- Email: [email protected]
Bionomics of a desert cockroach, Heterogamisca chopardi Uvarov, 1936 after the spring rainfalls in Saudi Arabia (Insecta, Blattaria, Polyphaginae)
~oum~ofAridEnvironments
(1995)31:325-334
Bionomics of a desert cockroach, Heterogamisca chopardi Uvarov, 1936 after the spring rainfalls Saudi Arabia (Insecta, Blattaria, Polyphaginae)
Philippe
in
Grandcolas
VRA 373 CNRS, Laboratoire de Primatologk - Biologk 6volutive, Station Biologique de Paimpont, F-35380 Paimpont, France (Received 7 January
1994, accepted 29 April 1994)
The habitat choice and population structure of Heterogamisca chopardi were studied in a middle altitude desert of Saudi Arabia (30 km east of Taif) during June 1992. Two populations were compared, located, respectively, in a 3-year-old protected area and in a grazed area. Cockroaches live in the sand beneath shrubs. They preferred shrub species according to their cushion form, possibly depending on grazing pressure. Population densities ranged between 0.25 and 0.42 individuals per m2. Most individuals in June were middle-&tar nymphs, with few first-instar nymphs and old females. Oothecae were frequently parasitixed by flies (Bombyliidae). In comparison with the protected area, the grazed area showed higher density, the presence of younger middle-instar nymphs and of old females, higher fecundity, larger oothecae, a sex ratio less biased towards females, and probably lower nymphal survival. 01995
Academic
Keywords:
Press Limited
cockroach;
habitat;
population
structure;
parasitism
Introduction Sand cockroaches of the subfamily Polyphaginae have long been known to inhabit deserts (Chopard, 1929; Chopard, 1938; Grandcolas; 1994a,6). The ecology of two speciesbelonging to the genus Arenivugu has been studied in North America (Hawke & Farley, 1973; Edney et al., 1974; Cohen & Cohen, 1981) and that of Hemelytroblattcz &icana in Egypt (Ghabbour et al., 1977, 1978, 1980). These studies showed that these inconspicuous species had both important densities and ecological roles (Ghabbour et al., 1977) and striking adaptations to drought (Edney, 1966; O’Donnell, 1977; Vannier 81 Ghabbour, 1982). To provide comparative data, the bionomics of a third polyphagine cockroach, Hetzrogamisca chopardi, were studied in Saudi Arabia after the spring rainfalls. The genus Heterogumiscais distributed in the deserts of North Africa and the Middle East (Bey-Bienko, 1950; Princis, 1962). Three species have been found in Saudi Arabia, among which H. chopardi is limited to sandy areas of middle altitude (mostly higher than 1200 m) (Grandcolas, 19944. This specieswas never mentioned (Yaman, 1972; 0140-1963/95/030325
+ 10 $12.0010
0 1995 Academic Press Limited
326
P. GRANDCOLAS
Walker & Pittaway, 1987) after its description by Uvarov (1936), despite its abundance. Its choice of habitat, as well as its densities and population structures, in both reproduction parameters and parasitism levels, have been investigated protected and grazed areas. This study has given an opportunity to compare the life habits and ecological roles of sand cockroaches between three different regions, namely North America, North Africa and the Middle East. The results could be used later in a comparative framework on the subfamily Polyphaginae (Grandcolas & Deleporte, 1992; Grandcolas, 1994~).
Material
and methods
The study was carried out in Saudi Arabia at one site located at the border of the Asir mountains (1400 m) in the vicinity of Taif (30 km east of Taif, on the Al Suddayrah road, NWRC reserve: 21”14’46 N, 40”42’05 E). The sampling programme was designed as far as possible to provide instantaneous estimates of population parameters after the spring rainfalls (from 13 to 21 June 1992). Both the protected and grazed (mostly by goats) areas (Figs 1 and 2) were 100 m away from each side of the wire netting of the reserve of the National Wildlife Research Center (a 3-year-old enclosure). To assess whether H. chopa&’ inhabited fi-ee sand, sand under shrubs, sand under rocks, or rock shelters, the following different locations were sampled: 8 rock shelters and 26 rocks (ranging from 1000 cm3 to 32,000 cm3). Two quadrats, 400 m* (20 m X 20 m) were selected in each of the protected and grazed areas. In the protected area, 20 samples of free sand (20 cm X 20 cm X 20 cm) were examined. The sand lying under 3 1 plants of less than 10 cm in diameter was also examined. The sand under all shrubs with a diameter larger than 10 cm was then examined: the loose sand was removed and sieved, down to consolidated sand at 20-30 cm depth. All individuals, exuviae, corpses, old and incubating oothecae were collected. Oothecae were checked over several months for nymphs and the emergence of parasitoids. All those which were undamaged were also measured to estimate the oothecal size, as a component of the female reproductive effort; the size was estimated by: length without the flange X height from the base up to the keel. The number of eggs was estimated after the extema1 deformation of the oothecal wail and was then compared to that obtained from several hatchings. Several tens of nymphs were kept in a breeding box to sample their internal parasitoids and to record the duration of their remaining nymphal development. The age of the nymphs was estimated with the measure of pronotal width and their sex was unambiguously determined through the observation
Figures
l-2. The protected and grazed areas where the two quadrats were settled.
Figures
34.
A male and a female of Hecerogamisca
chopad;
the
scale bar represents
5 mm.
of the last abdominal segments with a binocular microscope. The sand and the shrubs were observed nightly for 10 h to look for the possible activity of the cockroaches.
