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Infestation dynamics of Blatticola blattae Graeffe (Nematoda: Thelastomatidae), a parasite of Blattella germanica L. (Dictyoptera: Blattellidae)
lnrernotional Journal/or Printed in Great Brirain
Parasitology
002&7519/92 $5.00 + 0.00 Pergamon Press Lid ‘0 1992 Ausrralian Sociery for Parasrlology
Vol. 22, No. 7, pp. 983-989. 1992
INFESTATION DYNAMICS OF BLA TTICOLA BLATTAE GRAEFFE (NEMATODA: THELASTOMATIDAE), A PARASITE OF BLATTELLA GERMANICA L. (DICTYOPTERA: BLATTELLIDAE) SERGE *Laboratoire
de Biologie
tLaboratoire
d’Ethologie
MORAND*
and COLETTE
RIVAULT~
Animale (CNRS, URA 698), Centre de Biologie et d’Ecologie tropicale et mediterrantenne, Universitt de Perpignan, Avenue Villeneuve, Perpignan, France (CNRS, URA 373), UniversitC de Rennes I, Campus de Beaulieu, 35042-Rennes Cedex, France (Received 30 October 199 1; accepted 20 April 1992)
AbStMCt-MORAND S. and RIVAULT C. 1992.Infestation dynamics of Blafficola blaffae Graeffe (Nematoda: Thelastomatidae), a parasite of Bluffella germanica L. (Dictyoptera: Blattellidae). Infernational Journalfor Parasitology 22: 983-989. The life-cycle of the thelastomatid nematode Blatficola blatfae Graeffe, a parasite of the cockroach Bluffella germanica L., was experimentally studied. Male thelastomatids developed more rapidly than females. Analysis of the distribution of the nematode within a cockroach population revealed an important regulation of parasitic dynamics. The parasites were underdistributed in the samples of the host population. However, they were aggregated in first instar cockroach larvae. The sex ratio was unbalanced, in favour of males in younger cockroach larvae and in favour of females in older cockroaches. Analysis of the variations of this parasitism in relation to spatial structure of the population and host developmental stage revealed that infestation occurred mainly during the first three cockroach larval instars, and can originate from parasites in gravid female hosts. Finally, a strong regulation affects infrapopulations of the parasite, thus limiting males to one and females to one or two per host. These results can be compared with data on oxyurids parasitizing cockroaches of New Zealand.
INDEX
KEY
WORDS:
Blatficola
blattae; Blafiella germanica;
population
dynamics;
sex ratio;
distribution.
ing showed that Blattella germanica populations were distributed in aggregates which remained relatively stable in space and with time (Rivault, 1989, 1990; Rivault & Cloarec, in press).
INTRODUCTION
possess a particular reproduction biology, haplodiploidy. An egg will become a female if it has been fertilized, otherwise it will develop into a male (Adamson, 1989,199O). This reproduction mechanism must surely have some effect on the population dynamics and evolutionary biology of these parasites, but papers on the subject are rare. Zervos (1988a, b, c) presented some particularly interesting data concerning two thelastomatid nematodes, parasites of New Zealand cockroaches. The distribution of these parasites was underdispersed within the cockroach populations, one cockroach never carried more than seven nematodes. Zervos (1988b) also discovered the presence of autoregulation and competition for reproduction within parasitic infrapopulations; these factors produce underdispersion. Another thelastomatid parasite, Blatticola bIattae Graeffe is associated with Blattellagermanica L. These cockroaches are frequently observed in human habitats where they can cause unpleasantness when they pullulate. Previous studies in a swimming bath buildOXYURIDS
The aim of the present distribution this
cockroach
elopmental Possible
study
of the parasite population cycle and
after
under
relationships
of cockroaches
was to investigate
Blatticola
between infestation
blattae
describing
its dev-
laboratory the spatial
the within
conditions. distribution
mechanisms
will
be
discussed. MATERIAL
AND METHODS
Non-infested Bluffella germanica larvae were obtained by isolating ootheca when they reached the final maturation stage (Tanaka, 1976). After these larvae had hatched, absence of infestation was verified. In the laboratory, an experimental infestation was carried out: 50 non-infested Blatfellagermanica larvae (hatched 9 March 1990) were put 1 month later (10 April 1990) with310 infested adults taken from a laboratory population (mean abundance: 2.3 f 0.7 oxyurids per adult). A group of 10 larvae was examined every week and developmental stage and number of parasites 983
984
S.
MORAND and C. RIVAULI
found in their digestive tracts recorded. Hosts became adults 7 weeks after hatching under these experimental conditions and there were six larval instars. Previously samples of a Blattella germanica population (in a swimming bath building) were trapped weekly and preserved in 90% alcohol (Rivault, 1989). Four of these samples (called May, June, August and September 1987) were analysed. The 639 cockroaches from these four samples were sorted according to their developmental stage (six instars) and sex for adults. Oxyurids were collected from the posterior part of the digestive tract and sorted according to their developmental stage (males, females and larvae). The following parasitic characteristics were calculated from the above data: prevalence (proportion of infested hosts, in per cent), abundance (mean number of parasites per host), intensity (number of nematodes in one host) and sex ratio of parasites. in relation to host developmental stage for each of the four samples. All the parasites living in one host were called an infrapopulation. Spatial distribution of parasites in the host population was evaluated using the variance-mean ratio of parasitic abundance. There are three basic types of spatial distribution. (i) A random distribution (or Poisson series); in this model the variance is equal to the mean (a’jm = 1). (ii) A regular distribution (or underdispersion or uniform distribution) when the variance is less than the mean (a’/m < 1). (iii) A contagious distribution (or overdispersion or aggregated distribution) when the variance is greater than the mean (a’/m > I). Comparisons of means, proportions and adjustments to a Poisson series were made using STATITCF programs.
