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Notes and Comments

Ecology, 73(4), 1992, pp. 1514-1518 Materials and Methods


? 1992 by the Ecological Society of America
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-
LEA VES WITH DOMA TIA HA VE MORE plications of variable mite colonization rates on de-
ciduous leaves (Walter and Denmark 1991). Mites were
MITES
censused initially using all leaves from six shoots. Pow-
er was increased in later samples by using one leaf from
David Evans Walter and Dennis J. O'Dowd'
each of 10 shoots per plant. Each sample was bagged,
Mutualism, a widespread and abundant ecological taken to the laboratory, and all mites on each leaf were
interaction (Boucher 1985), has been of scant interest identified and counted. All domatia, trichomes, ar-
to most ecologists (see Risch and Boucher [1976], and thropod silk, and debris were dissected with a scalpel.
also a nearly identical redaction in Keddy [1990]). So We used gut contents, direct observations on field-
perhaps it is not surprising that a proposed mutualism collected leaves of mites feeding, and rearings on intact
between mites and plants with domatia, mite-sized leaves or waxed-paper disks suspended in water-sat-
shelters at the junctures of veins on the abaxial surface urated cotton to determine mite feeding biology. Eggs
of leaves (Lundstrdem 1887), was virtually ignored or were identified to species by hatching field-collected
anecdotally debunked for a century (reviewed in specimens or by inducing females to oviposit in the
O'Dowd and Willson 1989, 1991). However, the mite- laboratory. Voucher specimens were deposited at
domatium association is of great antiquity (O'Dowd Monash University and with the Australian National
et al. 1991), and it is not unreasonable to assume that Insect Collection, Canberra.

this may be a functional relationship. Because many domatia are elaborate pockets or pits
How could domatia benefit a plant? A reasonable in the vein axils, excision would have caused extensive
hypothesis might be that domatia provide shelter for damage; however, tuft domatia could be removed with
natural enemies of pests that can affect plant fitness. little damage by shaving trichomes with a curved scal-
Recent work has demonstrated that leaf domatia are pel, and checking the results with a hand lens (Fig. 1).
inhabited primarily by predatory or microbivorous (i.e., Occasionally some domatia, usually at the base of the
consumers of fungi, bacteria, or algae) mites (O'Dowd leaf, were missed or only partially removed (see Table
and Willson 1989, Pemberton and Turner 1989, Wal- 1). To determine the effect of tuft domatia on mite
ter and Denmark 1991). The effect of mycophagous distribution and numbers, paired leaves (blocks) on a
mites on phylloplane fungi in unknown, but many shrub of Viburnum tinus were marked and all domatia
predatory mites are effective biological control agents were shaved from a randomly selected leaf in each pair
of phytophagous mites, including those that are de- on 15 November. Mite numbers were censused after
structive pests in agroecosystems (Helle and Sabelis 2 wk. This experiment was repeated on 30 November
1985). using a completely random design with the addition
If domatia encourage mutualistic mites to remain of a treatment in which domatia were shaved on only
on leaves, then leaves with domatia should have more one half of the leaf to determine if the treatment caused
beneficial mites than those without domatia. In addi- an acarophobic response in the plant. These leaves
tion, vulnerable mite life stages (e.g., eggs, molting in- were allowed 6 wk for mite populations to recover.
dividuals) should be found in domatia. We examined Mite association and distribution of life stages in do-
these hypotheses in experiments on and comparisons matia were monitored using weekly samples from V.
of mite associations with leaves of cultivated plants in tinus between 25 October and 23 November. On 1
two gardens in surburban Melbourne, Australia. On December domatia also were shaved from leaves of a
two plant species we experimentally removed domatia semi-deciduous tree, Quercus robur, growing midway
and assessed the effect on mite abundance. We also between the two gardens, using a completely random
determined which mite species were predators, her- design.
bivores, or microbivores, and compared their distri- If mite distribution and abundance were influenced
butions and abundances on plants with and without by domatia, we expected that leaves of species without
leaf domatia. domatia would have fewer mites. We compared in-
dividuals of 19 species from 15 families of evergreen
' Department of Ecology and Evolutionary Biology, Mo- shrubs and small trees with and without leaf domatia
nash University, Clayton, Victoria 3168 Australia. 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- FIG. 1. Undersurface of leaf of Viburnum tinus (1.6 x). (A)
Location of tuft domatia in vein axils (arrow). (B) Intact do-
tially beneficial, or at least not deleterious, to the plant
matium (22.2 x). (C) Shaved domatium (22.2 x).
species on which they occurred. Eusejus elinae, Typh-
lodromus dossei (both Phytoseiidae), and Agistemus
longisetus (Stigmaeidae) fed on mites, and also on pol- (Chelytetidae) and Rubroscirus sp. (Cunaxidae), and
len. Eryngiopus sp. (Stigmaeidae) and Tydeus sp. (Ty- Anystis baccarum attacked mites and small insects (e.g.,
deidae) were not observed feeding, but both are prob- thrips). Triophtydeus sp. (Tydeidae) fed on both pollen
ably predators, and the latter possibly an omnivore and fungi, and Czenspinskia transversostriata (Win-
(Hessein and Perring 1976). Cheletomimus berlesei 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 Molting Active

Mite % N % N % 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 98.3 58 87.0 1193

* NA = not applicable.

