Reproductive Behavior of Ground Weta (Orthoptera: Anostostomatidae): Drumming Behavior, Nuptial Feeding, Post-copulatory Guarding and Maternal Care

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Reproductive Behavior of Ground Weta (Orthoptera:Anostostomatidae): Drumming Behavior, Nuptial Feeding,Post-copulatory Guarding and Maternal CareAuthor(s): Darryl T. GwynneSource: Journal of the Kansas Entomological Society, 77(4):414-428. 2004.Published By: Kansas Entomological SocietyDOI: http://dx.doi.org/10.2317/E-34.1URL: http://www.bioone.org/doi/full/10.2317/E-34.1

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Reproductive Behavior of Ground Weta(Orthoptera: Anostostomatidae): Drumming Behavior,

Nuptial Feeding, Post-copulatory Guarding andMaternal Care

DARRYL T. GWYNNE

Zoology Department, University of Toronto at Mississauga,

Mississauga, Ontario Canada L5L 1C6

ABSTRACT: Compared to other ensiferan Orthoptera such as true crickets (Gryllidae) and katydids

(Tettigoniidae) relatively little is known about the reproductive behavior of Anostostomatidae

(formerly Stenopelmatidae), the king crickets, weta and allies. Moreover, although the New Zealand

species (the weta) are best known, there is little knowledge of the biology of ground weta

(Hemiandrus species), a variable genus especially with regard to ovipositor length. This paper

presents observations of mating and post-mating behavior of several Hemiandrus species with short

ovipositors. Sexually active males and females drum their abdomens on the substrate, apparently as

local signals for mate attraction (pheromones may be involved in long distance communication).

After mating there is both maternal and paternal investment. Females provide care to eggs and young

larvae and males provide a spermatophylax to the female, a mating meal that, in other ensiferan

Orthoptera can be an important source of nutrition. In contrast to other ensiferans, however, the

spermatophylax of Hemiandrus species with short ovipositors is deposited on the female’s abdomen,

a separate location from the sperm ampulla. The spermatophylax is deposited while the male is

attached to the female’s underside, apparently to her modified 6th abdominal sternite. Also, in

contrast to related taxa, males remain with their mates while the mating meal is eaten. These

observations indicate that ground weta are excellent systems for examining behavioral and ecological

questions about the evolution of complex signals, as well as the evolution of maternal and paternal

investment.

KEY WORDS: Hemiandrus, parental investment, mating behavior, communication

‘‘The act of discovery is one of the greatest of joys;it is a bright flash in the darkness, with a rewardnot soon forgotten.’’H. E. Evans: 1993 Preface to Life on a Little Known Planet

Ensiferan orthopterans are model systems for studies of reproductive behavior. Most

work has focused on species in the families Gryllidae (true crickets) and Tettigoniidae

(katydids and bush-crickets) because of their elaborate acoustical signals or mating

behavior (Ewing, 1989; Bailey, 1991; Otte, 1992; Zuk and Simmons, 1997; Gwynne,

2001). Families closely related to tettigoniids (Gwynne, 1995; Flook et al., 1999;

DeSutter-Grandcolas, 2003) include Jerusalem crickets of North America and other

Stenopelmatidae (Weissman, 2001), as well as Anostostomatidae, a group found mainly in

the Southern Hemisphere and formerly included in the Stenopelmatidae. Anostostomatids

include king crickets of South Africa, and Australia and the weta of New Zealand (Johns,

1997). There is some information on the reproductive habits of some species (Field, 2001)

mainly those taxa of very large size or possessing elaborate weaponry used in combat

between males. The list includes king crickets (Bateman and Toms, 1998b; Monteith and

Field, 2001; Toms, 2001), and both giant weta (Deinacrida spp.) and tree weta (Hemideinaspp.) of New Zealand (subfamily Deinacridinae).

Accepted 25 March 2004; revised 11 August 2004

� 2004 Kansas Entomological Society

JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY77(4), 2004, pp. 414–428

Ground weta in the genus Hemiandrus are a third major group of New Zealand

Anostostomatidae (Johns, 1997; Gibbs, 2001). These weta are typically small species that

burrow in soil (see Barrett, 1991). Salmon (1950) recognized two genera, Hemiandrus and

Zealandosandrus, partially on the basis of a very short ovipositor and a modified 6th

abdominal sternite of females in the species he assigned to Hemiandrus. Johns (1997)

placed all species into Hemiandrus, a decision supported by a preliminary phylogenetic

analysis (Gerber, 1996). Despite the species diversity and the abundance of ground weta in

many areas of New Zealand (Johns, 2001), little is known about the bionomics of these

insects as indicated by a paucity of information about them in a recent volume on the biology

of Anostostomatidae (Field, 2001). Some observations on the behavior of ground weta have

appeared in unpublished theses and government monographs. These reports contain a few

notes on mating behavior before sperm transfer (in H. (formerly Zealandosandrus)subantarcticus: Cary, 1981), and suggestions that mating can take place either inside or

outside of burrows (Barrett, 1991; Cary, 1981). There is also evidence that vibratory sounds

are produced during courtship in H. (formerly Z.) subantarcticus (Butts, 1983) and H.(formerly Z.) maculifrons (Cary, 1981). Airborne sound communication by ground weta

seems unlikely, however, because these insects do not possess the tibial tympanae used by

singing ensiferans, including deinacridine weta (Field, 2001). Finally, there are several

references to female ground weta remaining with eggs and nymphs in subterranean

chambers (Salmon, 1950; Wahid, 1978; Barrett, 1991; van Wyngaarden, 1995).

