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Growth and reproduction in a rare desert isopod:Porcellio barroisi(Oniscidea; Porcellionidae) from the Central Negev Mountains
Journal of Arid Environments (1995) 31: 199–204
Growth and reproduction in a rare desert isopod: Porcellio barroisi (Oniscidea; Porcellionidae) from the Central Negev Mountains
M. R. Warburg Department of Biology, Technion, Haifa, 32,000, Israel (Received 9 February 1994, accepted 29 April 1994) The reproductive pattern of Porcellio barroisi, a slender, delicate and rare isopod, confined to the rocky habitats of the Central Negev Mountains, is described. This is an iteroparous, spring breeder which matures when 1-yearold, and can breed from two to three times during its life. ©1995 Academic Press Limited Keywords: Isopoda; Oniscidea; desert ecology; invertebrate reproduction; iteroparity
Introduction The isopod fauna of the Negev desert consists of seven species.* The first four are seasonally abundant and largely fossorial. Hemilepistus reaumuri (Aud. et Sav.) inhabits the loessian plains and is a semelparous, spring breeder. Armadillo albomarginatus Dollf. inhabits the Central Negev Mountains and is an iteroparous, autumn breeder. A detailed description of the reproductive patterns of these two species can be found in a previous paper (Warburg, 1992). Two additional desert isopod species, rarely found on the surface of the ground and then only in small numbers and during winter, are: Porcellio olivieri Aud. et Sav., which is large and found in sand-loess soil, and Agabiformius obtusus ssp. nov.,* a very small isopod found in the rocky region of the Central Negev. The reproductive patterns of these two species have already been described (Warburg, 1992, 1994). Finally, Porcellio barroisi Dollf. (Fig. 1) studied here, is a rather delicate, whitish, slender isopod, typical of the rocky habitats in the Central Negev Mountains, while a darker, more pigmented form occurs in Mediterranean fringe habitats bordering arid and semi-arid regions. P.barroisi inhabits shallow burrows under stones. In addition, two undescribed Porcellionides species* are currently under investigation. Available information on reproduction and life history patterns in isopods is based largely on isopod species inhabiting mesic habitats in temperate regions (Warburg, 1987, 1991, 1993, 1994; Warburg et al., 1984). Nothing is, so far, known on the life history of P.barroisi. These studies have shown that different isopod species differed in *The description and zoogeographic distribution of these desert isopods in the Negev is currently under study in collaboration with Dr H. Schmalfuss of the Stuttgart Natural History Museum. 0140–1963/95/020199 + 06 $12.00/0
© 1995 Academic Press Limited
200
M. R. WARBURG
Figure 1. Porcellio barroisi: left, enlarged; right, in burrow.
their life history patterns, in spite of the fact that they inhabited the same habitat. This was noticeable in isopod species from the arid region of the Negev (Warburg, 1992). It appeared that even such extreme, ambient conditions had no effect on reproductive patterns and strategies in oniscid isopods since both spring and autumn breeders as well as semelparous and iteroparous species were found side by side. Materials and methods P.barroisi (Fig. 1) was found solely under stones in the mountainous regions of the fringe area between the Mediterranean and the arid regions, and in the Central Negev desert, and then only during a restricted period in winter, due to its secretive and fossorial habits. It remains in the ground most of its life. Animals were brought into the laboratory, their sex was determined, and they were weighed (using a Mettler H-311 balance at ± 0·1 mg accuracy). The animals were weighed rather than having the head width measured in order to avoid excessive handling of these delicate animals which had to be kept alive for breeding experiments. They were kept at room temperature under natural light conditions for future observations. Most of the females were kept individually with or without males. In this way it was possible to find out whether they were parthenogenetic. It was possible to keep individuals for long periods as they thrived on potatoes. It was therefore possible to note the dates when marsupial eggs were found and when juveniles (mancas) were released. In this way the number of marsupial eggs or mancas could be determined accurately. Information about this species is based to a large extent on laboratory bred specimens. Results From the growth curves of several cohorts born and raised in the laboratory, it is clear that the animals reach maturity when 1-year-old (Figs. 2,3). Females weighing 20 mg were capable of breeding, but the majority of the breeding females weighed between
GROWTH AND REPRODUCTION IN A DESERT ISOPOD
201
30
(12) (21)
W (mg)
20
(11) (10)
(15)
(37)
10 (21)
(41) (39) 12
6 Age (months)
Figure 2. Growth curves of cohorts of Porcellio barroisi, raised in the laboratory (numbers in brackets indicate numbers of individuals in the cohort).
