<oological Journal of the Linnean So&& ( 1991) , 103: 2 1-60. With 13 figures
Marine insects: genital morphology, phylogeny
and evolution of sea skaters, genus HuZobutes
(Hemiptera:Gerridae)
N. MBLLER ANDERSEN
zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100
Copenhagen
Received J u h 1990, accepted for publication November 1990
Five species of sea skaters, genus Halobates Eschscholtz, are the only insects to have successfully
colonized the open ocean. In addition, 36 species are found in sheltered coastal waten throughout
tropical Indo-Pacific. The taxonomy of the genus is relatively well known, but reliable hypotheses
about phylogenetic relationships are required if the biogeography and evolution of sea skaters is to
he discussed in a meaningful way. This work presents the results of a study of new characters from
the genital segments, especially those of the male phallus and the female gynatrial complex, and a
reinterpretation for several other characters. In total 64 characters were scored for 26 species of
Halobates, two species of Asclepios and one species of Melrocoris. With Asclepios and Metrocoris species as
outgroups, the character state sets were analysed cladistically using the computer program Hennig86.
After critical evaluations of both characters and clades, a phylogeny for Halobates is presented and its
taxonomic implications are discussed. A number of monophyletic species groups are delimited. One
genus-level synonymy and three species-level synonymies are suggested. The evolution of Halobates is
discussed in the light of the reconstructed phylogeny and present knowledge of the ecology and
behaviour of sea skaters. A hypothesis of ecological evolution in halobatine water striders is proposed
and tested.
KEY WORDS:-Halobates - sea skaten - Hemiptera - genital morphology - cladistics ecology evolution.
~
CONTENTS
. . . . . .
Introduction .
Materials and methods
. . . .
Genital morphology .
. . . .
Male genital segments.
. . .
Phallus . . . . . . .
Female genital segments .
. .
Gynatrial complex
. . . .
Cladistic analysis . . . . . .
Characters .
. . . . .
Hennig86 analysis
. . , .
Evaluation of characters and clades
Discussion . . . . . . . .
Phylogeny and taxonomy .
. .
Evolution .
. . . . . .
Acknowledgements
. . . . .
References
. . . . . . .
Appendix: annotated list of characters .
0024-4082/91/090021+40 $03.00/0
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0 1991 The Linnean Society of London
22
N. M. ANDERSEN
INTRODUCTION
The evolutionary success of insects on land is unparalleled among the
metazoans. Although many insects occur in marine habitats (Cheng, 1976), the
only oceanic habitat colonized by insects is the sea-air interface. Five species of
sea skaters or ocean striders, genus Hdobates, are widespread in tropical oceans
and spend their entire lives on the sea surface. There are an additional 36
Halobates species in sheltered coastal waters throughout the tropical Indo-Pacific
(Andersen & Polhemus, 1976; Cheng, 1985).
After being largely ignored by biologists for decades, sea skaters have recently
become much better known and their behaviour, biology, and biochemistry have
been widely studied. Chiefly responsible for the revival of interest is Dr Lanna
Cheng of the Scripps Institution of Oceanography, La Jolla. Through numerous
scientific papers and reviews (e.g. Cheng, 1973b, 1974, 1985, 1989a), Dr Cheng
and her co-workers have greatly increased our knowledge about the life history,
ecology, distribution, behaviour, and special adaptations of these unique insects.
In addition, the near-shore species of Halobates have been subject of a number of
excellent behavioural and ecological studies (Birch, Cheng & Treherne, 1979;
Foster & Treherne, 1980, 1982, 1986; Treherne & Foster, 1980, 1981).
The most complete taxonomic treatment of Halobates is by Herring (1961),
who redescribed all previously known species, synonymized several names and
described 14 new species. He provided a key to 38 species, mapped their known
distribution, and briefly discussed their phylogeny. Since Herring’s work, eight
new species have been described (Herring, 1964; Miyamoto, 1967; Linnavuori,
1971; Polhemus, 1982; Polhemus & Cheng, 1982; Schmidt & Muller, 1973;
Malipatil, 1988).
Several authors (Herring, 1961;Jaczewski, 1972; Andersen & Polhemus, 1976;
Calabrese, 1980; Andersen, 1982; Newman & Cheng, 1983; Cheng, 1985,
1989a, b) have speculated about the origin and evolution of sea skaters, in
particular the open-ocean species. A meaningful discussion of such problems
requires reliable phylogenetic hypotheses of relationships between species and
between monophyletic species groups. The main objective of the present work is
to provide such hypotheses based upon the study of new characters (particularly
genital characters), re-evaluations of previously used characters, and more
precise analyses of phylogeny. Finally, the evolution of Halobates is discussed in
the light of the reconstructed phylogeny and new biological information.
MATERIAL AND METHODS
Most specimens used are deposited in the collections of the Zoological
Museum, University of Copenhagen, which contain representative material of
almost all known species of Halobates and Asclepios. A few species have been
studied during visits to other museums and collections, especially the J. T.
Polhemus collection, Englewood, Colorado.
New characters of phylogenetic significance were discovered by examining the
male and female terminalia. The last 2-3 abdominal segments and attached
genital segments were removed from the specimens and macerated in hot
potassium hydroxide (10%) for about 10 minutes. The abdominal segments
PHYLOGENY OF HALOBA TES
23
were then placed in a few drops of lactic acid (50% aqueous solution) in a small
dish and dissected. In order to reveal the details of the gynatrial complex, the
female terminalia were treated with Chlorazol Black E which dyes otherwise
transparent structures.
The male genitalia were dissected in the following species: Asclepios annandalei
Distant, Halobates alluaudi Bergroth, bryani Herring, darwini Herring, esakii
Miyamoto, Jijensis Herring, Javiventris Eschscholtz, formidabilis (Distant), galatea
Herring, germanus White, hayanus White, maculatus Schadow, mariannarum Esaki,
micans Eschscholtz, mjobergi Hale, panope Herring, peronis Herring, poseidon
Herring, princeps White, regalis White, robustus Barber, sericeus Eschscholtz, sexualis
Distant, sobrinus White, splendens Witlaczil, whiteleggei Skuse and zephyrus Herring.
The female genitalia were dissected in: Asclepios annandalei, Halobates darwini,
hiensis, javiventris, germanus, hayanus, maculatus, micans, mjobergi, poseidon, robustus,
sericeus, sobrinus and splendens.
Most examinations were performed using a LEITZ stereo microscope with
magnifications of 100-150 x . The light source was a VOLPI fibreglass lamp.
Some structural details required examination in a Reichert ZETOPAN research
microscope with interference contrast equipment (after Nomarski).
The cladistic analysis was performed using the program Hennig86 (by J. S.
Farris, New York), version 1.5. It provides facilities for calculating most
parsimonious trees from a character state matrix, either exactly or by effective
approximation methods. In terms of efficiency and speed, it is the most powerful
program for cladistic analysis currently available (Platnick, 1989; Fitzhugh,
1989). The Hennig86 analyses were performed on an Olivetti M300
microcomputer (80386SX microprocessor, 16 MHz clock-frequency) supplied
by the Danish Natural Science Research Council.
Abbreviations used in text figures: ac, accessory sclerites of vesica; ba, basal
apparatus of phallus; ap, ventral apodeme of female abdomen; bs, basal sclerite
of vesica; ca, fecundation canal of gynatrial complex; co, conjunctivum of
endosoma; ds, dorsal sclerite of vesica; fi, filiform process of second gonapophysis;
gc, genital chamber; gol, first gonapophysis; g02, second gonapophysis; gs,
gynatrial sac; gxl, first gonocoxa; lsl, ls2, lateral sclerites of vesica; ml, median
lobe of second gonapophysis; ov, oviduct; pa, paramere; ph, phallotheca; pg,
pygophore or segment 9 of male; pr, proctiger or segment 10+ 11; pu,
fecundation pump of gynatrial complex; ral , ra2, first and second ramus; ~ 5 5 ~ 8 ,
abdominal segments 5-8; sm, spermatheca; sp, spiracular process of segment 8;
sp8, spiracle of segment 8; st, styliform process; su, subanal plate; t9, tergum 9;
va, vermiform appendix of gynatrial sac; ve, vesica; vs, ventral sclerite of vesica;
x, entrance to fertilization chamber.
GENITAL MORPHOLOGY
Characters of the terminal segments of the male abdomen have been widely
used for taxonomic purposes (Herring, 1961). The present study has revealed
additional characters of both taxonomic and phylogenetic importance, especially
in the male phallus and female ovipositor and gynatrial complex.
N. M. ANDERSEN
24
Male genital segments
Pregenital abdomen
The male abdomen of Halobates is relatively short. Most of the pregenital
abdominal segments are reduced in length, but the genital segments are
prolonged and very conspicuous. The basal three mediotergites are fused with
each other and with the thoracic notum. Intersegmental sutures are usually only
distinct laterally. The fourth to seventh mediotergites are distinctly separated
from each other through broad, flexible, intersegmental membranes. The second
and third laterotergites are completely coherent except in H. mjobergi, while the
fifth to seventh laterotergites are reduced or only present as small sclerites. The
second to fifth abdominal sterna are very short, and the seventh sternum is large
and quadrangular (Fig. 1A, s7).
Genital segments
The male genital segments of Halobates are very prominent (Fig. 1A). The
eighth abdominal segment is cylindrical, usually as wide as long (Fig. lB, s8).
The dorsal hind margin is roundly produced in most species. Each of the
spiracles of the eighth segment is typically placed upon a spiracular process
(Fig. IB, sp) which may be rounded, tuberculate, or fingerlike. The ventral hind
margin of the segment is concave, with a pair of slender styliform processes
(Fig. lB, C , st). These processes vary in relative length, degree of asymmetry,
orientation, shape of apices, etc, as illustrated by Herring (1961). Typically,
I
S"1'
D
A
.
Figure 1. Halobates mjobergi Hale, male genital segments. A, Abdominal end, ventral view; B,
segment 8, ventral view, showing spiracular (sp) and styliform processes (st); C, segment 8, lateral
view; D, pygophore (pg) and proctiger (pr), dorsal view. All scale bars = 0.1 mm. Abbreviations:
see text.
PHYLOGENY OF HALOBA7ES
25
each styliform process bears scattered, suberect hairs and densely set, dark
denticles towards its apex.
The pygophore (segment 9) is much more uniform in structure and is subovate
in ventral outline in most species. I t is boat-shaped because its tergal part
(F’ig.ID, t9) is reduced to a narrow bridge proximally. The phallic organ (see
below) is inside the pygophore when not distended (Fig. 3A). I n many gerrids,
the lateral edges of the pygophore carry a pair of prominent parameres. These are
absent in all Halobates species except H . mjobergi (Fig. 3B, pa).
Theproctiger (segment 10 11) lies on top of the pygophore (Figs lD, 3A, pr).
It is plate-shaped, usually pentagonate in outline, with its lateral margins more
or less produced in most species. T h e shape of the proctiger is diagnostic in many
species of Halobates (Herring, 1961) . A semicircular subanal plate (Figs 1 D, 3A, su)
is inserted ventrally near the hind margin of the proctiger.
While the genital segments of H . mjobergi (Fig. 1) appear to be strictly
symmetrical, various degrees of asymmetry are observed in other Halobates
species (excellently illustrated by Herring, 1961). The highest degree of
asymmetry is found, e.g. in H . Javiventris, micans, splendens, mariannarum and
fiiensis. In the last species, together with H . salotae and katherinae, the fifth to
seventh abdominal segments are tubular and prolonged, and the genital
segments are rotated 90% in relation to the progenital abdomen.
Compared with Halobates, species of Asclepios are characterized by simpler
genital segments. The eighth segment is longer than wide (Fig. 2A, s8), which is
the typical state in gerrid males. The spiracles of segment 8 (Fig. ZA, sp8) are
not on spiracular processes. Although the ventral hind margin of the segment
carries a pair of styliform processes (Fig. 2A, B, st), these are relatively short and
robust with numerous denticles on their dorsal surface. The pygophore is similar
in structure to that of Halobates, including its lack of parameres (despite the
statement to the contrary by Matsuda, 1960: 299). T h e proctiger (Fig. 2C, pr) is
broadly ovate in outline. Overall, it seems that Asclepios species have genital
structures intermediate between those of Halobates and most freshwater species of
Halobatinae.
+
.
B
A
Figure 2. Asclepios annandalei Distant, male genital segments. A, Segment 8, ventral view, showing
spiracle (sp8) and styliform processes (st); B, segment 8, lateral view; C, pygophore (pg) and
proctiger (pr), dorsal view. All scale bars = 0.1 mm. Abbreviations: see text.
26
N. M. ANDERSEN
Function
The functional significance of the complex male terminalia of Halobates is
poorly understood. In the material examined, pairs preserved in copula are rare.
This probably indicates that the genital contact between the two sexes is brief (as
observed in H.jjfijiensis by Foster & Treherne, 1986) or not persistent enough to
endure when the specimens are killed and preserved. However, in H. robustus
(Foster & Treherne, 1982), the male stays mounted on the female for many
hours. This may represent prolonged mate-guarding without genital contact, as
frequently observed in other water striders (Andersen, 1982). However, in
H. maculutus at least, my observations suggest that the smaller male is more
firmly attached to the larger female than is characteristic of other gerrids. I have
examined pairs of this species where the first gonocoxa of the female is ‘pinched’
between the right styliform process and the pygophore proctiger of the male in
the absence of phallic contact. Thus, I hypothesize that the distinctive styliform
processes of male Halobates have evolved in the context of mate guarding.
+
Phallus
Basal structures
The type of insertion and basic structure of the male phallus of Halobates is
illustrated in Fig. 3. The phallus is attached to the boat-shaped pygophore
(segment 9) by means of a basal, articulatory apparatus (Fig. 3A, B, ba) which is a
simple, U-shaped sclerite. Theparameres (Fig. 3B, pa) are directly attached to the
articulatory apparatus, on each side of the pygophore.
The phallus is composed of two parts: a proximal phallotheca (Fig. 3B, ph) and
a distal endosoma. The latter is again divided into a membranous conjunctivum
(Fig. 3C, co) and a vesica (ve), which has an armature of sclerotized pieces. The
ejaculatory duct enters the phallus through the basal apparatus and continues as
a seminal duct within the phallotheca and endosoma where it opens terminally
on the ventral lobe of the vesica.
f
ve
B
Figure 3. Halobates mjobergi Hale, male genital segments (slightly schematized). A, Pygophore (pg),
proctiger (pr) and phallus (ph) lying upside down within pygophore, oblique lateral view; B, basal
apparatus (ba) with parameres (pa) and phallus removed from pygophore; C, vesica (ve) removed
from phallotheca and everted from conjunctivum (co). Scale bar = 0.1 mrn. Abbreviations: see text.
