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Reproductive System of Female ScorpionA Partial Review.

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THE ANATOMICAL RECORD 293:1738–1754 (2010)
Reproductive System of Female
Scorpion: A Partial Review†
M.R. WARBURG*
Department of Biology, Technion-Israel Institute of Technology, Haifa, Israel
ABSTRACT
The female scorpion ovariuterus was examined in 10 scorpion species
belonging to five families: Buthidae, Vaejovidae, Scorpionidae, Urodacidae, and Diplocentridae. Two main patterns of development are known in
scorpions: (1) The apoikogenic type with an ovariuterus containing yolkrich eggs housed in follicles. This type is found in many scorpion taxa
(largely buthids). A peculiar case of apoikogenic ovariuterus is a ‘‘beaded’’
ovariuterus where most of the ova’s embryogenesis takes place inside the
ovariuterus rather than on pedicels situated on the external wall of the
ovariuterus as in most buthids. This type is found in a few scorpion species. (2) The katoikogenic type with an ovariuterus where the embryo
develops in a diverticulum composed of four parts: a stalk (pedicel), a
thickened collar, a conical portion containing the ovum, and an appendix
containing the oral feeding apparatus where the embryos’ chelicerae grip
a ‘‘teat’’-like structure, described in four families: Hemiscorpiidae, Scorpionidae, Urodacidae, and Diplocentridae. There are three kinds of diverticulae: small rudimentary finger-like diverticulae, embryonic (ED) large
projections, and postpartum diverticulae (PPD) empty diverticulae, which
are remnants after parturition. The subject is reviewed and its bearing
on reproduction in scorpions are discussed. Anat Rec, 293:1738–1754,
C 2010 Wiley-Liss, Inc.
2010. V
Key words: scorpiones; katoikogenic; apoikogenic; ovariuterus
HISTORICAL REVIEW
Scorpion reproduction has interested zoologists for
more than six centuries. Most of the research on this
subject dealt with the ecological aspects of mating and
parturition. Already Aristotle and later both Gessner (in
the late 16th century) and Swammerdam (1669)
observed parturition and recognized that scorpions are
viviparous and that after parturition the females carry
their young on their back. A comprehensive historical
review of the very early research on scorpions was
recently compiled by Braunwalder and Cameron (2001).
Dissections of scorpions were carried out over three
centuries ago by Redi (1688). More than a century later,
Meckel (1809) provided an illustration of the female
scorpion ovariuteri in his ‘‘Beiträge zur vergleichenden
Anatomie der Skorpionen.’’ After a few years, Treviranus
(1812) work on the arachnids appeared (Ueber den inneren Bau der Arachniden). He was the first to describe
three ovariuterus tubes with three connecting tubes (see
p 12–14 and Figs. 11–13 there). Dufour (1817) provides
illustrations (Figs. 7 and 8 on p 454 there) of the ovariuterus of Buthus occitanus and its egg follicle. In his
C 2010 WILEY-LISS, INC.
V
large monograph, ‘‘Histoire Anatomique et Physiologique
des scorpions,’’ Dufour (1856) discusses the reproductive
system (see p 634–650 there), and provides illustrations
of the ovariuteri of both a buthid and a scorpionid
(Plate 4, Figs. 37 and 46, respectively, there).
Oscar Müller (1818) published his ‘‘Anatomie des
Skorpions,’’ and a decade later Johannes Müller (1828)
discussed the scorpion reproductive system in his anatomical monograph: ‘‘Beiträge zur Anatomie des Scorpions’’ (see p 53–59 there). The latter was the first to
present an illustration of the development in Buthus
(see Figs. 14–20 there). The state of the field was
reviewed by Gervais (1844), who gave a short historical
y
This paper is dedicated in memoriam of Dr. Gershom Levy
(1937–2009); a pioneer in scorpion research in the Middle East.
*Correspondence to: M.R. Warburg, Technion City, Haifa
32000. E-mail: warburg@tx.technion.ac.il
Received 26 February 2010; Accepted 17 June 2010
DOI 10.1002/ar.21219
Published online 4 August 2010 in Wiley Online Library
(wileyonlinelibrary.com).
SCORPION REPRODUCTION
1739
TABLE 1. List of 10 scorpion species in which
the ovariuterus was studied here
1
2
3
4
5
6
7
8
9
10
Fig. 1. Scheme. a: Apoikogenic ovariuterus. L: large oocyte, S:
small oocytes of three generations (1–3), Sc: scar of pedicle left after
last parturition. b: Beaded ovariuterus. L: large oocytes found inside
ovariuterus tube, S: small oocytes located on top of the large ones
and on the tube, Sc: scar. c: Katoikogenic ovariuterus. Rd: rudimentary diverticulae of four generations (1–4), Ed: embryonic diverticulum,
Dd: degenerated, postpartum diverticulae five generations (1–5).
