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Behavioral Ecology Vol. 12 No. 6: 691-697
© 2001 International Society for Behavioral Ecology
Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection
lhandskeAnimal Ecology, Department of Zoology, Göteborg University, Box 463, SE-405 30 Göteborg, Sweden
Address correspondence to P. Stlhandske.
E-mail:
pia.stalhandske{at}zool.gu.se
.
Received 13 September 2000; revised 29 January 2001; accepted 29 January 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The nuptial prey gift in the spider Pisaura mirabilis has been suggested to function as a male protection against sexual cannibalism during courtship and mating. This hypothesis together with two alternatives—male mating effort and paternal investment hypotheses—were tested in a laboratory experiment with sexually inexperienced males and females. One group of males offered no gift to the female while three groups of males offered small, medium, or large sized gifts, respectively. No male was cannibalized among 82 trials. Aggression was observed only in encounters where a gift was presented. Males without a gift courted females, and 40% of these males managed to copulate, compared to 90% of males offering a gift. The copulation duration was positively correlated with gift size. In general, the female terminated the copulation and ran away with the gift. The proportion of eggs fertilized increased with copulation time. Presence or size of the nuptial gift did not affect female fecundity or spiderling size significantly. The results refute the hypotheses of sexual cannibalism and paternal investment. The nuptial gift represents a male mating effort; it entices the female to copulate, facilitates coupling during copulation, and by prolonging copulation it may increase the amount of sperm transferred. I conclude that the nuptial prey gift in Pisaura mirabilis is maintained by sexual selection.
Key words: female choice, mating effort, natural selection, nuptial gift, paternal investment, Pisaura mirabilis, sexual cannibalism, sexual selection, spider.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Males of some species supply females "nuptial gifts" in the form of nutrients prior to, during, or shortly after copulation (Thornhill and Alcock, 1983
).
There is a variety of ways in which this nutrient transfer occurs, and nuptial
gifts are taxonomically widespread. Donation of captured prey or collected
food items occurs in some birds and insects, and in at least one spider (see
below). Some insect males give up certain body parts to their mates. Other
males are consumed during mating by sexually cannibalistic females. This type
of feeding can be found among certain spiders, mantids, scorpions, copepods,
and midges. Nuptial gifts can also take the form of seminal gifts and
different types of secretions as in some insects, centipedes, and onycophorans
(see references in Andersson,
1994; Elgar, 1992;
Gwynne, 1997;
Vahed, 1998;
Wedell, 1994). At least three hypotheses explain the adaptive significance of nuptial gifts in arthropods:
- The nuptial gift represents paternal investment and results from natural
selection: nutrients from the gift are used by the female to increase the
fitness of the gift-giving male's own offspring
(Downes, 1970;
Thornhill, 1976a;
Trivers, 1972).
- The nuptial gift represents mating effort and results from sexual
selection. This includes such functions as enticing the female to mate or
maintaining the position of the female while the male initiates copulation
(Kessel, 1955;
Thornhill, 1976b), and
maximizing ejaculate transfer (e.g., prolonging the duration of copulation),
thereby ultimately countering the effects of sperm competition
(Sakaluk, 1984;
Thornhill, 1976b).
- The nuptial gift protects the male from sexual cannibalism and results from
natural selection; the gift allows the male to mate without being eaten by the
female (Bristowe, 1958;
Kessel, 1955).
There has been considerable debate over the selective pressures responsible
for the evolution and maintenance of nuptial feeding in insects (see
Gwynne, 1986;
Quinn and Sakaluk, 1986;
Sakaluk, 1986;
Simmons and Parker, 1989;
Wickler, 1985). This
discussion has centered on the issue of whether nuptial gifts represent
paternal investment or mating effort. Recently Vahed
(1998) reviewed empirical
studies primarily related to the selective pressures responsible for the
maintenance of nuptial gifts in insects. The review
(Vahed, 1998) showed that
there exists a large amount of evidence in support of the mating effort
hypothesis, but a relative lack of good evidence to support the paternal
investment hypothesis. There is no evidence to support the hypothesis about
protection against sexual cannibalism. However, the hypotheses are not
mutually exclusive. For example, if a nuptial gift functions as mating effort,
this does not exclude the possibility that it also functions as paternal
investment, and vice versa (Vahed,
1998 and references therein). Furthermore, the selective pressures
responsible for the evolution of a nuptial gift need not be the same as those
responsible for its maintenance (Simmons
and Parker, 1989).