RESULTS
Developmental cycle of the parasite under laborator) conditions Infestation prevalence reached 100% by the end of the observations but maximum intensity was never more than three parasites per host (Table 1). The first oxyurid larvae were found 7 days after non-infested cockroach larvae had been put with infested adults. Male oxyurids appeared between I and 2 weeks after the beginning of the experiment and females appeared after 3 weeks. The first gravid females were observed 5-6 weeks after the beginning of the experiment. The variance-mean ratio was close to 1 for the first three observations, thus indicating a random distribution. This ratio decreased later, as the parasites tended to be distributed more regularly within the experimental group of cockroaches. No cockroach died during the experiment. Infestation characteristics within a cockroach population Infestation characteristics in relation to sample data. Between-sample comparisons of Blattella germanica infestation characteristics (Table 2) revealed the absence of significant differences between prevalences for
TABLE l-INFESTATIONDATAFOR Blattellagermanicaoe~~~~~~ UNDEREXPER~MENTALCONDITIONS(COCKROACHESH~~~~~~ ON 9 MARCH AND HWESTED wm Blatficola bla/tae ON 10 APRIL 1990)
17 April 1990 Number (number Prevalence
of hosts of adult hosts) (%)
Larvae* (range) Females*
24 April 1990 IO
10
10
IO
0
8
10
IO
30
40
50
90
100
0.3 + 0.5
0.3 f 0.5
0. I * 0.3
0.5 * 0.7
(0-l)
(O-1)
(o-1)
(O-2)
(O-1)
0.2 f 0.4
0.2 f 0.4
0.8 jz 0.8
(O-1)
(0-l)
(O-2)
0
0
*Mean abundance
O.lzkO.3
(O-1)
(range)
Variance/mean * standard
18 May 1990
0
0
Total’ (range)
IO May 1990
10
(range) Males*
Dates 2 May 1990
0.4f0.5
0.4zto.7
0.8 f 0.4
0.9 * 0.3
(O-1)
(g-1)
(0-I)
0.3*0.5
0.5f0.7
0.7f0.8
1.6f0.7
2.1*0.5
(@I)
(o-2)
(O-2)
(O-2)
(O-3)
0.85
0.98
0.91
0.30
0.12
deviation
Infestation
loo
dynamics
of B. blame
985
(a)
60 # -60 -1
04 LI
L2
L3
L4
L6
LS
Host developmental
Ll
Adults
stage
L2
L3
L4
L5
Host developmental
L6 Adults
stage
"1 Cd) 6
2
Ll
L2
L3
L4
L5
L6 Adults
Ll
L3
L2
L4
L.5
L6 Adults
>
Host developmental
stage
Host developmental
stage
FIG. 1.Characteristics of the infestation of BlatteNa germanica by Bhtricofa blatme, for each developmental stage of the host (four samples: May (-0-), June (-•-), August (- x -) and September (-•-) 1987); a, prevalence; b, mean abundance; c, distribution pattern (evaluated by the variance-mean ratio of abundance); d, sex ratio (males in relation to females).
TABLE
~-INFESTATION
DATA
FOR
Bialficola
blattae
IN FOUR
SAMPLES
OF
THE
Blattella
germanica
POPULATION
Dates Number
of hosts
Prevalence ( f confidence interval) Mean abundance (+ so) Variance/mean Poisson
May ‘87
June ‘87
180
130
66.6 f 6.9
64.65
1.07f0.95
(Chi square (Probability
=) = )
*for P > 95%
‘87
191
September
‘87
137
69.6h6.5
65.6 f 7.4
1.16iO.94
1.02f0.88
1.09f
0.84
0.76
0.76
0.94
6; 19.8%
no 55.54 0%
no 45.24 0%
no 5.47 17.0%
fit*
8.2
August
1.01
986
S. MORAND and C. RWAULT
the four samples (Standard error, P > 0.05). Similarly, no significant differences were found between the mean parasitic abundances for the four samples (t-test, P > 0.05). Between-sample comparisons of infestation characteristics for each host developmental stage revealed few significant differences (Standard error, P > 0.05) (Fig. la, b, Table 3). The only tendency which seems to emerge from these results concerns L3, L4 and LS instar larvae and for adults. Parasitic prevalence appeared higher in June than in May for L3 and L5 instar larvae and lower for adults and L6 instar larvae. Infestation characteristics in relation to host developmental stage. Pooled data for the four samples (Table 4) showed that total prevalence of Blatticola blattae increased regularly from 25.3% during the first instar (Ll) to 89.6% during the last (adults) host developmental stage. Increases were statistically significant between host instars Ll and L2 and between instars L2 and L3 (Standard error, P < 0.05) (Table 5). Increases of prevalence between two successive older host developmental stages were not significant. The proportion of infested hosts increased during host development, rapidly at first until instar L3, then more slowly. This increase follows an exponential function: Exp M = 0.108 (host developmental stage) + 0.0379, r’ = 0.805. Mean abundance also increased during host development, from 0.39 during instar Ll to 1.58 for adults. Differences between values for two consecutive host developmental stages were significant only between instars L2 and L3. Mean abundance always remained inferior to two nematodes per host. Data related to parasite developmental stage show that the number of parasite larvae decreased as host developmental stage increased, that prevalence of parasite
TABLE ~-SIGNIFICANT
DIFFERENCES BETWEEN INEESTATION DATA
SAMPLES(MAY, JUNE, AUGUST and SEFTEMBER1987)
Prevalence*
Ll
L2
_
May > Sept (2.348)
(U =)
Mean abundance** (0
May > August (2.121)
*Significant difference for P -C 0.05. **Significant difference for P < 0.05 U = value of the standard error. t = Student 1 value.
