DOI: 10.2478/s11686-008-0043-6
© 2008 W. Stefañski Institute of Parasitology, PAS
Acta Parasitologica, 2008, 53(3), 289–295; ISSN 1230-2821
Intraspecific density-dependent effects on growth
and fecundity of Diplosentis nudus (Harada, 1938)
Pichelin et Cribb, 2001 (Acanthocephala, Cavisomidae)
Reda M. El-S. Hassanine1* and Mohammed O. Al-Jahdali2
1Department of Sciences and Mathematics, New Valley-Faculty of Education, Assiut University, El-Kharga, New Valley,
2Department of Sciences, Jeddah Teacher’s College, King Abdul Aziz University, Jeddah, Saudi Arabia
Egypt;
Abstract
During June and July of 2007, a total of 130 specimens of the fish Rastrelliger kanagurta Cuvier (Teleostei, Scombridae), ranging between 19–31 cm in total length, were caught in the Red Sea off the coast of Sharm El-Sheikh, South Sinai, Egypt, and
examined for infections by acanthocephalans (65 fish/month). Of this number, 29 (22.30%) were slightly or heavily parasitized
by the acanthocephalan Diplosentis nudus (Harada, 1938) Pichelin et Cribb, 2001 (Cavisomidae); no other helminth parasites
were found in the intestine of R. kanagurta. Twenty-nine infrapopulations of D. nudus, ranging from 23–218 individuals were
collected from the infected fishes. These infrapopulations were distributed in a well-defined fundamental niche along the intestine of R. kanagurta, where the distribution of male worms was not random with respect to female worms size and position
and suggests that the male-male competition for access to female may be intense and may select for large males. No correlation between fish size and infrapopulation size was observed. Correlations between female-to-male sex ratio and infrapopulation size, numbers of females and their mean lengths, numbers of males and their mean lengths, mean female length and mean
male length within infrapopulation were very strong, and clearly suggest that as the infrapopulation size increased, the number of females and their mean lengths decreased and the number of males and their mean lengths increased. Combination of
these results strongly suggests density-dependent effects and competition between male worms. The relationship between the
mean female length or size and the number of eggs within its pseudocoel was strongly positive; egg production by female worm
significantly decreases as the infrapopulation size increases, suggesting density-dependent reduction in female worm fecundity. Tendency for the variability in male testes size was not significant in infrapopulations of D. nudus. All of these results are
discussed.
Keywords
Acanthocephala, Cavisomidae, Diplosentis nudus, intraspecific competition, density-dependent effect, fishes, Red Sea
Introduction
Acanthocephalans are polygamous parasites of vertebrates, in
most of them, females are usually larger than males (Crompton 1970, 1985), female-to-male sex ratios are typically female biased (Valtonen 1983, Crompton 1985, Poulin 1997a)
and large males are commonly favoured by sexual selection
(Andersson 1994, Sinisalo et al. 2004). In certain species, the
adult worms form a sexual congress to mate (Richardson et al.
1997), where male body size seems to be important during
mating as larger males have been shown to have greater access
to females (Parshad and Crompton 1981). During this, male
worms have a more active role than females (Parshad and
Crompton 1981); they can seek females, and a single male can
*Corresponding
inseminate several females, while other males do not succeed
in mating (Crompton 1974, 1985); after mating, they secrete
cement to plug the female gonopore (Crompton 1970, 1985),
preventing further inseminations in the near future and thus
sperm competition; they can also grab rival males and place
a cement plug on their reproductive organs (Abele and Gilchrist 1977), preventing them at least temporarily from inseminating females. Such a reproductive behaviour could lead to
male-male competition for access to females, particularly
when the percentage of males in an infrapopulation increased
(Sasal et al. 2000). Generally, there is much evidence for density-dependent regulation of gastro-intestinal helminth population (Keymer 1982, Shostak and Scott 1993, Dezfuli et al.
2002).
author: [email protected]
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The scombrid fish Rastrelliger kanagurta Cuvier in the
northern Red Sea is parasitised by the cavisomid acanthocephalan Diplosentis nudus (Harada, 1938) Pichelin et Cribb,
2001 (see Hassanine 2006). In the present study, a considerable number of this acanthocephalan infrapopulations were
observed to explore them for the first time in the light of the
above-mentioned information.
