Notes and Comments
Ecology, 73(4), 1992, pp. 1514-1518
? 1992 by the Ecological Society of America
LEA VES WITH DOMA TIA HA VE MORE
MITES
David Evans Walter and Dennis J. O'Dowd'
Mutualism, a widespread and abundant ecological
interaction (Boucher 1985), has been of scant interest
to most ecologists (see Risch and Boucher [1976], and
also a nearly identical redaction in Keddy [1990]). So
perhaps it is not surprising that a proposed mutualism
between mites and plants with domatia, mite-sized
shelters at the junctures of veins on the abaxial surface
of leaves (Lundstrdem 1887), was virtually ignored or
anecdotally debunked for a century (reviewed in
O'Dowd and Willson 1989, 1991). However, the mite-
domatium association is of great antiquity (O'Dowd
et al. 1991), and it is not unreasonable to assume that
this may be a functional relationship.
How could domatia benefit a plant? A reasonable
hypothesis might be that domatia provide shelter for
natural enemies of pests that can affect plant fitness.
Recent work has demonstrated that leaf domatia are
inhabited primarily by predatory or microbivorous (i.e.,
consumers of fungi, bacteria, or algae) mites (O'Dowd
and Willson 1989, Pemberton and Turner 1989, Wal-
ter and Denmark 1991). The effect of mycophagous
mites on phylloplane fungi in unknown, but many
predatory mites are effective biological control agents
of phytophagous mites, including those that are de-
structive pests in agroecosystems (Helle and Sabelis
1985).
If domatia encourage mutualistic mites to remain
on leaves, then leaves with domatia should have more
beneficial mites than those without domatia. In addi-
tion, vulnerable mite life stages (e.g., eggs, molting in-
dividuals) should be found in domatia. We examined
these hypotheses in experiments on and comparisons
of mite associations with leaves of cultivated plants in
two gardens in surburban Melbourne, Australia. On
two plant species we experimentally removed domatia
and assessed the effect on mite abundance. We also
determined which mite species were predators, her-
bivores, or microbivores, and compared their distri-
butions and abundances on plants with and without
leaf domatia.
' Department of Ecology and Evolutionary Biology, Mo-
nash University, Clayton, Victoria 3168 Australia.
Materials and Methods
All surveys and experiments were conducted during
the spring and summer of 1990-1991. Only evergreen
shrubs and small trees were surveyed to avoid the com-
plications of variable mite colonization rates on de-
ciduous leaves (Walter and Denmark 1991). Mites were
censused initially using all leaves from six shoots. Pow-
er was increased in later samples by using one leaf from
each of 10 shoots per plant. Each sample was bagged,
taken to the laboratory, and all mites on each leaf were
identified and counted. All domatia, trichomes, ar-
thropod silk, and debris were dissected with a scalpel.
We used gut contents, direct observations on field-
collected leaves of mites feeding, and rearings on intact
leaves or waxed-paper disks suspended in water-sat-
urated cotton to determine mite feeding biology. Eggs
were identified to species by hatching field-collected
specimens or by inducing females to oviposit in the
laboratory. Voucher specimens were deposited at
Monash University and with the Australian National
Insect Collection, Canberra.
Because many domatia are elaborate pockets or pits
in the vein axils, excision would have caused extensive
damage; however, tuft domatia could be removed with
little damage by shaving trichomes with a curved scal-
pel, and checking the results with a hand lens (Fig. 1).
Occasionally some domatia, usually at the base of the
leaf, were missed or only partially removed (see Table
1). To determine the effect of tuft domatia on mite
distribution and numbers, paired leaves (blocks) on a
shrub of Viburnum tinus were marked and all domatia
were shaved from a randomly selected leaf in each pair
on 15 November. Mite numbers were censused after
2 wk. This experiment was repeated on 30 November
using a completely random design with the addition
of a treatment in which domatia were shaved on only
one half of the leaf to determine if the treatment caused
an acarophobic response in the plant. These leaves
were allowed 6 wk for mite populations to recover.
Mite association and distribution of life stages in do-
matia were monitored using weekly samples from V.
tinus between 25 October and 23 November. On 1
December domatia also were shaved from leaves of a
semi-deciduous tree, Quercus robur, growing midway
between the two gardens, using a completely random
design.
If mite distribution and abundance were influenced
by domatia, we expected that leaves of species without
domatia would have fewer mites. We compared in-
dividuals of 19 species from 15 families of evergreen
shrubs and small trees with and without leaf domatia
growing in gardens 2 km apart. Plant species originated
 A0 II 1992
_ Nol"
AM a- - II :1-X1- I3 IUN"v J o _ 5or t