females increased between host developmental stages L3 and L6, and finally, that the only significant increase in prevalence for parasite males occurred between host developmental stages L2 and L3 (Table 5). Sex of adult hosts significantly influenced neither parasite prevalence (U = 0.541, P > 0.01) nor mean infestation abundance (t = 0.326, P = 0.37). Sex ratio variations. Parasite population dynamics during host development can be summarized as follows: emergence of parasite larvae during the first larval instar (Ll) of the host; parasite males can be found in host larvae from instar L2, and parasite females from host instar L3. The first gravid females were observed in host instar L5 larvae. Adult hosts carried significantly more female than male oxyurids. Prevalence as well as mean abundance differences stressed this discrepancy between parasite males and females (prevalence U: 3.902; P < 0.001, mean abundance t = 5.584, P < 0.001). Therefore parasite sex ratio was unbalanced and in favour of males in young cockroaches until host instar L3 (Table 4, Fig. Id). Later, this trend was reversed and the sex ratio became unbalanced in favour of females in adult cockroaches (Fig. Id). Parasite infrapopulations in adult hosts included at the most two females and one male. Parasite distribution characteristics. The distributions of parasites without taking developmental host stage into account within the four samples were underdispersed (Table 2). The distributions of parasites in relation to host developmental stage never followed a Poisson series (Table 3), although the distribution of parasites among host L2 larvae was the distribution which came the closest to a Poisson series
(PREVALENCE AND MEAN ABUNDANCE OF Blatticoia bluttae), FOR EACH DEVELOPMENTAL STAFEOF Blattella germanica
Host developmental stage L4 L3
L5
May > June (2.159) August r June (2.113)
May > June (2.454)
May > June (2.197) May>Sept (2.197)
August r June (2.497)
May > June (3.217) August > June (2.371)
_
L6
June>May (2.092)
LN I-‘OUR
Adults
June>May (2.57)
Infestation TABLE 4-INFESTATIONDATAFOR
dynamics
Blatticolablattae
Ll
L2
L3
95
61
100
987
of B. blattae
LNRELATIONTO Blattellagermanica
Host developmental stage L4 L5
DEVELOPMENTALSTAGE
L6
Males
Females
103
50
48
Number
of hosts
Larvae Prevalence* Mean abundance**
25.5168.7 0.39zkO.87
29.5zk 11.7 0.34*0.57
28.0zk8.2 0.38zkO.69
(O-5)
(O-2)
(o-3)
0 0 _
0 0 _
25.Ozk8.5 0.25f0.44
0 0 _
19.7f 10.0 0.2OrtO.40
40.0f9.6 0.41f0.51
(range) Females Prevalence Mean abundance (range) Males Prevalence Mean abundance (range) TO101 Prevalence Mean abundance (range)
(O-1)
89
93
6.3f6.8 0.06f0.25
15.1rt7.3 0.16zkO.40
14.5zk7.8 0.15zkO.35
10.0f 8.3 O.lOf0.30
(O-2)
(O-1)
(O-1)
(0-l)
58.lflO.O 0.65zkO.62
71.9f8.7 0.82zkO.59
80.0+11.1 l.OzkO.64
77.1~k11.9 0.92*0.61
(O-2)
(O-3)
(O-2)
(O-2)
(o-2)
46.lf 10.4 0.46f0.50
49.5f 10.2 0.51~110.52
48.5zk9.7 0.491tOo.50
46.0* 13.8 0.46zkO.50
58.3* 13.9 0.6OzkO.54
(O-1)
(O-2)
(o-1)
(O-1)
(O-2)
23.6zk8.8 0.27*0.52 (O-2)
42.7zk10.3 0.46f0.27
(o-1)
(o-2)
25.5zk8.7 0.39zkO.87
42.6f 12.4 0.53zkO.67
68.Oh9.1 1.04zkO.88
70.7*9.4 1.18*0.98
79.6zk8.2 1.28~kO.84
(O-5)
(o-2)
(o-3)
(04)
(O-3)
(O-3)
(04)
(O-3)
_
1.64
I .oo
0.78
0.60
0.46
0.66
0.87
0.74
0.82
0.55
0.48
0.55
0.45
:.;2 13.44
?I?:5 0.04
no 9.65 4.00
no 12.39 I .73
Sex ratio Variance/mean
1.93
Poisson fit*** (Chi-square =) (P% =)
no
no
no
5.53 19.78
1.28 80.4
7.83 9.04
84.5f7.0 1.45f0.84
no 33 0
86.0f9.6 1.56k0.93
89.6&8.7 1.58f0.85
* f Confidence interval. ** f Standard deviation. ***For P > 95%.
(80.4%). Parasites in Ll cockroach larvae follow an aggregative distribution (?/WI = 1.93) and data for the May and September samples confirm this observation (Fig. lc). Parasite distributions are underdispersed with older developmental stages of host (Fig. Ic and Table 3). DISCUSSION
In the laboratory as well as in the cockroach’s natural urban habitat, parasite males developed more rapidly. This phenomenon of male progenesis is well known in Oxyuridae and could be related to haplodiploidy in this group (Adamson, 1989). Under laboratory conditions 5-6 weeks were necessary for a thelastomatid to develop into a gravid female, and under the same conditions development of the host Blattella germanica lasted between 7 and 8 weeks from hatching until the imaginal moult. Considering these developmental periods it seems obvious that under natural conditions gravid parasite females will be
found only in hosts of older developmental stages. To understand infestation dynamics it is necessary to recall some ecological facts concerning the host’s population dynamics. The Blattella germanica population studied was distributed in aggregates. Each aggregate included in the centre a high proportion of young larvae (instars Ll and L2) and gravid females. Medium-stage larvae (L3, L4 and L5) were observed more often near the edges of the aggregate whereas older larvae (L6), males and non-gravid females returned towards the centre of the aggregate (Rivault, 1989, 1990). Parasite population dynamics in relation to host developmental stage as well as in relation to sample date appear quite stable. The infestation period occurs mainly during the first. cockroach developmental stages as nearly 70% of instar 3 larvae were infested and that mean abundance was already equal to one nematode per host as compared to the maximum of 1.6 in adults. Therefore, it appears very likely that the first
988
S,MORAND TABLE ~-VARIATIONS
andC.
RIVAULT
OF PREVALENCE AND MEAN ABUNDANCE
Blattellagermanicu
Ll/L2
OF Blutticolo blattae IN RELATION TO
DEVELOPMENTALSTAGE(FORALLSAMPLESI
Host developmental L2/L3 L3/L4
stage L4/L5
LS/M
LhjAdults
L&WC&?