review on reproduction (see p 36 there). Duvernoy (1853,
see the third fragment in that work, p 183–213 in which
he deals with scorpions), provides illustrations of the
female reproductive system in Buthus afer, a scorpionid
(probably Heterometrus or Pandinus), and the buthids
Androctonus occitanus (¼Buthus occitanus?), Scorpius
europaeus (see Planche V there). He was the first to
illustrate two different organizations of the female reproductive system, distinguishing between those found in
Scorpionidae (Buthus afer see Plate V, fig. 1 there), and
the Buthidae (see Fig. 8. Androctonus occitanus, and
Fig. 12. Scorpius europaeus, there). In the first, the egg
remains inside the diverticulum throughout its development, whereas in the buthids, the ova move inside the
lumen of the ovariuteran tube. He too (as did J. Müller
in 1828) noticed the length of the cord (which he named:
‘‘Baguettes’’) passing from the appendix of the follicle to
the mouth of the embryo comparing it with an umbilical
cord. Later, Dufour (1856) studying the ovariuteri of the
buthids, Buthus europaeus (¼Isometrus maculatus?) and
Katoikogenic
Scorpionidae
Scorpio maurus fuscus Ehrenberg, 1829 from the Galil
Mts and from the Golan Heights Israel
Pandinus imperator (Koch, 1841) from Cote d’Ivoire
Diplocentridae
Nebo hierichonticus (Simon, 1872) from the Galil Mts,
Israel
Urodacidae
Urodacus manicatus (Thorell, 1876) from Warumbungle Mts, NSW, Australia
Apoikogenic
Buthidae
Hottentotta judaicus (Simon 1872), from the Galil Mts.
and Mt. Carmel, Israel
Leiurus quinquestriatus (Hemprich and Ehrenberg,
1828), from the Negev Desert, Israel
Mesobuthus nigrocinctus (Ehrenberg, 1828) from the
Golan Heights
Orthochirus scrobiculosus negebensis (Shulov and
Amitai, 1960) from the Negev desert Israel
Compsobuthus werneri judaicus (Birula, 1905) from
Mt. Carmel, Israel
Vaejovidae
Vaejovis spinigerus (Wood, 1863) from Arizona,
USA
Buthus occitanus, mentioned the two kinds of reproductive patterns in scorpions: the oviparous and the viviparous (ovigère et vivipares). He also noticed the different
degrees of development of the ova in the ovarian tubes
(of the ovigères on p 641–642 there).
Laurie (1890, 1896a) gives a brief historical account
on the subject. He was the first to name these two main
types of ovariuteri in scorpions, the same types that
were identified almost 40 years previously by Duvernoy.
The first type: the Apoikogenous (Greek meaning ‘‘away
from home’’ found in the Buthidae, Chactidae, and Vaejovidae), and the second type: the Katoikogenous (Greek
meaning ‘‘at home’’, typical of the Scorpionidae and Diplocentridae). The first system with yolk-rich ova is common to most scorpions, and the second with yolk-poor
ova is found in a few scorpion families.
The female reproductive system is bilaterally symmetrical with a short atrium; one pair of oviducts (birth
canals) bifurcates into medial and lateral branches of
variable numbers of paired transverse anastomoses.
Pawlowsky in 1924, and in a more detailed study in Pavlovskij 1925, distinguished between two main kinds of
ovaries in scorpions based on the number of anastomoses
connecting between the three long ovarian tubes. Thus,
the buthids (i.e., Buthus eupeus (¼ Mesobuthus eupeus),
Parabuthus planicauda) have 10 (five pairs) anastomoses (or ‘‘Die Zehnbögige’’, i.e., connecting ovariuterine
tubes) connecting between the three ovarian tubes. All
remaining scorpion families studied by him: Chactidae,
Bothriuridae, Vaejovidae, and Scorpionidae have eight
(four pairs) anastomoses (Die Achtbögigen). Both the
longitudinal and transverse tubes bear ova.
Thus in Heterometrus fulvipes, the ovariuterus consists of three longitudinal hollow tubes interconnected
by four pairs of transverse anastomoses with six quadrilateral meshes (Subburam and Reddy, 1981).
1740
WARBURG
Fig. 2. Leiurus. A and B: Four generations of small oocytes (3 and
4 labeled) (LM, A: 35; B: 25). C: Three generations of oocytes (2–4)
(SEM, 100). D: Three generations of oocytes (2–4) (LM, 30). E: Section through part of the ovariuterus. Two generations of the smaller
oocytes are visible (W1 and W2). (LM, 150). F: Remnants of postpartum oocytes seen as warts (W1 and W2) they will later become scars
visible only in sections (SEM, 200).
Fig. 3. Vaejovis LM. A: Three oocytes situated inside the ovariuterus tube and some small ones (arrows)
on top of it (40). B: Part of the ovariuterus showing small oocytes (arrows) situated on the surface of the
ovariuterus tube (20). C: Beaded ovariuterus depicting oocytes inside the ovariuterus tube (6).
