Tải bản đầy đủ - 0 (trang)
2 The Origin of Mealybug Pest Status

2 The Origin of Mealybug Pest Status

Tải bản đầy đủ - 0trang


These were subdivided by Franco et al. (2004)

as follows:

1. Recent invasion by exotic mealybug species

(a) Lack of control by natural enemies

2. Application of non-selective pesticides

(a) Mortality differences between pests and

their natural enemies

(b) Indirect effects of pesticides on natural

enemies, for example, elimination of their


(c) Effects on predator and parasitoid host


(d) Trophobiosis – positive indirect effects of

pesticides on pests, mediated through

changes in the host plant

(e) Hormoligosis – positive direct effects of

pesticides on pests

(f) Effects of pesticides on insect behavior

(g) Effects of pesticides on interspecific competition among phytophagous species of

different taxa

3. Effect of environmental factors (tritrophic interactions: host-plant/mealybug/natural enemy)

(a) Host-plant susceptibility and/or hostplant characteristics

(b) Water stress

(c) Nitrogen fertilization

(d) Weather

(e) Mealybug defences, for example,


(f) Mealybug refuges from natural enemies

• Spatial refuge (cryptic behavior), for

example, under the bark and on roots

• Temporal refuge: ant interactions

• Other factors that may affect natural enemies, for example, intraguild predation

and interference, hyperparasitoids

Cause 1 is well documented with regard to

mealybug outbreaks and is mainly driven by the

combination of host susceptibility and absence of

natural enemies in the invaded region (Ben-Dov

1994; Blumberg et al. 1999; Muniappan et al.

2006; Nakahira and Arakawa 2006; Roltsch et al.

2006; Williams and Granara de Willink 1992).

The use of non-selective pesticides (Cause 2)

may lead to resurgence and secondary outbreaks.

M. Mani and C. Shivaraju

The mechanisms involved in these two types of

outbreaks were discussed by Hardin et al. (1995),

and studied by Franco et al. (2004) with regard to

the mealybug pests of citrus. Environmental factors (Cause 3) may also directly and indirectly

affect the tritrophic interactions that develop

between mealybugs, their host plants and their

natural enemies, thereby initiating mealybug outbreaks. Several mechanisms may be involved.

Host-plant characteristics may favour or be detrimental to the development, reproduction and survival of mealybugs (Boavida and Neuenschwander

1995; Calatayud et al. 1994b; Leru and Tertuliano

1993; Nassar 2007; Tertuliano et al. 1993;

Wysoki et al. 1977; Yang and Sadof 1995). The

resistance mechanisms of the host plant may

become involved in both the fixation (antixenosis) and the development of the mealybug (antibiosis) (Tertuliano et al. 1993). Tertuliano and

Leru (1992) concluded that the different levels of

resistance to the cassava mealybug, P. manhioti,

which were observed in different varieties of cassava, were not associated with the concentrations

of amino acids or sugars, with the ratios between

these concentrations, or with the compositions of

amino acids obtained from leaf extracts. The

identification and assay of cyanogenic and phenolic compounds in the phloem sap of cassava

and the honeydew of the cassava mealybug were

carried out by Calatayud et al. (1994a). Yang and

Sadof (1995) showed that variegation in Coleus

blumei could increase the abundance of the citrus

mealybug, P. citri. Sadof et al. (2003) found that

the life-history characteristics of P. citri on

Coleus blumei were not correlated with total

amino acids and sucrose contents in stem exudates, but were correlated negatively with the

proportions of shikimic acid precursors and positively with those of other nonessential amino

acids. Host-plant characteristics can also influence the performance of the natural enemies of

mealybugs (Serrano and Lapointe 2002; Souissi

and Leru 1997; Yang and Sadof 1997). Waterstressed plants may favour the population

increases of mealybugs (Calatayud et al. 2002;

Gutierrez et al. 1993; Lunderstadt 1998).

Mealybug life-history parameters/damage

may also be influenced by the levels of nitrogen



fertilization and leaf nitrogen concentration; high

nitrogen concentrations were shown to lead to

enhanced performance of the citrus mealybug, P.

citri (Hogendorp et al. 2006). The antibiotic

resistance of two varieties of cassava mealybug

increased with the addition of nitrogen (Leru

et al. 1994). Survival of immature sugarcane

mealybugs, S. sacchari, increased to a maximum

at a soluble nitrogen concentration of 320 mg L−1

in sugarcane, and decreased at higher levels,

whereas mealybug size increased with increasing

nitrogen concentration over the whole tested

range (Rae and Jones 1992). Weather conditions,

especially temperature and relative humidity, are

major ecological factors that affect both mealybugs and their natural enemies (Chong and