Pisaura mirabilis (Clerck; Pisauridae) is the only known spider
species where the male provides the female with a nuptial prey gift when
courting (Van Hasselt, 1884;
but see Itakura, 1993 and
Nitzsche, 1988 for two other
possible species). The nuptial gift consists of a prey the male has caught and
wrapped up in silk. The male offers this gift during courtship, and if the
female accepts the invitation she grabs the wrapped prey. While the female is
eating, the male inserts the mating organ and sperm is transferred.
More than a century has passed since Van Hasselt
(1884) first described the
nuptial feeding in Pisaura mirabilis, but its adaptive significance
is still unknown. Van Hasselt
(1884) suggested that the gift
served as a lure/bait for hungry females, whereas later writers consider the
gift as a device to reduce the probability of males being devoured during
mating (e.g., Bristowe, 1958;
Foelix, 1996;
Gerhardt, 1923). Sexual
cannibalism, defined as the killing and consumption of males by females at
some stage during either courtship, copulation or shortly thereafter, occurs
frequently among spiders (see Elgar,
1992, and references therein) and occurs within the family of
Pisauridae (Arnqvist, 1992;
Arnqvist and Henriksson, 1997).
Several features of the courtship and postcopulatory behavior of spider males
appear to have evolved in response to reducing the risk of sexual cannibalism
(Elgar, 1992). The hypothesis
that the nuptial prey gift in Pisaura mirabilis functions as a male
protection is therefore highly conceivable. This hypothesis, however, has been
questioned by Austad and Thornhill
(1986) and Nitzsche
(1988). Austad and Thornhill
(1986) instead suggested that
nuptial feeding in Pisaura mirabilis provides a direct reproductive
benefit to females.
In this article, I explore the current function of the nuptial prey gift in Pisaura mirabilis. The main questions asked were: (1) Are males without a gift more vulnerable to sexual cannibalism than males with a gift? (2) Do the presence and size of a nuptial gift affect male mating success and female reproductive success? In a laboratory experiment I manipulated the presence and size of nuptial gifts. I predicted that if the gift functions as protection against sexual cannibalism, then males without a gift should be attacked and eaten more often than males with a gift; if it functions as paternal investment, then female fecundity or spiderling size should vary with prey size; and if the gift functions as mating effort, then male mating success should vary with presence or absence of gift, or with gift size.
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MATERIALS AND METHODS |
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Study organism
Pisaura mirabilis (Pisauridae) is a large hunting spider (adult body length 9-15 mm) living in grasslands, heathlands, and woodland clearings. The life cycle of Pisaura mirabilis is biennial in southern Scandinavia. Spiderlings hatch in July—August and reach maturity in May—June 2 years later. Mature males can be found until July, whereas females may be seen until October (unpublished data).
The first phase of courtship includes the catching of a prey; the prey is
then wrapped up in silk to a white parcel. The prey may, for example, consist
of an insect or a spider (Nitzsche,
1988). The male walks about searching for a female, probably
following draglines of mature females. When the male finds a mate, he offers
the gift, and the female moves slowly towards him. The male leans further and
further backward with the gift raised upwards as she advances. When the female
reaches upwards and takes hold of the gift in her chelicerae, the male
readjusts his position and swivels around until his head is underneath her
sternum. The male is then facing the opposite direction in a nearly inverted
position under her sternum. While the female is eating, the male couples his
pedipalp with the female's epigyne and sperm is transferred. The male usually
uses both pedipalps in one copulation. At each change of palp he reenters the
start position and takes hold of the gift with his chelicerae
(Bristowe, 1958; unpublished
data).
Copulating pairs can be found in southern Scandinavia from May to July.
Mature females bearing egg sacs in their chelicerae can be seen in June to
July (unpublished data). The female carries the sac for about 3 weeks and
probably does not feed during this period. When spiderlings are ready to
emerge, the egg sac is attached to the vegetation and a tent of silk (a
nursery web) is spun over and around it. The mother stays on guard outside of
the tent. During this time the females feed and have even been observed to
mate again (Austad and Thornhill,
1986; personal observation). The emerged spiderlings disperse
within a week. The female probably seldom produces more than one egg sac in
her lifetime (Austad and Thornhill,
1986; personal observation). However, under laboratory conditions
females are able to produce more than one sac
(Drengsgaard and Toft, 1999;
this study).
