aphid dispersal flight disseminates fungal pathogens and parasitoids as natural control agents of...

Ecological Entomology (2007), 32, 97–104

© 2007 The AuthorsJournal compilation © 2007 The Royal Entomological Society 97

Introduction

Aphid dispersal by active flight over local vegetation or passive flight with winds for long distances is a well evolved life strategy that aphids rely upon for location of suitable plants ( Dixon & Laird, 1967; Dixon et al. , 1968; Dixon, 1969; Kring, 1972; Robert, 1987 ). This dispersal strategy is of general importance for aphids to complete holocyclic or anholocyclic life by parthe-

nogenesis ( Dixon, 1987a, b ). A large number of biological agents, such as fungal pathogens and parasitoids, play an impor-tant role in the natural control of aphids but the possible role of host dispersal flight in dissemination of those agents has not been recognised until recently.

Aphid-pathogenic fungi, mostly in the Entomophthorales ( Humber, 1989 ), can be strictly obligate to aphids (e.g. Conidiobolus obscurus , Entomophthora planchoniana , Neozygities fresenii , and Pandora neoaphidis ) or infect a wide range of host insects (e.g. Zoophthora radicans , Conidiobolus spp., and some species in hyphomycetes). Although a few species of the obligate pathogens, particularly P. neoaphidis , are

Correspondence: Professor Ming-Guang Feng, Institute of Micro -biol ogy, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, 310029, People’s Republic of China. E-mail: [email protected]

Aphid dispersal fl ight disseminates fungal pathogens and parasitoids as natural control agents of aphids

M I N G - G U A N G F E N G 1 , 2 , C H U N C H E N 1 , 2 , S U - W E I S H A N G 1 , S H E N G - H U A Y I N G 1 , Z H I - C H E N G S H E N 2 and X U E - X I N C H E N 2 1 Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, People’s Republic

of China and 2 Institute of Applied Entomology, College of Agriculture and Biotechnology, Zhejiang University,

Hangzhou, Zhejiang, People’s Republic of China

Abstract . 1. Dispersal flight, a well-known strategy for aphids to locate suitable plants, was studied for its possible role in disseminating fungal pathogens and parasitoids as natural control agents of aphids by air captures in Hangzhou, China during 2001 – 2005. Up to 3183 migratory alates of green peach aphid Myzus persicae were captured from air using a yellow -plus-plant trap on the top platform of a six-storey building in an urbanised area, and individually reared in a laboratory for ³ 7 days.

2. Among the captured alates, 28.9% survived on average for 2.5 days and then died from mycoses attributed to 10 species of obligate or non-obligate aphid pathogens. These were predominated by Pandora neoaphidis , which was causative of 80% of the mycosed alates. Another 4.4% survived for an average of 3.7 days, followed by mummification of Aphidius gifuensis (52.9%) and Diaeretella rapae (47.1%).

3. Numerous progeny colonies individually initiated by infected, parasitised, or healthy alates were monitored daily for 12 days, and fitted well to a logistic equation depicting the potential of their post-flight colonisation and fecundity. Both infected and parasitised alates from air were highly capable of initiating progeny colonies independently, although their potential fecundity was greatly reduced compared with that of healthy counterparts.

4. Our results confirmed that both obligate and non-obligate pathogens can be widespread with aphid dispersal flight, and demonstrated that parasitoids also took advantage of the host flight for their dispersal. This study provides new insights into aphid dispersal biology.

Key words . Aphid dispersal fl ight , Aphididae , Aphidiidae , aphid-pathogenic fungi , Entomophthorales , mycosis transmission , Myzus persicae , parasitoid dispersal , parasitoids .

98 Ming-Guang Feng et al.

© 2007 The AuthorsJournal compilation © 2007 The Royal Entomological Society, Ecological Entomology, 32, 97–104