Results
Very few rock shelters harboured H. chopardi: two out of eight showed only one nymph in their sandy ground. Only one nymph was found under 23 rocks. None of the freesand samples contained any cockroaches, likewise with the sand under the small shrubs. Conversely, the sand under larger shrubs, which were often cushion-like, harboured many cockroaches, corpses, exuviae, and oothecae at depths between 5 cm and 30 cm. They were all found surrounded by sand. When unearthed, cockroaches (Figs 3 and 4) either burrowed very rapidly or showed a freezing posture. Some were seen to protrude their hypopharynx from which a clear drop of fluid was produced. At depths below about 30 cm, the sand was compact and formed a dense layer without galleries harbouring cockroaches. Night observations did not reveal any activity at the surface level, even in the cushion shrubs. The different types of shrubs were compared with respect to the cockroach and ootheca frequencies under them (Fig. 5). In the protected area, Salsola sp. harboured cockroaches more often than did Zndigofera sp. or grass tufts. Other plants were either scarce (Cucumk sp., Acacia sp., Asteraceae) or not preferred (Lycium sp.). Comicula sp. was too scarce to assesswhether cockroaches really preferred it. In the grazed area, Salsolasp. and, to a lesser degree, Indigofera sp. were greatly damaged by goat grazing and so decreased in size and did not harbour cockroaches. Lycium sp., on the other hand, seemed resistant to grazing and acquired a cushion-like structure. It harboured many cockroaches and oothecae. The presence of cockroaches and oothecae was highly correlated with the sand under shrubs (see Fig. 5, Spearman non-parametric correlation coefficient, K = 0.992, p c 0.01). Only grass tufts (Poaceae) harboured relatively more nymphs than oothecae. In each area, either protected or grazed, the number of cockroaches and of oothecae was correlated with the shrub diameter (Fig. 6, Spear-man non-parametric correlation coefficient, for nymphs K = O-327 and K = 0.566, and for oothecae, K = 0.332 and K = 0.568, p < 0.01). Not all shrubs harboured both nymphs and oothecae; for example, of 28 shrubs with nymphs in the protected area, only 14 harboured oothecae. In the grazed area, of 21 shrubs harbouring nymphs, five lacked oothecae. In both areas, a few shrubs harboured oothecae but no nymphs (1 and 3 respectively). Respectively, 99 and 127 cockroaches were found in the protected and grazed quadrats which represented high densities (Table 1). Few adult females were present
P. GRANDCOLAS
328
in the grazed area only and adult males were not encountered (Table 1); these adult females were assumed to be old individuals, since their appendages were damaged and their hairs abraded. The total sex ratio was biased towards the females, especially in the protected area (Table 1). Exuviae and corpses seemed equally common in both areas. Oothecae were much more common in the grazed area (Table 2). The age structures of the populations are shown in the histograms of pronotal size in males and females (Fig. 7). Three cohorts were visible: first or second instar nymphs (less than 1.5 mm pronotal width), middle&star nymphs (around 5 mm) and adult females (more than 8 mm). The populations in the protected and grazed areas showed a clear difference: the lack of adults in the protected area. If one took into account only the middle cohort, significant differences also appeared: a lower mean age. This is significant in male nymphs (Wilcoxon two-sample test, W = 6005, p < 0.01) and not Protected area 0
50
100
0
I Zndigofem
(82)n
Salsola
(15)
m
Poaceae
(14)
B
Lycium
(8) -
Acacia
(2) -
Astemceae
(1) -
Cornulaca
(1)
Cucumis
(1) -
Grazed area I Zndigofem
(0) -
Salsola
(2) -
Poaceae
(0) -
Lycium Acacia
(36)
-
(3) Ku -
Cornulaca
(0) -
Cucumis
(0) -
5. Occupancy ratios (%) of sand under Merent species of shrubs in protected and grazed areas by cockroach individuals (W) and oothecae ( ; n-be= b brackets refer& to shrub numbers in the two quadrats.
Figure
BIONOMICS OF A DESERT COCKROACH
329
in female nymphs (IV = 6493, p > 0.10). The age of the middle female nymphs also showed a wider distribution in the grazed area but it was found not significant (twotailed test of Kolmogorov-Smimov, D = O-167, p > 0.10). Significant differences appeared in the numbers of oothecae in the two areas. Their total number was higher in the grazed area (cf: supra), but this was due only to a higher number of hatched oothecae; incubating oothecae were actually less numerous in the grazed area (Table 2). Oothecae were also larger in the grazed area (Wilcoxon twosample test, IV’ = 2040, p c O-05). However, the number of eggs seemed most often to be six in both the protected and grazed areas (Wilcoxon two-sample test, W = 328.5,
20
(a)
n
K= 0.32'7 p < 0.01
. . . .
.
i
.
n
n
mm
n
. .
n
n
n
n
n
I-
*
20
*
40
1
60
80
8
I
100
I
120
1
140
!20::, . . n
. n
.
. . n
t
m I
I
0
20
40
. n
.
.
1
60
I
1
80
100
t
I
I
120
140
Shrub diameter
Figure 6. Relationships (numbers
of individuals)
between the diameters of all shrubs (cm) and the cockroach abundance in the protected area (a) and the grazed area (b); K is the non-
parametric Spearman correlation coefficient.
P. GRANDCOLAS
330
Table 1. Populatbn parameters of H. chopardiin protected and grazed areas (2om
x 2om)
Grazed area
Protected area
Parameter Total number of cockroaches Cockroach density (per m2> Adult ratio Sex ratio Number of exuviae Number of corpses
99 O-25 0% O-24 19 1
127 0.32 9.4% o-41 18 2
p > 0. lo), following both the estimates from observations of oothecae (Table 2) and hatching counts (N = two hatchings). The number of eggs per ootheca ranged from four to eight in both areas. Twenty per cent of incubating oothecae (four of 20) releasedbombyliid flies (ExhyuZunthrux blunue) from two different shrubs of each area. An unidentified tachinid fly was also obtained from nymphs breeding. Laboratory breeding showed that nymphs could feed and develop on dead leaves. Old nymphs taken in the field became adult during summer 1992. Some sampled incubating oothecae hatched before summer 1992.