Prevalence* u P Mean abundance** P Females Prevalence lJ P Mean abundance
ll0
0.k
0.205 0.419 no 0.64 0.260
0.275 no 0.23 0.408
0.245 no 1.44 0.076
Yes 2.576 0.005
2n;7 0.129
P Males Prevalence U P Mean abundance
-
_
P Total Prevalence I: P Mean abundance P
050
Ofl"28
IT9 0.070
0.41 0.343
yes 2.070 0.019 yes 2.105 0.019
yes 2.020 0.022
no 0.128 0.449 no 0.45 0.329
0.841 0.200
no 0.458 0.324
Yes 3.29
on;7 0.394
0.73 0.234
ozo 0.339 no 0.425 0.34
123 0.085 no 0.78 0.21
Yes
(10
I10
yes 3.169 to.001 Yes 4.94
0.898 n0
2.676 0.004
yes 2.267 0.012 no I .04 0.15
no 1.430 0.077
yes 1.86 0.031
no 1.42 0.077 no 1.62 0.054
no 1.103 0.135 no
I .47 0.072
no 0.49 0.310 II0
0.82 0.209
no 0.894 0.186
O& 0.323
;‘;5 0.13
1.06 0.15
110
*Significant difference for P < 0.05%. **Significant difference for P
explained by death of highly infested hosts, as no mortality due to parasites was recorded in the hosts raised in the laboratory. This is consistent with the effects of other oxyurids which are not generaffy highly pathogenic for their invertebrate hosts (Poinar, 1975). On the contrary, McCallister (1988) reported that Prriplaneta americana cockroaches were larger and heavier when they carried thelastomatids than when they were not infested. Regulation of 3~attic~~ff hlattae infestation dynamics must therefore be explained as being the result of intraspecific competition for limited space (the digestive tract) and resources (bacteria). This appears to be the case for Periplaneta amerirana because females are larger than males but they also carry more
Infestation
dynamics
parasites (McCallister, 1988). However, although weights of male and female Bluttellu germanica differ significantly (Rivault, pers. obs.) there are no significant differences in infestation. Blatticola blattae males are particularly affected. Although they are much smaller than females (they measure approximately one-third of the length of females), an infrapopulation never includes more than one Blutticola blattae male. Zervos’ observations are similar for the same oxyurid species (Zervos, 1988~). This is also the case for the oxyurid Leidynema appendiculatum, a parasite of Periplaneta americana (Hominick & Davey, 1972). It is not rare to observe only Blatticola blattae females alone; this occurs in several other thelastomatids (Adamson, 1989). Zervos (1988b) recorded the presence of a regulation, at the infrapopulation level, which affected male as well as female thelastomatids. She supposed that there was competition between females for limited resources and between males to inseminate females. Zervos (1988b) suggested that the first male to mature in one host inhibited, by secreting an anthelminthic substance, the development of all other individuals of the same sex. This sort of competition could explain, moreover, the phenomenon of progenesis in males. Indeed, the males that developed the most quickly would have an advantage in this type of competition. The phenomenon of regulation of Blatticola blattae populations appears from this point of view similar to that described by Zervos (1988a, b, c) although it seems that limitation of the number of females is not due solely to competition for trophic resources. In addition, taking into account the spatial structure of host populations it appears that infestation of young hosts occurs mainly through oxyurids carried by gravid females. This observation, if it is confirmed, shows that inbreeding has been promoted greatly in this thelastomatid. Several questions still remain unanswered, especially concerning the way female oxyurids control their sex ratio in the presence of a male and concerning mechanisms regulating infrapopulations. Mechanisms limiting the number of males could be the result of an ESS (Evolutionary Stable Strategy) related to the haplodiploidy in this group, which could evaluate the number of males needed to inseminate all the females according to Hamilton’s (1967) theory.
of B. blattae
989
Acknowiedgements~We are particularly indebted to J.P. Hugot and P. Deleporte for comments and criticisms of earlier drafts of the paper. We thank J. Menou for technical assistance and A. Cloarec for the English translation.
REFERENCES ADAMSONM. L. 1989. Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Advances in Parasitology 28: i75-228. ADAMSON M. L. 1990. Haplodiploidy in the Oxyurida: decoupling the evolutionary processes of adaptation and speciation. Annales de Parasitologie Humaine et Compare% 65, Suppl. I: 31-35. HAMILTONW. D. 1967. Extraordinary sex ratios. Science 156: 477488. HOMINICKW. M. & DAVEY K. G. 1972. The influence of host stage and sex upon the size and composition of two species of thelastomatids parasitic in the hindgut of Periplaneta americana. Canadian Journal of Zoology 50: 1421-1432. KEYMER A. E. 1982. Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84: 537-582. MCCALLSTERG. M. 1988. The effect of Thelastoma Mhoesi and Hammerschmidtiella diesingi (Nematoda: Oxyurida) on host size and physiology in Periplaneta americuna (Arthropoda: Blattidae). Proceedings qf the Helminrhological Society of Washington 55: 12-14. POINARG. 0. 1975. Entomogenous Nematodes. E. J. Brill, Leiden. RIVAULT C. 1989. Spatial distribution of the cockroach, Biattella germanica, in a swimming-bath facility. Entomologia Experimentalis applicata 53: 247-255. RIVAULT C. 1990. Distribution dynamics of Blattella germanica, in a closed urban environment. Entomologia E?cperimentalis applicata 51: 85-9 1. RIVAULT C. & CLOAREC A. (in press) Food stealing in cockroaches. Journal ofEthology. TANAKAA. 1976. Stages in the embryonic development of the German cockroach Blaitella germanica L. Kontyli (Tokyo) 44: 512-525. ZERVOS S. 1988a. Population dynamics of a thelastomatid nematode of cockroaches. Parasito/ogy 96: 353-368. ZBRVOS S. 1988b. Evidence for population self-regulation, reproductive competition and arrhenotoky in a thelastomatid nematode of cockroaches. Parasitology 96: 369% 379. ZERVOS S. 1988~. Population regulation in parasitic nematodes (Thelastomatidae) of cockroaches. New, Zealand Journal qf Zoology 15: 335-338.
