To mate or fight? Male-male competition and ...

Behavioural Processes, 23 (1991) 163-l 72

163

0 1991 Elsevier Science Publishers B.V. 0376-6357/91/$03.50

BEPROC

00340

To mate or fight? and alternative

mating

antipodiana Mary Zoology

Department,

Male-male

competition in Argyrodes

strategies

(Theridiidae,

Araneae)

E.A. Whitehouse

University

of Canterbury,

Private Bag, Christchurch,

New Zealand

(Accepted 2 January 1991)

Abstract

Argyrodes antipodiana is a kleptoparasitic spider that builds its own web around the webs of other, larger host species. Males are more prone to have contests on webs of conspecific females than on webs of conspecific males. Males are also more likely to escalate interactions when on the females’ webs than on males’ webs, consistent with predictions from game theory models. Yet, in nearly half the tests, males on females’ webs did not escalate. Instead of just being “sampling error”, these failures to escalate may reflect the contest losers’ abilities to gain copulations by “sneaking”, an alternative mating tactic which enables males to obtain access to a female, not by fighting,

but by exploiting

the dominant

male’s dilemma

Key words: Sexual competition; Alternative Spider; Game theory

of whether

mating strategy;

to mate or fight.

Argyrodes

antipodiana;

Introduction Often animals compete for important resources by performing displays rather than fighting. Game theory arguments have been used to show how such behaviour can be evolutionarily stable (e.g. Maynard Smith 1974, Parker 1974, Maynard Smith and Riechert 1984). Some predictions extrapolated from game theory models are that

164

individuals

will

(1)

escalate

valuable,

(2)

balance

resource,

(3)

use

display

with

willing

to

ions

displays

uniform fight,

ownership are

generally

predicted

to assess

(5)

but

1983,

Weatherhead

1987).

One

ways

access

to the

to gain

initial

the

how

there

often 1986,

explanation

are

for this

contested

and

they

These

without

are

that

fail

individuals

the (4)

(e.g. to

prior

predict-

behave

1986,

resorting

more

actually

and other

Huntingford

is that these

resource

is (RHP),

contestants

1987).

individuals

Turner

stake

of winning

potential

longer

between

see Crafen

at

benefits

holding

much

asymmetries

Riechert

the

resource

of

(but

resource

against

each other’s

conflicts

upheld,

(eg Austad

when

interaction

regardless

use

to settle

more

of the

intensity,

and

or size)

contests

the costs

as

Eckert

and

have alternative

to direct,

aggressive

confrontation. Male-male Argyrodes in this

genus

1986).

Also,

about

four

host.

competition (Vollrath unlike

food

bundles prey

male

the

then,

males

webs

potential vary

models.

In

or avoid

If two competitor males

might

nents

and

mate with also

or to the female.

To

solve

be predicted.

Firstly,

opponent

of

of the

move

to steal

about

wrapped-up

the

host

on

courting

or

by

the

on

the

males

to

three

a male’s

web;

the female.

The

Other

opponents males

escalate

to

away

levels

responses

by

oppo-

by

totally

on

to use

males

of

away

that

the

time

(Peschke

and of

or

males

(Kodric-Brown Le Boeuf

1987, 19j7). are

Argyrodes

on a female’s

to each other

their

that

most

females (Cox

interactions

are able

the

opponent

attempts

when

the

to

either

1986)

from

males.

Alternatively, the

to

Ryan

with

with

has shown

attempts

higher

of the males

chasing work

access

respond

female

theory

(e.g.

mate

different

opponent.