SCORPION REPRODUCTION
Recently, six distinct types of ovariuteri were identifed
in 55 scorpion species (Volschenk et al., 2008). These differ in the number of cell meshes formed between the
ovarian tubes and the anastomoses. The authors distinguish between 2, 6, 8, and 9 such cell meshes.
Reviews on various aspects of scorpion reproduction
can be found in Millot and Vachon (1949), Williams
(1969), Francke (1982), Polis and Sissom (1990), and
more recently by Farley (1999, 2001), Benton (2001),
Warburg (2001), Volschenk et al. (2008), and in Peretti
(2010).
MATERIALS AND METHODS
In this study, the ovariuteri were examined in 10 scorpion species belonging to five families: Buthidae, Vaejovidae, Urodacidae, Scorpionidae, and Diplocentridae (see
Table 1).
1741
For this study, some of the females were dissected
soon after their collection, and the ovariuteri were
excised and placed into fixatives. For details of light
(LM), electron (TEM), and scanning electron microscopical (SEM) techniques (see previous publications Warburg
and Rosenberg, 1990, 1992a, b, 1993, 1994, 1996; Warburg and Elias 1998; Warburg et al., 1995). Both ooocyte
follicles and diverticulae were counted under a dissecting microscope, and their dimensions were measured. In
buthids, the diameter of the oocytes was measured,
whereas in the scorpionids and diplocentrids diverticular
length was measured, in both cases using a binocular
dissecting microscope (DM) with graticules. Smaller
oocytes and diverticular buds were observed by using
the SEM. In the buthids, the scars left by resorbed pedicles (after parturition) and in scorpionids or diplocentrids the warts remaining on the ovariuterus could be
counted only by using a SEM. They could not be seen
under DM. Two-micrometer thick sections of ovaries
that were embedded in Epon blocks were examined
using LM. All data presented in this study refer to the
number of small oocyte follicles or diverticulae as
counted under a DM. When counted under a SEM these
numbers almost doubled due to better resolution.
STRUCTURE AND FUNCTION
OF OVARIUTERUS
Makioka (personal communication) considers that ‘‘the
ovarian network of scorpions, consisting of ovarian tube
with a number of stalked oocytes, is a prototype of chelicerate ovaries.’’
The Apoikogenous Ovariuterus
Fig. 4. Compsobuthus LM (6) showing ovariuterus containing 12
large oocytes (O) and a few smaller ones (arrows).
A scheme depicting the three different types of ovariuteri is given in Fig. 1. The ovary is embedded in the digestive gland the hepatopancreas, which lies dorsal to it
(Laurie, 1890). Lobes of the hepatopancreas pass
through the meshes of the ovariuterus network. Laurie
distinguished
between
two
main
patterns
of
Fig. 5. Compsobuthus A (SEM -100), B (SEM -50), C (LM -6). Asterisks, arrows indicate maturing
oocytes.
Fig. 6. Urodacus LM (A, C, and D 6; B 12; E 20) E-Embryonic diverticulase; 1 and 2, two generations of postpartum divericulae; Rudimentary diverticulae-3.
Fig. 7. Urodacus LM. Different steps in clearing the ovariuterus while removing the hepatopancreas (H)
A–D (6). Emryonic diverticulae-1, postpartum diverticulae-2.
SCORPION REPRODUCTION
1743
Fig. 8. Nebo LM. Depicting two generations of postpartum diverticulae (PPd-1 and P-Pd-2). There are
no embryonic diverticulae to be seen only various sized rudimentary diverticulae. A (6); B (6); C (12);
D (6).
development: embryo developing in a diverticulum typical of the katoikogenic ovariuterus (Laurie, 1890,
1896b), which he described in Scorpionidae and Diplocentridae, and the apoikogenic ovariuterus found in
Buthidae with egg follicles containing an ovum þ envelop(s) of the ovocyte or ovum. These follicles are attached
by a short pedicle to the uterus tubes (see Fig. 2, Leiurus; Fig. 3, Vaejovis; Figs. 4 and 5, Compsobuthus; Figs.
6 and 7, Urodacus; Figs. 8–11, Nebo; Figs. 12–14,
Scorpio).
Apoikogenic scorpions have a simple ovariuterus without diverticulae; embryonic development takes place
inside follicles on the ovariuterus wall (Farley, 1996). Ova
differentiate from the inner germinal epithelium of the
ovariuterus tubules (Laurie, 1890). Ova of all stadia are
attached to the ovarian tube at any given time. Each
ovum forms a follicle on the surface of the ovariuterine
tubules. Laurie (1896b) described the apoikogenic development with large, yolk-rich eggs inside follicles; embryonic
development takes place in the lumen of the ovariuterus
(typical of the Bothriuridae, Buthidae, Chactidae, and
Vaejovidae). Laurie also described katoikogenic development with small alecithal ova inside diverticulae on the
wall of ovariuterus (Diplocentridae, Scorpionidae).