Collection and rearing conditions
Juvenile and subadult spiders were collected 1-2 May, 1996, from grasslands
surrounding the Mols Laboratory close to Aarhus, eastern Jutland, Denmark.
Initially, the spiders were kept individually in 30 ml plastic tubes. In the
laboratory the spiders were housed individually in plastic terraria (16
x 10 x 9 cm). In each terrarium some woody branches and a vial
containing water and moss (Sphagnum spp.) were provided. The spiders
were kept at room temperature (ca 20°C) and at natural photoperiod. Until
adulthood, spiders were fed ad libitum with laboratory reared field
crickets, Gryllus bimaculatus. After adulthood was reached the
spiders were kept on a diet of one cricket (mass ca 13 mg) per day.
Mating experiments
Experiments were conducted between 18 May and 6 June, 1996. Laboratory
reared field crickets of different instars were used as prey. Spider pairs
were randomly chosen and allotted into one of four groups. Males in group 0
had no gift to offer the female while males in groups S, M, and L were given
prey of ascending, not overlapping, weights
(Table 1). The volume of the
cricket used as a medium sized gift was similar to gift volumes found in the
field (Nitzsche, 1988;
personal observation).
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Observations on mating behavior were made in transparent plastic terraria
(45 x 27 x 14 cm). The inside bottom of each box was covered with
paper towels. Each female was placed in a separate box 1 day before the mating
experiment. While running and walking around the female produced draglines,
which are essential stimuli for the male in search for a mate (see Study
organism section). On the day of experiment, the box was divided into two
parts by a wall. The male was introduced to the part not occupied by the
female. When the male touched the drag-lines made by the female, he reacted by
"sexual excitement" that involves behavioral elements as trembling
of the palps and abdomen, jerking of the body, moving in jerks, and rapid
rubbing of the legs (Lang,
1996). When the male exhibited these behaviors a prey was
delivered to the male, and the male immediately started to wrap up the prey.
Five min later the partition wall was removed and the experiment started
(t = 0). Males in group 0 (without a nuptial gift) were treated in
the same way, except that trials started 5 min after the male first showed
"sexual excitement."
A total of 40 pairs (10 pairs per treatment group) were followed continuously during courtship and mating, and detailed notes about mating behavior were kept by means of a tape recorder. Trials where physical contact was not made within 80 min were interrupted, and the pair was replaced and removed from further analyses (three pairs in group 0, and one pair in group 2). Trials where copulation did not start within 60 min from first physical contact were interrupted and duration of copulation was set to 0 min (five pairs in group 0). Spiders were observed until the female or male terminated the copulation. Copulation duration is here defined as the time during which the male's pedipalp was coupled to the female's epigyne and was accompanied by clearly observable pulsations of the membranous base of the embolus. The female was fed one cricket (mass ca 13 mg) per day until an egg sac was produced. No food was provided during the period when the female carried the egg sac. When spiderlings emerged or the egg sac was abandoned by the female, the spiderlings, larva, prelarva, and unfertilized eggs were preserved in 70% alcohol. The feeding regime was then resumed and the female was allowed to produce a second sac. In addition, 42 trials were performed to increase sample sizes on male mating success and female reproductive success. These trials were not observed continuously but were checked with intervals of 5 min. Pairs were allowed to cohabit during 4 h, then they were separated. These females were fed (see above) and allowed to produce one egg sac.
Each individual was used only once. At mating, female age (i.e., number of days since maturity) was on average 6.6 days (SD = 1.7, n = 82) and male age was 6.6 days (SD = 2.0, n = 82). There were no differences in age between groups 0 to L, either among females or males (Kruskal-Wallis test, p =.47, n = 82, and p =.81, n = 82, respectively). Female, male, and spiderling sizes were measured as the maximum carapace width, using a Wild stereo microscope with an ocular eyepiece after they had been preserved in 70% alcohol. Female size was on average 3.6 mm (SD = 0.2, n = 81; one female's carapace in group M was destroyed during handling and consequently not measured) and male size was 3.4 mm (SD = 0.2, n = 82). There were no differences in size between groups 0 to L, either among females or males (Kruskal-Wallis test, p =.98, n = 81, and p =.57, n = 82, respectively). From each egg sac, 15 spiderlings were randomly chosen and measured. If the sac contained less than 15 spiderlings, (two sacs in group S [n1 = 1, and n2 = 8 spiderlings, respectively] and one in group M [n = 2 spiderlings]), I measured them all. Some egg sacs were opened prematurely (two in group M and one in group L). This meant that the proportion of fertilized eggs could be measured, but not spiderling size.
