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<oological Journal of the Linnean Sociely (1987), 89: 63-88. With 12 figures Regional environments, life-history patterns, and habitat use of spirostreptid millipedes in arid regions C. S. CRAWFORD Department of Biology, University of N e w Mexico, Albuquerque, N M 87131, U.S.A. K. BERCOVITZ AND M. R. WARBURG Department of Biology, Technion-Israel Institute of Technology, Hazfa 32000, Israel Received September 1985, accepted for publication November 1985 Among diplopods with desert populations, only three species of Spirostreptida have been studied in an ecological context. The present review compares regional environments, life-history patterns, and uses of habitat by Orfhoporus ornatus (Girard) from southwestern North America, Archispirostreptus tumuliporus judaicus (Attems) from the eastern Mediterranean seaboard, and Harpagophora nigra (Attems) from southwestern Africa. Published and unpublished studies are used to explore evidence for convergence among these species, as opposed to traits adapting them to physical aspects of given regions or habitats. Unlike A . t. judaicus, 0. ornatus and H . nigra are relatively restricted to arid habitats, although populations of all three species experience a variety of rainfall regimes and regional topographies. Where studied, 0. ornatus and H . nzgra hibernate during the long, often cool or cold dry season; they forage following warm-season rains. A . 1. judaicus, in contrast, forages during its long, warm dry season and hibernates in the cool, wet winter. Populations from the Judaean and Negev deserts differ from those inhabiting a mesic habitat (Megiddo) closer to the coast in regard to rates of development, seasonal activity and seasonal water balance. Convergence in the form of well-developed desiccation resistance characterizes the two strictly desert species. All three species, together with other subtropical millipedes exposed to long dry seasons, are convergent with respect to patterns of die1 surface activity and use of shelter. However species- and habitat-specific life-history features such as the seasonal timing of dormancy and emergence tend to mask convergence at the habitat level. Hence, the independent evolution of the three species with desert populations has resulted in life histories and habitat use that combine a moderate amount of convergence with considerable opportunistic adaptation to regional and local conditions. KEY WORDS:-Spirostreptid millipedes - regional environments life-history patterns egg pellets - postemergence development - seasonal biology feeding - dormancy - shelter water balance. ~ ~ ~ ~ CONTENTS Introduction . . . . . . . . . . . . . Regional environments of arid-land Spirostreptida . . . . Regional environments of Orthoporus ornatus . . . . . Regional environments of Archispirostreptus tumuliporousjudaicus Regional environments of Harpagophora nigra . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 65 65 67 69 63 0024-4082/87/010063 +26 $03.00/0 0 1987 T h e Linnean Society of London 64 C. S. CRAWFORD ET A L . Life history patterns of arid-Iand Spirostreptida . . . . . . . Orthoparus ornatus: events within and emergence from the egg pellet . Orthoparus ornatus: postemergence development . , . . , Archispirostreptus tumuliporusjudaicus: events within and emergence from the egg pellet . . . . . . . . . . . Archispirostreptus tumuliporusjudaicias: postembryonic development . Harpagophora nigra: some developmental characteristics . . . Habitat use by and-land Spirostreptida. . . . . . . . Orthoparus ornatus: the feeding season . . . . . . . Orthoparus ornatus: the dormancy season. . . . . . . Archispirostreptus tumuliporus judaicus: surface activity and feeding . Archispirostreptus tumuliporusJudaicus: dormancy . , . , . Harpagophora nigra: comments on habitat use . . , . , Discussion and conclusions . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . 71 71 13 75 17 79 80 80 82 83 84 85 85 87 87 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . INTRODUCTION Most species of millipedes inhabit mesic environments, which are generally much better known, faunistically, than are arid environments. As a consequence, much of what we know of diplopod biology derives from studies of forest and grassland taxa in the Holarctic realm (e.g. Camatini, 1979; Demange, 1981). Comparatively few groups of diplopods seem to be represented in arid regions, although species in the orders Polyxenida (Chamberlin & Mulaik, 1941; Wallwork, 1982; Lewis, 1984), Polydesmida and Julida (Chamberlin & Mulaik, 1941), and Spirobolida (Hoffman & Orcutt, 1960) have been so recorded. I t is in the generally large-bodied Spirostreptida, however, that most of the obvious arid-zone species occur. I n particular, three Spirostreptida families contain species that cope with long periods of drought. These are the Odontopygidae in Africa, the Harpagophoridae in Africa and the Indian subcontinent, and the Spirostreptidae in Africa, the Middle East and the New World (Lawrence, 1965, 1966; Krause, 1966; Hoffman, 1979; Krabbe, 1982). The presence of spirostreptids in subtropical deserts of Africa and North America has been attributed to morphological and biochemical traits that augment cuticular resistance to water loss, and to a presumed capacity in dormant individuals for water vapour uptake from unsaturated air (Crawford, 1979). I n the present review we focus on the regional environments, life-history patterns, and habitat use of two well-studied spirostreptids and one briefly investigated harpagophorid. Our purpose, through the use of published and unpublished studies, is to explore the extent to which adaptations may be convergent (or perhaps more correctly, “parallel”: Mayr, 197 1) in these distantly related and widely separated species. Our intial expectations were that convergence should be evident at several levels (e.g. physiological, morphological, behavioural), as it is in many desert plants and vertebrates (Cloudsley-Thompson, 1977; Luow & Seely, 1982). That our findings were generally not in accord with these expectations implies that the evolutionary responses of this ancient group of arthropods are adapted to quite different regional environments. BIOLOGY OF DESERT MILLIPEDES 65 Figure I . Climatic diagrams covering the geographical distribution of Orthoporus ornalus. Values on rach diagram are as follows: mean monthly temperatures in increments of 10°C (left margin), mean monthly precipitation in increments of 20 mm (right margin), and 2 month intervals beginning with January on the left (horizontal axis). Stippled areas represent periods of relativc drought. REGIONAL ENVIRONMENTS OF ARID-LAND SPIROSTREPTIIIA Regional environments of Orthoporus ornatus Because of its extensive distribution in southwestern North America (Causey, 1975), Orthoporus ornatus (Girard) (Spirostreptidae) experiences an extremely diverse set of regional environmental influences. I n general the regional climate is semi-arid to arid; however, such terms say little about the variable distribution of annual precipitation. That variation is illustrated in Fig. 1, which presents climatic diagrams covering locations where 0. ornatus has been found (mean monthly values are based on those reported by Wernsted (1972) 66 C. S. CRAWFORD E T AL Figure 2. Habitats of Orthoporus ornatus. A, Mid-Pleistocene volcanic escarpment several