The first sign of the formation of an ovum is the
increase in size of one of the cells of the inner layer of
the ovarian tube doubled to increase in size. As the apoikogenic egg develops, the pedicle becomes short and its
lumen increases in size (Laurie, 1890).
In most apoikogenic scorpions, oocytes develop in follicles in direct contact with the ovariuterus (Francke,
1982; see also Fig. 2 here).
In the katoikogenic scorpions, ova are situated inside
diverticulae on the external side of the ovariuterus wall
(see Figs. 1 and 2 in Warburg and Rosenberg, 1992a and
Figs. 4a–c in Warburg and Elias, 1998). It appears that
Fig. 9. Nebo LM. Embryonic diverticulae (Ed) containing embryos.
Arrows indicate rudimentary diverticulae. A (15); B (18).
apoikogenic scorpions have ovariuteri designated as
Type B Makioka (1988; see Fig. 10 there).
Measurements of oocyte dimensions were summarized
by Francke (1982, p 29). He found that in Centruroides
vittatus oocyte dimensions ranged between 0.4–0.51 mm
0.49–0.63 mm. The dimensions of oocytes in some
other species are summarized in Table 2. Counts and
measurements of six buthids are given in Fig. 15. In
none of these species was there an indication of any
relationship between either number of oocytes or their
diameter and the female’s mass. Likewise, no such
1744
WARBURG
Fig. 10. Nebo SEM. Three generations (1–3) of Rudimentary (arrows), embryonic, and postpartum
diverticulae (Ed and PPd). A (35); B (50); C (75); D (100).
Fig. 11. Nebo sections LM. Four generations of rudimentary (Rd1-4) and a postpartum diverticulum
(PPd) are noticeable. A (40); B (50).
relationship was forthcoming in a vaejovid (Fig. 16), a
diplocentrid, and a scorpionid (Fig. 17).
Soranzo et al. (2000) studied changes in ultrastructure
during oocyte development in Euscorpius carpathicus.
During previtellogenesis, the oocyte is <100 l. This is
followed by two vitellogenic stages characterized by the
accumulation of yolk. The oocyte becomes ovoid meas-
uring 270–360 l. The corpora-lutea are irregular-shaped
bodies (12 mm diameter) with many nuclei. They are the
collapsed remains of the follicles after the egg passed
out (Laurie, 1890). Remnants of these stems connecting
the oocyte with ovarian tube can be seen (Farley, 1996).
The number of oocytes in the ovariuterus of Tityus
bahiensis and Tityus trivittatus ranged between 200 and
SCORPION REPRODUCTION
1745
Fig. 12. Scorpio LM. Large Embryonic diverticulae (E) and two generations of small rudimentary diverticulae (arrows). A (15); B (6); C (12); D (9).
350 oocytes (Bücherl, 1971). Only 20–35 (10%) of these
are fertilized each year, sometimes twice a year. In Paruroctonus mesaensis (¼Smeringurus mesaensis) many
ova fail to develop (Farley, 1996). The percentage of the
various types of oocytes is given for five buthids in Fig.
18, a diplocentrid and a scorpionid (Fig. 19). Usually
studies on the scorpion ovariuterus are limited to one
season. In some species, this was followed over the
whole year. Seasonal changes in numbers and diameters
of different-sized oocytes (small, large, and degenerated)
are given for Compsobuthus, Hottentotta, and Leiurus
(Fig. 20).
The Beaded Ovariuterus
A peculiar case of apoikogenic scorpions was described
in Scorpiops montanus (Pawlowsky (1924; Fig. F there),
and Pavlovskij (1925; Plate VII Fig. 5, see also Figs. 1,
3, 19 there). Pawlowsky describes sphere-shaped swellings (named by him ‘‘Kugelartigen Anschwellungen’’) in
the ovariuterus and named this kind of ovariuterus:
‘‘Perlenschnurartig’’ (meaning pearl string-like or pearl
necklace-like). A similar ovariuterus containing the ova
inside the tube is illustrated for the buthid Lychas
tricarinatus (Mathew, 1960; Figs. 2 and 3 there).
Normally, in apoikogenous scorpions, the ova increase
in size while situated (inside the follicle) outside the
ovariuterus tube. When embryogenesis starts, the ova
move into the ovariuterus lumen, and can be clearly
identified inside the tube as the embryo enlarges (in
preparation). Both Scorpiops montanus (¼Euscorpiops
montanus), and Scorpiops leptochirus appear to have a
similar such beaded ovariuteri (Plate VII, Figs. 5 and
Fig. 13. Scorpio LM. Embryonic (Ed) and postpartum diverticulae
(PPd) (arrows). A (9); B (9); C (12); D (18).
