: as the male except as follows: first flagellomere yellowish-orange. Crossvein DM-Cu oblique posterobasally. Anepisternum on ventral part rarely with darker setulae. Legs without feathering; forefemur posteroventrally with pale pilosity, at least in basal part, distally sometimes dark setulae. Oviscape shorter than preabdomen. Aculeus at most six times longer than wide; tip with distinct apical indentation and lateral margin slightly sinuous.

Body length: 4.96 (4.25-5.30) mm; wing length: 5.34 (4.50-5.75) mm

Distribution

C. rosa s.s. is restricted to eastern and southern Africa. Records of C. rosa from central, western or southwestern Africa, refer to Ceratitis fasciventris. Both species have a largely allopatric distribution with only sympatric occurrence in Kenya (De Meyer and Freidberg, 2006). The northernmost limit observed so far is in the Central Highlands of Kenya. The records from Ethiopia, therefore, seem unreliable because all specimens studied by the author from Ethiopia belong to C. fasciventris. However, because the actual specimens on which these records are based could not be observed, and the proximity of Ethiopia to Kenya, these are currently considered as unreliable records that need confirmation. For further discussion of the distribution of C. rosa, refer to De Meyer (2001) and De Meyer and Freidberg (2006). See also UK CAB International (1985) and Smith et al. (1997b).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

C. rosa is originally a species restricted to the African mainland. It was introduced (probably accidentally) to two of the Mascarene Islands in the Indian Ocean: the island of Mauritius (first record dates from 1953) and the island of La Réunion (first record dates from 1955). Both introductions resulted in rapid spread and the species being distributed over large parts of the islands and is the dominant fly in some hosts such as strawberry guava (Normand et al., 2000). Only with the more recent introduction of Bactrocerazonata in La Réunion, the latter is colonizing niches previously used by C. rosa and other Ceratitis species, especially at low altitudes. C.rosa is generally dominant at high altitudes in La Réunion (Duyck et al., 2004).

C.rosa is known from the coastal area in Kenya. Recently the species seem to have been introduced in the Central Highlands of Kenya, probably around 2001 (Copeland and Wharton, 2006). In this region, it shares host plants with the closely related Ceratitisfasciventris.

Introductions

Risk of Introduction

C. rosa is of quarantine significance for EPPO, JUNAC and OIRSA. Although C. rosa has only established adventive populations in Mauritius (since ca. 1953) and Réunion, it has become a more important pest than Ceratitis capitata in Mauritius, suggesting that it could be at least as serious a threat as C. capitata in other areas; C. rosa displaced C. capitata within a few years of its introduction (Orian and Moutia, 1960). The same phenomenon has been observed in Réunion (Normand et al., 2000; Duyck and Quilici, 2002).

Habitat List

Hosts/Species Affected

C. rosa is a polyphagous species. The list of known host plants for C. rosa has been compiled using De Meyer et al. (2002) and by De Meyer (personal communication, Royal Museum for Central Africa, Belgium, 2008). Some specimens are questionable and require confirmation. Full details of specimens on which these records are based, can be found at http://projects.bebif.be/fruitfly/index.html. Transport of any of the host fruits could result in dispersal and distribution, if infested with fruit fly larvae.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

List of Symptoms/Signs

Biology and Ecology

Detailed biological data on C. rosa is lacking, but this species presumably resembles Ceratitis capitata (Smith et al., 1997a) in biology and survival capacity. Predictive ecological niche models (De Meyer et al., 2008) give a similar prediction for C. rosa as for C. capitata, with the latter probably tolerant to a wider range of climatic conditions. Duyck and Quilici (2002) have shown that C. rosa seems to be better adapted to low temperatures than C. capitata, based on a lower larval developmental threshold of 3.1°C (compared to 10.2°C in C. capitata). The immature stages of C. rosa lasted, on average, 18.8 days and 65.7 days at 30 and 15°C, respectively.

Environmental Requirements

Climate types in the environmental requirements table are based upon the present distribution of C. rosa in Africa using Köppen-Geiger subdivisions as indicated in Kottek et al. (2006). De Meyer et al. (2008) give a predictive model that includes some other potential climate classes throughout the world; however, C. rosa does not occur there currently. Its potential range is largely similar to that of C. capitata, except that it withstands less dry environments, but probably is more tolerant of colder and/or wetter environments. Duyck and Quilici (2002) indicated that C. rosa appeared to be better-adapted to low temperatures compared to C. capitata, because it showed a lower larval developmental threshold of 3.1°C (compared to 10.2°C for C. capitata).