PHYLOGENY OF HALOBA 7 E S
27
In Asclepios and Halobates the phallotheca is connected to the basal apparatus
by a relatively short and broad, median cord. The phallotheca is distinctly
sclerotized ventrally and laterally but membranous dorsally. The lateral parts of
the phallotheca are often separated from the ventral part by less sclerotized,
longitudinal areas.
The phallic organ is distended by haemolymphic pressure and the same effect
can be achieved by manual pressure on the abdomen of freshly preserved or live
males. In the deflated state, the vesica is inverted through the conjunctivum and
lies inside the phallotheca (Fig. 3B, ph). Through the spring-like action of the
connecting cord between the phallotheca and the basal apparatus, the phallus is
retracted and placed upside down within the pygophore (Fig. 3A, ph).
Vesical armature
The vesica has a complex armature of sclerotized pieces. In order to examine
the vesical armature, the phallus first has to be removed from the pygophore,
preferably still being attached to the basal apparatus (Fig. 3B). The endosoma is
then pushed or pulled out of the phallotheca (Fig. 3C) by means of a fine needle.
It is important to observe the orientation of the vesica in order to identify the
various sclerotized pieces properly: since the phallus is placed upside down
within the pygophore (Fig. 3A), the dorsal side of the vesica is the one facing the
membranous part of the phallotheca.
The basic structure of the halobatine vesica is probably close to that found in
Halobates mjobergi (Fig. 4B). The most conspicuous structure is an axial, heavily
sclerotized rodlike sclerite. It occupies a dorsal and distal position and is termed
the dorsal sclerite (Fig. 4B, ds). Its apical part is recurved, describing a semicircle.
The apex of the recurved part is widened and furcate. The dorsal sclerite is
slightly furcate proximally and closely associated with the less sclerotized ventral
sclerite (Fig. 4B, vs). This sclerite is very long, proximally and ventrally bandshaped, distinctly tapering to an almost thread-like distal part. There are two
pairs of lateral sclerites. The sclerites of the first or ventral pair (Fig. 4B, lsl) are
relatively thick, especially basally. The sclerites of the second or dorsal pair
(Fig. 4B, ls2) are long and slender, proximally converging and almost meeting
each other above the dorsal sclerite.
In addition to this armature of distinctly separated sclerites, the vesica usually
has more or less diffuse sclerotized areas or bands in the cover surrounding the
dorsal, lateral and apical parts of the vesica. Some of the ‘sclerotized pieces’
illustrated by China (1957: fig. 3e, ps2) are of this nature.
The vesical armature of H . mjobergi appears to be strictly symmetrical. This
state is also found in species of Asclepios (Fig. 4A) and is most probably the
primitive state within the Halobatini (as well as in most other Gerridae). In all
other species of Halobates examined, however, the vesical armature is more or less
asymmetrically developed. This is most distinctly observed in the shape of the
dorsal sclerite (Figs 4D, E, 5A-E). The distal, recurved part is usually twisted in
relation to the dorsal part. Its apex may be more or less distinctly enlarged as in
H. mjobergi (Fig. 4B), H. micans (Fig. 5A), poseidon (Fig. 6A), and robustus
(Fig. 6B), or reduced as in regalis (Fig. 5C), whiteleggei (Fig. 5D) and darwini
(Fig. 5E). Paired, accessory sclerites are found near the apex of the dorsal sclerite
in some species (Figs 5A, 6B, ac).
N. M. ANDERSEN
I
vs
__ _-_.
,
I
I
I+
I+
5
I
-
A
B
--..
ISl
.
c,
I
D
.
t
Figure 4. Vesical armature of male phallus; for each species shown in dorsal (top) and lateral view
(bottom);shading of homologoussclerites conventionalized:dorsal sclerite (ds) shown black, ventral
sclerite (vs) stippled, and lateral sclerites (lsl'and ls2) without shading. A, Ascfepios anmndafei
Distant; outline of vesica (ve) indicated; B, Halobates mjobngi Hale; C, H. maculatw Schadow; D,
H. hayanus White; E, H. g m n u s White. All scale bars = 0.1 mm. Abbreviations: see text.
The dorsal sclerite has a very characteristic, elongate or diamond-shaped
'hole' in species like H. muculatus (Fig. 4 C ) , hayanus (Fig. 4 D ) , germanus (Fig. 4 E ) ,
micuns (Fig. 5 A ) , Javiventris (Fig. 5 B ) , regalis (Fig. 5 C ) , whiteleggei (Fig. 5 D ) ,
durwini (Fig. 5 E ) and others. In the same species, the ventral sclerite is
completely fused with the base of the dorsal sclerite. The ventral sclerite is
usually band-shaped throughout most of its proximal and ventral part, more or
less twisted (e.g. as in Fig. 5 E ) , but distally tapering and sometimes very long
(Fig. 5A). In other species of Halobates (e.g. Figs 4B, 6A-D) and in Asclepios
(Fig. 4A), the ventral and dorsal sclerites are separated from each other. Because
these sclerites usually overlap, the separation is not always obvious.
The two pairs of lateral sclerites found in H. mjobergi (Fig. 4B, Is1 and ls2) are
also present in H. muculatus (Fig. 4 C ) , poseidon (Fig. 6 A ) , robustus (Fig. 6 B ) ,
princeps (Fig. 6C),Jijiensis (Fig. 6 D ) and others. The two sclerites of the first pair
are usually of about the same size and shape, while the sclerites of the second
pair are usually much smaller (Figs 4 C , 6 C ) and/or of different shape
PHYLOGENY O F HALOBA 7 E S
-=--=-I
A
29
B
Figure 5. Vesical armature of male phallus; further explanation in Fig. 4. A, Halobates micans
Eschscholtz; B, H.flaviventris Eschscholtz; C , H. regalis Carpenter; D, H. whiteleggei Skuse; E,
H. darwini Herring. All scale bars = 0.1 mm. Abbreviations: see text.
(Fig. 6B-D). With the exception of H. maculatus (Fig. 4C), the species just
mentioned have a basal sclerite (Fig. 6A, bs). This sclerite is not found in
H. mjobergi or in any species with a perforated dorsal sclerite.
The second pair of lateral sclerites has been lost in species such as H. hayanus
(Fig. 4D), germanus (Fig. 4E), micans (Fig. 5A), javiventris (Fig. 5B), regalis
(Fig. 5 C ) , whiteleggei (Fig. 5D), darwini (Fig. 5E) and others. The sclerites of the
first pair are usually very large and sometimes have hook-shaped bases (e.g. Figs
5A, B, 6D).
It is hypothesized (Fig. 6E) that the ancestral type of the halobatine vesical
armature was strictly symmetrical and composed of separate dorsal and ventral
sclerites and two pairs of lateral sclerites (as found in freshwater Halobatinae,
e.g. Metrocoris). From insects with this configuration, two lineages may have been
derived. In one lineage, a ‘hole’ was formed in the dorsal sclerite, the dorsal and
ventral sclerites were fused, and the second pair of lateral sclerites was eventually
lost. In the other lineage, a basal sclerite was developed but all the other sclerites
N. M. ANDERSEN
30
.
.
.A
.
I
R
Y
C
Is2
.
D
E
Figure 6. Vesical armature of male phallus; basal sclerite (bs) dotted; further explanation in Fig. 4.
A, Halobatss posdon Herring; B, H. robtutu Barber; C , H. princeju White; D, H. jjiensis Herring; E,
Evolution of vesical armature in Halobates. All scale bars = 0.1 nun. Abbreviations: see text.
were retained but modified in various ways. There was a trend in both lineages
towards a more and more asymmetrical vesical armature. This trend was only
partly correlated with the increasing asymmetry of the male genital segments.
The structures of the male phallus have not been used before as taxonomic
characters for Hulobutes, although the vesical armature in particular has proved
useful in several other groups of water striders. Imms (1936) illustrated the distal
part of the phallus in H. hayanus, but its structure was not properly understood
and two sclerotized pieces in the vesica were mistaken for parameres. China
(1957) described and illustrated the distended phallic organ (called ‘aedeagus’)
of H. mjobergi but used a slightly different terminology from that employed here
(Matsuda, 1960; Andersen, 1982). Finally, Miyamoto (1961) illustrated the
distended phalli of Japanese species of Asclepios and Hufobates. The present study
reveals a high degree of variation in the male genitalia of sea skaters and
emphasizes the importance of these structures, both in taxonomic and
phylogenetic studies of Hulobutes.
PHYLOGENY OF HALOBATES
31
ra2
J
C
Figure 7. Female genital segments. A, Halobates mjobergi Hale, abdominal end in ventral view; B,
H.mjobergi, ovipositor in ventral view; first gonapophysis ( g o l ) of left side removed; C, H.mjobergi,
second gonapophysis (g02) of left side in lateral view; D, H. gennanur White, second gonapophyses
(g02) in ventral view. All scale bars = 0.1 rnm. Abbreviations: see text.
Female genital segment5
Pregenital abdomen
The abdomen of female Halobates is relatively short and the pregenital
segments are quite similar to those of the male. The very flexible, intersegmental
membranes between the fourth to seventh segments enable the female abdomen
to be expanded to nearly twice its normal length and to accommodate as many
as 40 mature eggs (Andersen & Polhemus, 1976). The abdominal sterna, except
sternum 7 (Fig. 7A, s7), are very short.
Ocipositor
In female Halobates, the genital segments are composed of the relatively large
segment 8 (Fig. 7A, s8) and the small proctiger (Fig. 7B, pr). Segment 8 is
ventrally divided into two large, plate-shaped j u t gonocoxae (Fig. 7A, gxl). The
ovipositor is usually well developed, with plate-shaped, non-serrated
gonapophyses as in most gerrids (Andersen, 1982).
Thejrst gonupophyses (Fig. 7B, gol) belong to segment 8 and are attached to
the ventral corners of the gonocoxae. A proximal ramus (ral) connects each
gonapophysis with a dorsal gonangulum. The gonapophyses are elongate, only
partly sclerotized, and furnished with numerous hairs on their inner surfaces.
The apices of the first gonapophyses are membranous and more or less pointed.
‘The second gonapophyses (Fig. 7B, C , g02) belong to segment 9. They are
elongate and well sclerotized, with relatively long, free distal parts. The apex of
each gonapophysis is typically sharply pointed and hook-shaped (Fig. 7C). A
32
N. M. ANDERSEN
subapical, filiform outgrowth is found in Asclepios annandalei, and shiranui
(Matsuda, 1960: fig. 759; as A. coreanus miyamotoi Esaki) and in Halobates mjobergi
(Fig. 7B, fi). The two gonapophyses are connected by a partly sclerotized bridge
which carries a pair of median lobes (ml). These are rounded in Asclepios
mandalei and shiranui, and in Halobates mjobergi, micans, splendens and sobrinus
(Matsuda, 1960: fig. 767), reduced in H. maculatus, but distinctly setiform in
most other Halobates (Fig. 7D). Each gonapophysis is proximally provided with a
slender ramus (Fig. 7B-C, ra2) which also carries the rudimentary tergum 9. An
ovate, slightly sclerotized structure between the bases of the second
gonapophyses (Fig. 7B,x) marks the entrance to the genital chamber (see
below).
Imms (1936) described and illustrated the ovipositor in H. germanus (as
H . sewelli) but used a slightly different terminology than that employed here
(following Andersen, 1982 and Heming-Van Battum & Heming, 1986).
Matsuda (1960), also using a different terminology, described and illustrated the
female genitalia of Asclepios shiranui and Halobates sobrinus. My observations
confirm those made by previous authors on the structure and variation of the
female genital segments in sea skaters. The ovipositor of Asclepios species has
longer and more hairy gonapophyses than most Halobates species. In this respect,
the ovipositor ofH. mjobergi (Fig. 7B) is somewhat intermediate in structure. The
open-ocean species, in particular H. micam and splendens, have distinctly shorter
gonapophyses.
Oviposition and egg structure
The function of the ovipositor can be deduced from preserved Halobates
females with extended genital segments. The eighth segment is protruding from
the abdominal end with the two gonocoxae separated along the ventrdl midline.
The gonapophyses are unfolded and lowered to the substrate. During
oviposition, the egg is guided through the tube formed by the two pairs of
gonapophyses. The different ovipositor structure observed among Halobates
species probably reflects different modes of oviposition. I t is hypothesized that
the somewhat reduced ovipositor of open-ocean species is associated with their
habit of depositing eggs superficially on floating objects (Andersen & Polhemus,
1976). Observations on egg-laying behaviour in H. fijiensis (Foster & Treherne,
1986) indicate that females of coastal species may search more carefully with
their oviposit6r in order to find a suitable place for oviposition.
The eggs of Halobates are relatively large (1.0-1.2 mm) compared with the
body of the female (which rarely exceeds 5 mm). The elongate egg is deposited
lengthwise on the substrate, embedded in a gelatinous mass (Andersen &
Polhemus, 1976). Eggs of the open-ocean species are deposited on all kinds of
floating material (Lundbeck, 1914; Andersen & Polhemus, 1976) while coastal
species in natural habitats may oviposit on ‘grounded’ substrate like sea-grass
(Foster & Treherne, 1986), or on the concrete walls of an experimental tank
(Herring, 196 1) .
Eggs of Halobates can be divided into several groups on the basis of the
structure of the chorion. Lundbeck (1914) described and illustrated various
types of structures, some of which have branched processes, crenulations or
spines. Herring (1961) mentioned the chorionic structure of some species (from
observations of mature, ovarian eggs). He found that most species have smooth
PHYLOGENY OF HALOBA TES
33
eggs, viz. H . micans, sericeus, sobrinus, hawaiiensis and kelleni. A few species, such as
H. germanus, have the chorion surface covered with a fine, polygonal pattern
(Andersen & Polhemus, 1976; SEM-picture).
There is only one micropyle in Halobates eggs. It is located near the anterior,
slightly thickened end of the egg (Lundbeck, 1914). The egg of Asclepios
annandalei has one micropyle and a crenulated chorion sculpture (personal
observations).
Gynatrial complex
Structure
Female Halobates have a very complicated internal reproductive system for the
acceptance and distribution of sperm and fertilization of eggs. This system is
called the gnatrial complex and is unique to gerromorphan bugs (Andersen, 1982;
see Heming-Van Battum & Heming, 1986 for alternative interpretations of some
structures). It is composed of a large gnatrial sac (Fig. 8, gs) which arises from
the dorsal part of the fertilization chamber (fc), near its external opening. This
sac is normally extensively folded and therefore highly inflatable. In the
Gerridae, the walls of the sac are usually provided with gland cells (Andersen,
1982), but no traces of gland ductules could be observed in any of the species of
Asclepios or Halobates. The sac has a uermiform appendix (Fig. 8, va) which may be
more or less extensively coiled. A long and tubular spermatheca (Fig. 8, sm)
originates from the vermiform appendix.
The most intricate part of the gynatrial complex is thefecundation canal (Fig. 8,
cit). It is a very narrow canal which originates from the top of the vermiform
appendix, close to the opening of the spermathecal tube, and runs in wide loops
along the gynatrial sac and the dorsal side of the genital chamber, where it ends.