13, respectively, in Pavlovskij, 1925) as does another
buthid, Tityus serrulatus (Matthiesen, 1970a,b). It was
later illustrated by Mathew (1962; see Figs. A–D there).
1746
WARBURG
Fig. 14. Scorpio SEM. Three generations of Rudimentary (1–3), and postpartum diverticulae (PPd). A
(100); B (75); C (50); D (75); E (100); F (100).
This pattern of development of the ova can be seen also
in the vaejoviid Paruroctonus mesaensis (¼Smeringurus
mesaensis) (Farley, 1996, 1998).
On the other hand, in the beaded ovariuterus, ova do
not seem to develop as they normally would in most
apoikogenous scorpions: inside follicles on top of pedicels
situated outside the ovarian tube. A case of beaded ovariuteri was described in Vaejovis spinigerus (Fig. 3 here,
and Fig. 1 in Warburg and Rosenberg, 1996). According
to illustrations in Volschenk et al. (2008), the following
buthids have beaded ovariuteri: Centruroides gracilis,
Orthochirus scrobiculosus, and Odonturus dentatus (see
Figs. 1 and 2. there).
It is possible that although scorpions generally have
ovariuteri of Makioka’s (1988) Type B, the beaded ovariuterus belongs to Type C (described by Makioka, 1988;
see Fig. 10 there).
Farley (1998; see Figs. 1–6) describes in a sketch (no
micrograph of sections are provided) the early stages of
blastulation when the follicle is still on the exterior wall
of the ovariuterus. The stage of blastula invagination is
depicted in Fig. 5 (on p 192 there). Volschenk et al.
(2008) on p 668 there, wrote that they ‘‘observed regular
follicles in Vaejovis spinigerus, confirming to typical
apoikogenic development.’’ Also in this study, no microcraph is provided. To be certain that this unusual case is
just a phase in the normal apoikogenic development,
convincing histological proof will be needed to demon-
TABLE 2. Oocyte dimensions in some
apoikogenic scorpion species
Species
Buthidae
Hottentotta rugiscutis
Lychas tricarinatus
Centruroides vittatus
Hottentotta judaicus
Leiurus quinquestriatus
Compsobuthus werneri
Orthochirus innesi
Euscorpiidae
Euscorpius italicus
Scorpionidae
Heterometrus fulvipes
Dimension (mm)
Source
130 lm
Sareen and
Monga, 1973
Mathew, 1960
Francke, 1982
0.028–0.054
0.4–0.51 0.49–0.63
0.39–1.06
0.49–1.09
0.26–0.6
0.4–0.7
1.2 0.83
2
This
This
This
This
study
study
study
study
Laurie, 1891
Sareen and
Monga, 1973
strate that in Vaejovis, Paruroctonus, and other apoikogenous scorpions, development in follicles outside the
ovariuterus stops during oogenesis at gastrulation before
reaching the embryonic stage. In other words, the main
development of the embryo that takes place inside the
ovariuterus in these species needs to be demonstrated
by micrographs. Moreover, an attempt should be made
to find an explanation. It appears that the oocytes
SCORPION REPRODUCTION
1747
Fig. 15. Relationship between numbers, and diameter of oocytes and female mass in Compsobuthus.
Hottenttota Leiurus and Orthochirus. In all there was no relationship between the oocyte numbers or diameter and the female’s mass. Note that in Compsobuthusands Orthochirus only a few females had any
degenerated oocytes.
moved into the ovariuterus at a much earlier stage of
oogenesis or embryogenesis. What could be triggering
this? The matter needs careful histological investigation
of female scorpions dissected at intervals during their
gestation period. However, since no histological data
(microscopical sections) are available, a more definite decision on whether the beaded ovariuterus indicates a developmental stage or a different form of ovariuterus, will
have to await conclusive evidence for the former.
There is some histological evidence found in the euscorpiid, Euscorpio italicus that ‘‘unfertilized eggs’’ are situated outside the ovariuteran tube (Laurie 1890, see Plate
IX Fig. 7), and that inside the ovariuterus there are
‘‘embryos’’ (Laurie 1890, see Plate IX, 8) both statements
are not supported by sections. The fact that in most
buthid species, the major part of embryogenesis takes
place inside the follicle situated at the external side of the
ovariuterus’ wall, needs to be explained as well.
1748
WARBURG
The Katoikogenous Ovariuterus
Fig. 16. Relationship between numbers and diameter of Vaejovis
oocytes.
Structure and function of the diverticulum. Numbers and measurements of diverticular dimensions are
given in Fig. 17. Again there was no positive relationship between either numbers or dimensions of diverticulae and the mother’s mass. Likewise, no significant
relationship was found between the ovariuterus mass
and the body mass in 18 Scorpio females (Fig. 18A). Nor
was there a relationship between the ovariuterus mass
and the diverticular numbers (Figs. 18B).