2or--10 I
”
2
3 4 Pronotal
5 6 width
7
8
,)--W-.-L 2
3
2
3
4
5
6
7
8
4
5
6
7
8
20
5 p: m 10 &
0
2
3
4
5
6
7
8
0
Males
7. Age structuresof populationsfor malesand femalesin protected and grazed areas, after the pronotal width (mm) (H = larvae; = adults). Figure
BIONOMICS
Table
OF A DESERT
COCKROACH
331
2. Oothecal characterkrics in protected and grazed areas (20~1 x 2074
Characteristic Total number of oothecae Ratio of incubating oothecae Ratio of hatched oothecae Size (L x H)
Number of eggs Ratio of parasited oothecae
Protected area
Grazed area
48 25% 75% 14.7 (N=43) 5.7 (iV=16) 25%
81 9.9% 90.1% 15.2 (N=72) 6 (iV=30) 12.5%
Discussion Habitat
use and activity
The sand cockroach H. chopardi appeared principally to inhabit the sand beneath cushion shrubs that were more than 10 cm wide. It appeared to discriminate between shrubs on the basis of their morphology and not on the basis of species. Depending on grazing pressure, some shrubs became cushion-like and other became very small or nearly disappeared, and cockroaches shifted toward those which had become cushion shrubs. This habitat is very similar to that described in the Egyptian coastal desert for Hemelytroblatta ajiicana by Ghabbour et al. (1977, 1978, 1980), except that it also inhabited the sand beneath other species of cushion shrubs that were locally more abundant than Salsola or Lycium spp. Arenivaga invemgata or A. sp. seemed to be somewhat less linked to the shrubs in the North American deserts (Hawke & Farley, 1973; Edney et al., 1974; Cohen & Cohen, 198 1). They were observed to burrow into the sand anywhere or, when they inhabited sand under shrubs, to move away from them at night, leaving visible trails on the sand surface. This behaviour and the resulting trails were never observed in June 1992 for H. chopardi, the individuals of which were always under shrubs and were not seen moving away from them either during the day or at night. Two other species of Heterogamisca were observed in Saudi Arabia and their life habits were not strictly similar to those of H. chopardi (Grandcolas, 19946). H. marmowta was never found in the sand beneath shrubs, but only in rock shelters located in rocky areas. H. dispersa was extremely scarce and always solitary at the bases of small Acacia trees in central tablelands at low altitude. The co-occurrence was very weak between these three species, even if one does not take into account their different habitats, since they preferred respectively sandy areas, rocky areas of middle and high altitude, and low altitude areas. The life-habits of H. chopardi. were also clearly different from those of other eremophilous polyphagine species.Polyphaga spp. in Old World deserts (Bey-Bienko, 1950; Grandcolas, 19946) or Arenivaga apacha in the American deserts (Cohen & Cohen, 198 1) inhabit either burrows or rock shelters, and are only occasionally to be seen dispersing in the sand. Several individuals of H. chopardi were usually found under each shrub. This is indicative of gregarious habits. In solitary species, early nymphal dispersal occurs and individuals are separate (Grandcolas, 1993). The clumped distribution of H. chopardi was not due to the patchy distribution of the shrubs because individuals of the related species H. dispersa are to be found alone at the bases of Acacia trees which are also patchily distributed. Individuals of H. chopardi spent most of their time burrowing in the sand: they grew up, moulted, and laid oothecae there. They even absorbed water vapour from the sand (Grandcolas, 1994~). Activity was not observed at the surface, but may perhaps have
332
P. GRANDCOLAS
occurred at another season. Males and females may meet in this way (Chopard, 1938). Adult males were captured nightly when flying toward light (S. Biquand, pers. comm.). Some nymphs also dispersed from one shrub to another: this dispersal behaviour was attested by the ratio of shrubs with nymphs and without oothecae. More observations are needed to answer the question of whether the nymphs dispersed beneath the sand surface. Even the bombyliid parasitoids may search for oothecae in the sand, since females were never to be seen on the sand surface and deposited their oothecae deeply (one female was found burrowing while carrying its ootheca). These parasitoids are not known as parasitizing cockroach oothecae (Roth & Willis, 1960), but attack the oothecae of Orthoptera, moth pupae, fly puparia, and Hymenoptera cocoons @u Merle, 1975; Greathead, per-s. comm.). They exerted a high pressure on Heterogumiscu populations that could be compared with that exerted by some evaniid wasps on several other cockroach species. The ratio of parasitism was higher than that in the oothecae of wood-inhabiting Purcobkzttu in North America (Edmunds, 1952) and was similar to that of the oothecae of synanthropic Periplunetu americana in caves (Deleporte, 1976). Predation by scorpions on Arenivugu investigutu was often observed in North America (Hawke & Farley, 1973). These predators are also present in Saudi Arabia, but no predation was observed (pens. obs.).
Population structures and reproduction parameters The populations studied showed three cohorts: very recently hatched nymphs, older nymphs and, in one case, old females. The two first cohorts could be tentatively put in relation with the oothecae found in the sand: very young nymphs might have hatched from oothecae deposited approximately at the same time as the unhatched oothecae, while older nymphs had probably hatched from the old oothecae. The populations sampled in the grazed VS. protected areas differed in their life history parameters. However, it seems at first sight difficult to assess specifically the relative importance of reproductive effort in each area. Female densities and numbers were not known over the whole year and this does not permit numbers of oothecae to be compared. Density and sex ratio were only available for nymphal cohorts. Using this later sex ratio, it is possible to infer that the reproductive effort is much greater in the grazed area. Oothecae were twice as numerous then, but the sex ratio was less unbalanced toward females and density not much higher. This greater reproductive effort in the grazed area may also be deduced from the larger size of the oothecae. Oothecae seemed to be less often parasitized in the grazed area, however, that may also have increased the efficiency of the reproductive effort. One must, however, note that it is difficult to equate reproductive effort with population densities when one compares the protected area with the grazed area. Oothecae were twice as numerous (and larger); but population densities were only 28% higher. The survival of nymphs must be inferred to be less important. The range of variation in oothecal size appears similar when it is compared with that observed in the laboratory for l7zereu petivetiunu (Ananthasubramanian & Ananthakrishnan, 1952; pers. obs.), and small when compared with that of Arenivugu investigutu (Appel et al., 1983) and Erguulu cupensis (per-s. obs.). The structure of the populations also differed slightly between the two areas. In the grazed area, individuals of each cohort were younger: middle-instar nymphs slightly younger, and older females still alive. The sex ratio was strikingly biased but differed between the two areas. Protandry may not explain this: the youngest population showed the most unbalanced sex ratio. Different mortality ratios as well as different inheritable sex ratios may provide an explanation. These differences between grazed and protected areas were unexpected. The grazed area was intuitively considered to be a damaged environment with less vegetation and
BIONOMICS
OF A DESERT
COCKROACH
333
a lower capacity to shelter populations of detritivorous cockroaches. Cockroaches were, however, actually more abundant in the grazed area. Several factors could be responsible for that situation. First, what were envisaged as negative physical constraints in the grazed area could be enhancing factors for cockroach populations. For example, less vegetation cover allowed the wind to cause the sand to drift and to provide more favourable burrowing places at the bases of shrubs. This could also lead to larger accumulations of organic matter at the bases of shrubs. Goats were responsible for grazing the vegetation but could also provide local enrichment of the ground litter with their faeces. Grazing pressure caused a shift toward another species of shrub: this species (Lycium sp.) may provide litter with higher nutritive value, or present roots with palatable mycorhizal fungi, as documented for Arenivugu investigatu (Schal et al., 1984). Higher fecundity in terms of oothecal number and/or size is generally related to a better diet (e.g. Roth & Willis, 1954). Conversely, the later state of the population in the grazed area could be due to the lesser capacity of the environment to hold moisture (lesser vegetation cover etc.). Though several Polyphaginae cockroaches are able to absorb the atmospheric water vapour (Edney, 1966; Vannier & Ghabbour, 1982; Grandcolas, 19944, their populations are strongly influenced by the ground moisture content (Ghabbour et al., 1977). H. chopardi appears to be an important element in the poorly known soil fauna of the Saudi deserts. Its densities are high, and it is present in both protected and grazed areas. It is similar to Hemelytroblatta africana in Egypt (Ghabbour et al., 1977), but has several unique features-its biased sex-ratio, and parasitism by bombyliid flies. Its detritivorous habit suggests that it may play an important role in the cycling of organic matter in the soil beneath shrubs. Acknowledgements I am grateful to Abdulrahman Khoja, Sylvain Biquand and George Schwede for their invitation to work as a guest researcher at the National Wildlife Research Center in Saudi Arabia. Plant species in the study areas were identified with the help of S. Biquand. I also wish to thank the staff of NWRC for their kind assistance, P. Deleporte, L. Desutter, N. Menard and an anonymous reviewer for reading my manuscript, D. Greathead, L. Matile and L. Tsacas for the identification of parasitoids, and J. Marshall for the loan of the holotype of H. chopardi deposited in the British Museum.
