Reproductive patterns in three isopod species from the Negev Desert

]oUT7UJI ofArid Environments (1992) 22: 73-85

Reproductive patterns in three isopod species from the Negev Desert M. R. Warburg Department of Biology, Technion, Haifa 32000, Israel (Received 19 October 1990, accepted 29 October 1990) In the presentstudy, the reproductive patternsof three isopod species inhabiting the Negev Desert are described. These are: Porcellio olivieri, Hemilepistus reaumuri (Porcellionidae), and Armadillo albomatginatus (Armadillidae). The species differ in their breeding season: H. reaumuri breeds in spring, A. albomarginatus in the fall, and P. olivieri was bred in the laboratory almost continuously. They also differ in their oogenetic pattern, number of oocytes, marsupial eggs and mancas, and in their reproductive strategies. BothP. olivieri and A. albomarginatus are iteroparous whereas H. reaumuri is semelparous. Introduction Several isopod species inhabit the Negev Desert. (The zoogeographic distribution ofthese desert isopods in the Negev is currently under investigation.) Foremost among them is Hemilepistus reaumuri inhabiting the loessian plains. This large, diurnal isopod is active during early morning and in the afternoon even in mid-summer (Warburg, 1968). It inhabits burrows where it lives in families (Linsenmair, 1984). Some information about the water balance of both H. reaumuri and Armadillo albomarginatus is available (Warburg, 1987a; Hadley & Warburg, 1986). The small pillbug, Armadillo albomarginatus, is abundant under stones in the hilly regions, especially during winter and spring (Fig. 1). In addition there are a few more species which, being largely fossorial, are rarely found on the surface of the ground except during winter. These include Porcellio olivieri, Porcellio barringtoni and Agabiformius sp. * Only one of these, P. olivieri, will be discussed here. The community structure and distribution patterns of a few desert isopods, among them H. reaumuri and P. olivieri, have been described by Kheirallah (1980). Soil moisture seems to playa major role in the distribution of these isopods. Available information on reproduction and life history patterns in isopods is based largely on species inhabiting temperature regions (see reviews in Warburg et al., 1984; Warburg, 1987b). In recent years we have studied reproductive patterns and strategies in a few isopod species inhabiting the Mediterranean region (Armadillo officinalis, Schizidium tiberianum and others; Cohen, 1988; Warburg, 1990a). From these studies, it appeared that different isopod species inhabiting the same habitat differed in their life history patterns. Schizidium tiberianum is short-lived, breeds in spring, and is semelparous, whereas A. officinalis can survive 9 years (probably more), breeds in the fall, and is iteroparous. Furthermore, the species differed in their oogenetic pattern as well as in both numbers of marsupial eggs and mancas. It was therefore decided to study the isopod • The exact identity of this species is currently under investigation.

014(}-19631921010073 + 13$03'00/0

© 1992 Academic Press Limited

74

M. R. WAR BURG

species inhabiting this arid region in order to see whether such extreme conditions would affect their reproductive patterns and strategies in a similar way. Materials and methods

Isopods were collected in the Negev Desert during winter and spring when they were more abundant on the surface (Fig. 1). When necessary, one species (H. reaumuri), was dug out

---- ......

~~'

_--_.....

..

.........

'

,...~

Figure 1. Habitat in the hilly region of the Negev Desert (A). Armadillo albomatginatus is abundant there (B). (C) Porcellio olivieri is entering its burrow.

REPRODUCTIVE PATTERNS

75

of its burrows during summer. Armadillo albomarginatus is found typically in the mountainous parts of the Negev, whereas both H. reaumuri and P. olivieri are characteristic of the loessian plains (Fig. I). Porcellio olivieri can be found in the Negev only during a restricted period of the winter, due to its fossorial habits. All three species remain under the surface of the ground for most of their life. Animals were brought into the laboratory where their sex was determined, their weight recorded (using a Metler H -311 balance with ± 0.1 mg accuracy), and some of the females were dissected. Their ovaries were examined, and the dimensions of both the ovaries and oocytes were determined microscopically. The larger oocytes were counted. Some of the females were kept individually with or without males for future observations in order to note the dates when marsupial eggs were found and the dates of juvenile release. In that way the number of marsupial eggs or mancas could be determined accurately. As fresh isopods (of the two abundant species) were brought continuously from the desert, the information about breeding season, number of eggs and mancas, and the period of their release, was as close as possible to the natural conditions. However, our information about P. olivieri is based largely on laboratory-bred isopods.