The percentage of different kinds of diverticulae are
given for two katoikogenic species: Scorpio and Nebo
(Fig. 20A,B). The proportion of small diverticulae ranged
between 44.7–46.2%, that of large diverticulae ranged
between 24.1–27.5% and that of postpartum degenerated
diverticulae ranged between 27.8–29.7%.
A scheme depicting the structure of the katoikogenic
ovariuterus is given in Fig. 1 (see also Figs. 8–14 here).
Fig. 17. Numbers and length of Nebo and Scorpio diverticulae. No significant relationship between either number of diverticulae or their length and the female’s mass.
SCORPION REPRODUCTION
1749
Fig. 18. Female (A) and ovariuterus (B) mass as related to ED and
RD numbers in Scorpio. There was no significant relationship between
these diverticulae and either the female’s or the ovariuterus’ mass.
In diplocentrids and scorpionids, there are numerous
diverticulae each bearing small alecithal oocyte. These
are katoikogenous scorpions characterized by having a
pseudoplacental viviparity (Francke, 1982). Müller
(1828) noticed the peculiar elongated appendix (‘‘Fortsatz’’ see p 57 there) and suggested its function in
uptake of nourishments. Duvernoy (1853) called it
‘‘Baguette’’ (p 194 there).
The differentiation of the diverticulum into regions
was described by Laurie (1891) in the katoikogenic Scorpio fulvipes (¼Heterometrus fulvipes). He distinguished
between four distinct regions: a long stalk (pedicle), a
thickened collar, a conical part housing the ovum and an
elongated, and a coiled appendix longer than the rest of
the diverticulum. The latter region contains the oral
feeding apparatus. Likewise Pflugfelder (1930; see Fig.
11 there), describing the diverticulae in Hormurus (¼
Liocheles), distinguished between four parts: the ‘‘Endknöpfchen’’ (the equivalent of the button-shaped structure described by Laurie, 1896a), the appendix
connected by a stem (Stiel) to the distal part housing the
embryo. The latter is the main diverticular cavity especially formed to accommodate the developing embryo:
the Truncus diverticulum. Finally, the appendix that
contains the feeding apparatus of the embryo. The proportions of these parts change with growth and development of the embryo inside the cavity.
Pawlowsky (1924) identified in the diverticulum five
parts: Radix, Ampulla, Truncus, Collum, and Appendix.
Fig. 19. The percentage of different kinds of oocytes in five apoikogenic species. The proportion of small follicles ranged between 42.4–
67.1% that of large follicles ranged between 41.7–49%, and that of
postpartum, degenerated oocytes ranged between 7.3–12.2%.
Mathew (1948) in his study on Palamnaeus scaber distinguished between the end piece, handle, swollen middle region and the ‘teat’. In later studies on the same
species (Heterometrus scaber), Mathew (1959) suggests
that the truncus diverticulum encloses the chamber
1750
WARBURG
TABLE 3. The different parts composing the
katoikogenic diverticulum in Scorpions
Species
Family
Heterometrus
fulvipes
Scorpionidae
Heterometrus
fulvipes
Heterometrus
scaber
Scorpionidae
Parts
Long stalk
Thickened
collar
Conical
portion
Long
appendix
Radix
Source
Laurie,
1890
Pawlowsky,
1924
Ampula
Truncus
Collum
Appendix
Heterometrus
Scorpionidae End piece
Mathew,
scaber
Handle
1948
Swollen
middle
region
Teat
Liocheles
Hemiscorpiidae Radix,
Pawlowsky,
australasiae
Ampula
1924
Truncus
Collum
Appendix
Liocheles
Hemiscorpiidae Endknöpfchen Pflugfelder,
australasiae
Appendix
1930
Stiel
Diverticle
Fig. 20. The percentage of different kinds of diverticulae in two
katoikogenic species: Scorpio (A) and Nebo (B). The proportion of
small diverticulae ranged between 44.7–46.2% that of large diverticulae ranged between 24.1–27.5% and that of postpartum degenerated
diverticulae ranged between 27.8–29.7%.
specially formed for the accommodation of the embryo.
When the diverticulum is 3.5 mm the embryo is a gastrula the appendix is 7 mm long (Mathew, 1959).
Our present knowledge on this subject is summarized
in Table 3, and the proportions between the appendix
and the rest of the diverticulum are shown in Scorpio
(Figs. 22–25). Thus, the changes in diverticular length
during embryogenesis are seen in Figure 22. The proportions between the diverticular appendix length are
shown for 16 Scorpio females in Figure 23. Finally, the
percentage average length of each of the four diverticular components and the range are given for Scorpio
(Fig. 24). The largest variation in both percentage and
range of length is seen in the Radix followed by the appendix. The smallest is noted in the cavity.
In another katoikogenic scorpion, Urodacus novae-hollandiae, Laurie (1896) described a well marked, ‘‘bunshaped’’ thickened region at the top of the appendix.