kilometres west of Albuquerque, New Mexico. B, Outwash plain and sandstone cliff at Big Bend National Park, Texas; Fouquieria splendens is the most common shrub. for Mexico and by the National Oceanic and Atmospheric Administration (1980) for the United States. Winter precipitation generated by fronts moving inland from the Pacific Ocean is relatively important in the northwestern portion of the range. By contrast, summer rains resulting from monsoon air BIOLOGY OF DESERT MILLIPEDES 61 moving west and north from the Gulf of Mexico tend to be the dominant form of annual precipitation over its eastern portion. Overall seasonal averages vary from 105 mm (Yuma, Arizona), to 726 mm (Wichita Mountains, Oklahoma). Part of the winter precipitation in the northern portion of the range arrives as snow. Annual excursions of temperature in arid environments are of course considerable. In the context of this review that fact is dramatized by average monthly maximum and minimum temperatures, respectively, in July and January for Yuma, Arizona (42.6-9.4"C) and Albuquerque, New Mexico (37.3-1.8"C) (National Summary, 1980, Climatological Data, U.S. National Oceanographic and Atmospheric Administration). Variations in annual temperature are much smaller near seacoasts (e.g. Hermosillo, hlonterry) than at inland locations (Fig. 1 ) . Topographies, soils and vegetation in 0. ornatus habitats (Fig. 2) are by no means equivalent throughout the species' range, although combinations of these habitat features must provide populations with adequate shelter if drought, heat and cold are to be survived. Shelter often takes the form of rodent burrows and ant nests, as well as large surface stones and rock outcrops. Basalt-flow habitats confer excellent shelter to the north (Crawford, 1976, 1978), as do the lower slopes and terraces of large riparian channels such as those created by the Colorado River in the Grand Canyon (Causey, 1975; Crawford, unpubl. obs.). Such places probably constitute warm, post-Pleistocene refugia ('thermal islands' in effect) separated by terrain in which soils often freeze during winter. In contrast, populations to the south are commonly distributed over broad, flat expanses having surfaces of desert pavement. Most habitats of 0. ornatus support a flora dominated by shrubs. In some places a single shrub species dominates. This is true, for example, for Coleogyne ramosissima on the Grande Canyon's Tonto Plateau and for Larrea tridentata over much of the southern range, where Propasopis glandulosa may also provide significant cover. Species of Opuntia, Yucca, Fouquieria, Agave, Atriplex and Dalea may be locally abundant, as may the disturbance-induced subshrubs Gutierrezia sarothrae and Salsola kali. Grasses and forbs occur throughout this millipede's distribution, although grasslands as such are not commonly used habitats. Sandy loam aridosols are probably the most characteristic soils of 0. ornatus habitats. Powdery grey loam, comparatively heavy in clays, characterizes a floodplain used extensively by 0. ornatus in western Texas (Wooten, Crawford & Riddle, 1975). Regional environments o f Archispirostreptus tumuliporus judaicus Archispirostreptus tumuliporus judaicus (Attems)* (Spirostreptidae) has been rcported from diverse locations along the eastern seaboard of the .Mediterranean (Krabbe, 1982). We surmise that before the extensive establishment of human settlements in that region, populations of A. t. judaicus may have covered large areas. At present, however, they are restricted to widely separated habitats, *This is the A syrzacus (De Saussure) of Bercovitz (1984), Bercovitz & Warburg (1985),Crawford & Warburg (1982), and Crawford, Goldenberg & Warburg (1986) We use the new name in kcepng wlth the recent systematic revision of the Spirostreptidae by Krabbe (1982) ' C. S. CRAWFORD E T AL. 68 Megiddo i Brosh . -'Va 350 Figure 3. Climatic diagrams for the three main Archispirostrephs tumulzporzrs judaicus habitats in this study. Diagram values are as in Fig. 1. three of which were visited regularly in our study of this species in Israel (Fig. 3). One of these habitats, Megiddo, is the archaeological site of a n ancient town (Fig. 4A) on the southern fringes of the Jezrael Valley, 35 km southeast of Haifa. There, at a n elevation of 150 m above sea level, the climate is mild Mediterranean with long, dry summers. Annual rainfall a t Megiddo is 500-1000 mm. Vegetation on the site is heavily disturbed by human activities and dominated by the shrubs Prosopis fureata and Athagi maurorum. At Megiddo there are also a few palm trees, Washingtonia sp. and Phoenix dactylifera. Soils at Megiddo are of the redzina type and subject to considerable burrowing activity by large numbers of these millipedes. The second habitat, a site named Brosh (Fig. 4B), is much more xeric than Megiddo. Brosh is located on the eastern slopes of a large hill 200 m below sea level in the Jordan Valley, 70 km east of Haifa. Annual rainfall in the nearby Beit Shean Valley is 200-450 m. Vegetation at Brosh is typical fringe-type Mediterranean and consists mainly of ephemerals. Two perennials, Asphodelus m;rrnmrhi,r ,,l*Y,"YU, yu" anA UllU PnAnnnrmn "U".*"Y.IIU 1 r&nriim ' U Y U , , " ) .rr, "atJtn J""'n p a r tn L" he uL n a r t i r i i l a r l7 v " c ';fjm n;firQnt ""'"U"' tJ-1 cI-uAuL1 ac u u a u source of food and temporary shelter for A . t. judaicus. Rocky outcrops also BIOLOGY OF DESERT MILLIPEDES 69 Figure 4. Habitats of Archis@streptus tumuliporus juduzcus. A, Megiddo archaeological site with Wushingtonia palm. B, Brosh hillside with exposed limestone cliff harbouring many millipedes. C , Dimona hillside with limestone outcrops and collapsed caves; most shrubs are Hammaa'a sp. afford considerable shelter because of the crevices they provide. Soils are again of the redzina type. T h e third habitat, on the outskirts of the town Dimona (Fig. 4C), is situated in the northern Negev desert, 35 km south of Beer Sheva and at an elevation of 600m above sea level. The specific sites examined at Dimona occur on the eastern slope of a hill with limestone outcrops and collapsed caws. Between 50 and 100 mm rain falls there annually. Local vegetation is typified by the following shrubs: Haloxylon spp., Hammada spp., Roetema spp., Thymelea hirsuta and Asphodelus spp. The latter two are more typical of Mediterranean than Negev communities and may be relics from a more mesic period. Soils in this region are mixed sand-loess. Regional environments of Harpagophora nigra As with 0. ornatus and A . t. judaicus, Harpagophora nigra Attems (Harpagophoridae) is distributed over a great variety of habitats. Its distribution appears relatively continuous east of the escarpment that separates the Namib desert from the high veld to the east (Lawrence, 1965). A climatic 70 C. S. CRAWFORD E T A L . Figure 5. Climatic diagrams for two known habitats of Hurpugophoru nigru. Only the Mirabib habitat is discussed in this study. Diagram values are as in Fig. 1. diagram representing the latter area (ranging between 1000 and 1500m in elevation) is shown in Fig. 5, as is one estimated for Mirabib Hills in the lower desert to the west. A fringe population of H. nigru was studied at Mirabib (elevation 500 m) by Crawford & McClain (1983). There, the climate is much drier and, on an annual basis, more thermally stable than it is above the Figure 6. Habitat of Hurpugophoru n i p at Mirabib