30–40 mg. Egg, embryo and manca numbers were positively related to their mother’s weight (Fig. 4). The mature oocytes moved into the marsupium in February, but the bulk of marsupial females were found in March and April. These observations are based on animals brought from the desert (Fig. 4). Mancas were released during March and April and sometimes in May (Fig. 4). However, most females released their young at the end of March and in April. Discussion All but two of the oniscids studied previously have shown a single, discrete, annual reproductive period during which a marsupium was formed and the mancas released
N
5
1 20
30
40
50
60
70
W (mg)
Figure 3. The proportion of Porcellio barroisi reproducing females among the various weight classes.
202
M. R. WARBURG
within a few weeks (Warburg, 1991, 1992, 1994). In iteroparous species, this pattern repeats itself during the same season year after year in stocks of animals born and raised in the laboratory for several generations. In the semelparous species raised and kept in the laboratory, breeding remained a single, although still a seasonal, event. Two desert isopod species H.reaumuri and A.albomarginatus breed seasonally, during spring or in autumn respectively. This is in spite of the fact that they have two different reproductive strategies: H. reaumuri is semelparous, whereas A. albomarginatus is iteroparous (Warburg, 1991, 1992). The latter species breeds in the laboratory during the fall every year. This was seen also in other iteroparous isopod species from the Mediterranean region (Warburg, 1991, 1992, 1994). Isopods from the arid or Mediterranean regions have maintained their particular discrete and seasonal reproductive pattern in the laboratory year after year. Recently, a continuous breeding pattern was described in the laboratory for two desert isopods: P.olivieri and Agabiformius sp. (Warburg, 1995). Thus, breeding in the laboratory of both species was not confined to certain periods, and they bred continuously
N
10
5
0
Feb
Mar
Apr
May
Months
Mancas
50
30
Eggs/Embryos
10
50
30
10 10
20
30
40
50
60
70
W (mg)
B
F
Figure 4. The number of P.barroisi marsupial eggs / embryos (bottom), mancas (middle), and juveniles ( ) (top), as a function of their mother’s weight ( ).
GROWTH AND REPRODUCTION IN A DESERT ISOPOD
203
irrespective of seasonal changes. A similar phenomenon has been described in the cosmopolitan species Porcellionides pruinosus in Botswana (Dangerfield & Telford, 1990). It is unlikely that such continuous reproduction can be maintained under the harsh xeric conditions prevailing in their natural desert habitat. It is more probably a response elicited by the artificial conditions of the laboratory. The fact that isopods breed during different seasons could imply either that the onset of oogenesis is triggered by more than a single factor, or that species responds in various ways to similar stimuli, or both. The rise in temperature, or the fact that the desert loess is still moist during spring, could perhaps be the trigger for manca release in both H.reaumuri, P.olivieri, and P.barroisi, during spring (Warburg, 1992). Ovigerous females of P.olivieri have been found in the desert during May (Kheirallah & El-Sharkawy, 1981), whereas P.barroisi females with a marsupium were found in February–March. This implies that oogenesis began during late autumn and winter. A similar oogenetic pattern has been described in another spring breeder, H. reaumuri (Warburg, 1992). On the other hand, oogenesis in A.albomarginatus began in summer and the mancas were released in autumn when the soil is still extremely dry. This is based both on observations on animals brought freshly from the field as well as on laboratory-bred isopods. Thus, both dry soil and high temperatures seem to stimulate oogenesis in A.albomarginatus, and manca release in H.reaumuri, P.olivieri, and P.barroisi. 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. There is usually a positive relationship between the numbers of eggs or mancas and the female’s weight (Kheirallah & El-Sharkawy, 1981). Moreover, there is a difference in the number of offspring produced. The semelparous H.reaumuri produces more eggs and mancas than the remaining iteroparous species which have been found to produce during a single brood. Likewise, the females of the semelparous pillbug Schizidium tiberianum, produced a large number of mancas before they died during parturition (Warburg, 1994). Finally, the reproductive strategies of the desert species indicate that both semelparity and iteroparity are successful strategies under extreme arid conditions (Warburg, 1992, 1995). So far, only one desert isopod (H. reaumuri), has been proved to be semelparous (Shachak, 1980); all other species are iteroparous. Similarly, in isopods from the Mediterranean region only a single, semelparous species (S. tiberianum) is known. The technical assistance of Mrs Yelena Tichomirova is gratefully acknowledged.
