Diversity in mate-guarding types within the genus Anax

Diversity in mate-guarding types within the genus Anax
30. Juli 2012
113
Diversity in mate-guarding types within the genus Anax
(Odonata: Aeshnidae)
Andreas Martens 1, André Günther 2 and Frank Suhling 3
Biologie, Pädagogische Hochschule Karlsruhe, Bismarckstraße 10,
D-76133 Karlsruhe, <[email protected]>
2)
Institut für Biowissenschaften, Technische Universität Bergakademie Freiberg,
Leipziger Straße 29, D-09599 Freiberg, <[email protected]>
3)
Institut für Geoökologie, Technische Universität Braunschweig, Langer Kamp 19c,
D-38106 Braunschweig, <[email protected]>
1)
Abstract
Observations of non-contact guarding in Anax guttatus, A. immaculifrons, A. indicus, and
A. speratus are reported. In all four species males were observed following their mate and
hovering above her intensively during oviposition. As a result, the genus shows a high diversity in mate-guarding types, including contact-guarding (i.e., tandem oviposition), noncontact guarding and unguarded oviposition. A review on mate-guarding known to occur
in the genus Anax worldwide is also provided.
Zusammenfassung
Unterschiedliche Typen der Partnerbewachung während der Eiablage bei der Gattung
Anax (Odonata: Aeshnidae) – Vorgestellt werden Beobachtungen zur Bewachung der
Partnerin ohne festen Körperkontakt bei Anax guttatus, A. immaculifrons, A. indicus und
A. speratus. Bei allen vier Arten wurden die Männchen dabei beobachtet, wie sie ihrer
Partnerin am Gewässer folgten und während der Eiablage ausdauernd über ihr rüttelten.
Damit besitzt die Gattung Anax die gesamte Vielfalt im Partnerbewachungsverhalten nach
der Kopulation: die Eiablage im Tandem, die Bewachung ohne Körperkontakt und die unbewachte Eiablage. Eine weltweite Übersicht aller Vertreter der Gattung Anax und der von
ihnen bekannten Formen der Partnerbewachung wird präsentiert.
Introduction
In odonates males often guard their female partners from copulation with other
mates even after copulation and insemination. This behaviour offers benefits to
the guarding male by reducing sperm competition and ensuring his sperm fertiLibellula Supplement 12: 113-122
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Andreas Martens, André Günther & Frank Suhling
lizes the female’s eggs, as well as benefits to the female by reducing male harrassment during oviposition. Post-copulatory mate guarding in Odonata is represented by two different types: (1) grasping the female in tandem (contact guarding)
and (2) following and guarding the female without physical contact and driving
off other males (non-contact guarding). This phenomenom has been well-studied in the Libellulidae and the Zygoptera (for reviews, see Conrad & Pritchard
1992; Corbet 1999; Fincke et al. 1997; Waage 1984; for a recent approach, see
Schenk et al. 2004).
In the Aeshnidae, however, mate-guarding has only been reported occasionally
and in single species, mostly as tandem-guarding in the genera Anax (see below)
and Aeshna (especially A. affinis: Klein 1932; Utzeri & Raffi 1983). In the genus Anax most general publications or detailed descriptions of adult reproductive behaviour deal especially with cases of contact-guarding, as for example in
A. ephippi­ger, A. junius, A. papuensis, and A. parthenope (Young 1967; Miller
1983; Jacquemin & Boudot 1986; Rüppell & Hadrys 1987; Rowe 1988; Günther
& Mauersberger 1999). By contrast, in A. imperator the females strictly oviposit
unguarded and effectively repel males, which disturb them (Corbet 1957).
A single observation on A. immaculifrons by Busse (1993) in a faunistic paper
suggests that non-contact guarding occurs in the genus Anax. The first record was
considered as unreliable by many odonatologists, who remained unconvinced
even after additional proof was provided when that record was published as a
photograph in a renowned field guide (Kalkman 2006: 172).
Here we describe our own observations on non-contact guarding in Anax species
and review what is known about the mate guarding in the genus worldwide. Additionally, to obtain more details and a better overview, we reviewed the literature
and interviewed experts worldwide about their own unpublished observations of
ovipostion in Anax species.