(Crespi

male-male

contests

four

to

confrontations the

for

means

and

males

game

of Argyrodes

whether

copulation

to have contests

of aggressive responses

on

about

inclined

contests

concentrate

copulation

to

with the

other

also

males,

between

contests

to court

to a

For

from

by other

at least

mating

opponent’s

males’

hypotheses

are more

as

avoiding

their

their

try

avoid

attempts.

lose

is true

problem, might

and

chase

other

and “losers”

be examined.

this

and

avoid

often

and disrupt males

a dilemma

copulation

tend

that

conspecifics indicates

resource).

derived

to females

this

in a web

of contests

predictions

Perhaps

actively

female

the outcomes animals

and female

silk valuable

simultaneously

males

may try to disrupt

paper,

web;

1986). face

they

on

web,

of male

of females’

gain access

species

may

copulations

this

male’s

male

the silk

to test

however,

altogether,

the opponent’s

investigated: when

consist

to the orb web

alongside

(an especially

enabling

of studies,

Kodric-Brown

courting

1986)

value,

of any given

Dominant

In

species

(Whitehouse

generally

as Argyrodes)

host’s

simultaneously

presence

to be used

contests

concentrate

stop

Crespi

attached

using

other

spiders

groups

to simply

off the

between

the

of a mate

of webs

each

the

disrupting

Thus

in resource

1989,

males

female,

1986)

referred insects

examined like

of larger These

space web

to feed

can distinguish

a number

and Causey

although

and

presence

types

females,

“sneak”

in groups.

(herein trapped

host,

submitted).

different

might

is a kleptoparasite

it lives

was

A. antipodiana,

item.

Argyrodes

ignoring

the

(females)

Zealand.

in an irregular

to glean

from

resource

New

1979),

A. antipodiana

(Whitehouse,

same

a limited from

spiders,

living

and stealthily

same

on

1976,

most

individuals

Individual

slowly

for

a spider

antipodiana,

a female’s alternative

web than

than on

tactics

and to the female

a to

will

165

Met hods

Maintenance All spiders were collected from Te Aroha (North Island, New Zealand) and were maintained according to general procedures for spider studies described elsewhere (Jackson and Hallas 1986), in a room with controlled photoperiod (12:12, L: D) and temperature

(20-25°C).

Tests for male-male

Observations

took place during

daylight

hours.

contests

In each test, two males were introduced simultaneously to a recently (5-20 min) vacated web of either a conspecific male or a conspecific female. Each pair of males was tested on a male’s and on a female’s web on consecutive days (order The males were left on the web for a 20-min test period and were

random). observed

continuously. Twelve pairs of males were weighed (using a Cahn 21 electrobalance) before testing. Although each individual male was used more than once, a given pairing of two males was used for only one pair of tests. Results were analyzed using the McNemar tests for significance of changes with Yates’ Correction (Sokal and Rohlf 1981).

Tests for mating Two

tactics

males were placed on the web of a female, with

the female present,

and the

ensuing interactions observed until the trio became quiescent or 5 h had elapsed. If the spiders failed to interact within the first 30 min, the test was aborted. Although individual males were sometimes used in more than one test, a given pairing of two males was used only once. Interactions were video taped for later analysis. Information was gathered to establish the following: which male obtained the most copulations and which male copulated for the longest total time. If both males copulated, the reaction of each male to the other was examined.

Results

Male-male

contests

Terminology Animals “escalated” an interaction when they progressively switched to behaviours of greater “cost” (Fig. 1). Cost of a behaviour was estimated, not measured, based on judgment of the degree of danger to which the spider probably exposed itself when performing the behaviour. For instance, by shuddering, a spider apparently alerts its rival and thereby becomes more vulnerable to attack by the rival. Touching is ranked

166 4 GRAPPPLING Spiders face one another, spread their chelicerae, palps and legs apart and vibrate rapidly while moving closer

3 TOUCHING

Argyrodes extended a leg I and brought its tip into contact with the opponent

2 SHUDDERING/MOVING Shuddering and moving caused vibrations which alerted the opponent to the "displayer's" presence. To shudder

Argyrodes vibrated its in 1 second bursts

abdomen rapidly

1 STATIONARY no cost

Fig. 1. Diagrammatic podiana.

arbitrarily

higher

than

at close been

seen

which

the

to

place with

because

rival

lunge

which

they

suddenly

can last spiders

could

then,

if neither

Only

a shift

A spider while rival

between

male

Argyrodes

which

anti-

was estimated

bite

Argyrodes

2 min,

is

touching

ranked

spider

breaks

off the

the rival

close

range

spiders

interaction,

this

data).

behaviour

in positions

move

closer

the spiders

seem

and, have

(unpubl.

because

and apparently

would

is close

on rare occasions

higher

Grappling

of chelicerae

when

from still

each other

each other.

in position

only

Argyrodes,

In fact,

necessary

from

and

lock

closer

chelicerae

to inflict

serious

on a rival.

