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The reproductive biology of Parhyale basrensis Salman (Crustacea, Amphipoda) in the Shatt al-Arab river
Estuarine,
--
Coastal
and Shelf
(1986) 23,339-351
Science
The Reproductive Biology of Parhyale basrensis Salman (Crustacea, Amphipoda) in the Shatt al-Arab River
Malik Marine Received
H. Ali and Salman Science 28 May
Centre,
University
D. Salman of Basrah,
198.5 and in revised
form
Basrah,
11 October
IRAQ 1985
Keywords: Reproductivebehaviour,Amphipoda, Shatt al-Arab Basicbiologicalinvestigationson the intertidal amphipodFarhyale basrensis are made.The incubation period is l-2 weeks.The generationtime is 5-6 weeks. Femalesproduceat least4 broodsbeforethey die. The numberof eggscarriedby the femaleis a linear function of size of the female.Egg numbersvaries from 4-37. Maturity occursat a sizeof 4 mm for the femaleand45 mm for the male. The breeding seasonis extending from late February to late November or December.Recruitment startsat the beginningof May. Successive broodsmay have different life spans.The maximum life spanof the population is 13-15 monthsandthe minimumlife spanis6-7 months.
Introduction basrensis Salman, is a common speciesof talitrid amphipod in the Shatt al-Arab region. It inhabits the intertidal zone of the river and its tributaries; it is also found subtidally. It is frequently found on the river bank under stones,inside burrows of isopods or underneath vegetation carried by the tide. Although it is one of the fairly common speciesof crustaceans found in the region, it has only recently been named (Salman, in press). The present study aimed to investigate someaspectsof its basic biology. Purhyule
The sampling site and habitat The sampling site is an areaof about 20 m long of the river bank. It is located just opposite the Sailo of Basrah, near Al-Chibassy tributary where the intertidal zone is muddy. The amphipods were found along a narrow strip near the hightide mark. They tend to aggregate beneath stonesprotecting them from desiccation during the period of low tide. Shatt al-Arab in this region, is an oligohaline brackish water of a comparatively high temperature during summer and moderately low temperature during winter. It is also influenced by the semidiurnal tide of the Arabian Gulf. Different parts of the river surveyed for the presence of the amphipod. Animals were found among aquatic vegetation or sharing the burrows of the isopods Sphaeroma annandalei annandalei Stebbing, and Annina mesopotamica (Ahmed). 339 027;!-77
14/86/090339
+ 13 $03.00/O
Q 1986 Academic
Press Inc (London)
Limited
340
M.
H. Ali
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TABLE 1. Arbitrary Stage I Stage II Stage III Stage IV Stage V
development
stages for Parhyale
basremis
broods
Yolk cells Early blastula or embryonic tissue partly or wholly enveloping yolk cells. Caudal furrow present and limb segmented. Eye rudiments present or pigmented and appendages complete. Brood hatched.
Among the other macro-invertebrates found in the same habitat as the amphipod are: the crab Sesarma boulengeri Calman, the gastropods Melanopsis nodosa Ferussac, Melanoides tuberculata (Miiller), Theodoxus jordani (Sowerby), Gyraulus convexisculus (Hutton), Viviparus bengalensis Lamarck, Lymnaea tenera euphratica (Mousson), the bivalves Corbiculafluminalis (Miiller) and Corbiculafluminea (Miiller) and someannelids. Materials
and methods
This study is based on materials collected monthly in the intertidal zone in the period between April 1983 to September 1984. Samples were taken in quadrats (25 x 25 cm) during low tide. Two quadrats were taken every time. Stones and the animalsunderneath, together with mud from the substratum were removed to a depth of about 5 cm. Each samplewas then placed in a separateplastic bag, preserved in 40/oformalin and brought to the laboratory where sorting through a 0.425 mm mesh-sized sieve was done. This mesh-size was fine enough to retain all stagesof the amphipod. Total length measurements, from anterior margin of head to posterior end of telson, were taken to the nearest 0.5 mm with the aid of a binocular stereomicroscope fitted with an eye-piece micrometer. Animals were grouped into 1 mm size classes. Sexual dimorphism occurs in Parhyale basrensis; the male possessan expanded 2nd gnathopod, while the female is provided with oostegites. The determination of the reproductive status of the female was done on the basisof the condition of oostegite setae. The presence of oostegites with fringes of long setae is characteristic of females in the breeding condition (Hynes, 1954; 1955; Bregazzi, 1972; Hynes & Harper, 1972; Miller, 1982). In males, the number of flagellar articles of the 1st antenna were used in determining the reproductive states. It has long been known that, in the gammaridean amphipods, the number of flagellar articles of the 1st antenna increasesin the processof growth (Sexton, 1924). Recently too, Miller (1982) hasused the number of flagellar articles in determining the sexual maturity of male amphipods. Following the procedure of Miller (op. cit.) 55 pairs in precopula were collected during June and July 1984 and the males and females were separatedand preserved. The number of flagellar articles of normal 1st antennae of maleswere counted and the total length of the amphipods were measured. Eggs were removed from the brood pouch of each ovigerous female, counted and staged, arbitrarily, to the developmental stageslisted in Table 1. Egg dimensions were recorded as f(length+ width). Different generations were separated by the method of probability analysis described by Harding (1949) and modified by Cassie(1954). The two sexeswere treated separately while the unsexed individuals were divided equally between males and females (seeresults). Monthly air and water temperatures were recorded.
341
Reproductive biology of Parhyalebasrensis
TABLE 2. Air and water temperatures in “C taken between April 1983September 1984 Date
Air temperature
11 April 1983 11 May 1983 16 June 1983 24 July 1983 20 Aug 1983 24 Sep 1983 25 Ott 1983 26 Nov 1983 29 Dee 1983 23 Jan 1984 28 Feb 1984 31 March 1984 15 May 1984 8 June 1984 10 July 1984 25 Aug 1984 25 Sep 1984
20 22 33 33 32 22.5 22 18 12 11.5 15 17 20.5 29.5 35 30 26
on the day of sampling
Water
in the period
temperature 22 27 29 29 30 23 25 20.5 13 14 18.5 21 28.5 22 27 27 24
Results Air and water temperatures at the time of sampling are shown in Table 2. The water temperature ranged from 13°C in December 1983 to 30°C in August 1983. Sexual
maturity
In P. basrensis, the four pairs of oostegitesmake their first appearancein femaleswith body length of about 3-5 mm. Further examination of femalesin precopula and specimensfrom regular monthly samples showed that mature oostegites did not appear until females reached a length of 4 mm. The results of the 55 pairs in precopula shows that the attainment of sexual maturity in malesoccurred when there are 8 or more flagellar articles in the 1st antenna. This is equivalent to the size of 4.5 mm. Population
structure
The result of probability analysesof data on size-frequency distribution (Figures 1 and 2) for both years indicated that the population of both sexes were monomodal during November-April, trimodal in May and June, and bimodal in the period from JulyOctober. The presence of three generations during May and June may be justified on the basis that the old generation can produce two successivebroods in about 30 days. It was found that femalescarrying eggsin an advanced stageof development in their brood pouchescan have well developed oogonia in their ovaries. It is also apparent from Figures 1 and 2, that 50”, of the first brood may reach a size of about 5 mm in the middle of May 1983 and the second brood then produced shortly after the releaseof the first one. In the samemonth the old generation of males constituted only 8%, while the other two generations comprised 25% and 67% of male population respectively. In June 1983 the old generation of malesformed about 2O,,and the new generations 4Oq: and 589:) respectively. In July 1983 the old generation disappeared and the new ones comprised 4694 and 54O+,of the male population respectively. The bimodal distributions of the male population remained so until October, 1983. In November 1983 only one generation was present. The monomodal population remained
342
M.