Hills. Most specimens were excavated from soil at the base of this boulderous inselberg. BIOLOGY OF DESERT MILLIPEDES 71 escarpment. Rainfall at Mirabib is extremely variable and merages about 57 mm annually, mostly arriving in the local winter. This moisture is supplemented by a n annual average of 17 mm of fog precipitation that moves in from the Atlantic coast, some 100 km distant. T h e desert population was mainly in a state of subterranean clormancy when studied. Specimens were recovered from sandy-gravel soils containing some silt that fringed a boulderous inselberg (Fig. 6). Runoff from infrequent precipitation collects in these soils, which support a ‘gutter’ community characterized by the deciduous tree Acacia r@ciens, the dwarf shrub Adenolobus pechuelii, and the grass Stipagrostis hochstretterana (Robinson, 1975). Crawford & McClain (1983) found several millipedes at the base of the shrub-tree Commiphora saxicola next to the inselberg. Some specimens were also seen in rock crevices. LIFE-HISTORY PA1 I E R N S O F ARID-LAND SPIROSTREPTIDA Orthoporus ornatus: events wtthin and emergencef r o m the egg pellet Pellet material that appears to be partly o r completely fhecal in origin surrounds each egg of 0. ornatus; such a condition is known for other Diplopoda as well (references in Crawford & Matlack, 1979). Pellets of this North American desert millipede are deposited in clutches of approximately 50-500 within shallow subterranean chambers. Such excavations occur mainly in old rodent burrow systems and beneath rocks. Pellet deposition seems to take place within a month of adult emergence from the overwintering hibcrnaculum (see below). Judging from a record of stadium I larvae that emerged from a clutch of pellets collected on 3 July 1976 near Albuquerque, New Mexico (Table l ) , Table 1. Collection dates and key morphological features of postembryonic stadia within the egg pellets of Orthoporus ornatus Numbers of key features ~- ~~~~ Stadium 1 I1 I11 Dates collected* 19 March 1974” 3 July 1976 21 October 1977b 19 March 1974” 8 June 1976 12 June 1978‘ 22 June 1975 21 October 1977b 15 May 1974 15 May 1974d 111 June 1978’ 15 May 1974‘ Occlli Defence glands Pod0u.j segments I 0 0 3 1 2 6- 7 19 20 * Dates followed by a common letter indicate the presence of two different stadia within the same egg pellet clutch. Pellets collected on 15 May 1974 came from Big Bend National Park, Texas; all other came from a volcmic outcrop near Albuquerque, New Mexico. 72 C. S. CRAWFORD E l AL. Figure 7. Early development in Orthoporus ornatus. A, Anamorphic first stadium following removal from its egg pellet; note empty chorion (larva is 3 mm in length). B, Egg pellet from which presumably stadium 111 has emerged, leaving faecal pellets behind (pellet averages 6 mm in length). hatching in the summer occurs roughly 1 week after clutch deposition by the parent. However, Table 1 also shows that members of stadium I were collected in October and March. Moreover, in each instance stadium I1 larvae were also present in pellets belonging to the same clutch. First instars are anamorphic, having only three individual pairs of legs (Fig. 7A). Distinguishing features of what are probably the three within-pellet instars are given in Table 1. The first post-hatch moult can occur before late October near Albuquerque; this conclusion is derived from the finding mentioned above. However, stadium I1 larvae within their pellets were also found in March and June at the same location. Also, stadia I1 and I11 larvae were found together in the same clutches, both near Albuquerque and at Big Bend National Park, Texas. Stadium I1 larvae were studied for their water relations by Crawford & Matlack ( 1979), who stated incorrectly that these larvae possessed only three pairs of legs when in fact they possess two podous diplosegments as well as the original three leg pairs. Such individuals are able to ingest water orally and rectally, and can osmoregulate effectively. While the pellets are somewhat less capable of maintaining stable water activity (a,) than are the larvae themselves, pellet presence was felt to buffer additionally against fluctuations in soil moisture (Crawford & Matlack, 1979). The within-pellet moult, leading to what we surmise is the third stadium, may take place shortly before the onset of summer rains, generally in mid-May in west Texas and in late June or early July in central New Mexico (see Table 1 ) . Stadium I11 larvae feed extensively on the wall of the surrounding pellet, producing in turn faecal pellets of their own (Fig. 7B). Such feeding presumably enables acquisition of a gut flora capable of digesting materials such as cellulose, although this has not been examined. These larvae, with many podous diplosegments and repugnatorial glands, are easily distinguished from the previous stage (Table 1). Emergence from the pellet is probably triggered by rapid wetting of surrounding soil as a result of early summer rains. Pellets collected near Albuquerque in late June produced stadium I11 emergents within 48 h when water was applied topicaly and periodically in the laboratory during the following week (Crawford, unpubl. obs.). We surmise that these larvae soon BIOLOGY OF DESERT MILLIPEDES 73 would have moulted again in the field (they were not followed carefully after emerging), because large numbers of small larvae with at least 25 pairs of defence glands were seen on the surface at Big Bend in early June following very heavy rains. Nevertheless, such an appearance is extremely rare; new emergents nearly always remain underground and probably do not forage on the surface for another year. A J-shaped curve of mortality is surely typical for 0 . ornatus, assuming that the many clutches with pellets containing only a small bit of fungus-ridden, shrivelled tissue (Crawford, unpubl. obs.) are an accurate indicator of a n early death. Although no records were kept of the actual proportions of 'inviable' pellets, findings over the years suggest that this state occurs at least 90% of the time. The cause is not clear. Orthoporus orna tus: postemergence development We do not yet know the number of stadia occurring between emergence from the egg pellet and attainment of reproductive maturity. In lieu of reporting incomplete data on this matter we begin the present section with a discussion of the moulting phenology of 0. ornatus. Fortunately, fortuitous excavations of many individuals in late dormancy have provided a fairly believable picture of the timing of annual moult in New Mexico populations. The approximate proportions of excavated animals in some phase of moult is shown in Table 2. Specimens about to moult have fragile cuticles with white flecks (air spaces resulting from partial digestion of the old endocuticle). Moulting takes place along fracture lines in the exoskeletcin. Postmoult specimens are extremely soft; their complete or partly eaten exuviae remain next to them in the soil hibernaculum (Fig. 8). Regardless of the year, all New Mexico specimens in some phase of moult were observed during the month of June. And, as Table 2 indicates, in any given year most individuals in a population appeared to moult within 1 week of each other, a.lthough peak moulting activity varied by 3 weeks or more from year to year. Table 2. Field observations of moulting in Orthoporus orizatus Location BBNY* Jornadat A1 buq uerque i\lbuquerque Albuquerque