References Dangerfield, J. M. & Telford, S. R. (1990). Breeding phenology, variation in reproductive efforts and offspring size in a tropical population of the woodlouse Porcellionides pruinosus. Oecologia, 82: 251–258. Kheirallah, A. M. & El-Sharkawy, E. (1981). Growth rate and natality of Porcellio olivieri (Crustacea: Isopoda) on different foods. Pedobiologia, 22: 262–267. Shachak, M. (1980). Energy allocation and life history strategy of the desert isopod, Hemilepistus reaumuri. Oecologia, 45: 404–413. Warburg, M. R. (1987). Isopods and their terrestrial environment. Advances in Ecological Research, 17: 187–242. Warburg, M. R. (1991). Reproductive patterns in oniscid isopods. In: Juchault, P. & Mocquard, J. P. (Eds), Biology of Terrestrial Isopods, pp. 131–137. Poitiers: University of Poitiers Press. Warburg, M. R. (1992). Reproductive patterns of three isopod species from the Negev desert. Journal of Arid Environments, 22: 73–85. Warburg, M. R. (1993) Evolutionary Biology of Land Isopods. Berlin and Heidelberg: SpringerVerlag. 159 pp.
204
M. R. WARBURG
Warburg, M. R. (1994). Review of recent studies on reproduction in terrestrial isopods. Invertebrate Reproduction and Development (in press). Warburg, M. R. (1995). Continuous breeding in two rare, fossorial, oniscid isopod species from the central Negev desert. Journal of Arid Environments, 29: 383–393. Warburg, M. R., Linsenmair, K. E. & Bercovitz, K. (1984). The effect of climate on the distribution and abundance of isopods. Symposium of the Zoological Society of London, 53: 339–367.
Growth and reproduction in a rare desert isopod: Porcellio barroisi (Oniscidea; Porcellionidae) from the Central Negev Mountains
M. R. Warburg Department of Biology, Technion, Haifa, 32,000, Israel (Received 9 February 1994, accepted 29 April 1994) The reproductive pattern of Porcellio barroisi, a slender, delicate and rare isopod, confined to the rocky habitats of the Central Negev Mountains, is described. This is an iteroparous, spring breeder which matures when 1-yearold, and can breed from two to three times during its life. ©1995 Academic Press Limited Keywords: Isopoda; Oniscidea; desert ecology; invertebrate reproduction; iteroparity
Introduction The isopod fauna of the Negev desert consists of seven species.* The first four are seasonally abundant and largely fossorial. Hemilepistus reaumuri (Aud. et Sav.) inhabits the loessian plains and is a semelparous, spring breeder. Armadillo albomarginatus Dollf. inhabits the Central Negev Mountains and is an iteroparous, autumn breeder. A detailed description of the reproductive patterns of these two species can be found in a previous paper (Warburg, 1992). Two additional desert isopod species, rarely found on the surface of the ground and then only in small numbers and during winter, are: Porcellio olivieri Aud. et Sav., which is large and found in sand-loess soil, and Agabiformius obtusus ssp. nov.,* a very small isopod found in the rocky region of the Central Negev. The reproductive patterns of these two species have already been described (Warburg, 1992, 1994). Finally, Porcellio barroisi Dollf. (Fig. 1) studied here, is a rather delicate, whitish, slender isopod, typical of the rocky habitats in the Central Negev Mountains, while a darker, more pigmented form occurs in Mediterranean fringe habitats bordering arid and semi-arid regions. P.barroisi inhabits shallow burrows under stones. In addition, two undescribed Porcellionides species* are currently under investigation. Available information on reproduction and life history patterns in isopods is based largely on isopod species inhabiting mesic habitats in temperate regions (Warburg, 1987, 1991, 1993, 1994; Warburg et al., 1984). Nothing is, so far, known on the life history of P.barroisi. These studies have shown that different isopod species differed in *The description and zoogeographic distribution of these desert isopods in the Negev is currently under study in collaboration with Dr H. Schmalfuss of the Stuttgart Natural History Museum. 0140–1963/95/020199 + 06 $12.00/0
© 1995 Academic Press Limited
200
M. R. WARBURG
Figure 1. Porcellio barroisi: left, enlarged; right, in burrow.