H. Ali
~5 S. D. Salman
1 . ,. 8 6 E
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E
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2
:
8 6
I . 0.1
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90
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.
99 99.5
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I
4
0.1
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1
10
50
90
99
99.!
lO/o 1
Figure 1. Population analysis of Male P. basrensis for the period from April 1983September 1984. Solid circles and curves indicate the distribution of the mean numbers of males in each size-class of the sample. Open circles and straight lines represent the generations.
Reproductive
biology
of Parhyale basrensis
343
10 8 6 4 2 8
8 6
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Jun.
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Jan. 7 Feb. / Mar.
6 4 2 8 6
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Cumulative frequency r% 1 Figure 2. Population analysis of Female P. basrensis for the period from April 1983September 1984. Further explanations as in Figure 1.
sountil the end of April 1984 where the new releasesoccurred. In the rest of the sampling period of 1984the generations followed precisely the samepattern of that of 1983, but with different proportions (Figure 1).
344
M. H. Ali & S. D. Salmatl
In May 1983 the old generation of females comprised about 4”, of the female population, while the other two generations were 16”,, and 800;, respectively (Figure 2). In June 1983 the three generations constituted about 30x0,21O0and 76O,,, respectively. In July 1983 the old generation disappeared and the other generations formed about 36”, and 647; of the female population respectively. In August-October 1983 the female population remained bimodal. In November through April 1984 the population became monomodal, and from May 1984 till the end of the sampling, the female generations repeated the samepatterns of the previous year (Figure 2). Life cycle
The size frequency histograms for samplestaken between April 1983and September 1984 are given in Figure 3. In January all the females in the population were mature and by late February none was found less than 4 mm in length and the modal size-class during the months February, March and April was 5-6 mm. A few gravid females and precopulas were observed during February with largest females breeding first. In late March 1984 and April 1983 the frequency of gravid females increased to 80% and 709, of the total adult females, respectively. Ovigerous females found in April represented those of the old generation which overwintered. The peak of ovigerous females occurred around July of both years represented ovigerous femalesof the new generation. Breeding continued until November where only one ovigerous female was found (Figure 4). The smallest ovigerous female found was 4 mm long and the maximum size of female recorded throughout the whole sampling period was 8.5 mm. Females which hatch in early May, reach a size of about 5 mm by late May. The first die-off of the older femalesin 1983 occurred in June, while in 1984it occurred in July. Females:
In April 1983 only about 5% of the adult males were lessthan 6 mm in length, while in March 1984, none were less than 6mm long. The modal size-class during February-April was 7-8 mm. In May the population showed a great reduction in the numbers of adult males of the old generation. This decreasewas especially in the sizeclass7-8 mm. Adult malesof the new generation become dominant. The newly released juveniles grew rapidly to a size not lessthan 5.5 mm at the end of May. The malesof the new generation reached by June a size of 8.0 mm. The first die-off of larger males(9 mm or more) occurred in July of both years. In November 1983 a second die-off occurred. The maximum size of malesrecorded throughout the sampling period was 10.5 mm. Mules:
The newly hatched amphipods were 1.25-l ‘50 mm long. Individuals lessthan this size were found inside the brood pouch of brooding females. Observations on the growth of juveniles of Purhyale busrensis revealed that the secondary sexual characters appeared at a size of 3.5 mm, with evidence that the growth in maleswas more rapid than in females. The new generation appeared in May of both years. The releaseof juveniles remained steady in June of both years, but there was a rapid increase in numbers of the newly hatched amphipod in July of the two years, and a slightly lesspronounced peak in September 1983. Therefore, three peaksof releaseoccurred in the population throughout the breeding season.The first peak of May was the result of the breeding activity of the old generation. The other two peaksof July and September were produced by females of the new generation. No sign of releaseof juveniles was observed in the period between
Juvendes:
Reproductive biology
-3
L7
ri““,“,G RIn13
11
Allr
-2 4
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6-
8- 1012 .-.-
20 AUP.
1
345
of Parhyale basrensis
2
4
6 8 10 12
2
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4
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a Jun.
In
8
Ian. 1984
120
-
100
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16 Jul. 8
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80
I.,
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6 8 1012
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63
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2 4 6 8 1012 2 4 6 8 1012 Tote1 length mm
2 4 6 8 IO
Figure 3. Size frequency distribution of I’. basrensis in the Shatt al-Arab River. Juveniles (dotted, upper); males (unshaded, upper); non ovigerous females (unshaded, lower); ovigerous females (black, lower). Numbers inside circles represent number of specimens collected. January-April. However in February and the following two months the number of ovigerous females gradually increased (Figures 3 and 4). Therefore the breeding season was found to extend from late February to late November or early December. Egg size and incubation period The mean diameter of ova (68 ova) of P. basrensis was estimated to be 0.387 mm f 0.061. Amphipod broods were counted and classified into five arbitrary developmental stages
346
M.
H. Ali
& S. D. Salman
80
70 60 50 L 0 0 f Z
LO
30 20 IO
Figure 4. Mean numbers the period of sampling. 3. Means over a year
TABLE
Female size (mm) Mean number of eggs with S.E.