References Ananthasubramanian, K.S. & Ananthakrishnan, T.N. (1959). The structure of the ootheca and egg laying habits of Cotydiu petiveriuna L. (Blattidae). Indian Journal of Entomology, 21: 59-64. Appel, A.G., Van Dyke, A.M. & Rust, M.K. (1983). A technique for rearing and some notes on the biology of a desert sand cockroach, Arenivugu investtgutu (Dictyoptera: Polyphagidae). Ibceedings of the Enwmologicul Society of Wushington, 85: 598-600. Bey-Bienko, G.I. (1950). Fauna of the USSR. Insects. Bluttodeu. Moscow: Institute of Zoology, Academy of Sciences of the URSS. 342 pp. Chopard, L. (1929). Orthoptera palaearctica critica. VII. Les Polyphagiens de la faune palearctique. Eos, 5: 223-358. Chopard, L. (1938). La Biologie des Orthoptkes. XX. Encyclop.4die enwmolog@ue. Paris: Lechevalier. 541 pp. Cohen, A.C. & Cohen, J.L. (1981). Microclimate, temperature and water relations of two species of desert cockroaches. Comparative Biochemistry and Physiology, 69: 165-l 67. Deleporte, P. (1976) L’organisution Sociule Chez Perzplaneta Americana (LXcyopdres): aspects bcokthologiques, ontogenbe des relations interindividuelles. Universite Rennes: These Doctorat 3eme cycle. 60 pp.
334
P. GRANDCOLAS
Du Merle, P. (1975). Les h&es et les stades pr&imaginaux des Diptltres Bombylidae: revue bibliographique armotee. UIBS, Bulletin SROP I WRS Bulletin: l-289. Ednumds, L.R. (1952). Some notes on the habits and parasites of native wood-roaches in Ohio (Grthoptera: Blattidae) . Entomologuxzl News, 63: 14 l-l 45. Edney, E.B. (1966). Absorption of water vapour from unsaturated air by AYeniqV SP. (Polyphagidae: Dictyoptera). Comparative Biochemisny and Physiology, 91: 387-408. E&ey, E.B., Haynes, S. & Gibo, D. (1974). Distribution and activity of the desert cockroach Armivaga invescigata (Polyphagidae) in relation to microclimate. EcoZO~, 55: 420-427. Ghabb&r, S.I., M&hail, W.Z.A. & Rizk, M.A. (1977). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. I. Summer populations of soil mesofauna associated with major shrubs in the littoral sand dunes. Revue d’Ecologie et de Biologie du Sol, 14: 429459. Ghabbour, S.I. & M&hail, W.Z.A. (1978). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. II. Soil mesofauna associated with Thymelea hirsutu. Revue d’Ecologie et de Biologie du Sol, 15: 333-339. Ghabbour, S.I. & Shakir, S.H. (1980). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. III. Analysis of Thymelea mesofauna populations at the Mariut frontal plain. Revue d’Ecologie et de Biologie du Sol, 17: 327-352. Grandcolas, P. (1993). Habitats of solitary and gregarious species in the neotropical Zetoborinae (Insecta, Blattaria). Studies in Neotropical Fauna and Environment, 28: 179-190. Grandcolas, P. (19940). The appearance of xylophagy in cockroaches: two case studies with reference to phylogeny. youma of Onhoptera Research, 2: 000-000. Grandcolas, P. (1994b). Phylogenetic systematics of the subfamily Polyphag-inae, and assignment of Ctypwcercus Scudder, 1862 to this taxon (Blattaria, Blaberoidea, Polyphagidae). Systematic Entomology, 19: 145-158. Grandcolas, P. (1994~). Evidence for hypopharynx protrusion and presumptive water vapour absorption in Heterogamisca chopardi (Dictyoptera: Blattaria: Polyphaginae). Ann&s de la Societl Enwmologigue de France (NS.), 30: 361-362. Grandcolas, P. (19944. Blattaria (Insecta, Dictyoptera) of Saudi Arabia: a preliminary study. In: Biittiker & Krupp, (Ed.), Fauna of Saudi Arabia, pp. 40-58. NCWCD, Pro Entomologia, Riyadh, Basle. ’ Grandcolas, P. & Deleporte, P. (1992). La position systematique de Cmrocercus Scudder, 1862 au sein des Blattes et ses Implications evolutives. Comptes-Rendus de Z’Acadkmie &s Sciences de Paris, @rie III), 315: 317-322. Hawke, S.D. & Farley, R.D. (1973). Ecology and behaviour of the burrowing cockroach, Arenivaga sp. Oecologia, 11: 263-279. O’Donnell, M.J. (1977). Site of water vapor absorption in the desert cockroach, Arenivuga invesugara. Proceedings of the National Academy of Sciences of USA, 74: 1757-1760. Princis, K. (1962). Pars 3: Blattariae: Subordo Polyphagoidea: Fam. Polyphagidae. &&prerorum Cutalogus. ‘s-Gravenhage: Junk. 74 pp. Roth, L.M. & Willis, E.R. (1954). The reproduction of cockroaches. Smithsonian Miscellaneous col-lmions, 122: l-49. Roth, L.M. & Willis, E.R. (1960). The biotic associations of cockroaches. Smithsonian Miscelkzneous Collections, 141: l-470. Schal, C., Gautier, J.Y. & Bell, W.J. (1984). Behavioural ecology of cockroaches. Biological Review, 59: 209-254. Dvarov, B. (1936). I. Studies in the Arabian Orthoptera. I. Descriptions of new genera, species, and subspecies. Journal of the Linnean Society of Lordon, Zoology, 39: 531-549. Vannier, G. 8~ Ghabbour, S.I. (1982). Effect of rising ambient temperature on transpiration in the cockroach Heterogumiu syriuca Sauss. from the mediterranean coastal desert of Egypt. In: hbm, P., Andre, KM., Medts De, A., Gregoire-Wibo, C., Wauthy, G. (Ed), New Trends in Soil Biologv. Proceedings of the VIII International Colloquium of soil zoology. Louvain-la-Nmue (Belgium). August 3GSeptember 2, 1982, pp. 441-453. Ottignies, Louvain-la-Neuve: DieuBrichart. 709 pp. Walker, D.H. & Pittaway, A.R. (1987). Insects of Eastern Arabia. London: MacMillan. 177 PP. Yaman, 1.K.A. (1972). Orthoptera of the central province of Saudi Arabia. Z&,&rift fiir Angewandte Enwmologie, 70: 88-92.
