Watermite Parasitism of Corixidae: Infection Parameters, Larval Mite Growth,
Competitive Interaction and Host Response
P. Reilly; T. K. McCarthy
Oikos, Vol. 60, No. 2. (Mar., 1991), pp. 137-148.
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Mon Nov 5 10:53:53 2007
OIKOS 60: 137-148. Copenhagen 1991
Watermite parasitism of Corixidae: infection parameters, larval
mite growth, competitive interaction and host response
P. Reilly and T. K. McCarthy
Reilly, P. and McCarthy, T. K. 1991. Watermite parasitism of Corixidae: infection
parameters, larval mite growth, competitive interaction and host response. - Oikos
60: 137-148.
Parasitism of four corixid species in Lough Corrib, western Ireland, by larval watermites of the genera Hydrachna and Eylais was investigated. Differences in abundances of mite s ~ e c i e swere noted in resDect of host s ~ e c i e sand different samoline
localities. ~nfectionparameters were ndt affected byLhostsize, although host se;
seemed to influence Hydrachna ~arasitism.Partial t e m ~ o r a se~aration
l
of mites was
observed in respect of larval atiachment to hosts and emergdnce of nymphs. The
largest nymphs were generally recorded from the largest hosts and from single
infections. Intraspecific and interspecific competition was evident among parasites
for host nutritive resources and growing space, especially on smaller hosts. The
feeding intensity of parasitised Cymatia bonsdorfi was significantly greater than that
of unparasitised bugs. Increased feeding by parasitised C. bonsdorfi may have been
an attempt to compensate for the effects of nutritional drain by H. conjecta.
P. Reilly (correspondence) and T. K. McCarthy, Dept of Zoology, Univ. College
Galway, Ireland.
Introduction
Species assemblages of lesser waterboatmen (Heteroptera: Corixidae) are typical of the littoral zones of most
European lakes, ponds and slow-flowing rivers. Characteristically these corixids are parasitised by larval watermites (Acari: Hydrachnellae) of the genera Hydrachna
and Eylais. Newly hatched mite larvae either actively
(Hydrachna) or passively (Eylais) contact corixids and
after a period of engorgement, detach from the host as
protonymphs (nymphs). Larval water mites feed on the
host haemolymph, which transfers nutritional reserves
from the fatbody to various organs of the host. It appears that parasitic larval water mites can have a considerable impact on the host. Crisp (1959) recorded
interference with ovarian development as a result of
mite parasitism. Davids and Schoots (1975) and Smith
(1977) observed a reduced mean egg number in mite
parasitised corixids. Martin (1975) suggested a hormoAccepted 2 October 1990
0
OIKOS
10 OIKOS 60:2 (1991)
nal effect, rather than a nutritional drain, as an explanation for mite-induced host castration. Parasitism may
also interfere with flight and flight muscle development
of infected corixids (Simpson 1968, Jansson 1971, Jansson and Scudder 1974, Smith 1977).
The aim of this paper is to describe the parasitic phase
of the life cycles of watermite species infecting corixid
species in Ireland and to examine the principle factors
influencing larval development. The infection parameters for these parasitic larvae are summarised and the
seasonal growth patterns are detailed for four mite species on four host species. Larval mite growth is examined in relation to host size and host sex, number of
mites parasitising and larval attachment sites. The relationships between host feeding and mite parasitism are
examined and the effects of parasitism on host ecology
and behaviour are discussed.
Table 1. The prevalence (P), mean intensity (m1) and abundance (A) of mite species parasitic on four corixid host species. The
frequency (%P) of mite infested bugs, the total numbers of hosts examined (H), mites recorded (M), the range of infection (R) and
the sex ratio (%F, expressed as the percentage of female hosts examined).
Host species
Locality
H. conjecta
P m I
H. cruenta
A
P m I
E. discreta
A
P m I
E. infundibulzfera
A
P m I
A
% p H
M
R
%
S.scotti
Annaghdown
C. bonsdorfi
Hurneys Pt.
Creeve
Mounthenry
Annaghdown
Muckrush
Menlo
Total
S. distincta
Mounthenry
C. panzeri
Mounthenry
Muckrush
Menlo
Total
Localities and methods
Corixid samples were obtained from six localities on
Lough Corrib, western Ireland: Hurneys Pt. (Irish National Grid Reference M254314) and Creeve
(M1354437), located on the western shores of the lake
and Mounthenry (M200486), Annaghdown (M288380),
Muckrush (M288340) and Menlo (M287284, located on
the River Corrib at the outflow from the lake) on the
eastern shores. A t each locality, except Creeve, mud
substrates were predominant, with Chara and Phragmites being the most common vegetation types. Creeve
differed from other localities, being an exposed area
with sandigravel substrate. The main vegetation types at
Creeve were Juncus, Lobelia and Myriophyllum, with
extensive growths of Nostoc during summer months.
Corixids were collected by sweeping a pond-net (300
meshes ~ m - through
~ )
vegetation and over mudisand.
Samples were taken every two weeks during summer
months (1983 and 1984) and thereafter every month.