4.0 4.9 kO.3
of ovigerous
and standard
4.5 5.9 kO.26
error
5.0 7.4 kO.35
females of P. basrensis in every
for egg counts of Parhyde
5.5 9.2 kO.46
6.0 12.8 kO.75
6.5 18.3 f3.2
sample throughout
basrensis females
7.0 17.0 k1.79
7.5 23.5 k2.77
averaged
8.0 31.0 k5.1
(Table 1). The mean numbers of each brood developmental stage in each monthly sample for the period between April 1983September 1984 were calculated. These data suggest that the incubation time was very short and to determine the incubation period 8 pairs in precopula were maintained in the laboratory during October 1984 (temperature 2529°C). After about two days the males and females separated, the females moulted and eggs appeared in the brood pouch. Ovigerous females were then put in glass dishes. Water was changed every day and food (water plants) was supplied. The release of juveniles began on the 8th day and by the 10th day all females were found to have empty brood pouches. Fecundity Table 3 shows the mean and standard error of the number of eggs produced by each size-class of females. It is evident that the number of eggs was a linear function of the size of the female. The relationship can be expressed by the following linear regression equation: Number
of eggs = (total
length
r = 0.866;
in mm)
5.499
- 19.324;
df 237
The number of eggs/female in the samples ranged from 4 eggs carried by a female of 4 mm total length to 37 eggs carried by a female 8.0 mm long. Females with 4 eggs comprised about 10% of the total gravid females. It seems likely that females with fewer than 4 eggs in their brood chambers, had lost eggs during the process of sampling and preservation. Sex ratio Analysis of sex ratio for the size class 3-4 mm, i.e. the size at which sexual dimorphism is possible, shows no significant difference at the 5 y0 level between the two sexes for most of
Reproductive
biology
of
Parhyale basrensis
347
TABLE 4. Numbers of males and females P. barrensis for every generation sample with the X2 values (significant values indicated by a star)
Date 11 Apr 1983 11 May 1983
16 Jun 1983
24 July 1983 20 Aug 1983 24 Sep 1983 25 Ckt 1983 26 29 23 28 31 15
Nov 1983 Dee 1983 Jan 1984 Feb 1984 Mar 1984 May 1984
8 Jun 1984
10 Jul 1984 25 Aug 1984 25 Sep 1984
Generation A A B C A B c B C B C B C B C C c C C C C D E C D E D E D E D E
No. of males
No. of females
Total no.
53 11 46 0 3 70 0 95 103 67 79 51 69 63 148 154 97 36 64 34 12 50 9 16 123 6 111 78 41 38 33 33
36 2 43 0 1 33 0 56 84 39 78 23 57 20 114 170 108 21 38 24 11 42 10 8 103 8 82 49 31 35 16 37
89 13 89 0 4 103 0 151 187 106 157 74 126 83 262 324 205 57 102 58 23 92 19 24 226 14 193 127 72 73 49 70
at each
monthly
X2 3.25 6.30* 0.111 1.24 13.29* 10,08* 1.92 7.39* 0.01 10.60* 1.15 22.28* 4,40* 0.78 0.58 3.96* 6,34* 1.73 0.08 0.70 0.10 2.70 1.76 0.35 4.36* 6.62* 1.40 0.12 5.91* 0.23
the samples, except in October and December 1983 when females outnumbered males 1.7: 1 (X2 = 4.10, P> 0.05) and 4.8: 1 (X2 = 7.21, P> 0.05), respectively. However, the sample of December was very small (n = 14), so these differences in the sex ratio may be entirely due to difficulties in identification of juvenile males. Moreover, the cumulative sex ratio of this size-class for the whole period of sampling was not significant (X’ = 3.6, PC: 0.05). An attempt was then made to calculate the sex ratio for each year-class to follow the changes in proportions of each sex in different generations. The data are presented in Table 4. It is evident that different generations have different sex ratios. The males of the short-lived generation B were significantly more than females of the same generation, but not significantly so in May 1983. In generation C, which have a life span of 11 months, the females only exceeded the males in November and December 1983, but the difference was not significant. The males significantly outnumbered the females only in October 1983, January and February 1984. The D-generation of May 1984, which corresponds to B-generation of May 1983, shows a predominance of males over the females, but significantly so in July and September 1984. In the E-generation, which corresponds to C-generation of 1983, a significant difference was only obtained in July 1984. In
348
M. H. Ali & S. D. Salmarr
September 1984, the numbers of females rose slightly, but the difference was not significant. The sex ratio for each sample, irrespective of generations, showsthat there is an overall preponderance of males over the females, except possibly in November and December 1983, when females slightly but not significantly, outnumbered the males. Moreover, significant differences of the ratio of males to the females were obtained in most of the samples,particularly in the year 1983. However, the cumulative sex ratio of malesto the females for the whole period of sampling was estimated to be 1.31 which is statistically significant (X2 = 54.027, P> 0.005) from the hypothetical ratio 1:1. Discussion It is evident from the present observation&rat the breeding seasonof Purhyale basrensis in the Shatt al-Arab region extends from late February to late November or early December. Although, no gravid femaleswere encountered in December, yet individuals in precopula were observed to occur in late December 1984 in an area further to the north of the sampling site. The incubation time of this speciesmay exhibit seasonalvariations depending largely on temperature. In a laboratory experiment during October 1984, the incubation period was found to be 8-10 days. However, at the beginning of the breeding seasonthe incubation period may be much longer than that at any other time of the season,and this probably accounted for the low water temperature (Table 1). A similar result was obtained by Nilsson (1977) who found that the incubation time for Gammaruspulex was60 days at 5°C and 100 days at 0°C. Moreover, Hiwatari & Kajihara (1984) found that the duration of egg development of Hyale barbicornis varies from about 26 days at 12°C to about 7 days at 28°C.
The mean eggsize of P. basrensis is 0.387 mm. This is quite similar to that of Parhyalella Schellenberg from Madagascar, which is 0.392 mm (Steele, 1973). These egg sizes are small when compared with data from Wildish (1979) on the eggs of some talitrid species vis’ Orchestia cavimana, 0.69 mm; 0. remyi roffensis, 0.62 mm; 0. mediterranea mediterranea, 0.72 mm; 0. mediterranea aestuarensis, 0.72 mm. The potential advantages of having small eggswere discussedby Van Dolah and Bird (1980). As a result of possessingsmall eggsthe incubation time is shortened, ultimately the time of attainment of sexual maturity might be short (Van Dolah & Bird, 1980). The time lapse from hatching to sexual maturity for female P. basrensis is about 3-4 weeks which is the time between the first peak of releaseof juveniles and the rise in numbers of sexually matured femalesof the new generation in May (Figure 4). The generation time therefore, is 5-6 weeks. This seemsto agree very much with reports on someother talitrid amphipods from tropical and subtropical regions such asParhyalella pietschmanni Schellenberg from Madagascar in which the generation time is 5-6 weeks (Steele, 1973). Moreover, Talorchestia margaritae, from Venezuela, reached aminimum reproductive size 2-3 weeks after hatching (Venables, 1981) and Hyale barbicornis, from Japan, attained sexual maturity in about 29 days (Hiwatari & Kajihara, 1984). However, the generation time in polar and temperate amphipods (seeTable V in Bregazzi, 1972) is usually more than those of tropical and subtropical speciesin general, and of P. basrensis in particular. As a result of relatively short incubation time (l-2 weeks), female P. basrensis may produce more than one brood in the breeding season.Moreover it was found that the female of this speciesbecome sexually mature at a size of 4 mm. Therefore, those females
pietschmanni
Temperate Ampelisca macrocephala Lilljeborg Gammarus p&x L. Gammarus duebeni Lilljeborg Gammarus pulex pulex (L.) Gammarus lacustris Sars Gammarus fasciatus Say Gammarus pseudolimnaeus Bousfield Corophium volutator (Pallas) Subtropical Hyale barbicotnis Hiwatari & Kajihara Austrochitonia australis (Sayce) Parhyale basrensis Salman Australia Iraq
Japan
Denmark Denmark U.K. U.K. U.K. U.K. Canada Sweden
Antarctic Antarctic
(Pfeffer) (Miers)
Polar Cheirimedonfemoratus Tryphosella kergueleni
of some amphipods
Locality
strategy
Species
TABLE 5. Reproductive
from
different
2-9 months 2 9 months 6-14 months
15-2 years 1-2 years 15-18months 13-14 months 15-16 months 13-15 months 15 months 5-7 months
3 years 4 years
Life history
latitudes
Semiannual Semiannual Semiannual
Annual Annual Annual Semiannual Annual Semiannual Annual Semiannual
Biannual Biannual
Type of life history
(1972) (1972)
(1955)
Hynes
Hiwatari Smith
& Kajihara (1984) & Williams (1983) Present study
Hynes & Harper (1972) Mliller 81 Rosenberg (1982)
(1954)
Hynes
Kanneworff (1965) Iversen & Jessen (1977)
Bregazzi Bregazzi
Reference
350
M.