Statistical analyses were performed using StatView 5.0 software
(SAS, 1998). Data were checked
for normality before performing tests. Some data were normally distributed but
others were still nonnormally distributed after transformations, hence both
parametric and nonparametric tests were used.
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RESULTS |
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Mating behavior in relation to the nuptial gift
Generally, the male made the first physical contact, and the female remained inactive. There were no time differences for first physical contact between experimental groups (Kruskal-Wallis test, p =.56, n = 40; Table 2). The time until the female took hold of the gift (female acceptance) did not vary with gift size (Kruskal-Wallis test, p =.32, n = 30; Table 2). Physical contact did not necessarily end in copulation. However, 29 out of 30 males with a gift copulated, while only 50% of the males without a gift managed to copulate (Table 2). If all trials were included, that is, also trials that were not continuously observed, the corresponding figures for accomplished copulations in groups 0 to L were 40%, 85%, 95%, and 90%, respectively (Table 3). Among continuously observed matings all males without a gift courted and tried to mate, but the absence of a gift seemed to make it more difficult to enter mating position. There was a significant difference between groups regarding starting time for copulation (Kruskal-Wallis test, p =.04, n = 34). Copulation start was delayed in group 0 compared to group M (Table 2).
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Usually, the female terminated the copulation. In total 26 out of 34 copulations (76%) were terminated by the female (Figure 1). In all these trials the female interrupted while the male's pedipalp was inserted in the epigyne. She got loose and ran away, leaving the male on the spot. All copulations in the group without a gift were terminated by the female; in groups S to L the corresponding proportions were 89%, 80%, and 50% (Figure 1). Four males that terminated copulations were all allowed to copulate for a long time (>90 min). In the remaining four trials I had difficulties in deciding who terminated the copulation (Figure 1). These trials ended up with the male suddenly running away from the mating spot, leaving the female (and gift) behind.
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In 24 out of 29 cases (83%) the female had the gift when copulation was terminated. She often terminated the copulation herself and then ran away with the gift (in 19 out of 24 cases, 79%). Only four out of 29 cases (14%) ended with the male keeping the gift. In one trial only (in group S) the female ate up the gift before copulation ended. All females, however, consumed their gifts after copulation was terminated. In one trial (in group S) the female made the first physical contact in an aggressive way, and the male dropped the gift and ran away and no copulation was accomplished.
No male was cannibalized during the experiment (n = 82 pairs), although the female had several opportunities to do so. There were, however, some aggressive interactions between females and males, but these occurred only when the male had a gift to offer. Aggressions consisted of fights in trials where the copulation was ended by the female and where the female ran away with the gift. In 12 out of 19 cases (nS = 4, nM = 3, and nL = 5), these actions were accompanied by aggressive fights.
There was a significant positive relationship between size of the gift and duration of copulation (Spearman correlation, rs =.63, p =.0003, n = 34; Figure 2).
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Reproductive success in relation to the nuptial gift
In total, 77 out of 82 females (94%) produced egg sacs. Because only 64
females out of 82 were observed to copulate, females obviously could produce
an egg sac without copulation (Table
3). An egg sac was produced by 62 (97%) out of 64 mated females,
two females failed because they died shortly after copulation and two females
produced sacs without eggs. A second sac was produced by 31 out of 40 females;
two of these were empty (Table
3). Females producing empty sacs were excluded from further
analyses.
Laying date for the first egg sac was recorded for 59 females
(Table 3). An analysis of
covariance with gift size (0—L) as factor and female size (cephalothorax
width) as covariate indicated that the number of days between mating and
oviposition differed significantly between groups (F3,53 =
3.033, p =.037). The interval was not influenced by female size
(F1,53 = 0.045, p =.83) or an interaction between
gift size and female size (F3,50 = 0.87, p =.46).
However, post hoc tests (Scheffé) failed to
reveal any significant differences between group means (p 
.087),
and there was no indication that the mating-oviposition interval was
correlated with gift size (Table
3).
