61-76 moharm2

International Journal of Development, Vol.4, No.(1) (2015): 61-75

ISSN: 2314-5536 e-ISSN: 2314-5544 (Online)

www. ijd.byethost13.com e-mail: [email protected]

Reproductive biology of males pipefish, Trachyramphus bicoarctatus (Teleostei:

Syngnathidae) at Lake Qarun, Egypt

Ahmad M. Azab*, Hassan M. M. Khalaf-Allah and Moharam A. M. Afifi

Marine Biology and Ichthyology branch, Zool. Dept., Fac. Sci., Al-Azhar Univ., Cairo, Egypt.

*[email protected]

ABSTRACT

The reproductive biology of male pipefish, Trachyramphus bicoarctatus at Lake

Qarun in El-Fayoum Governorate, Egypt was investigated to determine sex ratio, male length

at first sexual maturity, maturity distribution of male, parental care and male fecundity. A

total of 1214 pipe fish were collected from the lake from December 2013 to November 2014.

From the total collected pipefish specimens, 511 individuals (42.09%) were males and

703 individuals (57.09%) were females. Male - female sex ratio was 1:1.37, which highly

significant differed from the expected 1:1 ratio; either through the whole study period or

during all months. Male pipefish reached sexual maturation for the first time at length of

7.9cm. Male maturation and brooding male were significantly increased with increasing of

fish length and weight. Mature males and brooding males with eggs and embryos in the brood

pouch were captured from December till April.

The parental care in pipefish T. bicoarctatus is unusual. Male possesses a ventral

brood pouch embedded in the skin in which the eggs are deposited. Fertilized eggs were

attached in two or three longitudinal strips inside the brood pouch. These eggs may have

different developmental stages in the same brooding pouch. A total of 7198 embryos were

recorded in brooding males during this study. Male fecundity was strongly correlated to fish

length and weakly correlated to fish weight; it ranged from 42 to 111 eggs or embryos in the

brood pouch. The reproductive period of T. bicoarctatus was extended from December to

April and the peak value occurred during February.

Key words: Pipefish, Trachyramphus bicoarctatus, Syngnathidae, Lake Qarun, Reproductive

biology, fecundity, brooding pouch.

INTRODUCTION

The order Syngnathiformes consists of five families: Aulostomidae, Centriscidae,

Fistulariidae, Solenostomidae and Syngnathidae. The family Syngnathidae (pipefish and

seahorses) is the most numerous and comprises two subfamilies, Syngnathinae (pipefish) and

Hippocampinae (seahorses). The former subfamily comprises 105 genera; the latter consists

of 8 genera ]1[.

Syngnathidae is a very large family in the order Syngnathiformes. It is very widely

distributed in tropical and temperate zones; it lives in coastal waters to depth of about 90 m

and inhabited littoral pools, lagoons, estuaries and fresh water. There are approximately 200

species of pipefish. Most pipefish are marine dwellers, usually 35–40cm in length and

generally inhabit sheltered areas in coral reefs; sea grass beds and sandy lagoons ]2[.

Pipefish are zooplankton feeder and attract economic interest for their value as a live

aquarium fish, curio trade, as ingredients in traditional Chinese medicine, as supplements in

some specialized cuisine and as curios ]3&4[.

The members of the family Syngnathidae, pipefish and seahorses, have an elongated

body entirely covered by bone plates connected to each other to form belts (rings). A

mailto:[email protected]

http://en.wikipedia.org/wiki/Marine_%28ocean%29

Ahmad M. Azab et al.

62

characteristic feature of fish in this family is the unusual brood chamber or pouch that is used

to bear embryos and is located ventrally on the body or tail of the male ]5&6[. The Bent stick

Pipefish, Trachyrhamphus bicoarctatus is generally native in marine waters throughout much

of the Indo-West Pacific, common in the Red Sea, Mediterranean Sea and Lake Qarun. It

lives in bays and estuaries on sand or mud, from the shallows to at least 40 m depth. This

species is sometimes observed with the anterior part of the fish raised above the substrate and

the head facing into the current. The posterior part of the body and thickened ventral ray of

the caudal fin are used to anchor the fish in place. Copepods, amphipods and small eggs were

the main food items consumed by this species. Reproduction occurred during winter ]7&8[.

Few studies are available on the pipefish, T. bicoarctatus; such as identification,

common information and distribution ]7&9[ . However, information on the reproductive

biology on the pipe fish, T. bicoarctatus are lacking. Therefore, the principal objective of the

present work is to investigate the reproductive biology of male T. bicoarctatus at Lake Qarun,

Egypt, to determine sex ratio, male length at first maturity, frequency of male maturation and

pregnancy, parental care and male fecundity.