Part of the fecundation canal is modified as a fecundation pump (Fig. 8, pu). The
gynatrial complex is provided with muscles arising from the body wall. Lateral
muscles insert on the two flanges of the fecundation pump and medial muscles
Figure 8. Female gynatrial complex of Halobates (schematized) shown in position relative to
abdominal sterna 5-7 (s5-s7), ventral apodeme (ap), lateral oviducts (ov), and fertilization
chamber (fc); all muscles omitted. Abbreviations: see text.
N. M. ANDERSEN
34
insert on the fertilization chamber; the last mentioned muscles arise from an
apodeme originating on the anterior margin of sternum 7 (Figs 7A, 8, ap).
The gynatrial complex of Halobates mjobergi (Fig. 9A) has an extensive, lightly
sclerotized band in the gynatrial sac which continues on the vermiform
appendix. The appendix has 5-6 coils. A partly sclerotized gynatrial sac is also
found in H. poseidon and in the single species of Metrocoris examined. In all other
species of Halobates examined, the gynatrial sac is membranous and extensively
folded. In some species, the pattern of folds seem to be more permanent, e.g.
H . hayanus (Fig. 9B) and micans (Fig. 9C). The vermiform appendix is usually
more or less coiled. It is extremely long in H. mjobergi (Fig. 9A, va), H. micans
(Fig. 9C) and others, where the distal part of the appendix is folded into the
basal coils. The gynatrial complex of Asci@ios annandalei is simple, with a
relatively short vermiform appendix.
The fecundation canal is slightly variable in the species examined. The distal
part is usually slightly sinuate (Fig. 9A, C, ca) but more distinctly meandering in
a few Halobates species (Fig. 9B). In most gerrids (incl. Metrocoris), the
fecundation pump has relatively broad flanges. These are elongate and narrow
srn
A
...
B
Figure 9. Female gynatrial complex of Halobates species, dorsal view. A, Halobates mjobergi Hale; B,
H. hayanus White; C , H. micans Eschscholtz; D, H.fiuiumhis Eschscholtz. All scale bars = 0.1 mm.
Abbreviations: see text.
PHYLOGENY OF HALOBATES
35
in species of Asclepios and in Halobates mjobergi (Fig. 9A, pu) and hayanus
(Fig. 9B), and spinelike and curved in H . micans (Fig. 9C), splendens, Javiventris
(Fig. 9D, pu), sobrinus and sericeus.
Function
The function of the gynatrial complex of the Gerridae was first interpreted by
Andersen ( 1975). The processes of insemination and fertilization were
extensively discussed by Heming-Van Battum & Heming (1986, 1989) for
gerromorphan bugs in general. During copulation, the male deposits a mass of
sperm at the entrance of the gynatrial sac. The female draws the sperm into her
gynatrial sac at the end of copulation. The very long spermatozoans (longer than
the egg or even longer than the female body in some gerromorphans) are
transferred into the lumen of the extremely long and narrow spermatheca.
Before fertilization, the spermatozoans are drawn from or swim out of the
spermatheca into the fecundation canal and are probably guided through the
canal by the action of the fecundation pump. When the egg passes the
fertilization chamber, the spermatozoans enter the lumen of the chamber
through the opening of the fecundation canal and fertilize the egg. The
functional significance of the elaborate gynatrial complex of gerromorphan bugs
is probably that it enables the female to control the distribution of sperm and
fertilization of the large eggs (Heming-Van Battum & Heming, 1986).
CLADI STIC ANALYSIS
Characters
A total of 64 characters (numbered 0-63) were selected to describe the
morphological variation in 27 species of Halobates and two species of Asclepios.
These characters are listed in the Appendix with extensive comments. For each
character, a number of discrete states (usually 2-3) were delimited. Only a few
characters describe relative measurements. The range of variation of these
characters was arbitrarily divided into two or three states.
The states of each character are symbolized by numbers (see the Appendix
and Fig. 10). Based upon preliminary outgroup comparisons, the zero (0) state
usually denotes the most primitive (plesiomorphic) state. For characters with
more than two states, it is usually assumed that the transformation series is
linear, ordered or additive (e.g. 0 + 1 + 2). For a small number of characters, it
was uncertain what were the most appropriate ordering of states. Such
characters were analysed as unordered or nonadditive (marked by an asterisk (*)
in the Appendix).
It should be emphasized (see e.g. Wiley, 1981), that a computerized cladistic
analysis based upon the principle of parsimony does not require decisions about
polarity (primitive-derived
sequence) to be made for the characters
beforehand. Including outgroup taxa or an ancestral taxon (hypothetical or
otherwise) in the analysis, the program decides character polarities based on the
same parsimony criterion used in constructing the phylogenetic tree.
PHYLOGENY OF HALOBATES
37
Hennig86 analysis
Analytical procedure
The ingroup taxa of the Hennig86 analyses were 27 species of the genus
Halobates. Two species of the genus Asclepios, A. annandalei and shiranui, were used
both as outgroup and ingroup taxa. As outgroup taxon representing the tribe
Metrocorini, the species Metrocoris histrio Esaki was selected. This species is
believed to be one of the most primitive members of its genus (P. Chen, personal
communication).
The character state matrix is shown in Fig. 10. For 15 species, all of the 64
characters could be scored. For 14 species of Halobates and one species of Asclepios,
characters of the female genitalia (nos 54-62) were unavailable. Characters not
scored for any state are marked by a question mark (?) in the matrix (Fig. 10).
The Hennig86 analyses were carried out as follows (see Farris, 1988 for details
about commands and options). First the complete data set (Fig. 10) was
analysed with the command rnhennig which calculates multiple trees without
branch breaking. Metrocoris (taxon no. 29), was selected as the outgroup. A
single tree of length 208 steps was found with a consistency index (ci) of 0.42 and
a retention index (ri) of 0.68 (for an explanation of the meaning of these indices,
see Farris, 1988, 1989). The command mhennig*, which calculates multiple trees
by branch swapping, found 7 shorter trees, length 206 steps, ci = 0.43, and
ri = 0.68. Finally, the command bb* was activated. This command applies
extended branch swapping to the trees in the current tree file and all available
memory to store the results. The results were 282 trees, all of length 206 steps,
ci = 0.43, and ri = 0.68. With the command nelsen, a Nelson consensus tree was
calculated for these multiple trees.
Another analysis was performed on the same data set (Fig. 10) but with
Metrocoris (taxon no. 29) omitted. The two species of Asclepios (nos 27, annandalei,
and 28, shiranui) were now selected as outgroups. Using the same procedure as
described above, the results were 98 trees, all of length 191 steps, ci = 0.42 and
ri 0.69.
The data set was also subjected to the command ie- (implicit enumeration)
which identifies at least one tree certain to be of minimum length. However, the
procedure was terminated after three hours of computation. The relatively large
number of taxa and low consistency of the character state set are probably
responsible for the failure in applying this command.
The results of the Hennig86 analyses were logged into a number of files and
printouts were produced for inspection and manual analyses. The following
commands and options were applied: plot, for producing diagrams of selected
trees (as in Fig. 1 IA); tlist, for listing a larger number of trees in parenthetical
notation; xsteps m, for listing character consistencies and fits; and xsteps h, for
listing possible character states of each hypothetical ancestor (node) on a selected
tree. The tree editor, command xx (‘Dos Equis’), was used to evaluate the results
of modifications of individual trees, and also to trace the changes in the states of
selected characters along the branches of a tree.
Cladogram structure
Using the Metrocoris (taxon no. 29) as the outgroup, a total of 282 trees each of
length 206 steps were found. With respect to the relative positions of taxa
N. M. ANDERSEN
38
included, all 282 trees have the two species of Asclepios (nos 27 and 28) placed
next to the outgroup, Metrocoris and outside the species of Halobates. Besides
obtaining this information, the 282 trees were not examined in further details.
A total of 98 equally parsimonious trees were found by analysing the data set
(Fig. 10) using the two species of Asclepios as outgroups. These trees are of length
191 steps, i.e. 15 of the 206 steps of the trees produced in the first analysis can be
attributed to Metrocoris. The consistency (ci = 0.42) of the 191-step trees is
satisfying, considering the number of taxa and characters of the data set. A closer
inspection of the 98 trees reveals that they are composed of seven subsets, each
containing eight trees, and seven other subsets, each containing six trees (which
are identical with six of the eight trees). The eight trees of each subset differ only
in the relative positions of eight species (nos 19-26), viz. mariannarum, j i j i m i s ,
japonicus, galatea, matsumurai, esakii, princeps and alluaudi. A Nelson consensus
analysis for the eight trees resulted in a polytomy for the species nos 19-26, i.e.
the relationships between these taxa are unresolved.
Most of the 14 subsets of trees differ in the relative positions of only nine taxa:
the species maculutus (no. 1) is placed in three different positions (exemplified by
Fig. 1 1A, D, E); the species zephyrus (no. 10) is placed in three different positions
(Fig. 1 1A, D, F); four species (nos I 1-14), viz. regalis, whiteleggei, damini and
peronis are placed in three different ways (Fig. 11A, D, F); and robustus (no. 15),
bryani (16) and poseidon (18) assume five different positions (Fig. 1 1A, D, and
F-H). In one subset of trees (Fig. 1lA), hayanus (no. 2) and formidabilk (3) are
found in relative positions different from those seen in other subsets
(Fig. 11D-H).
Evaluation of characters and clades
Characters
The character state set (Fig. lo), with Metrocoris (taxon no. 29) omitted,
comprises 44 two-state characters, 18 three-state characters, and one four-state
character. This gives a minimum of 83 steps in a cladogram based on these
characters (since character 63 is constant in all terminal taxa when Metrocoris is
omitted). The length of 191 steps in the most parsimonious trees indicates that
there are many cases of homoplasious evolution (convergences or reversals)
along the branches of each tree.
Inspection of the list of possible character states for the hypothetical ancestors
(nodes) of the cladograms confirms most of the preliminary assumptions about
the primitive-derived sequence of states. However, alternative polarizations of
transformation series are suggested for some characters. Comments on these
characters are included in the Appendix.
Clades
The following evaluation is chiefly clade-oriented. Each clade is dealt with in
turn, with particular reference to the synapomorphiessupporting the monophyly
of the group in question. Clades are identified by the numbers attached to the
internodes of the cladograms in Fig. 11. In cases where more than one
hypothesis of relationships is suggested by the 191-step ciadograms, the
synapomorphies supporting alternative hypotheses are contrasted. The
characters are referred to by their numbers in the list of characters found in the
Appendix. Figures in square brackets denote character states.
\
PHYLOGENY O F HALOBATES
39
7annandalei
8shi ranu i
micans
splendens
floviventris
I
mjobergi
36~Ssericeus
,+o&aernonus
B
ljaponicus
Zealatea
3natsuclurai
4esokii
6alluaudi
C
u-5 3
lbbrvani
mjobergi
Ir26alluoudi
9 4 0 f ijiensis
A
liaponicus
Zgolot ea
23matsunurai
32E24esakii
lmaculatus
D
mjoberai
lmaculatus
I
H
f7419-26
15rabustus
6E16brvani
leposeidon
G
Figure 11. Selected cladograms generated by Hennig86-analyses of the data matrix (Fig. 10) for
species of Halobates (terminal taxa nos 0-26) and Asclepios (outgroup, taxa nos 27-28); clades
discussed in text identified by figures on internodes. A, One of the 191-step cladograms; B,
subcladogram for taxa nos 4-9; C, subcladogram for taxa nos 19-26; C H , other 191-step
cladograms with taxa nos 4-9, 19-26 and 27-28 omitted. See text for further explanations.
Clade 55. The monophyly of the tribe Halobatini is supported by the
autapomorphies 16[1], 26[1] and 63[1]. Matsuda (1960: 294-295) lists a
number of other characters as ‘peculiar evolutionary trends’ in Asclepios and
Halobates. None of these, however, are synapomorphies for the two genera.
Clade 54. The monophyly of the genus Halobates is supported by the
autapomorphies 6[1], 18[1], 19[1], 22[1], 23[1], 25[1], 26[2], 34[1] and 43[1].
40
N.
M.ANDERSEN
Several structures of the male terminal abdominal segments are most significant,
viz. the distinctly widened segment 8 carrying spiracular processes, the long
styliform processes, and laterally widened proctiger. Compared with Halobates,
the genus Asclepios seems to be primitive in most characters. One autapomorphy
for Asclepios is the strongly modified male fore femora, 9[1].
As first suggested by China (1957), mjobergi (no. 0) is undoubtedly the most
primitive member of the genus Halobates. In many respects-such as colour
pattern, ventrally modified male fore femora, hair fringe restricted to middle
tibia, and strictly symmetrical vesical armature, H. mjobergi is quite similar to
species of Asclepios. However, since mjobergi shares all of the characters listed as
autapomorphies for Halobates (above), it clearly belongs to that genus.
Clade 53. Synapomorphies for all species of Halobates, except mjobergi, are the
characters 0[1], 1[1], 9[0], 12[1], 41[1] and 56[1]. The most significant of these
is the asymmetrical development of the male vesical armature.
Clade 51. Three different positions of H. maculatus (no. 1) are observed among
the 191-step cladograms. The first hypothesis places maculatus in a group with
species nos 2-14 (Fig. 11A). Synapomorphies for this group are 42[1], 44[1]
and 50[l]. These characters describe the structure of the dorsal sclerite of the
male vesica which has an elongate or diamond-shaped hole and is fused to the
ventral sclerite. This structure is quite unique within the Halobatini and strongly
support the monophyly of this group.
A second hypothesis suggests that muculatus is sister group of all other Halobates
except mjobergi (Fig. 11D). The synapomorphies supporting this hypothesis are
14[1] and 27[1]. A third and final hypothesis suggests that maculatus is sister
group of the Halobates species nos 15-26 (Fig. 1IE). This implies convergencies
in the characters 46 and 54 (see above). Following a critical evaluation of
synapomorphies, the last two hypotheses are rejected.
C l d 48. This clade comprises the Halobates species nos 2-14. Synapomorphies
for this group are 46[1] and 56[2]. The number of lateral sclerites in the male
vesica is reduced to only one pair, a significant change in the development of the
vesical armature in the Halobatini.
Clade 44. This clade comprises the Halobates species nos 2-9. Synapomorphies
for this group are 0[2], 32[0], 39[1] and 42[2]. Neither of these are particularly
significant.
Clude 40. This clade comprises the species nos 4-9 with germanus (no. 4) placed
as the sister group of the species nos 5-9. The synapomorphies supporting this
group are 1[2], 2[2], 3[1], 5[1], 17[1], 29[1] and 53[1]. Most ofthese characters
are quite significant. However, the inclusion offlauiventris (no. 6) in this clade
implies a number of character reversals in this species.