Results

Breeding patterns Two main reproductive seasons were apparent: spring and fall. Armadillo albomarginatus was found to breed in September-october (Tables 1,2), whereasH. reaumuri bred during 5 weeks in spring (Table 3). Most reproductively mature females of A. albomarginatus weighed between 50 and 100 mg (Fig. 2). From our observations on juveniles grown in the laboratory, they breed for the first time during their 2nd or 3rd year. The high survival rate of A. albomarginatus during its first 18 months of life may be an indication of its longevity (Fig. 3), whereas H. reaumuri is known to survive 18 months at the most. Porcellio olivieri bred in the laboratory almost continuously (Table 4). It is possible that their main breeding season in nature is spring, as observed on the original specimens captured in the field. Since males were found in natural populations as well as in batches born in the laboratory, it is unlikely that this species is parthenogenetic. Furthermore, the male: female ratio of the juveniles is about 1: 1.

Table 1. Reproductioe period of Armadillo albomarginatus and the number of reproducing females Month

September

Week 1

Total

2

2

37

4 1

7 15

3

October

Number reproducing females

2 3 4

5 2 2

1

71

0'0608 ± 0·0058 (5) 0'0904 ± 0·0090 (5) 0·0584 ± 0·0066 (4) 0·0716 ± 0·0108 (13) 0'0734 ± 0·0112 (25)

July

Average weight (g)

0·2494 ± 0'0040 (22) 0·3124 ± 0·0769 (8) 0'3097 ± 0.0733 (9) 0·2685 ± 0·0333 (13) O·2980 ± 0·0338 (17)

Month

February

-

-

9·92

-

± 2'94

Marsupial egg N

9·15 ± 1-48 (67)

MancasN

-

-

-

-

-

-

-

-

164'3 ± 25·2 (20) 147·0 ± 48·5 (35) 115'6 ± 38'6 (35)

0·20 ± 0·01 (20) 0·31 ± 0·03 (8) 0'53 ± 0'09 (9)

0·6 ± 0'1 (22) 0·8 ± 0·2 (16) 1'2 ± 0'2 (17)

9·0 ± 0·5 (22) 9·7±1·7 (8) 11'9 ± 1'6 (17)

OocyteN

Oocyte 0

Ovary Wi

Ovary L

-

100·8 ± 25'6 (13)

Marsupial egg N

66'4 ± 25·8 (17)

MancaN

mm); Wi, average width (in mm); D, average diameter (in rom); N, average number of oocytes, eggs or mancas; (n), number of specimens.

L, average length (in

May

May

April

March

± 0·05

(4)

-

± 6·8 (5) 11·25 ± 1-48 (4) 18'4

± 8·6

(5)

± 0'08

(5)

(5)

26'2

OocyteN

± 0'06

0

diameter (in mm); N, average number of oocytes, eggs or mancas;

0·45

0·49

0'47

Oocyte

Table 3. Ovary and oocytedimensions and numbers, and both marsupial eggs and manca numbers ofHemilepisms reaumuri

D, average

-

-

-

-

0·51 ± 0'08 (5) 0·57 ± 0'05 (5) 0·46 ± 0·04 (4)

Ovary Wi

3·45 ± 0·13 (5) 4·56 ± 0·06 (5) 3·22 ± 0'02 (4)

Ovary L

mm); Wi, average width (in mm); (n), number of specimens.

L, average length (in

September/October

August/September

September

August

Average weight (g)

Month

Table 2. Ovary and oocyte dimensions and numbers, and bothmarsupial eggs and manca numbers of Armadillo albomarginatus

~

~

?'

~

..... 0\

REPRODUCTIVE PATTERNS

77

10

z

so

------'--:-::-::-'------'-------- --100

WeiQhl (mQ)

Figure 2. Numbers of breeding A. albomarginatus females and their weight.

Oogenesis In both H. reaumuri and A. albomarginatus the ovarian and oocyte dimensions, as well as the oocyte number, change during oogenesis (Tables 2,3). There appears to be a loss in oocytes as fewer marsupial eggs were found in both species (Figs 4, 5). A similar loss in marsupial eggs was noticeable in H. reaumuri when compared with the number of mancas released (Fig. 5). No similar loss was observed in A. albomarginatus (Fig. 4). There was a great difference in the structure of the ovaries of these three species (Figs 6, 7, 8). The ovary of H. reaumuri consists of two rows of homogeneously sized oocytes (Fig. 6). The ovaries of P. olivieri and A. albomarginatus contain both large and small oocytes (Figs 7, 8). The latter will mature in future years. They stand out when the ovary empties after the larger oocytes have matured and moved into the marsupial sac. There is a positive relationship between the number of eggs or mancas, and the female's weight (Figs 9, 10, 11). This was noticeable in P. olivieri (Fig. 9). In H. reaumuri and A. albomarginatus this relationship was less apparent (Figs 10, 11). There seems to be some relationship between the number of mancas and weight loss in female H. reaumuri (Fig. 12).