their life history patterns, in spite of the fact that they inhabited the same habitat. This was noticeable in isopod species from the arid region of the Negev (Warburg, 1992). It appeared that even such extreme, ambient conditions had no effect on reproductive patterns and strategies in oniscid isopods since both spring and autumn breeders as well as semelparous and iteroparous species were found side by side. Materials and methods P.barroisi (Fig. 1) was found solely under stones in the mountainous regions of the fringe area between the Mediterranean and the arid regions, and in the Central Negev desert, and then only during a restricted period in winter, due to its secretive and fossorial habits. It remains in the ground most of its life. Animals were brought into the laboratory, their sex was determined, and they were weighed (using a Mettler H-311 balance at ± 0·1 mg accuracy). The animals were weighed rather than having the head width measured in order to avoid excessive handling of these delicate animals which had to be kept alive for breeding experiments. They were kept at room temperature under natural light conditions for future observations. Most of the females were kept individually with or without males. In this way it was possible to find out whether they were parthenogenetic. It was possible to keep individuals for long periods as they thrived on potatoes. It was therefore possible to note the dates when marsupial eggs were found and when juveniles (mancas) were released. In this way the number of marsupial eggs or mancas could be determined accurately. Information about this species is based to a large extent on laboratory bred specimens. Results From the growth curves of several cohorts born and raised in the laboratory, it is clear that the animals reach maturity when 1-year-old (Figs. 2,3). Females weighing 20 mg were capable of breeding, but the majority of the breeding females weighed between
GROWTH AND REPRODUCTION IN A DESERT ISOPOD
201
30
(12) (21)
W (mg)
20
(11) (10)
(15)
(37)
10 (21)
(41) (39) 12
6 Age (months)
Figure 2. Growth curves of cohorts of Porcellio barroisi, raised in the laboratory (numbers in brackets indicate numbers of individuals in the cohort).
30–40 mg. Egg, embryo and manca numbers were positively related to their mother’s weight (Fig. 4). The mature oocytes moved into the marsupium in February, but the bulk of marsupial females were found in March and April. These observations are based on animals brought from the desert (Fig. 4). Mancas were released during March and April and sometimes in May (Fig. 4). However, most females released their young at the end of March and in April. Discussion All but two of the oniscids studied previously have shown a single, discrete, annual reproductive period during which a marsupium was formed and the mancas released
N
5
1 20
30
40
50
60
70
W (mg)
Figure 3. The proportion of Porcellio barroisi reproducing females among the various weight classes.
202
M. R. WARBURG
within a few weeks (Warburg, 1991, 1992, 1994). In iteroparous species, this pattern repeats itself during the same season year after year in stocks of animals born and raised in the laboratory for several generations. In the semelparous species raised and kept in the laboratory, breeding remained a single, although still a seasonal, event. Two desert isopod species H.reaumuri and A.albomarginatus breed seasonally, during spring or in autumn respectively. This is in spite of the fact that they have two different reproductive strategies: H. reaumuri is semelparous, whereas A. albomarginatus is iteroparous (Warburg, 1991, 1992). The latter species breeds in the laboratory during the fall every year. This was seen also in other iteroparous isopod species from the Mediterranean region (Warburg, 1991, 1992, 1994). Isopods from the arid or Mediterranean regions have maintained their particular discrete and seasonal reproductive pattern in the laboratory year after year. Recently, a continuous breeding pattern was described in the laboratory for two desert isopods: P.olivieri and Agabiformius sp. (Warburg, 1995). Thus, breeding in the laboratory of both species was not confined to certain periods, and they bred continuously
N
10
5
0
Feb
Mar
Apr
May
Months
Mancas
50
30
Eggs/Embryos
10
50
30
10 10
20
30
40
50
60
70
W (mg)
B
F
Figure 4. The number of P.barroisi marsupial eggs / embryos (bottom), mancas (middle), and juveniles ( ) (top), as a function of their mother’s weight ( ).