The cladistic analysis does not support the monophyly of a group comprising
the species H. germanus (no. 4), sericeus (5), micans (7), splendens ( 8 ) and sobrinus
(9). This is the so-called open-ocean group of Halobates (Herring, 1961). The
status of this group is further discussed below.
Clade 36. This clade, comprising sericeus (no. 5), Javiuentris (6), micans (7),
splendens ( 8 ) , and sobrinus (9), is supported by the synapomorphies 4[1], 37[1],
39[0] and 62[2]. The last character is especially significant.
Clade 33. This clade, comprisingflaviventris (no. 6), micans (7), splendm ( 8 ) and
sobrinus (9), is supported by the synapomorphies 13[1], 30[2], 44[0], 47[1], 49[1]
and 54[2]. The orientation of the male styliform processes and the structure of
the male vesica strongly support the monophyly of this group.
Clade 31. The 191-step cladograms all suggest a sister-group relationship
PHYLOGENY OF HALOBA TES
41
between JEauiventris (no. 6) and sobrinus (9) (Fig. 11A) as supported by the
synapomorphies 25[0], 28[0], 29[0], 42[1] and 61[0]. All of these are character
reversals and provide rather weak evidence of a closer relationship between these
two species. An alternative hypothesis (although not represented among the
191-step cladograms) is thatJEauiuentrisis more closely related to the species pair
micans and splendens (Fig. 11B). This hypothesis is supported by a rather strong
synapomorphy, 33[3], and is therefore preferred. This adds one extra step to the
most parsimonious cladograms.
Clade 30. The sister-group relationship between micans (no. 7) and splendens (8)
is supported by the synapomorphies 14[2], 55[0] and 57[1]. Besides, the very
similar shape and orientation of the male styliform processes strongly support the
close relationship between these two species.
Clade 39. The sister-group relationship between hayanus (no. 2) and formidabilis
(3) (Fig. 11A) is supported by the synapomorphies 28[0], 29[0] and 31 [I]. The
last synapomorphy is significant. In addition, both species have groups of lateral
spines on the male proctiger, a character only shared with germanus (no. 4).
An alternative hypothesis is that hayanus is more closely related to the species
nos 4-9 than to formidabilis (Fig. 11WH). The support for this hypothesis, 2[ I ]
and 5 1[ 11, however, is weak and it is therefore rejected.
Clade 45. This clade comprises the species Zephyrus (no. lo), regalis ( 1 l ) ,
whiteleggei (12), darwini (13) and peronis (14) (Fig. 1lA, E). The only
synapomorphy for this group is 27[1], which is a relatively strong character
although paralleled in the Halobates species nos 15-26.
An alternative hypothesis is that sephyrus is sister group to the species nos 2-9
(Fig. 1lF-H), with the synapomorphies 28[0], 29[0], 37[0] and 44[1]. All of
these are character reversals. A third hypothesis suggests that the species
nos 10-14 should be joined with the species nos 15-26 (Fig. 1 ID) instead of the
species 2-9. This hypothesis implies convergences in the structure of the dorsal
and ventral sclerites of vesica. Both of the alternative hypotheses are therefore
rejected.
Clade 41. This clade comprises the species regalis (no. 1 I ) , whiteleggei (12),
darwini ( 13) and peronis ( 14) (Fig. 1 1A). The synapomorphies for this group are
29[1], 37[1] and 44[2]. Especially the last one is significant. The alternative
hypothesis (Fig. 11F-G) is rejected.
Clade 37. This clade comprises the species whiteleggei (no. 12), darwini (13) and
peronis (14) (Fig. 11A). Only one, relatively weak synapomorphy, 4[1], supports
this group.
Clade 34. The sister-group relationship between darwini (no. 13) and peronis
(14) is supported by the synapomorphies 31[2], 32[2], 33[2], 37[2], 43[2] and
5 1[ 11. The boot-shaped apices of the male styliform processes, the fingerlike
prolonged lateral extensions of the male pygophore, and the distally reduced
dorsal sclerite of the male vesica strongly supports the monophyly of this group.
Clade 52. This clade comprises the Halobates species nos 15-26.
Synapomorphies for this group are 27[1] and 45[2]. The presence of a basal
sclerite, small or large, in the male vesica, strongly supports the monophyly of
this group.
‘There are alternative hypotheses in which the species poseidon (no. 18) assumes
different positions (Fig. 1 IE, F, H ) . These hypotheses imply convergent
development of a basal sclerite of the vesica or other convergencies in the vesical
structure. They are therefore rejected.
Clade 49. This clade comprises the Halobates species robustus (no. 15), bryani
42
N. M. ANDERSEN
(16) and poseidon (18). The single synapomorphy for this group, 57[2], is weak,
since this character was only scored for a limited number of species.
An alternative hypothesis joins the species nos 15-16 and 19-26, thus
excluding poseidon (no. 18) (Fig. 11D) . The single synapomorphy for this group
is 29[2]. In all these species, the male styliform processes are asymmetrical with
the left process being longest. This is probably a strong synapomorphy and this
hypothesis is preferred.
Clade 46. The sister-group relationship between robustus (no. 15) and bryani
(16) is supported by the synapomorphy 48[1]. This character state is also found
in other species and therefore not very reliable.
Clude 50. This clade comprises punope (no. 17) and the species nos 19-26. The
synapomorphies supporting the monophyly of this group are 4[1], 10[1], 12[2]
and 13[1]. The large padlike ‘file’ of the male fore tibia1 process is the most
significant of these. Most species are relatively large and have a fore tarsus with a
relatively long second segment.
Clade 47. This clade comprises the species mariannarum (no. 19),jjiensis (ZO),
juponicus (2 1) , galatea (22), mutsumurui (23), esakii (24), princeps (25) and alluaudi
(26). It is supported by the synapomorphies 0[2], 18[0], 30[1], 36[1] and 44[1].
That the hind tarsal segments are distinctly separated (character 18[0]) is here
treated as a reversal, i.e. an apomorphy (see Appendix).
Eight different branching patterns between the 8 species just mentioned were
observed among the 191-step cladograms. This reflects the absence of
synapomorphies that consistently resolve the relationships between these species.
However, a critical evaluation of characters (as synapomorphies) reveals the
following groupings (Fig. 11C):
Clade 47B. A clade comprised by the species nos 19-20 and 22-26, thus
excluding juponicur (no. 21), is supported by 13[2]. The relatively long first
segment of fore tarsus probably reflects the larger body size of the species
involved.
Clade 42. The relationships between the species mariannarum (no. 19),jjiensis
(20),princeps (25) and ulluuudi (26) is supported by 38113. The subparallel lateral
extensions of the male proctiger is a significant synapomorphy.
Clude 42B. The relationship between muriunnurum (no. 19) and jjiensis (20) is
supported by 28[2] and 45[1]. The distinctly asymmetrical male styliform
processes is a strong synapomorphy.
Clade 35. The relationships between galatea (no. 22), matsumurai (23) and esakii
(24) is supported by 31[2], 32[2] and 33[1]. The widened apices of the male
styliform processes is the most significant of these.
The set of relationships defined by these clades (Fig. 11C) is not found among
the set of eight patterns mentioned above and it adds extra steps to the most
parsimonious, 191-step cladogram. If strict adherence to parsimony is preferred,
the relationships between the Halobates species nos 19-26 must remain
unresolved, i.e. a polytomy.
DISCUSSION
Phylogeny and taxonomy
Separating Asclepios and Halobates
The genus Asclepios Distant (1915) was erected for A . annandalei Distant,
described from Calcutta and Ennar, India. Three other species have been
PHYLOGENY OF HALOBATES
43
assigned to this genus, two of which were originally described in Halobates (Esaki,
1924). The species A . coreanus Esaki (1930) has been reduced to a subspecies of
A. shiranui (Esaki, 1924).
Herring (1961) lists five criteria for separating the genus Asclepios from
Halobates. Of these, only the shape of the male tergum 9 (proctiger) is diagnostic
(see also Polhemus & Cheng, 1982). However, the proctiger is hardly
‘cylindrical’ (Herring 1961: 235) but rather ovate in Asclepios (Fig. 2C), while in
Halobates it is usually dilated laterally (Fig. ID).
Matsuda (1960) lists six characters he considers to be more primitive in
Asclepios than in Halobates. Some of these are not valid for all species of Asclepios,
viz. two-segmented hind tarsi (one-segmented in annandalei) and hair fringe of
middle leg confined to the tibia (present on the middle tarsus in annandalei).
Besides, I could not find parameres in males of annandalei or shiranui.
Newman & Cheng (1983) found different chromosome numbers in Asclepios
shiranui, 2n (male) = 23, and in four species of Halobates, 2n (male) = 31. The
latter is the highest chromosome number reported for any gerrid (Andersen,
1982).
The following characters separate the two genera of Halobatini.
Asclepios. Small species, length 3.0-4.0 mm, with extensive yellow markings on
head, pronotum, thoracic pleura and abdominal dorsum; venter chiefly pale.
Intersegmental suture between meso- and metanotum distinct laterally. Male
fore femora always modified ventrally (dilated, spinous). First segment of fore
tarsus very short. Male abdominal segment 8 (Fig. 2A, s8) longer than wide,
without spiracular processes; styliform processes short, straight, and with blunt
apices. Male proctiger (Fig. 2C, pr) ovate in outline.
Halobates. Size variable, length 3.2-6.5 mm. Chiefly dark coloured or silvergrey species without extensive pale markings except on venter and on head (few
species). Intersegmental suture between meso- and metanotum reduced to a pair
of lateral V-shaped pits. Male fore femora rarely modified ventrally. First
segment of fore tarsus variable in length. Male abdominal segment 8 (Fig. lB,
s8) wider than long, with rounded, tuberculate or fingerlike spiracular
processes; styliform processes present, usually long and slender. Male proctiger
(Fig. 1D, pr) pentagonate in outline, usually distinctly dilated laterally.
Species groups of Halobates
The results of the cladistic analysis of relationships between selected species of
Halobates are summarized in the reconstructed phylogeny (Fig. 12A-D) . A
number of monophyletic species groups are recognized and discussed below.
Species not included in the cladistic analysis are assigned to group, at least on a
tentative basis.
The mjobergi group: H . mjobergi. Small species with very short first segment of
fore tarsus. Head and pronotum with light colour pattern. Vesical armature
strictly symmetrical, two pairs of lateral sclerites (Fig. 4A). Pygophore with
distinct parameres (Fig. 3B, pa).
The proavus group: H . proavus and maculatus. Small species (especially males)
with short first segment of fore tarsus. Styliform processes of male relatively short
and robust, slightly asymmetrical. Vesical armature asymmetrical, with elongate
hole in dorsal sclerite and two pairs of lateral sclerites (Fig. 4C).
The species of the following three groups all share the same characters of the
male vesica, viz. vesical armature strongly asymmetrical; dorsal sclerite with a
diamond-shaped hole; only one pair of lateral sclerites (Figs 4D, E, 5A-E).
44
-
nijoberg'
-
micans group
hqyanus group
b
rqalis group
-
p r o m s group
poseidon group
- -
robustus
-
A
btyani
-
japonicus
matsumurai group
L
I
mariannamm group
micans
splendens
flaviwntris
hawaiiensis
-
micuns group
kelleni
-
regalis
whitelqgei
senralis
The micans group: ff. micans, splendens, sobrinus, gemanus, sericeus, flauiventris
(synonym H . kudrini Nasanov, 1894; Herring, 1961), huwaiiensis and possibly
trynu Herring (1964). Species of small or intermediate size. Except for the last
three species, this group is characterized by the reduced pale markings of head,
concolorous venter, relatively small eyes, strongly developed hair fringe on
middle tarsi, and reduced female ovipositor. Halobates Jlaviventris (synonym
H . eschscholtzi Herring; Polhemus & Polhemus, 1991) shares the hook-shaped
PHYLOGENY OF HALOBATES
45
lateral sclerites of the vesica (Fig. 5B) and the spine-like flanges of the
fecundation pump (Fig. 8D) with at least micans (Figs 5A, 8C) and splendens. The
relationships between species are presented in a cladogram (Fig. 12B).
The hayanus group: H. hayanus (synonym H . australiensis Malipatil, 1988; syn.
nov.), calyptus Herring and fomzidabilis. Species of intermediate size. Styliform
processes of male slender and almost symmetrical, with slightly recurved apices.
Male proctiger with lateral groups of dark spines.
The regalis group: H. regalis, whiteleggei, zephyrus, darwini, acherontis Polhemus
( 1982), herringi Polhemus & Cheng ( 1982), peronis, and sexualis Distant. Small
species with short first segment of fore tarsus. Head with light colour pattern in
darwini and zephyrus. Apical part of dorsal, vesical sclerite modified (reduced or
absent; Fig. 5C-E) except in zephyrus. Styliform processes with blunt or bootshaped apices, sometimes flattened. A preliminary cladogram of relationships
between species is presented (Fig. 12C).
The relationships between the micans, hayanus and regalis groups are not
completely settled. This is reflected by a trichotomy in the cladogram
(Fig. 12A).
The species of the following groups all share the same characters of the male
vesica, viz. basal sclerite present, dorsal sclerite solid, ventral sclerite separated
from dorsal sclerite, two pairs of lateral sclerites present (Fig. 6A-D) .
The poseidon group: H. poseidon and melleus Linnavuori ( 1971) (synonym
H. mangrouensis Schmidt & Muller, 1973; syn. nov.) are both small species with
a fore tarsus with a short basal segment. Head with light colour pattern in
melleus. The latter species is probably related to poseidon (not to mjobergi as
suggested by Linnavuori, 1971).
The robustus group: H. robustus and bryani may be sister species although most
of their characters are relatively primitive. Both species are small and the basal
segment of the fore tarsus is short. Head with light colour pattern in bryani. The
unsettled relationships between these species is reflected by a trichotomy in the
cladogram (Fig. 12A).
The panope group: H. panope. Small species and the first segment of the fore
tarsus is relatively short. Hind tarsus one-segmented (segments fused).
The remaining species constitute a monophyletic group. They are all large,
elongate (especially males), steel-grey, with yellow markings on venter. First
segment of the fore tarsus is relatively long.
Thejaponicus group: H. japonicus. Hind tarsus distinctly two-segmented (shared
with the following groups).
The matsumurai group: H. matsumurai, browni, nereis, esakii and galatea. Hind
tarsus distinctly two-segmented except in galatea. Male styliform processes with
widened apices and proctiger basally tumose.
The princeps group: H. princeps (synonym ashmorenris Malipatil, 1988; syn.
nov.). A very large species. Lateral extensions of male proctiger parallel and
emarginate. The relationships between this species and the following two groups
are not settled which is reflected by the trichotomy in the cladogram (Fig. 12A).
The alluaudi group: H. alluaudi, tethys and undescribed species from India
(N. M. Andersen & W. A. Foster, unpublished observations). Lateral extensions
of male proctiger subparallel (shared with the following group).