H. Ali
& S. D. Salman
released early in the season, in May, may be able to produce at least 4 broods before they die in August (Figure 4). In addition, those females released early in November 1983, overwintered and reached maturity in February or March 1984. They may produce 4 broods before they die in July 1984. Other species, for instance, Gammarus duebeni in Southern England, may produce 4-7 broods (Sheader, 1983). The sex ratio may be affected by three mechanisms: the migration of one sex out of the habitat, the balance between the sex ratio of the recruitment, the differential mortality. There is no evidence of migration of one of the two sexesout of the adult habitat in P. basrensis, nor is there any dramatic change of body form seenin someother amphipods as Ampelisca macrocephala Lilljeborg (Kanneworff, 1965). Furthermore, there is always balanced production of the two sexesat recruitment. It is likely, therefore, that the differential mortality is the mechanism which regulates sex ratio in this species. The sizefrequency distribution indicates that mortality amongst females produced in 1983 is higher than that of femalesof 1984. The present account might suggestthat the life cycle of P. basrensis, in the Shatt al-Arab region, extended from May of one year to June of the next year, giving a life span of 13-14 months. However, since there were three peaks of brood release,in May, July and September 1983, it is more likely that the oldest individuals present in June 1984 were the remnants of the last peak of release(September 1983). The disappearancein July of the old generation of the bimodal population of June of both years may support this assumption. Therefore, the overall life span is more likely to have been 9-10 months. Furthermore, evidence from probability analysis indicated that mortality in November, probably, represents the die-off of the first peak of releasein May. Hence the life span of this brood may be only 6-7 months. This difference in the life span of successivebroods of the same specieshas also been noticed in Gammarus pseudolimnaeus Bousfield (Miller, 1982) and in Corophium volutator (Pallas) (Moller & Rosenberg, 1982) and in Hyale barbicornis Hiwatari and Kajihara (Hiwatari & Kajihara, 1984). It can be concluded therefore, that P. basrensis, has a semiannual life history, whereby young produced early in the growing seasonmature during the sameseasonand yield a second or more generations during that season (Wildish, 1982). This reproductive strategy is well known in temperate and, particularly, tropical species (Table 5). An adaptation of this kind probably corresponds to the long period of food availability and suitable temperature which give the animals more chance to produce successive generations in a short period, in contrast to high latitude localities where temperatures are lower and there are shorter periods of food availability. Acknowledgements We are grateful to the skipper and crew of R. V. ‘Jamiat Al-Basrah’ for assistancein sampling and Miss V. K. Al-Bazzi and Mrs. Nidhall Jabbar for help in the laboratory. Thanks are due to Dr Y. T. Daoud of the department of Biology for reading the manuscript. References Bregazzi,P.
K. 1972 Life cycles and seasonal movements of Cheirimedon femorarus kergueleni (Miers) (Crustacea: Amphipoda). British Antarctic Survey Bulletin Cassie, R. M. 1954 Some uses of probability paper in the analysis of size frequency Journal of Marine and Freshwater Research $513-522.
(Pfeffer) and Tryphosellu 30, l-34. distributions. Australian
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Parhyale basrensis
351
Harding, J. I?. 1949 The use of probability paper for the graphical analysis of polymodal frequency distributions. Journal of the Marine Biological Association of the United Kingdom 28, 141-153. Hiwatari, T. & Kajihara, T. 1984 Population dynamics and life cycle of Hyale barbicornis (Amphipoda, Crustacea) in a blue mussel zone. Marine Ecology-Progress Series 20,177-183. Hynes, H. B. N. 1954 The ecology of Gammarus duebeni Lilljeborg and its occurrence in fresh water in western Britain. Journal of Animal Ecology 23,38-84. Hynes, H. B. N. 1955 The reproductive cycle of some British fresh water Gammaridae. Journal of Animal Ecology 24(2), 352-387. Hynes, H. B. N. & Harper, F. 1972 The life histories of Gammarus lacustris and G. pseudolimnaeus in southern Ontario. Crustaceana (Supplement] 3,329-341. Iversen, T. M. & Jessen, J. 1977 Life cycle, drift and production of Gammarus pulex L. (Amphipoda) in a Danish spring. Freshwater Biology 7,287-296. Kanneworff, E. 1965 Life cycle, food, and growth of the amphipod Ampelisca macrocephala Lilljeborg from the Oresund. Ophelia 2(2), 305-318. Miller, S. A. 1982 The life history of Gammarus pseudolimnaeus Bousfield in a central Wisconsin Stream (Amphipoda: Grammaridea). Crustaceana 43(l), 89-99. Moller, P. & Rosenberg, R. 1982 Production and abundance of the amphipod Corophium volutator on the west coast of Sweden. NetherlandsJournal of Sea Research 16, 127-140. Nilsson, L. M. 1977 Incubation time, growth and mortality of the amphipod Gammarus pulex under laboratory conditions. Oikos 29,93-98. Salman, S. D. (in Press) Parhyale basrensis, a new species of talitrid amphipod from Shatt al-Arab region. Crustaceana. Sexton, E. W. 1924 The moulting and growth-stages of Gammarus, with descriptions of the normal and intersexes of G. chevreuxi. Journal of the Marine Biological Association of the United Kingdom 13(2). 340-401. Sheader, M. 1983 The reproductive biology and ecology of Gammarus duebeni (Crustacea: Amphipoda) in Southern England. Journal of the Marine Biological Association of the United Kingdom 63,517-540. Smith, M. J. & Williams, W. D. 1983 Reproduction cycles in some freshwater amphipods in southern Australia. In Papersfrom the Conferenceon the Biology and Evolution of Crustacea (Lowry, J. K.,ed.). The Australian Museum Memoir, 18,183-194. Steele, D. H. 1973 The biology of Parhyalellapietschmanni Schellenberg, 1938 (Amphipoda: Hyalellidae) at Nosy Be, Madagascar. Crustaceana 25(3), 276-280. Van Dolah, R. F. & Bird, E. 1980 A comparison of reproductive patterns in epifaunal and infaunal gammaridean amphipods. Estuarine and Coastal Marine Science 11,593-604. Venables, B. J. 1981 Aspects of the population biology of a Venezuelan beach amphipod, Talorchestia margaritae (Talitridae), including estimates of biomass and daily production, and respiration rates Crustaceana 41(3), 271-286. Wildish, D. J. 1979 Reproductive consequences of the terrestrial habit in Orchestia (Crustacea: Amphipoda) InternationalJournal of Invertebrate Reproduction 1,9-20. Wildish, D. J. 1982 Evolutionary ecology of reproduction in gammaridean amphipoda. InternationalJourna! of Invertebrate Reproduction 5,1-19.