Materials and methods
During June and July of 2007, a total of 130 specimens of the
fish Rastrelliger kanagurta Cuvier (Teleostei, Scombridae),
ranging between 19–31 cm in total length, were examined for
infections by acanthocephalans (65 fish/month). These fish
were caught by hand net (by scuba-diving) in the Red Sea off
the coast of Sharm El-Sheikh, South Sinai, Egypt, and identified according to Randall (1983) and the names follow
Froese and Pauly (2007). To avoid parasite post-mortem or
other migration along the gastro-intestinal tract, the fish were
killed immediately after capture by a blow to the head and
examined in a field laboratory (within 30–45 min after capture). Then the entire alimentary canal of each fish was immediately removed and the intestine (26.8–41.6 cm in length) cut
into 10 equal sections. Each section was opened and its contents examined separately under a dissecting stereomicroscope; all the worms found were carefully teased out, and the
opened section was then shaken vigorously in a jar of saline to
dislodge further worms and to remove mucus. Acanthocephalan infrapopulations collected from each individual fish host
was carefully counted, its position and distribution in the intestine recorded and it was then preserved in 75% ethanol for
subsequent species identification and statistical analysis. All
acanthocephalan infrapopulations recovered were arranged
according to their densities, identified, sexed and measured
(trunk length, mm) using a stereomicroscope with an eyepiece
micrometer; female worms were dissected with fine needle
and the eggs within their pseudocoel were counted using a
counting chamber under microscope, and the counting was facilitated by the use of neutral red. Some acanthocephalans
were fixed in hot 10% formalin under a slight coverslip pressure, stored in 75% ethanol, stained in acid carmine, cleared in
terpineol and mounted in Canada balsam. Voucher specimens
were deposited in the Helminthological Collection of the Red
Sea Fishes, Suez Canal University, Ismailia, Egypt (Reg.no.
2007.9.16.1-30). The coefficient of dispersion (variance/mean
= S2/x)) was used to assess aggregation of acanthocephalans
in their hosts. Spearman’s rank correlation coefficient (rs) was
calculated to determine possible correlations between femaleto-male sex ratio and infrapopulation size, numbers of females and their mean lengths, numbers of males and their
mean lengths, mean female length and mean male length, mean
female length and number of eggs in its pseudocoel, and
between mean testes length-to-male trunk length ratio and
male trunk length.
Reda M. El-S. Hassanine and Mohammed O. Al-Jahdali
Results
Of the 130 R. kanagurta examined, 29 (22.30%) were slightly or heavily parasitised by the acanthocephalan Diplosentis
nudus (Harada, 1938) Pichelin et Cribb, 2001 (Cavisomidae);
fresh infections were not observed throughout the period of
collection, and no other helminth parasites were observed in
the intestine of this fish. A relatively large number of D. nudus
(3114 specimens) belonging to 29 infrapopulations, ranging
from 23–218 individuals were collected from the infected
fishes, with a high mean intensity of 107.37 worms/host; no
correlation between fish size and size of D. nudus infrapopulations was observed. The coefficient of dispersion (S2/x))
value was 148.43. This value and the relatively low prevalence and high intensity of this parasite indicate that it has a
tendency to exhibit a strong aggregation pattern within its host
individuals. Diplosentis nudus infrapopulations were arranged according to their densities and the corresponding entire
data set is shown in Table I.
Diplosentis nudus infrapopulations were distributed in the
anterior 30% of the intestine of R. kanagurta and never observed in the other intestinal regions. Thus, D. nudus infrapopulations were distributed in a well-defined fundamental
niche along the intestine of this fish; absence of other intestinal helminth parasites excludes the confounding influence of
interspecific interaction.