Interestingly, several Hemiandrus species with long ovipositors (formerly Zealandosand-rus) do not show this sort of maternal care (Cary, 1981; Butts, 1983; and Gwynne, unpubl.).

In the present paper I provide detailed observations on mating and maternal behavior of

H. pallitarsis and several other ground weta species with short ovipositors.

Taxonomy of Ground Weta

In his synonomy of the genus Hemiandrus, Johns (1997) listed seven described species

(of which five were formerly in the genus Zealandosandrus). Later, Johns (2001) added 28

undescribed species of Hemiandrus, placing their species names in quotes while

disclaiming these names as ‘‘not available’’ as per Article 8.3 of the International Code

of Zoological Nomenclature (1999). In lieu of formal species names, which will appear in

forthcoming taxonomic descriptions (see Johns, 2001), when referring to undescribed

species I follow Johns’ usage of names in quotations.

Methods

Hemiandrus pallitarsis (formerly H. furcifer Walker) is a widespread species on New

Zealand’s North Island (Johns, 2001). I observed mating or newly-mated females of this

species during January 1994, 1997, 1998, 2000 and 2002 on low vegetation in two suburban

gardens in Palmerston North, and in a site with native forest at Kiriwhakapapa. Both sites are

within the reported geographical range forH. pallitarsis (Salmon, 1950; Johns, 2001). In fact,

no other Hemiandrus species has been recorded from the region encompassing these two

sites (Johns, 2001). Some individuals from Palmerston North were moved to the laboratory

and allowed to establish burrows in three large terraria in 1994 and a further three in 2002

(each terrarium measured 420 3 420 sm 3 270 cm high and contained no more than 6

individuals). Terraria were located in an outdoor garden hut (at ambient outdoor

temperatures). Each was partially filled with soil to allow the insects to burrow. In 1994,

VOLUME 77, ISSUE 4 415

individual male H. pallitarsis were housed in 175 ml plastic yogurt containers with screen

tops and no soil.

Most observations on other species (all undescribed species from the South Island (see

Johns, 2001 for geographical distributions)) were made in the laboratory, using the same

size of terraria described above (one terrarium per species, using individuals collected

during 2002 either from leaves or from baits of oatmeal placed on the ground). Collected

specimens included: H. ‘‘onokis’’ (distributed in the Puketeraki Mountain Range and

southern part of the Kaikora Ranges) from forest on the Jollies Pass Road, Hamner Springs

(collected on 22 January 2002); H. ‘‘promontorius’’ from its only known locality at

Marfell’s Beach north of Cape Campbell (24 January 2002); and H. ‘‘vicinius,’’ distributed

throughout the Marlborough Sounds area, from the Whites Bay-Rarangi track near

Blenheim (25 January 2002). Finally, a few observations were made in the field for two

South Island species: H. ‘‘vicinius’’ on Maud Island (8–12 April 2003); and H.‘‘peninsularis’’ (‘‘horomaka’’ in Johns, 2001), a species from the Banks Peninsula. H.‘‘peninsularis’’ were observed in bushland (27 January 1997) at Mt. Vernon, Akaroa.

In early July 1994 and on 14 June 2002, I excavated each individual female H. pallitarsisthat had dug a brood chamber in laboratory terraria in New Zealand. Large terraria were used

in 1994 whereas in 2002 only females of H. ‘‘onokis’’ and H. ‘‘vicinius’’ dug brood

chambers in large terraria. In 2002 female H. pallitarsis excavated brood chambers in

individual large plastic pots (20 cm high36 cm diameter) with screen lids and 15 cm of soil.

In both 1994 and 2002, each female and her eggs were subsequently transferred into an

artificial brood chamber made from potter’s clay approximately the size and shape of the two

half shells of a hollow walnut. The clay had initially been allowed to dry but was kept moist

by spraying with water. A female and brood were placed into one clay half shell, the other

half shell was used as a cover and the seam was sealed with wet clay. Clay chambers were

placed on moist vermiculite in a 7 cm diameter (3 8 cm high) plastic jar in a constant

temperature room at the University of Toronto and maintained at a constant 188C in 1994,

and in 2002 at 108C until 12 September when the temperature was raised to 148C (the

temperature regime in 2002 was selected to better approximate New Zealand winter

conditions). In 2002 I examined the contents of brood chambers once per month until the

first larvae hatched in late August, after which chambers were inspected 2–3 times per week.

Behavioral Methods

Mating behavior was observed directly in all years except 2002 and 2003 when I used

a Sony 420 digital video camera in complete darkness using the infra-red ‘‘night shot’’

feature to record not only mating but also maternal behavior. Maternal behavior was

videotaped within newly excavated brood chambers as well as in artificial brood chambers

(with the camera lens directed at a microscope slide window inserted into a cut-out section

of the chamber wall).