Using a fine needle, parasitic mite larvae were removed
from the hosts, mounted in lactophenol and left overnight before being identified. All larval mite identifications were based on the descriptions of Lanciani (1969),
Davids (1973)
and Nielsen and Davids (1975). The
~,
parasitological terminology used throughout the text
follows that defined by Margolis et al. (1982). Following
the methods of Lanciani (1971), the area of the dorsum
was used as an estimate of larval mite body size and was
calculated using the formula 0.5 length x 0.5 width x
3.14. All larval or nymphal sizes quoted are in mm'. For
comparison of host size the latter formula was also used
to calculate corixid host dorsum area, as bugs examined
were also approximately elliptical in outline. Cymatia
\
,
bonsdorfi (C. Sahlb.) used in feeding studies were collected at Hurneys Pt., Creeve, Annaghdown and
Menlo. Field and laboratory observations indicated that
Oligochaeta, Cladocera, Copepoda, Gammarus, Diptera and Ephemeroptera were the most likely prey
groups of C. bonsdorfi. Antisera against each of these
prey categories were prepared and an immuno-double
diffusion technique was used to identify these prey prey
groups from the gut contents of bugs (Reilly and
McCarthy 1990). Mite larvae were removed from the
host, prior to serological analysis, and processed as
described above.
Infection parameters
A total of 8099 specimens of four corixid species were
examined for ectoparasitic larval mites. The larvae of
Hydrachna conjecta Koenike, H, cruenta Muller, Eylais
discreta Koenike and E. infundibulifera Koenike were
parasitic on three host species, Sigara scotti (Fieb.), S.
distincta (Fieb.) and Corixa panzeri (Fieb.). Only one
larva of E. infundibulifera was found on the sample of
5385 potential hosts of C. bonsdorfi. Hydrachna conjecta and both Eylais species were parasitic in the subhemelytral air space, H. conjecta larvae attached to the
underside of the hemelytra, while those of Eylais were
found on the abdominal tergites. Larvae of H. cruenta
attached to the outer body surfaces of the host, generally the ventral abdomen, thorax and legs.
Percentages of the four corixid populations infected
by larval watermites varied little between months and
F
Table 2. Chi-square values (derived from Kruskal-Wallis one-way analysis of variance tests) and significance levels for between
host and between sampling locality differences in prevalence, mean intensity and abundance of four mite species (see Table 1).
H. conjecta
H. cruenta
E. discreta
E. infundibulifera
Between host
Prevalence
Mean intensity
Abundance
420.0
54.6
303.2
0.00001
0.00001
0.00001
287.9
14.5
68.6
0.00001
0.01
0.00001
93.5
8.1
16.6
0.00001
0.05
0.01
Between locality
C. bonsdorfi
Prevalence
Mean intensity
Abundance
172.8
20.3
189.9
0.00001
0.01
0.00001
114.3
11.4
81.3
0.00001
0.05
0.00001
98.8
0.00001
31.2
0.00001
55.8
11.3
0.00001
0.01
44.9
14.1
0.00001
0.01
C. punzeri
Prevalence
Abundance
6.3
6.1
0.05
0.05
therefore subsequent analyses were performed on
pooled monthly data. There were highly significant differences between hosts in prevalence, mean intensity
and abundance of each mite species (Tables 1 and 2).
Sigara distincta was most heavily parasitised in terms of
prevalence and abundance of both Hydrachna species.
Hydrachna conjecta was the most abundant parasite on
S. scotti, S. distincta, and C. bonsdorfi (except at
Creeve, where H. cruenta was more abundant), while
C. panzeri had the highest recorded prevalence of E.
discreta and the lowest prevalence of H. conjecta. In the
case of C. bonsdorfi, there were highly significant
(x'= 324.5, p < 0.00001) between sampling locality dif-
498.9
10.7
0.00001
0.01
ferences in the proportion of mite infected bugs (Tables
I and 2). Less than 30% of C. bonsdorfi were parasitised at west-shore localities (Hurneys Pt. and Creeve),
compared to values which were always greater than
38% at east-shore localities. This east-west difference
was also evident in the prevalence of H. conjecta and E.
discreta. At Creeve the prevalence of H. cruenta was at
least twice as great as that from any other locality (Table
1). Significant differences in the prevalence of both
Hydrachna species and E. discreta were also recorded
for C. panzeri from different localities (Table 2). The
prevalence of E. discreta on C. panzeri increased from
Mounthenry through Muckrush to Menlo (representing
Table 3. The numbers and % of each corixid species, from each locality, uninfected o r infected by one, two or three mite species.
The proportion of infected hosts ( % P ) parasitised by one o r more species of larval mites are also included.
Host species
Locality
No. mite species
0
no.
S. scotti
Annaghdown
C. bonsdorfi
Hurneys Pt.
Creeve
Mounthenry
Annaghdown
Muckrush
Menlo
Total
S. distincta
Mounthenry
C. panzeri
Mounthenry
Muckrush
Menlo
Total
1
YO
no.
%
3
2
%P
no.
%
%P
no.
%
%P
Table 4. (A) The observed (Ob.) and expected (Ex.) frequencies of occurrence of larval mite species pairs, for each host species.
Significance levals, calculated from chi-square analyses are indicated.
(B) Spearman rank correlation coefficients (r,) calculated for the relationships between each species pair. The number of cases
(no.) on which correlations were made are included and the significance levals are indicated.
