Table Of ContentAPHIDS ON
THE WORLD'S TREES
An Identification and Information Guide
R.L. Blackman and V.F. Eastop
Department of Entomology
The Natural History Museum
London
SW7 5BD
UK
CAB INTERNATIONAL
in association with
The Natural History Museum
APHIDS ON THE WORLD'S TREES
An Identification and Information Guide
CONTENTS
Preface vii
I INTRODUCTION 1
The Association Between Aphids and Trees 1
Life Cycles and Polymorphism 3
II THE TREES AND THEIR APHIDS 14
Notes on the Use of this Section 14
Morphology and Key Characters 15
Host Lists and Keys for Each Tree Genus (in alphabetical order) 21
Key to Polyphagous Tree-dwelling Aphids 532
III THE APHIDS 538
Introduction 538
Systematic Treatment of Aphid Genera (in alphabetical order) 539
IV TECHNIQUES 926
Collecting Methods 926
Preservation and Mounting 927
Labelling and Storage 928
V BIBLIOGRAPHY 930
Regionally Classified Works on Tree-dwelling Aphids 930
List of References 930
VI INDEX TO SPECIES NAMES OF APHIDS 967
VII PHOTOGRAPHS OF SLIDE-MOUNTED APHIDS 987
PREFACE
One of the first responses that we had to the book Aphids on the World's
Crops, soon after its publication in 1984, was from a colleague in forest
entomology, who pointed out that, despite the title of the work, we had
neglected even to mention a crop that he regarded as rather important, namely
timber. Almost ten years later, we hope that we have now gone some way
towards rectifying that omission.
When we compiled Aphids on the World's Crops (1984) we had good
reason to turn a blind eye to the aphids on timber trees, as we knew that keys
to identify tree-dwelling aphids would be a very different task, much more
complicated than the rather simple keys that we put together ten years ago
to identify the aphids most commonly found on agricultural and horticultural
crops. When we actually got down to the job, we found it necessary to adopt
a far more comprehensive approach than in the earlier work, as we could think
of no justifiable reason for including some aphid species and omitting others.
There was also no way of providing keys to identify aphids that had not been
slide-mounted, as many of the key couplets involve relatively minor differ-
ences between closely related species, requiring microscopic examination. We
think, nevertheless, that non-specialist entomologists will be able to use this
book to identify tree-dwelling aphids at least to genus, and it may then be
possible to confirm the identity of a species by taking into account the
biological information provided in Section III.
Another small problem was to decide what is, and what is not, a tree. We
claim no expertise in this matter, and have relied on standard botanical refer-
ence works, especially Bailey (1949), Uphof (1968), Willis (1973), Boutelje
(1980) and Mabberley (1987). If a genus contains plant species classified as
trees by any or all of these authorities then we have included it. If, as is often
the case, the same genus includes species of shrubby habit, then we have also
generally included such shrubs in the host lists because, in choosing a host plant,
aphids have a lot of regard for its genus but very little regard for its growth habit.
Vll
Preface
We are grateful to several colleagues who have given permission for the
results of their (as yet) unpublished work to be included; namely B. Agarwala,
S. Akimoto, S. Aoki, S. Barbagallo, P.A. Brown, C.I. Carter, S. Chakrabarti,
R. Danielsson, J. Holman, N. Moran, J.H. Martin, D. Noordam, W.
Quednau, G. Remaudière, J.T. Sorensen, D. Stern, M.B. Stoetzel and D.J.
Voegtlin.
INTRODUCTION
THE ASSOCIATION BETWEEN APHIDS AND TREES
The known world fauna of aphids (Aphidoidea) consists of 4401 species,
placed in 493 currently accepted genera. Of these, 1758 species in 270 genera
spend all or part of their life feeding on trees. Thus, only 40% of aphid species
but members of 55% of aphid genera occur on trees. The anomaly results from
the numerous members of the evolutionarily recent subfamily Aphidinae
which feed on the evolutionarily more recent herbaceous plants. It will be seen
from Table 1 that all the other major groups of aphids are mostly or even
entirely associated with trees.