The mariannarum group: H. mariannarum, kelleni, katherinae, jjienris, salotae.
Styliform processes of male more or less asymmetrically developed. In the last
46
N. M. ANDERSEN
three species, the male terminalia are strongly modified, the pygophore and
proctiger rotated 90°, the female abdomen has a ventral pocket for the reception
of the terminal segments, etc. The relationships between species are presented in
the cladogram (Fig. 12D).
Herring ( 1961) recognized also several species groups within Halobates and
depicted the relationships between these groups in a ‘phylogenetic diagram’ (his
fig. 115). From Herring’s discussion (Herring, 1961: 235-236), it is clear that he
had some ideas of which species were primitive and specialized. However, some
of his species groups were explicitly based on primitive characters (e.g. light
colour-pattern, short first anterior tarsal segment) and are therefore not
monophyletic in the strict sense.
For instance, the mjobergi group (H. mjobergi, zephyrus, whiteleggei, durtoini,
peronis, regalis and robustus) was identified by Herring (1961: 236) as the most
primitive within Halobates, exhibiting many of the characteristics of Asclepios.
This group of species was characterized only by primitive characters and is
therefore paraphyletic. Most of these species belong to the regalis group
(Fig. 12C) and are closer to members of the hayanus and micans groups
(Fig. 12A). Herring placed robustus in the tnjobergi group with some reservations,
suggesting that it might belong to the open-ocean group instead. However,
H. robustus is closer to species like bryani and poseidon (Fig. 12A) than to any of the
above mentioned species.
Another of Herring’s groups, the proauus group ( H . proauus, maculatus, calyptus,
hayanus, sexualis, bryani and poseidon), is also a paraphyletic assemblage of species.
Halobates maculatus and the closely related proavus have a basic position in the
cladogram (Fig. 12A). Halobates sexualis belongs to the regalis group (Fig. 12C).
Herring recognized an ‘open-ocean’ group ( H . micans, sobrinus, splendens,
germanus, sericeus and eschscholtzi) and stated (Herring, 1961: 236) that this group
“appears to be monophyletic”. Apart from the oceanic habit, these species are
characterized by the rather flattened body, small eyes, and concolorous, dark
venter. Halobates eschscholtzi Herring, known only from the type series of females,
has recently been synonymized with H. Jlaviuentk (Polhemus & Polhemus,
1991). Later, Herring (1964) also included H . t p m in the open-ocean group
although this species seems to live in coastal habitats (N. M. Andersen,
unpublished observations).
The cladistic analysis (see above) questions the monophyly of the open-ocean
group of Hulobates. The uniformly dark ventral surface, small eyes, and in
particular the well developed hair fringe on the middle tarsi, are probably
adaptations towards the life on the ocean surface. I t is hypothesized that some or
all of these characters have evolved independently in different oceanic species.
The cladistic analysis (Fig. 12B) suggests that H. micans and splendens are more
closely related to H. flauiuentris, its sibling huwaiiensis, and perhaps trynae, than to
other oceanic species.
The remaining species of Halobates were by Herring (1961) united in three
species groups characterized by a longer first anterior tarsal segment, more
streamlined body with silver-grey pubescence, females often with stout, black
bristles on the thorax, and usually with yellow markings ventrally. The katherinae
group ( H . kathezinue, Jijiensis and salotae) was identified as the most specialized
group because of the strongly modified male and female terminalia.
With the exclusion of H . formidabilis, Jauiuentris and the closely related
hawaiiensis, these three groups together form a monophyletic group (Fig. 12A,
PHYLOGENY OF HALOB.4 TES
47
D). Herring did not specify the relationships between species except that the
(Herring, 1961: 236) “succession from left to right and from group to group
indicates affinity of related forms”. However, H . tethys and alluaudi, which
Hdrring placed in different groups, are most probably closely related. That the
katherinae group is closest to the group which include H . mariannarum and kelleni is
confirmed by the present study (Fig. 12D).
The status of Hilliella
China (1957) proposed the subgenus Hilliella for Halobates mjobergi Hale (type
species) and H . apicalis Esaki. Characters used to motivate this subgenus were
the absence of a hair fringe in the first segment of middle tarsus, the pale striping
of the fore and middle femora and tibiae, and the hairy processes of the eighth
abdominal segment in the male. More recently, Polhemus & Cheng (1982) also
placed H. Zephyrus in Hilliella because of its supposed relationship with
H . mjobergi. However, the present analysis shows that H . zephyrus belongs to the
regalis group (see above).
In my opinion, Hilliella is of doubtful taxonomic value. Halobates apicalis, one
of the species assigned by China (1957) to his subgenus, clearly belongs to
Asclepios. One of the characters used by China, viz., the absence of a tarsal hair
fringe, is not even valid for separating Asclepios and Halobates (see above). The
other characters are at most species-specific for H. mjobergi. Although being
unique in many ways, it is hardly justified to uphold a separate subgenus for this
species. I therefore synonymize Hilliella China, 1957, syn. nov., with Halobates
Eschscholtz, 1822.
Evolution
The cladistic methods of phylogenetic reconstruction applied in the previous
section are based upon the principle of parsimony. Although there is no reason to
believe that evolution always has proceeded in the most parsimonious way,
parsimony is a necessary principle of logic in choosing among many, equally
possible phylogenetic hypotheses (Nelson & Platnick, 1981).
Testing evolutionary scenarios
The ability of cladistic methods to elucidate patterns of phylogeny, to which
all other evolutionary patterns must relate at some level, offers the possibility of
creating, and to some extent testing, scenarios proposed in other fields, including
biogeography, adaptive evolution, ecology and behaviour (Coddington, 1988;
Carpenter, 1989; Brooks & McLennan, 1991). The historical biogeography of
sea skaters will be analysed and discussed elsewhere. Here, I will discuss the
evolution of sea skaters, trying to present arguments to support specific
hypotheses or scenarios describing the adaptive evolution of this remarkable
group of marine insects and, wherever possible, perform or suggest critical
testing of these hypotheses.
The origin of Halobates
In a cladistic system, the origin of a monophyletic group can be determined as
the event where the group was separated from its sister group by the splitting of
a common ancestor. From the reconstructed phylogeny of the sister groups and
knowledge about their distributions, we can discuss the place of origin of both
groups and the adaptive changes associated with their origin.
48
N. M. ANDERSEN
The known distribution of sea skaters covers the whole of the Indo-Pacific
region (for the moment excluding the presence of Halobates micans in the Atlantic
Ocean). This is not only because of the widespread occurrence of a few, openOcean species. There are endemic species in such distantly separated places as the
Red Sea (H. melleur) and the Galapagos Islands (H. roburtus). It is therefore
hardly possible to delimit a place of origin for Halobates based only upon the
present distribution of the genus. It has been common practice also to use
relative species diversities to determine the place of origin for a group. Using this
argument, Newman & Cheng (1983) suggested that Halobates originated in
south-east Asia. There are no reasons, however, a priori to assume that ancestral
sea skaters diversified before expanding their area of distribution.
The sister group of Halobates is the genus Asclepios. The three described species
are found along the coasts of South and East Asia (Esaki, 1930, 1937; Andersen,
1982; Polhemus & Cheng, 1982). Assuming that the actual distribution of
Asclepios also represents the ancestral distributional area for this genus, we may
hypothesize that the vicariance event (whatever this was) separating Halobates
from Asclepios took place in south or east Asia. From this hypothesis it can be
predicted that the most primitive Halobates species should be found either in
South and East Asia or in adjacent areas. Halobates mjobergi is undoubtedly the
most primitive, living species of the genus. However, since this species is found
along the coasts of tropical Australia (China, 1957), the above prediction is not
met. Extinction among the early lineages of Halobates is one of the most plausible
explanations for this.
The closest relatives of sea skaters are water striders belonging to the tribe
Metrocorini (subfamily Halobatinae). They are widely distributed in the
Ethiopian and Oriental regions, but absent from the Australian region. Only one
genus and species, Metrocoris celebensis D. Polhemus ( 1990) has crossed Wallace’s
line. Taking the present distribution of the freshwater relatives of sea skaters into
account, it seems very likely that the first members of the tribe Halobatini
originated in the Indo-Malayan area and that Halobates was separated from
Asclepios somewhere in the same geographical area. Other authors have come to
a similar conclusion (Herring, 1961; Jaczewski, 1972; Andersen, 1982; Cheng,
1985).
Evolution of the marine habit in sea skaters
The marine Halobatini undoubtedly evolved from related freshwater gerrids.
All species belonging to the tribe Metrocorini live in lotic freshwater habitats, in
mountains as well as in coastal lowlands. It is therefore hypothesized that
ancestral sea skaters invaded near-shore, marine habitats from lotic freshwater
habitats, probably via estuarine habitats. The following observations
corroborate this hypothesis.
The three described species of Asclepios live in coastal habitats, such as bays,
canals and reservoirs more or less isolated from the sea (Esaki, 1930, 1937) as
well as in tidal canals in mangroves (Cheng & Hill, 1980; personal observations
in Phuket, Thailand). Similar habitats are preferred by a number of Halobates
species, e.g. mjobe7gi (China, 1957), darwini (Polhemus, 1982),poseidon (Polhemus
& Cheng, 1982), melleus (Schmidt & Muller, 1973, as H . mangrovmis), roburtus
(Birch et al., 1979; Foster & Treherne, 1982), and bryani (Foster & Treherne,
1986). One species of sea skaters H . acherontis has even been captured in a river
PHYLOGENY OF HALOBATES
49
(Daly River, Australia: N.T.), about 70 miles above the river mouth (Polhemus,
1982). Although the salinity of the water was not recorded, it probably was
much lower than usually experienced by coastal sea skaters, thus indicating a
wide range of tolerance towards salinity in some Halobates species.
Most of the adaptations required for life in the marine environment are
already present in the freshwater relatives of sea skaters (Andersen, 1976, 1977,
1982). These adaptations make it possible for the insects to live permanently on
the water surface. The hydrofuge property of the surface hair-layers is
particularly critical and may have been further improved in sea skaters
(Andersen, 1977; Cheng, 1985).
Sea skaters are always wingless, perhaps because the ability to fly has lost its
importance in the extremely stable marine environment. This adaptation,
however, is only a continuation of a trend exhibited by most groups of freshwater
gerrids where winged individuals are extremely rare (Andersen, 1982).
Apart from the tolerance of eggs and newly hatched nymphs towards the
saline water and the development of an ability to maintain a hypotonic body
fluid (Cheng, 1985), there seem to be very few special adaptations in sea skaters.
New adaptations are the development of hair fringes on the middle tibiae and
tarsi and probably improvements in the hydrofuge properties of the hair-layers
of the body surface and legs (Cheng, 1973; Andersen & Polhemus, 1976;
Andersen, 1977). Most species of the freshwater Metrocorini prefer shaded
habitats and are more or less extensively pale coloured. Sea skaters (except the
mangrove species) cannot seek shade and are dark coloured with a thick, greyish
or silvery hair layer, possibly a protection against the UV-radiation from the sun
(Cheng et al., 1978).
Halobatine sea skaters are not the only marine water striders. It is estimated
that the marine environment has been invaded many times during the evolution
of the hemipterous infraorder Gerromorpha (Andersen & Polhemus, 1976;
Andersen, 1979, 1982, 1989a, b).
The diversification of sea skaters
Although it is the open-ocean species of Halobates that have attracted most
interest, the majority of the 41 described species of sea skaters prefer near-shore,
marine habitats. Our knowledge about the ecology of sea skaters is quite
insufficient and usually limited to notes about the locality where species were
collected accompanied by casual biological observations. Fortunately, a few
coastal species have been studied more intensively during the past decade or so,
first and foremost by W. A. Foster and the late J. E. Treherne, University of
Cambridge.
Halobates robustus was studied in the Galapagos Islands (Birch et al., 1979;
Foster & Treherne, 1982; Treherne & Foster, 1980, 1981). This species inhabits
protected, rocky coasts with mangroves. Adults tend to aggregate in large
‘flotillas’ very close to mangrove trees or rocks. Nymphs (all instars) are usually
found further away from the shore. Mating pairs are very frequently observed
and the male (which is smaller than the female) stays with the female for a
prolonged period of time (mate-guarding behaviour) . Egg-laying was never
observed but oviposition probably takes place on rocks and/or mangroves.
Similar habitat preferences and behaviour were observed in H . bryani in the Fiji
Islands (Foster & Treherne, 1986).
50
N. M. ANDERSEN
Another coastal species, H . j j i e m i s , was studied in the Fiji Islands (Foster &
Treherne, 1986). I t inhabits bays and lagoons fringed with mangroves. Ybunger
nymphs are always found in sheltered waters amongst mangroves. Older nymphs
and adults are found in more open water, sometimes several hundred metres
from the mangroves. Mating pairs were infrequently observed, and the
encounters between male and female (male slightly larger than female) were
brief. Egg-laying was observed to take place on stands of sea-grass or coralline
green algae near the low-water mark, at extreme low water springs. The newly
hatched nymphs then have to make their way for hundreds of metres to the
protecting mangroves. Casual observations indicate that H. mariannarum
(Micronesia), kellmi (Samoa), and salotae (Tonga), and alluaudi (Seychelles,
Aldabra Atoll) may have the same type of biology (Cheng, 1981; D. Polhemus,
1990; W. A. Foster, in litt.).
Most near-shore species of Halobates seem to prefer habitats that are sheltered
from winds and wave action. Very few species of Halobutes tolerate more exposed
conditions. Observations of the distribution of H. jpaviventris in Palau, West
Caroline Islands (Cheng, 1981) suggest that this species aggregates along the
outer margins of fringing coral reefs where thousands of adults and nymphs (all
instars) could be collected. The same species was most typically encountered
over the fore reef of the Aldabra Atoll, western Indian Ocean, 500 to 1000
metres offshore. Its tendency to cruise over fore reef waters parallel to the reef
crest was similar to the behaviour observed for H. princeps in the Malay
Archipelago (D. Polhemus, 1990).
From these studies and observations, it is hypothesized that near-shore species
of Halobates have diversified with respect to habitat preferences of adults and
nymphs, tolerance towards surface winds and wave action, and probably also in
oviposition sites and mating strategies. From casual observations of other sea
skaters, it is predicted that H. mjobergi (China, 1957), poseidon (Polhemus &
Cheng, 1982), damini (Polhemus, 1982), and possibly other ‘mangrove’ species
(especially those belonging to the regalis group) are ecologically and
behaviourally quite similar to H. robustus. The same probably applies to the
species of Asclepios which live in the same kind of habitats (see above).
So far, we do not know how widespread the 3jiensi.s’ type is. However, by
taxonomic inference we can predict that most species of the Halobates matsumurai,
princeps (but see above), alluaudi and murimnurum groups (Fig. 12A, D) have a
similar type of ecology. The fflaviventlis’ type is probably less common but since
H. hayanus and proauus often are found near the margin of coral reefs (personal
observation in Phuket, Thailand), these species may also tolerate more exposed
conditions.