from Asia (7), Europe (3), North American (2), South

America (2), New Zealand (1), and Australia (4). None
of the Australian species were native to the Melbourne
area. Ten shrub species (4 with domatia, 6 without)
were sampled on 15 October. Eight shrub species with
domatia (all that were present) and 11 species without
domatia were sampled in the gardens on 13 December.
Six shrubs each of two commonly planted garden
shrubs, Viburnum tinus (tuft domatia) and Photinia
glabra (no structures in vein axils), were sampled on
13 November to assess the effects of individual plant
variation.
Treatments were randomly assigned and samples
were haphazardly taken unless otherwise stated. Num-
ber of mites per leaf or mean number of mites per leaf
(if shoots were sampled) were nested within species for
analysis of variance (ANOVA). Transformed counts
{log[0.5 + (count x 10)]} were used to homogenize
variances and normalize data before ANOVA. Data
could not be normalized in one shaving experiment,
so a nonparametric test was used.

Results

Fourteen species of mites were collected during this

study. Except for a single herbivore (Tetranychus sp.),
all were predators or microbivores, and thus poten-
tially beneficial, or at least not deleterious, to the plant
species on which they occurred. Eusejus elinae, Typh-
lodromus dossei (both Phytoseiidae), and Agistemus
longisetus (Stigmaeidae) fed on mites, and also on pol-
len. Eryngiopus sp. (Stigmaeidae) and Tydeus sp. (Ty-
deidae) were not observed feeding, but both are prob-
ably predators, and the latter possibly an omnivore
(Hessein and Perring 1976). Cheletomimus berlesei
FIG. 1. Undersurface of leaf of Viburnum tinus (1.6 x). (A)
Location of tuft domatia in vein axils (arrow). (B) Intact do-
matium (22.2 x). (C) Shaved domatium (22.2 x).
(Chelytetidae) and Rubroscirus sp. (Cunaxidae), and
Anystis baccarum attacked mites and small insects (e.g.,
thrips). Triophtydeus sp. (Tydeidae) fed on both pollen
and fungi, and Czenspinskia transversostriata (Win-
terschmidtiidae), Tarsonemus sp. near waitei (Tarso-

TABLE 1. Effect of removal of domatia (shelters) from leaves of Viburnum tinus on mite abundance. Domatia on leaves were
left untreated, shaved from one side of the midrib, or shaved from both sides (15 leaves/treatment). Abundance is given
for total mites, for feeding groups (predators, epiphyll feeders, and unknown), and for the five most abundant species. Mites
were censused 2 wk (Experiment 1) or 6 wk (Experiment 2) after treatment. In both experiments total mite numbers were
significantly lower on leaves with both sides shaved (ANOVA, Expt. 1: F1.13 = 11.3, P = .005; Expt. 2: F2,42 = 10.8, P <
.0001).

Experiment 1 Experiment 2

Both sides One side Both sides

Untreated shaved Untreated shaved shaved

Abundance (mean ? 1 SE)