nemidae), Scapheremaeus sp. (Cymbaerimaeidae), and on leaves with and without domatia. Pooling across all
Zygoribatula sp. (Oribatulidae) fed on a variety of fun- mite and plant species in the two gardens in December,
gi. 72.3% of mite eggs, 60% of quiescent, molting mites,
Total mite numbers per leaf on V. tinus were sig- and 25.2% of active mites were collected in leaf doma-
nificantly reduced when most domatia were removed tia. If only mites outside of domatia were compared,
(untreated and half-shaved leaves did not differ sig- then mite abundances did not differ significantly be-
nificantly, P = .515, Tukey's HSD test; Table 1). With tween plant species with or without domatia (ANOVA,
few exceptions, this effect was consistent for all mite F. j5 = 0.4, P = .535).
species and feeding groups. Even within half-shaved Across individuals of V. tinus, number of domatia
leaves, mite abundance was six times as great on the ranged from 2 to 10 per leaf and was positively cor-
side with domatia as on the shaved side. On Q. robur, related with the number of mites (R 2 = 0.176, F.58 =
only a few Triophtydeus sp., a microbivore, were pres- 12.4, P = .001). Mites were ten times as abundant on
ent on leaves with domatia (10.0 ? 3.3 individuals per V. tinus as on P. glabra (66.0 ? 13.4 vs. 6.3 ? 1.8
10 leaves), but no mites were present on oak leaves individuals per 10 leaves; ANOVA, F.,10 = 38.8, P <
from which the domatia had been shaved (P < .003, .0001). Again, when mites in domatia were subtracted
Mann-Whitney U test). from the counts, the difference disappeared (ANOVA,
Results of the shaving experiments were consistent F,0 = 0.6, P = .453).
with the observations that most mite developmental
Discussion
stages, particularly eggs and quiescent molting indi-
viduals, were associated with leaf domatia in V. tinus The mites identified in this study comprise a pred-
over a 5-wk period (Table 2). When not in domatia, ator-microbivore fauna that is broadly distributed
eggs of Euseius elinae and Agistemus longisetus, two across plant species, but most abundant on plants with
large predatory mites, were often associated with silken domatia. Domatia directly account for the significant
strands from spiders, psocids, or tetranychid mites. differences in mite abundance between leaves with and
Males were often found guarding female deutonymphs without domatia. We experimentally demonstrated this
in domatia. by removing tuft domatia from two plants. Further,
Shrubs and trees with leaf domatia generally had across a broad variety of unrelated plant species of
more mites per leaf than those plants without domatia. diverse geographical origins, elevated abundances of
In October, any comparison between sites was sacri- mites on domatium-bearing leaves resulted from mites
ficed because only two species were sampled from the in domatia and not those on the leaf surface. Even
second garden; however, over four times as many mites within individuals of a single plant species, V. tinus,
(39.7 ? 15.2 individuals per 10 leaves) were found on 17.6% of the variation in mite numbers per leaf was
leaves of plants with domatia as on those without do- explained by domatium number.
matia (9.1 ? 3.6 mites per 10 leaves) (ANOVA, F. 8 Increased mite abundance on leaves with domatia
= 7.5, P = .025). In December, mite abundances were could result from a tendency of mites to stay longer,
eight to ten times higher on plants with domatia com- survive better, or lay more eggs than on leaves without
pared to those without domatia at the two sites (Table domatia. The shelter provided by domatia, acting as
3). Site and site x domatia interaction were not sig- protection from either natural enemies or abiotic stress,
nificant. is the most likely explanation for the increased abun-
If domatia were an important factor determining dance of mites. Although domatia comprise only a
mite abundance on leaves, then subtracting those mites small fraction of total leaf area, they contain most in-
in domatia from totals should result in similar counts 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 in Poland (Kropczynska et al. 1985). Since phytoph-
adults). agous mites were very rare in our gardens, we could
Phytophagous mite populations are often controlled not determine if herbivore numbers were suppressed
by predators (Helle and Sabelis 1985), and the high on leaves with domatia. However, it is unlikely that
predator populations present in these two gardens no plants rely solely on predaceous mites for protection.
doubt contributed to the low numbers of herbivores. Domatia are just one of the many possible defenses
Similarly high predatory and low phytophagous mite against herbivorous mites.
populations on deciduous woody ornamentals that are These results extend beyond initial surveys showing
known to have domatia have been reported from parks 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- Chapter 3.2.13, Woody ornamentals. Pages 385-393 in W.
mark 1991, Willson 1991) by demonstrating a rela- Helle and M. W. Sabelis, editors. Spider mites, their biol-
ogy, natural enemies and control. Elsevier, New York, New
tionship between domatia and higher numbers of po-
York, USA.
tentially beneficial mites on leaves of a wide variety of Lundstrbem, A. N. 1887. Pflanzenbiologische Studien. II.
plants. Although our data do not demonstrate that Die Anpassungen der Pflanzen an Thiere. Nova acta Regiae
plants benefit from increased mite abundance, the po- Societatis scientarum upsaliensis, Series 3, 13:1-87.
O'Dowd, D. J., C. R. Brew, D. C. Christophel, and R. A.
tential for mite-plant mutualism is clear.
Norton. 1991. Mite-plant associations from the Eocene
Acknowledgments: We thank J. Addicott, R. Colwell, of Southern Australia. Science 252:99-101.
O'Dowd, D. J., and M. F. Willson. 1989. Leaf domatia and
B. Downes, R. B. Halliday, E. E. Lindquist, P. W. Price,
mites on Australasian plants: ecological and evolutionary
G. Quinn, and two anonymous referees for comments implications. Biological Journal of the Linnean Society 37:
that improved the manuscript. A. O'Dowd drew Fig. 191-236.
1. This research was supported by the Australian Re- O'Dowd, D. J., and M. F. Willson. 1991. Associations be-
search Council. tween mites and leaf domatia. Trends in Ecology and Evo-
lution 6:179-182.

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