Albuquerque Albuquerque Albuquerque Albuquerque A1 buq uerq ue Albuquerque Date 14 May 1974 4 June 1972 22 June 1975 27 June 1975 8 June 1976 8 June 1977 16 June 1977 12 June 1978 15 June 1978 21 June 1978 24 June 1979 Soil temperature ("C)at lOcm depth at visit ~ 25 25 ~ 26-28 27 26-28 ~ 23-24 25 -~ Proportions in various stages of moult (and estimates of total numbers observed) One small individual moulting, two I ecently moulted About half moulted ( % 100) Nearly all moulted (50-100) Most recently moulted (30-50) All recently moulted (50-100) Few moulted, most appear ready (30-50) About half moulted, rest pre- or postmoult (50-100) About 25% moulting, rest premoult (30-50) Nearly all moulted (30-50) All recently moulted ( % 100) Less than half moulted, rest premoul (10-30) *Big Bend National Park (Tornillo Flat), Texas. z 40 km north of Las Cruces, New Mexic3. t New Mexico State University research site, 74 C. S. CRAWFORD E T AL. Figure 8. Recently moulted Orthoporus ornatus (medium size) excavated in its overwintering soil hibernaculum. Note complete exuvium, part of which is usually eaten. Postmoult emergence from the hibernaculum coincides with the onset of major summer rains in New Mexico and west Texas, and is often manifested by spectacular numbers of individuals moving in many directions (Causey, 1975; unpubl. obs.). The emergence act itself becomes possible with a wetting of the previously hard, dry soil. I n order for these millipedes to move to the surface, however, they must possess hardened cuticles, and since this process takes roughly 1 week, approximately that amount of time must elapse between moult and onset of first rain if that rain is to be effective in promoting emergence. I t would be interesting to determine the life-history consequences of inappropriately timed moult with respect to the first heavy rain. By early July in much of New Mexico, dormant millipedes have not eaten for 7-9 months, have used a relatively great amount of energy in ecdysis (inference from data in Wooten & Crawford, 1974), and may have lost a great deal of body water to their surroundings during ecdysis (Crawford, 1978). Relatively early emergence should therefore be important to survival, and perhaps to subsequent reproduction and maintenance. I n Big Bend National Park (western Texas) monsoon rains usually arrive from the Gulf of Mexico in May, and also promote emergence in local populations of 0. ornatus. I n contrast, occasional rains in New Mexico that derive from the same May frontal systems do not bring on significant emergence. However, in the Albuquerque region a small number of usually large specimens sometimes come to the surface as early as April. These may have overwintered at shallow depths in loose soil and may have responded to unusually substantial spring rains. While on the surface they feed; whether they moult later with the rest of the population is not known. Once 0. ornatus adults have emerged from their soil hibernacula, another 3-4 months are available to them for ovarian development and reproductive events. Copulation in the field is seldom seen but was recorded by Crawford during morning hours following days of heavy rains at Big Bend (early June 1972) and BIOLOGY O F DESERT MILLIPEDES 75 near Albuquerque (late July 1977). Egg laying, in contrast, has never been recorded, probably because gravid females dig subterranean chambers in which they deposit their egg-containing pellets. Chambers are often within 10-20 cm of walls and floors of crevices (in rocky areas) or vertebrate burrows. Such proximity to pre-existing channels fits with the observation that 0. ornatus digs poorly in all but moist and loosely packed soils. Ovarian development is better understood. Many dissections ol’ Albuquerque specimens have shown that adult females in premoult dormancy contain oocytes no larger in mean diameter than 1.0 mm and mostly less than 0.5 mm. A low proportion of these small oocytes exists in a state of “apparent reabsorption” (Crawford & Warburg, 1982). (A single female collected on 15 April 1982 by Norman Scott at Tiburon Island in the Gulf of California also contained small oocytes.) Within 1 week of postmoult emergence (near Albuquerque) larger oocytes (1.0-2.0 mm) have developed, and before 1 month has elapsed the largest size ( >2.0 mm) is in evidence (Crawford & Warburg, 1982). Comparable development occurs more than 1 month earlier at Big Bend, judging from field dissections of recent postmoult individuals there on 3 June 1978 (Crawford, unpubl. obs.). Thus, regardless of the population, there must be a similar vitellogenic response to the commencement of summi:r rains. Archispirostreptus tumuliporus judaicus: events within and emergence f r o m the egg pellet As with 0. ornatus, a maternally formed pellet surrounds the egg and early stages of A . t.judaicus (Fig. 9A). Development a t and beyond this point has been Figure 9. Early development in Arrhispzrostreptw turnuliporus judaicus. A, Chorionated embryo within its cgg pellet. B, Stadium IV larva removed from cgg pellet. Note delicate defence glands a t posterior end of body. Scale is in millimetres. C. S. CRAWFORD E T AL. 76 ov en I fI ad nIIIrnYmmnmZxxmxm XE xmm Figure 10. Diagram comparing life histories of Archispirostreptus tumuliporus juduzcus populations from Brosh (above) and Megiddo (below). Months are represented on the vertical axis, stadia on the horizontal axis. Years of life are shown in circles. Bars indicate duration of the stadium; lines connecting bars indicate periods of inactivity following emergence from the egg pellet. ov = oviposition period; en = period of encapsulation in egg pellet; fl = duration of free-living larva: ad = duration of adult stadia. studied extensively by Bercovitz (1984) and Bercovitz & Warburg (1985). Clutches averaging about 64 (Megiddo females) and 75 (Brosh females) pellets were observed in the laboratory (at the bottom of rearing boxes containing soil), but were not seen in the field where they are presumed also to be subterranean. Figure 10 shows that females collected from Megiddo produced pellets between July and August, whereas females from Brosh did this from mid-April to the end of July. Bercovitz (1984) noted that male presence was not necessary for pellet formation. Three stadia are passed in the pellet by Megiddo and Brosh millipedes. I n Brosh these stadia spend relatively little time in each stage (Fig. 10). At Megiddo (Fig. 9B) emergence from the pellet by stadium I11 larvae occurs in winter, near the end of the rainy season; however, at Brosh it takes place a t least 1 month after the end of the winter rains (Fig. 10). Thus, unlike 0. Ornatus in North America, this species does not seem to depend on moisture to trigger emergence from the pellet. BIOLOGY OF D E S E R l MILLIPEDES 77 Archispirostreptus tumuliporus judaicus: postemergence dever'opmenl Much more*isknown about the postembryonic development of A . t. judaicus than of the North American millipede. Also, we now know that the development of at least two populations of A . t. judaicus differ in regard to phenology (Fig. lo), and to some extent in morphology (Tables ::-6). At Megiddo, the newly emerged third stadium moults in mid-April. Stadium I V individuals remain active until October; then they move underground only to re-emerge as stadium V the following spring. I n the third year of life Megiddo specimens moult in