--
Coastal
and Shelf
(1986) 23,339-351
Science
The Reproductive Biology of Parhyale basrensis Salman (Crustacea, Amphipoda) in the Shatt al-Arab River
Malik Marine Received
H. Ali and Salman Science 28 May
Centre,
University
D. Salman of Basrah,
198.5 and in revised
form
Basrah,
11 October
IRAQ 1985
Keywords: Reproductivebehaviour,Amphipoda, Shatt al-Arab Basicbiologicalinvestigationson the intertidal amphipodFarhyale basrensis are made.The incubation period is l-2 weeks.The generationtime is 5-6 weeks. Femalesproduceat least4 broodsbeforethey die. The numberof eggscarriedby the femaleis a linear function of size of the female.Egg numbersvaries from 4-37. Maturity occursat a sizeof 4 mm for the femaleand45 mm for the male. The breeding seasonis extending from late February to late November or December.Recruitment startsat the beginningof May. Successive broodsmay have different life spans.The maximum life spanof the population is 13-15 monthsandthe minimumlife spanis6-7 months.
Introduction basrensis Salman, is a common speciesof talitrid amphipod in the Shatt al-Arab region. It inhabits the intertidal zone of the river and its tributaries; it is also found subtidally. It is frequently found on the river bank under stones,inside burrows of isopods or underneath vegetation carried by the tide. Although it is one of the fairly common speciesof crustaceans found in the region, it has only recently been named (Salman, in press). The present study aimed to investigate someaspectsof its basic biology. Purhyule
The sampling site and habitat The sampling site is an areaof about 20 m long of the river bank. It is located just opposite the Sailo of Basrah, near Al-Chibassy tributary where the intertidal zone is muddy. The amphipods were found along a narrow strip near the hightide mark. They tend to aggregate beneath stonesprotecting them from desiccation during the period of low tide. Shatt al-Arab in this region, is an oligohaline brackish water of a comparatively high temperature during summer and moderately low temperature during winter. It is also influenced by the semidiurnal tide of the Arabian Gulf. Different parts of the river surveyed for the presence of the amphipod. Animals were found among aquatic vegetation or sharing the burrows of the isopods Sphaeroma annandalei annandalei Stebbing, and Annina mesopotamica (Ahmed). 339 027;!-77
14/86/090339
+ 13 $03.00/O
Q 1986 Academic
Press Inc (London)
Limited
340
M.
H. Ali
& S. D. Sahan
TABLE 1. Arbitrary Stage I Stage II Stage III Stage IV Stage V
development
stages for Parhyale
basremis
broods
Yolk cells Early blastula or embryonic tissue partly or wholly enveloping yolk cells. Caudal furrow present and limb segmented. Eye rudiments present or pigmented and appendages complete. Brood hatched.
Among the other macro-invertebrates found in the same habitat as the amphipod are: the crab Sesarma boulengeri Calman, the gastropods Melanopsis nodosa Ferussac, Melanoides tuberculata (Miiller), Theodoxus jordani (Sowerby), Gyraulus convexisculus (Hutton), Viviparus bengalensis Lamarck, Lymnaea tenera euphratica (Mousson), the bivalves Corbiculafluminalis (Miiller) and Corbiculafluminea (Miiller) and someannelids. Materials
and methods
This study is based on materials collected monthly in the intertidal zone in the period between April 1983 to September 1984. Samples were taken in quadrats (25 x 25 cm) during low tide. Two quadrats were taken every time. Stones and the animalsunderneath, together with mud from the substratum were removed to a depth of about 5 cm. Each samplewas then placed in a separateplastic bag, preserved in 40/oformalin and brought to the laboratory where sorting through a 0.425 mm mesh-sized sieve was done. This mesh-size was fine enough to retain all stagesof the amphipod. Total length measurements, from anterior margin of head to posterior end of telson, were taken to the nearest 0.5 mm with the aid of a binocular stereomicroscope fitted with an eye-piece micrometer. Animals were grouped into 1 mm size classes. Sexual dimorphism occurs in Parhyale basrensis; the male possessan expanded 2nd gnathopod, while the female is provided with oostegites. The determination of the reproductive status of the female was done on the basisof the condition of oostegite setae. The presence of oostegites with fringes of long setae is characteristic of females in the breeding condition (Hynes, 1954; 1955; Bregazzi, 1972; Hynes & Harper, 1972; Miller, 1982). In males, the number of flagellar articles of the 1st antenna were used in determining the reproductive states. It has long been known that, in the gammaridean amphipods, the number of flagellar articles of the 1st antenna increasesin the processof growth (Sexton, 1924). Recently too, Miller (1982) hasused the number of flagellar articles in determining the sexual maturity of male amphipods. Following the procedure of Miller (op. cit.) 55 pairs in precopula were collected during June and July 1984 and the males and females were separatedand preserved. The number of flagellar articles of normal 1st antennae of maleswere counted and the total length of the amphipods were measured. Eggs were removed from the brood pouch of each ovigerous female, counted and staged, arbitrarily, to the developmental stageslisted in Table 1. Egg dimensions were recorded as f(length+ width). Different generations were separated by the method of probability analysis described by Harding (1949) and modified by Cassie(1954). The two sexeswere treated separately while the unsexed individuals were divided equally between males and females (seeresults). Monthly air and water temperatures were recorded.