Oetting 2007; Gutierrez et al. 1993, 2008a;

Nakahira and Arakawa 2006). Encapsulation

may adversely affect the degree of biological

control exerted by mealybug parasitoids, as it

may either prevent the establishment of exotic

parasitoids in new regions or reduce parasitoid

efficacy (Blumberg 1997). The cryptic behavior

and tending of mealybugs by ants may, respectively, originate spatial and temporal refuges

from natural enemies. Several other factors may

affect mealybugs’ natural enemies, which include

intraguild predation and interference (Chong and

Oetting 2007), and hyperparasitoids (Moore and

Cross 1992).


Baumann P (2005) Biology of bacteriocyte-associated

endosymbionts of plant sap-sucking insects. Annu

Rev Microbiol 59:155–189

Ben-Dov Y (1994) A systematic catalogue of the mealybugs of the world (Insecta: Homptera: Coccoidea:

Pseudoccocidae and Putoidae) with data on their geographical distribution, host plants, biology and economic importance. Intercept, Andover

Ben-Dov Y (2006) Scales in a family/genus query.

Available at http://www.sel.barc.usda.gov/scalecgi/

chklist.exe?Family=Pseudococcidae&genus .

Accessed 14 Aug 2008

Blumberg D (1997) Parasitoid encapsulation as a defense

mechanism in the Coccoidea (Homoptera) and its

importance in biological control. Biol Control



Blumberg D, Ben-Dov Y, Mendel Z (1999) The citriculus

mealybug, Pseudococcus cryptus Hempel, and its

natural enemies in Israel: history and present situation.

Entomologica Bari 33:233–242

Boavida C, Neuenschwander P (1995) Influence of host–

plant on the mango mealybug, Rastrococcus invadens.

Entomol Exp Appl 76:179–188

Calatayud PA, Rahbe Y, Delobel B, Khuonghuu F,

Tertuliano M, Leru B (1994a) Influence of secondary

compounds in the phloem sap of cassava on expression of antibiosis towards the mealybug Phenacoccus

manihoti. Entomol Exp Appl 72:47–57

Calatayud PA, Tertuliano M, Leru B (1994b) Seasonal

changes in secondary compounds in the phloem sap of

cassava in relation to plant genotype and infestation by

Phenacoccus manihoti (Homoptera, Pseudococcidae).

Bull Entomol Res 84:453–459

Calatayud PA, Polania MA, Seligmann CD, Bellotti AC

(2002) Influence of water-stressed cassava on

Phenacoccus herreni and three associated parasitoids.

Entomol Exp Appl 102:163–175

Chong JH, Oetting RD (2007) Intraguild predation and

interference by the mealybug predator Cryptolalemus

montrouzieri on the parasitoid Leptomastix dactylopii.

Biocontrol Sci Tech 17:933–944

Franco JC, Silva EB, Carvalho JP (2000) Mealybugs

(Hemiptera, Pseudococcidae) associated with citrus in

Portugal. ISA Press, Lisbon (in Portuguese)

Franco JC, Suma P, da Silva EB, Blumberg D, Mendel Z

(2004) Management strategies of mealybug pests of

citrus in Mediterranean countries. Phytoparasitica


Gullan PC, Kosztarab M (1997) Adaptations in scale

insects. Annu Rev Entomol 42:23–50

Gullan P, Martin JH (2003) Sternorrhyncha (jumping

plant lice, whiteflies, aphids, and scale insects). In:

Resh VH, Cardé RT (eds) Encyclopedia of insects.

Academic, Amsterdam

Gutierrez AP, Neuenschwander P, Vanalphen JJM (1993)

Factors affecting biological control of cassava mealybug by exotic parasitoids – a ratio-dependent supplydemand driven model. J Appl Ecol 30:706–721

Hardin MR, Benrey B, Coll M, Lamp WO, Roderick GK,

Barbosa P (1995) Arthropod pest resurgence: an overview of potential mechanisms. Crop Prot 14:3–18

Hogendorp BK, Cloyd RA, Swiader JM (2006) Effect of

nitrogen fertility on reproduction and development of

citrus mealybug, Planococcus citri Risso (Homoptera:

Pseudococcidae), feeding on two colors of coleus,

Solenostemon scutellarioides L. Codd. Environ

Entomol 35:201–211

Kim KC (1993) Insect pests and evolution. In: Kim KC,

McPheron BA (eds) Evolution of insect pests: patterns

of variation. Wiley, New York

Kono M, Koga R, Shimada M, Fukatsu T (2008) Infection

dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs.