Climate

Latitude/Altitude Ranges

Natural enemies

Notes on Natural Enemies

Very little information is available on the natural enemies of C. rosa. Clausen et al. (1965) reared parasitoids from samples taken in Kenya, but all in low numbers. The braconid, Fopius ceratitivorus was described from a.o. C. rosa, from Kenya (Wharton, 1999). Recently, several hymenopteran parasitoids (Psyttalia concolor, Psyttalia cosyrae, Tetrastichus giffardii) were tested in Kenya for their effectiveness in population control of C. rosa, but in most cases usually encapsulation of the eggs was observed (Mohamed et al., 2003; 2006; 2007). Limited survival rate was observed for Fopius arisanus in Réunion (Rousse et al., 2006).

Means of Movement and Dispersal

Natural Dispersal

Adults tend to remain in the area of emergence, flight is rarely more than a few hundred metres.

Accidental introduction

C. rosa is a fruit-infesting species. Eggs are laid within fruits and the larvae develop inside the fruit. When mature, larvae leave the fruits and pupate in the soil. Introduction is usually accidental through transport and import of infested fruits. This can be through commercial shipments or in luggage of individual passengers. Introduction through soil that includes puparia could theoretically be possible, but there are no records or such introductions for this or similar fruit fly species.

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Economic Impact

C. rosa is a polyphagous species attacking a wide variety of unrelated fruits, including several commercial fruits. It can cause severe damage to commercial fruit crops, resulting in heavy losses. It is known to displace other fruit flies such as Ceratitiscapitata and Ceratitiscatoirii and to be predominant over a large range of ecological conditions in some places where it was introduced like the island of La Réunion (Hancock, 1989; Normand et al., 2000; Duyck et al., 2007). This indicates that it can be a serious pest species with high economic impact.

Environmental Impact

Impact on Biodiversity

It has been shown that invasive fruit fly species can be competing with native fruit flies, or with earlier introduced fruit flies, for the same host resources (Duyck et al., 2004, 2007). The introduced C. rosa has, in combination with the equally introduced C. capitata, caused the decline of the indigenous C. catoirii populations on the Mascarene islands of Mauritius and La Réunion (Duyck et al, 2004; Normand et al., 2000).

Threatened Species

Social Impact

Although the impact of C. rosa is mainly economic, it has some social consequences in Africa. Large part of the fruit cultivation in Africa is by small-holder farms (Lux, 1999). Because of the high infestation rate and the consequent loss of production, this has an impact on the income of these farmer communities. It is also anticipated that the loss of fruit crops might have an impact on fruit consumption, hence the health of the local population.

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
• Capable of securing and ingesting a wide range of food
• Benefits from human association (i.e. it is a human commensal)
• Has high reproductive potential

• Conflict
• Host damage
• Negatively impacts agriculture
• Negatively impacts human health
• Negatively impacts livelihoods
• Reduced native biodiversity
• Threat to/ loss of endangered species
• Threat to/ loss of native species

• Causes allergic responses
• Interaction with other invasive species

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally
• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control

Detection and Inspection

C. rosa can be monitored by traps baited with male lures. Like Ceratitis capitata, and members of subgenera Ceratitis and Pterandrus in general, it is attracted to trimedlure and terpinyl acetate, but not methyl eugenol or cue lure. The responses to baits of 16 Ceratitis species were tabulated by Hancock (1987).

Trimedlure (t-butyl 4(or 5) chloro-2-methyl cyclohexane carboxylate) is the most widely used lure for C. capitata and the following information could also be relevant for C. rosa. The history of trimedlure development and the problems of isolating the best of the eight possible isomers was discussed by Cunningham (1989). The lure is usually placed on a cottonwool wick suspended in the middle of a plastic trap that has small openings at both ends. Suitable traps were described by White and Elson-Harris (1994). Lure can either be mixed with an insecticide or a piece of paper dipped in insecticide can be placed in the trap. Traps are usually placed in fruit trees at a height of ca. 2 m above ground and should be emptied regularly as it is possible to catch hundreds of flies in a single trap left for just a few days, although the lure may remain effective for a few weeks.

A detailed study of trap position effects was carried out by Israely et al. (1997). A review of the biological aspects of male lures was presented by Cunningham (1989) and the use of lures was described more fully by Drew (1982). A trapping system used to monitor for possible introductions of C. capitata into New Zealand has been described by Somerfield (1989) and should also be effective for C. rosa. The possibility of the development of pheromone based trapping systems was discussed by Landolt and Heath (1996) and it may be possible to extend that approach to C. rosa. Trapping efficiency of C. capitata is also enhanced by the use of fluorescent colours, particularly light green (Epsky et al., 1996). This may also apply to C. rosa.