Parasitology
002&7519/92 $5.00 + 0.00 Pergamon Press Lid ‘0 1992 Ausrralian Sociery for Parasrlology
Vol. 22, No. 7, pp. 983-989. 1992
INFESTATION DYNAMICS OF BLA TTICOLA BLATTAE GRAEFFE (NEMATODA: THELASTOMATIDAE), A PARASITE OF BLATTELLA GERMANICA L. (DICTYOPTERA: BLATTELLIDAE) SERGE *Laboratoire
de Biologie
tLaboratoire
d’Ethologie
MORAND*
and COLETTE
RIVAULT~
Animale (CNRS, URA 698), Centre de Biologie et d’Ecologie tropicale et mediterrantenne, Universitt de Perpignan, Avenue Villeneuve, Perpignan, France (CNRS, URA 373), UniversitC de Rennes I, Campus de Beaulieu, 35042-Rennes Cedex, France (Received 30 October 199 1; accepted 20 April 1992)
AbStMCt-MORAND S. and RIVAULT C. 1992.Infestation dynamics of Blafficola blaffae Graeffe (Nematoda: Thelastomatidae), a parasite of Bluffella germanica L. (Dictyoptera: Blattellidae). Infernational Journalfor Parasitology 22: 983-989. The life-cycle of the thelastomatid nematode Blatficola blatfae Graeffe, a parasite of the cockroach Bluffella germanica L., was experimentally studied. Male thelastomatids developed more rapidly than females. Analysis of the distribution of the nematode within a cockroach population revealed an important regulation of parasitic dynamics. The parasites were underdistributed in the samples of the host population. However, they were aggregated in first instar cockroach larvae. The sex ratio was unbalanced, in favour of males in younger cockroach larvae and in favour of females in older cockroaches. Analysis of the variations of this parasitism in relation to spatial structure of the population and host developmental stage revealed that infestation occurred mainly during the first three cockroach larval instars, and can originate from parasites in gravid female hosts. Finally, a strong regulation affects infrapopulations of the parasite, thus limiting males to one and females to one or two per host. These results can be compared with data on oxyurids parasitizing cockroaches of New Zealand.
INDEX
KEY
WORDS:
Blatficola
blattae; Blafiella germanica;
population
dynamics;
sex ratio;
distribution.
ing showed that Blattella germanica populations were distributed in aggregates which remained relatively stable in space and with time (Rivault, 1989, 1990; Rivault & Cloarec, in press).
INTRODUCTION
possess a particular reproduction biology, haplodiploidy. An egg will become a female if it has been fertilized, otherwise it will develop into a male (Adamson, 1989,199O). This reproduction mechanism must surely have some effect on the population dynamics and evolutionary biology of these parasites, but papers on the subject are rare. Zervos (1988a, b, c) presented some particularly interesting data concerning two thelastomatid nematodes, parasites of New Zealand cockroaches. The distribution of these parasites was underdispersed within the cockroach populations, one cockroach never carried more than seven nematodes. Zervos (1988b) also discovered the presence of autoregulation and competition for reproduction within parasitic infrapopulations; these factors produce underdispersion. Another thelastomatid parasite, Blatticola bIattae Graeffe is associated with Blattellagermanica L. These cockroaches are frequently observed in human habitats where they can cause unpleasantness when they pullulate. Previous studies in a swimming bath buildOXYURIDS
The aim of the present distribution this
cockroach
elopmental Possible
study
of the parasite population cycle and
after
under
relationships
of cockroaches
was to investigate
Blatticola
between infestation
blattae
describing
its dev-
laboratory the spatial
the within
conditions. distribution
mechanisms
will
be
discussed. MATERIAL
AND METHODS
Non-infested Bluffella germanica larvae were obtained by isolating ootheca when they reached the final maturation stage (Tanaka, 1976). After these larvae had hatched, absence of infestation was verified. In the laboratory, an experimental infestation was carried out: 50 non-infested Blatfellagermanica larvae (hatched 9 March 1990) were put 1 month later (10 April 1990) with310 infested adults taken from a laboratory population (mean abundance: 2.3 f 0.7 oxyurids per adult). A group of 10 larvae was examined every week and developmental stage and number of parasites 983
984
S.
MORAND and C. RIVAULI
found in their digestive tracts recorded. Hosts became adults 7 weeks after hatching under these experimental conditions and there were six larval instars. Previously samples of a Blattella germanica population (in a swimming bath building) were trapped weekly and preserved in 90% alcohol (Rivault, 1989). Four of these samples (called May, June, August and September 1987) were analysed. The 639 cockroaches from these four samples were sorted according to their developmental stage (six instars) and sex for adults. Oxyurids were collected from the posterior part of the digestive tract and sorted according to their developmental stage (males, females and larvae). The following parasitic characteristics were calculated from the above data: prevalence (proportion of infested hosts, in per cent), abundance (mean number of parasites per host), intensity (number of nematodes in one host) and sex ratio of parasites. in relation to host developmental stage for each of the four samples. All the parasites living in one host were called an infrapopulation. Spatial distribution of parasites in the host population was evaluated using the variance-mean ratio of parasitic abundance. There are three basic types of spatial distribution. (i) A random distribution (or Poisson series); in this model the variance is equal to the mean (a’jm = 1). (ii) A regular distribution (or underdispersion or uniform distribution) when the variance is less than the mean (a’/m < 1). (iii) A contagious distribution (or overdispersion or aggregated distribution) when the variance is greater than the mean (a’/m > I). Comparisons of means, proportions and adjustments to a Poisson series were made using STATITCF programs.