During the period of collection (June to July), all the female worms of D. nudus were fully-gravid (distended with embryonated eggs). The distribution of male worms was not random with respect to female worms size and position; in most
of large infrapopulations, larger females were found aggregated in the anterior region of the fundamental niche (anterior 10%
of the intestine), with no males close to them; smaller females
and most males were found aggregated at the middle of the
fundamental niche (second 10% of the intestine), where larger males were more close to females than smaller ones, and
some females had cement plugs remain attached to their posterior ends; some smaller males (9–16 individual/infrapopulation) with cement plug on their gonopores were found scattered in the posterior region of the fundamental niche (third
10% of the intestine), and no females close to them. Thus,
larger females seemed to be copulated in the anterior region of
the fundamental niche prior to the smaller ones, which copulated next to them in the middle region of the fundamental
niche, or larger females may copulated posteriorly and then
moved anteriorly in the fundamental niche; smaller males
seemed to be excluded from this process. These observations
suggest that the male-male competition for access to female
may be intense in D. nudus infrapopulations and may select
for large males.
In D. nudus infrapopulations, there is a strong negative
correlation between female-to-male sex ratio and infrapopulation size (rs = –0.9683, P = 0.0001) (Fig. 1), i.e. as the
infrapopulation size increases, the number of males increases relative to the number of females in an infrapopulation.
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Intraspecific density-dependent effects on growth and fecundity of D. nudus
Stanis³a
Table I. Data set corresponding to 29 Diplosentis nudus infrapopulations collected from the intestine of the scombrid fish Rastrelliger
kanagurta
&
%
Infrapopulations
(no. individuals)
no. (%)
mean length
(mm)±SD
mean no.
eggs±SD
no. (%)
mean length
(mm)±SD
testes mean
length/trunk
length
I (n = 23)
II (n = 30)
III (n = 34)
IV (n = 37)
V (n = 41)
VI (n = 44)
VII (n = 49)
VIII (n = 57)
IX (n = 65)
X (n = 71)
XI (n = 75)
XII (n = 83)
XIII (n = 86)
XIV (n = 92)
XV (n = 96)
XVI (n = 102)
XVII (n = 107)
XVIII (n = 120)
XIX (n = 124)
XX (n = 139)
XXI (n = 148)
XXII (n = 155)
XXIII (n = 166)
XXIV (n = 174)
XXV (n = 183)
XXVI (n = 191)
XXVII (n = 198)
XXVIII (n = 206)
XXIX (n = 218)
14 (60.86)
18 (60.00)
21 (61.76)
22 (59.45)
25 (60.97)
27 (65.85)
31 (63.26)
34 (59.64)
36 (55.38)
41 (57.74)
40 (53.33)
44 (53.01)
41 (47.67)
42 (45.65)
43 (44.79)
45 (44.11)
47 (43.92)
50 (41.66)
53 (42.74)
55 (39.56)
57 (38.51)
61 (39.35)
60 (36.14)
67 (38.50)
66 (36.06)
70 (36.64)
72 (36.36)
72 (34.95)
75 (34.40)
9.26±1.50
8.99±1.48
9.69±1.34
9.38±1.59
8.85±1.31
8.97±1.26
8.57±1.49
9.71±1.37
9.11±1.11
9.67±1.43
8.81±0.99
8.63±0.97
8.25±0.90
7.94±0.85
7.82±0.84
7.61±1.07
7.48±0.91
7.21±0.97
7.13±1.28
7.34±1.05
6.98±0.89
7.09±1.15
6.42±0.94
6.68±1.10
7.03±0.84
6.11±0.91
6.29±1.03
5.98±0.70
6.44±0.78
9,751±778
9,776±790
10,229±702
9,971±840
9,622±714
9,868±693
9,184±802
10,357±740
9,799±603
10,081±745
9,381±559
9,447±548
8,796±522
8,775±473
8,457±454
8,245±589
7,706±468
7,725±534
7,387±661
7,236±519
6,882±490
7,105±596
6,704±535
6,866±565
7,013±428
6,654±492
6,246±727
6,109±397
5,781±426
9 (39.13)
12 (40.00)
13 (38.23)
15 (40.54)