(1995)31:325-334
Bionomics of a desert cockroach, Heterogamisca chopardi Uvarov, 1936 after the spring rainfalls Saudi Arabia (Insecta, Blattaria, Polyphaginae)
Philippe
in
Grandcolas
VRA 373 CNRS, Laboratoire de Primatologk - Biologk 6volutive, Station Biologique de Paimpont, F-35380 Paimpont, France (Received 7 January
1994, accepted 29 April 1994)
The habitat choice and population structure of Heterogamisca chopardi were studied in a middle altitude desert of Saudi Arabia (30 km east of Taif) during June 1992. Two populations were compared, located, respectively, in a 3-year-old protected area and in a grazed area. Cockroaches live in the sand beneath shrubs. They preferred shrub species according to their cushion form, possibly depending on grazing pressure. Population densities ranged between 0.25 and 0.42 individuals per m2. Most individuals in June were middle-&tar nymphs, with few first-instar nymphs and old females. Oothecae were frequently parasitixed by flies (Bombyliidae). In comparison with the protected area, the grazed area showed higher density, the presence of younger middle-instar nymphs and of old females, higher fecundity, larger oothecae, a sex ratio less biased towards females, and probably lower nymphal survival. 01995
Academic
Keywords:
Press Limited
cockroach;
habitat;
population
structure;
parasitism
Introduction Sand cockroaches of the subfamily Polyphaginae have long been known to inhabit deserts (Chopard, 1929; Chopard, 1938; Grandcolas; 1994a,6). The ecology of two speciesbelonging to the genus Arenivugu has been studied in North America (Hawke & Farley, 1973; Edney et al., 1974; Cohen & Cohen, 1981) and that of Hemelytroblattcz &icana in Egypt (Ghabbour et al., 1977, 1978, 1980). These studies showed that these inconspicuous species had both important densities and ecological roles (Ghabbour et al., 1977) and striking adaptations to drought (Edney, 1966; O’Donnell, 1977; Vannier 81 Ghabbour, 1982). To provide comparative data, the bionomics of a third polyphagine cockroach, Hetzrogamisca chopardi, were studied in Saudi Arabia after the spring rainfalls. The genus Heterogumiscais distributed in the deserts of North Africa and the Middle East (Bey-Bienko, 1950; Princis, 1962). Three species have been found in Saudi Arabia, among which H. chopardi is limited to sandy areas of middle altitude (mostly higher than 1200 m) (Grandcolas, 19944. This specieswas never mentioned (Yaman, 1972; 0140-1963/95/030325
+ 10 $12.0010
0 1995 Academic Press Limited
326
P. GRANDCOLAS
Walker & Pittaway, 1987) after its description by Uvarov (1936), despite its abundance. Its choice of habitat, as well as its densities and population structures, in both reproduction parameters and parasitism levels, have been investigated protected and grazed areas. This study has given an opportunity to compare the life habits and ecological roles of sand cockroaches between three different regions, namely North America, North Africa and the Middle East. The results could be used later in a comparative framework on the subfamily Polyphaginae (Grandcolas & Deleporte, 1992; Grandcolas, 1994~).
Material
and methods
The study was carried out in Saudi Arabia at one site located at the border of the Asir mountains (1400 m) in the vicinity of Taif (30 km east of Taif, on the Al Suddayrah road, NWRC reserve: 21”14’46 N, 40”42’05 E). The sampling programme was designed as far as possible to provide instantaneous estimates of population parameters after the spring rainfalls (from 13 to 21 June 1992). Both the protected and grazed (mostly by goats) areas (Figs 1 and 2) were 100 m away from each side of the wire netting of the reserve of the National Wildlife Research Center (a 3-year-old enclosure). To assess whether H. chopa&’ inhabited fi-ee sand, sand under shrubs, sand under rocks, or rock shelters, the following different locations were sampled: 8 rock shelters and 26 rocks (ranging from 1000 cm3 to 32,000 cm3). Two quadrats, 400 m* (20 m X 20 m) were selected in each of the protected and grazed areas. In the protected area, 20 samples of free sand (20 cm X 20 cm X 20 cm) were examined. The sand lying under 3 1 plants of less than 10 cm in diameter was also examined. The sand under all shrubs with a diameter larger than 10 cm was then examined: the loose sand was removed and sieved, down to consolidated sand at 20-30 cm depth. All individuals, exuviae, corpses, old and incubating oothecae were collected. Oothecae were checked over several months for nymphs and the emergence of parasitoids. All those which were undamaged were also measured to estimate the oothecal size, as a component of the female reproductive effort; the size was estimated by: length without the flange X height from the base up to the keel. The number of eggs was estimated after the extema1 deformation of the oothecal wail and was then compared to that obtained from several hatchings. Several tens of nymphs were kept in a breeding box to sample their internal parasitoids and to record the duration of their remaining nymphal development. The age of the nymphs was estimated with the measure of pronotal width and their sex was unambiguously determined through the observation
Figures
l-2. The protected and grazed areas where the two quadrats were settled.
Figures
34.
A male and a female of Hecerogamisca
chopad;
the
scale bar represents
5 mm.
of the last abdominal segments with a binocular microscope. The sand and the shrubs were observed nightly for 10 h to look for the possible activity of the cockroaches.