I

100

~> ~

,e

•

I I

~L_

I

v.

I

1

IV.

VICIrI

Figure 3. Survival of juvenile A. albomarginatus during their first 18 months.

2

78

M. R. WARBURG

Table 4. Reproductive period of Porcellio olivieri and thenumber of reproducing females Month

Week

January

1 2 3 4 1 2 3 4 1 2 3 4 I 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4

February

March

April

May

June

July

Total

Number of reproducing females

2 3 6 2 4

3 2 3 2

2

33

Reproductive strategy Of the isopod species studied here one, H. reaumuri, was semelparous, whereas the other, A. albomarginatus, was iteroparous. Hemilepistus reaumuri breeds during its 2nd year, and

survives for only a few months afterwards. During that period, it provides food and guards the juveniles inside their burrow. Armadillo albomarginatus breeds during its 2nd or 3rd year. Growth of the juveniles of this species in the laboratory indicates that only after 2 years does the female reach the minimal weight for breeding (Fig. 13). It is capable of breeding at least once more (in the laboratory), probably more often judging from the growth curve (Fig. 13), and from the presence of small oocytes in the ovary (Fig. 8). As the rate of survival of juveniles is high (Fig. 3), this can also be taken as an indication that A. albomarginatus is capable of breeding several times. Porcelio olivieri is iteroparous based on our laboratory observations as well as on the ovary structure. As it starts breeding in its 2nd year while still growing, it presumably will continue breeding for several years before reaching maximal size. Our observations on this species are so far based largely on laboratory stock. It is possible that in nature growth is quicker, and thus they may attain maximal size sooner. Consequently they may not live so long.

REPRODUCTIVE PATTERNS

79

I 30

20 IZ

1 j

+

10

I

/:

1

~

Stoges

1 ! !

10

~

Figure 4. Oocyte (~), egg (D) and juvenile (~) numbers in A. albomarginatus.

Discussion The desert isopods studied here breed during two main seasons: spring and fall. This has also been seen in isopods from the Mediterranean region (Cohen, 1988; Warburg, 1990a). Unlike P. olivieri, which bred continuously (in the laboratory), the other two desert species bred once annually during a well defined period lasting only a few weeks. This difference could imply that the onset of breeding is triggered by different factors, or that different species respond in a different manner to the same stimuli. During spring, the rise in temperature, or the fact that the desert loess is still moist, could perhaps be the trigger for manca release in both H. reaumuri and P. olivieri. Ovigerous females of P. olivieri were found in May by Kheirallah & El-Sharkawy (1981). This would mean that oogenesis had already started during winter. On the other hand, oogenesis in A. albomarginatus starts in summer and the man cas are released in fall when it is still extremely dry. All this is based on observations on animals brought freshly from the field as well as on laboratory-bred isopods. Thus, dry soil and high temperatures seem to stimulate oogenesis in A. albomarginatus and manca release in both H. reaumuri and P. olivieri. On the other hand, increased soil moisture triggers the onset of oogenesis in both P. olivieri and H. reaumuri, and manca release in A. albomarginatus, IOO~------.

IZ

so

Stages

Figure 5. Number of oocytes (~), marsupial eggs (D) and maneas (~) in H. reaumuri.

80

M. R. WARBURG

Figure 6. Ovary of H. reaumuri (a) showing two rows of homogeneously sized oocytes (arrow indicatesoviduct, x9). (b) SEM view (x200).

The possibility that species belonging to the genus Armadillo are all autumn breeders can be excluded, since we have found one Armadillo sp. inhabiting a mesic habitat in the Mediterranean region, which breeds during mid-summer (Warburg, 1990b). In general, there is a positive relationship between the numbers of eggs or mancas and the female's weight (Kheirallah & EI-Sharkawy, 1981). However, there is a difference in the number of offspring produced. The semelparous H. reaumuri produces many more eggs and mancas than the other two iteroparous species. This phenomenon is known from other isopods found in the Mediterranean region (Cohen, 1988). Thus, the semelparous pillbug Schizidium tiberianum produces a large number of mancas before it dies. Finally, the reproductive strategies of the desert species indicate that both semelparity and iteroparity are successful strategies under extreme arid conditions. We have previously observed this also among isopods of the Mediterranean region (Cohen, 1988; Warburg, 1990a).