MATERIALS AND METHODS

1- The study area:

The study area in this work included the South coast of Lake Qarun, Egypt

(Fig. 1). It is located about 80 Km southwest of Cairo and lies between longitudes of

30°.41778` & 30°.8275` E and latitudes 29°.44194` & 29°.51111` N in the lowest part of El-

Fayum depression. Fish samples were monthly collected in the Southern shoreline of Lake

Qarun during the period from December, 2013 to November, 2014.

Fig. (1): Map of Lake Qarun showing the 6 stations selected in the study area.

2-Specimens collection:

Pipefish samples were collected by using a seine net of 5 meter length x 1.5 meter

depth, with 5 mm mesh size. The net was dragged 5 times in each station over an area of

about 5x10 = 50 m2 from the beach with an average depth of about 50 cm. Collected fish

within the net were preserved in 10% formalin solution for latter examination. In the

laboratory, fish were identified according to Randall ]7[; total and standard lengths were

measured to the nearest millimeters and recorded. Fish were also weighed to the nearest 0.1

gram and then the following studies were carried out.

63



3- Reproductive studies:

A- Sex ratio:

Pipefish were sexed by morphological examination (pipefish were sexed by presence

of anal fin in females or absent in males). The sex ratio of T. bicoarctatus was monthly

determined by recording the number of males and females of each month from the collected

samples during the study period. Sex ratio was calculated as percentage of males to females

of each month. Frequencies of each month were determined for pooled data for males and

females. The ratio was calculated by chi squire test:

χ2 = ∑

E

Eo 2)(

Where: χ2: Is Chi Square O: Is the observed frequency in each category

E: Is the expected frequency in the corresponding category

B- Length at first maturity of male pipefish:

The length at first sexual maturity can be determined graphically, on the curve

representing the percentage of individuals in the process of maturation depending on presence

of brood pouch in mature males. The point on the curve where 50 % of individuals are

considered mature is taken as the index of the first maturity. Progression from 0 to 100 %

takes longer for some species than others. Fish of different length groups were classified into

either immature or mature were studied according to Pitt ]10[.

C- Frequency of maturation and pregnancy in male pipefish:

The monthly frequency variations of male maturation and pregnancy with length,

weight were calculated as the percentage of mature males relative to the total males and

percentage of pregnant males relative to mature males.

D- Fecundity of male pipe fish:

In the present study, the male fecundity was expressed as the number of brooding

eggs or embryos. To study fecundity, pregnant males were collected during the spawning

season. The brood pouch of brooding (pregnant) male pipefish was opened and the contents

(deposited eggs and/or developing embryos) were counted to estimate male fecundity.

The relationships between male fecundity and fish length and body weight were

estimated according to the following formula:

Log F = log a b log X ]11[

Where: F: is the absolute fecundity. X: is independent variable (length or weight).

a: is the intercept . b: is an exponent.

Data were analyzed statistically by using Microsoft Excel ver. 2010.


64

RESULTS

1. Sex Ratio:

Data in Table (1) showed that, out of 1214 examined individuals of T. bicoarctatus

during the study, 511 (42.09%) were males and 703 (57.09%) were females. The sex ratio of

a whole catch was 1:1.37 (Male: Female). Monthly variation in the value of the sex ratio

(males to females) revealed that, the maximum value (1: 10.33) was recorded during June

(P>0.05) and the minimum value (1: 0.2) was recorded during September. In the studied

samples of T. bicoarctatus, the proportion in all months was significantly (P > 0.05) varied

from 1:1 male to female.

2. Length at first sexual maturity: Males of T. bicoarctatus were classified according to their maturation into two

categories; immature and mature fish. Results in Table (2) showed that, the smallest mature

male was recorded at total length of 5 cm with a lowest maturity percentage (1.35%) of total

males. Then, maturation gradually increased with increasing fish length reaching 53.33 % at

length of 8 cm. Mathematical method indicated that the maturation of male fish recorded

50% at 7.9 cm (Fig. 2). Larger fish showed an increasing in the frequency of mature fish and

that 100% of maturity for males of the fish was recorded at total length of 11cm.