Results
Very few rock shelters harboured H. chopardi: two out of eight showed only one nymph in their sandy ground. Only one nymph was found under 23 rocks. None of the freesand samples contained any cockroaches, likewise with the sand under the small shrubs. Conversely, the sand under larger shrubs, which were often cushion-like, harboured many cockroaches, corpses, exuviae, and oothecae at depths between 5 cm and 30 cm. They were all found surrounded by sand. When unearthed, cockroaches (Figs 3 and 4) either burrowed very rapidly or showed a freezing posture. Some were seen to protrude their hypopharynx from which a clear drop of fluid was produced. At depths below about 30 cm, the sand was compact and formed a dense layer without galleries harbouring cockroaches. Night observations did not reveal any activity at the surface level, even in the cushion shrubs. The different types of shrubs were compared with respect to the cockroach and ootheca frequencies under them (Fig. 5). In the protected area, Salsola sp. harboured cockroaches more often than did Zndigofera sp. or grass tufts. Other plants were either scarce (Cucumk sp., Acacia sp., Asteraceae) or not preferred (Lycium sp.). Comicula sp. was too scarce to assesswhether cockroaches really preferred it. In the grazed area, Salsolasp. and, to a lesser degree, Indigofera sp. were greatly damaged by goat grazing and so decreased in size and did not harbour cockroaches. Lycium sp., on the other hand, seemed resistant to grazing and acquired a cushion-like structure. It harboured many cockroaches and oothecae. The presence of cockroaches and oothecae was highly correlated with the sand under shrubs (see Fig. 5, Spearman non-parametric correlation coefficient, K = 0.992, p c 0.01). Only grass tufts (Poaceae) harboured relatively more nymphs than oothecae. In each area, either protected or grazed, the number of cockroaches and of oothecae was correlated with the shrub diameter (Fig. 6, Spear-man non-parametric correlation coefficient, for nymphs K = O-327 and K = 0.566, and for oothecae, K = 0.332 and K = 0.568, p < 0.01). Not all shrubs harboured both nymphs and oothecae; for example, of 28 shrubs with nymphs in the protected area, only 14 harboured oothecae. In the grazed area, of 21 shrubs harbouring nymphs, five lacked oothecae. In both areas, a few shrubs harboured oothecae but no nymphs (1 and 3 respectively). Respectively, 99 and 127 cockroaches were found in the protected and grazed quadrats which represented high densities (Table 1). Few adult females were present
P. GRANDCOLAS
328
in the grazed area only and adult males were not encountered (Table 1); these adult females were assumed to be old individuals, since their appendages were damaged and their hairs abraded. The total sex ratio was biased towards the females, especially in the protected area (Table 1). Exuviae and corpses seemed equally common in both areas. Oothecae were much more common in the grazed area (Table 2). The age structures of the populations are shown in the histograms of pronotal size in males and females (Fig. 7). Three cohorts were visible: first or second instar nymphs (less than 1.5 mm pronotal width), middle&star nymphs (around 5 mm) and adult females (more than 8 mm). The populations in the protected and grazed areas showed a clear difference: the lack of adults in the protected area. If one took into account only the middle cohort, significant differences also appeared: a lower mean age. This is significant in male nymphs (Wilcoxon two-sample test, W = 6005, p < 0.01) and not Protected area 0
50
100
0
I Zndigofem
(82)n
Salsola
(15)
m
Poaceae
(14)
B
Lycium
(8) -
Acacia
(2) -
Astemceae
(1) -
Cornulaca
(1)
Cucumis
(1) -
Grazed area I Zndigofem
(0) -
Salsola
(2) -
Poaceae
(0) -
Lycium Acacia
(36)
-
(3) Ku -
Cornulaca
(0) -
Cucumis
(0) -
5. Occupancy ratios (%) of sand under Merent species of shrubs in protected and grazed areas by cockroach individuals (W) and oothecae ( ; n-be= b brackets refer& to shrub numbers in the two quadrats.
Figure
BIONOMICS OF A DESERT COCKROACH
329
in female nymphs (IV = 6493, p > 0.10). The age of the middle female nymphs also showed a wider distribution in the grazed area but it was found not significant (twotailed test of Kolmogorov-Smimov, D = O-167, p > 0.10). Significant differences appeared in the numbers of oothecae in the two areas. Their total number was higher in the grazed area (cf: supra), but this was due only to a higher number of hatched oothecae; incubating oothecae were actually less numerous in the grazed area (Table 2). Oothecae were also larger in the grazed area (Wilcoxon twosample test, IV’ = 2040, p c O-05). However, the number of eggs seemed most often to be six in both the protected and grazed areas (Wilcoxon two-sample test, W = 328.5,
20
(a)
n
K= 0.32'7 p < 0.01
. . . .
.
i
.
n
n
mm
n
. .
n
n
n
n
n
I-
*
20
*
40
1
60
80
8
I
100
I
120
1
140
!20::, . . n
. n
.
. . n
t
m I
I
0
20
40
. n
.
.
1
60
I
1
80
100
t
I
I
120
140
Shrub diameter
Figure 6. Relationships (numbers
of individuals)
between the diameters of all shrubs (cm) and the cockroach abundance in the protected area (a) and the grazed area (b); K is the non-
parametric Spearman correlation coefficient.
P. GRANDCOLAS
330
Table 1. Populatbn parameters of H. chopardiin protected and grazed areas (2om
x 2om)
Grazed area
Protected area
Parameter Total number of cockroaches Cockroach density (per m2> Adult ratio Sex ratio Number of exuviae Number of corpses
99 O-25 0% O-24 19 1
127 0.32 9.4% o-41 18 2
p > 0. lo), following both the estimates from observations of oothecae (Table 2) and hatching counts (N = two hatchings). The number of eggs per ootheca ranged from four to eight in both areas. Twenty per cent of incubating oothecae (four of 20) releasedbombyliid flies (ExhyuZunthrux blunue) from two different shrubs of each area. An unidentified tachinid fly was also obtained from nymphs breeding. Laboratory breeding showed that nymphs could feed and develop on dead leaves. Old nymphs taken in the field became adult during summer 1992. Some sampled incubating oothecae hatched before summer 1992.
2or--10 I
”
2
3 4 Pronotal
5 6 width
7
8
,)--W-.-L 2
3
2
3
4
5
6
7
8
4
5
6
7
8
20
5 p: m 10 &
0
2
3
4
5
6
7
8
0
Males
7. Age structuresof populationsfor malesand femalesin protected and grazed areas, after the pronotal width (mm) (H = larvae; = adults). Figure
BIONOMICS
Table
OF A DESERT
COCKROACH
331
2. Oothecal characterkrics in protected and grazed areas (20~1 x 2074
Characteristic Total number of oothecae Ratio of incubating oothecae Ratio of hatched oothecae Size (L x H)
Number of eggs Ratio of parasited oothecae
Protected area
Grazed area
48 25% 75% 14.7 (N=43) 5.7 (iV=16) 25%
81 9.9% 90.1% 15.2 (N=72) 6 (iV=30) 12.5%
Discussion Habitat
use and activity
The sand cockroach H. chopardi appeared principally to inhabit the sand beneath cushion shrubs that were more than 10 cm wide. It appeared to discriminate between shrubs on the basis of their morphology and not on the basis of species. Depending on grazing pressure, some shrubs became cushion-like and other became very small or nearly disappeared, and cockroaches shifted toward those which had become cushion shrubs. This habitat is very similar to that described in the Egyptian coastal desert for Hemelytroblatta ajiicana by Ghabbour et al. (1977, 1978, 1980), except that it also inhabited the sand beneath other species of cushion shrubs that were locally more abundant than Salsola or Lycium spp. Arenivaga invemgata or A. sp. seemed to be somewhat less linked to the shrubs in the North American deserts (Hawke & Farley, 1973; Edney et al., 1974; Cohen & Cohen, 198 1). They were observed to burrow into the sand anywhere or, when they inhabited sand under shrubs, to move away from them at night, leaving visible trails on the sand surface. This behaviour and the resulting trails were never observed in June 1992 for H. chopardi, the individuals of which were always under shrubs and were not seen moving away from them either during the day or at night. Two other species of Heterogamisca were observed in Saudi Arabia and their life habits were not strictly similar to those of H. chopardi (Grandcolas, 