Soft Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors)

9 1997 Elsevier Science B.V. All rights reserved. 339

1.3.3 Crawler Behaviour and Dispersal

DAVID J. GREATHEAD

INTRODUCTION

Many important pest species of Coccoidea have been spread by man through the
movement of cuttings, nursery stock and produce, to the extent that they are now
virtually cosmopolitan (Simmonds and Greathead, 1977). Consequently, natural
dispersal mechanisms have been a largely neglected topic for research. Because most
crawlers settle close to the parent female (e.g. Bodenheimer, 1935) and because coccids,
except males, lack any obvious means of movement over greater distances, there has
been a widespread belief that their powers of dispersal are poor. Phoretic transfer of
crawlers and gravid females on human clothing, in the hair of mammals and on the
plumage of birds is commonly believed to be an important means of dispersal, but
Washburn and Frankie (1981), working in California, showed that, whilst crawlers and
ovisacs of the iceplant scale, Pulvinariella mesembryanthemi (Vallot), could adhere to
clothing and the hair of dogs and could survive long enough for transport to another site,
laboratory tests indicated that survival on mice was less than one hour and on parakeets
only 15 minutes. Thus, they concluded that this means of dispersal is probably less
important than wind. Studies on this and other species of soft scales, using sticky traps,
have shown that crawlers can be dispersed over considerable distances on wind currents,
as was first demonstrated by Quayle (1916) for the black scale, Saissetia oleae (Olivier),
in Californian citrus groves. Experimental results demonstrating the importance of wind
in the dispersal of crawlers of armored scales (Diaspididae), principally Aulacaspis
tegalensis (Zehntner) and Aonidiella aurantii (Maskell), has been reviewed in an
accompanying volume in this series (Greathead, 1989). Information is also available on
the dispersal of representatives of other families, notably mealybugs on cocoa in Ghana
(Comwell, 1958, 1960); margarodids Icerya seychellarum Westwood on Aldabra Atoll
in the Indian Ocean (Hill, 1980) and Matsucoccus resinosae Bean and Godwin on red
pine in Connecticut (Stephens and Aylor, 1978); an eriococcid, Cryptococcus fagisuga
Lindinger, on beech trees in England (Wainhouse, 1980) and a dactylopiid, Dactylopius
austrinus De Lotto, on Opuntia aurantiaca Lindley in South Africa (Moran et al., 1982).
These studies have all shown that dispersal by wind currents is a common feature among
Coccoidea but there is less information on the behaviour associated with this
phenomenon.
The most comprehensive study of dispersal of soft scale crawlers has been made on
P. mesembryanthemi and Pulvinaria delottoi (Gill) in California (Washburn and Frankie,
1981, 1985; Washburn and Washburn, 1984). Other relevant observations have been
made on the citrus scale, Coccus hesperidum L. in Texas (Hoelscher, 1967; Reed et al.,
1970), the pine tortoise scale, Toumeyella numismaticum (Pettit and McDaniel)
[ = Toumeyella parvicornis (Cockerell] in Manitoba (Rabkin and Lejeune, 1954), S. oleae
(Mendel et al., 1984) and the Florida wax scale, Ceroplastes floridensis Comstock

Section 1.3.3 references, p. 342

340 Ecology

(Yardeni, 1987), the latter two species on citrus in Israel. Because of the similarity in
behaviour and dispersal mechanisms exhibited by the crawlers of the investigated species
from the various families, this review draws on these observations to supplement the
meagre information on dispersal by soft scale crawlers.

CRAWLER BEHAVIOUR

Under alternating light:dark regimes, crawlers of S. oleae emerge from beneath the
female at the onset of the light phase in laboratory tests (Mendel et al., 1984) and so
would emerge shortly after dawn in the field, as do the crawlers of armored scales
(Greathead, 1989), lcerya seychellarum (Hill, 1980) and presumably most scale insects.
Survival of S. oleae crawlers depends on temperature and humidity, varying from over
twelve days at 23~ at 100% RH to less than a day at 29~ at any humidity (Mendel
et al., 1984). Pulvinariella mesembryanthemi crawlers appear to be more robust and
survive about four days in dry air and eight days in moist air (Washburn and Frankie,
1981). The majority of crawlers of all the species studied wander for less than a day
before settling near the female - 80% of those of S. oleae settled within 24 hours
(Mendel et al., 1984). Washburn and Frankie (1981) measured the speed ofwalking of
P. mesembryanthemi crawlers as 0.72-1-0.22 mm sec ~ in a greenhouse experiment (but
Greathead (1975) had shown that the speext of movement of Aulacaspis tegalensis
crawlers was strongly affected by humidity). They also demonstrated that there was
little movement between plants laid out on a grid in the greenhouse. The crawlers move
upwards on the plant which has the effect of bringing them to younger leaves which are
the preferred feexling sites (Washburn and Frankie, 1985). In laboratory tests, 80% of
the crawlers moved into the illuminated areas of a test arena (Washburn and Frankie,
1981) and thus were positively phototropic and negatively geotropic, as are those of
armored scales (Greathead, 1989). Evidently not all scale insects respond to gravity
because Wainhouse (1980) was only able to demonstrate phototaxis in Cryptococcus
fagisuga. These behaviours bring crawlers to young tissue which is preferred and also
to the tops of plants where those that have not settled can be dislodged by air currents.
Wind tunnel experiments with P. mesembryanthemi showed that the crawlers exhibit
take-off behaviour (Washburn and Washburn, 1984) (as did the white sugarcane scale,
Aulacaspis tegalensis) but apparently not in another armored scale, the citrus red scale,
Aonidiella aurantii (Greathead, 1989) and so this behaviour may not be present in all
species. Crawlers submitted to wind strengths of between 1.8 and 4.0 m sec ~ take up
a characteristic position which facilitates removal from the substrate. They rise, facing
away from the air current, on their second and third pairs of legs, or on the third pair
only, with the antennae and free legs outstretched. This position appears to facilitate
dislodgement by increasing drag and reducing the grip of the tarsal claws on the
substrate. This behaviour is only exhibited by crawlers over 76 hours old, i.e. those
which have not settled during the first 24 hours. In the field, crawlers accumulate at the
tips of leaves at the tops of the host plants from which they are carried away by the
wind.

