Download Regional environments, lifehistory patterns, and

<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 Published and unpublished studies are used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.
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CONTENTS
Introduction . .
. . . . . . . . . . .
Regional environments of arid-land Spirostreptida . . . .
Regional environments of Orthoporus ornatus . . . . .
Regional environments of Archispirostreptus tumuliporousjudaicus
Regional environments of Harpagophora nigra
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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.
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Archispirostreptus tumuliporus judaicus: surface activity and feeding .
Archispirostreptus tumuliporusJudaicus: dormancy . , . , .
Harpagophora nigra: comments on habitat use . . ,
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Discussion and conclusions . . . . . . . . . . .
Acknowledgements
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References. . . . . . . . . . . . . . .
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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
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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.
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