19946). H. marmowta was never found in the sand beneath shrubs, but only in rock shelters located in rocky areas. H. dispersa was extremely scarce and always solitary at the bases of small Acacia trees in central tablelands at low altitude. The co-occurrence was very weak between these three species, even if one does not take into account their different habitats, since they preferred respectively sandy areas, rocky areas of middle and high altitude, and low altitude areas. The life-habits of H. chopardi. were also clearly different from those of other eremophilous polyphagine species.Polyphaga spp. in Old World deserts (Bey-Bienko, 1950; Grandcolas, 19946) or Arenivaga apacha in the American deserts (Cohen & Cohen, 198 1) inhabit either burrows or rock shelters, and are only occasionally to be seen dispersing in the sand. Several individuals of H. chopardi were usually found under each shrub. This is indicative of gregarious habits. In solitary species, early nymphal dispersal occurs and individuals are separate (Grandcolas, 1993). The clumped distribution of H. chopardi was not due to the patchy distribution of the shrubs because individuals of the related species H. dispersa are to be found alone at the bases of Acacia trees which are also patchily distributed. Individuals of H. chopardi spent most of their time burrowing in the sand: they grew up, moulted, and laid oothecae there. They even absorbed water vapour from the sand (Grandcolas, 1994~). Activity was not observed at the surface, but may perhaps have
332
P. GRANDCOLAS
occurred at another season. Males and females may meet in this way (Chopard, 1938). Adult males were captured nightly when flying toward light (S. Biquand, pers. comm.). Some nymphs also dispersed from one shrub to another: this dispersal behaviour was attested by the ratio of shrubs with nymphs and without oothecae. More observations are needed to answer the question of whether the nymphs dispersed beneath the sand surface. Even the bombyliid parasitoids may search for oothecae in the sand, since females were never to be seen on the sand surface and deposited their oothecae deeply (one female was found burrowing while carrying its ootheca). These parasitoids are not known as parasitizing cockroach oothecae (Roth & Willis, 1960), but attack the oothecae of Orthoptera, moth pupae, fly puparia, and Hymenoptera cocoons @u Merle, 1975; Greathead, per-s. comm.). They exerted a high pressure on Heterogumiscu populations that could be compared with that exerted by some evaniid wasps on several other cockroach species. The ratio of parasitism was higher than that in the oothecae of wood-inhabiting Purcobkzttu in North America (Edmunds, 1952) and was similar to that of the oothecae of synanthropic Periplunetu americana in caves (Deleporte, 1976). Predation by scorpions on Arenivugu investigutu was often observed in North America (Hawke & Farley, 1973). These predators are also present in Saudi Arabia, but no predation was observed (pens. obs.).
Population structures and reproduction parameters The populations studied showed three cohorts: very recently hatched nymphs, older nymphs and, in one case, old females. The two first cohorts could be tentatively put in relation with the oothecae found in the sand: very young nymphs might have hatched from oothecae deposited approximately at the same time as the unhatched oothecae, while older nymphs had probably hatched from the old oothecae. The populations sampled in the grazed VS. protected areas differed in their life history parameters. However, it seems at first sight difficult to assess specifically the relative importance of reproductive effort in each area. Female densities and numbers were not known over the whole year and this does not permit numbers of oothecae to be compared. Density and sex ratio were only available for nymphal cohorts. Using this later sex ratio, it is possible to infer that the reproductive effort is much greater in the grazed area. Oothecae were twice as numerous then, but the sex ratio was less unbalanced toward females and density not much higher. This greater reproductive effort in the grazed area may also be deduced from the larger size of the oothecae. Oothecae seemed to be less often parasitized in the grazed area, however, that may also have increased the efficiency of the reproductive effort. One must, however, note that it is difficult to equate reproductive effort with population densities when one compares the protected area with the grazed area. Oothecae were twice as numerous (and larger); but population densities were only 28% higher. The survival of nymphs must be inferred to be less important. The range of variation in oothecal size appears similar when it is compared with that observed in the laboratory for l7zereu petivetiunu (Ananthasubramanian & Ananthakrishnan, 1952; pers. obs.), and small when compared with that of Arenivugu investigutu (Appel et al., 1983) and Erguulu cupensis (per-s. obs.). The structure of the populations also differed slightly between the two areas. In the grazed area, individuals of each cohort were younger: middle-instar nymphs slightly younger, and older females still alive. The sex ratio was strikingly biased but differed between the two areas. Protandry may not explain this: the youngest population showed the most unbalanced sex ratio. Different mortality ratios as well as different inheritable sex ratios may provide an explanation. These differences between grazed and protected areas were unexpected. The grazed area was intuitively considered to be a damaged environment with less vegetation and
BIONOMICS
OF A DESERT
COCKROACH
333
a lower capacity to shelter populations of detritivorous cockroaches. Cockroaches were, however, actually more abundant in the grazed area. Several factors could be responsible for that situation. First, what were envisaged as negative physical constraints in the grazed area could be enhancing factors for cockroach populations. For example, less vegetation cover allowed the wind to cause the sand to drift and to provide more favourable burrowing places at the bases of shrubs. This could also lead to larger accumulations of organic matter at the bases of shrubs. Goats were responsible for grazing the vegetation but could also provide local enrichment of the ground litter with their faeces. Grazing pressure caused a shift toward another species of shrub: this species (Lycium sp.) may provide litter with higher nutritive value, or present roots with palatable mycorhizal fungi, as documented for Arenivugu investigatu (Schal et al., 1984). Higher fecundity in terms of oothecal number and/or size is generally related to a better diet (e.g. Roth & Willis, 1954). Conversely, the later state of the population in the grazed area could be due to the lesser capacity of the environment to hold moisture (lesser vegetation cover etc.). Though several Polyphaginae cockroaches are able to absorb the atmospheric water vapour (Edney, 1966; Vannier & Ghabbour, 1982; Grandcolas, 19944, their populations are strongly influenced by the ground moisture content (Ghabbour et al., 1977). H. chopardi appears to be an important element in the poorly known soil fauna of the Saudi deserts. Its densities are high, and it is present in both protected and grazed areas. It is similar to Hemelytroblatta africana in Egypt (Ghabbour et al., 1977), but has several unique features-its biased sex-ratio, and parasitism by bombyliid flies. Its detritivorous habit suggests that it may play an important role in the cycling of organic matter in the soil beneath shrubs. Acknowledgements I am grateful to Abdulrahman Khoja, Sylvain Biquand and George Schwede for their invitation to work as a guest researcher at the National Wildlife Research Center in Saudi Arabia. Plant species in the study areas were identified with the help of S. Biquand. I also wish to thank the staff of NWRC for their kind assistance, P. Deleporte, L. Desutter, N. Menard and an anonymous reviewer for reading my manuscript, D. Greathead, L. Matile and L. Tsacas for the identification of parasitoids, and J. Marshall for the loan of the holotype of H. chopardi deposited in the British Museum.