Observations
Anax guttatus
Mahé, Seychelles; pond of 30 m x 25 m in the garden of the Allamanda Hotel
(04°46’36’’S, 55°31’23’’E), 18-viii-2004 (AM). – At 15:05 h local time (15:27 h
solar time), a tandem pair arrived at the pond, crossed the water and landed as a
tandem for oviposition in the emergent vegetation several times. After ca. 5 minutes in tandem the male released her and began guarding her without physical
contact while she continued oviposition. When the female changed oviposition
sites, the male followed her at a distance of 20-30 cm, flying slightly higher. Whenever she landed again, he hovered closely above her and started flying in narrow
circles, these becoming wider and wider in the course of time. In one instance he
rested above her on the same stalk. Within the first 10 minutes after releasing
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her, he defended the female successfully from one rival. After a total of 5 minutes
in tandem and 28 minutes of non-contact guarding she left the water with her
abdomen curved. The male did not interfere with her and continued to patrol the
pond.
More than 30 minutes before these observations, another pair of A. guttatus were
seen at this pond. Oviposition also occurred in tandem before he released her and
guarded her without physical contact. She moved oviposition sites several times,
during which time he lost sight of her. A rival male detected her, grasped her and
carried her in tandem, disappearing into a banana tree. It might be that both returned to the water and were the same pair described above.
Mahé, Seychelles, the same pond, 20-viii-2004 (AM). – At 14:07 h solar time a
tandem pair appeared at the same pond. During their first 11 minute long visit,
the female curled her abdomen to oviposit 23 times, generally for less than one
minute, once for 81 s. At 14:28 h the pair landed within a wider area of jumbled
emergent vegetation for a longer stay. After 4:01 minutes of continuous oviposition the male released the female, and flew in circles above her expelling one rival
male. He continued to fly over the site, attacked and grasped the female again, 34 s
after release. The pair formed a copulation wheel on the wing, ending in a tree
with a copulation duration of 10:59 minutes. Afterwards the pair returned to the
pond in tandem and resumed oviposition behaviour. After about 10 minutes they
left the water in tandem.
Thailand, Ban Bang Khaya Nai, flooded pit (08°43’57’’N, 98°14’30’’E), 9-iv-2009
(AG). – At 15.15 h local time an ovipositing female was observed inside an open
Typha reedbed. A male hovered continuously about 1 m above her. After 3 minutes the female changed sites and the male followed her immediately.
Anax immaculifrons
India, Pench National Park, small tributary stream of the Pench river
(21°38’15.67’’N, 79°13’34.41’’E), 13-xi-2008 (AG). – At 12.45 h local time a female
was ovipositing into roots in the rocky bank of a pothole of about 5 m diameter
wide. A male circled the pothole very low over the water and periodically hovered over or in front of the female for 5-120 seconds. Arriving rival males were
attacked immediately and driven off by short chasing flights (n = 3). After the territory owner was captured, the female resumed oviposition for 3 minutes. About
2 minutes later another male arrived at the site. He formed a tandem and carried
the female into the forest. 10 minutes later a female (the same individual?) was
laying eggs at the same site, again non-contact guarded by a male.
Anax indicus
India, lake west of Gondakhari (21°08’28.93’’N, 78°51’3.49’’E), 15-xi-2008 (AG).
– At 11:15 h local time a single male was patrolling, inspecting a shallow lagoon
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inside a floating Ipomoea stand by the lake shore. An arriving female was grasped
within a few seconds. The copulation wheel was formed in flight, and copulation completed in the Ipomoea mats after 4:30 minutes. Immediately afterwards
they separated, both partners flew up and the female began ovipositing into the
Ipomoea stems. The male followed her to several oviposition sites, flying 30-100
cm above or next to her. After 5 minutes of oviposition the female left the site
together with the guarding male.
Anax speratus
Namibia, Naukluft Mountains; spring-fed pool of 3 m x 4 m at the Olive Trail
(24°13’41.88’’S, 16°16’49.4’’E), 13-iv-2004 (FS). – On arrival at the spring, a pair
in copula was spotted but then disappeared immediately. However, after a few
minutes a female arrived, landed and started ovipositing. For most of the duration of the oviposition a male hovered 20-30 cm above her and followed her when
she changed sites. Non-contact guarded oviposition continued for about 10 minutes. The oviposition substrates were dead as well as living leaves of terrestrial
grass; no other vegetation was present.