S. scotti
(A)
H. conjectalH. cruenta
1E. discreta
IE. infitndibulifera
H. cruentaIE. discreta
/E. itzfundibulifera
E. discretalE. infundlbulifera
(B)
C. bonsdorfi
S. distincta
C. panzeri
Ob.
Ex.
Ob.
Ex.
Ob.
Ex.
Ob.
Ex
21
11
42.9 * * *
27.8 * * *
113
79
232.3 * * *
169.5 * * *
106
35
134.7 * * *
42.0 *
15
21
36.9 * * *
59.2 * * *
H. cruenta
E. discreta
E. infundibulifera
H . conjecta
r
S.scotti
C. bonsdorfi
S. distincta
C. panzeri
H. cruenta
S. scotti
C. bonsdorfi
S. distincta
C. panzeri
E. discreta
S. scotti
S. distincta
C. panzeri
-0.383
-0.438
-0.277
-0.803
no.
339 * * *
1551 * * *
419 * * *
215 * * *
a north-south gradient in L. Corrib), while the reverse
trend was evident for the prevalence of H. conjecta
(Table 1).
When the sexes were analysed separately with regard
to prevalence some differences were indicated. The
prevalence of H. conjecta on S. scotti was significantly
(x2= 6.1, p < 0.05) greater on females (41.4% infected)
than on males (32.5% infected). Prevalence of H.
cruenta on C. bonsdorfi collected from Annaghdown
was significantly (x2= 9.25, p < 0.003) greater for males
(10.9% infected) than for females (5.7% infected).
Male C. panzeri were more frequently parasitized by H.
conjecta, (18% infected) than females (6.7% infected)
(x2= 39.4, p <0.001) and by H. cruenta where 10.6% of
males were parasitised as opposed to 5.3% of females
(x2= 11.3, p <O.OOl).
Except for one individual of S. distincta all four species of larval mites were not found simultaneously on a
single host. The proportions of infected hosts parasitized by one, two or three mite species were similar for
S. scotti, C. bonsdorfi and C. panzeri (Table 3). Compared to the other three host species, proportionately
fewer S. distincta were infected by one species of mite
only, but a greater proportion of hosts were infected
with two or three mite species (Table 3). For each host
rs
-0.334
-0.395
-0.137
-0.758
no.
331 ***
1509 * * *
373 * *
264 * * *
no.
318 * * *
81 * * *
476 * * *
197 * * *
231 * * *
66 * * *
380 ***
146 * * *
215 * * *
98 * * *
51 * * *
110 * * *
154 * * *
species contingency table analyses were performed on
all pairs of parasite species (Table 4A, no assumptions
were made when calculating expected values for the
heterogeneity test [x2]).For almost all pairs of parasites
analysed the observed numbers of co-occurrences of
species pairs were significantly less than the expected
frequencies (in tests where the minimum expected value
was not less than five). Spearman rank correlation coefficients (two-tailed test of significance), also revealed
negative association between all pairs of parasite species
from each host species (Table 4B).
Hydrachna and Eylais larvae: seasonal growth
and growth in relation to host size and sex
Attachment of H. conjecta larvae to the four host species occurred mainly during July and August, while
attachment of H. cruenta and E. dkcreta was later,
during August and September. Too few E. infundibulifera were recorded to make a definite assessment of
attachment times. The seasonal growth of parasitic larvae is shown in Fig. 1(with mean larval size [expressed
in mm2] being plotted, irrespective of number of mites,
number of mite species or site of attachment of larvae).
Fig. 1. The seasonal growth
of Hydrachna and Eylais
larvae, ectoparasitic on four
corixid host species,
expressed as mean monthly
size (mm2, see Methods).
2.0
l.o
0.5
0,0
A S O N D J F M A M J
A S O N D J F M A M J J A S
O'
1.5
1
J A S
S distinctu 1
E. discreta
1.0
A S O N D J F M A M J J AS
A S O N D J F M A M J J A S
1983
1984
2.0
1.5
1.o
0.5
0.5
0.0
0.0
FMAMJJASONDJFMAMJJASO
A S O N D J F M A M J J AS
FMAMJ 1 AS ONDJ FMAMJ J AS 0
A S O N D J F M A M J J A S
FMAMJ JASONDJ FMAMJ J A S O
A S O N D J F M A M J J A S
1983
1983
1984
1984
Table 5. The mean size (mm2,see Methods) of each corixid host species, the maximum recorded size of each mite species and the
size of the mite relative to the host (expressed as a % of mean host size). Data for H. conjecta refers to emerging nymphs, while
data for other species refers to engorged larvae.
S. scotti
Host size
- mean
- female
- male
H . conjecra
H. cruenta
E. discreta
E. infundibulifera
C. bonsdorfi
S . distincta
C. panzeri
size
size
size
%
size
%
6.90
7.22
6.25
2.44
1.14
0.63
2.59
35.36
16.52
9.13
37.53
3.49
1.84
2.64
**
37.64
19.84
28.47
* Larval H. conjecta attached to S. distincta failed to engorge.
* * C. bonsdorfi was not parasitised by E. infundibulifera.