The proportion of tree-living aphid species is probably even higher than
indicated, as the unknown hosts of many species are likely to be trees. The
trees most favoured as hosts tend to be the older evolutionary groups such
as Coniferae, Lauraceae, Fagaceae, Betulaceae, Hamamelidaceae, Ulmaceae
and Juglandaceae, and it seems likely that the major groups of aphids differ-
entiated before the appearance of herbaceous plants. Only three groups at the
tribal level live only on herbs; the Saltusaphidini (subfamily Drepanosiphinae)
which live on Cyperaceae and Juncaceae, the Siphini (subfamily Chaito-
phorinae) living on Gramineae, and the Tramini (subfamily Lachninae) living
mostly on roots of Compositae.
Aphids are predominantly a northern temperate group, with remarkably
few species in the tropics. Dixon (1987) postulated that the great diversity of
the tropical forest fauna mitigates against short-lived host-specific insects such
as aphids. Certainly the absence of aphids from many tropical forest trees is
striking, with whole families (e.g. Dipterocarpaceae) seeming almost immune
from attack. The absence of records of aphids from economically important
tropical forest trees such as mahogany (Swietenia mahogoni, Meliaceae) and
rosewood (Dalbergia nigra, Leguminosae) can hardly be due to negligence by
collectors, and suggests that aphids really do not occur on such trees. We
1
2 Introduction
think, however, that the explanation for this can be found in the evolutionary
history of aphids rather than in their present-day host relations or ecology.
Psyllids have similar ecology and host relations to aphids, yet many tropical
trees with few aphids bear a large psyllid fauna. It seems likely to us that
aphids have failed to diversify in the tropics because of one particular,
primitive feature of aphid biology, their cyclical parthenogenesis.
Cyclical parthenogenesis is a very successful way of exploiting the short-
lived growth flushes of temperate plants, but cannot be readily adapted
to tropical conditions. Aphids moving into the tropics simply lose the sexual
phase of the life cycle, and in doing so they lose the potential to evolve
and diversify that is dependent on the recombination of genes. The tropics
may also have acted in this way as a barrier to aphid colonization of southern
temperate regions, which also have very small indigenous aphid faunas.
The occurrence of Neophyllaphis on Podocarpus, Araucaria and related
conifers throughout the southern continents testifies to the age of aphid-tree
relationships, but very little is known about such evolutionarily ancient asso-
ciations. Most ecological and experimental studies of aphid-tree interactions
have concerned introduced species. In Britain, economic damage to spruce by
sporadic outbreaks of Elatobium abietinum has been documented since 1846.
Damage to the more recently introduced Picea sitchensis is particularly severe,
heavy infestations resulting in complete needle loss. Aphid infestations have
been shown to reduce the accretion of wood (e.g. of sycamore; Dixon, 1971a),
and have deleterious effects on tree root growth (e.g. of Tilia; Dixon, 1971b).
However, none of these trees is native to Britain. There are no native British
Picea, sycamore is an introduction from Central Europe, and the common
British lime tree (or linden) is thought to be a hybrid between a native and
an introduced species.
Planted forests of exotic trees cover enormous areas of the globe. There
are more than 5.5 million hectares of planted forests in Brazil, of which at
least 40% are Eucalyptus spp. (Anon., 1985). Pinus radiata occupies only a
small area in its native California but has been widely planted in New Zealand
and elsewhere. During this century many European, oriental and American
species of Pinus were introduced to various parts of Africa and grew aphid-
free for many years. In recent times three aphids, Eulachnus rileyi from
Europe, Cinara cronartii from North America and Pineus boerneri of uncer-
tain origin, have appeared on pines in Africa and caused far greater damage
than they do in Europe or America. Similarly, Cinara cupressi is much more
damaging to Cupressaceae in Africa than in Europe. These exotic conifers may
be growing under stress, and the aphids are certainly without the complex of
natural enemies associated with them in their countries of origin.
Most aphid damage to trees seems to result directly from feeding, either
by removal of sap or wounding of tissue, or in at least some cases by the toxic
effect of saliva. Aphids are rarely recorded as vectors of viruses infecting trees
(Biddle and Tinsley, 1967). Given the astronomical numbers of aphids in the
air and the length of life of trees, there must be strong selection among trees
for resistance to aphid-transmitted viruses. It would be interesting to know
the mechanism of this resistance, and whether it could be transferred to
Introduction 3
shorter-lived crop plants. Perhaps the energy required to maintain such
defences would be uneconomic for annual or biennial plants.
The problem of how a long-lived plant genotype such as an individual tree
survives, when its herbivores have numerous generations in which to evolve
methods of breaking its defences, is discussed by Whitham (1983), who
showed that there is a similar range of resistance to attack by Pemphigus betas
among different branches of one cottonwood tree, as there is among trees in
a population. He concluded that long-lived plants are mosaics of phenotypic
and/or genetic variability, the genetic differences possibly arising by somatic
mutation (Whitham and Slobodchikoff, 1981).