3. Maturation and pregnancy of male T. bicoarctatus:

3.1. According to total length:

The annual abundance of male T. bicoarctatus was 511 individuals in all length

classes. The mature males of pipefish were abundant specimens (241); they represent about

47.16% of all collected males. The maturation of males was gradually increased with the

increase of body length (Table 2 and Fig. 2). The total number of pregnant males was 111; it

represented 46.05% from all mature males. The highest ratios of pregnant males to mature

males were 63.46% and 64%, they recorded at length classes 11and 12 cm, respectively

(Table 2 and Fig. 3).

3.2. According to body weight:

The frequency of mature male T. bicoarctatus considerably varied with the changing

of body weight. The lowest frequency of mature male fish was recorded at weight class of 0.1

gm; it represented 6.3% of total males, then it gradually increased to reach the complete

maturation in class weight 0.6 gm; representing 100% of total males (Table 3 and Fig. 4). The

percentage of pregnant male pipefish to all mature males was varied from 18.51% at weight

class 0.3 gm to 100% at weight class 1.2 gm (Table 3 and Fig. 5).

3.3. According to months:

The abundance of mature male pipefish is 241 individuals. The maximum number of

mature pipefish (170 individuals) was recorded during April; it represented 64.88% and the

minimum (only one) occurred during May; it represented by low percentage (Table 4 and

Fig. 6). The abundance of pregnant males of T. bicoarctatus varied considerably from month

to month. It was recorded during winter and spring. The highest percentage of pregnant male

(100%) was recorded during February and the lowest (41.76%) occurred during April. It was

entirely absent in summer and autumn (Table 4 and Fig. 7). These data showed that, the

reproductive season of male T. bicoarctatus extends from December to April.

65



Table (1): Sex ratio of T. bicoarctatus, collected from Lake Qarun, at different months

during the period from December, 2013 to November, 2014.

Months Total no.

of fish

No. of

males

No. of

females

Sex ratio χ

2

Male : Female

December 81 31 50 1:1.61 2.22

January 28 10 18 1:1.8 1.14

February 58 13 45 1:3.46 8.82*

March 147 40 107 1:2.67 15.29**

April 542 262 280 1:1.06 0.30

May 206 100 106 1:1.06 0.09

June 34 3 31 1:10.33 11.53**

July 28 11 17 1:1.54 0.64

August 51 13 38 1:2.92 6.13*

September 6 5 1 1:0.2 1.33

October 33 23 10 1:0.43 2.56

November 0 0 0 - -

Total 1214 511 703 1:1.37 15.18**

* = significant; **= highly significant

Table (2): Variation in maturity, pregnancy and male fecundity according to length in males

of T. bicoarctatus, collected from Lake Qarun during the period of study.

Length

Class

(cm.)

No.

of

males

Mature

males

Pregnant

males Total

no. of

embryo

Absolute fecundity Calculated

fecundity No. % No. % Range Average ±SD

3 7 0 0 0 0 -- -- -- -- --

4 45 0 0 0 0 -- -- -- -- --

5 74 1 1.35 0 0 -- -- -- -- --

6 60 2 3.33 1 50 48 -- 48 0 43.86

7 57 12 21.05 3 25 152 48-56 50 4.61 49.54

8 45 24 53.33 7 29.17 388 42-80 55.42 12.73 55.05

9 73 56 76.71 16 28.57 832 44-72 52 7.26 60.42

10 63 59 93.65 29 49.15 1858 46-88 64.06 11.87 65.67

11 52 52 100 33 63.46 2190 44-90 66.96 13.08 70.80

12 25 25 100 16 64 1288 60-

102 80.5 12.74 75.83

13 9 9 100 5 55.56 331 54-99 66.2 19.24 80.78

14 1 1 100 1 100 111 - 111 0 85.65

Total 511 241 47.16 111 46.05 7198 42-

102 64.85 19.77 65.29


66

Fig. 2: Length at first maturity of male Trachyramphus bicoarctatus, collected from

Lake Qarun, at different months during the period of study.

0

20

40

60

80

100

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

Pre

gnan

t (

%)

Length classes (Cm)

Fig. 3: Relationship between length classes and pregnancy of male T. bicoarctatus

samples collected from Lake Qarun during the period of study.

67



Table (3): Variation in maturity, pregnancy and male fecundity according to weight in

males of T. bicoarctatus, collected from Lake Qarun during the period of study.

Weight

class

(gm.)