RESULTS
Developmental cycle of the parasite under laborator) conditions Infestation prevalence reached 100% by the end of the observations but maximum intensity was never more than three parasites per host (Table 1). The first oxyurid larvae were found 7 days after non-infested cockroach larvae had been put with infested adults. Male oxyurids appeared between I and 2 weeks after the beginning of the experiment and females appeared after 3 weeks. The first gravid females were observed 5-6 weeks after the beginning of the experiment. The variance-mean ratio was close to 1 for the first three observations, thus indicating a random distribution. This ratio decreased later, as the parasites tended to be distributed more regularly within the experimental group of cockroaches. No cockroach died during the experiment. Infestation characteristics within a cockroach population Infestation characteristics in relation to sample data. Between-sample comparisons of Blattella germanica infestation characteristics (Table 2) revealed the absence of significant differences between prevalences for
TABLE l-INFESTATIONDATAFOR Blattellagermanicaoe~~~~~~ UNDEREXPER~MENTALCONDITIONS(COCKROACHESH~~~~~~ ON 9 MARCH AND HWESTED wm Blatficola bla/tae ON 10 APRIL 1990)
17 April 1990 Number (number Prevalence
of hosts of adult hosts) (%)
Larvae* (range) Females*
24 April 1990 IO
10
10
IO
0
8
10
IO
30
40
50
90
100
0.3 + 0.5
0.3 f 0.5
0. I * 0.3
0.5 * 0.7
(0-l)
(O-1)
(o-1)
(O-2)
(O-1)
0.2 f 0.4
0.2 f 0.4
0.8 jz 0.8
(O-1)
(0-l)
(O-2)
0
0
*Mean abundance
O.lzkO.3
(O-1)
(range)
Variance/mean * standard
18 May 1990
0
0
Total’ (range)
IO May 1990
10
(range) Males*
Dates 2 May 1990
0.4f0.5
0.4zto.7
0.8 f 0.4
0.9 * 0.3
(O-1)
(g-1)
(0-I)
0.3*0.5
0.5f0.7
0.7f0.8
1.6f0.7
2.1*0.5
(@I)
(o-2)
(O-2)
(O-2)
(O-3)
0.85
0.98
0.91
0.30
0.12
deviation
Infestation
loo
dynamics
of B. blame
985
(a)
60 # -60 -1
04 LI
L2
L3
L4
L6
LS
Host developmental
Ll
Adults
stage
L2
L3
L4
L5
Host developmental
L6 Adults
stage
"1 Cd) 6
2
Ll
L2
L3
L4
L5
L6 Adults
Ll
L3
L2
L4
L.5
L6 Adults
>
Host developmental
stage
Host developmental
stage
FIG. 1.Characteristics of the infestation of BlatteNa germanica by Bhtricofa blatme, for each developmental stage of the host (four samples: May (-0-), June (-•-), August (- x -) and September (-•-) 1987); a, prevalence; b, mean abundance; c, distribution pattern (evaluated by the variance-mean ratio of abundance); d, sex ratio (males in relation to females).
TABLE
~-INFESTATION
DATA
FOR
Bialficola
blattae
IN FOUR
SAMPLES
OF
THE
Blattella
germanica
POPULATION
Dates Number
of hosts
Prevalence ( f confidence interval) Mean abundance (+ so) Variance/mean Poisson
May ‘87
June ‘87
180
130
66.6 f 6.9
64.65
1.07f0.95
(Chi square (Probability
=) = )
*for P > 95%
‘87
191
September
‘87
137
69.6h6.5
65.6 f 7.4
1.16iO.94
1.02f0.88
1.09f
0.84
0.76
0.76
0.94
6; 19.8%
no 55.54 0%
no 45.24 0%
no 5.47 17.0%
fit*
8.2
August
1.01
986
S. MORAND and C. RWAULT
the four samples (Standard error, P > 0.05). Similarly, no significant differences were found between the mean parasitic abundances for the four samples (t-test, P > 0.05). Between-sample comparisons of infestation characteristics for each host developmental stage revealed few significant differences (Standard error, P > 0.05) (Fig. la, b, Table 3). The only tendency which seems to emerge from these results concerns L3, L4 and LS instar larvae and for adults. Parasitic prevalence appeared higher in June than in May for L3 and L5 instar larvae and lower for adults and L6 instar larvae. Infestation characteristics in relation to host developmental stage. Pooled data for the four samples (Table 4) showed that total prevalence of Blatticola blattae increased regularly from 25.3% during the first instar (Ll) to 89.6% during the last (adults) host developmental stage. Increases were statistically significant between host instars Ll and L2 and between instars L2 and L3 (Standard error, P < 0.05) (Table 5). Increases of prevalence between two successive older host developmental stages were not significant. The proportion of infested hosts increased during host development, rapidly at first until instar L3, then more slowly. This increase follows an exponential function: Exp M = 0.108 (host developmental stage) + 0.0379, r’ = 0.805. Mean abundance also increased during host development, from 0.39 during instar Ll to 1.58 for adults. Differences between values for two consecutive host developmental stages were significant only between instars L2 and L3. Mean abundance always remained inferior to two nematodes per host. Data related to parasite developmental stage show that the number of parasite larvae decreased as host developmental stage increased, that prevalence of parasite
TABLE ~-SIGNIFICANT
DIFFERENCES BETWEEN INEESTATION DATA
SAMPLES(MAY, JUNE, AUGUST and SEFTEMBER1987)
Prevalence*
Ll
L2
_
May > Sept (2.348)
(U =)
Mean abundance** (0
May > August (2.121)
*Significant difference for P -C 0.05. **Significant difference for P < 0.05 U = value of the standard error. t = Student 1 value.