Alstad and Edmunds (1983) found that the black pine-leaf scale,
Nuculaspis californica, seemed to establish demes with genetic adaptations to
counteract the defence patterns of individual ponderosa pine trees. It is not
known whether any aphids develop such long-term natural associations. Tree-
dwelling aphids, especially those of the large subfamily Drepanosiphinae, tend
to be rather more active insects than the aphids which colonize herbaceous
plants, and may frequently move between trees - although the extent of move-
ment by individual aphids is still largely unknown. Most aphid species in
several other subfamilies alternate annually or biennially between their tree
host and a herbaceous host (see below), and therefore cannot develop
genotype-specific associations, unless of course they were to return to the same
tree year after year.
LIFE CYCLES AND POLYMORPHISM
Aphid life cycles can be quite complicated and involve a succession of morpho-
logically different forms (morphs) of the same species. The complexity - and
the terminology created to describe it - can be daunting to the non-specialist.
Rather than add to the pages of descriptive text already available on aphid life
cycles (e.g. Hille Ris Lambers, 1966e; Blackman, 1974; Dixon, 1985; Miyazaki,
1987), we will merely summarize the essential features, avoiding jargon as much
as possible, and use diagrams (Figs 1-7) to illustrate typical life cycles of tree-
dwelling aphids. Some unavoidable additional terminology - for example that
needed to describe adelgid morphs and life cycles - can be picked up by study-
ing the life cycle diagrams. The essential features of aphid life cycles are:
1. The various families and subfamilies of Aphidoidea each have life cycles
with characteristic features, indicating that they have evolved independently.
2. A complete life cycle (that is, a holocycle) typically consists of one genera-
tion of sexual morphs (sexuales) and several generations in which only parthe-
nogenetic females are produced. This phenomenon of cyclical parthenogenesis
is a basic, primitive feature of aphid biology.
3. In the more primitive families, Adelgidae and Phylloxeridae, both sexual and
parthenogenetic females are oviparous, but in the Aphididae parthenogenetic
females always give birth to live young; in Aphididae the parthenogenetic
4 Introduction
Table 1. Some features of the biology, host associations and life cycles of Aphidoidea. The
bracketed figures are total numbers of genera/total numbers of species : numbers of genera
known to live on trees/numbers of species known to live on trees. The classification follows
that used in B & E (1984) rather than that of Heie (1980), which raises most subfamilies to
family level. Table 3 (p. 539) compares the two classifications.
1 ADELGIDAE (2/49:2/49) alternation from galls on Picea to other Pinaceae, holarctic
1.1 Pineini (1/21:1/21) Picea to Pinus,
1.2 Adelgini (1/28:1/28) Picea to Larix, Pseudotsuga, etc.
2 PHYLLOXERIDAE (8/75: 7/64) Dicotyledons, holarctic
2.1 Phylloxerinini (1/7:1/7) Salicaceae
2.2 Phylloxerini (7/68:7/57) mostly Juglandaceae and Fagaceae, a few spp. on
Ulmaceae, Rosaceae and Vitaceae
APHIDIDAE
3 Pemphiginae (48/319:47/204) dwarf arostrate sexuales, oviparae produce only one egg
3.1 Eriosomatini (13/96 :13/58) galls or pseudogalls on Ulmaceae to various
angiosperms, often on roots, with ants; holarctic
3.2 Pemphigini (18/168 :17/108) holarctic
3.2.1 Pemphigina (6/78 :6/49) galls on Populus to roots of various herbs, more
rarely trees or aerial parts of herbs
3.2.2 Prociphilina (12/90:7/59) pseudogalls on various dicot trees to roots of
Coniferae, more rarely other plants
3.3 Fordini (17/55:17/38) alternation from galls on Anacardiaceae
3.3.1 Fordina (12/41:12/26) Pistacia, mostly to grass roots with ants, mostly
Mediterranean and East Asia, 1 American genus
3.3.2 Melaphidina (5/14:5/12) Rhus, mostly to mosses, mostly oriental, 1 American