341
Reproductive biology of Parhyalebasrensis
TABLE 2. Air and water temperatures in “C taken between April 1983September 1984 Date
Air temperature
11 April 1983 11 May 1983 16 June 1983 24 July 1983 20 Aug 1983 24 Sep 1983 25 Ott 1983 26 Nov 1983 29 Dee 1983 23 Jan 1984 28 Feb 1984 31 March 1984 15 May 1984 8 June 1984 10 July 1984 25 Aug 1984 25 Sep 1984
20 22 33 33 32 22.5 22 18 12 11.5 15 17 20.5 29.5 35 30 26
on the day of sampling
Water
in the period
temperature 22 27 29 29 30 23 25 20.5 13 14 18.5 21 28.5 22 27 27 24
Results Air and water temperatures at the time of sampling are shown in Table 2. The water temperature ranged from 13°C in December 1983 to 30°C in August 1983. Sexual
maturity
In P. basrensis, the four pairs of oostegitesmake their first appearancein femaleswith body length of about 3-5 mm. Further examination of femalesin precopula and specimensfrom regular monthly samples showed that mature oostegites did not appear until females reached a length of 4 mm. The results of the 55 pairs in precopula shows that the attainment of sexual maturity in malesoccurred when there are 8 or more flagellar articles in the 1st antenna. This is equivalent to the size of 4.5 mm. Population
structure
The result of probability analysesof data on size-frequency distribution (Figures 1 and 2) for both years indicated that the population of both sexes were monomodal during November-April, trimodal in May and June, and bimodal in the period from JulyOctober. The presence of three generations during May and June may be justified on the basis that the old generation can produce two successivebroods in about 30 days. It was found that femalescarrying eggsin an advanced stageof development in their brood pouchescan have well developed oogonia in their ovaries. It is also apparent from Figures 1 and 2, that 50”, of the first brood may reach a size of about 5 mm in the middle of May 1983 and the second brood then produced shortly after the releaseof the first one. In the samemonth the old generation of males constituted only 8%, while the other two generations comprised 25% and 67% of male population respectively. In June 1983 the old generation of malesformed about 2O,,and the new generations 4Oq: and 589:) respectively. In July 1983 the old generation disappeared and the new ones comprised 4694 and 54O+,of the male population respectively. The bimodal distributions of the male population remained so until October, 1983. In November 1983 only one generation was present. The monomodal population remained
342
M.
H. Ali
~5 S. D. Salman
1 . ,. 8 6 E
4
E
2
z
2
:
8 6
I . 0.1
10
1
.
50
90
.
.
99 99.5
Cumulative
I
4
0.1
frequency
1
10
50
90
99
99.!
lO/o 1
Figure 1. Population analysis of Male P. basrensis for the period from April 1983September 1984. Solid circles and curves indicate the distribution of the mean numbers of males in each size-class of the sample. Open circles and straight lines represent the generations.
Reproductive
biology
of Parhyale basrensis
343
10 8 6 4 2 8
8 6
6 4 2
4 2
Jun.
3% 8
Jan. 7 Feb. / Mar.
6 4 2 8 6
Jul.
361 10
4 E
Mav.
6%
8
2
EE6 4
ES
Aug.
48%
zhs =4
f2 z
2 I
z
2
Sep.
c"8
2
I749
6 4 2
0
Oct.
.
8 6 4
Jun.
c”8
26%
6 4
12 10
&??c,
I
10
Jul.
46%
8 6 4
2
2
Aug.
8 6
,fi%
4 2
I
8 6 4 2
8 6 4 2 0.1
IO
60
90
99
99.9
27;
Sep.
73: + 0.1
10
50
90
9999.9
Cumulative frequency r% 1 Figure 2. Population analysis of Female P. basrensis for the period from April 1983September 1984. Further explanations as in Figure 1.
sountil the end of April 1984 where the new releasesoccurred. In the rest of the sampling period of 1984the generations followed precisely the samepattern of that of 1983, but with different proportions (Figure 1).
344
M. H. Ali & S. D. Salmatl
In May 1983 the old generation of females comprised about 4”, of the female population, while the other two generations were 16”,, and 800;, respectively (Figure 2). In June 1983 the three generations constituted about 30x0,21O0and 76O,,, respectively. In July 1983 the old generation disappeared and the other generations formed about 36”, and 647; of the female population respectively. In August-October 1983 the female population remained bimodal. In November through April 1984 the population became monomodal, and from May 1984 till the end of the sampling, the female generations repeated the samepatterns of the previous year (Figure 2). Life cycle
The size frequency histograms for samplestaken between April 1983and September 1984 are given in Figure 3. In January all the females in the population were mature and by late February none was found less than 4 mm in length and the modal size-class during the months February, March and April was 5-6 mm. A few gravid females and precopulas were observed during February with largest females breeding first. In late March 1984 and April 1983 the frequency of gravid females increased to 80% and 709, of the total adult females, respectively. Ovigerous females found in April represented those of the old generation which overwintered. The peak of ovigerous females occurred around July of both years represented ovigerous femalesof the new generation. Breeding continued until November where only one ovigerous female was found (Figure 4). The smallest ovigerous female found was 4 mm long and the maximum size of female recorded throughout the whole sampling period was 8.5 mm. Females which hatch in early May, reach a size of about 5 mm by late May. The first die-off of the older femalesin 1983 occurred in June, while in 1984it occurred in July. Females:
In April 1983 only about 5% of the adult males were lessthan 6 mm in length, while in March 1984, none were less than 6mm long. The modal size-class during February-April was 7-8 mm. In May the population showed a great reduction in the numbers of adult males of the old generation. This decreasewas especially in the sizeclass7-8 mm. Adult malesof the new generation become dominant. The newly released juveniles grew rapidly to a size not lessthan 5.5 mm at the end of May. The malesof the new generation reached by June a size of 8.0 mm. The first die-off of larger males(9 mm or more) occurred in July of both years. In November 1983 a second die-off occurred. The maximum size of malesrecorded throughout the sampling period was 10.5 mm. Mules:
The newly hatched amphipods were 1.25-l ‘50 mm long. Individuals lessthan this size were found inside the brood pouch of brooding females. Observations on the growth of juveniles of Purhyale busrensis revealed that the secondary sexual characters appeared at a size of 3.5 mm, with evidence that the growth in maleswas more rapid than in females. The new generation appeared in May of both years. The releaseof juveniles remained steady in June of both years, but there was a rapid increase in numbers of the newly hatched amphipod in July of the two years, and a slightly lesspronounced peak in September 1983. Therefore, three peaksof releaseoccurred in the population throughout the breeding season.The first peak of May was the result of the breeding activity of the old generation. The other two peaksof July and September were produced by females of the new generation. No sign of releaseof juveniles was observed in the period between
Juvendes:
Reproductive biology
-3
L7
ri““,“,G RIn13
11
Allr
-2 4
1lRB
6-
8- 1012 .-.-
20 AUP.
1
345
of Parhyale basrensis
2
4
6 8 10 12
2
6 8
4
10
12
a Jun.