females increased between host developmental stages L3 and L6, and finally, that the only significant increase in prevalence for parasite males occurred between host developmental stages L2 and L3 (Table 5). Sex of adult hosts significantly influenced neither parasite prevalence (U = 0.541, P > 0.01) nor mean infestation abundance (t = 0.326, P = 0.37). Sex ratio variations. Parasite population dynamics during host development can be summarized as follows: emergence of parasite larvae during the first larval instar (Ll) of the host; parasite males can be found in host larvae from instar L2, and parasite females from host instar L3. The first gravid females were observed in host instar L5 larvae. Adult hosts carried significantly more female than male oxyurids. Prevalence as well as mean abundance differences stressed this discrepancy between parasite males and females (prevalence U: 3.902; P < 0.001, mean abundance t = 5.584, P < 0.001). Therefore parasite sex ratio was unbalanced and in favour of males in young cockroaches until host instar L3 (Table 4, Fig. Id). Later, this trend was reversed and the sex ratio became unbalanced in favour of females in adult cockroaches (Fig. Id). Parasite infrapopulations in adult hosts included at the most two females and one male. Parasite distribution characteristics. The distributions of parasites without taking developmental host stage into account within the four samples were underdispersed (Table 2). The distributions of parasites in relation to host developmental stage never followed a Poisson series (Table 3), although the distribution of parasites among host L2 larvae was the distribution which came the closest to a Poisson series
(PREVALENCE AND MEAN ABUNDANCE OF Blatticoia bluttae), FOR EACH DEVELOPMENTAL STAFEOF Blattella germanica
Host developmental stage L4 L3
L5
May > June (2.159) August r June (2.113)
May > June (2.454)
May > June (2.197) May>Sept (2.197)
August r June (2.497)
May > June (3.217) August > June (2.371)
_
L6
June>May (2.092)
LN I-‘OUR
Adults
June>May (2.57)
Infestation TABLE 4-INFESTATIONDATAFOR
dynamics
Blatticolablattae
Ll
L2
L3
95
61
100
987
of B. blattae
LNRELATIONTO Blattellagermanica
Host developmental stage L4 L5
DEVELOPMENTALSTAGE
L6
Males
Females
103
50
48
Number
of hosts
Larvae Prevalence* Mean abundance**
25.5168.7 0.39zkO.87
29.5zk 11.7 0.34*0.57
28.0zk8.2 0.38zkO.69
(O-5)
(O-2)
(o-3)
0 0 _
0 0 _
25.Ozk8.5 0.25f0.44
0 0 _
19.7f 10.0 0.2OrtO.40
40.0f9.6 0.41f0.51
(range) Females Prevalence Mean abundance (range) Males Prevalence Mean abundance (range) TO101 Prevalence Mean abundance (range)
(O-1)
89
93
6.3f6.8 0.06f0.25
15.1rt7.3 0.16zkO.40
14.5zk7.8 0.15zkO.35
10.0f 8.3 O.lOf0.30
(O-2)
(O-1)
(O-1)
(0-l)
58.lflO.O 0.65zkO.62
71.9f8.7 0.82zkO.59
80.0+11.1 l.OzkO.64
77.1~k11.9 0.92*0.61
(O-2)
(O-3)
(O-2)
(O-2)
(o-2)
46.lf 10.4 0.46f0.50
49.5f 10.2 0.51~110.52
48.5zk9.7 0.491tOo.50
46.0* 13.8 0.46zkO.50
58.3* 13.9 0.6OzkO.54
(O-1)
(O-2)
(o-1)
(O-1)
(O-2)
23.6zk8.8 0.27*0.52 (O-2)
42.7zk10.3 0.46f0.27
(o-1)
(o-2)
25.5zk8.7 0.39zkO.87
42.6f 12.4 0.53zkO.67
68.Oh9.1 1.04zkO.88
70.7*9.4 1.18*0.98
79.6zk8.2 1.28~kO.84
(O-5)
(o-2)
(o-3)
(04)
(O-3)
(O-3)
(04)
(O-3)
_
1.64
I .oo
0.78
0.60
0.46
0.66
0.87
0.74
0.82
0.55
0.48
0.55
0.45
:.;2 13.44
?I?:5 0.04
no 9.65 4.00
no 12.39 I .73
Sex ratio Variance/mean
1.93
Poisson fit*** (Chi-square =) (P% =)
no
no
no
5.53 19.78
1.28 80.4
7.83 9.04
84.5f7.0 1.45f0.84
no 33 0
86.0f9.6 1.56k0.93
89.6&8.7 1.58f0.85
* f Confidence interval. ** f Standard deviation. ***For P > 95%.
(80.4%). Parasites in Ll cockroach larvae follow an aggregative distribution (?/WI = 1.93) and data for the May and September samples confirm this observation (Fig. lc). Parasite distributions are underdispersed with older developmental stages of host (Fig. Ic and Table 3). DISCUSSION
In the laboratory as well as in the cockroach’s natural urban habitat, parasite males developed more rapidly. This phenomenon of male progenesis is well known in Oxyuridae and could be related to haplodiploidy in this group (Adamson, 1989). Under laboratory conditions 5-6 weeks were necessary for a thelastomatid to develop into a gravid female, and under the same conditions development of the host Blattella germanica lasted between 7 and 8 weeks from hatching until the imaginal moult. Considering these developmental periods it seems obvious that under natural conditions gravid parasite females will be
found only in hosts of older developmental stages. To understand infestation dynamics it is necessary to recall some ecological facts concerning the host’s population dynamics. The Blattella germanica population studied was distributed in aggregates. Each aggregate included in the centre a high proportion of young larvae (instars Ll and L2) and gravid females. Medium-stage larvae (L3, L4 and L5) were observed more often near the edges of the aggregate whereas older larvae (L6), males and non-gravid females returned towards the centre of the aggregate (Rivault, 1989, 1990). Parasite population dynamics in relation to host developmental stage as well as in relation to sample date appear quite stable. The infestation period occurs mainly during the first. cockroach developmental stages as nearly 70% of instar 3 larvae were infested and that mean abundance was already equal to one nematode per host as compared to the maximum of 1.6 in adults. Therefore, it appears very likely that the first
988
S,MORAND TABLE ~-VARIATIONS
andC.
RIVAULT
OF PREVALENCE AND MEAN ABUNDANCE
Blattellagermanicu
Ll/L2
OF Blutticolo blattae IN RELATION TO
DEVELOPMENTALSTAGE(FORALLSAMPLESI
Host developmental L2/L3 L3/L4
stage L4/L5
LS/M
LhjAdults
L&WC&?