Recording and Analysis of Drumming

I analysed video recordings from 2002 (in which abdomen movement rate, length of

movement trains and between train intervals were measured by slowing video to half speed

during playback). Differences between species were statistically analysed using Kruskal-

Wallis tests. In 1994 I recorded vibrations of males housed in plastic containers using

a Sony electret condenser microphone (ECM T-140) connected to a Sony WM-D6C

Stereo Cassette-Corder. Recordings were analysed by bandpass filtering (40–3500 Hz)

416 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

through a Krohn-Hite filter (#3382) and then fed into a Tucker-Davis Technologies (TDT)

analog-digital converter where they were amplified by 40 dB. The samples were then

digitized by the TDT converter using custom written software. Once digitized, recordings

were imported into analysis software (DADiSP 3.01, DSP Development Corp.).

Three drumming bouts were analyzed in DADiSP (two from one male and one from

another). The following parameters of the signal were measured: 1) Total drumming bout

duration (seconds), 2) Number of pulses within a drumming bout, 3) Number of

oscillations within one pulse (median value), and 4) Inter-pulse interval (seconds).

Results and Discussion

Pair-Formation and Premating Behavior

After sunset, I occasionally observed individual H. pallitarsis on the ground where they

had apparently just emerged from burrows, but adults of both sexes in the four main

species studied as well as H. ‘‘horomaka’’, were most common perched alone on leaves

such as kawakawa (Macropiper excelsa, found in both native and garden vegetation) and

also on broad leaves of garden vegetation, and on ferns (at Kiriwhakapapa). All matings

were also observed on leaves indicating that perched individuals may signal from these

locations to attract mates. There are two likely modes of sexual communication in ground

weta. First, the insects may use pheromones to detect each other over long distances

(pheromone communication is known in an African anostostomatid: Bateman and Toms,

1998). A possible source of pheromone communication in ground weta is from anal

secretions. I noted a male H. ‘‘promontorius’’ depositing a spot of brown liquid on the

substrate. For H. pallitarsis, the species for which I have field observations of mating,

similar brown droplets were frequently seen on the tops of leaves in areas where the weta

were mating. These droplets emitted a strong foul odor and may mediate chemical

attraction of mates. However, as the insects were commonly observed perched on leaves,

a more localized form of communication to bring the sexes together in ground weta are

vibratory signals conducted through the plant substrate (see Bell, 1980). To investigate this

possibility, I observed for five minutes focal individuals perched on leaves. Observations at

Palmerston North using a headlight with a red filter of 21 males and nine females (in 1997

and 1998) showed a single male drumming his abdomen onto the substrate. To exclude the

possibility that red light disturbed many of the insects sampled, in 2002 I videotaped five

minute samples of four males and six females on leaves at Palmerston North using infra red

night shot: three of four males and two of six females drummed their abdomens. One of the

females was videotaped in an apparent drumming dialogue with a male; he moved to her

leaf and she attempted copulation and was eventually rejected by the male.

I also observed males in laboratory terraria drumming on leaves and occasionally on the

soil surface. Although I could not hear most of the field and laboratory incidences of

drumming on soil or leaves, these signals were audible each night from many of the males

housed individually in plastic cups (apparently due to amplification of drumming

vibrations by the plastic).

Video analysis of abdomen movement during drumming by field and laboratory males

in 2002 reveal significant differences between species in number of abdomen hits of the

substrate in a train of hits and the length of this train (see Fig. 1; Table 1). The intervals

between trains of abdomen hits also appear to be different; this parameter was not analysed

statistically because sample sizes were small. Differences between species do not appear to

be a result of different recording conditions such as differences in temperature: all


recordings were made in the same sized terraria inside a garden hut in Palmerston North.

Furthermore, drumming parameters from video recordings for all four species conducted

over a one hour period one evening were not obviously different from the overall medians

for drumming parameters (see Table 1).

Video analysis of the single female H. pallitarsis observed drumming apparently in

response to a male (see above) showed the drumming pattern to be different from

conspecific males in that there were no long intervals between drumming bouts. Female

drumming consisted of 23 rapid bouts of drumming in which each bout consisted of 6–8

hits of the substrate. The interval between each train of hits was 2.2 sec (mean).

Drumming bouts for solitary H. pallitarsis recorded from plastic cups (Fig. 1, all from

Palmerston North) were 1.51 long for one male and 4.23 and 4.73 sec for the second. The

lengths of drumming bouts were consistent with lengths of the bouts of abdomen

movements from video analysis for this species (Table 1). Each drumming bout contained

8 (male 1) and 20 or 24 pulses (male 2): the latter male’s pulse number is consistent with

number of abdomen movements observed in video analysis of males of this species (Table

1). The number of oscillations within a pulse (a mean determined for each) was 3 (male 1)

and 3.5 and 4 (male 2) and the inter-pulse interval (a mean determined for each bout) were

0.083 (male 1), and 0.089 and 0.092 sec (male 2).

Finally, drumming behaviors appear to occur only as pre-mating signals; I saw no rapid

abdomen movements during or after copulation.