16 (39.02)
17 (38.63)
18 (36.73)
23 (40.35)
29 (44.61)
30 (42.25)
35 (46.66)
39 (46.98)
45 (52.32)
50 (54.34)
53 (55.20)
57 (55.88)
60 (56.07)
70 (58.33)
71 (57.26)
84 (60.43)
91 (61.48)
94 (60.64)
106 (63.86)
107 (61.49)
117 (63.94)
121 (63.35)
126 (63.63)
134 (65.04)
143 (65.60)
7.16±0.78
6.84±0.72
6.98±0.62
7.23±0.80
7.46±0.64
7.79±0.89
7.55±1.44
7.93±0.82
8.07±1.14
8.17±0.90
7.92±1.65
8.23±1.71
8.65±1.36
8.46±1.24
8.51±1.61
8.79±1.67
9.29±1.77
9.57±1.69
9.36±1.34
9.89±1.87
10.16±2.19
9.94±2.11
10.04±1.94
10.29±2.08
10.53±2.28
11.41±2.32
10.37±2.04
10.81±2.17
10.72±2.26
0.17
0.17
0.19
0.20
0.19
0.18
0.17
0.19
0.20
0.17
0.18
0.18
0.20
0.18
0.17
0.21
0.18
0.22
0.19
0.17
0.17
0.18
0.19
0.18
0.21
0.17
0.19
0.22
0.19
1.55
1.50
1.61
1.46
1.56
1.58
1.72
1.47
1.24
1.36
1.14
1.12
0.91
0.84
0.81
0.79
0.78
0.71
0.74
0.65
0.62
0.64
0.56
0.62
0.56
0.57
0.57
0.53
0.52
XXIX
XXVII
XXVIII
XXV
XXVI
XXIV
XXII
XXIII
XX
XXI
XIX
XVII
XVIII
XV
XVI
ship between number of females and their mean lengths (rs =
–0.9273, P = 0.0002) (Fig. 2A), i.e. as the number of females
increased, their mean lengths decreased. In contrast, there is
XIV
XII
XIII
X
XI
IX
VIII
VI
VII
V
IV
III
I
II
Therefore, large infrapopulation of D. nudus is generally characterized by significantly more male worms than found in
small infrapopulation. There is also a clear negative relation-
Female/male
sex ratio
Fig. 1. Relationship between female-to-male sex ratio and infrapopulation size, across 29 Diplosentis nudus infrapopulations arranged according to their densities
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Reda M. El-S. Hassanine and Mohammed O. Al-Jahdali
Roborzyñski
fjad kadsææ¿æ
XXIX
XXVII
XXVIII
XXV
XXVI
XXIV
XXII
XXIII
XX
XXI
XIX
XVII
XVIII
XV
XVI
XIV
XII
XIII
X
XI
IX
VII
VIII
V
VI
IV
III
I
II
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
XII
XIII
XIV
XV
XVI
XVII
XVIII
XIX
XX
XXI
XXII
XXIII
XXIV
XXV
XXVI
XXVII
XXVIII
XXIX
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
XII
XIII
XIV
XV
XVI
XVII
XVIII
XIX
XX
XXI
XXII
XXIII
XXIV
XXV
XXVI
XXVII
XXVIII
XXIX
rosbœŸæv
Fig. 2. Relationships between number of females and their mean lengths (A), number of males and their mean lengths (B) and between number of females and number of males (C), across 29 Diplosentis nudus infrapopulations arranged according to their densities
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Intraspecific density-dependent effects on growth and fecundity of D. nudus
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
XII
XIII
XIV
XV
XVI
XVII
XVIII
XIX
XX
XXI
XXII
XXIII
XXIV
XXV
XXVI
XXVII
XXVIII
XXIX
293
Fig. 3. Relationship between mean female body length or size and mean number of eggs in its pseudocoel, across 29 Diplosentis nudus
infrapopulations arranged according to their densities
a strong positive relationship between number of males and
their mean lengths (rs = 0.9891, P = 0.0001) (Fig. 2B), i.e. as
the number of males increased, their mean lengths increased.
However, there is a strong negative correlation between mean
female length and mean male length (rs = –0.9226, P = 0.0001)
(Fig. 2C), i.e. as the mean female length decreased, the mean
male length increased. Thus, as the infrapopulation size increased, the number of females and their mean lengths decreased and the number of males and their mean length increased. Combination of these results strongly suggests density-dependent effects and competition between male worms.