well known causative of aphid epizootics worldwide ( Feng et al. , 1991 , 1992; MacLeod et al. , 1998; Hatting et al. , 2000; Nielsen et al. , 2001; Plantegenest et al. , 2001; Steinkraus et al. , 2002 ), initiation of their seasonal prevalence in host populations has not been well understood. Due to the presence of resting spores in most of the obligate pathogens ( Humber, 1989; Li, 2000 ), primary infection may rise from resting spores or un-known form of inoculum in soil ( Latteur, 1977; Latteur & Godefroid, 1983; Nielsen et al. , 2003 ). However, no form of resting spores has yet been discovered in P. neoaphidis , which is the most important of the aphid-pathogenic fungi ( Humber, 1989; Feng et al. , 1990; Li, 2000; Shah et al. , 2004 ). Other possible means of spreading fungal infection among aphids include activities of contaminated predators ( Roy et al. , 2001 ) or airborne conidia within the crop canopy ( Hemmati et al. , 2001 ). Recently, some fungal pathogens have been found in the alates of cereal and vegetable aphids separately trapped during a 2-month period ( Feng & Chen, 2002; Chen & Feng, 2004a ). Although P. neoaphidis has been seen to spread with the artifi-cially infected alates of green peach aphid Myzus persicae and English grain aphid Sitobion avenae in simulation flight experi-ments under controlled conditions ( Chen & Feng, 2004b, 2005, 2006a; Feng et al. , 2004 ), data from natural conditions are needed to address if and how fungal pathogens are dispersed by migratory alates of their hosts.

Hymenopteran parasitoids are also important in the natural control of aphids ( Starý, 1988 ), and their multitrophic interac-tions have been studied extensively ( Hufbauer, 2001; Schellhorn et al. , 2002; Snyder & Ives, 2003; Tylianakis et al. , 2004; Bezemer et al. , 2005 ). However, no effort has been made to demonstrate possible dispersal of parasitoids with host flight, although specialists, such as Aphidiidae, are closely associated with aphid hosts. Thus, the potential role of the host dispersal flight in aphid – parasitoid interactions is unknown.

The colour yellow is highly attractive to winged aphids. This tropism has been widely utilised for monitoring aphid popula-tions in the field ( Robert et al. , 1988 ). In the present study, a large number of migratory alates of M. persicae infesting up to 44 families of plants ( Blackman & Eastop, 1984 ) were captured for examination by a yellow-plus-plant trap during 2001 – 2005. The objectives were to identify fungal pathogens and parasi-toids borne by migratory alates, to elucidate whether, why, and how both types of aphid mortality agents spread with host dis-persal flight by modelling the individual performance of cap-tured alates during the early period of post-flight colonisation, and to focus on previously ignored aspects of aphid dispersal biology that could be of merit for understanding mechanisms involved in the interactions of pathogens and parasitoids with aphids and the role of their natural control.

Materials and methods

Trapping of migratory alates from air

A large piece of yellow waterproof cloth (2 × 4 m) was used as a yellow trap to collect migratory alates throughout the cur-rent study. The trap was set up on the central area of the outdoor

roof platform ( ≈ 1500 m 2 ) of a six-storey, open-view building (> 20 m tall) at the centre of Zhejiang University Huajiaci Campus (30°14 ′ N, 120°09 ′ E), Hangzhou, a capital city of Zhejiang Province in eastern China ( Feng & Chen, 2002 ). The campus ( ≈ 85 ha) is located in a highly urbanised area, sur-rounded by streets and buildings for business and residential use, and is 5 – 15 km away from farmland . Within the campus are roads, sport grounds, and buildings standing in grassed and landscaped areas. The local climate is of subtropical monsoon type with an annual mean of 17.8 °C in temperature (monthly mean: 3.8 – 28.6 °C; hottest in July and August and coldest in January), annual mean 70% relative humidity, and mean annual totals of 1047 mm of rainfall and 1875 hours of sunshine.

Placed on the yellow cloth were 20 – 25 potted Chinese cab-bage plants at roughly equal distances. The potted plants were grown in fertilised soil free of aphids and any other insects, and were renewed when necessary. The potted plants were exam-ined every morning, or as soon as possible on the same day if rain did not allow examination. All alates appearing on the plants at each visit time were regarded as migratory alates trapped from air during the previous 24-h period and thus were collected and taken back to the laboratory for further observa-tion. Any nymphs observed on the potted plants at the visit time were destroyed immediately using a wet towel. The trapping began from late October 2001 and terminated in early June 2005. No trapping was made during the hot (June to September) and cold (January to February) months of each year because very few alates were obtained in earlier attempts during these months.