OIKOS 60:2 (1991)
%
*
2.09
2.88
1.11
14.18
20.31
7.82
4.74
0.17
4.57
1.99
%
18.20
0.65
17.54
7.64
Table 6. The monthly mean size (mm2, see Methods) of H.
conjecta, when only one mite was present, on S. scotti and C.
bonsdorfi. (s.d. = standard deviation, no. = number of hosts
examined.
S. scotti
C. bonsdorfi
H. conjecta
size
s.d.
no.
size
s.d.
no
1983
Aug
S ~ P
Oct
Nov
Dec
1984
Jan
Feb
Mar
Apr 11
"
30
May
Jul
Larval H. conjecta attached to S. distincta failed to grow
and the mean size never exceeded 0.1 mm2. Limited
growth of H. conjecta occurred on the other three host
species during autumn. Hydrachna conjecta larvae attached to C. bonsdorfi did not increase in size during
winter months and a slight decrease in mean larval size
was noted on S. scotti and C. panzeri (Fig. 1 ) . Growth
of H. cruenta larvae was not evident immediately after
attachment, however larval size increased from October
onwards. Resumption of growth of H. conjecta and E.
discreta generally occurred during February. Maximum
H. conjecta larval size was recorded during April and
May and ranged from 0.85 mm2 for larvae from S. scotti,
2.1 mm2 for larvae parasitising C. bonsdorfi and 4.4
mm' from C. panzeri. Hydrachna cruenta nymphs appeared to leave C. bonsdorfi earliest, but at approximately the same time (mid to late April) as H. conjecta
nymphs left S. scotti. Nymphs of E. discreta emerged
earlier than those of H. conjecta on C. panzeri (Muckrush) and C. bonsdorfi (Annaghdown) and earlier than
H. cruenta on S. distincta. Eylais infundibulifera
nymphs had a later emergence period than E. discreta
on both Sigara host species.
The maximum recorded H. conjecta (emerging
nymph) and E. discreta (engorged larval) size increased
with increasing host species size (Table 5). This trend
was also evident for H. cruenta larvae parasitising the
three smaller host species, however the largest individual E. infundibulifera was recorded from S. scotti,
the smallest host species. The size of the parasite species
in proportion to the the size of the host (Table 5) was
almost similar for H. conjecta and H. cruenta infecting
S. scotti and C. bonsdorfi, while the same observation
was true for each Eylais species parasitising the two
larger host species, S. distincta and C. panzeri. The
effect of host size on the seasonal growth of H. conjecta
larvae was examined by comparing the mean monthly
size of larvae parasitising S. scotti and C. bonsdorfi
(Table 6). This analysis was confined to hosts infected
with one mite larva only, thereby eliminating the possible effects of multiple infections on larval growth. O n
each successive month from August (1983) until April
(1984) the mean size of H. conjecta larvae were greater
from C. bonsdorfi, the larger host, even though larvae
attaching during August were of similar size. During
April nymphs emerged earlier from S. scotti, while H.
conjecta parasitising C. bonsdorfi remained on the host
for a longer period of time, emerging as larger nymphs.
The reduced larval size observed during May (Table 6)
could partly be attributed to late developing larvael
nymphs and also to an overall reduction in mean larval
size due to host infection by early attaching larvae.
For each corixid species examined m e a n female size
was greater than mean male size (Table 5). Parasite data
for each sex was therefore analysed separately to determine whether differences existed in larval mite growth
on male and female hosts (this analysis was confined to
hosts infected with one mite larva only). During February, March and April, when larvae were actively growing on the hosts, the mean size of H. conjecta parasitic
on S. scotti was significantly (p<0.05) greater on females (0.796 mm2, s.d. 0.674, n = 55) than on males
(0.464 mm2, s.d. 0.505, n = 48).
Larval growth in relation to number of mites
present
The effects of multiple infections on larval growth was
investigated by comparing mean larval size to number
of attached larvae of all species, during the months
when larvae were actively growing (generally February
to May). The largest Hydrachna and E. discreta larvae
Number of H. conjecto
Fig. 2. Hydrachna conjecta larval size (mm2, see Methods) in
relation to number of larvae infecting S. scotti and C. bonsdorfi, the numbers of hosts examined are also indicated.
Table 7. (A) The mean size (mm2,see Methods) of H. conjecta larvae attached to the left (L) or right (R) hemelytra of S. scotti and
C. bonsdorfi, when either two or three larvae were present.
(B) The mean monthly size of three H. conjecta larvae attached to the left (L) or right (R) hemelytra of C. bonsdorfi
(s.d. = standard deviation, no. = number of hosts examined).
(A)
size
s.d.
(B)
no.
S. scorti
Two H. conjecta
1L + 1R
2L or 2R
C. bonsdorfi
Two H. conjecta
1L + 1R
2L or 2R
2L only
2R only
Three H. conjecta
3 together
3L only
3R only
2-1 division
1L +2R
1L vs.
2L vs.