“avoided”

“chasing” quickly

is possible

attack.

at other

over

almost

readily

together,

or death

touching

can readily

together. injury

in fights

of escalation

it moved to the next level in “cost”

when

on the amount of probable danger the display exposed the actor to.

shuddering

range,

Grappling, takes

representation

The fight escalated

another

occurred

moved

away,

when

when

one

it moved spider

excluding

at its normal quickly

interactions

speed

moved in

away

towards

which

one

its male

from

its rival,

rival

and

was

initially

its

copulating. In

a “contest”,

other

spider

(the

types

of contests

the

“winner”

“loser”) depending

which,

was

a spider

in turn,

on whether

that

consistently

consistently or not

a spider

moved

moved

away.

fast

grabbed.

towards

There

were

the two

167 TABLE 1 Level of escalation reached by pairs of males on male and female webs Level of escalation

1

2

3

4

male web

3

17

2

0 n=22

female

4

6

5

7 n=22

web

To “fast grab”, one spider (always the winner) pulled rapidly with his front legs on the dragline of the loser, as if he was trying to haul in the other spider. Once a spider had fast grabbed at its opponent, again by his opponent. Contests

he was very rarely (4 cases out of 151 chases) chased in which the winner fast grabbed are called type 1.

ln tests where spiders did not fast grab (type 2), the two spiders tended to take turns chasing each other. In these tests, the “winner” was the spider that predominantly

(more

than c 80% of the time)

chased the other

male (the

loser).

If spiders

chased each other equally, no winner or loser was designated. It needs to be emphasized that fast grabbing and chasing were not simply steps in escalation sequences. Instead, they could occur after any of the other behaviours (Fig. 1). Findings Out of 22 test pairs, males fast grabbed (i.e. had type 1 contests) in only one interaction on males’ webs but fast grabbed in 16 interactions on females’ webs,

indicating that males are more inclined to contest a female’s web than a male’s web (x2 = 11.53, P < 0.001). Male-male interactions tended to escalate to higher levels on females’ webs than on males’ webs (Wilcoxon’s signed rank test, P < 0.05, n = 22 test pairs). Nevertheless, in nearly half the tests (IO), males did not escalate beyond level 2 on females’ webs and “losers” were still established in (Table 1). In these instances, though, “winners” type 2 contests. In the 12 tests with weighed males on females’ webs, larger spiders usually won the fights (8 out of 12 tests). There was no evidence, however that escalation correlated with size difference (multiple regression: r = 0.004, NS).

Mating

tactics

Terminology “Copulation” is defined as the period during which the male’s palpal organ was engaged on the female’s epigynum. Spiders are “courting” if they are performing displays specifically associated with mating as defined in Whitehouse (submitted). One male “disrupted” another male’s copulation by moving towards, displaying towards, or touching the copulating pair, resulting in the pair separating. To “drum”, a male extended his straightened legs I anteriorly and moved them up and down in alternating phase (i.e., when one leg is maximally dorsal, the other is maximally ventral), articulating at the bases of the legs (the coxa-trochanter joints) so rapidly that the two moving legs appeared as a blur.

168

TABLE 2 Interactions * both

between

copulations

showed

no interest

Test

individuals took

within

place with

in copulating

tests.

the second

male before

the males

fought

(the

female

after the fight).

Total

Total

Number

period of

number of

copulations

activity

interactions

Number

of

Number

of

of

male-female

male-male

interactions

interactions

(excluding copulations) 2h

1

14

2

2*

18

2

5h

227

50

103

74

3

4h

175

49

49

77

4

3:20

130

45

28

57

5

2:4Oh

186

45

67

74

h

Findings Individuals escalated the

10 tests,

the

other

in 2 tests

38 min).

interaction

were

called

10

the

Thus,

tests

and

tests.

female

only

with

both usual

female,

the

winners Females

5 tests

were

were were

copulated

first

female

began,

and “second”

copulated

sequence

and the

the

the “first”

the female

tests, The

in

in 8 of these

only

established

receptive, once

available

for

(in full

in

each.

though, one

Fights

in only

case for

7 of

3 min,

in

analysis.

copulations

Once which

and

for

Gaining fight

interacted

to grappling

more

than

and second

male

of events

was that

winner

then

mated

the

winner

male,

once

after

managed the

with

the

males’

to copulate

males the

and

loser

respectively.

fought,

female.