Domatia per leaf 7.1 ? 0.5 2.0 ? 0.5 6.9 ? 0.3 3.1 ? 0.2 0.8 ? 0.2
Total mites per 10 leaves 66.4 ? 11.0 10.7 ? 2.9 44.0 ? 7.8 24.7 ? 3.8 7.3 ? 2.5
Predators 15.0 ? 4.5 2.1 ? 1.1 4.7 ? 1.7 4.7 ? 2.4 1.3 ? 0.9
Euseius elinae 6.4 ? 2.5 1.4 ? 1.0 1.3 ? 0.9 0 0
Agistemus longisetus 5.7 ? 2.9 0.7 ? 0.7 0.7 ? 0.7 2.7 ? 1.5 1.3 ? 0.9
Epiphyll feeders 45.7 ? 11.1 7.1 ? 3.0 37.3 ? 7.5 19.3 ? 3.2 4.7 ? 2.4
Czenspinskia transversostriata 19.3 ? 8.7 2.9 ? 1.9 10.7 ? 4.8 4.0 ? 1.9 0.7 ? 0.7
Triophtydeussp. 26.4 ? 5.7 4.3 ? 1.7 26.7 ? 5.0 15.3 ? 3.1 4.0 ? 1.9
Other
Tydeus sp. 5.7 ? 2.3 1.4 ? 1.0 2.0 ? 1.5 0.7 ? 0.7 1.3 ? 1.3
 1516 NOTES AND COMMENTS Ecology, Vol. 73, No. 4
TABLE 2. Association of eggs, of quiescent molting immatures and of active stages of the most abundant mite species with
leaf domatia on a Viburnum tinus shrub over a 5-wk period (6 shoots per week, 247 leaves sampled in total).
Egg
Mite % N
Euseius elinae 77.9 149 NA* 64.9 202
Agistemus longisetus 37.9 29 100.0 5 84.6 78
Czenspinskia transversostriata 98.8 258 100.0 19 95.2 114
Triophtydeus sp. 100.0 84 87.5 8 86.9 297
Tydeus sp. 100.0 20 100.0 26 95.2 481
Total mites 89.3 552
* NA = not applicable.
nemidae), Scapheremaeus sp. (Cymbaerimaeidae), and
Zygoribatula sp. (Oribatulidae) fed on a variety of fun-
gi.
Total mite numbers per leaf on V. tinus were sig-
nificantly reduced when most domatia were removed
(untreated and half-shaved leaves did not differ sig-
nificantly, P = .515, Tukey's HSD test; Table 1). With
few exceptions, this effect was consistent for all mite
species and feeding groups. Even within half-shaved
leaves, mite abundance was six times as great on the
side with domatia as on the shaved side. On Q. robur,
only a few Triophtydeus sp., a microbivore, were pres-
ent on leaves with domatia (10.0 ? 3.3 individuals per
10 leaves), but no mites were present on oak leaves
from which the domatia had been shaved (P < .003,
Mann-Whitney U test).
Results of the shaving experiments were consistent
with the observations that most mite developmental
stages, particularly eggs and quiescent molting indi-
viduals, were associated with leaf domatia in V. tinus
over a 5-wk period (Table 2). When not in domatia,
eggs of Euseius elinae and Agistemus longisetus, two
large predatory mites, were often associated with silken
strands from spiders, psocids, or tetranychid mites.
Males were often found guarding female deutonymphs
in domatia.
Shrubs and trees with leaf domatia generally had
more mites per leaf than those plants without domatia.
In October, any comparison between sites was sacri-
ficed because only two species were sampled from the
second garden; however, over four times as many mites
(39.7 ? 15.2 individuals per 10 leaves) were found on
leaves of plants with domatia as on those without do-
matia (9.1 ? 3.6 mites per 10 leaves) (ANOVA, F. 8
= 7.5, P = .025). In December, mite abundances were
eight to ten times higher on plants with domatia com-
pared to those without domatia at the two sites (Table
3). Site and site x domatia interaction were not sig-
nificant.
If domatia were an important factor determining
mite abundance on leaves, then subtracting those mites
in domatia from totals should result in similar counts
Molting Active
% N % N
98.3 58 87.0 1193
on leaves with and without domatia. Pooling across all
mite and plant species in the two gardens in December,
72.3% of mite eggs, 60% of quiescent, molting mites,
and 25.2% of active mites were collected in leaf doma-
tia. If only mites outside of domatia were compared,
then mite abundances did not differ significantly be-
tween plant species with or without domatia (ANOVA,
F. j5 = 0.4, P = .535).
Across individuals of V. tinus, number of domatia
ranged from 2 to 10 per leaf and was positively cor-
related with the number of mites (R 2 = 0.176, F.58 =
12.4, P = .001). Mites were ten times as abundant on
V. tinus as on P. glabra (66.0 ? 13.4 vs. 6.3 ? 1.8
individuals per 10 leaves; ANOVA, F.,10 = 38.8, P <
.0001). Again, when mites in domatia were subtracted
from the counts, the difference disappeared (ANOVA,
F,0 = 0.6, P = .453).
Discussion
The mites identified in this study comprise a pred-
ator-microbivore fauna that is broadly distributed
across plant species, but most abundant on plants with
domatia. Domatia directly account for the significant
differences in mite abundance between leaves with and
without domatia. We experimentally demonstrated this
by removing tuft domatia from two plants. Further,
across a broad variety of unrelated plant species of
diverse geographical origins, elevated abundances of
mites on domatium-bearing leaves resulted from mites
in domatia and not those on the leaf surface. Even
within individuals of a single plant species, V. tinus,
17.6% of the variation in mite numbers per leaf was
explained by domatium number.
Increased mite abundance on leaves with domatia
could result from a tendency of mites to stay longer,
survive better, or lay more eggs than on leaves without
domatia. The shelter provided by domatia, acting as
protection from either natural enemies or abiotic stress,
is the most likely explanation for the increased abun-
dance of mites. Although domatia comprise only a
small fraction of total leaf area, they contain most in-
active stages (eggs and quiescent, molting mites), and
 August 1992 NOTES AND COMMENTS 1517

TABLE 3. Mite abundance (mean ? 1 SE) on leaves fr

in Clayton, Victoria, Australia, on 13 December 199
given. Mean total number of mites is significantly
sites) than on those lacking domatia (11.4 and 5.3

