Behavioral Ecology
doi:10.1093/beheco/arj037
Advance Access publication 11 January 2006
Emasculation to plug up females:
the significance of pedipalp damage in
Nephila fenestrata
Lutz Fromhagea,b and Jutta M. Schneidera,b
Biozentrum Grindel, University of Hamburg, Martin-Luther-King, Platz 3, Hamburg D-20146,
Germany, and bInstitute of Evolutionary Biology and Ecology, University of Bonn,
An der mmenburg 1, D-53121 Bonn, Germany
a
Female multiple mating selects for male adaptations that maximize fertilization success in a context of sperm competition. While
male mating strategies usually reflect a trade-off between present and future reproduction, this trade-off is largely removed in
systems where the maximum number of matings for males is very small. Selection may then favor extreme mechanisms of
paternity protection that amount to a maximal investment in a single mating. Males in several arthropod taxa break off parts
of their copulatory organs during mating, and it has frequently been suggested that mutilated males can thus secure their
paternity. Nevertheless, such a mechanism has rarely been confirmed directly. Here we study the golden orb spider Nephila
fenestrata, which has a mating system with potentially cannibalistic, polyandrous females, and males that are often functionally
sterile after mating with one female only. We show that males in this species can indeed protect their paternity by obstructing the
female’s genital openings with fragments of their copulatory organs. Key words: Araneoidea, mating plug, paternity protection,
pedipalp damage, sexual cannibalism. [Behav Ecol 17:353–357 (2006)]
ale animals, especially in species where males provide
little or no parental investment, are generally expected
to maximize their fitness by mating with several females
(Bateman, 1948; Clutton-Brock and Vincent, 1991; Trivers,
1972). There are, however, exceptions to this rule. Monogyny
(male monogamy), in the absence of a noticeable parental investment by males, is a rare but taxonomically widespread mating strategy that occurs in mammals (Brotherton and Rhodes,
1996), fish, mollusks, crustaceans (Vollrath, 1998), insects
(Moritz and Southwick, 1992) and spiders (Andrade, 1996;
Foellmer and Fairbairn, 2003). Theory suggests that monogyny
may have evolved in these systems because males attained an
advantage through maximally investing in paternity protection
(Fromhage et al., 2005; see also Andrade, 1996; Thornhill and
Alcock, 1983; Yamamura and Tsuji, 1989). Nevertheless, relatively little is known about the mechanisms by which monogynous males protect their paternity. Notable exceptions include
the dwarf antelope Madoqua kirkii, where males engage in mate
guarding (Brotherton and Rhodes, 1996), the redback spider
Latrodectus hasselti, where males increase their paternity by actively sacrificing themselves to cannibalistic females (Andrade,
1996), and the spider Argiope aurantia, where males die spontaneously during copulation to form whole-body mating plugs
(Foellmer and Fairbairn, 2003). In a number of spider and
insect species, monogynous males regularly incur damage of
their copulatory organs during mating (e.g., Andrade, 1996;
Knoflach, 2002; Knoflach and van Harten, 2001; Monnin and
Peeters, 1998; Moritz and Southwick, 1992), and it has been
suggested that the mutilated males can thus secure their paternity. Nevertheless, the putative effect of copulatory organ damage on paternity has rarely been confirmed directly (but see
Snow and Andrade, 2005; Snow et al., 2005).
M
Address correspondence to L. Fromhage. E-mail: lutzfromhage@
web.de.
Received 29 July 2005; revised 12 December 2005; accepted 14
December 2005.
The Author 2006. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
Here we study the golden orb web spider Nephila fenestrata,
where males often damage both of their paired mating organs,
the pedipalps, while copulating with a single female (Fromhage
and Schneider, 2005a). We hypothesize that pedipalp breakage
may prevent female remating by placing a physical barrier
inside the female tract (the mating plug hypothesis) or because
pedipalp fragments provide a cue by which subsequent suitors
are deterred from mating (the nonvirginity cue hypothesis). If
an N. fenestrata female mates with two males, the relative number of copulatory insertions achieved per male predicts paternity (Fromhage and Schneider, 2005a). We hence evaluate the
significance of male pedipalp damage with respect to the number of insertions achieved by a subsequent suitor.