The relationship between the mean female length or size
and the number of eggs within its pseudocoel was strongly
positive (rs = 0.9871, P = 0.0002) (Fig. 3), i.e. the egg output
increases with the female size and the vice versa is true. As
shown in Table I, D. nudus infrapopulations were arranged
according to their densities, where 12 infrapopulations (I–XII)
ranging in size from 23–83 individuals were female biased,
while the others 17 infrapopulations (XIII–XIX) ranging in
size from 86–218 individuals were male biased. In femalebiased infrapopulations, the mean female length (ranging from
8.57–9.71 mm) was larger than the mean male length (ranging
from 6.84–8.23 mm) and the mean egg output ranging from
9,184–10,357 eggs/female worm, while in male-biased infrapopulations, the mean female length (ranging from 5.98–8.25
mm) was smaller than the mean male length (ranging from
8.46–11.41 mm) and the mean egg output ranging from 5,781–
8,775 eggs/female worm. Thus, egg production by female
worm significantly decreases as the infrapopulation size increases, suggesting density-dependent reduction in female
worm fecundity.
The mean testes length-to-male trunk length ratio did not
correlate with male trunk length (rs = 0.197563, P = 0.246),
i.e. tendency for the variability in male testes size was not significant in D. nudus infrapopulations, where the mean testes
length-to-male trunk length ratio was nearly similar (= 0.17–
0.22) in all infrapopulations.
During July, many worms were naturally dead, and some
dead female and male worms were seen hanging out of the
anus in many fishes. However, embryonated eggs of D. nudus
were not observed among the intestinal contents of R. kanagurta.
Discussion
Williams et al. (1991) showed that certain methods of fish
capture (traps or nets) result in significant stress to fish. Such
stress causes regurgitation and contributes towards the expelling of some intestinal helminths. According to Mackenzie
and Gibson (1970), the migration of parasitic helminths along
the gastro-intestinal tract of fish, during periods of starvation
or after death, may also affect their normal distribution. Generally, the method of fish collection may affect the normal
distribution of helminths along their gastro-intestinal tracts. In
the present research, fish were caught by hand net (by scubadiving) and examined in a field laboratory in the least possible
time after capture in order to avoid significant changes.
The typical distribution of helminth numbers between host
individuals follows an aggregated pattern (Shaw and Dobson
1995, Shaw et al. 1998), where few hosts harbour large parasite infrapopulations and most hosts harbour few or no parasites. The present observations suggest that distribution of
D. nudus between its host individuals exhibits a strong tendency to follow this pattern. Such an aggregated pattern of distribution may increase the chances of mating (Kennedy 1976)
or may reduce the effects of interspecific competition, if present (Dobson 1985, Dobson and Roberts 1994).
In ecological studies of gastro-intestinal helminth parasites, the “fundamental niche” of a parasite is the distribu-
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tional range of sites within the gut where the parasite occurs in
single species infections (Poulin 2001). Surely, such niche has
a carrying capacity, i.e. has a capacity for a certain maximum
number of worms that can exist within it without intraspecific competition. In the present study, all D. nudus infrapopulations were found distributed in the anterior 30% of the intestine of R. kanagurta, i.e. in a well-defined fundamental niche,
but infrapopulations ranging in size from 23–83 individuals
were female biased, where density-dependent effects were not
noticeable, while infrapopulations ranging from 86–218 individuals were male biased, where density-dependent effects
were clearly noticeable. Thus, carrying capacity of the fundamental niche plays an important role in density-dependent
effects.
In certain acanthocephalan species, the adult worms form
a sexual congress to mate (Richardson et al. 1997), where
male body size seems to be important during mating as larger males have been shown to have greater access to females
(Parshad and Crompton 1981, Andersson 1994, Sinisalo et al.
2004). Such a reproductive behaviour could lead to male-male
competition for access to females, particularly when the percentage of males in an infrapopulation increased (Sasal et al.