Similar enlargements of the appendix’s tip were
described also in both Nebo hierichonticus (Warburg and
Rosenberg, 1992a; Fig. 2. there also Fig. 10 here), and
Urodacus manicatus (Warburg and Rosenberg, 1994;
Figs. 1 and 6, there also Figs. 6 and 7 here). In immature females, the ovarian tube is very slender and does
not possess diverticulae (Subburam and Reddy, 1981,
1989).
Polis and Sissom reviewing the subject in 1990, distinguished between four parts of the diverticulum: a stalk
(pedicel), a thickened collar, a conical portion containing
the ovum, and an appendix containing the oral feeding
apparatus, where the embryo’s chelicerae grip the teatlike structure of the appendix.
Diverticular differentiation. Duvernoy (1853)
provided an illustration showing the different kinds of
diverticulae (a–f in Fig. 7b in Plate V there). Pflugfelder
(1930) distinguished between three kinds of diverticulae:
those containing embryos, the degenerated diverticulae,
and the young diverticulae. Rosin and Shulov (1963)
studying Nebo hierichonticus, recognized two sizes of
small spherical diverticulae, developed diverticulae and
degenerated diverticulae of two sizes (see Fig. 4. there).
Smith (1966) named the three kinds of diverticulae he
found in Urodacus abruptus: small rudimentary (RD)
finger-like projections, embryonic (ED) large projections
with knob-like structures containing the developing
embryo at their tip, and postpartum diverticulae (PPD)
that are small, infolded remnants left of the EDs in the
wake of parturition. Probst (1972) studying Isometrus
maculatus, distinguished in the ovariuterus between
these same three types of follicles: RD before an embryo
is formed, ‘‘embryonic’’ and ‘‘postpartum’’ (¼corpus
luteum), degenerated follicles, the latter being yellow.
Figure 1 depicts in a scheme these three types of
diverticulae: RD, embryonic and degenerated, and PPD.
After birth, the empty diverticulum shrinks. Smith
(1990) suggested that the sum of the diverticulae is a
measure of lifetime fecundity.
SCORPION REPRODUCTION
1751
Fig. 21. Seasonal changes in numbers and diameter of Compsobuthus, Hottenttota, and Leiurus oocytes. In Compsobuthus, the number
of small and large oocytes increased from winter to spring. Most
degenerated oocytes were observed during autumn. The diameter of
the large oocytes peaked in autumn. In Hottentotta, the number of
large oocytes decreased from winter to autumn. In Leiurus, the number of large oocytes decreased from winter to summer increasing
greatly during autumn. The diameter of the large oocytes showed an
opposite pattern increasing significantly from winter to summer dropping significantly toward autumn.
The degenerating PPD. In both scorpionid and diplocentrid ovaries, the follicles shrink after parturition
following the collapse of the extended diverticulae due to
the embryos moving inside the ovariuterus; they degenerate into irregular-shaped, folded, brown bodies in the
lumen containing still remnants of substance (Pavlovskij, 1925). Degenerating remnants of these PPD can be
seen in the ovariuteri of katoikogenic scorpions for a
long period of time (Pfugfelder, 1930). Even after their
disappearance they can be identified until the follicle
turns into a wart-like structure.
In Heterometrus scaber, the empty diverticulae contract rapidly, becomes flabby and degenerate. They
remain attached to the ovarian tubes but will never
again serve for developing a new batch of embryos. Vestiges of earlier series in various stages of breakdown are
noticeable (see Fig. 10 in Mathew, 1959)
Shorthouse (1971) and Shorthouse and Marples (1982)
studying Urodacus yaschenkoi found that the number of
PPDs ranged from 8 to 15. The average number in brood
was 11.75. They noticed that in two Urodacus yaschenkoi females, the number of PPDs was doubled, composed
of two generations indicating remnants of more than one
(probably two) parturitions.
Makioka (1992a,b) found in Liocheles australasiae that
the number of empty diverticulae present between pregnancies, corresponds to the number of broods. Thus, after
a second parturition, females had two sizes of empty
1752
WARBURG
Fig. 22. The change in average length of diverticulae during four
stages of embryogenesis from the onset (1) to parturition (4). The radix
greatly increases toward parturition.
Fig. 24. Average percentage of length (A), and average range in
length (B) of the four diverticular components as measured in 16 Scorpio females. The longest component of the diverticulum is the radix,
followed by the appendix.
Fig. 23. Average (total) diverticular length in 16 Scorpio females.
The length of the diverticulae varies greatly among the different
females.
diverticulae. This was confirmed by Yamazaki and
Makioka (2001), who showed that the number of empty
diverticulae roughly equals the number of neonates.