Fig. 1. Time–amplitude trace of a single drumming bout by a H. pallitarsis male. The top trace shows a single

train of pulses recorded from a drumming male and the bottom trace, two pulses from within the bout showing

three oscillations per pulse.


Copulation

I recorded the details of copulation for a number of laboratory and field matings for

Palmerston North H. pallitarsis and for H. ‘‘onokis.’’ The copulation position was typical

of ensiferans in the closely related families Tettigoniidae, Haglidae and Stenopelmatidae,

as well as other anostostomatids (Brown and Gwynne, 1997) with the female mounted

above the male (achieved either by the male backing up (Barrett, 1991) or by the female

mounting the male). However, in contrast to these other ensiferans, the male H. pallitarsisdoes not curl up behind the female during the transfer of the spermatophore. Instead the

pair remained in the initial mounted position while the male directed the tip of his

abdomen upwards and forward to attach an ampulla with two sperm chambers to the tip of

the female’s abdomen (typical of the related Stenopelmatidae, Tettigoniidae and Haglidae:

Gwynne, 1995). From the observations of H. pallitarsis from 1994 to 2000, ampulla

attachment to the female occurred a median 3 min (range 2–4 min, N¼ 5) after the initial

mount (Gwynne, 2002). Ampulla attachment occurred after 8 min in the one field

observation. The transfer of an ampulla was quickly followed by the uncoupling of the

male’s genitalia from the female’s primary genitalia after which he moved his genitalia

forward on her underside and attached his genitalia to her mid-abdomen, apparently

coupling with her modifed 6th abdominal sternite, an elbowed, elongate accessory organ

(Gwynne, 2002). While in this position he deposited a spermatophylax on this ventral part

of her abdomen (Gwynne, 2002).

A more detailed analysis of copulations was conducted from videotaped matings in 2002

for several Hemiandrus species. For two field and two laboratory H. pallitarsis and one

laboratory H. ‘‘onokis’’, video recordings showed that the dorsal part of the male genitalia

were attached to the female’s mid abdomen (6th sternite region) at the beginning of

copulation. This important detail was not detected in a previous observational analysis of

copulation in H. pallitarsis (Gwynne, 2002). The male then remains attached to her mid

abdomen while the ventral parts of his genitalia stretch back to couple with the female’s

primary genitalia. The male’s subgenital plate then drops and his paired phallus is extruded

a median 46 sec (n¼2 field) and 74 sec (n¼2 laboratory) after the start of copulation in H.pallitarsis and 45 sec after the start in the H. ‘‘onokis’’ laboratory mating. The paired sperm

ampullae of the spermatophore were then attached to the female 22 sec (median: n ¼ 2,

field) and 42 sec (n¼ 2, laboratory) later in H. pallitarsis and 31 sec later in H. ‘‘onokis.’’

For H. pallitarsis 117 sec (n ¼ 2, field) and 167 (n ¼ 2, laboratory) after the start of

copulation the male disconnected from his mate’s primary genitalia and the tip of his

Table 1. Parameters of the male drumming movements in four Hemiandrus species. The table shows overall

medians and ranges for the means of each drumming parameter calculated for each male. Numbers in parentheses

are medians for data from males of all four species video taped in a one hour period on February 8 2002. Sample

size¼7 for pallitarsis (five in terraria, two in field) number of drumming hits and length of train of hits; and n¼3

for all other variables except ‘‘promontorius’’ where n ¼ 1 for all three variables. All recordings of ‘‘onokis,’’

‘‘vicinius’’ and ‘‘promotorius’’ were in terraria.

Species Number of hits in a train Length of train Between-train interval

pallitarsis 20 (22), 18–21 5 (5), 4–6 sec 69.5, 54–85 sec

‘‘onokis’’ 11.3 (12.5), 8.7–12.5 3 (3), 2–3.1 sec 10.6, 4.8–16.4 sec

‘‘vicinius’’ 8.1 (8.3), 7–8.6 1.1–1.8 sec 6.1, 3.4–8.8 sec

‘‘promotorius’’ �7.8 �2.8 �15.3

K–W test 11.14, P ¼ 0.01 11.3, P ¼ 0.01


abdomen dropped back to remain attached to her mid abdomen where 145 sec (n¼3, field)

and 111 sec (n¼ 2, laboratory) later his elongated paired phalli deposited the two lobes of

a spermatophylax onto the ventral side of her abdomen just forward of the secondary

copulation location and completely separated from the ampulla. In contrast, the male

genitalia in H. ‘‘onokis’’ remained attached to both the female’s genitalia and her mid-

abdomen while the spermatophylax was delivered to the ventral side of her abdomen 53 sec

after the start of copulation. Interestingly, the female 6th sternite of this species consists of

a bilobed posterior margin of the sternite as in all other Hemiandrus with short ovipositors

except H. pallitarsis. H. pallitarsis is the only species in which the 6th sternite is modified

into an elaborate elongate (‘‘elbowed’’) structure (Johns, 2001). I hypothesize that this

elaborate structure of the H. pallitarsis 6th sternite is necessary to allow the male to maintain

his attachment with only the female’s sternite in the latter part of copulation. This

hypothesis predicts that in all species except H. pallitarsis the male remains attached to both

the 6th sternite and the female’s primary genitalia throughout copulation.