early summer. As members of the sixth stadium they stay underground between early October and mid-March (a hibernation pattern repeated throughout the rest of their lives, although in subsequent years moulting always occurs during hibernation). At Brosh the newly emerged larvae (in stadium V) apparently moult three times (rather than once) in the second year of life. Hence it is stadium VIII (rather than I V at Megiddo) that enters hibernation for the first time. Such dormancy, moreover, is considerably shorter in the Brosh population, since it takes place between mid-October and mid-February. Moult to stadium IX occurs in late spring at Brosh; thereafter all moults occur in early spring following the domancy period. While the phenology of moult in this species has only been inferred from laboratory observations of larval specimens, two points seem clear enough: (1) timing of moult differs between the populations studied; and (;!) only in the Megiddo population does moult occur during the dormant period (as it does in 0. ornatus). Table 3. Progression and duration of key morphological features of Archispirostreptus tumuliporus judaicus from Megiddo (pooled data from both sexes) Condition and stadium* Duration? (weeks) N ~ or. podous segments: No. of apodous segments No. of leg pairs N ~ or. defence glands I n egg pellet I 8 3 8 12 4 6 26 ? I1 20 6 I 47 0 1 21 37 18 37 52 52 52 52 52 32 35 42 49 55 62 68 73 3 7 7 6 7 6 5 3 59 65 79 91 105 117 127 133 26 30 37 44 50 57 63 68 52 52 76 77 77 1 0 0 135 137 137 71 72 72 I11 Free larvae IV v VI \'I I VIII IX X XI Adults XI1 XI11 XIV ? *Determined according to number of ocelli (Vachon, 1947). +These do not include an inactive period (hibernation) of about 10 weeks. $ Includes the collum. C. S. CRAWFORD E T A L 78 Table 4. Morphological measurements (E+ s . E . ) of early larval Archispirostreptus tumuliporus judaicus* from Megiddo ( M ) and Brosh (B) _____ _____ ____ ~ No. of specimens ~ No. of defence glands ~ Total no. of segments ~ Stadium M B M B M B 11 111 7 17 12 3 17 4 8 II 2 4 I +o 21 kO.2 26k0.2 30k03 37k0.3 120 21 k0.l 26+0 32k0.2 37f0.3 42f0 49k0.2 27+0 33k0.3 38k0.2 44k0.1 50k0.1 IV V VI 27k0.2 32k0.5 37k0.7 * All specimens were reared from eggs in the laboratory except stadia V (from Brosh), and V and VI (from Megiddo). Table 5. Morphological measurements (2+_s.E.) of male Archispirostreptus tumuliporus judaicus from Megiddo ( M ) and Brosh (B) No. of specimens Total no. of segments ~~~ Stadium ~ Mid-segment width (mm) ________~ M B M B M B 40 32 26 27 29 5 4 1 12 16 16 29 55k0.2 62+0.2 68f0.3 74 k0.5 7650.3 78k0.3 78k0.8 55k 1.0 60 68 f0.8 74 k 0.5 78k0.3 78k0.3 2.8k0.02 3.7 k0.05 3.7 k0.05 4.3f0.08 4.8 0.10 4.5 5 0.55 2.6+0.05 2.8 3.9+0.10 4.7 kO.10 5.2k0.10 5.5 k0.07 5.6+0.05 Larvac VII VII IX X XI XI1 XI1 Adults XI XI I XI11 IV 7 7 45 16 5 !I 5 77k0.6 77k0.1 78k0.7 - ~ ~ 79 k 0.9 79k0.4 79k1.3 + ~ 5.7 & 0.10 5.9k0.03 5.8k 0.06 - 5.8 k 0.10 5.9 k 0.07 6.0 & 0.10 Average body measurements of two morphological features in developing (and adult) specimens collected at Megiddo and Brosh are given in Tables 5 and 6, These show that females tend to be of greater diameter than males of the same stadium, although numbers of body segments in each sex are quite similar. Tables 5 and 6 also indicate that individuals in some stadia, in both sexes, may be either larvae or adults. (Criteria for determining if millipedes were functional adults included size of gonopods and gonads, and evidence of copulation, the latter occurring mainly in laboratory specimens. Copulation was rarely observed in the field; it occurs toward the end of the oocyte maturation period: May at Megiddo, March-April at Brosh.) Reproduction maturity in both sexes (Fig. 10) at Megiddo usually begins at 8 years of age (i.e. stadium XII), although a small number of males there mature earlier (Table 5). At Brosh, maturity is reached 2 years earlier (Fig. 10) (also in BIOLOGY O F DESER'I' MILLIPEDES 79 Table 6. Morphological measurements ( 2 s.E.) of female Archispirostreptus tumuliporus judaicus from Megiddo ( M ) and Brosh (B) ~ ~ ~~ Larvae VII VII IX ** 33 45 26 23 28 5 X XI XI1 XI1 Adults XI XI1 XlII Iv ** 19 31 16 33 18(4) ~ 33 ( 20) 46(21) 14 - * Number examinrd ** Not observed. Mid-sesment width (mm) ~~~ B M Stadium ~~~~~ Total no. of segments No. of' specimens* ~ 24(9) 46( 12) 7(2) M B M 55k0.3 62k0.2 68k0.2 73k0.2 76k0.2 77k0.2 - 2.8k0.02 3.3k0.04 3.7k0.5 4.4k0.10 5.0k0.14 5.850.15 - 77k0.3 77k0.4 78k0.5 - ~ 68k0.7 75k0.3 78k0.6 78k0.4 78k 1.2 ~ 78k0.6 79k0.7 81 k0 ~ 6.5i0.05 6.6k0.04 6.6k0.06 ~ B ~ - 3.8k0.09 4.7k0.07 5.5f0.15 5.8k0.08 6.3 kO.09 - 6.8k0.07 7.0k0.05 6.9k0.15 for total number or segments stadium XI1 for males) but not in females, which are in stadium XI11 when they reach maturity (Table 6). Only a few stadium XIV millipedes were seen a t Megiddo, indicating a maximal longevity of 1 1 years (Fig. 10). At Brosh more stadia (up to 16) are compressed into a shorter (9 years) life-span. As with other desert millipedes, we know very little about causes of premature death. Flooding, and entrapment on the surface in hot dry weather are possible abiotic factors. Predation by the scorpion Neb0 hierichonticus, which occurs a t both Megiddo and Brosh, was seen in the laboratory (Warburg, unpubl. obs.). Harpagophora nigra: some developmental characteristics Some information on size-class (and probably stadia) distribution of this hapagophorid was obtained from specimens excavated at the base of a Namib desert inselberg (see above) by Crawford & McClain (1983). Most if not all of the millipedes studied were immature, with mid-segment widths ranging from 1.8 to 5.1 mm; a member of the same species collected there 1 year before had a mid-segment width of 10.3 mm. U p to a body width of about 4 mm the number of podous diplosegments (those with legs) continued to increase. Between widths of 4 and 10 mm the number apparently stabilized at about 48; rneanwhile the number of caudal apodous diplosegments dropped to zero (from it previous two to five) in the larger animals. The number of ocelli in the dorsal row of each eye increased progressively (from 5 to 11) from the smallest to the largest of these mi 1li ped es. Six or seven fairly discrete size classes can be inferred from the data of Crawford & McClain (1983). If one assumes that the smallest individuals collected were at least 1 year old, and that after the first year only one moult occurs per year (as in 0. ornatus, but not as in A . t.judaicus), then the potential 80 C. S. CRAWFORD E T AL. life-span of H. nigra may be somewhat less than a decade. We know nothing about its reproductive biology, including the timing of its reproductive activities. HABITAT USE BY ARID-LAND SPIROSTREPTIDA Orthoporus ornatus: the feeding season Most of the obvious foragers in this species appear on the surface at the onset of summer rains (Fig. 1 I ) . Their feeding season seems to average 3-4 months, although its termination is poorly defined since a few stragglers can be observed on relatively warm days in late autumn. The sight of many bleached exoskeletons on volcanic outcrop sites suggests that some of these late-season foragers resist, at their peril, returning below ground at a time when temperatures drop quckly at night. A very different set of problems, namely excessive heat and dryness, must be faced on most days of the feeding season. Not unexpectedly, individuals