No. of

males

Mature

males

Pregnant

males Total

embryo

Absolute fecundity Calculated

fecundity No. % No. % Range Average ±SD

0.01 96 -- -- -- -- 0

0.1 111 7 6.31 3 42.86 184 48-88 61.33 23.09 23.44

0.2 61 22 36.07 5 22.73 264 44-62 52.8 7.01 30.12

0.3 44 27 61.37 5 18.52 290 42-80 58 13.7 34.87

0.4 42 32 76.19 8 25 424 44-72 54.14 8.2 38.68

0.5 42 38 90.48 13 34.21 758 44-72 53 8.88 41.93

0.6 29 29 100 17 58.62 1068 44-88 62 13.19 44.78

0.7 31 31 100 22 70.97 1382 48-84 65.8 11.06 47.35

0.8 18 18 100 11 61.11 798 48-102 72.54 17.32 49.69

0.9 16 16 100 10 62.5 740 58-90 74 13.06 51.85

1 6 6 100 5 83.33 338 54-82 67.6 13.44 53.86

1.1 7 7 100 5 71.43 370 54-96 74 17.88 55.75

1.2 2 2 100 2 100 142 68-74 71 4.24 57.53

1.3 4 4 100 3 75 245 56-99 81.66 22.67 59.21

1.4 2 2 100 2 100 195 84-111 97.5 19.09 60.82

Total 511 241 47.16 111 46.06 7198 42-111 64.85 12.37 46.42

Table (4): Monthly variation in maturity, pregnancy and male fecundity during different

months in males of T. bicoarctatus, collected from Lake Qarun during the

period of study.

Months No. of

males

Mature

males

Pregnant

males

Total

No. of

embryo

Absolute fecundity

No. % No. % Range Average ±SD

December 31 24 77.42 13 54.16 858 48-88 66 12.54

January 10 7 70 6 85.71 424 48-102 70.66 21.22

February 13 6 46.15 6 100 450 60-90 75 11.64

March 41 23 56.09 15 65.21 1000 44-90 66.66 17.38

April 262 170 64.89 71 41.76 4466 42-111 62.9 14.75

May 100 1 1 0 0 - - - -

June 3 1 33.33 0 0 - - - -

July 11 4 36.36 0 0 - - - -

August 13 3 23.08 0 0 - - - -

September 5 2 40 0 0 - - - -

October 22 0 0 0 0 - - - -

November -- -- -- -- -- - - - -

Total 511 241 47.16 111 46.06 7198 42-111 64.85 4.67


68

0

20

40

60

80

100

0 0.2 0.4 0.6 0.8 1 1.2 1.4

Mat

ure

(%

)

Weight classes (g)

Fig. 4: Relationship between body weight and mature of male T. bicoarctatus samples

collected from Lake Qarun during the period of study.

0

20

40

60

80

100

0 0.2 0.4 0.6 0.8 1 1.2 1.4

Pre

gnan

t (

%)

Weight classes (g)

Fig. 5: Relationship between body weight and pregnant of male T. bicoarctatus

samples collected from Lake Qarun during the period of study.

69



0

10

20

30

40

50

60

70

80M

atu

re (

%)

Months

Fig. 6: Monthly variation in maturity % of male T. bicoarctatus samples collected from

Lake Qarun during the period of study.

0

20

40

60

80

100

Pre

gnan

t (%

)

Months

Fig. 7: Monthly variation of pregnant % of male T. bicoarctatus samples collected from

Lake Qarun during the period of study.


70

4. Fecundity of male:

In the present study, the male fecundity was expressed as the number of brooding

eggs/embryos. Fecundity of male T. bicoarctatus according to the total length, fish weight

and months are showed in Tables (2-4) and graphically represented in Figures (8-10).

4.1. Fecundity and total length relationship:

The regression equation representing this relationship is:

Log F = 1.03 + 0.87 log L

Data in (Table 2) showed that, the fecundity increases with the increasing of the fish

length. This relation was found to be significant and the correlation coefficient “r” was 0.86.

The observed and calculated fecundity were related to each length group. The absolute

fecundity varied from 48 to 111 for fish length of 6 and 14 cm, respectively (Fig. 8).

4.2. Fecundity and body weight relationship:

The regression equation representing this relationship is:

Log F = 1.57+ 0.12 Log W

Data in Table (3) showed that, the absolute fecundity of T. bicoarctatus was

correlated with the body weight of the fish and exhibited weakly correlation coefficient (0.4).

Fecundity showed irregular linear relationship with body weight of the fish. The absolute

fecundity varied from 42 to 111 for fish body weight of 0.1 and 1.4 g, respectively. The

average of absolute fecundity was varied from 53± 7 to 98± 19 at weight 0.2 to 1.4 g,

respectively (Fig. 9).