Determination of fungal pathogens and parasitoids in trapped alates

All daily captured alates, ranging from zero to more than 30, were reared individually on detached leaves on 2% agar in Petri dishes (65 mm diameter) at 23 ± 2 °C and LD 12:12 h. The agar plates contained nutrients and 0.1% naphthalene acetic acid for outgrowths of hairy roots into the agar, so that each detached leaf was able to support a colony of the alate and offspring for 2 weeks. In earlier trapping sessions , the alates were reared for 7 days and daily deaths were recorded; the latent period of fungal infection is usually in the range of 3 – 6 days ( Feng & Johnson, 1991; Feng et al. , 1998 ). In the following sessions, the alates were reared for up to 12 days and records of mycosed or mum-mified alates were taken along with monitoring the number of nymphs produced by each trapped alate during the early period of colonisation. Mycosed cadavers were individually mounted on slides and examined microscopically to identify fungal path-ogens, referring to Humber (1989), Feng et al. (1990) , and Li (2000) . Alate mummies were kept individually in glass vials at 23 ± 2 °C and L:D 12:12 h and the emerged wasps were identi-fied by referring to Starý and Schlinger (1967) . Alates mycosed or mummified within 7 days after trapping were considered to have been infected by the fungal pathogens or parasitised by the wasps when they were trapped on the potted plants on the yellow cloth. In other words, their infection or parasitism occurred prior to the capture. Counts of the infected alates were made for each

Dissemination of aphid pathogens and parasitoids 99


fungal pathogen while fewer parasitised counts were pooled be-cause wasp species could not be identified until emergence.

Assessment of post-fl ight potential fecundity of trapped alates

While the trapped alates were individually reared to initiate progeny colonies, the number of nymphs produced per alate was recorded daily. All progeny colonies were classified into three groups: (1) mother alates mycosed within 7 days after trapping (infected), (2) mother alates mummified within 7 days after trapping (parasitised), and (3) mother alates free of fungal infection and parasitism (healthy) because they became neither mycosed nor mummified while being reared. The counts of daily deaths in groups 1 and 2 were used to compute their mean survival durations under the influence of pre-flight infection by each fungal pathogen or parasitism by all wasps. Infected or parasitised alates were considered to have successfully colonised plants if they survived for ³ 1 day or left one or more nymphs before they were killed. For the three groups, post-flight poten-tial fecundity were assessed and compared as below.

Firstly , the increasing trend of the mean size ( N– ; number of aphids per colony) of progeny colonies initiated by the alates of each group over colonisation days ( D ) was fitted to a logistic equation N– = K /[1 – exp( a + rD )], where K was the potential colony size for the concerned group to reach, a an intercept for the fitted trend, and r the rate of daily increase in colony size.

Secondly, fecundity data from each of the groups were fitted to a probability model in the form of a logistic equation ( Chen & Feng, 2006b ). Assume that the trapped alates individually pro-duced m nymphs per capita ( m = 0, 1, 2 ..., N– ) before they be-come mycosed (group 1) or mummified (group 2) or surviving during the same period (group 3). The counts of the alates pro-ducing m nymphs ( n m ) were then made for each group and a sum of those counts was estimated as n = ∑ N0 n m . A cumulative probability [ P ( m £ N )] for each group to produce no more than m nymphs per capita ( m £ N ) was thus computed as P ( m £ N ) = ∑ N 0 p m , where p m = n m / n . Subsequently, the m and P ( m £ N ) relationship was fitted to the logistic equation P ( m £ N ) = K /[1 + exp( � + � m )], where K = 1 due to P ( m £ N ) £ 1, � was an intercept for the fitted curve and r the variability in post-flight

fecundity within each group. The probability of each group of the alates with a specific fecundity ( m nymphs per alate) was then solved to P̂ m = P̂ ( m � N ) – P̂ [ m � ( N – 1)] based on the fitted model. The homogeneity between the counts of the alates ( n m ) observed to have a specific fecundity and the fitted counts ( n̂ m = np̂ m ) was examined based on likelihood-ratio G -test. All statistic and modelling analyses were performed using DPS software ( Tang & Feng, 2002 ).

Results

Fungal pathogens and parasitoids in air captures

From late October 2001 to early June 2005, 3183 alates of M. persicae were collected from the yellow-plus-plant trap and reared individually ( Table 1). There was no failure to obtain air captures despite a large difference in quantity from one trapping season to another. Of those, 28.9% ( n = 921) were infected by fungal pathogens and 4.4% ( n = 106) parasitised by wasps.