exposed to such conditions thermoregulate behaviourally. Wooten et al. (1975) demonstrated that heat-related patterns of relocation within and beneath vegetation are similar for populations in very different habitats. Surface activity ceased when air temperatures rose above about 35"C, which is roughly 5°C below the estimated upper lethal limit (Crawford, 1972). Within the acceptable thermal range, large specimens often bask on shrub branches in the midmorning sunlight, a process that may enhance rates of digestion and egg maturation, although this remains to be tested. The relatively great body mass Figure 1 1 . Three Orihoporus ornatus consuming mainly Atriplex leaf litter in July near Albuquerque, New Mexico. Large specimen is an adult, about 12 cm in length. BIOLOGY OF DESERT MILLIPEDES 81 of large individuals insures slow heating and cooling, anld surface-core differences in body temperature of 3-4°C are not uncommon at that time of day (Crawford, unpubl. obs.). While travelling on the ground or in vegetation, and while feeding, individual 0. ornatus give no clear indication that their spatial positioning is being influenced by nearby conspecifics. However, they do show mutual attraction when seeking or using shelter such as rock crevices or mammal burrows. I n these places there exists a strong tendency to aggregate, and numbers of 20-30 in a narrow crevice during the midday hours are not unusiial (Crawford, unpubl. obs.). Foraging during this period results in a measurable increase in biomass. Crawford ( 1976) estimated that feeding-season production, two-thirds of which was new cuticle, in Big Bend National Park was at least 0.85 kg h a - ’ . Rates of biomass increase were significantly higher in the Albuquerque outcrop population. Minimal consumption of annual net primary production was estimated a t 0.24%, a proportion equivalent to the low ends of ranges given for other diplopod species in mesic habitats (Crawford, 1976). Assimilation efficiency a t this time is high ( - 33%) in 0. orrz.atus compared with values recorded for other millipedes (Wooten & Crawford, 1975). This must be due in large part to the high activity of cellulolytic microbes in the gut of the desert millipede (Taylor, 1982a). Feeding in this species is very generalized, and a broad range of digestive enzymes occurs in the gut (Nunez & Crawford, 1976). Nevertheless, choice tests show that ingestion of fungi b y 0. ornatus can be quite selective (Taylor 198213). At moult, when most of the hindgut flora is eliminated, recolonization of these vital symbionts is presumably accomplished by ingestion of soil and/or the exuvium, as well as by recruitment from residual organisms in the midgut-foregut complex (Crawford, Minion & Boyers, 1983). Feeding as it does on the exposed soil surface and in mainly shrubby vegetation, 0. ornatus is potentially vulnerable to desiccation in the summer months. Desiccation is alleviated in that period by the presence of a relatively waterproof cuticle and by taking up water after extrusion of rfectal tissues on moist soil (Crawford, 1972). Water is also ingested with food, which includes succulent leaves, cactus pads, fresh carrion and hygroscopic detritus. Simultaneously, both the proportion of body water in the gut ‘compartment’ and the absolute volume of water in the gut approximately double over values derived from overwintering specimens (Crawford, 1978). It seems that behavioural attributes are crucial to the maintenance of feeding-season water balance in 0. ornatus. Besides coping with potentially deleterious aspects of the physical environment, surface-active 0. ornatus must also contend with a (certain amount of predation, and perhaps with gut parasites. It is not uncommon to see broken sections of these millipedes, as well as individuals with dark ‘scars’ from previous injuries. Lizards, birds (such as shrikes) and rodents (such as Onjchomys spp.) probably account for most of the damage. Larvae of zarhz$pus spp. (Coleoptera: Phengodidae) can be seen predating 0. ornatus in western Texas and southern (but not central) New Mexico (Crawford, unpubl. obs.). Tiemann (1967) has described millipede predation by Xarhippus in California. Wir hin the desert millipede’s hindgut are almost invariably found large numbers of the C . S. CRAWFORD E T AL. a2 thelastomatid nematode, Thelastoma collare (Upton, Crawford & Hoffman, 1983). Whether these are commensals or parasites remains to be determined. Orthoporus ornatus: the dormancy season In searching for dormant members of this species, one learns eventually that the discovery of a single individual almost always guarantees the presence of others coiled within a few centimetres distance. I t is not unusual, in fact, to encounter well over 100 individuals clumped beneath a single rock. Likewise, it is not exceptional to spend hours searching in attractive habitats and find nothing. Overwintering sites in rocky outcrops are indicated by holes made by millipedes as they enter moist soil between rocks. Such entrances are often situated at the bases of large rocks that slope inward as they contact the soil. Careful excavation with a trowel or spoon may produce a coiled specimen within 10 cm of the entrance, although dormant millipedes are usually found a t greater depths. Using continously recording thermistor probes, Crawford (unpubl. obs.) recorded temperatures of such hibernation sites between midDecember 1977 and mid-June 1978. A range of - 1 to 40°C was measured. Sites in soils lacking surface rocks are also revealed by entrance holes. One such opening a t Tornillo Flat led to a packed mass of 73 millipedes roughly 0.3 m below the surface (Crawford, unpubl. obs., September 1974). Nests of social insects house dormant spirostreptoids in Africa (Lawrence, 1966; Gillon & Gillon, 1979). In southern New Mexico and southwestern Texas 0. ornatus often uses nests of the harvester ant, Novmessor cockerelli for shelter during dormancy. (Compared to nests of many sympatric ant species, nests of this relatively carnivorous myrmicine have entrances with diameters suitable for millipede transit.) Data on nest use by 0. ornatus are taken from an unpublished study conducted between January and September 1972, and recorded in Table 7. Eighty-three nests were excavated at the Jornada Experimental Range, Table 7. Distribution of dormant Orthoporus ornatus in nests of the harvester ant Novomessor cockerelli Number of nests 0 1 2 3 4 5 6 7 8 9 10 Observed frequency of millipedes per nest Expected frequency of millipedes per nest* 18 18 12 8 0.004 0.332 1.245 3.129 5.910 8.931 11.230 12.1 18 11.454 9.595 7.256 a 7 5 1 4 0 2 * Derived from the calculated Poisson distribution (STATPAC). - BIOLOGY OF DESERT MILLIPEDES 83 - each to a depth of 1 m (the approximate depth of a hard caliche layer). 