Copulation duration was 114 sec long in H. ‘‘onokis’’ compared to a longer duration in

H. pallitarsis where the male ended copulation by pulling away from the female a median

275 sec (n ¼ 2, field) and 298 sec (n ¼ 2, laboratory) after copulation began. A brief

copulation also occurred in two other laboratory H. ‘‘onokis’’ matings and two laboratory

H. ‘‘vicinius’’ matings where I had stopped observing them for only a couple of minutes

and returned to see only the end of copulation as the female was bending to eat the

spermatophylax. In these four matings for the two species, the spermatophylax was

deposited on the venter of the female’s abdomen in a similar location to that noted for H.pallitarsis. A ventrally-placed spermatophylax separate from the ampulla was also noted in

a single field H. ‘‘vicinius’’ mating in 2003. Copulation durations in the Hemiandrus with

short ovipositors studied here are much shorter than the 2 hr copulation duration reported

for H. (formerly Zealandosandrus) gracilis (Cary, 1981). Although spermatophore

transfer was not seen in this species, a photograph of a female Hemiandrus (formerly

Zealandosandrus) species with a long ovipositor in Gibbs (1998) clearly shows an opaque

white-colored spermatophylax attached directly to the sperm ampulla, the conventional

association of the two parts of the spermatophore observed in other ensiferans (Brown and

Gwynne, 1997) including other Anostostomatidae (Monteith and Field, 2001).

After copulation ended, each H. ‘‘vicinius,’’ H. ‘‘onokis’’ and H. pallitarsis female

immediately moved her head to her underside to grasp the spermatophylax. In earlier

observations with H. pallitarsis the female immediately removed the spermatophylax in

one laboratory mating, after 30 sec in a second laboratory mating and after three min in

a field mating (Fig. 2). Details from videotaped matings in 2002 showed that the female

bent her abdomen to begin eating the spermatophylax in a median of 10 sec (n¼ 4, field)

and 3 sec (n¼ 2, laboratory) after copulation ended.

The spermatophylax, which had a ‘‘watery’’ consistency and compared to other

ensiferans (Fig. 2) was removed in its entirety when first grasped by the female H.pallitarsis in all laboratory observations and in 8 of 9 field observations where this behavior

was noted (Fig. 2). While being consumed, the colour of this food gift changed from a clear

translucent to dark as it apparently mixed with the female’s crop contents. The whole

discoloured spermatophylax was observed in the mouthparts in a further 26 field

observations of recently mated H. pallitarsis females at Palmerston North and

Kiriwhakapapa sites. Finally, it took the female 42 min (laboratory) and 51, 60 and 67

min (3 field observations) to consume the spermatophylax to a point at which it was no

longer visible in her mouthparts. The sperm ampulla was removed and eaten after a further


22, 10 and 33 min (one laboratory and two field matings, respectively where this behavior

was observed).

Following mating, in most pairs of H. pallitarsis observed in nature (20 of 28 at

Palmerston North and Kiriwhakapapa), and in all five laboratory matings, the male

remained near the female while she consumed the spermatophylax. In the eight matings in

which the male was not observed, the female was almost certainly in the last stages of

eating the spermatophylax. In all 11 field matings observed in 2002, the male remained

with the female. In field pairings the male was noted from one to 40 cm away from the

female (median distance between the sexes when first observed ¼ 2 cm) (Fig. 3). Post-

copulatory association of male and female probably functions as male guarding. In the

field in 2002 I observed a guarding male to kick at an intruding male that had moved close

to the recently mated pair.

Maternal Care

In early July 1994, about five months after matings were observed in terraria, I excavated

three males and nine female Palmerston North H. pallitarsis from the soil in terraria. Eight

of nine females were in small underground chambers with eggs (Fig. 4). In 2002, approx.

four months after they had been collected in the field after consuming a spermatophylax

(and subsequently allowed to burrow in individual containers: see Methods), four of five

Kiriwhakapapa and all five Palmerston North H. pallitarsis females were found in brood

chambers with eggs. Brood chambers were smooth walled cells 3.75 cm long32.5 cm wide

(mean of five; range 2.5–4.4 cm in length). Two of the nine chambers were beneath leaves

close to the soil surface. The remaining seven were at a mean depth of 2.5 cm (n¼7, range

0.6 to 3.75 cm). In 1994, Palmerston North female H. pallitarsis had a mean clutch size of

40.3 eggs (range ¼ 24 to 63). In 2002, mean clutch size of the Palmerston North females

was 51.5 (range 30 to 72, n¼ 6); and the Kiriwhakapapa females averaged 43.5 eggs per

Fig. 2. Nuptial feeding in H. pallitarsis. Left. A newly-mated female bends to grasp the spermatophylax

which has pooled between her abdomen and the substrate. The rest of the spermatophore, the sperm ampulla, is

the lobed structure beneath her cercus. Right. A mated female has removed the spermatophylax, which is visible

as a dark sphere in her mouthparts as she eats it. The ampulla, a white spherical shape, is still present on

her genitalia.


clutch (range 17 to 64; n¼4). Other Hemiandrus species with short ovipositors have similar

brood sizes and brood chambers. I excavated: a single laboratory H. ‘‘vicinius’’ female with

41 eggs from smooth walled chamber 2.5 3 1.25 cm in size excavated under a leaf; and

a single H. ‘‘promontorius’’ female with 30 eggs from a chamber 5 cm under the soil.