In
8
Ian. 1984
120
-
100
@ L
80 60 i’
16 Jul. 8
n
.I...“. 100 @ in 25 Sep.
80
I.,
_.
2
4
.
--
6 8 1012
1
63
I
2 4 6 8 1012 2 4 6 8 1012 Tote1 length mm
2 4 6 8 IO
Figure 3. Size frequency distribution of I’. basrensis in the Shatt al-Arab River. Juveniles (dotted, upper); males (unshaded, upper); non ovigerous females (unshaded, lower); ovigerous females (black, lower). Numbers inside circles represent number of specimens collected. January-April. However in February and the following two months the number of ovigerous females gradually increased (Figures 3 and 4). Therefore the breeding season was found to extend from late February to late November or early December. Egg size and incubation period The mean diameter of ova (68 ova) of P. basrensis was estimated to be 0.387 mm f 0.061. Amphipod broods were counted and classified into five arbitrary developmental stages
346
M.
H. Ali
& S. D. Salman
80
70 60 50 L 0 0 f Z
LO
30 20 IO
Figure 4. Mean numbers the period of sampling. 3. Means over a year
TABLE
Female size (mm) Mean number of eggs with S.E.
4.0 4.9 kO.3
of ovigerous
and standard
4.5 5.9 kO.26
error
5.0 7.4 kO.35
females of P. basrensis in every
for egg counts of Parhyde
5.5 9.2 kO.46
6.0 12.8 kO.75
6.5 18.3 f3.2
sample throughout
basrensis females
7.0 17.0 k1.79
7.5 23.5 k2.77
averaged
8.0 31.0 k5.1
(Table 1). The mean numbers of each brood developmental stage in each monthly sample for the period between April 1983September 1984 were calculated. These data suggest that the incubation time was very short and to determine the incubation period 8 pairs in precopula were maintained in the laboratory during October 1984 (temperature 2529°C). After about two days the males and females separated, the females moulted and eggs appeared in the brood pouch. Ovigerous females were then put in glass dishes. Water was changed every day and food (water plants) was supplied. The release of juveniles began on the 8th day and by the 10th day all females were found to have empty brood pouches. Fecundity Table 3 shows the mean and standard error of the number of eggs produced by each size-class of females. It is evident that the number of eggs was a linear function of the size of the female. The relationship can be expressed by the following linear regression equation: Number
of eggs = (total
length
r = 0.866;
in mm)
5.499
- 19.324;
df 237
The number of eggs/female in the samples ranged from 4 eggs carried by a female of 4 mm total length to 37 eggs carried by a female 8.0 mm long. Females with 4 eggs comprised about 10% of the total gravid females. It seems likely that females with fewer than 4 eggs in their brood chambers, had lost eggs during the process of sampling and preservation. Sex ratio Analysis of sex ratio for the size class 3-4 mm, i.e. the size at which sexual dimorphism is possible, shows no significant difference at the 5 y0 level between the two sexes for most of
Reproductive
biology
of
Parhyale basrensis
347
TABLE 4. Numbers of males and females P. barrensis for every generation sample with the X2 values (significant values indicated by a star)
Date 11 Apr 1983 11 May 1983
16 Jun 1983
24 July 1983 20 Aug 1983 24 Sep 1983 25 Ckt 1983 26 29 23 28 31 15
Nov 1983 Dee 1983 Jan 1984 Feb 1984 Mar 1984 May 1984
8 Jun 1984
10 Jul 1984 25 Aug 1984 25 Sep 1984
Generation A A B C A B c B C B C B C B C C c C C C C D E C D E D E D E D E
No. of males
No. of females
Total no.
53 11 46 0 3 70 0 95 103 67 79 51 69 63 148 154 97 36 64 34 12 50 9 16 123 6 111 78 41 38 33 33
36 2 43 0 1 33 0 56 84 39 78 23 57 20 114 170 108 21 38 24 11 42 10 8 103 8 82 49 31 35 16 37
89 13 89 0 4 103 0 151 187 106 157 74 126 83 262 324 205 57 102 58 23 92 19 24 226 14 193 127 72 73 49 70
at each
monthly
X2 3.25 6.30* 0.111 1.24 13.29* 10,08* 1.92 7.39* 0.01 10.60* 1.15 22.28* 4,40* 0.78 0.58 3.96* 6,34* 1.73 0.08 0.70 0.10 2.70 1.76 0.35 4.36* 6.62* 1.40 0.12 5.91* 0.23
the samples, except in October and December 1983 when females outnumbered males 1.7: 1 (X2 = 4.10, P> 0.05) and 4.8: 1 (X2 = 7.21, P> 0.05), respectively. However, the sample of December was very small (n = 14), so these differences in the sex ratio may be entirely due to difficulties in identification of juvenile males. Moreover, the cumulative sex ratio of this size-class for the whole period of sampling was not significant (X’ = 3.6, PC: 0.05). An attempt was then made to calculate the sex ratio for each year-class to follow the changes in proportions of each sex in different generations. The data are presented in Table 4. It is evident that different generations have different sex ratios. The males of the short-lived generation B were significantly more than females of the same generation, but not significantly so in May 1983. In generation C, which have a life span of 11 months, the females only exceeded the males in November and December 1983, but the difference was not significant. The males significantly outnumbered the females only in October 1983, January and February 1984. The D-generation of May 1984, which corresponds to B-generation of May 1983, shows a predominance of males over the females, but significantly so in July and September 1984. In the E-generation, which corresponds to C-generation of 1983, a significant difference was only obtained in July 1984. In
348
M. H. Ali & S. D. Salmarr
September 1984, the numbers of females rose slightly, but the difference was not significant. The sex ratio for each sample, irrespective of generations, showsthat there is an overall preponderance of males over the females, except possibly in November and December 1983, when females slightly but not significantly, outnumbered the males. Moreover, significant differences of the ratio of males to the females were obtained in most of the samples,particularly in the year 1983. However, the cumulative sex ratio of malesto the females for the whole period of sampling was estimated to be 1.31 which is statistically significant (X2 = 54.027, P> 0.005) from the hypothetical ratio 1:1. Discussion It is evident from the present observation&rat the breeding seasonof Purhyale basrensis in the Shatt al-Arab region extends from late February to late November or early December. Although, no gravid femaleswere encountered in December, yet individuals in precopula were observed to occur in late December 1984 in an area further to the north of the sampling site. The incubation time of this speciesmay exhibit seasonalvariations depending largely on temperature. In a laboratory experiment during October 1984, the incubation period was found to be 8-10 days. However, at the beginning of the breeding seasonthe incubation period may be much longer than that at any other time of the season,and this probably accounted for the low water temperature (Table 1). A similar result was obtained by Nilsson (1977) who found that the incubation time for Gammaruspulex was60 days at 5°C and 100 days at 0°C. Moreover, Hiwatari & Kajihara (1984) found that the duration of egg development of Hyale barbicornis varies from about 26 days at 12°C to about 7 days at 28°C.