There

of

contest. with

the

apparently

However,

the

were

preceding

four

tests

in

In each of these female for

in test

(Table

access 1, the

2).

to the second

TABLE 3 Copulation performed Test

behaviour.

The numbers

in the parentheses

are the percentages

of the copulations

by the male that were disrupted. Number

of

copulations

Time spent

Number

copulating

copulations

of

disrupted

2

Male I

Male II

Male

42

8

24:16

13:47

min

min

I

Male II

3

42

7

25:49

4

42

3

27:14 min

min

5

36

9

18:21

16:15

min

min

min

Male I

Male II

;:8%)

:63%)

(9L1%)

i43%)

7204%)

;67%)

::8%)

;89%)

6:56 min 4:05

169 male

managed

refused

to copulate

to copulate

In all tests, tests the

the

interacting female,

although

after spiders

over

and

with

the female

the fight. were

100

times

obtained

Thus

active

for

(Table

2). The

many

in test 5 the second

before

the

test 1 could

more

2 to 5 hours, first

almost

fought,

with

male

copulations

male spent

males

not be used the

always

than

as much

and the

for

further

female

analysis.

individuals

in most

interacted

the

second

time

mating

more

male

with

(Table

as the first

3),

male.

Chasing and avoiding There

was

a total

of 249

male

in 147 of these,

male

avoided

the

male.

Thus

male

predominantly

first

the first the

the web.

chased

the

male second

male.

formed

the

Males

but

while

the

also

first

was

from

that

male

first

first

the

male

male

never

the second the

was

away

the

able to return

the

female,

by courting

are normally

each

still

other

performed

and actively the

first

while

trying

male

the

to

9 times

only

approached

female

in which

apparently

second

the second

often

to the female

second

the

whereas

male

from

the second

4. The

avoided

male

second

chased

in only

first

in 13 of the 147 instances

interacted

displays

the

However,

male

away

The

chased

chased

first.

For example,

moving

same

the

the second

second,

times,

male

predominantly

female

continued

89

avoided

and courted

interactions.

the second

male

male

moving

over

male-male

whereas

(i.e.,

first

chase

the

they

per-

in male-female

interac-

tions).

Disruptions Males there

often

were

second

male

touching

The

courting male

Males with choose

towards

he did not drum

of the disruption the female

by

however, (16

(2 times).

(5

Thus

trying

(5

times) the first

to mate with

to disrupt

by the second

The times),

or shuddering

touching

by directly

or shudder

attempts

tests,

copulations.

(8 times),

towards

either

all

by courting

primarily

or moving

In

male’s

primarily

male

copulations

3).

first

copulations,

male.

Disruptions

or both.

courtships simultaneously being

ended one

the pair;

of the

moving

second

to mate (4 times),

at the male,

female

courtships

the

(Table

than

copulations

(9 times),

the second’s

characteristic

courted

the

trying

copulations

second

male’s

disrupted

or by touching

Simultaneous

first

drumming

disrupted

directed

other’s

of the

the

male

(4 times),

usually

as was often were

times), first

the female

each

disruptions

disrupted

(16

times).

disrupted

more

when

male

over

on

aggressive

25

one male chased the other

occasions.

towards

one

or

the other.

Nine

of

both

males

Females

in any of the tests

with

these

courtships

and

did not appear

simultaneous

ended

2 simultaneous actively

courtship

to

by 2

males.