1.5 m were sufficient to include all ant galleries Excavation diameters of above the caliche. T h e distribution of 222 millipedes in these nests departed from randomness (Poisson distribution) in a highly significant manner = 78.181; P < 0.001). We conclude from this analysis and from previously cited information that the tendency of 0. ornatus to aggregate when not feeding or walking carries over to its choice of dormancy sites. One can only speculate that the benzoquinone secreted by its defence glands (Eisner et al., 1965) acts as an aggregation pheromone as well as a deterrent against predators. (x' Archispirostreptus tumuliporus judaicus: surface activity anal feeding The seasonal timing and duration of surface activity varies in A. t. judaicus according to habitat location (Fig. 12). At Megiddo, the mesic habitat in this study, millipedes are seen on the ground between mid-Ma.rch and late October/early November (Bercovitz, 1984). Activity in the spring is essentially diurnal and lasts most of the daylight hours; in summer the millipedes become crepuscular and nocturnal. I n the arid habitat of Brosh, A . t. judaicus becomes surface-active earlier (in February) and remains so for somewhat longer (into November at least) with some animals occurring on the surface even in the winter. Otherwise, their die1 patterns of activity, both at Broshl and Dimona (Warburg, unpubl. obs.), are seasonally similar to those of the Megiddo population. Detrital food in all habitats is abundant and therefore should have no limiting effects. At Megiddo, occasional feeding on green leaves of the legume Alhagi and on fallen dates was observed. Green leaves of the borage Podouosma and the shrub Thymelaea are eaten at Brosh and Dimona, respectively. Figure 12. Adult ArchiJpirostreptus tumuliporusjudaicus, 12 cm in length, near Brosh. A large stone ijust rcrnovrd) was being used as shelter. Note snails nearby. 84 C. S. CRAWFORD E T AL. Surface-active A. t. judaicus obviously experience different annual climatic regimes, depending on the habitat. However, in all three of the habitats concerned the active season coincides fairly well with the long, dry summer. As a consequence, populations on the surface are faced with potentially dehydrating conditions for much of the year. Accepting the strong possibility that these populations also have ready access to cool and relatively moist subterranean passages, one must still question whether rehydration and water conservation can regularly balance loss via respiration and cuticular transpiration. This matter was addressed in a comparative study by Crawford et al. (1986), which showed that females from Megiddo are not as resistant to water loss as are Orthoporus ornatus and Harpagophora nigra. (Water loss in A. t. judaicus is very difficult to measure since stressed specimens defecate frequently.) The study also revealed that, on a seasonal basis, total body water in all three populations was lowest in summer. I n the winter, a relatively high proportion was in the gut and haemolymph, the osmolality of which simultaneously decreases. These patterns of seasonal body water and haemolymph osmolality are the seasonal opposites of those in 0. ornatus. Thus, in both species, the wet season is associated with relatively great ingestion of moisture and elevation of body water levels. O n comparing the three populations of A . t. judaicus, Crawford et al. (1986) found that although total body water levels were approximately equal in the winter months, they were lower in summer in the desert populations than in the Megiddo population. The desert millipedes also had higher haemolymph osmolalities in the summer and, unlike Megiddo specimens, responded to moderate dehydration by shifting water from the gut to haemolymph and/or other tissues and cuticle. Hence the Brosh and Dimona millipedes appear to be under a certain amount of desiccation stress during their longer, hotter and drier summers. Further, they seem able to hydrate tissues from the gut reservoir more readily than Megiddo millipedes. From an evolutionary standpoint it may be asked whether desiccation stress has any adverse effect on fitness. Crawford & Warburg (1982) approached this question by recording apparent oosorption in A . t. judaicus exposed to moderate drying (19 days at 76% relative humidity and 20-22°C). Compared to hydrated controls (which, like the experimental specimens, were also starved) there was no significant difference in degree of oosorption. Field controls resorbed oocytes to a significantly lesser degree than either of the above groups. Results of this experiment were clearly equivocal. Gut symbionts are common in A . t.judaicus. At least in the spring, most adults (both sexes) have thelastomatid nematodes in the hindgut, while some also have gregarines in the midgut (Crawford, unpubl. obs.). Gregarines were not observed in the other two species considered in this review. Archispirostreptus tumuliporus judaicus: dormancy As indicated above (see especially Fig. lo), a period of winter hibernation is common to this species. It lasts for a somewhat longer period in the mesic habitat (Megiddo) than in the desert. Physical constraints (crevices, rocky or deep soils) have so far prevented any serious attempts to excavate hibernating specimens in the winter, so we cannot report on the metabolism and water balance of such individuals. BIOLOGY O F DESERT MILLIPEDES 85 Harpagophora nigra: comments on habitat use Limited observations by E. L. McClain (pers. comm.) reveal that H. nigra emerges after relatively heavy rains. Whether emergence occurs a t any time of year following precipitation is not known; one imagines that it might since rainfall is normally scarce and erratic, and since daytime tempera.tures in winter are warm in the Mirabib location. The wet and dry weights of gut contents from six excavated specimens correlated significantly with specimen size (mid-segment width), suggesting that when in dormancy these animals retain a full complement of ingested food and water (Crawford & McClain, 1983). Root hairs and thin strips of plant tissue were among the organic matter within the gut. No nematodes or gregarines were observed in any part of the gut. Harfiagophora nigra appears to have a well-developed capacity to maintain a stable water balance when underground in the winter months, although in this state its ability to resist transcuticular water loss is inferior to that of 0. ornatus (Crawford & McClain, 1983). However, specimens studied were able to lose over 50% of their body water without dying. Since changes in gut water content were significantly greater than changes in tissue and cuticle water when H. nigra was desiccated for 8 days, it appears that the gut of overwintering individuals of this species is an important initial reservoir. DISCUSSION AND CONCLUSIONS T h e three species of Spirostreptida considered here live on separate continents, yet they share a common exposure to subtropical environments having long periods of annual drought. Because lengthy dry seasons in such relatively arid parts of the world are associated with morphological, physiological and behavioural convergence in many organisms (e.g. Hadley, 1972), we anticipated convergence for the spirostreptids as well. Three examples of this phenomenon are now mentioned in the context of the more complete adaptational picture, in which convergence plays an important but not exclusive role. A fairly obvious form of convergence in these species is an enhanced capacity to resist water loss, and therefore to maintain a positive water balance under what surely would be desiccating conditions for most diplopods (Crawford, 1972; Crawford & Warburg, 1982; Crawford & McClain, 1983). Desiccation resistance appears to be most strongly developed in the two sprcies having no mesic-habitat populations. A second convergent trait relates to die1 surface activity, which tends to be bimodal in the hot months and more unimodal or uniform when temperatures are