We also study another aspect of mating behavior that
involves physical damage to males. During copulation,
N. fenestrata males often cast off (autotomize) some of their
anterior legs when attacked by the potentially cannibalistic
female. Copulation then continues while the female consumes the legs. We manipulate the opportunity for leg autotomy to assess potential effects on male copulation success and
sexual cannibalism.
METHODS
Spiders were F2 offspring derived from 74 individuals collected in 2003 in KwaZulu-Natal, South Africa. Females were
housed in separate Perspex frames (60 3 60 3 12 cm), where
they built typical orb-webs. They were watered on 6 days per
week, fed 5–8 Calliphora flies 2–3 times per week, and weighed
on the day after their final molt. Their fixed body size was
taken by measuring the tibia-patella length of a foreleg with
calipers after the experiment. Males were maintained in individual cups (150 ml) on a diet of Drosophila. On the day after
the final molt, each male was weighed and the tibia-patella
length of a foreleg was measured while he was anesthetized
with CO2.
Sexual cannibalism in N. fenestrata reduces male fitness by
precluding the possibility of postcopulatory mate guarding
Behavioral Ecology
354
(Fromhage and Schneider, 2005a,b). Autotomy might lower
the risk of cannibalism because lost legs are consumed by the
female, and mating with feeding females has been shown to
be less risky for males (Fromhage and Schneider, 2005a). To
manipulate the opportunity for leg autotomy, we experimentally removed males’ forelegs (‘‘foreleg autotomy’’ treatment;
n ¼ 18), predicting that males without forelegs (the legs most
frequently lost in normal matings) should be more prone to
cannibalism than others. To control for potential effects of leg
loss per se, we used the following control treatments: in the
‘‘autotomy control’’ treatment (n ¼ 17) we removed one leg
on either body side, randomly chosen from all legs excluding
the forelegs. In the ‘‘intact control’’ treatment (n ¼ 17) we
handled males similarly but removed no legs. Each leg to be
removed was grasped with tweezers, which lead to its immediate detachment by the male. Males were left for at least 24 h
after this procedure before being used in the experiment.
To initiate a trial, we introduced a (control or experimental) male into an upper corner of the female’s web. If mating
did not occur within 5 h, the male was removed and introduced again 7 days later. This was repeated again if necessary.
If mating did still not occur at this stage (N ¼ 3), both male
and female were excluded from the experiment. After mating,
males were removed from the web and a second, unmanipulated, male was introduced as described above. At this stage,
we gave the female a mealworm (Tenebrio molitor), so that the
second male could safely initiate mating while the female was
feeding. We thus offered favorable mating conditions to second males, which provides a conservative test of the hypothesis
that emasculation can prevent female remating. The second
male was given 3 h to initiate mating. After this period, he was
removed and reintroduced 7 days later for a period of 5 h. We
recorded all mating activities as well as occurrences of leg loss
and cannibalism. Females did not significantly differ between
treatments in mass, age, or fixed body size; nor did first or
second males (Kruskal-Wallis tests, all v22 , 3:38, p . .19).
Males used one or both of their pedipalps for one copulatory insertion each; hence measurements of copulation duration include 1–2 insertions. Copulation was usually preceded
by repeated poking of the female’s genital openings with the
male’s pedipalps, which we refer to as pseudocopulation (PC).
PCs are much shorter than true copulations, lack rhythmical
movements typical of the latter, and do not result in measurable paternity gains (Fromhage and Schneider, 2005a). Because males perform PCs more or less continually between
mounting a female and the beginning of copulation, we quantified pseudocopulatory activity as the time a male spent
mounted on a female (hereafter PC-duration) before his first
copulatory insertion. If no copulation occurred, PC-duration
refers to the total time a male spent mounted on a female.
Figure 1
Mated Nephila fenestrata male, ventral view (legs removed). The
conductor (C) is intact on the right pedipalp but missing on the left
side (asterisk). Scanning electron microscope image.
the pedipalp (Figure 1) that is anchored to the female’s genitals during copulation. The embolus (Figure 2) is a flexible
tube that is normally hidden within the conductor, but it
can be extended during copulation to enter the female’s
spermatheca.