REPRODUCTIVE PATTERNS

81

Figure 7. Ovary of P. olivieri showing large and small oocytes (a, small arrow). Large arrow indicates oviduct (x2S). (b) Enlarged (xSO). (c) Shows empty ovary after the larger oocytes have moved into the marsupium (x40). Small arrow indicates small oocytes, medium arrow indicates empty sleeve of ovary.

Figure 8. Ovary of A. albomarginatus (c) showing large and small oocytes (small arrow, x40). Large arrow indicates oviduct. (a) and (b) show ovary after the large oocytes have moved into the marsupium. (a) SEM (x 75); (b) (x 18). Small arrow indicates small oocytes, medium arrow indicates empty ovarian sleeve.

CJ

;>::;

c::

ttl

>;>::;

:;:s

;>::;

;:::

00 N

REPRODUCTIVE PATTERNS

83

40

30

..c

~

> ~

Z

20

10

..

.\

o?05~0""'0---~---------------' 0·1000

0·2000

Figure 9. Relationship between the number of mancas and the weight of P. olivieri females. Only a few large females were available.

x x

100

x x

'0 d

x

x

x

x xx x

Z

1

1

300

3eO

400

Wei9ht of females (m9)

Figure 10. The relationship between the number of mancas and the weight of H. reaumuri females := 15).

(n

84

M. R. WARBURG 30

2'

I!lv ~

'0

~

•••

•

20

c

15

•

•

• ••

..

10

•

5

.....

0

0

aE

• • • •• • • • ••

~

s-

~

10

'0 0

Z

-

•

15

5

0

40

50

60

70

10

10

we'Qht ollemOln (m9)

Figure 11. The relationship between the numbers both of eggs/embryos and mancas, and the weight of A. albomarginatus females.

X

100 '-

X

..

X X

X

.

~

i:

.!

'0

~

!lOr-

X

x

x

X

x

x

x

I

I

~

~

0/0

I

w

WeillM loss ofter parluritlOn

Figure 12. The relationship between the number of juveniles and the weight lost by H. reaumuri females following parturition (n = 14).

REPRODUCTIVE PATTERNS

85

60

50

r:7'

E

40

20 -

10

"------:'::"-------::-::-----=---' 10

20

30

Aqe (months)

Figure 13. Growth rate of juvenile A. albomarginatus. Each point indicates average weight of 10 juveniles (± S.E.).

References Cohen, N. (1988). Soil invertebrate communities in the Segev-wood, population structure and reproductive strategies of two pillbugs: Armadillo officinalis and Schizidium tiberianum in the Segev-wood. Unpubl. M.Sc. Thesis, Technion, Haifa. Hadley, N. F. & Warburg, M. R. (1986). Water loss in three species of xeric-adapted isopods: correlation with cuticular lipids. Comparative Biochemistry and Physiology, 8SA: 669-672. Kheirallah, A. M. (1980). Aspects of the distribution and community structure of isopods in the Mediterranean coastal desert of Egypt. Journalof Arid Environments, 3: 69-74. Kheirallah, A. M. & EI-Sharkawy, E. (1981). Growth rate and natality of Porcellio olivieri (Crustacea: Isopoda) on different foods. Pedobiologia, 22: 262-267. Linsenmair, K. E. (1984). Comparative studies on the social behaviour of the desert isopod Hemilepistus reaumuri and a Porcellio species. Symposium of theZoological Society of London, 53: 423-453. Warburg, M. R. (1968). Behavioural adaptations in terrestrial isopods. American Zoologist, 8: 545559. Warburg, M. R. (1987a). Haemolymph osmolality, ion concentration and the distribution of water in body compartments of terrestrial isopods under different ambient conditions. Comparative Biochemistry andphysiology, 86A: 433-437. Warburg, M. R. (l987b). Isopods and their terrestrial environment. Advances in Ecological Research, 17: 187-242. Warburg, M. R. (1991). Reproductive patterns in oniscid isopods. In: Tuchauh, P. & Mocquard, J. P. (Eds), Biology of Terrestrial Isopods. pp, 131-137. Poitiers, France. Warburg, M. R. (1992). Life history patterns of terrestrial isopods from mesic habitats in the temperate region of northern Israel. Studies onNeotropical FaunaandEnvironment, 27 (in press). Warburg, M. R., Linsenmair, K. E. & Bercovitz, K. (1984). The effect of climate on the distribution and abundance of isopods. Symposium of theZoological Society of London, 53: 339367.