1R
from C. bonsdorfi and the largest H. conjecta larvae
from S. scotti occurred as single infections and in general, for these two smaller host species, increased larval
numbers resulted in overall reductions in mean larval
size. This phenomenon was evident when the numbers
of H. conjecta larvae, (in the absence of other parasitic
mite species) were plotted against the mean size of the
larvae (Fig. 2, this figure also illustrates the effect of
host size on H. conjecta size). In both instances the
relationships were highly significant (Spearman rank
correlations, r = -0.246, p <0.001 for C. bonsdorfi and
r = -0.403, p <0.001 for S. scotti). The presence of, or
increasing numbers of, E. discreta or H. cruenta larvae,
parasitising C, bonsdorfi, resulted in overall decreased
mean size of H. conjecta larvae (r = -0.089, p <0.01
and r = -0.09, p < 0.05) and while the reciprocal relationships produced similar results, they were not significant. The relationship between the (increasing) numbers of H. cruenta larvae and mean larval size (decreasing) was significant from S. distincta (r = -0.265,
p <0.05). The largest H. conjecta larvae parasitising C.
panzeri were from multiple infections and E. discreta
larvae from the same host showed no decrease in mean
size with increasing infection level.
OIKOS 60:2 (1991)
size
s.d.
no.
C. bonsdorfi
Three H. conjecta
Feb
1L + 2R
1L vs.
2R
2L + 1R
2L vs.
1R
Mar
1L + 2R
1L vs.
2R
2L + 1R
2L vs.
1R
AP~
1L + 2R
1L vs.
2R
2L + l R
2L vs.
1R
Hydrachna conjecta growth in relation to site of
attachment
Hydrachna conjecta larvae were exclusively parasitic on
the ventral sides of the hemelytra of S. scotti and C.
bonsdorfi. Therefore, when two or more larvae infected
a host, the limiting effects of subhemelytral space on
larval growth could be examined by observing growth of
larvae attached to a single hemelytron or when the
larvae were divided between the hemelytra (Table 7A).
For both S. scotti and C. bonsdorfi mean larval size was
greater when the two larvae attached to different hemelytra (as opposed to both larvae being found together,
on either the left or right hemelytron) and in the case of
S. scotti this difference was significant (Mann Whitney
U-Test, p <0.05). Three H. conjecta larvae, exclusive of
other mite species, were present on 43 C. bonsdorfi
examined (Table 7A). When all three larvae were attached to the same hemelytron, their mean size was less
than that for larvae which were divided (2-1) between
the hemelytra. It was however noted that the two larvae
attached to either the left o r right hemelytra had a
greater mean size than the single larva on the opposite
hemelytron. Larvae which were attached to the left
hemelytron (whether all three together, two left and
one right, or the single, left attached, specimen from
triple infections) had a greater mean size when compared to those larvae attached to the right hemelytron.
Table 8. The total numbers and % of positive feeding reactions
recorded from C. bonsdorfi, unparasitised or parasitised by H.
conjecta, from each sampling location (A) and during each
season (B). Chi-square values and significance levals are given
when significant differences were noted.
Unparasitised
Parasitised
(A)
no.
%
no.
Hurneys Pi.
Female
Male
Creeve
Female
Male
Annaghdown
Female
Male
Menlo
Female
Male
Total
Female
Male
(B)
Winter
Female
Male
Spring
Female
Male
Summer
Female
Male
Autumn
Female
Male
209
105
104
46.3
44.7
48.1
52
22
30
90
53
37
48.9
49.1
48.7
12
5
7
131
53
50.6
50.3
51.0
60
36
24
197
108
89
627
344
283
64.2
62.4
66.4
52.2
51.3
53.4
93
48
45
209
105
104
174
89
85
46.3
44.7
48.0
45
22
23
148
72
76
40.5
38.1
43.2
92
52
40
158
97
61
68.4
65.1
74.4
10
7
3
147
86
61
64.2
64.2
64.2
62
24
38
78
x2
Yo
These trends were not as distinct or unidirectional when
data for C. bonsdorfi, infected with three H. conjecta,
was analysed o n a monthly basis (Table 7B), over the
three months of maximum larval growth (the one case
for May was omitted). Hydrachna conjecta as single
infections from C. bonsdorfi also exhibited limited leftright hemelytral size difference, with mean size from the
left hemelytron being 1.105 mm2 (s.d. 0.643, n = 168)
and that from the right being 1.046 mm2 (s.d. 0.632,
n = 218).
Hydrachna conjecta parasitism and feeding by
C. bonsdorfi
A total of 1769 adult C. bonsdorfi were immunologically examined for the presence of six prey categories.
There was no evidence of feeding on Oligochaeta and
only three positive reactions to Gammarus were detected. Diptera was the principal prey group of C. bons-
dorfi, accounting for 91.4% of all positive reactions
recorded. Cladocera, Copepoda and Ephemeroptera
were the prey groups next utilized: accounting for
9.1°/0, 6.1% and 5.5% of all positive reactions respectively. The majority of positive reactions to these prey
groups occurred as double or triple reactions (i.e. where
two or three prey groups were detected simultaneously
from one bug), in which Diptera was also one of the
prey items taken. Therefore the four prey groups were
combined and considered as a single food resource. The
impact of H. conjecta parasitism alone, o n the feeding
of C. bonsdorfi, was investigated as prevalence of H.
cruenta and E. discreta were relatively low (Table 1).