Statistical analyses
Statistical analyses were carried out with JMP 5.0. Where possible, data were transformed to fit a normal distribution. We
used both parametric and nonparametric tests as appropriate.
For details of the tests used, see Sall et al. (2005). Sample sizes
can differ between analyses because not all data were available
for all trials. Means are given 6SE.
Ethical note
Autotomy is very common in spiders in nature and is considered an adaptive mechanism to prevent predation. Spiders
Genital morphology
To detect pedipalp damage arising from mating, the males’
pedipalps were visually inspected before and after the experiment, using a 403 stereomicroscope. Similarly, the epigynum
of each female (a sclerotized structure where her paired genital openings are located; Figure 2) was inspected after each
episode of cohabitation by a male. To detect pedipalp fragments inside insemination ducts and spermathecae, each female’s genital tract was excised after her death and macerated
with NaOH. Specimens used for electron microscopy were
dehydrated in ethanol, dried in a Balzers CPD 030 critical
point dryer, coated with gold in a Balzers MED 010 sputtering
device, and examined in a Philips XL20 scanning electron
microscope.
The following details of male morphology are relevant to
our study: the conductor is a sclerotized, hook-like process of
Figure 2
Genital region of mated Nephila fenestrata female. Each genital
opening is plugged by a conductor (C) and its corresponding
embolus (E). Scanning electron microscope image.
Fromhage and Schneider • Emasculation in spiders
355
have a special muscular mechanism to detach limbs that have
been grasped, and the wound seals naturally with negligible
loss of body fluids (Foelix, 1996; Roth VD and Roth BM, 1984).
In this study, we invoked the natural autotomy response by
grasping a spider’s leg. All spiders survived this treatment
and resumed locomotory activity immediately afterward.
RESULTS
Pedipalp damage and second males’ copulation success
Of 78 pedipalps used by first males in the experiment, 75
(96%) were visibly damaged after use. The most common
kind of damage (55 instances, 71%) was a clear-cut loss of
the conductor (Figure 1). Conductor loss usually coincided
with loss of the corresponding embolus, so that the number of
emboli protruding from the epigynum (Figure 2) after mating
of the first male was predicted by his number of lost conductors (0–2; Spearman correlation: rs ¼ .86, p , .0001). Alternative kinds of pedipalp damage include blunted conductors,
and pedipalps with oddly protruding emboli. Examination
of macerated females revealed that broken emboli and conductors within the female tract were not always visible from
the outside. The copulatory pattern in N. fenestrata can be
either contralateral (i.e., his right pedipalp inserts into her
left opening and vice versa) or ipsilateral (i.e., right and left
pedipalp insert into the corresponding sides of the female).
Therefore it was often impossible to assign the origin of a particular embolus or conductor within a macerated female to
a particular male. Hence we decided not to use data obtained
through maceration to explain copulatory behavior of second
males. Maceration revealed that 15 of 50 females (30%) had
more than one embolus inside the same insemination duct.
One of these females even had three emboli inside a duct,
indicating that one of her sires had used both pedipalps to
inseminate the same duct.
Across treatments, the number of broken conductors of the
first male negatively predicted the number of insertions (0–2)
achieved by the second male (Figure 3; Spearman correlation:
rs ¼ .4, p ¼ .0042, N ¼ 49). However, a negative correlation
between the numbers of insertions achieved by the first and
the second male (as reported in Fromhage and Schneider,
2005) was marginally nonsignificant (Spearman correlation
rs ¼ .27, p ¼ .057, N ¼ 52). Second males’ body size and
mass did not predict their number of insertions (Spearman
correlations: rs , .04, p . .7, N ¼ 52).
Pseudocopulation
Across treatments, the PC-duration was much shorter for first
(5.68 6 1.33 min) than second males (38.16 6 7.85 min;
Wilcoxon matched-pairs signed-rank test: T ¼ 332.5, p ,
.0001). The PC-duration of second males was significantly
shorter in trials where a copulation eventually ensued (27.05 6
7.45 min), compared to trials where the second male did not
copulate (80.38 6 20.7 min; Wilcoxon rank sums test: N1 ¼
10, N2 ¼ 38, z ¼ 3.09, p ¼ .002). Moreover, PC-duration of
second males was positively predicted by the number of conductors lost by first males (Spearman correlation: rs ¼ .66,
p , .0001).