GROWTH AND REPRODUCTION IN A DESERT ISOPOD
203
irrespective of seasonal changes. A similar phenomenon has been described in the cosmopolitan species Porcellionides pruinosus in Botswana (Dangerfield & Telford, 1990). It is unlikely that such continuous reproduction can be maintained under the harsh xeric conditions prevailing in their natural desert habitat. It is more probably a response elicited by the artificial conditions of the laboratory. The fact that isopods breed during different seasons could imply either that the onset of oogenesis is triggered by more than a single factor, or that species responds in various ways to similar stimuli, or both. The rise in temperature, or the fact that the desert loess is still moist during spring, could perhaps be the trigger for manca release in both H.reaumuri, P.olivieri, and P.barroisi, during spring (Warburg, 1992). Ovigerous females of P.olivieri have been found in the desert during May (Kheirallah & El-Sharkawy, 1981), whereas P.barroisi females with a marsupium were found in February–March. This implies that oogenesis began during late autumn and winter. A similar oogenetic pattern has been described in another spring breeder, H. reaumuri (Warburg, 1992). On the other hand, oogenesis in A.albomarginatus began in summer and the mancas were released in autumn when the soil is still extremely dry. This is based both on observations on animals brought freshly from the field as well as on laboratory-bred isopods. Thus, both dry soil and high temperatures seem to stimulate oogenesis in A.albomarginatus, and manca release in H.reaumuri, P.olivieri, and P.barroisi. 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. There is usually a positive relationship between the numbers of eggs or mancas and the female’s weight (Kheirallah & El-Sharkawy, 1981). Moreover, there is a difference in the number of offspring produced. The semelparous H.reaumuri produces more eggs and mancas than the remaining iteroparous species which have been found to produce during a single brood. Likewise, the females of the semelparous pillbug Schizidium tiberianum, produced a large number of mancas before they died during parturition (Warburg, 1994). Finally, the reproductive strategies of the desert species indicate that both semelparity and iteroparity are successful strategies under extreme arid conditions (Warburg, 1992, 1995). So far, only one desert isopod (H. reaumuri), has been proved to be semelparous (Shachak, 1980); all other species are iteroparous. Similarly, in isopods from the Mediterranean region only a single, semelparous species (S. tiberianum) is known. The technical assistance of Mrs Yelena Tichomirova is gratefully acknowledged.
References Dangerfield, J. M. & Telford, S. R. (1990). Breeding phenology, variation in reproductive efforts and offspring size in a tropical population of the woodlouse Porcellionides pruinosus. Oecologia, 82: 251–258. Kheirallah, A. M. & El-Sharkawy, E. (1981). Growth rate and natality of Porcellio olivieri (Crustacea: Isopoda) on different foods. Pedobiologia, 22: 262–267. Shachak, M. (1980). Energy allocation and life history strategy of the desert isopod, Hemilepistus reaumuri. Oecologia, 45: 404–413. Warburg, M. R. (1987). Isopods and their terrestrial environment. Advances in Ecological Research, 17: 187–242. Warburg, M. R. (1991). Reproductive patterns in oniscid isopods. In: Juchault, P. & Mocquard, J. P. (Eds), Biology of Terrestrial Isopods, pp. 131–137. Poitiers: University of Poitiers Press. Warburg, M. R. (1992). Reproductive patterns of three isopod species from the Negev desert. Journal of Arid Environments, 22: 73–85. Warburg, M. R. (1993) Evolutionary Biology of Land Isopods. Berlin and Heidelberg: SpringerVerlag. 159 pp.
204
M. R. WARBURG
Warburg, M. R. (1994). Review of recent studies on reproduction in terrestrial isopods. Invertebrate Reproduction and Development (in press). Warburg, M. R. (1995). Continuous breeding in two rare, fossorial, oniscid isopod species from the central Negev desert. Journal of Arid Environments, 29: 383–393. Warburg, M. R., Linsenmair, K. E. & Bercovitz, K. (1984). The effect of climate on the distribution and abundance of isopods. Symposium of the Zoological Society of London, 53: 339–367.