Nymphochrysalid membranes, present on 54 of the bugs
subjected to dietary analysis. indicated that H. conjecta
nymphs had already detached from these hosts and
consequently these bugs were omitted from subsequent
analyses. Therefore, 1552 C. bonsdorfi were subjected
to further analyses, with a El. conjecta prevalence of
22.6%. The mean intensity of infection was 1.515 and
the range 1-6. Prevalence of H. conjecta on male C.
bonsdorfi was 24.5% (n = 702) and 21.2% on females
(n = 850).
There was no difference between male and female C.
bonsdorfi in respect of total feeding, with 55.1% of
males and 52.8% of females giving positive reactions.
There was however, a significant difference in the numbers of positive reactions from parasitised and unparasitised bugs (Table 8A). This relation held when sexes
were considered separately and also when the data for
different sampling localities were analysed independently. A t Creeve, where relatively few C. bonsdorfi were infected by H. conjecta, 3.6% more unparasitised female bugs gave positive reactions than parasitised females. During each season parasitised bugs had a
greater feeding intensity than unparasitised and this
difference was highly significant during spring (Table
8B). When seasonal data for each sex were analysed
independently this difference was significant only for
females during spring (Table 8B). Analyses of individual monthly samples of C. bonsdorfi revealed that
from a total of 43 samples feeding intensity was highest
among parasitised bugs in 32 (74.4%) of these samples.
Discussion
Variations among hosts in mite infection parameters,
such as those described in this paper, have previously
been observed and attributed to the combined effects of
specific differences in mite behaviour as well as differences in the micro-distribution of particular host and
parasite species (Efford 1963). Smith (1977) found that
under equivalent exposure, two Cenocorixa species
were unequally parasitised by four mite species and
therefore relative susceptibility of hosts, and mite
preferences can lead to different levels of infection.
OIKOS 60:2 (1991)
Data presented above suggests that infection parameters may not be greatly affected by differences in
host size, although host sex seemed to influence Hydrachna parasitism, especially in the case of of C. panzeri.
Geographical patterns in mite infections, such as the
overall lower infection levels on C. bonsdorfi from west
shore localities and the north-south gradients in the
prevalence of H. conjecta and E. discreta probably reflect underlying patterns in physical, chemical and biotic
aspects of the littoral habitats of this large and complex
ecosystem. For example, poor growth of submerged
macrophytes at Creeve probably diminished the numbers of suitable oviposition sites for H. conjecta and this
may account for its low prevalence on C. bonsdorfi at
that locality.
The absence of E. infundibulifera as a parasite of L.
Corrib C. bonsdorfi may have resulted from their contrasting biotope preferences. Smith (1977) noted the
preference of Eylais for open water, rather than thick
vegetation in western Canada, while C. bonsdorfi was
always associated with areas of submerged vegetation in
L. Corrib. Adult C. bonsdorfi feed extensively on chironomid larvae in L. Corrib however, first and second
instar nymphs utilize Cladocera to a greater extent than
the adults (Reilly and McCarthy 1990) and may take
smaller invertebrates such as ostracods (Walton 1943).
Free living Eylais adults and nymphs also feed on such
small invertebrates. During summer, when free living
watermites temporarily co-exist with nymphal corixids,
perhaps E. infundibulifera and C. bonsdorfi minimize
competition by occupying different microhabitats, with
consequent diminished encounters between infectious
larvae and potential hosts.
Larval H. conjecta infecting S. distincta failed to grow
and the place of attachment was often marked by a
necrotic spot. Davids (1973) described a similar condition for H. conjecta infecting Sigara falleni (Fieb.), and
concluded that the inhibition of larval growth was as a
result of some unidentified, noncellular haemolymph
component reacting to the mite saliva and obstructing
the development of a normal stylostome. The high susceptibility of S. distincta to infection by Hydrachna larvae (Table 1) was in effect reduced by the failure of H.
conjecta to engorge. Sigara falleni, on which H. conjecta
failed to engorge, also had the highest prevalence of this
mite when compared to two other host species (Davids
1973). Very little growth of H. cruenta occurred on C.
panzeri and this was also the case with E. discreta infecting S. scotti (Table 5). As previously noted C. bonsdorfi was not parasitised by E. infundibulifera. Therefore each of the four hosts examined in this study was
effectively parasitised by only three of the four mite
species.
When compared to other host species examined, the
higher proportion of S. distincta infected by more than
one mite species may be explained in terms of the high
prevalence of Hydrachna species on this host. Multi-
specific parasitism by larval mites was observed from all
host species. Negative associations between pairs of
mite species, and the significantly fewer observed than
expected co-occurrences of mite species pairs (Table 4),
may indicate avoidance of multi-specific parasitism
among larval mites attempting to form associations with
corixid hosts. Smith (1977) considered a lower than
expected rate of multiple interspecific parasitism an indication of avoidance of interspecific competition, but
found no evidence from field or laboratory observations
to suggest such avoidance. Considering the likelihood of
host discovery by mite larvae, Smith (1977) concluded
that it was probably a better strategy to attempt to
outcompete the previously attached mite. Avoidance of
multi-specific parasitism should be evident from smaller
hosts, such as S. scotti and C. bonsdbrfi, in view of the
relatively limited nutritive resources and available
growing space. Similar results from C. panzeri (Table 4)
are more difficult to explain as (discussed below) larger
hosts potentially offer greater resources to parasitic larvae.