Appl Environ Microbiol 74:4175–4184


Kosztarab M, Kozár F (1988) Scale insects of Central

Europe. Dr. W. Junk Publishers, Dordrecht

Leru B, Tertuliano M (1993) Tolerance of different hostplants to the cassava mealybug Phenacoccus manihoti

Matile-Ferrero (Homoptera, Pseudococcidae). Int

J Pest Manag 39:379–384

Leru B, Diangana J, Beringar N (1994) Effects of nitrogen

and calcium on the level of resistance of cassava to the

mealybug P manihoti. Insect Sci Appl 51:87–96

Lunderstadt J (1998) Impact of external factors on the

population dynamics of beech scale (Cryptococcus

fagisuga) (Hom., Pseudococcidae) in beech (Fagus

sylvatica) stands during the latency stage. J Appl

Entomol/Zeits Angew Entomol 122:319–322

Mittler TE, Douglas AE (2003) Honeydew. In: Resh VH,

Cardé RT (eds) Encyclopedia of insects. Academic,


Moore D, Cross AE (1992) Competition between two primary parasitoids, Gyranusoidea tebygi Noyes and

Anagyrus mangicola Noyes, attacking the mealybug

Rastrococcus invadens Williams and the influence of a

hyperparasitoid Chartocerus hyalipennis Hayat.

Biocontrol Sci Technol 2:225–234

Muniappan R, Meyerdirk DE, Sengebau FM, Berringer

DD, Reddy GVP (2006) Classical biological control

of the papaya mealybug, Paracoccus marginatus

(Hemiptera: Pseudococcidae) in the Republic of

Palau. Fla Entomol 89:212–217

Nakahira K, Arakawa R (2006) Development and reproduction of an exotic pest mealybug, Phenacoccus

solani (Homoptera: Pseudococcidae) at three constant

temperatures. Appl Entomol Zool 41:573–575

Nassar NMA (2007) Cassava genetic resources and their

utilization for breeding of the crop. Genet Mol Res


Rae DJ, Jones RE (1992) Influence of host nitrogen levels

on development, survival, size and populationdynamics of sugarcane mealybug, Saccharicoccus

sacchari (Cockerell) (Hemiptera, Pseudococcidae).

Aust J Zool 40:327–342

Roltsch WJ, Meyerdirk DE, Warkentin R, Andress ER,

Carrera K (2006) Classical biological control of the pink

hibiscus mealybug, Maconellicoccus hirsutus (Green) in

southern California. Biol Control 37:155–166

Sadof CS, Neal JJ, Cloyd RA (2003) Effect of variegation

on stem exudates of coleus and life history characteristics of citrus mealybug (Hemiptera: Pseudococcidae).

Environ Entomol 32:463–469

Serrano MS, Lapointe SL (2002) Evaluation of host plants

and a meridic diet for rearing Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) and its parasitoid

Anagyrus kamali (Hymenoptera: Encyrtidae). Fla

Entomol 85:417–425

M. Mani and C. Shivaraju

Silva EB, Mexia A (1999) Histological studies on the stylet pathway, feeding sites and nature of feeding damage by Planococcus citri (Risso) (Homoptera:

Pseudococcidae) in sweet orange. Entomol Bari


Souissi R, Leru B (1997) Effect of host plants on fecundity and development of Apoanagyrus lopezi, an endoparasitoid of the cassava mealybug Phenacoccus

manihoti. Entomol Exp Appl 82:235–238

Terra WR, Ferreira C (2003) Digestive system. In: Resh

VH, Cardé RT (eds) Encyclopedia of insects.

Academic, Amsterdam

Tertuliano M, Leru B (1992) Interaction between cassava

mealybugs (Phenacoccus manihoti) and their host

plants – amino-acid and sugar contents of sap. Entomol

Exp Appl 64:1–9

Tertuliano M, Dossougbete S, Leru B (1993) Antixenotic

and antibiotic components of resistance to the cassava

mealybug Phenacoccus manihoti (Homoptera,

Pseudococcidae) in various hostplants. Insect Sci Appl


Thao ML, Gullan PJ, Baumann P (2002) Secondary

(gamma-proteobacteria) endosymbionts infect the primary (beta-proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts.