Fungal pathogens observed in the trapped alates and their relative frequencies are listed in Table 2. In total, 921 alates were mycosed within 7 days after trapping but only a very few survived for more than 5 days. Up to 97.7% of the infected alates were attributed to the Entomophthorales, including five species of obligate aphid pathogens, i.e. P. neoaphidis , C. obscurus , E. planchonian , N. fresenii , and Zoophthora anhuiensis . The last fungal species is recorded only in China ( Li, 2000 ). Noticeably, P. neoaphidis formed the majority (81.9%) of those infected by entomophthoralean fungi and also appeared in a few cross-infected alates. Other fungal pathogens were occasionally found in the trapped alates, including three Entomophthorales ( Conidiobolus coronatus , Conidiobolus thromboides , and Z. radicans ) and two hyphomycetes ( Beauveria bassiana and Lecanicillium lecanii ), but they were non-obligate to aphids. On average, all infected alates survived for 2.49 days despite varia-tion among the involved fungal pathogens. This survival period was shorter than those known for the latent period of entomoph-thoralean infection ( Feng & Johnson, 1991; Feng et al. , 1998 ), indicating that the alates became infected before they were trapped from air.

Table 1. Counts and proportions of migratory alates infected by fungal pathogens or parasitised by wasps in air captures in Hangzhou, Zhejiang, China during 2001 – 2005.

Trapping period No. of alates trapped

Pathogen-infected alates Wasp-parasitised alates

Counts % Counts %

October – December 2001 760 266 35.00 Ignored October – December 2002 310 130 41.94 11 3.55 February – June 2003 1081 229 21.18 45 4.16 November – December 2003 72 16 22.22 1 1.39 February – May 2004 107 23 21.50 6 5.61 October – December 2004 760 227 29.87 30 3.95 May – June 2005 93 30 32.26 13 13.98 Overall 3183 921 28.93 106 4.37 *

* An estimate excluding the number of alates trapped during the fi rst period.



Surprisingly, 106 alate mummies were obtained from the air captures after the first trapping season ( Table 2 ). Primary parasi-toids that emerged were sorted into two species: Aphidius gifuensis (52.9%) and Diaeretella rapae (47.1%). Both wasps attack a wide range of host aphids throughout the world ( Starý & Schlinger, 1967 ). The parasitised alates survived on average for 3.75 days, a period significantly longer than that of the infected alates (Student’s t 1025 = 10.12, P < 0.0001).

Development of progeny colonies

The observed and fitted trends in the mean sizes of the prog-eny colonies of the three groups over days after capture are il-lustrated in Fig. 1. The observations were obtained daily by monitoring all progeny colonies initiated individually by the trapped alates in group 1 ( n = 473; infected), group 2 ( n = 86; parasitised), and group 3 ( n = 381; healthy) during the 12-day period of colonisation. Overall mean (± SEM) size of the prog-eny colonies in group 3 was estimated as 2.0 ± 0.10 nymphs per colony on day 1, 6.2 ± 0.18 on day 3, and 11.6 ± 0.33 on day 6. These estimates were significantly larger than those in groups 1 ( t 852 = 9.23, 20.60, and 25.92 for days 1, 3, and 6 respectively, P < 0.0001) and 2 ( t 465 = 3.64, 10.12, and 18.32 for days 1, 3, and 6 respectively, P � 0.0003). Moreover, the colonies in group 1 were significantly smaller than those in group 2 on days 2 – 4 after colonisation (day 1: t 557 = 1.58, P = 0.114; day 2: t 557 = 2.00, P = 0.048; day 3: t 557 = 2.14, P = 0.034; day 4: t 557 = 2.36, P = 0.020; day 5: t 557 = 2.32, P = 0.022; day 6: t 557 = 1.93, P = 0.054). Overall mean sizes of groups 1 and 2 on day 6 were 2.4 ± 0.11 and 3.1 ± 0.33 nymphs per colony respectively. From then on, the increases of the progeny colony sizes in all groups were accelerated due to recruitment of new adults that devel-oped from the early born nymphs (as pointed out by the arrow in Fig. 1 ) at the controlled temperature ( Liu, 1991 ). On day 12, groups 1 – 3 had the mean sizes of 21.5 ± 0.99, 37.1 ± 4.0, and

50.6 ± 1.93 individuals per colony respectively. The colony in-creasing trends over colonisation days were fitted very well to the logistic equation with high coefficients of determination ( r 2 � 0.986) for all three groups. The potential mean sizes of the colonies (the estimates of the parameter K ) achieved during the 12-day period were fitted as 25.7 individuals per capita for group 1, 38.6 for group 2, and 92.8 for group 3 respectively. These indicate that the infected and parasitised alates from air

Table 2. Post-fl ight survival of air-trapped migratory alates infected by different species of fungal pathogens or parasitised by wasps.