The mean eggsize of P. basrensis is 0.387 mm. This is quite similar to that of Parhyalella Schellenberg from Madagascar, which is 0.392 mm (Steele, 1973). These egg sizes are small when compared with data from Wildish (1979) on the eggs of some talitrid species vis’ Orchestia cavimana, 0.69 mm; 0. remyi roffensis, 0.62 mm; 0. mediterranea mediterranea, 0.72 mm; 0. mediterranea aestuarensis, 0.72 mm. The potential advantages of having small eggswere discussedby Van Dolah and Bird (1980). As a result of possessingsmall eggsthe incubation time is shortened, ultimately the time of attainment of sexual maturity might be short (Van Dolah & Bird, 1980). The time lapse from hatching to sexual maturity for female P. basrensis is about 3-4 weeks which is the time between the first peak of releaseof juveniles and the rise in numbers of sexually matured femalesof the new generation in May (Figure 4). The generation time therefore, is 5-6 weeks. This seemsto agree very much with reports on someother talitrid amphipods from tropical and subtropical regions such asParhyalella pietschmanni Schellenberg from Madagascar in which the generation time is 5-6 weeks (Steele, 1973). Moreover, Talorchestia margaritae, from Venezuela, reached aminimum reproductive size 2-3 weeks after hatching (Venables, 1981) and Hyale barbicornis, from Japan, attained sexual maturity in about 29 days (Hiwatari & Kajihara, 1984). However, the generation time in polar and temperate amphipods (seeTable V in Bregazzi, 1972) is usually more than those of tropical and subtropical speciesin general, and of P. basrensis in particular. As a result of relatively short incubation time (l-2 weeks), female P. basrensis may produce more than one brood in the breeding season.Moreover it was found that the female of this speciesbecome sexually mature at a size of 4 mm. Therefore, those females
pietschmanni
Temperate Ampelisca macrocephala Lilljeborg Gammarus p&x L. Gammarus duebeni Lilljeborg Gammarus pulex pulex (L.) Gammarus lacustris Sars Gammarus fasciatus Say Gammarus pseudolimnaeus Bousfield Corophium volutator (Pallas) Subtropical Hyale barbicotnis Hiwatari & Kajihara Austrochitonia australis (Sayce) Parhyale basrensis Salman Australia Iraq
Japan
Denmark Denmark U.K. U.K. U.K. U.K. Canada Sweden
Antarctic Antarctic
(Pfeffer) (Miers)
Polar Cheirimedonfemoratus Tryphosella kergueleni
of some amphipods
Locality
strategy
Species
TABLE 5. Reproductive
from
different
2-9 months 2 9 months 6-14 months
15-2 years 1-2 years 15-18months 13-14 months 15-16 months 13-15 months 15 months 5-7 months
3 years 4 years
Life history
latitudes
Semiannual Semiannual Semiannual
Annual Annual Annual Semiannual Annual Semiannual Annual Semiannual
Biannual Biannual
Type of life history
(1972) (1972)
(1955)
Hynes
Hiwatari Smith
& Kajihara (1984) & Williams (1983) Present study
Hynes & Harper (1972) Mliller 81 Rosenberg (1982)
(1954)
Hynes
Kanneworff (1965) Iversen & Jessen (1977)
Bregazzi Bregazzi
Reference
350
M.
H. Ali
& S. D. Salman
released early in the season, in May, may be able to produce at least 4 broods before they die in August (Figure 4). In addition, those females released early in November 1983, overwintered and reached maturity in February or March 1984. They may produce 4 broods before they die in July 1984. Other species, for instance, Gammarus duebeni in Southern England, may produce 4-7 broods (Sheader, 1983). The sex ratio may be affected by three mechanisms: the migration of one sex out of the habitat, the balance between the sex ratio of the recruitment, the differential mortality. There is no evidence of migration of one of the two sexesout of the adult habitat in P. basrensis, nor is there any dramatic change of body form seenin someother amphipods as Ampelisca macrocephala Lilljeborg (Kanneworff, 1965). Furthermore, there is always balanced production of the two sexesat recruitment. It is likely, therefore, that the differential mortality is the mechanism which regulates sex ratio in this species. The sizefrequency distribution indicates that mortality amongst females produced in 1983 is higher than that of femalesof 1984. The present account might suggestthat the life cycle of P. basrensis, in the Shatt al-Arab region, extended from May of one year to June of the next year, giving a life span of 13-14 months. However, since there were three peaks of brood release,in May, July and September 1983, it is more likely that the oldest individuals present in June 1984 were the remnants of the last peak of release(September 1983). The disappearancein July of the old generation of the bimodal population of June of both years may support this assumption. Therefore, the overall life span is more likely to have been 9-10 months. Furthermore, evidence from probability analysis indicated that mortality in November, probably, represents the die-off of the first peak of releasein May. Hence the life span of this brood may be only 6-7 months. This difference in the life span of successivebroods of the same specieshas also been noticed in Gammarus pseudolimnaeus Bousfield (Miller, 1982) and in Corophium volutator (Pallas) (Moller & Rosenberg, 1982) and in Hyale barbicornis Hiwatari and Kajihara (Hiwatari & Kajihara, 1984). It can be concluded therefore, that P. basrensis, has a semiannual life history, whereby young produced early in the growing seasonmature during the sameseasonand yield a second or more generations during that season (Wildish, 1982). This reproductive strategy is well known in temperate and, particularly, tropical species (Table 5). An adaptation of this kind probably corresponds to the long period of food availability and suitable temperature which give the animals more chance to produce successive generations in a short period, in contrast to high latitude localities where temperatures are lower and there are shorter periods of food availability. Acknowledgements We are grateful to the skipper and crew of R. V. ‘Jamiat Al-Basrah’ for assistancein sampling and Miss V. K. Al-Bazzi and Mrs. Nidhall Jabbar for help in the laboratory. Thanks are due to Dr Y. T. Daoud of the department of Biology for reading the manuscript. References Bregazzi,P.
K. 1972 Life cycles and seasonal movements of Cheirimedon femorarus kergueleni (Miers) (Crustacea: Amphipoda). British Antarctic Survey Bulletin Cassie, R. M. 1954 Some uses of probability paper in the analysis of size frequency Journal of Marine and Freshwater Research $513-522.
(Pfeffer) and Tryphosellu 30, l-34. distributions. Australian
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