All four corixid species examined from L. Corrib had
one generation per year. As adult bugs died off from
mid to late summer, adult mites oviposited and newly
hatched larvae were infectious at approximately the
same time as the new generation adult corixids appeared. A degree of temporal separation in attachment
to the hosts was observed for the various mite species,
with H. conjecta attaching earlier than H. cruenta or E.
discreta. Retarded growth of H. conjecta, during autumn and winter months, was considered to be a diapause by Davids (1973). Such a winter diapause was not
evident for H. cruenta in Lough Corrib and growth of
this species o n the hosts examined (except C. panzeri)
commenced at approximately the same time as H. conjecta and Eylais larvae ceased (winter) growing. Emergence times of nymphs of the four mite species varied
within and between host species. Differences in attachment, growing and emergence times could therefore
minimize interspecific competition for host resources.
Davids (1973) observed that a greater developmental
time was necessary for H. conjecta larvae parasitic on
the smaller of two host species, thus resulting in a prolonged parasitic phase on the smaller host. In L. Corrib,
H. conjecta nymphs detached from S. scotti (the smallest host) earlier and at a smaller size than from C.
bonsdorfi. In view of the limited growth potential available on small hosts it may be a better strategy by H.
conjecta, parasitic on small hosts, to spend a greater
proportion of the life cycle in the free-living nymphal
and adult stages, if adults must reach a certain minimum
size before maturity and, in the case of females, before
egg laying.
Host size was an important factor governing growth
of parasitic larvae and size of emerging nymphs (Table
5) and, in general the largest larvaelnymphs were from
the largest hosts. Lanciani (1971) concluded that growth
of Eylais appeared to be a function of the available
space under the wings of the host and also of host size,
especially for parasites of smaller hosts. Smith (1987)
however, suspected that the nutritive resources of the
host would be limiting before space constraints became
important. The different growth of H. conjecta larvae
from single infections on S. scotti and C. bonsdorfi
(Table 6) during the months immediately after attachment, when larvae were relatively small and subhemelytral space was not limiting, suggests that nutritive resources were indeed more readily available from the
larger host. The size of H. conjecta parasitic on male
and female S. scotti differed during spring when larvae
were reaching them maximum size. This size-difference
most likely resulted from limited subhemelytral space
available on the smaller male hosts. O n the largest host
examined (C. panzeri) subhemelytral space was not limiting and larvae from multiple infections were often
larger than those from single infections. Therefore, for
parasites of smaller hosts, nutritive resources appear to
be the primary factor limiting larval growth, with the
availability of growing space becoming a limiting factor
during the final stages of larval development. For parasites of larger hosts, where subhemelytral space is not
limiting, it would be expected that nutritive resources
would be limiting before space constraints were important.
Based on analyses of the structure of enteric helminth
communities in two populations of bats (Chiroptera)
Lotz and Font (1985) suggested that if two parasite
species compete for a necessary and limited resource
they may also compete with the host for that resource.
Therefore, as a host-helminth association evolves, the
immune response of the host should hold helminth intensities below levels at which exploitation competition
occurs with the host. As a consequence, helminth intensities are held below levels at which competition
would occur between themselves. Although each of the
four corixid species studied was effectively parasitised
by three of four parasite species, there was no evidence
of a host response holding mite intensities below a critical level, and (as discussed in more detail below) there
was evidence of competition between larval mites and
the host for host nutritional reserves. Intraspecific and
interspecific competition between mites was also evident by reduced mean larval size with increasing mite
intensities. Subhemelytral space was a limiting factor
governing parasite growth and this resource may have
been contested (by H. conjecta and Eylais species)
through interference. By partitioning the subhemelytral
space (i.e. attaching to different hemelytra) H. conjecta
larvae (parasitic on the smaller hosts) achieved a greater
size. Larval H. conjecta from multiple infections, irrespective of position on the hemelytra, were always
smaller than those of single infections, suggesting that
competition was not confined t o that for subhemelytral
space alone. Larvae of H. cruenta, parasitic on the
exterior body surfaces of S. distincta, also exhibited a
significant reduction in mean size with increasing in-
tensities. As growing space was not limited on the outer
body surface of the host, these larvae must have been
coapcting with each other for host nutrient alone.
Synergistic interactions between nutrition and parasitism are undoubtedly complex with evidence from diverse host-parasite relationships indicating that the nutritional status of the host must be considered an important variable in host-parasite population dynamics
(Keymer et al. 1983). A parasite harms its host by
reducing the amount of energy available for growth,
reproduction and maintenance functions and therefore
the effect of a parasite is likely to be influenced by the
nutritional status of the host (Lanciani 1975). The frequency of positive feeding reactions recorded from
parasitised or unparasitised C. bonsdorfi were consistently different, suggesting a relationship between parasitism and the level of feeding. Whether this difference
represented actual increased feeding intensity, o r increased nutrient intake, in response to the effects of
parasitism, could not be directly determined using the
~mmunologicaltechnique employed in analysis of the
natural diet of C. bonsdorfi.