The test of adaptational hypotheses requires cladistic hypotheses based upon
other traits than those to be tested (Coddington, 1988). This condition is met in
the set of morphological characters used for the cladistic analysis (see the
Appendix). The hypothesis to be tested is as follows: sea skaters have evolved
through a series of transitions between habitats, from lotic freshwater habitats
(stage 0), through estuaries and mangroves (stages 1 and 2), exposed coral and
rocky coasts (stage 3) to the open ocean (stage 4). Each stage is characterized by
certain structural and functional (incl. behavioural) adaptations. Stage 1 is the
‘robustus’ type, stage 2 the ‘jjiensis’ type, stage 3 the ‘j?auiventris’ type of ecology
and behaviour mentioned above, and stage 4 is the oceanic way of life.
PHYLOGENY OF HALOBATES
51
HalobaIm
I
1
1
4
3
1
3
?
1
1
1
1
2
2
3
2
2
4
4
3
3
4
Y
-i‘.
0
B
3
Figure 13. Cladograms of relationships for sea skaters with stages of habitat preferences
superimposed. A, Cladogram of relationships between Asclepzos and the species groups of Halobates;
B, cladogram for the micans group. Meaning of stages: 0, lotic freshwater; 1, estuaries and mangroves
(‘robustus’ type); 2, mangroves (.J;jimris. type); 3, exposed coral and rocky coastS (tpaviventrzs’ type);
and 4, open ocean. A cross bar indicates transitions between habitats. See text for further
explanations.
These stages are then superimposed upon the reconstructed phylogeny of
Halobates and Asclepios (Fig. 12A) with Metrocoris added (representing freshwater
Metrocorini). By inspection of the cladogram (Fig. 13A) it is observed that
stage 1 is found in taxa terminating the most basal clades, viz. Asclepios spp.,
Halobates mjobergi, the poseidon group, and H . robustus and bryani. Only one
transition 0 + 1 is needed to explain most occurrences of the ‘robustus’ type. The
hypothesis that this is the most ancestral type of ecology and behaviour in sea
skaters is therefore more parsimonious than any other hypothesis. Incomplete
information about the habitat preferences in the proavus and hayanus groups limits
the testability of this part of the cladogram. However, stage 1 is predominant in
species of the regalis group and probably ancestral to this clade. This means that
the supposed freshwater habit of H . acherontis (Polhemus, 1982) must be a case of
habitat reversal.
Stage 2 or the ‘jiiiensis’ type has seemingly evolved from stage 1 only once
(Fig. 13A), but more data about the ecology and behaviour of species belonging
to the matsumurai, alluaudi, and mariannarum groups are needed to test this
hypothesis. Halobates princeps has seemingly reached stage 3.
The assumption of a linear progression between stages, 1 + 2 --+ 3 + 4, does
not pass the cladistic test. Instead, the independent sequences 1 -+2 + 3 and
52
N. M. ANDERSEN
1 43 44 seem more plausible. Casual observations (see above) suggest that in
terms of ecology and behaviour, H. hayunus and prouvus belong to stage 3 or the
‘flaviventris’ type. The hypothesis that stage 3 is transitional between adaptations
towards nearshore and oceanic habitats is essential to our understanding of how
sea skaters have colonized the surface of the great oceans (see below).
The ecological and behavioural diversification of sea skaters has made it
possible for several species to coexist in the same geographical area. Foster &
Treherne (1986) found Halobates bryani (stage 1) andjjiensis (stage 2) in different
localities in the Fiji Islands. On Aldabra Atoll, western Indian Ocean, D. A.
Polhemus (1990) found Halobates poseidon (stage 1) in mangroves along the
margins of the lagoon; H . alluaudi (stage 2) typically inside the reef crest, over
the back reef lagoon; H.javiuentris (stage 3) over the fore reef, 500 to 1000 m
offshore; and H . germanus and micans (stage 4) over the fore reef or on the deeper
ocean beyond, 1000 m or more offshore. The diversification of sea skaters within
the marine environment has probably been one of the major agents in promoting
the evolutionary success of these marine insects.
The colonization of the open ocean
Both adults and nymphs of the five open-ocean species of Halobates live
permanently upon the sea surface, always at some distance from nearest land.
Eggs are deposited on various floating objects (Lundbeck, 1914; Andersen &
Polhemus, 1976). The open-ocean group comprises five species: H . germunus
(Indian and West Pacific Ocean), sericeus (Pacific Ocean), sobrinus (East Pacific),
micans (Atlantic, Indian and Pacific Ocean), and splendens (south-east Pacific).
Herring ( 1961, 1964) also included H . eschcholtzi (Zanzibar) and tynae (Bay
of Bengal), but neither of these species are truly oceanic. The cladistic analysis of
Halobates (see above) has seriously questioned the hypothesis that the five openocean species alone constitute a monophyletic group. On the contrary, there is
rather strong support for the hypothesis that the oceanic species pair H. micans
and splendens is more closely related to the coastal species H.javiventris and its
sibling h u i i e n s i s than to the three other open-ocean species (Fig. 12B).
One scenario could be that the oceanic habit evolved in the common ancestor
of the micans group, but that the species pair H.Javiventris and hawaiiensis
reversed their preferences from open-ocean to coastal habitats (Fig. 13B). If such
a habitat reversal is accepted, this is the most parsimonious hypothesis. An
alternative, though less parsimonious hypothesis, implies that the oceanic habit
evolved independently four times within the micum group.
The closest relatives of the micans group (Fig. 12A) all live in near-shore
habitats. It is therefore hypothesized that the surface of the oceans was colonized
by coastal populations of sea skaters developing a tolerance (or preference) for
more exposed habitats. The sequence of habitat preferences may have proceeded
from coasts fringed by mangroves or other vegetation, via exposed coral or rocky
coasts, and finally to the far-shore sea surface.
It is interesting that the near-shore relative of oceanic sea skaters,
H. jauiuentris, seems to tolerate more exposed situations than most coastal sea
skaters (Cheng, 1981; D. Polhemus, 1990). This species, together with its sibling
H. huwaiiensis, is also the most widely distributed of the coastal sea skaters with
disjunct distributional areas along the coast of East Africa, south and south-east
Asia, in Micronesia, in the Hawaiian, Society and Marquesas Islands, and the
PHYLOGENY OF HALOBATES
53
Tuamotu Archipelago (Herring, 1961). Halobates hayanus is another widespread
species, known from the Red Sea, south-east Asia, the Malay Archipelago, New
Guinea and Australia. Such patterns of distribution seem to indicate that at least
some near-shore species of Halobates are able to cross wide stretches of open sea,
either as adult individuals or as eggs attached to floating objects.
The tendency of the most primitive of the oceanic species, H . germanus, to stay
closer to the coasts than other open-ocean species (Cheng, 1989a) indicates that
the oceanic habit might have evolved in a gradual way. I prefer this scenario to a
more dramatic one, which imagines populations of coastal species ‘washed’ or
‘blown’ out to sea and forced to stay there (Newman & Cheng, 1983).
The most significant adaptations associated with life on the ocean surface seem
to be the overall darker pigmentation, the smaller eyes and shorter antennae,
larger mesotibio-tarsal hair fringes (Miyamoto & Senta, 1960), and reduced
female ovipositor. Behavioural adaptations may also have changed, especially
the shift in egg-laying habit from ovipositing on ‘grounded’ substrate to floating
objects of different kinds. A shift in the behaviour of the younger nymphal instars
has also been necessary. In coastal sea skaters, the younger instars tend to
aggregate in places protected by mangroves or rocks (Foster & Treherne, 1982,
1986). Nymphs of the oceanic species have to face the adversities of the open sea
through the whole of their development.
ACKNOWLEDGEMENTS
I an indebted to Dr Lanna Cheng of the Scripps Institution of Oceanography,
La Jolla, and to Dr W. A. Foster of the Zoological Museum, University of
Cambridge, for sending me material of marine water striders and for their
valuable comments and suggestions when reading an early manuscript version of
this paper. I am further indebted to Dr D. A. Polhemus, Honolulu, and to Dr
J. R. Spence, Edmonton, for valuable suggestions on the manuscript, and to Dr
J. T. Polhemus, Englewood, Colorado, for placing his collection of marine water
striders at my disposal, for giving me access to his field notes, and for his kind
hospitality during my stay in Englewood, Colorado. A grant from the Danish
Natural Science Research Council enabled me to spend three weeks at the
Phuket Marine Biological Center, Thailand, collecting and studying the biology
of marine water striders. I am grateful to the Director and staff of the PMBC,
and to Dr J. Hylleberg, for excellent working facilities offered during my stay in
Phuket. This work is part of a project supported by grants from the Danish
Natural Science Research Council.
REFERENCES
ANDERSEN, N. M., 1975. The Limnogonus and Neogerris of the Old World, with character analysis and a
reclassification of the Gerrinae (Hemiptera: Gerridae). Entomologica Scandinavica, Supplement, 12: 1-96.
ANDERSEN, N. M., 1976. A comparative study of locomotion on the water surface in semiaquatic bugs
(Insecta, Hemiptera, Gerromorpha). Videnskabelige Meddelelser f r a Dansk Naturhistorisk Forening, 139:
337-396.
,%NDERSEN, N. M., 1977. Fine structure of the body hair layers and morphology of the spiracles of
semiaquatic bugs (Insecta, Hemiptera, Gerromorpha) in relation to life on the water surface. Videnskabelige
Meddelelser fra Dansk Naturhistorisk Forening, 140: 7-37.
.9NDERSEN, N. M., 1979. Phylogenetic inference as applied to the study of evolutionary diversification of
semiaquatic bugs (Hemiptera: Gerrornorpha). Systematic ~ o o l o g y ,28: 554-578.
54
N. M. ANDERSEN
ANDERSEN, N. M., 1982. The semiaquatic bugs (Hemiptera, Gerromorpha). Phylogeny, adaptations,
biogeography, and classification. Entomonograph, 3: 1-455.
ANDERSEN, N. M., 19%. The coral bugs, genus Halouelia Bergroth (Hemiptera, Veliidae). I. History,
classification, and taxonomy of species except the H. &ya-group. Entomologica Scandinarrica,20: 75-120.
ANDERSEN, N. M., 1989b. The coral bugs, genus Hulooclia Bergroth (Hemiptera, Veliidae). 11. Taxonomy of
the H. malaya-group, cladistics, ecology, biology, and biogeography. Entmlogica Scandinauica, 20: 179-227.
ANDERSEN, N. M. & POLHEMUS, J. T., 1976. Water-striders (Hemiptera: Gerridae, Veliidae, etc.). In
L. Cheng (Ed.), Ma& Insects: 187-224. Amsterdam: North-Holland.
BIRCH, M., CHENG, L. & TREHERNE, J. E., 1979. Distribution and environmental synchronization of the
marine insect, Halobates robustus, in the Galapagos Islands. Proceedings of the Ryal SmkQ of London, Series B,
206: 33-52.
BROOKS, D. R. & McLENNAN, D. A., 1991. Phylogeny, Ecology, and Behauiour. A Research Program in
Conparatbe Biology. Chicago: University of Chicago Press.
CALABRESE, D. M., 1980. Zoogeography and cladistic analysis of the Gerridae (Hemiptera: Heteroptera).
Miscellancm Publicatkt of the Entomological S h y of America, I 1 (5): 1-1 19.
CARPENTER, J. M., 1989. Testing scenarios: Wasp social behaviour. ClndistiCs, 5: 131-144.
CHENG, L., 1973a. Marine and freshwater skaters: Differences in surface fine structures. Nature, 242: 132-133.
CHENG, L., 1973b. Halobatcs. Oceanography and Marine Biology, Annual R&w, 11: 223-235.
CHENG, L., 1974. Notes on the ecology of the oceanic insect HaLobatcs. Marine Fisheries Ztcuim, 36 (2): 1-7.
CHENG, L. (Ed.), 1976. Marine Insects. Amsterdam: North Holland.
CHENG, L., 1981. Halobates (Heteroptera: Gerridae) from Micronesia with notes on a laboratory population
of H. mariannamm. Microncsica, 17: 97-106.
CHENG, L., 1985. Biology of Halobates (Heteroptera: Gemdae). Annual Rcmew of Entomology, 30: 11 1-135.
CHENG, L., 1989a. Factors limiting the distribution of Halobates species. In J. S. Ryland & P. A. Tyler (Eds),
Reproduction, Gmtics and Distribution of Marine Organisms: 357-362. Fredensborg: Olsen & Olsen.
CHENG, L., 1989b. Biogeography and phylogeny of the sea-skaters Halobates. Chinese Journal of Oceanology and
Limnology, 7: 233-239.
CHENG, L. & HILL, D. S., 1980. Marine insects of Hong Kong. In B. S. Morton & C. K. Tseng (Eds), The
Marine Flora and Fauna of Hong Kong and SouUrern China: 173-183. Hong Kong: Hong Kong University Press.
CHENG, L., DOUEK, M. & GORING, D. A. I., 1978. UV absorption by gerrid cuticles. Limnology and
Oceanography, 23: 554-556.
CHINA, W. E., 1957. The marine Hemiptera of the Monte Be110 Islands, with descriptions of some allied
species. Journal of the L k a n S h y , London, <oology, 40: 342-357.
CODDINGTON, J. A., 1988. Cladistic tests of adaptational hypotheses. Cladistics, 4: 3-22.
ESAKI, T., 1924. On the genus Halobates from Japanese and Formosan coasts (Hemiptera: Gemdae). Pvche,
21: 112-1 18, pl. 5.
ESAKI, T., 1930. Marine water-striders from the Corean coast (Hemiptera, Gemdae). The Entomologist's
MonMy Magazine, 65: 158-161.
ESAKI, T., 1937. A new Asclcpios from Japan. Mushi, 9: 135-136.
FARRIS, J. S., 1988. Hemig86 reference. Version 1.5. New York.
FARRIS, J. S., 1989. The retention index and homoplasy excess. Systematic <oology, 38: 406-407.
FITZHUGH, K., 1989. Cladistics in the fast lane. Review ofJ. S. Farris, Hennig86. Version 1.5. Jounrnl of the
New Tork Entomological So&& 97: 234-241.
FOSTER, W. A. & TREHERNE, J. E., 1980. Feeding, predation and aggregation behaviour in a marine
insect, Halobates robustus Barber (Hemiptera: Gerridae) in the Galapagos Islands. Proceedings of the Royal
Sociee of London, Series B, 209: 539-553.
FOSTER, W. A. & TREHERNE, J. E., 1982. Reproductive behaviour of the ocean skater Halobates robustus
(Hemiptera: Gemdae) in the Galapagos Islands. Oecologi~(Berlin), 55: 202-207.