Namibia, Naukluft Mountains; Tsams Ost Spring (24°15’16.2’’S, 16°06’34.2’’E),
13-iv-2004 (FS, together with participants of the pre-symposium tour of the
2007 Congress of Odonatology). – The site was a small stream, not more than
1 m in width and running, depending on year and season, along a stretch of about
500 m. Most parts of the stream were overgrown by reeds except for few open
areas, some of them kept so by Black Rhinoceros Diceros bicornis and other game.
On our arrival a pair in a copulation wheel was spotted. They flew up but remained sitting in a nearby bush. After about 10 minutes the pair separated and
both immediately flew to an open part of the stream, where the female began
ovipositing in floating reed stems. Again the male guarded the female by hovering
above her an a distance of 10-50 cm and following her when changing oviposition
sites.
Zambia, Lwamfumu River above Mumbuluma Falls (10°55’45.94’’S,
28°44’14.55’’E), 05-iv-2011 (AG). – At ca. 9:00 h local time a female appeared at
the observation site and began ovipositing into root masses, floating grass and
other plants. She changed sites frequently and disappeared from view several
times. At 9:22 h a male appeared patrolling along the stream. He grasped the flying female at 9:34 h. The mating took place in a tree near the bank but was not
clearly visible. Both individuals returned at 9:45 h to the stream bank and the
female started oviposition behaviour. She was guarded all the time by the male
hovering an a distance of 20-50 cm. An approaching male was driven off by the
guarding male at 9:53 h. Guarded oviposition was observed until 9:57 h, after
which both individuals left my field of view. On 12-iv-2011 a single unguarded
female of A. speratus was seen ovipositing at the same site for about two hours.
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Discussion
Adult Aeshnidae are strong-flying and wide-ranging insects. Therefore, the most
difficult problem is interpreting observations on their reproductive behaviour. As
a result, the general overview of reproductive behaviour in odonates has been
based mainly on observations of taxa other than Aeshnidae, such as Libellulidae
and Zygoptera (for reviews, see Waage 1984; Conrad & Pritchard 1992; Fincke
et al. 1997; Corbet 1999).
Our report confirms the observations of non-contact guarded oviposition of Anax
immaculifrons by Busse (1993). Furthermore, we describe non-contact guarding
in three other Anax species. In most of our observations, there is no doubt that the
observed males were the mating-partners. Due to the low density of individuals
and the open habitat, it was easy to observe that the males were accompanying
the females during ovipositon. As a consequence, one has to conclude that the
males were guarding their own mates as they were following them and protected
them from rival males. In two cases, in A. speratus and A. indicus, the sequence
from mating to oviposition was directly observed, so that it is certain that the
mating male was the guarding one. In one case in A. guttatus the phase of noncontact guarding lasted only about 30 s before the uncoupled male-grasped the
female again. This case may show the limitation of the non-contact guarding system, suggesting that the guarding male also needs specific landmarks or an open,
clearly defined habitat to relocate his mate once separated.
The observations on A. guttatus show that there is a high plasticity of guarding
behaviour in that species. Tandem-oviposition and non-contact guarding may
appear in the same pair in the sequence (1) tandem-guarding, (2) non-contact
guarding. That sequence is also known from the libellulid genera Sympetrum
(Uéda 1979; Singer 1987), Pantala (AM unpubl.) and Zygonyx (Martens 1991).
Unguarded oviposition takes place in these genera as well.
The genus Anax includes at least 29 extant species worldwide (Tab. 1). According
to Peters (2000), Anax including Hemianax forms a well-defined monophyletic
group. In two thirds of species, some reproductive behaviour has been observed
(Tab. 1). However, more detailed systematic studies have not been made. Therefore there is a considerable potential to gain new insights into their mating systems. The compilation in Table 1 shows that all three types of mate guarding are
present in the genus Anax. Whereas in nine species so far only unguarded oviposition has been observed, six species perform tandem oviposition and four practise
non-contact guarding. Anax guttatus was the only species in which a switch in
behaviour has been observed, although we have no doubt that in most species a
change from contact or non-contact guarding to no guarding might occur, especially towards the end of the oviposition.