Wahid (1978) reported a mean clutch size of 50 excavated from brood chambers of H.‘‘peninsularis’’ (‘‘horomaka’’ in Johns, 2001) from sites in the Hortone Valley on the South

Island. A published report of brooding by Salmon (1950) describes from 6 to 14 larval

Hemiandrus (species not identified) in chambers with females.

In 1994 the excavated H. pallitarsis females showed evidence of tending eggs by

remaining with the eggs during excavation, and being remarkably attentive to the clutch

after transfer to the artificial chambers, making the transfer a relatively straightforward task

(one female palpated eggs while she and her clutch were in my hand). Other females used

their mandibles to pick small pieces of soil from the eggs and used moist soil to plaster

breaks in their brooding chambers.

Further details of maternal care were obtained in 2002 from direct observations and

from video of three Palmerston North and three Kiriwhakapapa females. None of these

females had been observed on the surface of the soil during the several months after

burrowing into the soil. This, and the fact that excavations of brood chambers revealed no

obvious exit burrows, indicates that females remain with their brood throughout this time.

Surprisingly, while I excavated chambers, only two of the six females straddled their eggs

and showed apparent aggression by opening their mandibles. After nymphs hatched in the

laboratory, four of seven females straddled the nymphs with mandibles agape after I had

removed the top half shell of the clay chamber.

When tending eggs, all six females were observed to take soil in their mandibles and

apparently to mix it with salivary secretions as they plastered certain areas of their brood

chambers. This included plastering over translucent plastic forming the side of the

chamber (one female) and forming a plastered mud slightly domed roof over the chamber

Fig. 3. The male (left) H. pallitarsis remains in the vicinity of the mated female.


in the 24 hours after I had excavated the soil from the top of the chamber (four of six

females). One of the six females was observed to pick up soil from the eggs and another to

place the eggs on the bottom of the chamber. After artificial brood chambers were moved

to environmental rooms one chamber was flooded and its occupant subsequently ex-

cavated through the clay bottom of her chamber, and several cm of vermiculite beneath, to

move all her eggs into a pile on the dry plastic bottom of the housing container.

Infra-red video of 15 to 30 min samples of six females with nymphs in clay brood

chambers showed that, although larvae often moved, the adult female rarely moved. Adult

movement was associated mainly with picking up soil particles and in one case to plaster

moist soil around the glass slide ‘‘window’’ of her clay chamber (Fig. 4).

In 1993, hatched H. pallitarsis larvae first appeared in late September on the outside of

a clay chamber in which the female had died. By 6 October, three additional females had

died and larvae has begun emerging from clay chambers. One live female was found in

a clay chamber with larvae. Of four surviving females on October 27, two had no larvae,

one had larvae in her chamber and one was found with eggs. Wahid (1978) found that eggs

laid in July hatched in about 40 days. He found no evidence of an egg diapause. In my

Fig. 4. The main photograph shows a female H. pallitarsis with eggs in a partially excavated brooding chamber.

The female has moved to the hole broken into the top of the chamber. Several eggs are visible beneath her head.

The inset photograph shows a female guarding her larvae in an artificial clay brood chamber.


study, eggs had been laid by the beginning of July (1994) and by the beginning of June

(2002) when chambers were first inspected.

In 2002, more detailed observations showed that most female Hemiandrus survived in

their brooding chambers until larvae hatched: only one of nine female H. pallitarsis died

(in mid July); her eggs became covered with fungal growth and did not hatch. However,

although each female H. ‘‘promontorius’’ and H. ‘‘vicinius’’ had been removed from her

eggs as a voucher specimen, the orphaned ‘‘promontorius’’ eggs hatched (the ‘‘vicinius’’

eggs became mouldy and failed to hatch).

The first H. pallitarsis eggs hatched in the first week of September; five of nine clutches

had hatched by the last week of September (two Kiriwhakapapa and two Palmerston North

remained unhatched); seven of nine by the first week of October and all nine clutches had

begun hatching by the end of second week of October. Hatching within clutches was

spread out over several weeks. Median percentage hatch was 45.5 for Palmerston North

clutches (range 34 to 82%, n ¼ 5) and 44% for Kiriwhakapapa clutches (range 22–66%,

n¼ 3). Interestingly, the lowest percentage hatches (22, 24 and 34%) were, respectively,

for the smallest (14) and two largest clutches produced (72 and 67 eggs).

Egg hatching of Hemiandrus in September and October is consistent with a cohort of

half grown larvae being present with a cohort of adults in populations of these weta

observed on vegetation during the late summer mating period (January to March).