FOSTER, W. A. & TREHERNE, J. E., 1986. The ecology and behaviour of a marine insect, Ha1obatesjjien.G
(Hemiptera: Gemdae). <oologiCal Journal of the Linnean SocieQ, w6: 391-412.
HEMING-VAN BATTUM, K. & HEMING, B. S., 1986. Structure, fbnction and evolution of the
reproductive systems in females of Hebrur pusillus and H. tujceps (Hemiptera, Gerromorpha, Hebridae).
Journal of Morphology, 190: 121-167.
HEMING-VAN BATTUM, K. & HEMING, B. S., 1989. Structure, function and evolutionary significanceof
the reproductive system in males of Hebrur pusillus and H. rujcejs (Heteroptera, Gerromorpha, Hebridae).
Journal of Morphology, 202: 281-323.
HERRING, J. L., 1961. The genus Halobates (Hemiptera: Gerridae). P m z Insects, 3: 223-305.
HERRING, J. L., 1964. A new species of Halobatcs from the Bay of Bengal. Proceedings of the Entomological Soncty
of Warlungton,66: 85-86.
IMMS, A. D., 1936. On a new species of Halobates, a genus of pelagic Hemiptera. The John Murray Expedition
193.%34, SmntjtiC RLfirts, &logy, 4 /1936-38]: 71-78.
JACZEWSKI, T., 1972. Geographical distribution of oceanic Heteroptera and the Continental Drift. Bulletin
a2 PAcadlmie Polonaise dcs Sciences, StriC dcs scintcCs biologiquc, 20: 415-417.
LINNAVUORI, R., 1971. Hemiptera ofthe Sudan, with remarks on some species of adjacent countries. I. The
aquatic and semiaquatic families. Annales <mlogici Fenmci, 8: 340-366.
PHYLOGENY O F H A L O B A T E S
55
LUNDBECK, W., 1914. Some remarks on the eggs and egg-deposition of Halobates. MindeskrEft for Japetus
Steenstrup, 2 (27): 1-13.
MALIPATIL, M. B., 1988. TWOnew species of Halobates Eschscholtz (Hemiptera: Gerridae) from Australia.
Journal of the Australian Entomological Society, 27: 157-160.
MATSUDA, R., 1960. Morphology, evolution and a classification of the Gerridae (Hemiptera-Heteroptera).
University of Kansas Science Bulletin, 41: 25-632.
MIYAMOTO, S., 1961. Hemiptera: Genidae. Insecta Japonica, Series 1, Parf 3: 1-39. [In Japanese.]
MIYAMOTO, S., 1967. Gerridae of Thailand and North Borneo taken by the Joint Thai-Japanese Biological
Expedition 1961-62. Nature and L$e in Southeast Asia, 5: 217-257.
MIYAMOTO, S. & SENTA, T., 1960. Distribution, marine condition and other biological notes of marine
water-striders, Halobates spp., in the south-western sea area of Kyushu and western area of Japan Sea.
Sieboldia, 2: 171-186. [In Japanese with English summary.]
NEWMAN, L. J. & CHENG, L., 1983. Chromosomes of five species of sea-skater (Gerridae-Heteroptera).
Genetica, 61: 2 15-2 17.
NELSON, G. & PLATNICK, N., 1981. Systematics and Biogeography. Cladistics and Vicariance. New York:
Columbia University Press.
PLATNICK, N., 1989. An empirical comparison of microcomputer parsimony programs, 11. Cladistics, 5:
145-161.
POLHEMUS, D. A,, 1990. Heteroptera of Aldabra Atoll and nearby islands, western Indian Ocean, Part 1.
Marine Heteroptera (Insecta): Gemdae, Veliidae, Hermatobatidae, Saldidae and Omaniidae, with notes
on ecology and insular zoogeography. Atoll Research Bulletin, 345: 1-16, 9 figs.
POLHEMUS, J. T., 1982. Marine Hemiptera of the Northern Territory, including the first fresh-water species
of Halobales Eschscholtz (Gerridae, Veliidae, Hermatobatidae and Corixidae). Journal of the Australian
Entornological Socieb, 21: 5-1 1.
I’OLHEMUS, D. A. & POLHEMUS, J. T., 1991. Distributional data and new synonymy for species of
Halobates Eschscholtz (Heteroptera: Gerridae) occurring on Aldabra and nearby atolls, western Indian
Ocean. Journal of the New rork Entomological Society, 99: 2 17-223.
POLHEMUS, J. T. & CHENG, L., 1982. Notes on marine water-striders with descriptions of new species.
PacljFc Insects, 24: 2 19-227.
SCHMIDT, H. E. & MOLLER, R., 1973. Marine water striders of the genus Halobates (Hemiptera: Gerridae)
from the Red Sea and Gulf of Aqaba. Israel Journal of <oology, 22: 1-12.
TREHERNE, J. E. & FOSTER, W. A,, 1980. The effects of group size on predator avoidance in a marine
insect. Animal Behaviour, 28: 1119-1 122.
TREHERNE, J. E. & FOSTER, W. A., 1981. Group transmission of predator avoidance behaviour in a
marine insect: the Trafalgar effect. Animal Behaviour, 29: 91 1-917.
WHITE, F. B., 1883. Report on the pelagic Hemiptera. Vyage of Challenger, Reports, <oology, 7: 1-82.
WILEY, E. O., 1981. Phylogenetics. The Theory and Practice of Phylogenetic Systematics. New York: John Wiley &
Sons.
APPENDIX
Annotated list of the characters used in the cladistic analysis of Halobates and Asclepios (Hemiptera: Gerridae)
(Characters with non-additive (unordered) states are marked with an asterisk (*). Species are referred to both
by names and by their numbers in the data matrix, Fig. 10).
Colour
0. Dorsal colour dark brown and yellow (O)/uniformly dark brown or black (I)/greyish or silverish (2).
Halobates mjobergi (taxon no. 0 ) , and Asclepios annandalei (27) and shiranui (28) are brown with yellow
markings like many freshwater halobatines (incl. Metroconr). Most species of Halobates are predominantly
dark brown or black. Owing to the extensive layers of hairs and microtrichia covering most of their body
surface (Cheng, 1973a; Andersen & Polhemus, 1976; Andersen, 1977), sea skaters usually appear greyish
or silverish when they are dry.
1. Head with extensive pale markings (O)/pale markings reduced to a crescent-shaped mark extending
forward toward the eyes (l)/pale markings reduced to a pair of basal spots (2).
In Halobates mjobergi (no. 0 ) , the dorsal surface of the head is yellow except for a central dark stripe.
Similar pale markings are found on the head of Ascleplos (nos 27-28), and in Halobates zephyrus (10).
Most species of Halobates have a crescent-shaped, pale marking at the base of head. In the open-ocean
species, g e m n u s (no. 4),sericeus (5), micans (7), splendm (8) and sobrinlrs (9), the pale markings are
reduced to a pair of small triangles.
2. Ventral surface of female with extensive pale markings (O)/pale markings restricted to abdominal
sternum (I)/ventralsurface uniformly dark (2).
Asclepios species and several species of Halobates (e.g. mjobergi) are more or less extensively pale on their
ventral body surface, especially in the female. This colouration is typical in freshwater halobatines (incl.
Metrocoris). The open-ocean species of Halobates, species nos 4-5 and 7-9, have an almost uniformly dark
ventral surface.
56
N. M. ANDERSEN
Head
3. Interocular width of head less than 3.6 x width of an eye (O)/subequal to or more than 3.6 X width of an
eye (1).
The ratio between the interocular width (greatest distance between eyes) and the width of an eye is used
to separate the open-ocean species from coastal species ofH
(Herring, 1961). Open-ocean species
have the interocular with over 4 times the width of an eye, while coastal species have a smaller ratio,
usually 3-3.5 times the width of an eye. However, the individual variation is relatively large as seen from
the following ratios between interocular width and width of a n eye in 10 males: H . germanus, mean value
4.6 (range 3.9-4.8); H. hayanus, mean value 3.4 (range 3.0-3.7). Besides, the open-ocean species
H. sobrinus has a ratio of 3.6 (range 3.4-3.7), thus approaching the state in coastal species.
4. Antennae relatively long, 3 or more the length of male body (O)/antennae shorter, 3 or 4 the length of
male body (1).
5. Fourth antennal segment distinctly longer than second segment (I)/subequal to or shorter than second
segment (0).
The short antennae, but relatively long fourth antennal segment, is characteristic of the open-ocean
Halobates species nos 4-5 and 7-9.
Thorax
6. Intersegmental suture between meso- and metanotum distinct, at least laterally (O)/suture indistinct or
reduced to lateral pits (1).
The dorsal, intersegmental suture between meso-, and metathorax is only traceable laterally in Asclepios.
In species of Halobaks, this suture is typically reduced to a pair of lateral, V-shaped pits.
7. Female meso-metanotum strongly raised (I)/not as before (0).
Although the meso-metanotum may be more or less convex in Halobates females, the species alluaudi
(no. 26) is the only one where the meso-metanotum is strongly raised.
8. Metasternum short but wide, almost reaching the metacetabula laterally (O)/metasternum reduced to a
small, triangular plate (1).
The metasternum is strongly reduced in halobatine water striders. In the Metrocorini, the metasternum
is reduced to a small triangular plate (Matsuda, 1960). I t is less reduced (more primitive) in Asclepios
and Halobates where it reaches the acetabula of the hind legs laterally. I t carries the scent orifice
medially. The metathoracic scent apparatus is well developed (Andersen, 1982: fig. 440).
Legs
9. Fore femur of male with a tubercle or spine on ventral margin (I)/not as before (0).
Ventral modifications of the male fore femur occur both in the two A s c l e ~ o sspecies examined
(nos 27-28) and in Halobates mjobngi (no. 0 ) ,although of a different nature. A reversed polarity ( 1 + 0)
of states is therefore suggested for this character.
10. Fore femur of male with a row of evenly spaced, dark bristles on ventral surfaces (O)/dark bristles near
.
base of femur inserted close together (1).
The primitive arrangement of bristles on the male fore fcmora is probably that observed in the Asclepios
species (nos 27-28), viz., two rows of evenly scattered, dark bristles. In some Halobates species, e.g.
fijieenris (no. 20), princeps (25) and alluaudi (26), the ventral row is reduced to a few, densely set, spinous
hairs near the base of femur.
11. Fore tibia of male with a spinelike process on inner margin (l)/without such a process (0).
Only the male of Halobates formidabilis (no. 3) has a prominent spine on the inner margin of the fore
tibia. It fits into a groove on the incrassate femur and is probably a device for grasping the female thorax
during copulation.
12. Apical process of fore tibia with small ‘file’ (l)/tibial process with large, padlike ‘file’ (2)ltibial process
without ‘file’ (0).
The ‘file’ is a pad of minute pegs or spines on the apical process of the male fore tibia. It was described
by Imms (1936) in Halobatesgmnus (as H. sewelli Imms), but I have found this structure in all species
of Halobates except mjobergi (no. 0). In some species, e.g. mariannarum (no. 19),jji& (20),galatea (22),
esakii (24),princeps (25) and alluaudi (26), the ‘file’ is rather conspicuous, subovate.
13. First segment offore tarsi distinctly shorter than second segment (O)/tarsal segments subequal in length
(I)/first segment distinctly longer than second segment (2).
The relative length of the two segments of the fore tarsus is an important taxonomic character in
Halobates (Herring, 1961). However, before using relative measurements, one must take into account
that different segmcnts often grow at different rates (allometry). In Gerridae, the length of the first tarsal
segment usually increases at a steeper rate than that of the second segment (Matsuda, 1960). By
comparing Halobates males of different size, it was observed that the fore tarsal ratio varies between 3.1
(maculufus, length 3.0 mm) and 0.6 (princeps, length 6.2 mm) as predicted. Thus, this character is of
doubtful value. There are, however, some deviating species. H. mjobergi has the largest ratio, 5.3,
although it is not the smallest species (3.6 mm). In that respect, mjobergi comes close to the species of
Asclepios which have a ratio of 5.4 (length 2.7-3.0 mm). The extremely short first segment of the fore
tarsus is probably the primitive state in the Halobatinae (shared with all freshwater species).
PHYLOGENY OF HALOBATES
57
14. Middle femur less than 1.1 x hind femur (O)/between 1.1 and 1.4 x hind femur ( 1)/more than 1.4 x hind
femur (2).
It was hypothesized that a relatively short middle femur as compared with hind femur was the most
primitive state in Halobatcs. However, since the two species of Asclepios are different in this respect, the
polarity of states is undecided for this character.
15. Middle tibia distinctly longer than hind tibia (O)/subequal to or shorter than hind tibia ( I ) .
The middle tibia is relatively short in some Halobates species, viz. sericeus (no. 5), micans (7) and
splendms (8).
*16. Only middle tibia with fringe of long hairs ventrally (I)/both middle tibia and tarsus with hair fringe
(2)lneither middle tibia nor tarsus with hair fringe (0).
One of the most distinct features of the legs of Halobates is a fringe of long hairs along the ventral surface
of the middle tibia and tarsus as illustrated by Andersen & Polhemus (1976) and Andersen (1982;
SEM-pictures). The hair fringe is usually collapsed in dried specimens and therefore not as distinct as in
liquid-preserved specimens. Since the two species of Asclepios have mesotibial hair fringes of different
structure, two alternative hypotheses of character evolution are suggested for this character. One
postulates that the hair fringe of the middle leg first evolved on the tibia of the Halobatini, later on the
tarsus in both Asclepios annandalei (no. 27), and in the species of Halobates except mjobergi (no. 0). The
other postulates that the hair fringe of the middle leg evolved simultaneously on the tibia and tarsus in
the Halobatini including Asclepios, but that the tarsal fringe was lost independently in shiranui (no. 28),
and in Halobates mjobergi (no. 0 ) . The number ofsteps is the same in both alternatives. Since convergent
loss seems more likely than convergent gain of structures, the last alternative is preferred.
17. Hair fringe of middle tarsus composed of hairs which are distinctly shorter than second segment of
middle tarsus (O)/hairssubequal to or longer than second segment of middle tarsus (1).
Already White (1883) noticed that coastal species of Halobates have mesotibio-tarsal fringes with shorter
hairs than open-ocean species like sericeuc (no. 5) and H . micam (7). This difference was excellently
illustrated by Miyamoto & Senta (1960). However, there are also differences among the open-ocean
species. The hairs of the tarsal fringes in gemanus (no. 4) and sobrinus (9) are relatively shorter than in
sericeus (5) and micans (7), although not as short as in the coastal species. In splendens (8), the mesotibial
hair fringe is reduced.
18. Hind tarsal segments fused (I)/tarsal segments more or less distinctly separated (0).
It was believed that the two-segmented hind tarsi of some Halobates species was the primitive state as
found in Metrocoris and most other gerrids. However, this implies that the hind tarsal segments have been
fused several times independently of each other. A more parsimonious explanation is that the twosegmented hind tarsi in some Halobates species represents a reversal.