genus
4 Hormaphidinae (45/183:42/144) host alternating, with small rostrate sexuales
4.1 Cerataphidini (13/91:10/57) galls on Styrax to Gramineae (esp. Bambuseae),
Palmaceae, Zingiberaceae, where often with ants; oriental
4.2 Hormaphidini (4/11:4/11) galls on Hamamelis to Betula, holarctic
4.3 Nipponaphidini (28/81:28/76) galls on Distylium to Lauraceae, Fagaceae, etc., where
often with ants; oriental
5 Phloeomyzinae (1 ?+) Populus, alate sexuales; all viviparae apterous; holarctic
6 Thelaxinae (3/12:3/12) Betulaceae, Fagaceae, Juglandaceae, often with ants; small
apterous sexuales; holarctic
7 Anoeciinae (2/34:2/15)
7.1 Aiceonini (1/14:1/9) Lauraceae; alate males; Asia
7.2 Anoeciini (1/20:1/6) alternation, Cornus to roots of Gramineae; sexuparae producing
small apterous males
8 Mindarinae (1/5:1/5) Pinaceae; Picea and Abies, few generations per year, holarctic
9 Drepanosiphinae (88/530:74/382) free-living on leaves, mostly on trees; fundatrices often
alate, oviparae apterous, many without ants
9.1 Drepanosiphini (7/45:6/37) Aceraceae; all viviparae alate; holarctic
9.2 Phyllaphidini (72/410:68/345) many on Fagaceae and Betulaceae, some on
Lauraceae, Annonaceae, Magnoliaceae, Ulmaceae, Juglandaceae, Combretaceae,
Burseraceae, Rosaceae, Leguminosae, bamboo; often all viviparae alate
Introduction 5
Table 1. (cont.)
9.3 Saltusaphidini (9/75:0/0) Cyperaceae and Juncaceae; apterous viviparae common;
holarctic
10 Chaitophorinae (11 /159:6/138) free-living on leaves and shoots, apterous viviparae
common, often with ants
10.1 Chaitophorini (6/138:6/138) holarctic
10.1.1 Chaitophorina (3/91:3/91) Salicaceae
10.1.2 Periphyllina (3/47:3/47) Aceraceae
10.2 Siphini (5/21:0/0) Gramineae; holarctic
11 Greenideinae (18/154:13/87) dicot trees, esp. Fagaceae, mostly East Asia
11.1 Greenideini (9/132:7/77) oviparae often alate
11.2 Cervaphidini (9/22:6/10) mostly southern hemisphere; 4 genera in Australia, 1 in
South America
12 Aphidinae (244/2517:59/299) fundatrices and oviparae large, males apterous or alate;
worldwide but mostly holarctic
12.1 Pterocommatini (5/49:5/37) Salicaceae, without host alternation; holarctic
12.2 Aphidini (25/665:14/90) alternation in many genera but many species are
monoecious; often with ants
12.2.1 Aphidina (20/585:9/67) mostly Rosidae and Asteridae
12.2.2 Rhopalosiphina (5/80:5/23) alternation, Rosaceae to Gramineae and
Cyperaceae
12.3 Macrosiphini (214/1803:40/222) alternation in many genera but many species are
monoecious on herbs, often without ants
13 Lachninae (20/361:14/299) fundatrices and oviparae large, males alate or apterous
(sometimes small); often with ants
13.1 Lachnini (9/57:8/50) mostly Fagaceae and Rosaceae; holarctic, esp. central and
eastern palaearctic
13.2 Cinarini (6/269:5/248) Coniferae; holarctic, most numerous in nearctic
13.3 Tramini (5/35:1/1) roots, mostly Compositae; palaearctic, esp. central and eastern
females are therefore termed viviparae, and the sexual females are distin-
guished as oviparae.
4. The more complex life cycles involve host alternation; the technical term
is heteroecy. In heteroecious aphids, the sexuales mate and fertilized eggs are
laid on a tree or shrub, the primary host, but a regular migration occurs
at some stage in the life cycle to another, totally unrelated plant, which may
be herbaceous or woody - the secondary host. On the secondary host, only
parthenogenetic generations (exules) occur, and a return migration to the
primary host is needed before the next sexual generation.
5. Because host alternation has evolved several times independently in
Aphidoidea, there are important differences at the family and subfamily levels
in the way in which it is achieved (see Figs 1-4). It may occur as part of a one-
year cycle (this happens in all Aphidinae, Hormaphidinae, Pemphigini,
Eriosomatini), or the complete cycle may take two years (Adelgidae, Fig. 1;
Fordina, Fig. 2).