(Gwynne, unpubl.). These Hemiandrus species appear therefore to have a two-year life

cycle. Two-year life cycles are common in all ensiferan families except Gryllidae and

Tettigoniidae where development from hatchling to adult typically occurs within a year

(Gwynne, 1995). There are exceptions, however, including the alpine weta Hemideinamaori (Jamieson et al., 2000) in which marked adults were commonly observed over more

than one breeding season.

General Discussion

In nature, I observed courtship and mating by Hemiandrus with short ovipositors almost

exclusively on leaves. Mating in burrows, suggested by Stringer (2001) and Barrett (1991)

seems unlikely because the confines of a burrow are likely to restrict drumming behavior

and movements during copulation and spermatophylax consumption.

Pair formation in vegetation would be assisted by communication using substrate

vibration, a mode of signalling known in other ensiferan Orthoptera that mate in vegetation,

both through drumming and body shaking (tremulation) or as a consequence of tegminal

stridulation (Bell, 1980; Morris, 1980; Markl, 1983; Dambach, 1989). In gryllacridids

(Field and Bailey, 1997) and stenopelmatids (Weissman, 2001) males produce drumming

signals (complex and species-specific in Stenopelmatus) and there is evidence that females

respond to these signals. In tettigoniids vibratory signals from stridulation can be used by

females to locate a male (Stiedl and Kalmring, 1989). Several observations suggest that

male H. pallitarsis might use drumming signals to attract receptive females (although, as

stated above, chemical communication is also likely: Bateman and Toms, 1998). First, in

nature mating was always observed on the tops of leaves where motionless perched

individuals of both sexes were very commonly observed. Males could be using leaves as

a drumming substrate while females might perch in vegetation in order to locate themselves

in areas where these signals can be detected, eliciting a female response drumming and

subsequent vibrotaxis from the male. I observed direct evidence of drumming in these

contexts from both sexes. I have also heard drumming by males of an unknown Hemiandrus


(formerly Zealandosandrus) species (from the Rock and Pillars Range, Otago, and probably

H. focalis) that were housed in plastic cups (Gwynne, unpubl.). Cary (1981) also reported

spontaneous abdomen drumming by male H. (formerly Z.) maculifrons housed in terraria.

Note that Hemiandrus are also known to stridulate. However, stridulation appears to be used

exclusively as a defensive mechanism (Field and Glasgow, 2001).

One feature of mating that H. pallitarsis shares with many other species in the

Tettigoniidae-Haglidae-Stenopelmatidae group is a large spermatophylax transferred as

a food gift from male to female (Brown and Gwynne, 1997). Such gifts can be important to

female and offspring fitness in Tettigoniidae (Gwynne, 2001). Interestingly, a large

spermatophylax gift is lacking in a South African king cricket (Libanasidus: Bateman and

Toms, 1998a) and both the New Zealand giant weta (Deinacrida) and tree weta

(Hemideina) (Brown and Gwynne, 1997) (the latter has a very reduced spermatophylax)

but is present in some Australian anostostomatids (Monteith and Field, 2001) and in

at least one Hemiandrus (formerly Zealandosandrus) species with a long ovipositor

(photograph in Gibbs, 1998). However, in all these other ensiferans the spermatophylax

is attached to the sperm ampulla. Therefore, a highly derived character in at least

three Hemiandrus species with short ovipositors is the complete separation of the

spermatophylax food gift from the rest of the spermatophore (the sperm ampulla); the gift

is placed on the mid-venter of the female’s abdomen. This separation of the food gift from

the ampulla is associated with the presence of a modified 6th sternite in females (Salmon,

1950). In H. pallitarsis this highly modified sternite functions as a secondary copulatory

appendage for the sole attachment of the male’s genitalia during the final stage of

copulation when the spermatophylax gift is transferred to the female’s abdomen. This

follows the attachment of the ampulla to her primary genitalia (Gwynne, unpubl.).

Following almost all copulations in Hemiandrus, the male remained close to the female.

This sort of post copulatory association has not been noted in related families such as

Tettigoniidae and Haglidae but has been observed in another anostostomatid (a king

cricket, Libanasidus vittatus: Bateman and Toms, 1998) and is common in many Gryllidae

when the male stays in antennal contact with the female after mating (Brown and Gwynne,

1997; Zuk and Simmons, 1997). In gryllids post copulatory guarding may function in

preventing the female from eating the sperm ampulla before insemination has occurred,

although other functions are also likely (Sakaluk, 1991; Bateman and MacFadyen, 1999).

In the king cricket, males pass many small spermatophores to the female during a single

mating bout so guarding appears to function in keeping rival males from disrupting

insemination. In the ground weta, however, the guarding male is not usually in direct

antennal contact with his mate and is present after the sole spermatophore is transferred

(Fig. 3). These observations and the fact that the female is distracted away from the

ampulla by the spermatophylax meal seem to rule out protection of the ejaculate from the

female as a function for post-copulatory association of the sexes. One possible function is

that male presence keeps other ground weta away from the female as she consumes her

spermatophore gift. In tettigoniids, conspecifics can opportunistically feed on another

individual’s spermatophylax (Gwynne, unpubl.) and a spermatophylax attached to the

ampulla can act to protect the ejaculate (Gwynne, 2001). Thus the presence of a vigilant

male H. pallitarsis may prevent his unprotected sperm ampulla from being dislodged by

intruders.