Number of alates mycosed or mummifi ed over days post-fl ight No. of Survival days

Fungal pathogens or parasitoids Day 1 Day 2 Day 3 Day 4 Day 5 Day 6 Day 7 alate cadavers obtained

after trapping (mean ± SD)

Pandora neoaphidis 153 301 174 61 36 8 4 737 2.41 ± 1.16 Conidiobolus spp. * 8 30 17 14 6 1 0 76 2.76 ± 1.15 Entomophthora planchoniana 2 9 9 1 5 0 0 26 2.92 ± 1.23 Zoophthora spp. † 9 8 10 4 3 0 0 34 2.53 ± 1.26 Neozygities fresenii 2 1 1 2 0 0 0 6 2.50 ± 1.38 Cross-infected ‡ 4 5 6 6 0 0 0 21 2.67 ± 1.11 Beauveria bassiana 0 4 9 7 0 0 0 18 3.17 ± 0.79 Lecanicillium lecanii 1 1 0 0 1 0 0 3 2.67 ± 2.08 Total infected 179 359 219 100 51 9 4 921 2.49 ± 1.18 Parasitoids § 5 15 35 17 16 17 1 106 3.75 ± 1.47

* Including mainly Conidiobolus obscurus and occasionally Conidiobolus thromboides and Conidiobolus coronatus. † Including mainly Zoophthora anhuiensis and occasionally Zoophthora radicans. ‡ Cross-infected by Pandora neoaphidis with one of the other entomophthoralean species . § Pooled counts for Aphidius gifuensis and Diaeretella rapae .

Fig. 1. Mean sizes of progeny colonies (number of aphids per colony; N–

) individually initiated by air-trapped migratory alates over days after colonisation ( D ). �, Observations from infected alates ( n = 473) and the fi t to N

– = 25.677/[1 + exp(5.8980 – 0.6388 D )] ( r 2 = 0.986, F 2,9 = 317,

P < 0.001). � , Observations from parasitised alates ( n = 86) and the fi t to N–

= 38.567/[1 + exp(8.0475 – 0.9342 D )] ( r 2 = 0.989, F 2,9 = 397.5, P < 0.001). � , Observations from healthy alates ( n = 381) and the fi t to N

– = 92.757/[1 + exp(3.8821 – 0.3418 D )] ( r 2 = 0.996, F 2,9 = 1145,

P < 0.001). The inset graph illustrates differences of the observations among the groups within the fi rst 7 days. The arrow indicates the time at which the early born nymphs became adults and started reproduction. Error bars for observations: SEM.



were capable of initiating progeny colonies independently, although their colony increase potential was largely reduced compared with that of healthy counterparts.

The effect of post-flight survival time on the fecundity of both infected and parasitised alates is plotted in Fig. 2. Generally, more nymphs were produced by those surviving longer. After they be-came mycosed or mummified, no more nymphs were recruited to their colonies until the early born nymphs developed into adults. In some colonies, initiated by the infected alates, nymphs became mycosed because of transmission of fungal infection within the colonies. During the 12-day period, 13.2% of the colonies whose mother alates died from P. neoaphidis suffered from secondary infection, which further caused tertiary infection in one-third of the secondarily infected colonies ( Table 3). This is a reason for the smaller sizes of the progeny colonies initiated by the infected alates than those initiated by the parasitised alates.