Prevalence* u P Mean abundance** P Females Prevalence lJ P Mean abundance
ll0
0.k
0.205 0.419 no 0.64 0.260
0.275 no 0.23 0.408
0.245 no 1.44 0.076
Yes 2.576 0.005
2n;7 0.129
P Males Prevalence U P Mean abundance
-
_
P Total Prevalence I: P Mean abundance P
050
Ofl"28
IT9 0.070
0.41 0.343
yes 2.070 0.019 yes 2.105 0.019
yes 2.020 0.022
no 0.128 0.449 no 0.45 0.329
0.841 0.200
no 0.458 0.324
Yes 3.29
on;7 0.394
0.73 0.234
ozo 0.339 no 0.425 0.34
123 0.085 no 0.78 0.21
Yes
(10
I10
yes 3.169 to.001 Yes 4.94
0.898 n0
2.676 0.004
yes 2.267 0.012 no I .04 0.15
no 1.430 0.077
yes 1.86 0.031
no 1.42 0.077 no 1.62 0.054
no 1.103 0.135 no
I .47 0.072
no 0.49 0.310 II0
0.82 0.209
no 0.894 0.186
O& 0.323
;‘;5 0.13
1.06 0.15
110
*Significant difference for P < 0.05%. **Significant difference for P
explained by death of highly infested hosts, as no mortality due to parasites was recorded in the hosts raised in the laboratory. This is consistent with the effects of other oxyurids which are not generaffy highly pathogenic for their invertebrate hosts (Poinar, 1975). On the contrary, McCallister (1988) reported that Prriplaneta americana cockroaches were larger and heavier when they carried thelastomatids than when they were not infested. Regulation of 3~attic~~ff hlattae infestation dynamics must therefore be explained as being the result of intraspecific competition for limited space (the digestive tract) and resources (bacteria). This appears to be the case for Periplaneta amerirana because females are larger than males but they also carry more
Infestation
dynamics
parasites (McCallister, 1988). However, although weights of male and female Bluttellu germanica differ significantly (Rivault, pers. obs.) there are no significant differences in infestation. Blatticola blattae males are particularly affected. Although they are much smaller than females (they measure approximately one-third of the length of females), an infrapopulation never includes more than one Blutticola blattae male. Zervos’ observations are similar for the same oxyurid species (Zervos, 1988~). This is also the case for the oxyurid Leidynema appendiculatum, a parasite of Periplaneta americana (Hominick & Davey, 1972). It is not rare to observe only Blatticola blattae females alone; this occurs in several other thelastomatids (Adamson, 1989). Zervos (1988b) recorded the presence of a regulation, at the infrapopulation level, which affected male as well as female thelastomatids. She supposed that there was competition between females for limited resources and between males to inseminate females. Zervos (1988b) suggested that the first male to mature in one host inhibited, by secreting an anthelminthic substance, the development of all other individuals of the same sex. This sort of competition could explain, moreover, the phenomenon of progenesis in males. Indeed, the males that developed the most quickly would have an advantage in this type of competition. The phenomenon of regulation of Blatticola blattae populations appears from this point of view similar to that described by Zervos (1988a, b, c) although it seems that limitation of the number of females is not due solely to competition for trophic resources. In addition, taking into account the spatial structure of host populations it appears that infestation of young hosts occurs mainly through oxyurids carried by gravid females. This observation, if it is confirmed, shows that inbreeding has been promoted greatly in this thelastomatid. Several questions still remain unanswered, especially concerning the way female oxyurids control their sex ratio in the presence of a male and concerning mechanisms regulating infrapopulations. Mechanisms limiting the number of males could be the result of an ESS (Evolutionary Stable Strategy) related to the haplodiploidy in this group, which could evaluate the number of males needed to inseminate all the females according to Hamilton’s (1967) theory.
of B. blattae
989
Acknowiedgements~We are particularly indebted to J.P. Hugot and P. Deleporte for comments and criticisms of earlier drafts of the paper. We thank J. Menou for technical assistance and A. Cloarec for the English translation.
REFERENCES ADAMSONM. L. 1989. Evolutionary biology of the Oxyurida (Nematoda): biofacies of a haplodiploid taxon. Advances in Parasitology 28: i75-228. ADAMSON M. L. 1990. Haplodiploidy in the Oxyurida: decoupling the evolutionary processes of adaptation and speciation. Annales de Parasitologie Humaine et Compare% 65, Suppl. I: 31-35. HAMILTONW. D. 1967. Extraordinary sex ratios. Science 156: 477488. HOMINICKW. M. & DAVEY K. G. 1972. The influence of host stage and sex upon the size and composition of two species of thelastomatids parasitic in the hindgut of Periplaneta americana. Canadian Journal of Zoology 50: 1421-1432. KEYMER A. E. 1982. Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84: 537-582. MCCALLSTERG. M. 1988. The effect of Thelastoma Mhoesi and Hammerschmidtiella diesingi (Nematoda: Oxyurida) on host size and physiology in Periplaneta americuna (Arthropoda: Blattidae). Proceedings qf the Helminrhological Society of Washington 55: 12-14. POINARG. 0. 1975. Entomogenous Nematodes. E. J. Brill, Leiden. RIVAULT C. 1989. Spatial distribution of the cockroach, Biattella germanica, in a swimming-bath facility. Entomologia Experimentalis applicata 53: 247-255. RIVAULT C. 1990. Distribution dynamics of Blattella germanica, in a closed urban environment. Entomologia E?cperimentalis applicata 51: 85-9 1. RIVAULT C. & CLOAREC A. (in press) Food stealing in cockroaches. Journal ofEthology. TANAKAA. 1976. Stages in the embryonic development of the German cockroach Blaitella germanica L. Kontyli (Tokyo) 44: 512-525. ZERVOS S. 1988a. Population dynamics of a thelastomatid nematode of cockroaches. Parasito/ogy 96: 353-368. ZBRVOS S. 1988b. Evidence for population self-regulation, reproductive competition and arrhenotoky in a thelastomatid nematode of cockroaches. Parasitology 96: 369% 379. ZERVOS S. 1988~. Population regulation in parasitic nematodes (Thelastomatidae) of cockroaches. New, Zealand Journal qf Zoology 15: 335-338.