The majority of studies on the impact of mite parasitism on corixid or other hemipteran hosts have dealt
with the effects on ovarian development or flight activity. It has been shown with haemolymph parasites of
insects that there is competition between the host tissues and the parasite(s) for the hosts nutritional reserves (Vinsion 1975). In Hemiptera the nutritional reserve is stored as triglyceride and is relayed to the
organs via the haemolymph as diglyceride conjugated
with haemolymph proteins (Chino and Gilbert 1965,
Gilbert 1967, Gilbert and Chino 1974, Thomas 1974).
This lipid reserve seems to be shared by flight muscle
and ovaries, as flight muscle development can sometimes be bypassed during ovarian development (Young
1965). Dispersal and reproduction in insects may also be
temporarily separated because of nutritional competition problems (Dingle 1965, Johnson 1953, Johnson
1969). Therefore, if parasitic mites exert a sufficient
drain on the resources of the host, competition with
ovarian development, flight muscle development and
flight could be expected (Smith 1977). Cymatiu bonsdorfi was generally brachypterous in Lough Corrib, rendering these morphs flightless (eight macropters were
recorded from a total of 5385 specimens examined).
Consequently, the effects of mite parasitism on the
flight activity of C. bonsdorfi was negligible.
The phenomenon of parasite-mediated host castration is not uncommon in invertebrate host-parasite relationships. Moore (1983, and other works cited therein)
noted that female Armadillidium vulgare (Isopoda)
which contained acanthocephalan cystacanths did not
develop ovaries and concluded that the energy demands
placed on the host by the parasite may have exceeded
those allowing ovarian development. Female C. bonsdorfi infected with H. conjecta larvae did not produce
eggs (Reilly 1986). When nymphs detached however (as
indicated by the presence of nymphochrysalid membranes), ovarian development resumed and fully developed eggs were produced. While studying the effects of
mite parasitism on the reproduction and survival of
Hydrometra myrae (Hemiptera: Hydrometridae), Lanciani (1975) demonstrated that higher food levels enabled the host to compensate for parasitic energy losses
and prompted greater egg production. Variations in the
feeding intensity of C. bonsdorfi paralleled seasonal
fluctuations in temperature and densities of available
prey in Lough Corrib (Reilly and McCarthy 1990).
Therefore, the relatively high frequency of positive
feeding reactions, from both parasitised and unparasitised bugs, during summer and autumn, may in part be
attributed to increased water temDeratures and numbers of available prey. The significantly greater proportion of positive feeding reactions from parasitised female C. bonsdorfi during spring, suggests that at the
onset of ovarian development, there was an attempt to
compensate for the effects of parasitism by increased
feeding. The effects of H. conjecta parasitism on the
fitness of male C. bonsdorfi was more difficult to determine. Jaenike (1988) found that male Drosophila testacea parasitised by the nematode Howardula aoronymphium were less successful in mating than unparasitised
males and that females mated with parasitised males
were less likely to produce viable offspring, than those
mated with uninfected males. In view of the overall
feeding intensity of parasitised male bugs, being greater
than that of unparasitised males, it may be assumed that
H. conjecta was exerting some nutritional drain on male
C. bonsdorfi.
The present study has presented data on various aspects of the parasitic phase of watermites and the interactions of the parasites with their hosts. Here we summarise some problems solved and some which the present data may help to approach. Data on infection
parameters indicate that the physical, chemical and
biotic properties of the habitat, the degree of hostparasite interaction at the micro-habitat level, and to a
lesser extent host sex (but not host size) were important
factors influencing mite infection levels. From physical
evidence and previous studies, it was assumed that a
host response prevented engorgement by H. conjecta on
S. distincta. This host response may itself be a response
to a high level of susceptibility o r may have evolved to
allow S. distincta tolerate high encounters between host
and parasite. Avoidance of multi-specific parasitism
may have been occurring on all hoits examined. For
mites attempting to form associations with smaller hosts
this has obvious advantages, for larger hosts it is less
clear, unless mite larvae cannot distinguish between
hosts of different size. Increasing numbers of parasitic
larvae, especially on the smaller hosts, resulted in decreased mean larval size. Evidence of intra- and interspecific competition for host resources has also been
presented. Host nutritive resources were identified as
the primary factor limiting larval growth on smaller
hosts, with growing space limiting during the final stages
of larval development. Differences in times of larval
attachment,
and emergence of nymphs help
minimize competition for these host resources. The earlier emergence time of H. conjecta from S. scotti, the
smallest host, suggests that the parasite may 'trade'
growth at the parasitic stage in the life cycle for growth
in free-living stages. There were indications that H.
conjecta growth was greater on the left hemelytra of C.
bonsdorfi than on the right although, as will be discussed in a future publication, the right hemelytra were
more often infected than the left. By attaching to different hemelytra H. conjecta increased mean larval size,
presumably by reducing competition for growing space,
although this was not supported when triple infections
on C. bonsdorfi were investigated. Perhaps the stylostomes formed by two parasites can compete more efficiently for host nutrient than that formed by a single
larva. Finally this paper has approached the question of
the effects of parasites on host ecology and behaviour
and presents data to suggest that the corixid host may
attempt to compensate for the effects of parasitism by
increased feeding.
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