Hemiandrus pallitarsis females show substantial care for eggs and offspring by

sequestering themselves for a long period of time in an underground chamber that appears

to be sealed off from access burrows. There are a number of possible functions of maternal


care of eggs and larvae including protecting eggs from fungal growth as well as from

predation by soil animals such as the onychiurid collembolans and amphipod crustaceans

that are common in the soil where weta burrows occur. There was no evidence in the

laboratory that females left (the artificial clay) chambers so mothers appear to stay with

offspring until death as suggested in Wahid’s (1978) study of H. ‘‘peninsularis’’. Some sort

of maternal association with eggs and larvae in chambers in the soil has been noted in a few

other orthopteran species, including two gryllid genera, several gryllotalpids, schizo-

dacylids, and a rhaphidophorid. (Gwynne, 1995, and references therein). The presence of

maternal care in ensiferan Orthoptera is associated with a shortening or loss of the typically

long ensiferan ovipositor, presumably because eggs are not injected into a substrate but

simply placed on the bottom of the chamber. The very short ovipositor of H. pallitarsis is

consistent with this pattern (Gwynne, 1995). Ovipositor length and presence or absence of

maternal care vary within the genus Hemiandrus. Evidence suggests that species with long

ovipositors do not show maternal care: both H. (formerly Z.) subantarcticus (Butts, 1983)

and H. (formerly Z.) focalis (Gwynne, unpubl.)—species with long ovipositors (Salmon,

1950)—lay eggs into the ground in a similar manner to most Ensifera (Rentz, 1991).

Interestingly H. (formerly Z.) maculifrons uses a long ovipositor to oviposit into the walls

of underground burrows (Cary, 1981) and may represent an intermediate stage in the

evolution of the association of females with offspring in underground chambers. Moreover,

from a molecular phylogenetic analysis of Hemiandrus, Gerber (1996) concluded that the

evolution of a short ovipositor is recent within the genus.

The long ovipositor of some ground weta was a key character for Salmon (1950) to

separate these species into a new genus Zealandosandrus. Another key character for

Zealandosandrus was the lack of a modified 6th abdominal sternite in females (Salmon,

1950) that is associated with the delivery of the spermatophylax mating meal in Hemiandruswith short ovipositors (Gwynne, 2002). However, as stated in the Introduction, this basis for

dividing the New Zealand ground weta into two groups has no support. First, a phylogenetic

analysis of ground weta shows no natural groupings based on ovipositor length (Gerber,

1996). Secondly, the taxonomy ofHemiandrus (Johns, 2001) shows not only that there are at

least three different lengths of ovipositor among the 25 or so species, but also that among the

species with short ovipositors, variation in the structures on the female 6th abdominal sternite

is much more complex than described by Salmon (1950). Only H. pallitarsis has an

elongated centrally-located process on the 6th abdominal sternite. In a number of other

species this sternite has a bilobed posterior margin. Even Hemiandrus species with long

ovipositors usually have slight abdominal modifications in the female—typically a pair of

pits or ‘‘pockets’’ under the hind edge of the 6th sternite (Johns, 2001, and pers. comm.). The

results of the present study show abdominal deposition of the spermatophylax in several

species with short ovipositors, and coupling by males to both the female’s 6th sternite and her

genitalia (in H. ‘‘onokis’’ and probably other species with a distinct bilobation of the

posterior margin of the female’s 6th sternite). The elaborate elbowed accessory organ of H.pallitarsis appears to be exceptional and may function in allowing the male to remain

detached from her primary genitalia while he delivers the spermatophylax gift.

Interspecific variation of these accessory organs and ovipositors, and thus by inference

variation in male gift-giving behavior and female care of offspring, as well as drumming

behavior, suggests that Hemiandrus species have a unique potential for addressing

evolutionary questions about the evolution of complex signals and both maternal and

paternal investment.


Acknowledgments

A voucher series of the ground weta has been placed in the collection of the Royal

Ontario Museum. Thanks to Graham Wallis, Ian Jamieson (Otago University), Ed Minot,

Jay McCartney, Doug Armstrong and Ian Stringer (Massey University) and other faculty,

staff and graduate students in these two institutions for technical assistance and discussion;

To Mary Brooks and the late Prof. Robert R. Brooks for introducing me to weta in their

garden; to Clint Kelly and Sarah Gwynne for help in the field; to Peter Johns who

identified the species and provided valuable natural history information and comments on

the manuscript; to Mary McIntyre, George Gibbs, and the members of IBG (University of

Toronto) for discussion; to Paul DeLuca for the sound analysis; to Glenn Morris for the

use of his equipment for sound analysis; and to Jay McCartney and Mary Morgan-

Richards for comments on the manuscript. This research was supported by research grants

from NSERC (Canada) and the National Geographic Society (U.S.A.).

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Documents

Reproductive Behavior of Ground Weta (Orthoptera: Anostostomatidae): Drumming Behavior, Nuptial Feeding, Post-copulatory Guarding and Maternal Care