Modelling of post-fl ight fecundity probability

The counts of the nymphs individually produced by the in-fected (group 1) or parasitised (group 2) alates prior to mycosis

or mummification or by the healthy ones (group 3) during the same period differed largely within each group or from one group to another. Alates in groups 1, 2, and 3 produced 0 – 19, 0 – 12, and 0 – 40 nymphs per capita respectively. Within- or between-group variations of the counts were well quantified by the cumulative probability [ P ( m £ N )] for no more than a certain number of nymphs per alate ( m ), as shown in Fig. 3. Based on the fitted relationships between m and P ( m £ N ), the healthy alates trapped from air were highly capable of producing more nymphs than those infected or parasitised. For instance, the fit-ted (vs. observed) probabilities for producing ³ 10 nymphs per alate were 0.013 (0.015) in group 1, 0.035 (0.012) in group 2, and 0.538 (0.496) in group 3 respectively. In contrast, the prob-ability of the alates producing no nymphs was up to 0.369 (0.378) in group 1 and 0.298 (0.314) in group 2, although they survived for ³ 1 day. The infected and parasitised alates had high probabilities of producing only a few nymphs, e.g. 0.716 and 0.597 for £ 3; 0.870 and 0.773 for £ 5.

The fitted cumulative probabilities for the trapped alates with a variable range of fecundity gave an exact solution to the prob-ability of each group with a specific fecundity ( p m ). The fitted counts for the three groups in terms of their specific probabili-ties coincided very well with those observed ( Fig. 4; P ³ 0.063 in the likelihood-ratio G -tests).

Discussion

The above results highlight the significant role of aphid disper-sal flight in disseminating both pathogens and parasitoids in host populations across vegetation or geographic areas. Most of the fungal species carried by the alates fell within the

Fig. 2. The impact of survival duration of migratory alates [(a) in-fected, (b) parasitised] on the sizes of their progeny colonies during the early period of colonisation. Error bars: SEM.

Fig. 3. Cumulative probabilities ( P ( m £ N ) of migratory alates produc-ing m nymphs per capita within 6 colonisation days. � , Observed trend of 473 infected alates and the fi t to the bold solid curve P ( m £ N ) = 1/[1 – exp(0.538 – 0.448 m )] ( r 2 = 0.9994, F 1,15 = 23221, P < 0.0001). � , Observations from 86 parasitised alates and the fi tted solid curve P ( m £ N ) = 1/[1 – exp(0.858 – 0.417 m )] ( r 2 = 0.9919, F 1,10 = 1220, P < 0.0001). � , Observations from 381 healthy alates and the fi tted dashed curve P ( m £ N ) = 1/[1 – exp(2.903 – 0.275 m )] ( r 2 = 0.9938, F 1,32 = 5107, P < 0.0001). All fi tted parameters are signifi cant in t -tests ( P < 0.0001).



Entomophthorales, being obligate or non-obligate to aphids, and all may form resting spores, except P. neoaphidis , which was seen most frequently in the captures. Two entomopathogenic hyphomycetes, B. bassiana and L. lecanii , also appeared in the captures at a low frequency, as seen in the alates of vegetable and cereal aphids trapped in Yunnan, south-west China ( Feng et al. , 2004 ). Over 4% of the trapped alates were parasitised by the two wasp species, A. gifuensis and D. rapae . Moreover, the fecundity of the infected and parasitised alates was sufficient to initiate progeny colonies independently. Biological effects of aphid dispersal flight on the host – pathogen or host – parasitoid interactions are discussed below.

Firstly, a reasonable interpretation of seasonal prevalence of obligate pathogens that cause aphid epizootics has been rarely satisfactory despite previous attempts based on a large amount of field work ( Feng et al. , 1991 , 1992; MacLeod et al. , 1998; Hatting et al. , 2000; Nielsen et al. , 2001; Plantegenest et al. , 2001; Steinkraus et al. , 2002 ). Since infected alates have been shown experimentally to be able to actively fly, by wing vibra-tion, for 0.1 – 10 km in 1 – 5 h in a flight mill system ( Chen & Feng, 2004b, 2005, 2006a; Feng et al. , 2004 ) and to produce suf-ficient progeny for colonisation in this study, the conclusion can be drawn that the fungal pathogens are primarily disseminated in host populations with their host flight dispersal for locating suit-able plants. Based on documented records of the vast potential of aphid dispersal flight ( Dixon et al. , 1968; Kring, 1972; Robert, 1987 ), normal seasonal patterns of weather and cropping systems, and inseparable aphid – pathogen interactions ( Humber, 1989 ), the seasonal prevalence of aphid epizootics, attributed to the very