2000). In the present study, the distribution of female and male
worms of D. nudus within the fundamental niche agrees typically with these concepts, and seems to be dynamic with
males always seeking new mating opportunities, and the presence of cement plugs on the small males gonopores strongly
suggests that male-male competition for access to females can
be intense in D. nudus infrapopulations and may select for
large males. Thus, sexual selection, i.e. intensity of male-male
competition for access to females (Ghiselin 1974, West Eberhard 1983) may play an important role in determining the spatial distribution of female and male worms of D. nudus within the fundamental niche (anterior 30% of the intestine of
R. kanagurta).
According to Lawlor et al. (1990) acanthocephalan males
choose their mate, and they choose females which are larger
and located anteriorly in the intestine. The present results show
that the mating success of a female D. nudus is associated with
its size, but not exactly as in Lawlor et al.’s (1990) study.
Instead, larger males firstly approach larger females in the
anterior 10% of the intestine (anterior region of fundamental
niche), and then move slightly posteriorly to approach smaller females in the second 10% of the intestine (middle region
of fundamental niche), or larger females can move anteriorly
after being inseminated posteriorly in the fundamental niche.
Sex ratios of acanthocephalan infrapopulations are typically female-biased (Valtonen 1983, Crompton 1985, Poulin
1997a). Comparative data suggest that as the infrapopulation
size increases, the sex ratio should become less female-biased
to increase the probability of mating, and at the same time the
size of males relative to females should increase in response to
stronger male-male competition for access to females (May
and Woolhouse 1993; Poulin 1997a, b). These expected patterns were clearly observed in this study, with significantly
more and significantly larger male worms being found in large
Reda M. El-S. Hassanine and Mohammed O. Al-Jahdali
infrapopulations of D. nudus. The present results also suggest
that increment in female body size negatively affected as the
infrapopulation size increases (see Table I).
In D. nudus infrapopulations, there is a strong positive
relationship between mean female length and number of eggs
within its pseudocoel, i.e. egg output increases with the female
size, and because of the strong negative relationship between
the female-to-male sex ratio and the infrapopulation size, egg
production by the female worm significantly decreases as the
infrapopulation size increases, suggesting density-dependent
reduction in female worm fecundity. In most gastro-intestinal helminths, density-dependent reductions in female worm
size or length are often accompanied by reductions in mean
egg output, due to the strong positive relationship between the
female body size and the egg output (Shostak and Scott 1993,
Irvine et al. 2001, Richards and Lewis 2001, Dezfuli et al.
2002).
Tendency for the variability in male testes size was not significant in D. nudus infrapopulations. The use of copulatory
plugs by acanthocephalan males greatly reduces the likelihood of sperm competition (Crompton 1970, 1985), and the
relative investment in testis growth decreases as the intensity
of male-male competition for access to females increases
(Poulin and Morand 2000), a situation clearly observed in the
present study.
According to Hassanine (2006), the life span of D. nudus
in R. kanagurta is about 11 months (from October to August),
and the worms begin to die off naturally in July, prior to their
elimination from the intestine of R. kanagurta. Therefore,
competition for space is probably less important for males
than competition for access to females.
The embryonated eggs of D. nudus were not observed
among the intestinal contents of R. kanagurta, and some female and male worms were seen hanging out of the anus in
many fishes. According to Hassanine (2006), females of D. nudus may not lay eggs, but pass out of the intestine of R. kanagurta, where they degenerate in the environment and the
released embryonated eggs are ingested by the intermediate
host. This is in accordance with the suggestion of Muzzall and
Rabalais (1975) when explaining a similar case in their study
of the seasonal cycle of Acanthocephalus jacksoni Bullock,
1962.
Acknowledgements. We are very grateful to Dr David I. Gibson and
Dr Rodney A. Bray (Zoology Department, Natural History Museum,
London) for their continuous advice and assistance. We should also
like to extend our appreciation to Dr Ebrahim M. Yassen, Department
of Sciences and Mathematics, New Valley-Faculty of Education,
Assiut University, Egypt for his help during the collection of the
material.
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Intraspecific density-dependent effects on growth and fecundity of D. nudus
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(Accepted April 7, 2008)
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