Mite abundance (no./10 leaves)

Domatia Typhlo- Agis- Trioph-

__________________ Euseius dromus temus tydeus Tydeus
Species (Family) Type Number/leaf elinae dossei longisetus sp. sp. All mites
Site 1
Domatia present
Alnus jorullensis
(Betulaceae) Pocket 12.5 ? 0.4 4 ? 2 2 ? 1 0 5 ? 4 8 ? 5 20 ? 6
Annona reticulate
(Annonaceae) Pocket 23.9 ? 2.0 10 ? 4 0 12 ? 7 379 ? 82 29 ? 8 430 ? 87
Elaeocarpus reticulatus
(Elaeocarpaceae) Pocket 15.1 ? 0.6 2 ? 1 0 0 17 ? 6 0 19 ? 6
Luculia gratissima
(Rubiaceae) Pocket 13.3 ? 0.9 16 9 17 ? 11 7 ? 4 24 ? 5 3 ? 2 69 ? 11
Coprosma hirtella
(Rubiaceae) Pit 5.9 ? 0.4 6 3 1 ? 1 0 20 ? 7 21 ? 11 52 ? 18
Domatia absent
Acmena smithii
(Myrtaceae) ... ... 0 0 0 13 ? 12 0 13 ? 12
Bougainvillea spectabilis
(Nyctaginaceae) 1. +1 0 12 ? 4 12 ? 6 0 26 ? 7
Fortunella japonica
(Rutaceae) ... ... 0 0 0 1 ? 1 0 1 ? 1
Gardenia jasminoides
(Rubiaceae) 0 0 0 0 0 0
Garrya elliptica
(Garryaceae) ... ... 0 3 ? 2 15 ? 8 10 ? 4 1 ? 1 36 ? 12
Ilex aquifolium
(Aquifoliaceae) ... ... 0 0 0 1 ? 1 0 1 ? 1
Macadamia tenuifolia
(Proteaceae) ... ... 0 3 ? 2 0 7 ? 3 0 10 ? 3
Magnolia grandiflora
(Magnoliaceae) ... ... 0 0 1 ? 1 3 ? 2 0 4 ? 2
Site 2
Domatia present
Coprosma repens
(Rubiaceae) Pit 5.4 ? 1.1 1 ? 1 0 0 9 ? 4 0 10 ? 4
Laurus nobilis
(Lauraceae) Pit 2.9 ? 0.5 0 0 0 68 ? 30 0 68 ? 30
Viburnum tinus
(Caprifoliaceae) Tuft 6.1 ? 0.3 15 ? 6 0 7 ? 3 30 ? 5 1 ? 1 55 ? 10
Domatia absent
Camellia japonica
(Theaceae) ... ... 0 0 0 2 ? 2 0 2 ? 2
Citrus limon (Rutaceae) 1 ? 1 0 0 0 0 1 ? 1
Photinia glabra
(Rosaceae) ... ... 7 ? 5 0 2 ? 1 4 ? 2 0 13 ? 6

a large fraction of active stages (larvae, nymphs, and
adults).
Phytophagous mite populations are often controlled
by predators (Helle and Sabelis 1985), and the high
predator populations present in these two gardens no
doubt contributed to the low numbers of herbivores.
Similarly high predatory and low phytophagous mite
populations on deciduous woody ornamentals that are
known to have domatia have been reported from parks
in Poland (Kropczynska et al. 1985). Since phytoph-
agous mites were very rare in our gardens, we could
not determine if herbivore numbers were suppressed
on leaves with domatia. However, it is unlikely that
plants rely solely on predaceous mites for protection.
Domatia are just one of the many possible defenses
against herbivorous mites.
These results extend beyond initial surveys showing
mite association with domatia (O'Dowd and Willson
 1518 NOTES AND COMMENTS Ecology, Vol. 73, No. 4
1989, Pemberton and Turner 1989, Walter and Den-
mark 1991, Willson 1991) by demonstrating a rela-
tionship between domatia and higher numbers of po-
tentially beneficial mites on leaves of a wide variety of
plants. Although our data do not demonstrate that
plants benefit from increased mite abundance, the po-
tential for mite-plant mutualism is clear.
Acknowledgments: We thank J. Addicott, R. Colwell,
B. Downes, R. B. Halliday, E. E. Lindquist, P. W. Price,
G. Quinn, and two anonymous referees for comments
that improved the manuscript. A. O'Dowd drew Fig.
1. This research was supported by the Australian Re-
search Council.
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Manuscript received 11 March 1991;
revised 26 August 1991;
accepted 10 October 1991.