less extreme (Wooten et al., 1955; Bercovitz & Warburg, unpubl. obs.). Finally, there is the convergent use of crevices, nests of social insects, and vertebrate burrows for shelter (Wooten el al., 1975; Crawford, 1978; Crawford & McClain, 1983; Bercovitz & Warburg, unpubl. obs.). This behaviour, which involves aggregation, is also found in other millipedes inhabiting regions with long dry periods (Lawrence, 1966; Gillon & Gillon, 1979). These three traits also characterize other groups of arid-adapted arthropods (e.g. Edney, 1977; Crawford, 198I ) , therefore are broadly ‘convergent’ in the usually accepted sense of the term (Mayr, 1971); Pianka, 1978). However, they 86 C . S. CRAWFORD E T A L . are not all the traits that enable arid-adapted millipedes to dwell in the variety of habitats mentioned earlier in this paper. Convergence, if it operates at the habitat level, tends to be masked in these species by species-specific or even population-specific patterns of life history and habitat use. To illustrate this we turn first to the relationship of seasonal dormancy and foraging in arid-land millipedes. In the two truly desert species, Orthotorus ornatus and Harpagophora nigra, dry season dormancy takes up at least half of the year and spans periods of both cold and heat. While shelter is certainly available in the habitats of these two species, it is neither as obvious nor as extensive as the collapsed limestone caves and multiple limestone rock crevices that typify desert habitats of A. t. judaicus. Prolonged dry-season foraging by that species is accomplished in the immediate vicinity of such refuges, many of which lead to relatively cool and moist subterranean environments. A. t. judaicus is something of a cavernicolous species that uses desert caves. Under these circumstances a long foraging season should pose relatively few risks, whereas for the two essentially desert species the relative paucity of large entrances to shelters, coupled with soil that only becomes soft enough for burrowing when wet, should increase the chance of being trapped on the surface if foraging is a t all extensive during the dry season. Clearly, some life-history patterns in each of these cases conform to topographic constraints. Termination of dormancy in the later stadia of the two well-studied species is followed by surface activity. I n 0. ornatus, appearance on the surface normally does not occur until the arrival of summer rains, several weeks after latedormancy moult in the hibernaculurn. I n A. t . judaicus from Megiddo, moult in the later stadia also appears to take place shortly before surface appearance (which is in early spring and coincides with the end of the wet season). Members of the Brosh population, in contrast, appear to emerge in these stadia prior to the annual moult. Likewise, the timing of emergence from egg pellets is quite different in the two spirostreptid species, and in different populations of A . t. judaicus as well. As with its emergence from the hibernaculum, emergence from the egg pellet by 0. ornutus is rainfall triggered. This is not so for A . t. judaicus, whose Megiddo larvae (stadium 111) emerge from the egg pellet before the end of the winter rains, while Brosh larvae at the same stage emerge 1 month after the rains end. Thus release from subterranean confinement is dependent on rainfall onset in the strictly desert millipede. In the species with less definite desert associations emergence of all stages occurs at or following termination of winter rains. Assuming that use of caves and large crevices as shelter occurred over long stretches of evolutionary time, A . t. judaicus and its immediate ancestors may not have developed life-history patterns that relied on the proximal stimulus of precipitation. However, if the low moisture input of the Negev and Judaean deserts restricts nutritional gains (either via primary production or by limiting access to available detritus), then rainfall may have an ultimate influence on this species. Perhaps this constraint is reflected in the relatively compressed life histories of the Brosh population. In any event the arrival of moisture appears to mean more, in a proximal sense, to life-history patterns in 0. ornatus. We surmise the same is true for other desert species such as H. nigru. Seasonal water balance in these Spirostreptida also relates to patterns of life history and habitat use. It has been recently pointed out by Crawford et al. BIOLOGY O F DESERT MILLIPEDES 87 (1986) that A . t. judaicus retains a higher proportion of its total body water in the gut and haemolymph (as opposed to tissue and cuticle) in the cool wet months than it does in the summer months. The opposite is true for 0. ornatus, which only forages in the summer. Moreover, as mentioned earlier, seasonal patterns of total body water are essentially reversed in the two species: low levels occur in their respective dry seasons, regardless of activity. Also, within a single species, A . t. juduicus, seasonal differences in body water levels and haemolymph osmolalities must be considered in the context of habitat differences. We conclude that the independent evolution of each of these three species has produced patterns of life-history and habitat use that combine a moderate amount of convergence, particularly in desert species and populations, with a great deal of ‘opportunistic’ adaptation to highly variable regaonal and local environments. Key features of these environments (e.g. the timing of seasonal precipitation, and the nature of shelter in specific habitats) appear to have a disproportionate influence on these patterns. Finally, although we have not emphasized the point, the evolutionary history of each species must in each instance constrain the extent to which patterns in a given population can be realized. ACKNOWLEDGEMENTS Sources supporting studies by the authors that led to this review include the International Biological Programme; the National Science Foundation (U.S.A.); the Lady Davis Foundation, the Technion Institute’s Research and Development Funds and its Funds for the Promotion of Research (Israel); the Council for Scientific and Industrial Research, the Transvaal Museum, and the Directorate of Nature Conservation (South Africa); and the University of New Mexico Research Allocations Committee. Many forms of assistance were provided over the years by persons acknowledged in earlier papers. Meteorological data used in the present work were kindly supplied by the Israel Meteorological Service at Bet Dagan and Prof Z. Ketzinel of the Nuclear Research Center at Dimona; by Prof I. V. Bennett, Department of Geography, University of New Mexico; and by Dr M. K. Seely, Desert Ecological Research Unit, Namib Desert Research Station. REFERENCES BERCOVITZ, K., 1984. Factors affecting the reproductive strategy of Archispirostreptus syriacus ( D e Saussure) (Diplopoda, Spirostreptidae). Unpublished D. Sc. Thesis, Haifa: Technion Institute. BERCOVITZ, K. & WARBURG, M. R., 1985. Developmental patterns in two populations of the millipede Archispirostreptus griacus (De Saussure) in Israel. Bijdragen tot de Dierkunde (Amsterdam), 55: 3 7 4 6 . CAMA’IINI, M . (Ed.), 1979. Myriapod Biology. London: Academic Press. CAUSEY, N. B., 1975. Desert millipedes (Spirostreptidae, Spirostreptida) of the southwestern United States and adjacent Mexico. 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