Mahsberg and Warburg (2000) studying laboratory
raised Pandinus imperator found that virgin females had
no embryonic EDs or PPDs, whereas the mother did not
have EDs but had the same number of PPDs as the number of juveniles born in the laboratory 2 years earlier. The
relationships between large, small, and degenerated
diverticulae are shown in a scorpionid and a diplocentrid
(Figs. 18, 19), and their percentages in the ovariuteri are
shown in shown in Figures 19 and 20.
In a Nebo female (weighing 5.74 g) that gave birth to
25 juveniles and was dissected 3 months later, four different kinds of degenerated diverticulae were distinguished by their different coloration and length (Fig.
Fig. 25. Number and length of Nebo diverticulae 3 months after
parturition. No large diverticulae were seen. Two generations of small
diverticulae were observed. Although their numbers was almost equal
they differed in length. There were four generations of degenerated
diverticulae. The number of the fourth generations (D-4) was significantly higher than the others. The reason could be that the rate of
resorption drops, and thus, D-4 includes perhaps two or more
generations.
25). The largest type was white and was 5.5 mm long
(the appendix 3 mm). These diverticulae apparently harbored the most recent embryo generation. The second
type, yellowish in color, was 4.5 mm long (appendix, 3
mm). These diverticulae contained resorbed embryos.
The third kind of degenerated diverticulae was light
brown in color and shorter (3.5 mm and a shorter
appendix).
1753
SCORPION REPRODUCTION
Finally, a fourth kind of degenerated diverticulum was
dark brown and half the size of the third kind. These
two latter types of diverticulae are most likely remnants
of previous parturitions that took place in previous
years. (These are not necessarily subsequent years since
Nebo females do not necessarily breed on consecutive
years). Altogether, the ovariuterus of that female contained 25 diverticulae of the first kind, 11 of the second
kind, 23 of the third kind, and 35 of the fourth kind.
The high number of third and fourth kinds of PPDs may
indicate that they are remnants of a larger number of
parturitions.
ACKNOWLEDGMENTS
The author is indebted to many persons for their help
in his scorpion research throughout the many years: Dr.
Marlow Anderson for his kind hospitality and help in
my research on the Chihuahuan Desert fauna in the
late 1950s to Samuel Geiser and Herbert Stahnke, for
their kind help with scorpions from the Sonoran Desert
in the late 1950s; Neil Hadley, Victor Fet, and Stanley
Williams for their help in his research in later years.
Thanks are due to both Drs. Adam Locket and Graeme
Smith for their help and collaboration on scorpion
research in South Australia and Western Australia,
respectively. Finally, the author wishes to thank Dr. Gershom Levy, Mr. Avinoam Luria, and Mr. Pinhas Amitai,
and his son Ittai Warburg of the Hebrew University, Jerusalem for helping in various aspects of his scorpion
research in Israel. Over the many years of his research
on scorpions several colleagues helped by advice or literature coverage. Among them are Drs. Chris Brown,
Roger Farley, Oscar Francke, F.R. Matthiesen, Alfredo
Peretti, Lorenco Perendini, Gary Polis, Dave Sissom,
Dave Shorthouse, Roland Stockmann, and Marco Vannini. For all the help they rendered he is most grateful.
Likewise, he is grateful to Prof. John Cloudsley-Thompson for providing an outlet to publish some of his earlier
papers on scorpion physiological-ecology, to Dr. Gary
Polis for inviting him to write a chapter in a book he
was editing, and to Drs. Victor Fet and Phil Brownell
who asked him to participate in the book in memory of
Gary. Finally, the author wishes to thank Dr. Dieter
Mahsberg for enabling our collaboration on studying
Pandinus imperator raised in his laboratory. During this
long-term study, the author was assisted by several students: (alas, too many to be mentioned by name) who
helped in maintaining the many live scorpions each of
which was kept individually and for maintaining the
auxiliary mealworm culture over 27 years. Skillful technical assistance in my physiological studies was provided
by Mrs. Shoshi Goldenberg, in my ecological studies by
Dr. Dina Rankevitch, and in microscopy (LM, SEM) by
Mrs. Mira Rosenberg my collaborator in this scorpion
research for more than 10 years. Two of his students
who studied scorpions, A. Ben-Horin and Ms. Rivka
Elias, helped in obtaining valuable scientific information. Several projects on scorpion life history were conducted in his laboratory over the years by Horacio Bach,
George Kasabrah, Gamal Abu-Salah, Meital Cohen,
Yoram Ronen, Murad Hayat, Wasim Daher, Idit Lehrer,
Rafi Feinsud, Yael Schwartz, Jakob Slutki, and Salim
Halabi, all of whom contributed to their knowledge.
Finally, the author is grateful to the late Prof. Aharon
Shulov, whom, as a young lad in the early 1940s, the
author helped collect scorpions on the slopes of Mt. Carmel, and about 10 years later, as an undergraduate student at the Hebrew University, he invited the author to
be his teaching assistant in the Entomology laboratory.
During that period, his laboratory was very active in
scorpion research.
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