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Andreas Martens, André Günther & Frank Suhling
Table 1. Extant Anax species of the world, with a comparison of their known mate-guarding behaviour during oviposition. Crosses indicate that the respective guarding behaviour
was observed at least once. The category ‘no guarding’ is likely present in all species. Here
we only list species under this category if no other guarding behaviour has been observed.
– Tabelle 1. Die Liste der bekannten Anax-Arten der Welt, mit einem Vergleich ihres Partnerbewachungsverhaltens durch das Männchen während der Eiablage; ENG Exclusively no
guarding, grundsätzlich ohne Bewachung; NCG Non-contact guarding, Bewachung ohne
Körperkontakt; CG Contact guarding, Eiablage im Tandem.
Species
ENG NCG CG References
Anax amazili (Burmeister, 1839)
x
x Esquivel (2006),
W. Piper unpubl.,
J. Hoffmann unpubl.
Anax bangweuluensis Kimmins, 1955
Anax chloromelas Ris, 1911
Anax concolor Brauer, 1865
Anax congoliath Fraser, 1953
Anax ephippiger (Burmeister, 1839)
x
Anax fumosus Hagen, 1867
x
Anax georgius Selys, 1872
Anax gibbosulus Rambur, 1842
Anax guttatus (Burmeister, 1839)
x
x
x
Anax immaculifrons Rambur, 1842
Anax imperator Leach, 1815
Anax indicus Lieftinck, 1942
Anax julius Brauer, 1865
Anax junius (Drury, 1773)
Anax longipes Hagen, 1861
Anax maclachlani Förster, 1898
Anax mandrakae Gauthier, 1988
Anax nigrofasciatus Oguma, 1915
Anax panybeus Hagen, 1867
Anax papuensis (Burmeister, 1839)
Libellula Supplement 12: 113-122
x
x
x
(x)1
x
x
x
x
x
x
x
Distribution
S & Central America, Texas
and Florida to Brazil,
Galapagos Isl.
Central Africa
Africa from Sierra Leone
and Uganda to Zambia
and Mozambique
Paulson (2009)
Texas to Brazil
Congo Basin
Miller (1983), Jac- Africa, W Palaearctic
quemin & Boudot
(1986), Günther
& Mauersberger
(1999)
AG unpubl –
Asia from Japan to
ssp. celebense
Indonesia
Timor
A.G. Orr unpubl.
Australia
this study,
Seychelles to Japan and
Orr (2001)
N Australia, Pacific Islands
Corbet (1999)
S/SE Asia to E Mediterra­
nean
Corbet (1957)
Africa, W Palaearctic
this study
India, Sri Lanka
Peters (1987)
E Asia
Young (1967)
North America
Paulson (2009)
E United States
New Guinea,
Bismarck Archipelago
Madagascar
K. Wilson unpubl. Himalaya to Japan
K. Wilson unpubl. Japan to Myanmar and
Indonesia
Rowe (1988)
Australia, New Zealand,
New Guinea, Indonesia
Diversity in mate-guarding types within the genus Anax
Species
119
ENG NCG CG References
Anax parthenope (Selys, 1839)
Anax pugnax Lieftinck, 1942
Anax selysi Förster, 1900
Anax speratus Hagen, 1867
Anax strenuus Hagen, 1867
Anax tristis Hagen, 1867
x
Anax tumorifer McLachlan, 1885
Anax walsinghami McLachlan, 1882
x
Distribution
x Miller (1983)
x
Palaearctic
New Guinea
New Guinea
this study
Sub-Saharan Africa, Arabia
Hawaii
AM, AG, FS unpubl. Sub-Saharan Africa,
Madagascar
Madagascar
R. Novelo-Gutierrez California and Texas to
unpubl.
Honduras
There exists a description of a single tandem-oviposition in A. imperator (Balança & Visscher 1989).
We regard this as a rare exception. It is common knowledge among odonatologists in Europe that
females of A. imperator oviposit alone.