References Ananthasubramanian, K.S. & Ananthakrishnan, T.N. (1959). The structure of the ootheca and egg laying habits of Cotydiu petiveriuna L. (Blattidae). Indian Journal of Entomology, 21: 59-64. Appel, A.G., Van Dyke, A.M. & Rust, M.K. (1983). A technique for rearing and some notes on the biology of a desert sand cockroach, Arenivugu investtgutu (Dictyoptera: Polyphagidae). Ibceedings of the Enwmologicul Society of Wushington, 85: 598-600. Bey-Bienko, G.I. (1950). Fauna of the USSR. Insects. Bluttodeu. Moscow: Institute of Zoology, Academy of Sciences of the URSS. 342 pp. Chopard, L. (1929). Orthoptera palaearctica critica. VII. Les Polyphagiens de la faune palearctique. Eos, 5: 223-358. Chopard, L. (1938). La Biologie des Orthoptkes. XX. Encyclop.4die enwmolog@ue. Paris: Lechevalier. 541 pp. Cohen, A.C. & Cohen, J.L. (1981). Microclimate, temperature and water relations of two species of desert cockroaches. Comparative Biochemistry and Physiology, 69: 165-l 67. Deleporte, P. (1976) L’organisution Sociule Chez Perzplaneta Americana (LXcyopdres): aspects bcokthologiques, ontogenbe des relations interindividuelles. Universite Rennes: These Doctorat 3eme cycle. 60 pp.
334
P. GRANDCOLAS
Du Merle, P. (1975). Les h&es et les stades pr&imaginaux des Diptltres Bombylidae: revue bibliographique armotee. UIBS, Bulletin SROP I WRS Bulletin: l-289. Ednumds, L.R. (1952). Some notes on the habits and parasites of native wood-roaches in Ohio (Grthoptera: Blattidae) . Entomologuxzl News, 63: 14 l-l 45. Edney, E.B. (1966). Absorption of water vapour from unsaturated air by AYeniqV SP. (Polyphagidae: Dictyoptera). Comparative Biochemisny and Physiology, 91: 387-408. E&ey, E.B., Haynes, S. & Gibo, D. (1974). Distribution and activity of the desert cockroach Armivaga invescigata (Polyphagidae) in relation to microclimate. EcoZO~, 55: 420-427. Ghabb&r, S.I., M&hail, W.Z.A. & Rizk, M.A. (1977). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. I. Summer populations of soil mesofauna associated with major shrubs in the littoral sand dunes. Revue d’Ecologie et de Biologie du Sol, 14: 429459. Ghabbour, S.I. & M&hail, W.Z.A. (1978). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. II. Soil mesofauna associated with Thymelea hirsutu. Revue d’Ecologie et de Biologie du Sol, 15: 333-339. Ghabbour, S.I. & Shakir, S.H. (1980). Ecology of soil fauna of mediterranean desert ecosystems in Egypt. III. Analysis of Thymelea mesofauna populations at the Mariut frontal plain. Revue d’Ecologie et de Biologie du Sol, 17: 327-352. Grandcolas, P. (1993). Habitats of solitary and gregarious species in the neotropical Zetoborinae (Insecta, Blattaria). Studies in Neotropical Fauna and Environment, 28: 179-190. Grandcolas, P. (19940). The appearance of xylophagy in cockroaches: two case studies with reference to phylogeny. youma of Onhoptera Research, 2: 000-000. Grandcolas, P. (1994b). Phylogenetic systematics of the subfamily Polyphag-inae, and assignment of Ctypwcercus Scudder, 1862 to this taxon (Blattaria, Blaberoidea, Polyphagidae). Systematic Entomology, 19: 145-158. Grandcolas, P. (1994~). Evidence for hypopharynx protrusion and presumptive water vapour absorption in Heterogamisca chopardi (Dictyoptera: Blattaria: Polyphaginae). Ann&s de la Societl Enwmologigue de France (NS.), 30: 361-362. Grandcolas, P. (19944. Blattaria (Insecta, Dictyoptera) of Saudi Arabia: a preliminary study. In: Biittiker & Krupp, (Ed.), Fauna of Saudi Arabia, pp. 40-58. NCWCD, Pro Entomologia, Riyadh, Basle. ’ Grandcolas, P. & Deleporte, P. (1992). La position systematique de Cmrocercus Scudder, 1862 au sein des Blattes et ses Implications evolutives. Comptes-Rendus de Z’Acadkmie &s Sciences de Paris, @rie III), 315: 317-322. Hawke, S.D. & Farley, R.D. (1973). Ecology and behaviour of the burrowing cockroach, Arenivaga sp. Oecologia, 11: 263-279. O’Donnell, M.J. (1977). Site of water vapor absorption in the desert cockroach, Arenivuga invesugara. Proceedings of the National Academy of Sciences of USA, 74: 1757-1760. Princis, K. (1962). Pars 3: Blattariae: Subordo Polyphagoidea: Fam. Polyphagidae. &&prerorum Cutalogus. ‘s-Gravenhage: Junk. 74 pp. Roth, L.M. & Willis, E.R. (1954). The reproduction of cockroaches. Smithsonian Miscellaneous col-lmions, 122: l-49. Roth, L.M. & Willis, E.R. (1960). The biotic associations of cockroaches. Smithsonian Miscelkzneous Collections, 141: l-470. Schal, C., Gautier, J.Y. & Bell, W.J. (1984). Behavioural ecology of cockroaches. Biological Review, 59: 209-254. Dvarov, B. (1936). I. Studies in the Arabian Orthoptera. I. Descriptions of new genera, species, and subspecies. Journal of the Linnean Society of Lordon, Zoology, 39: 531-549. Vannier, G. 8~ Ghabbour, S.I. (1982). Effect of rising ambient temperature on transpiration in the cockroach Heterogumiu syriuca Sauss. from the mediterranean coastal desert of Egypt. In: hbm, P., Andre, KM., Medts De, A., Gregoire-Wibo, C., Wauthy, G. (Ed), New Trends in Soil Biologv. Proceedings of the VIII International Colloquium of soil zoology. Louvain-la-Nmue (Belgium). August 3GSeptember 2, 1982, pp. 441-453. Ottignies, Louvain-la-Neuve: DieuBrichart. 709 pp. Walker, D.H. & Pittaway, A.R. (1987). Insects of Eastern Arabia. London: MacMillan. 177 PP. Yaman, 1.K.A. (1972). Orthoptera of the central province of Saudi Arabia. Z&,&rift fiir Angewandte Enwmologie, 70: 88-92.