Discussion Males webs

females’ of the simply

were

escalated webs, resource

more

likely

to higher there being

to differences

was

to fight levels

when

than those

no escalation,

contested. in size,

on females’ on males’ despite

would

and contests Yet,

the evident

Lack of escalation as this

webs, webs.

have

does resulted

not

on females’

in half the contests

importance seem

to the

on

males

to be attributable

in a negative

correlation

170

between

size

difference

and level of escalation,

as shown

by Wells

(1988).

Such a

trend was not evident in the 12 tests using males of known weight. To understand why males did not escalate, it may be important to ask whether males have alternative ways of gaining access to females. It is helpful to envisage competition between males for access to females as being divided into two contests. In the first, a ritualized fight establishes a winner and a loser. In the second, both the loser (who stays in the web) and the winner try to mate with the female. In the second contest, the first obtained more copulations

male (i.e. the winner

of the fight in the first contest)

and copulated for longer.

He actively chased the second

male away from the female, and disrupted the second male’s copulation attempts. The second male, in contrast, tended to obtain fewer copulations than the first, avoided the first male by moving away from him, and very rarely chased the first male, but did disrupt the first male’s copulations. It appears, therefore, that in these encounters, the first male was “dominant” while the second male gained copulations by sneaking. However, the picture is not as straightforward as this because the first male tolerated the second when both courted the female simultaneously, male disrupted the first male’s copulation attempts.

and the second

To understand these behaviours, it is necessary to consider the options available to a male when another male is courting the same female. A male might avoid or ignore his opponent and just try to mate with the female, or he might chase or disrupt his opponent. It was usually the first male that chased the second male away rather than vice versa. Chasing an opponent away, however, had disadvantages for the first male because, to do so, he had to terminate his own copulation attempts and the second male always returned. As an alternative, the first male occasionally ignored its opponent and continued to court and copulate with the female. The first male appears to be faced with a dilemma of whether to mate or chase and this may have helped the second male obtain copulations. To mate, the first male must ignore the second male, enabling the second male to approach the female. To attempt to chase the second male away, the first male has to leave the female, providing the second male with an opportunity of finding the female, courting and copulating with her. Although the second male usually avoided the first male, he did sometimes actively disrupt the first male’s copulations. The second male did this mainly by performing courtship displays: in first male and simply male did sometimes drumming at the pair.

these instances, the second male may have been ignoring the attempting to mate with the female. Nevertheless, the second seem to disrupt the first male’s copulations deliberately by Argyrodes males are very sensitive to distraction while mating

and readily separate from the female when disturbed, but the process of untangling itself from copulating with female apparently entails a delay in the copulating male’s attack on the disrupter. Because of this, second males appear to be able to disrupt the first male’s copulation attempts with relative impunity. Does the second male’s tactic of sneaking copulations seriously undermine the first male’s success? Does the option of sneaking undermine the importance of winning the initial fight? There are a number of factors that probably affect the second male’s prospects of fertilizing eggs. First, the second male did not spend as much time mating as the first, suggesting that second males tend not to transfer as much sperm as first males.

171

However, majority

it is not clear when, during

the c 5 hours

of sperm is actually transferred.

of courtship

Some behaviours,

and copulation,

classified

the

as “copulations”,

probably are actually courtship or even plug depositing behaviours resulting in no sperm transfer (Whitehouse submitted). Second, Austad (1984) suggested that spiders with conduit spermathecae are morphologically predisposed to use sperm in the order in which it is deposited. Argyrodes has conduit spermathecae, suggesting that the first male tends to have an advantage as he usually mates with the female immediately after the fight and before his competitor can sneak copulations. However, the first male to mate is unlikely to fertilize all of a female’s eggs. It is known that partial displacement of sperm by the second male, or a mixing of sperm from the two males, occurs in some spiders with conduit spermathecae (Jackson 1980). Sperm usage patterns by Argyrodes have not been studied, but it seems probable that sneaky copulations are an effective alternative mating tactic and the availability of this tactic to Argyrodes

reduces the importance

of winning

fights.

Acknowledgements I would like to thank Robert Jackson, tan McLean, Joe Waas, Curt Lively, Beth Jakob, Brenda Poulsen, and Ian Plant for constructive comments on the manuscript. I would also like to thank Tracy Robinson for help with preparation of the manuscript.

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