few obligate pathogens in the world, can become understood. Primary infection of aphids by the predominating P. neoaphidis , or other less prevalent pathogens in the field, start from landing of healthy and infected immigrants on plants. At that point, my-cosis develops by contagious infection within or between host colonies as the host population increases. The activities of con-taminated predators ( Roy et al. , 2001 ) or airborne conidia within crop canopy ( Hemmati et al. , 2001 ) may augment local trans-mission, particularly in infected populations, but their roles would be secondary. Soil-borne inoculum could be another source of aphid infection by the fungal pathogens that possess resting spores ( Latteur, 1977; Latteur & Godefroid, 1983 ) but this needs more direct supporting evidence. However, fungal pathogens with resting spores can also be associated with the host flight because they appear in air captures and do not neces-sarily overwinter as resting spores in soil, as seen in E. plancho-niana ( Wilding, 1973; Keller, 1987 ) and N. fresenii ( Vingaard et al. , 2003 ). Whether the mycosis develops into an epizootic that controls or collapses the host population depends largely on environmental suitability ( Feng & Li, 2003 ), and this happens to be most concerned in previous field studies. When the aphid den-sity is high or the plants grow old, alate emigrants fly for disper-sal and simultaneously carry fungal infections to elsewhere.

Secondly, parasitoids were found to be dispersed with aphid flight for the first time. This may help to explain why no association between mtDNA haplotypes of D. rapae and host aphid species was found in its ancestral or introduced ranges ( Baer et al. , 2004 ) and why genetic variation were not detected in the same wasp species ( Baker et al. , 2003 ). The lack of

Table 3. Transmission of fungal ( Pandora neoaphidis ) infection in the progeny colonies of the infected mother alates after they died from mycosis.

Infection mode *

Number of progeny colonies infected over days

Total 1 2 3 4 5 6 7 8 9 10 11 12

Primary 76 162 89 38 16 3 1 385 Secondary 4 7 5 13 2 4 2 7 4 3 51 Tertiary 1 5 0 0 3 4 4 17

* The infection of the trapped alates in places where they emigrated was primary. The infection of aphids in the same colonies whose mothers or sisters were mycosed at least 2 days earlier was considered secondary or tertiary.

Fig. 4. Likelihood-ratio G -test for the heteroge-neity (present if P < 0.05) between the observed ( n m : open bars) and fi tted ( n̂ m = np̂ m : fi lled bars) counts of air-trapped migratory alates produc -ing m nymphs per capita within 6 days after colonisation.



D. rapae host races probably relates to the flight dispersal po-tential of its hosts. If the dispersal of parasitoids with aphid flight was a general phenomenon, it could have a profound in-fluence on their distribution, coevolution, and interactions with host aphids. Unfortunately, this possible influence has not been recognised in previous studies on aphid – parasitoid interactions ( Hufbauer, 2001; Schellhorn et al. , 2002; Snyder & Ives, 2003; Tylianakis et al. , 2004; Bezemer et al. , 2005 ). Because only a limited number of parasitised alates from air captures were ob-tained in this study, it is not possible to make any conclusion at this time. However, this study has shed light upon the possible impact of host dispersal flight on biological aspects of parasitoids as aphid mortality agents, warranting more studies in the future.

Finally, the results presented in this study suggest a new ap-proach to the survey of aphid pathogens and parasitoids in a geo-graphic region, i.e. using the yellow-plus-plant trap to capture migratory alates and rearing them for a period of time. This type of survey is suitable for either specialists or opportunists such as Conidiobolus spp. Accumulated data would greatly increase knowledge about the significant role of host dispersal flight in natural dispersal of aphid pathogens and parasitoids. It is thus proposed that dispersal flight not only enables aphids to disperse themselves to suitable plants, but this dispersal is also utilised by aphid pathogens and parasitoids to readily locate hosts for attack, which in turn regulates host populations for longer maintenance in situ . Therefore, aphid dispersal biology merits attention in fu-ture studies of aphid – pathogen or aphid – parasitoid interactions.

Acknowledgements

We thank Qi-Yi Tang (College of Agriculture and Biotechnology, Zhejiang University, China) for helping with data analysis and modelling. Funding for this study was provided by the Natural Science Foundation of China (30070514), the National ‘Program 973’ of the Ministry of Science and Technology of China (2003CB114203), and the Innovation Research Team Program of the Ministry of Education of China (IRT0535).

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Accepted 5 October 2006

aphid dispersal flight disseminates fungal pathogens and parasitoids as natural control agents of...

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