Appl Environ Microbiol 68:3190–3197

Tobih FO, Omoloye AA, Ivbijaro MF, Enobakhare DA

(2002) Effects if field infestation by Rastrococcus

invadens Williams (Hemiptera; Pseudococcidae) on

the morphology and nutritional status of mango fruits

Mangifera indica. Crop Prot 21:751–761

Tonkyn DW, Whitcomb RF (1987) Feeding strategies and

the guild concept among vascular feeding insects and

microorganisms. In: Harris KF (ed) Current topics in

vector research, vol 4. Springer, New York

von Dohlen CD, Kohler S, Alsop ST, McManus WR

(2001) Mealybug beta-proteobacterial endosymbionts

contain gamma-proteobacterial symbionts. Nature


Williams DJ, Granara de Willink MC (1992) Mealybugs

of Central and South America. CABI, Wallingford

Wysoki M, Izhar Y, Swirski E, Gurevitz E, Greenberg S

(1977) Susceptibility of avocado varieties to longtailed mealybug, Pseudococcus longispinus (Targioni

Tozzetti) (Homoptera- Pseudococcidae), and a survey

of its host plants in Israel. Phytoparasitica 5:140–148

Yang JS, Sadof CS (1995) Variegation in Coleus blumei

and the life history of citrus mealybug (Homoptera:

Pseudococcidae). Environ Entomol 24:1650–1655

Yang JS, Sadof CS (1997) Variation in the life history of

the citrus mealybug parasitoid Leptomastix dactylopii

(Hymenoptera: Encyrtidae) on three varieties of

Coleus blumei. Environ Entomol 26:978–982

Mealybugs as Vectors


R. Selvarajan, V. Balasubramanian,

and B. Padmanaban

Mealybugs are well-known sap-sucking insects

which transmit plant viruses. They are omnipresent, polyphagous, can cause more damage as

pests and are less uncommon as virus vectors.

The feeding behavior of these vectors has profound ecological and evolutionary implications

for the viruses they transmit, as the acquisition

and inoculation of viruses occurs during vector

feeding. In most cases, there is an intimate relationship between the virus and its vector, and no

transmissions occur without the insects feeding

in a specific manner. This feeding behavior often

causes considerable economic loss to agriculture

through direct damage to crops and via virus

transmission (Golino et al. 2002; Miiler et al.

2002). They are considered pests as they feed on

the plant juices of economically important crop

plants, and also act as vectors for several plant

viral diseases. The transmission of the plant virus

species belonging to Caulimoviridae and

Closteroviridae by different species of mealybugs is furnished in detail in this chapter.

R. Selvarajan (*) • V. Balasubramanian

National Research Centre for Banana,

Tiruchirapalli 620 102, India

e-mail: selvarajanr@gmail.com

B. Padmanaban

ICAR-National Research Centre for Banana,

Tiruchirappalli 620 102, India


Feeding Behaviour

of Mealybugs

Mealybugs are found in moist and warm climates. They are less mobile on plants than other

groups of vectors, such as aphids and leaf hoppers, a feature that makes them relatively inefficient as virus vectors. They spread from one plant

to another when in contact with them, and crawling nymphs move more readily than adults. Adult

females can be extremely polyphagous and feed

by sucking on plant sap. The stylet pathway to

the phloem is intercellular and contains several

intracellular punctures (Calatayud et al. 1994).

These bugs have less control over fine stylet

movements than aphids and produce fewer

(8–20/h) and longer intracellular punctures (20 s)

along the entire route to the phloem (Calatayud

et al. 1994; Cid and Fereres 2010). Mealybugs

rarely produce brief probes; they often reach the

phloem after a single probe, and it takes a relatively long time to reach the phloem. Some mealy

bugs are unable to tap into the phloem sieve elements even after a period of 20 h, but most are

able to reach the phloem in 1–6 h (Calatayud

et al. 1994; Cid and Fereres 2010). Mealybug stylets are exceedingly long and are coiled within

their body when they are not feeding.

This unique morphology of their mouth may

explain the propensity of mealybugs to make a

single stylet insertion and their inability to reach

the phloem quickly, as is seen with other

hemipterans. Once in the phloem, the mealybugs

© Springer India 2016

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural

and Horticultural crops, DOI 10.1007/978-81-322-2677-2_10


R. Selvarajan et al.


may continue to feed from the same sieve tube

for several days. Xylem ingestion is also a predominant feeding behavior for some mealybug

species (Calatayud et al. 1994; Cid and Fereres


aphid transmitted viruses; apparently, the virus is

carried on or near the stylets of the mealybug.


10.3.1 Viruses of Caulimoviridae

Types of Transmission

Mealybugs are phloem feeders, and a minimum

inoculation time of 15 min is needed for successful transmission. The virus persists through the

moult, and for 2–3 days in starved or feeding vectors. All mealybug-transmitted viruses appear to

have a semi-persistent mode of transmission

based on retention times; however, the Grapevine

leafroll-associated virus 3 (GLRaV-3) was found

in the salivary glands of its mealybug vector,

suggesting a circulative mode of transmission

(Cid et al. 2007). Mealybug-transmitted viruses

appear to have a high rate of acquisition and a

low rate of inoculation (Cid and Fereres 2010).