The total number of eggs in the first egg sac (fecundity) did not differ between experimental groups (Table 3). An analysis of covariance with size of nuptial gift as factor and female size as covariate showed that fecundity was significantly influenced by female size (F1,54 = 7.80, p =.0072), but not by nuptial gift size (F3,54 = 0.88, p =.46) or an interaction between these two variables (F3,51 = 0.11, p =.95). A comparison of the total number of eggs in the first egg sac of females that did (mean value = 146.0, SE = 7.0, n = 51) and did not (mean value = 125.5, SE = 10.7, n = 8) receive a gift indicated no difference between groups. Fecundity was significantly influenced by female size (ANCOVA, F1,56 = 8.029, p =.0064), but not by gift size (F1,56 = 2.58, p =.11), the interaction being not significant (F1,55 = 0.036, p =.85).
There were no significant differences between groups in total fecundity for mated females producing two sacs with eggs (Table 3). An analysis of covariance showed that total fecundity was significantly influenced by female size (F1,24 = 7.42, p =.012), but not by size of the nuptial gift (F3,24 = 0.35, p =.79) or an interaction between these variables (F3,21 = 0.27, p =.84). A comparison of total fecundity of females that did (mean value = 232.1, SE = 14.4, n = 24) and did not (mean value = 219.6, SE = 31.9, n = 5) receive a nuptial gift indicated no difference between groups. Total fecundity was significantly influenced by female size (ANCOVA, F1,26 = 7.70, p =.010), but not by gift size (F1,26 = 0.48, p =.50), the interaction being not significant (F1,25 = 0, p = 1.0).
Only 33 out of 60 mated females (55%) produced fertilized eggs in their first sac, and 17 out of 29 mated females (59%) produced fertilized eggs in the second sac. In spite of a great variation in offspring production there was a positive relationship between the duration of copulation and the percentage of fertilized eggs in the first egg sac (Spearman correlation, rs =.37, p =.035, n = 33; Figure 3), that is, the longer the copulation the more eggs were fertilized. This correlation was even more pronounced when the proportion of fertilized eggs based on females producing two sacs was analyzed (rs =.52, p =.0062, n = 29).
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An analysis of covariance indicated a significant difference in spiderling
size between experimental groups (F3,24 = 3.022,
p =.049). Spiderling size was not influenced by female size
(F1,24 = 0.005, p =.94) or by an interaction
between gift size and female size (F3,21 = 0.57,
p =.64). However, post hoc tests
(Scheffé) failed to detect any significant
differences between group means (p .11), and there was no
indication that spiderling size was correlated with gift size
(Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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My experimental results showed that no male without a gift was cannibalized. The presence and size of the nuptial gift affected male mating success in at least three ways: (1) a male with a gift was more successful in accomplishing a copulation than a male without a gift, (2) the larger the gift, the longer the copulation, and (3) the longer the copulation, the more eggs were fertilized. Female reproductive success in terms of timing of reproduction, fecundity and offspring size was not statistically significantly affected by the presence or the size of the nuptial gift. In this discussion I will argue that the nuptial prey gift in Pisaura mirabilis mainly functions as male mating effort.
Male protection against sexual cannibalism?
Bristowe wrote "Variations in the normal [mating] procedure add spice
to the story and a male who has been put in a female's enclosure with no fly
to offer has been eaten himself"
(Bristowe, 1958: 187). Ever
since then his suggestion that the nuptial prey gift in Pisaura
mirabilis function as a protection against sexual cannibalism has been
cited (see Austad and Thornhill,
1986; Elgar, 1992;
Foelix, 1996). However, this
hypothesis has up to now never been tested. If it is true one would expect
that males without a gift should not approach or court females, females should
attack and consume courting males without a gift more often than males with a
gift, and aggressions should be more common when a gift is missing. These
predicted behaviors were not observed in my experiment. My observations on the
mating behavior of males without a gift rather indicated that the failure to
accomplish copulation was due to difficulties to enter and remain in mating
position.
I varied only presence and size of the gift in my experiment. Under field
conditions there is probably a lot more variability: from a female
perspective, for example, mating experience (naive or not), age, hunger,
reproductive status, number of available mates, and male size. All these
variables may theoretically affect the female cannibalistic behavior towards a
courting male (Newman and Elgar,
1991). Empirical studies on cannibalistic praying mantises
(Birkhead et al., 1988) and
redbacked spiders (Andrade,
1998) indicate that hungry females are more aggressive towards
males than well-fed females. In contrast, Arnqvist and Henriksson
(1997) found no indication of
female food availability/consumption on females' decision to mate or attempt
to cannibalize courting males in Dolomedes fimbriatus (Pisauridae).