Similarities to Other Species/Conditions

The males of most species of subgenus Pterandrus have rows of stout setae on both the anterior and posterior edges of each mid-tibia, giving a feathered appearance. The males lack the spatulate head appendages of subgenus Ceratitis or the shiny frons and spotted abdomen of subgenus Pardalaspis. They can be differentiated from representatives of other subgenera within the genus Ceratitis by the presence of a dark band on the abdomen. C. rosa can be separated from most other members of this subgenus by having the feathering confined to slightly more than the distal half of the tibia and by lacking stout setae on the underside of the mid-femur. The closely related Ceratitis fasciventris has similar feathering on the mid tibia. It can be separated by the fact that in C. fasciventris the feathering is confined to less than the distal half of the tibia. These features are illustrated in De Meyer and Freidberg (2006) who also provide an identification key for both sexes of representatives of the subgenus Pterandrus. Illustrations depicting the main differentiating characters can be consulted at http://projects.bebif.be/fruitfly/index.html.

There is no simple method of recognizing females of C. rosa from C. fasciventris.

Prevention and Control

Very little specific information has been written about the control of C. rosa. Most of the information given here is general information applicable to a large number of fruit fly species. When detected, it is important to gather all fallen and infected host fruits and destroy them. Traps containing male lures should be used to monitor population size and spread continuously (Ramsamy, 1989). Insecticidal protection is possible by using a cover spray or a bait spray (Schwartz, 1993). A bait spray consists of a suitable insecticide (for example, malathion) mixed with a protein bait. Both male and female fruit flies are attracted to protein sources emanating ammonia. Insecticides can therefore be applied to just a few spots in an orchard and the flies will be attracted to these spots. The protein most widely used is hydrolysed protein, but some supplies of this are acid hydrolysed and are highly phytotoxic.

Smith and Nannan (1988) have developed a system using autolysed protein; in Malaysia this has been developed into a very effective commercial product derived from brewery waste (developed for Bactrocera spp.).

Phytosanitary Measures

Consignments of potential host fruits from countries where C. rosa occurs should be inspected for symptoms of infestation and those suspected should be cut open in order to look for larvae. It is recommended that such fruits should come from an area where C. rosa does not occur, or from a place of production found free from the pest by regular inspection for 3 months before harvest. By analogy with C. capitata, fruits may also be treated in transit by cold treatment or, for certain types of fruits, by vapour heat.

Plants of host species transported with roots from countries where C. rosa occurs should be free from soil, or the soil should be treated against puparia. The plants should not carry fruits. The importation of such plants may be prohibited.

Biological Control

Parasitoids for biological control of C. rosa and other fruit flies were introduced in Mauritius in 1939 and 1957 (Greathead, 1971) and in Réunion during the 1960s and 1970s (Greathead, 1971; OPIE, 1986), but none became established.

Gaps in Knowledge/Research Needs

Limited information is available on climatic thresholds, based on rearing experiments. There is some indication that C. rosa can withstand colder temperatures and/or wetter environments than its current distribution would indicate which is important for determining the risk of establishment in new regions.

In order to fully understand the impact of individual polyphagous pest species, a detailed study of interspecific competition and resource partitioning between the different species (both natural and invasive) is needed. Copeland et al. (2006) is an example of such study, which should be repeated in other parts of the geographic range of C. rosa.

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Somerfield KG, 1989. Establishment of fruit fly surveillance trapping in New Zealand. New Zealand Entomologist, No. 12:79-81

UK CAB International, 1985. Pterandrus rosa. [Distribution map]. Distribution Maps of Plant Pests, December. Wallingford, UK: CAB International, Map 153 (Revised).

Wharton RA, 1999. A review of the Old World genus Fopius Wharton (Hymenoptera: Braconidae: Opiinae), with description of two new species reared from fruit-infesting Tephritidae (Diptera). Journal of Hymenoptera Research, 8(1):48-64; 33 ref.

Wharton RA; Gilstrap FE, 1983. Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s.l. (Diptera: Tephritidae). Annals of the Entomological Society of America, 76(4):721-742

White IM; Elson-Harris MM, 1992. Fruit flies of economic significance: their identification and bionomics. Wallingford, UK: CAB International, 601 pp.

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Links to Websites

Organizations

Kenya: International Centre for Insect Physiology and Ecology, P.O. Box 30772-00100, Nairobi, http://www.icipe.org/

Tanzania: Sokoine University of Agriculture, P.O. Box 3000 Chuo Kikuu, Morogoro, http://www.suanet.ac.tz/

Belgium: Royal Museum for Central Africa, Leuvensesteenweg 13, 3080 Tervuren, http://www.africamuseum.be

Contributors

11/12/2007 Updated by:

Marc de Meyer, Department of Entomology, Koninklijk museum voor Midden Afrika, Leuvensesteenweg 13, B-3080 Tervuren, Belgium

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