4.3. Fecundity with month's relationship:

Data in Table (4) showed that, the reproductive period of T. bicoarctatus in Lake

Qarun was extended from December to April. The mean number of embryos recorded was 66

during December, then gradually increased during January (70), reached to the peak value

during February (75) and decreased gradually during March (67) and April (63). It was

entirely absent during remaining months (Fig. 10).

5. Parental care:

The parental care in pipefish T. bicoarctatus is unusual. Male possesses a ventral

brood pouch embedded in the skin in which the eggs are deposited. The brood pouch is

located under the genital opening towards the caudal fin (PLATE I- A & B). The ovulated

eggs in females are transported to male brood pouch after fertilization. Fertilized eggs were

attached in two or three longitudinal strips inside the brood pouch (PLATE I C & D). These

eggs may have different developmental stages in the same brooding pouch. Results showed

that, a lot of individuals carried different developmental stages of eggs/embryo in the same

brood pouch (PLATE I- E & F).

The well-developed embryos leave the brood pouch, keeping other less developing

embryos (PLATE I G).These born embryos or larvae leave the brood pouch at a quite

developing stage; they already have developed rostral apparatus and lack yolk sacs, their

bodies are covered with ring plates, and they are capable of feeding independently (PLATE

I- H).

71



0102030405060708090

100110

5 6 7 8 9 10 11 12 13 14 15

Nu

mb

er

of

emb

ryo

s

Total length classes (Cm)

Mean

Calculated

Fig. 8: Relationship between observed and calculated absolute fecundity and total

length of male T. bicoarctatus samples collected from the Lake Qarun during the

period of study.

0

10

20

30

40

50

60

70

80

90

100

0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6

Nu

mb

er

of

em

bry

os

Weight classes (g)

Mean

Calculated

Fig. 9: Relationship between observed and calculated fecundity and body weight of

male pipefish collected from Lake Qarun during the period of study.

55

60

65

70

75

80

December January February March April

Mea

n f

em

bry

os

Months

Figure 10: Relationship between Absolute fecundity and months of T. bicoarctatus

samples collected from Lake Qarun during the period from December, 2013

to November 2014.


72

A

B

C

D

E

F

G

H

PLATE I: A & B: Male and female pipefish, T. bicorcatus showing the brooding pouch in male;

C-F: Opened brooding pouches in male showing: D- presence of 2 - 3 strips of eggs with

embryos (arrows); E & F: different developmental stages in eggs and embryos; G: the empty

part of brooding pouch after some embryos are labored; H: Pipefish larva after hatching and

release from brooding pouch.

73



DISCUSSION Reproduction is the process by which species are propagated. The success of any fish

species is ultimately determined by the ability of its members to reproduce successfully in a

fluctuating environment ]12[.

In the present study, the determination of sex perfected by presence of anal fin in

female or absence in male, not uses of brood pouch, because the young males without a brood

pouch. ]13[ noticed that, the determination of sex by the presence or absence of the brood

pouch may have introduced some error since young males, without a brood pouch or with a

developing brood pouch may be mistaken for immature individuals, even with macroscopic

examination of the gonads.

Sex ratio indicates the proportion of male and female in the population and is

expected to be 1:1 in nature. Any deviation from this ratio may indicate the dominance of one

sex over the other. This happens because of differential behavior of sexes, environmental

conditions, fishing activities, etc. ]14[. In nature, mate availability is usually not a limiting

factor for pipefish males even if there is some evidence suggesting that males may have

difficulties finding partners under male-biased sex ratio or at a low frequency also under even

sex ratio ]15[.

In the present study, sex ratio for male to female was found to be 1.0:1.37 (i.e.

females dominated males through the year). This may be due to that male receiving the

fertilized eggs from more than one female. This result was agreement with that obtained by

Oliveira et al. ]13[on the deep-snouted pipefish, Syngnathus typhle (2.56 females: 1 male).

The dominance of females in other syngnathid species populations has been described by

other authors ]16 -18[. This means that there is a difference in availability of both sexes for

fishery. ] Mendonça et al.[19[mentioned that, this may be due to a spatial segregation of

sexes or because of different behavior in relation to the fishing gear.