DISPERSAL BY AIR CURRENTS

Washburn and Frankie (1981) used sticky boards on 1 m poles and 3.5 m towers to
demonstrate wind dispersal of P. mesembryanthemi and measured a maximum
interception rate 10 cm above the canopy of 225 crawlers h ~ over their 48 hour sampling
period, when the average wind speed was 13.4 km h ~. Crawler density decreased with
height and was highest on boards facing into the wind. Crawlers were captured up to
a maximum of 50 m above the ground (Washburn and Frankie, 1985). From these
Crawlerbehaviour 341

observations, and from the results of laboratory experiments indicating a sinking speeA
of 26.2 cm see ~ for live crawlers in still air, Washburn and Washburn (1984) concluded
that crawlers could be transported well over 190 km in 24 hours at a wind speed of 8
km h ~
Other investigators have measured downwind dispersal with traps laid out at distances
from source populations of scales. Thus, Rabkin and Lejeune (1954) found crawlers of
Toumeyella numismaticum (Pettit & McDaniel) [= Toumeyella parvicornis (Cockerell]
up to 4.8 km (3 miles) downwind and Hoelscher (1967) trapped Coccus hesperidum
crawlers 55 m from the source. Reed et al. (1970) observed infestations near
windbreaks and noted that they were lower on the lee side, where catches on sticky
boards were also less, confirming that airborne crawlers are an important source of
infestation (see Greathead, 1972, for similar observations on Aulacaspis tegalensis and
explanation of the effect of windbreaks on the distribution of air-borne insects). Yardeni
(1987), working with Ceroplastesfloridensis in Israel, found that 79% of crawlers on
sticky traps were captured downwind of infested trees and that clean trees downwind of
the source developed infestations more frequently on the upwind side (26 %) than on the
downwind side (8 %).

DISCUSSION

These observations on soft scales are consistent with those obtained with the crawlers
of armored scale insects (Greathead, 1989), namely that the principal natural means of
dispersal from host plant to host plant within an area and over greater distances between
suitable habitats is by transport on air currents. However, there is no proof that
dispersal over distances of tens or hundreds of kilometres actually takes place although
there is strong circumstantial evidence that this happened in eastern Africa with
A. tegalensis, which feeds only on sugarcane. The longest observed distance travelled
by airborne crawlers relates to Icerya seychellarum which was trapped over water
3.5 km downwind of an infestation (Hill, 1980). Wainhouse (1980) quotes evidence that
Cryptococcus fagisuga spread at a rate of 6-8 km yr m following its introduction into
North America in 1890. Both A. tegalensis, which feeds on sugarcane, and
P. mesembryanthemi, which feeds on the iceplant Carpobrotus edulis (L.), have been
shown to exhibit take-off behaviour which indicates that, in these species at least,
dispersal on air currents is not accidental. They are also unusually fecund;
P. mesembryanthemi produces up to 2,400 crawlers (Washburn and Frankie, 1985)
whereas Toumeyella parvicornis, feeding on pine trees, produces only 534 +50 eggs.
Another scale insect which exhibits take-off behaviour is Dactylopius austrinus. The
crawlers of this species are sexually dimorphic, the female crawlers developing long wax
threads which aid dispersal. The males do not develop these waxy threads but are able
to disperse as winged adults, unlike the females (Moran et al., 1982).
In keeping with the ecological explanation of migratory behaviour put forward by
Southwood (1962) and Johnson (1969), Greathead (1972) suggested that take-off
behaviour is an adaptation to short-lived host plants which constitute temporary habitats,
whereas the majority of scale insects feed on trees which can be regarded as permanent
habitats. These authors propose that migrant species occupy temporary or unstable
habitats. Thus, it would also be expected that the majority of pest species, feeding on
tree crops, will be less adapted for dispersal and less fecund. However, even if they do
not disperse as readily, the observations reviewed here do indicate that movement
between trees is predominantly on air currents and that transport on the bodies of
animals is likely to be less important. Gunn (1979) attempted to verify this hypothesis
by collecting information from the literature on the fecundity of scale insects but he was

Section 1.3.3 references, p. 342

342 Ecology

u n a b l e to fred clear e v i d e n c e to substantiate it. H o w e v e r , as p o i n t e d out by W i l l i a m s

( 1 9 7 0 ) , m a n y p u b l i s h e d estimates o f fecundity are serious u n d e r e s t i m a t e s , so that such
c o m p a r i s o n s are unreliable.

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