1)
All Anax species that are known to show migratory behaviour (sensu Corbet
1999: 408) – A. junius, A. parthenope, A. julius, A. ephippiger, and A. papuensis –
oviposit in tandem, and A. guttatus switches between contact and non-contact
guarding. All these species may occur in high densities at the oviposition site
when migrating swarms arrive. The high intensity guarding may be an adaptation
to temporary high densities at oviposition sites. At least two of the non-contact
species, A. immaculifrons and A. speratus, are typical running water species. Most
probably, non-contact guarding is highly efficient at streams. Males are able to
drive off rivals by chasing flights. Presumably this would be much easier along
a linear habitat than on a broad lake were rivals would approach from all directions. In species that do not guard, individual males often dominate a pond temporarily, such as A. imperator and A. tristis. Interestingly, in A. imperator females
are able to repel males very effectively.
Besides the male’s benefit of protecting his mate against rivals and sperm removal, there are some specific clues which may help us also understand the female’s
perspective by being guarded. The females within the genus Anax, as in some
other aeshnid species, often have damaged, dented compound eyes. This damage
is caused by the male’s epiproct (Ris 1910; Calvert 1920; Dunkle 1979) when
the female is being grasped by the male. In general, this damage may occur during
pre-copula, when the male grasps the female, during the copulation wheel, and
also in post-copula tandem. The amount of damage should increase especially
during oviposition in tandem, when both mates have to synchronously change
oviposition sites several times. What could be the female’s strategies to reduce
the risk of, or the trade-off from eye damage? One option may be for females to
have a smaller body size and mass which may reduce the mechanical stress in
the tandem-linkage. The alternative trend would be the size extension in cases
without tandem guarding. We suppose that the larger body size and mass in fe-
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Andreas Martens, André Günther & Frank Suhling
males may be helpful in effectively repelling males. As known so far, the very large
species in Anax, such as A. tristis and A. walsinghami, do not show mate guarding.
The genus Anax is a phylogenetic young and modern clade within the Aeshni­dae
(Peters 1987, 2000). The members are persistent long-distance fliers (Peters
2000) and have a high dispersal ability. Most species have the potential to colonise
a wide variety of habitats and have a short life-cycle, compared to other aeshnids
(Corbet et al. 2006). They are even successful in arid areas, which are otherwise
dominated by libellulids (Suhling et al. 2003). The ability of Anax females to deposit their eggs in the smallest piece of plant tissue (A. imperator: many observations from rock pools in the Mascarene Islands and Namibia; AM unpubl.), or wet
soil (A. ephippiger: Miller 1983) reduces the limitations of endo­phytic oviposition. The tendency to be a habitat opportunist is indicated in the diversity and
flexibilty of reproductive behaviour. On one hand, we suppose that sexual conflict
is a driver for an opportunistic choice of habitat, when females swerve to sub-optimal habitats to avoid male harassment. Anax amazili females were observed ovipositing without guarding males in suboptimal (saline) habitats, whereas in typical habitats they were guarded (J. Hoffmann pers. comm.). Females may seek such
suboptimal habitats as a trade-off for not being bothered by males. On the other
hand, opportunism needs behavioural adaptations to the wide range of population densities, caused by the high variance in breeding success in time and space.
The genus Anax shows high variabilty in reproductive behaviour. To our knowledge it is the only genus of the Aeshnidae in which all three types of guarding occur. We suggest that intense guarding may be finally associated with the various
effective densities that prevail at the oviposition habitat in the different species.
No guarding may indicate that the females have evolved effective repellent behaviour. In such a species guarding may occur never or very rarely. In species that
otherwise show intense guarding, no guarding may be observed when females
avoid male harassment by selecting suboptimal habitats and opportunistic choice
of a wide spectrum of waters. However, it is far too early for conclusions. On the
one hand, more detailed observations on guarding behaviour are needed, as well
as information about female male-repelling behaviour, preferably in all species of
Anax. On the other hand, a phylogeny to the species level is required to assess the
phylogenetic background of the guarding behaviour.
Acknowledgements
Günther Peters had an enormous impact on the development of our scientific
style and work. Therefore, we are proud to have a birthday present in his special
field. We would like to thank Rodolfo Novelo-Gutierrez, Joachim Hoffmann, Jens
Kipping, Albert G. Orr, Werner Piper and Keith Wilson for their information on
Anax behaviour. Special thanks to Albert G. Orr for comments on the manuscript
and improving the English.
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121
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