Possibly, sexual cannibalism may occur in Pisaura mirabilis if other
variables are manipulated, but nevertheless my results suggest that sexual
cannibalism is not common.
Although I did not find any case of sexual cannibalism in this laboratory
experiment (n = 82 trials), I have observed it about five times under
laboratory conditions (n > 200 trials, unpublished data). This
frequency of sexual cannibalism is in accordance with laboratory observations
made by Austad and Thornhill
(1986) and Drengsgaard and Toft
(1999). In all these cases the
male had a nuptial gift. As far as I know, no field data on sexual cannibalism
in Pisaura mirabilis have been published. The absence of a distinct
sexual size dimorphism in Pisaura mirabilis
(Lang and Klarenberg, 1995;
unpublished data) may explain part of the low cannibalism rate. The ability of
a female to capture a male may depend on his size relative to the female
(Elgar, 1992).
Paternal investment?
If the nuptial gift in Pisaura mirabilis functions as paternal
investment, one would expect that female fecundity or offspring fitness is
affected: the larger the gift, the more fecund the female and the larger the
size of the offspring. I found no support for this hypothesis. Female
fecundity and spiderling size did not differ significantly among the
experimental groups.
Austad and Thornhill (1986)
have studied food consumption and its reproductive significance for
Pisaura-females. The authors suggested that nuptial feeding provide a
direct reproductive benefit to females. Austad and Thornhill found that
tripling the feeding rate affected reproduction by increasing fecundity and
decreasing the interval between mating and oviposition. Fecundity and the
mating-oviposition interval were not affected in my experiment with
single-mated females. But since Austad and Thornhill assigned females to
different feeding regimes already during penultimate stages, their results can
be interpreted as large females (measured as sclerotized size) reproducing
better than small females.
My results suggested that fecundity was related to female size, that is,
the width of the sclerotized cephalothorax, rather than to presence and size
of the nuptial prey gift. Sclerotized adult size typically explains a very
large proportion of both intraspecific (e.g.,
Arnqvist and Henriksson, 1997
and references therein; Austad and
Thornhill, 1986) and interspecific
(Marshall and Gittleman, 1994)
variance in fecundity of spiders. The size of a sclerotized part as the
cephalothorax is determined at the maturity moult and is not affected by the
female foraging as an adult (Foelix,
1996). Because food consumption in preadult stages determines
subsequent adult sclerotized size, the foraging success in preadult stages
appears relatively more important than adult food consumption to determine
female fecundity (see Arnqvist and
Henriksson, 1997 and references therein). To conclude, it seems
unlikely that one prey item donated by a single Pisaura male during
courtship should significantly affect female fecundity.
Food donation may, however, become important for female reproductive
success if females mate with several males and receive several gifts.
Pisaura females have been observed to mate with more than one male,
both in the field (Austad,
1984; Austad and Thornhill,
1986;) and in the laboratory
(Drengsgaard and Toft, 1999;
unpublished data). If females are polyandrous in Pisaura mirabilis,
this further weakens the paternal investment hypothesis. On theoretical
grounds, males are unlikely to have been selected to provide parental
investment before fertilization because of the uncertainty of parentage
(Alexander and Gerald, 1979;
Gwynne, 1984a;
Wickler, 1985). Existing
observations on Pisaura mirabilis suggest that the male cannot be
sure that the gift will benefit his offspring. First, a first male sperm
priority pattern seems to exist, but males late in mating order can obtain a
large proportion of the fertilizations
(Drengsgaard and Toft, 1999).
Second, there is a long interval (ca 2 weeks) between female maturation and
oviposition (Drengsgaard and Toft,
1999; unpublished data), and spider eggs are not fertilized until
oviposition (Foelix, 1996).
This enables the female to mate with several males, especially since females
seem to have short non-receptive periods
(Drengsgaard and Toft, 1999;
unpublished data). Third, the male is unable to monopolize the female, mainly
because females live longer than males
(Austad, 1984;
Drengsgaard and Toft, 1999;
personal observation).
Male mating effort?
I found that males without a gift were allowed to court and copulate, but
they were not as successful in obtaining matings as males with a gift. This
observation suggests that the nuptial gift functions to entice the female to
copulate. Earlier papers on Pisaura mirabilis (e.g.,
Austad and Thornhill, 1986;
Lang, 1996) claim that females
never copulate unless the male offers a nuptial gift (but see
Nitzsche, 1988). The present
study, however, shows that naive and virgin females under laboratory
conditions do allow males without a gift both to mate and to father
offspring.