Ants that tend to carry the mealybugs may move

them from one plant to another (Sether et al.

1998), and occasionally, long-distance dispersal

by wind may also occur. An important factor

contributing to the slow rate of spread is that

newly infected trees are not infective for some

weeks, or even months, and the virus may not

become fully systemic in large trees for at least 1

year. Temperature-mediated mealybug activity

may be an important variable in transmission

efficiency, and the virus spread can occur through

the airborne dispersal of young, GLRaV-3infected crawlers (Cabaleiro and Segura 1997).

Cacao swollen shoot virus (CSSV) is transmitted

in a semi-persistent mode, meaning that the virus

is taken up into the vector's circulatory system

but does not replicate within it (Dzahini-Obiatey

et al. 2010). The feeding period required for the

acquisition of the virus is a minimum of 20 min,

but optimally 2–4 days (Posnette and Robertson

1950). Once acquired, the virus can be transmitted within 15 min, but optimal transmission

occurs 2–10 h after acquisition. No transmission

of the virus occurs through the mealybug eggs.

The relationship between the CSSV and mealybugs has some similarities to the non- persistent


Plant Viruses Transmitted

by Mealybugs

Nineteen species of mealybugs belonging to 13

genera are known to occur on Musaceae (Watson

and Kubiriba 2005). The Banana streak virus

(BSVs) (Fig. 10.1a) is transmitted by Planococcus

citri (Risso) and Saccharicoccus sacchari

(Cockerell), both of which colonize bananas

(Lockhart et al. 1992). Sugarcane bacilliform

virus (SCBV) is serologically related to BSVs

(Lockhart and Autrey 1988), and is reported to be

transmitted from sugarcane to banana by

Saccharicoccus sacchari (Cockerell) (Lockhart

and Olszewski 1993). Experimental transmission

of BSV’s has also been demonstrated with the

pink pineapple mealybug Dysmicoccus brevipes

(Cockerell) (Kubiriba et al. 2001) and

Pseudococcus comstocki (Kuwana) (Su 1998).

Ferrisia virgata (striped mealybug) (Fig. 10.1b)

has been found to be able to transmit the Banana

streak Mysore Virus (BSMYV) from banana to

banana (Selvarajan et al. 2006). Meyer et al.

(2008) reported that the transmission of activated

episomal Banana streak OL virus (BSOLV) to

cv. Williams banana (Musa sp.) by three mealy

bug species, viz. Dysmicoccus brevipes,

Planococcus citri and P. ficus.

Planococcus citri transmitted episomal

BSOLV and the Banana streak GF virus

(BSGFV) from tissue-culture derived plants of

FHIA-4 to cv. Williams plants. Using FHIA-TC

10 as the donor plant for transmission, the vector

transmitted a 100 % episomal BSOLV to

Williams’s plants after 3 months, and the numbers of mealybugs feeding on individual recipient plants during the inoculation access period

(IAP) ranged from 2 to 25 (Meyer et al. 2008).

Episomal BSVs were transmitted by D. brevipes.

At 3 months post transmission, the virus was

detected and symptoms had appeared. Due to the

reluctance of the mealybugs to move to Musa spp.,



Mealybugs as Vectors











Fig. 10.1 (a) Electron micrograph of BSV; (b) Ferrisia

virgata feeding on banana; (c) Pink pineapple mealybug,

Dysmicoccus brevipes; (d) Gray pineapple mealybug, D.

neobrevipes; (e) Electron micrograph of GLRaV; (f)

Electron micrograph of GVB; (g) Vine mealybug; (h)

Symptoms of BSV in banana; (i) GLRaV infected grapevine; (j) Symptoms of mealybug wilt of pineapple

the low numbers survived the inoculation access

period; the virus was transmitted from the TC-5

to the William banana. However, no episomal

BSGFV could be transmitted by D. brevipes from

the FH-4 donor to the recipient plants (Meyer

et al. 2008). The fact that none of the mealybug

species were able to transmit integrated BSOLV

from the FHIA-4 to Williams proves that the integrated form of BSV is not likely to be transmitted

by mealybugs; even highly efficient mealybugs

Tài liệu bạn tìm kiếm đã sẵn sàng tải về

2 The Origin of Mealybug Pest Status

Tải bản đầy đủ ngay(0 tr)