The present study showed that, the observed and calculated length at the first sexual

maturity was about 7.9 cm for male T. bicoarctatus. Also, length classes 11and 12 cm have

the highest percentages of pregnancy. It means that, both of maturity state and pregnancy are

correlated with fish length. The total length at which the brood pouch develops is very

variable, as described by Watanabe and Watanabe ]20[ for Syngnathus schlegeli and Oliveira

et al. ]13[ for Syngnathus typhle. On the other hand, the presence or absence the brood pouch

of T. bicoarctatus to differentiate between mature or immature male shows similarities with

other species in this family ] 13, 20 - 22[.

In the present study, each of male parental care, fertilizing and arrangement of eggs/

embryos inside brooding pouch are similar to that obtained by Drozdov et al. ]23 [ and

Movchan ]24[. However, ]25[ mentioned that, the males of Primor’e pipefish Syngnathus

acusimilis are polygamous species have rather large brood pouches. In contrast, ]26 [ found

that embryos removed from the brood pouch completed normal development and don't

primarily depend on paternal nourishment in Syngnathus scovelli.

The present study showed that, the male fecundity (egg/embryos) of T. bicoarctatus

with total length in pregnant males was found to be strongly correlated (0.86) and the relation

with body weight was weakly correlated (0.40). In contrast, a very weak relationship was

found between egg number of pregnant males and standard length as described by Lyons &

Dunne ]27[ for Nerophis lumbriciformis and by Gasparini & Teixeira ]28[ for Syngnathus

scovelli.


74

The present study concluded that T. bicoarctatus in Lake Qarun has lengthy breeding

season extended from December to April, with the peak of male fecundity recorded during

February.

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مصز ،فى بحيزة قارون( تزاكيزامفوس بايكواركتاتش) األوبوبيتبيولوجيت التكاثز لذكور األصماك

محزم عادل دمحم عفيفى ، حضه مشحوث دمحم خلف هللا ،*أحمد مضعد عزب

.يصش –انقاشة -يذت صش -جايعت األصش -كهت انعهو - قسى عهى انحا -مسا األبحاس انو شعبت عه

قذف بحشة قاس بحافظت انفو يصش األببت بنجت انخكارش نزكس األمسا دسامست ذف زا انبحذ ان

، انزكس ان انضج انجس صف عذدانز صم عذ انطل ، سبت انزكش ان االاد اححذذ حضج عاصش انذسامست

األبت شعات كزنك ان، انخخهفتانشس خالل تانص تانطن نهجعاثبانسبت اناضجت هزكسانخكشاس نخصع ان

انحايم. نزكسذ ان الخصابتا عذ انزكس

. قذ 3125إن فبش 3124ف انفخشة ي دسبش قاس ي بحشة ي األمسا األببت عت 2325 عجححى

٪(. كاج 63.14فشدا ي األاد بسبت ) 314٪( 53.14فشدا ي انزكس بسبت ) 622انعاث ز ي إجان ا جذ

خشة انذسامست. ف جانا أ مساء ششا ،(2: 2) تانخقعانسبت ع جخخهفاانخ (، 2:2.43انزكس ) :سبت اإلاد

قذ . مسى3.4 % ي انزكس ان انضج انجس انكايم61انطل انز صم عذ أظشث انذسامست أقذ

انزكس اناضجت عاث قذ ظشثطل انص. انكم ي بشكم يهحظ يع صادة ت جسا ضجاانزكس انأعذاد صادث

بشم.أحخ ي دسبش انفخشة جت ف األأ انبض بذاخه ححمانحضات انز عه كس انخ ححخ انزكسكزنك

حذ أ ، غش عادت حشاكشايفس باكاسكخاحس األببت انسكتركس انشعات األبت ف أضحج انذسامست أ

انخصب ف انبض ضعانز خى ت عه انبط؛ جهذعباسة ع صائذة انبض بذاخه انزكش خهك كس نحضات

. انكسيخخهفت ف فس حطسانبض يشاحم اقذ ك نز ؛طنتانششائظ ان ي رالرتأ ارعه شكم


76

فخشةخالل ركش( 222انحايم )انزكس أكاس ف تيخصب تبض 3247خائج االخصابت نذ انزكس مسجهج

إن انص. بانسبت ا ضعف إسحباطا إن طل األمسا انسبت ب قا ف انزكس إسحباطا االخصابت جاسحبطقذ انذسامست.

ذذ انفخشة حححى كا . احذان انكسف ج ا بضت 222 53 عذاد انبض أ األجت ف انكس يا ب أ حشاحجزا

انزسة خالل شش فبشاش. ي دسبش ان ابشم كاج األببت انسكتزكس اإلجابت ن

61-76 moharm2

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