Abdomen
19. Intersegmental sutures between all mediotergites distinct (O)/sutures between basal three mediotergites
obliterated except laterally ( 1 ) .
In Halobates, the basal three abdominal rnediotergites are fused with each other and with the thoracic
notum. Intersegmental sutures are usually only distinct laterally. In species of Asclepios (and most other
gerrids), all intersegmental sutures are more or less distinct.
20. Second and third laterotergites distinctly separated (O)/fused ( 1 ).
In most Gerridae, including Metrocoris, the second and third laterotergites are primitively separated by a
distinct suture. This state is found in Halobates mjobergi (no. 0 ) and Asclepios annandalei (27), while the
suture is indistinct or absent in other species of Halobatini. Although the character polarity is undecided
in the cladistic analysis, 1 maintain that convergent loss is more likely than convergent gain of the suture.
Male genital segments
(For explantion of terminology, etc., see the section on Genital morphology).
21. Segment 7 tubular prolonged, concealing segment 8 (O)/not modified as before (1).
In the male of Halobates Jijiensis (no. 20), the last genital segments are tubular prolonged, enclosing
segment 8.
22. Segment 8 longer than wide ( O ) / shorter than wide ( 1 ) .
In species of Asclepios the eighth segment of males is cylindrical, but longer than wide (Fig. 2A, S8) thus
resembling the structure found in most Gerridae (Andersen, 1982). The very broad eighth segment of
Halobates species (Fig. IB, S8) is probably derived &om this state.
23. Segment 8 with spiracular processes (I)/without spiracular processes (0).
24. Spiracular processes of segment 8 long, fingerlike (O)/processeslow, rounded ( 1 j.
The presence of spiracular processes on segment 8 is an autapomorphy for the genus Halobates. It is
therefore not possible to score any state for this character in the two species of Asclepios. It was
hypothesized that the evolution has proceeded from fingerlike to low and rounded spiracular processes.
However, following the cladistic analysis, the polarity of states is undecided for this character.
25. Segment 8 with dorsal margin produced, cove+g base of proctiger (O)/not produced ( I ) .
In males of the Asclepios species (and most other gerrids) the dorsal hind margin of segment 8 is
produced, covering the base of the proctiger. Most species of Halobates show a derived state where the
base of the proctiger is more or less exposed and sometimes swollen or tumose, e.g. in species nos 19-26.
N. M. ANDERSEN
58
26. Segment 8 without styliform processes (O)/with short and stout styliform processes (])/with long and
slender styliform processes (2).
The presence of styliform processes on the male segment 8 is a strong autapomorphy for the Halobatini.
The presence of short and stout processes in Asclcpos spp. (nos 27-28) (Fig. 2A, B) is probably the
primitive state.
27. Styliform processes widely separated at base (O)/processesmore or less arising from a common base (1).
The bases of the styliform processes are primitively widely separated as in Asclepios spp. (nos 27-28)
(Fig. 2A) and Hafobates mjobergi (no. 0 ) (Fig. 1B). The derived state, where the processes arise from a
common base has probably evolved twice, once in the Halobates species nos 10-14 and again in species
nos 15-26 (reversed in bryani, no. 16).
28. Styliform processes of about same length (O)/slightlydifferent in length (I)/of widely different lengths
(2).
*29. Styliform processes of about same length (O)/right process longest (l)/left process longest (2).
*30. Styliform processes subparallel or simply diverging (O)/one of the processes turned more outward ( I ) /
both processes turned to the same side (2).
From the symmetrically developed styliform processes of Asclcpios spp. (nos 27-28) (Fig. 2A), Halobates
mjobergi (no. 0 ) (Fig. lB), and a few other species, the styliform processes have become more or less
asymmetrically developed in most Halobates. This development, however, seems to have taken different
courses. In the species nos 15-26 the left process is longer than the right process, most distinctly so in
manammum (no. 19) andjEj;cnris (20). In species 1ikeJzpaviomhis(no. 6), micans (7) and s p l d n s (8), the
right process is the longest and the left process is turned outward, etc.
*31. Apices of styliform processes simple and straight (O)/apices slightly recurved (1 )/otherwise
orientated (2).
The styliform processes have recurved apices in Halobatas hqymus (no. 2) and fonnidabilis (3).
*32. Apices of styliform processes simple and pointed (O)/simplebut blunt (I)/otherwise shaped (2).
The styliform processes are short and robust with blunt apices in the two species of Asclepios examined
(Fig. 2A, B). Within Halobatts it was believed that the type of styliform processes with more or less
pointed apices was the most primitive one. However, the cladistic analysis suggest an alternative
polarization ( 1 + 0 + 2) of states.
*33. Apices of styliform processes simple, pointed or blunt (O)/widened (l)/boot-shaped (2)lsickle-shaped (3).
A great deal of variation in the apices of the styliform processes is observed in Halobates, e.g. apices
widened as in esokii (no. 24) and others, boot-shaped as in danuini (13) and peronis (14), and sickleshaped as inflauivnhis (6),micans (7) and splmdmr (8).
34. Proctiger subovate in outline (O)/penta- or hexagonate in outline, with distinct lateral extensions (1).
35. Proctiger subequal to or longer than wide (O)/distinctly shorter than wide (1).
36. Proctiger dorsally strongly tumose at base (l)/not as before (0).
37. Lateral extensions of proctiger rounded or subparallel (O)/distinctlyproduced, more or less pointed ( I ) /
fingerlike prolonged (2).
38. Lateral extensions of proctiger rounded or pointed (O)/subparallel (1).
The male proctiger of Halobates is typically pentagonate in dorsal outline, with distinct lateral extensions
(Fig. ID). This type has been diversified in different ways. The proctiger has (probably independently)
been shortened in H . maculatur (no. 1I and s o b r k s (9). The lateral extensions have been uroloneed
" and
fingerlike in sobrinUr (no. 9), &mini (13), and p o n i s (14), or expanded in manamrum (19),jjimtis (20),
princeps (25) and alluaudi (26).
39. Lateral extensions of proctiger with groups of dark spines (I)/without such spines (0).
Lateral groups of spines are found in Halobates hayanus (no. 2), f m i d a b i h , (3) and germanus (4).
40. Parameres present (O)/absent (1).
Most gerrid males have a pair of parameres. In Metrocoris (no. 29), the parameres are prominent
structures. In the Halobatini, parameres are only found in Hafobates mjobergi (no. 0 ) (Fig. 3B, pa).
Although the cladistic analysis suggests the alternative polarization ( 1 + 0), i.e. convergent gain of
parameres in mjobergi, I maintain that convergent loss in Asclepws and most Halobates species is more
likely.
\
I
\
I
Male phallus
(For explanation of terminology, etc., see the section on Genital morphology)
41. Vesical armature symmetrically developed (O)/more or less asymmetrically developed (1).
The vesical armature in Asclejios spp. (nos 27-28) (Fig. 4A) and Halobates mjobergi (no. 0 ) (Fig. 4B),
appears to be strictly symmetrical. This state is probably the primitive state within the Halobatini (as
well as in most other Gerridae). In all other Halobates species examined, the vesical armature is more or
less asymmetrically developed.
42. Dorsal sclerite of vesica with a hole in proximal half (])/with a hole in distal half (2)lwithout such a
hole (0).
The dorsal sclerite has a very characteristic, elongate or diamond-shaped hole in the Halobates species
nos 1-14 (Fig. 6E). Other species of Halobates (including mjobergi, no. 0 ) and Asclcpios spp. (nos 27-28),
have a non-perforated dorsal sclerite.
PHYLOGENY O F H A L O B A T E S
59
*43. Apical, recurved part of dorsal sclerite shorter than half length of dorsal sclerite (O)/longer than half
length of dorsal sclerite (I)/reduced (2).
*44. Apex of dorsal sclerite strongly enlarged (O)/widened but relatively small ( 1 )/reduced (2).
Most species of Halobates have a relatively long, distally recurved, dorsal sclerite which usually has its
apex more or less enlarged. The latter structure is also found in Asclepios annandalei (no. 27) (Fig. 4A).
The distal part of the dorsal sclerite is more or less reduced in Halobates regalis (no. 1 I ) , whiteleggei (12),
damini (13) and peronis (14).
*45. Vesica without basal sclerite (O)/with small basal sclerite (l)/with large basal sclerite (2).
The Halobates species nos 15-26 all have a basal, vesical sclerite (Fig. 6A, bs), a feature not found in
mjobergi (no. 0) or in Asclepios spp. (nos. 27-28).
46. Vesica with two pairs of lateral sclerites (O)/with only one pair of lateral sclerites (1).
The two pairs of lateral sclerites found in Asclepios anmndaln' (no. 27) (Fig. 4A) and Halobates mjobergi
(no. 0) (Fig. 4B) are also present in maculatus (no. 1) (Fig. 4C), and the species nos 15-26 (Figs 6A-D).
47. Lateral sclerites (first pair) of vesica with hook-shaped basal part (])/not as before (0).
The Halobates species nos 6-9 have lateral sclerites (first pair) with a characteristic, hook-shaped basal
part (Fig. 5A, B). This state is probably derived from a more simple, rodlike shape (Fig. 4A).
.48. Lateral sclerites (second pair) of widely different shape (I)/of about same shape (0).
Both pairs of lateral sclerites are symmetrically developed in Asclepios annandalei (no. 27) (Fig. 4A) and
Halobates mjobergi (no. 0) (Fig. 4B), which probably is the primitive condition (shared with Metrocoris,
no. 29). In the Halobates species nos 15-26, the sclerites of the first pair are of about the same size and
shape while the sclerites of the second pair usually are much smaller and/or of different shape
(Fig. 6A-D). Because the second pair of lateral sclerites is absent in Halobates species nos 2-14, this
character could not be scored for these species.
49. Vesica with accessory, apical sclerites (I)/without such sclerites (0).
Accessory, apical sclerites of vesica seem to be convergently developed in the Halobates species nos 6-9
(Fig. 5A, B, ac) and in robustus (no. 15) (Fig. 6B).
50. Ventral sclerite of vesica separated from dorsal sclerite (O)/fusedwith dorsal sclerite (1).
The ventral sclerite is completely fused with the base of the dorsal sclerite in the Halobates species
nos 1-14. Since the dorsal and ventral sclerites are separated in mjobergi (no. 0 ) (Fig. 4B) and Asclepios
annandalei (no. 27) (Fig. 4A), the fusion between the dorsal and ventral sclerites is probably derived.
*:)I Ventral sclerite band-shaped but not distinctly wider than dorsal sclerite (O)/distinctly wider than dorsal
sclerite (I)/ventral sclerite otherwise shaped (2).
The shape and relative length of the ventral sclerite of vesica is very variable within Halobates and it is
difficult to see any distinct trends. It is likely, however, that the relatively short and narrow ventral
sclerite of Asclepios annandalei (no. 27) represents the primitive state.
Fernale genital segments
(For explanation of terminology, etc., see the section on Genital morphology)
52. Female abdomen with a triangular pocket on venter receiving the abdominal end (l)/not modified as
before (0).
In the female of Halobatesjjiensis (no. 20), katherinae and salotae the abdominal sterna can be telescoped
into each other so that genital segments are bent downward and enclosed within a ventral pocket.
53. First gonocoxae relatively long, subequal to or longer than sternum 7 (O)/distinctly shorter than sternum
7 (1).
The gonocoxae (ventral parts of segment 8) are large and distinctly exposed behind the pregenital
abdomen in female Asclepios and in most species of Halobates. However, the gonocoxae seem to be
somewhat reduced in the open-ocean species nos 4-5 and 7-9.
'54. First gonapophyses with dense fringe of hairs along inner margin ( I )/with more sparsely set hairs (2)/
without hairs on inner margin (0).
In all females of Asclepios and Halobates examined the first gonapophyses have a fringe of long hairs along
their inner margin. These hair fringes are especially well-developed in Asclepios annandalei (no. 27), but
absent in Metrocoris (29).
55. Second gonapophyses with simple apices (O)/with distinctly hook-shaped apices (1).
Most female gerrids, including Metrocoris (no. 29), have second gonapophyses with lobate or rounded
apices. Asclepios annandalei (no. 27) and most species of Halobates have gonapophyses with very
characteristic, hook-shaped apices (Fig. 7C). It is most probable that the lobate apices found in micans
(no. 7) and splendens (8) represent a character reversal.
56. Apices of second gonapophyses with filiform outgrowth (O)/withoutfiliform outgrowth (1).
Both Asclepios annandalei (no. 27) and Halobates mjobergi (no. 0) have a filiform outgrowth (Fig. 7B, fi)
near the apex of each second gonapophysis. This structure was not observed in other species of Halobates
examined.
*57. Median lobes of second gonapophyses indistinct or absent (O)/medianlobes present, rounded (I)/median
lobes present, setiform (2).
The presence of median lobes on the second gonapophyses (Fig. 7B, ml) is probably the primitive state
60
N. M. ANDERSEN
in Halobatini (shared with Metrocoris). The setiform lobes of most Halobates (Fig. 7D) were probably
developed from the rounded type.
58. Proctiger broad, about as wide as long (O)/narrow, longer than wide (1).
The cladistic analysis implies that a relatively narrow female proctiger is the primitive state. This state is
also found in Metrocoris.
F d e &vMtrial comglex
(For explanation of terminology, etc., see the section on Genital morphology)
59. Gynatrial sac with sclerotized areas (O)/without sclerotized areas (1).
The single species of Metrocoris (no. 29) examined has a female gynatrial sac without sclerotizations. This
is probably the primitive state within the Halobatinae.
60. Gynatrial sac with permanent folds (I)/with extensive but not permanent folds ( 0 ) .
The gynatrial sac appears to be extensively folded in all species of Asckpios and Halobaks examined. In
some H a l h k s species, viz. lulymrur (no. 2) (Fig. 9B),gmnmcw (4), sniGnrr (5),&paviuntriS (6) (Fig. 9D)
and m i c m (7) (Fig. 9C), these folds seem to be more permanent.
*61. Vermiform appendix relatively short, with few coils (O)/long, with many coils (l)/very long,
band-shaped (2).
The cladistic analysis is ambiguous about the polarity of the states of this character which is also
weakened by the small number of species examined. The gynatrial sac in Asclepws annandalei (no. 27),
however, has a relatively short vermiform appendix with few coils. This might he the most primitive
state.
62. Fecundation pump with short and broad flanges (O)/with long and narrow flanges (])/as before but
flanges spinelike (2).
The flanges of the fecundation pump are quite narrow in all species examined. However, the pump
flanges of the Halobatcs species nos 5-8 are very characteristic (Figs 9 G D , pu), spinelike and curved.
Other charackrs
63. Wings present, at least in some adult individuals (O)/wings absent in all adults ( 1 ) .
Although thousands of individuals have been examined, no winged specimens have ever been recorded
for any species of Asclepios or Halobatcs. I t is therefore assumed that all species of these genera are
obligatorily flightless.