Absence of a gift seemed to obstruct the male in maneuvering the female into mating position (see Study organism section). Because of this, the male had difficulties in reaching the female's epigyne. Consequently, my results suggest that the nuptial prey gift in Pisaura mirabilis also facilitates coupling. This aspect may, however, be a secondary consequence arising after this mating behavior first evolved.
I found a significant positive correlation between nuptial prey size and
copulation duration. This relation has also been observed in four species of
bittacid hangingflies (Alcock,
1979; Gwynne,
1984b; Thornhill,
1976b,
1983), and one dance-fly
(Svensson et al., 1990). I
also observed a significant positive correlation between copulation duration
and the proportion of hatched offspring. This type of evidence concerning
nuptial prey gifts, as far as I know, has never been published before. My
result suggests that there may be a positive relation between copulation
duration and number of sperm transferred. Such clear positive relations in
gift-giving species have been documented by Thornhill
(1976b), and by Sakaluk
(1984). Consequently, my
results suggest that the prey gift in Pisaura mirabilis, besides
enticing the female to copulate and facilitating coupling, also increase sperm
transfer. However, copulation duration and fertilization rate also varied
within experimental groups, indicating that gift size was not the only source
of variance in male success.
Recently, Drengsgaard and Toft
(1999) showed that a first
male sperm priority pattern is operating in Pisaura mirabilis. This
result is in accordance with the hypothesis that the sperm precedence in
Pisaura mirabilis is a consequence of female spermathecae anatomy
(Austad, 1984). However,
Drengsgaard and Toft (1999)
also observed that some males late in mating order obtained a large proportion
of the fertilizations, especially if their copulation duration exceeded that
of previous males. Thus, combining findings of Drengsgaard and Toft
(1999) with my results
suggests that the donation of a prey gift is associated with countering the
effects of sperm competition. Females use sperm from more than one male when
mated with several males (Drengsgaard and
Toft, 1999), and the results of this study suggest that the
proportion of a female's eggs fertilized by a given male is correlated with
the size of his gift. A male donating a large gift may dilute or displace
rival sperm, thereby increasing his own success
(Elgar, 1998).
Generally the female interrupted the copulation, and thereby she controlled
the length of the copulation. The proportion of copulations terminated by the
female seemed to decrease with increased size of the nuptial gift. Since
females terminated copulations before finishing eating, and continued eating
afterwards, it was not a passive consequence of larger gifts taking longer to
consume (Vahed, 1998). My
observations suggest that the female actively favored large gifts.
Interrupting the copulation, the female seemed to affect the proportion of
fertilized eggs. Females allowing short copulations had a low reproductive
success in terms of fertilized eggs. This behavior seems nonadaptive unless
the female can be sure that several males under natural conditions will court
her. The most obvious reason for Pisaura females being polyandrous is
that each courting male donates a food item, that is, the female obtains
nutritional benefits in return for mating. This study shows that one gift did
not markedly affect female fecundity. Male donations may, however, become
important for female fecundity (Austad and
Thornhill, 1986; Elgar,
1998) or longevity if they mate with several males. Longevity is
probably of great importance for female reproductive success
(Stlhandske, in preparation). While trading
copulation time against gift size, the female may encourage several males to
copulate. The females may always benefit, and males that are able to catch and
handle large prey may often also benefit. However, the aggressive encounters I
observed, always involving a nuptial gift, suggest that female and male
interests do not always coincide.
|
ACKNOWLEDGEMENTS |
|---|
I thank B. Gunnarsson, M. Andersson, D. Blomqvist, M. Elgar, S. Toft, and one anonymous referee for constructive comments on earlier versions of the manuscript. I also thank the staff of Mols Laboratory in Denmark for hosting the fieldwork, and I. Blindow and G. Kudo for translating papers written in Dutch and Japanese, respectively. This work was funded by Anna Ahrenbergs fond för vetenskapliga m fl ändam
l,
Rdman och Fru Ernst Collianders stiftelse,
Evers och COs fond för
vetenskapsmäns studier i Danmark, Kungliga och
Hvitfeldtska stipendiestiftelsen, Royal Swedish Academy of Sciences, and
Wilhelm och Martina Lundgrens Vetenskapsfond. Financial support was also
received from the Swedish Natural Science Research Council by a grant to B.
Gunnarsson. |
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