Depending on whether pedipalp fragments are mating
plugs or nonvirginity cues, PC may represent unsuccessful
copulation attempts or be a mechanism to assess female status
(cf. Suter, 1990). Hence, patterns of PC-duration may allow us
to distinguish between the mating plug and the nonvirginity
cue hypothesis. Because a female’s mating status should be
most easily detectable by a male when emboli are protruding
from both of her genital openings (as in Figure 2), we com-
Figure 3
Number of copulatory insertions achieved by the second male as
a function of the number of broken conductors of the first male.
Frequency of occurrence is reflected by marker size and given
numerically within each circle. Regression line included for display
purpose only.
pared second males’ PC-duration with such females to that
observed in the remaining cases. PC-duration with such females (83.21 6 19.66 min) was significantly longer than with
females bearing either one (34.2 6 10.6 min; Wilcoxon rank
sums test: N1 ¼ 12, N2 ¼ 20, z ¼ 2.73, p ¼ .0064) or no protruding embolus (9.31 6 11.85 min; Wilcoxon rank sums test:
N1 ¼ 12, N2 ¼ 16, z ¼ 4.05, p , .0001).
Autotomy treatment and first males’ copulation success
Although the treatment affected the opportunity for leg
loss during mating (Table 1), it did not significantly affect
first males’ number of insertions, PC-duration, copulation
duration, number of lost conductors, the number of emboli
protruding from the epigynum after mating, or sexual
cannibalism (Table 1).
DISCUSSION
Pedipalp damage in first males affected the behavior of second males such that the latter spent more time performing
PCs but achieved fewer copulatory insertions. These findings
suggest that pedipalp fragments reduced female remating by
presenting a physical barrier to future copulations, rather
than by revealing her mating status to subsequent suitors.
In contrast, we found no support for a role of male leg
autotomy in mediating mating success or in preventing sexual
cannibalism.
Males in many animal species employ mating plugs as
a mechanism to prevent female remating. Mating plugs can
be formed of secretory substances, as occurs in mammals
(Gomendio et al., 1998), spiders (Suhm et al., 1996), and insects (Sauter et al., 2001). Moreover, it has been suggested that
detached male mating organs may function as mating plugs
in spiders (e.g., Berendonck and Greven, 2002; Knoflach,
2002; Knoflach and van Harten, 2001; Schneider et al.,
2005) and insects (Kamimura and Matsuo, 2001; van Veen
and Sommeijer, 2000). To validate the latter view, however,
it is not sufficient to show that male parts remain attached to
the female after mating. For example, Winston (1987) argued
that detached male genitalia in the honey bee may reduce
Behavioral Ecology
356
Table 1
Effects of autotomy treatment on mating of first males
a
Dependent variable
Foreleg autotomy
Autotomy control
Intact control
Test
Legs lost per survivor
Mounting latency (min)
PC-duration
Copulation durationa (min)
Insertions (0–2)
Broken conductors (0–2)
Emboli protruding from epigynum (0–2)
% males cannibalized
0.7 6 0.26
118.71 6 23.15
8.19 6 2.36
100.61 6 26.52
1.5 6 0.17
1.17 6 0.19
0.89 6 0.18
44% (18)
1.89 6 0.42
123.82 6 23.15
5 6 2.29
137.18 6 24.15
1.7 6 0.11
1.07 6 0.18
0.94 6 0.18
47% (17)
2.57 6 0.43
124.89 6 23.15
4 6 2.29
123.94 6 23.29
1.59 6 0.12
1.13 6 0.18
0.88 6 0.19
18% (17)
v22 ¼ 8:88; p , .012
F2,48 ¼ 0.019, p ¼ .98
F2,47 ¼ 0.88, p ¼ .42
F2,47 ¼ 0.19, p ¼ .83
v22 ¼ 0:73; p , .70
v22 ¼ 0:19; p , .91
v22 ¼ 0:07; p , .97
G2 ¼ 4.19, p , .12
Test statistics indicate use of the following tests: G ¼ G-test, v2 ¼ Kruskal-Wallis test, F ¼ ANOVA.
Test performed on log-transformed data.
sperm flow from the queen’s vagina, rather than preventing
multiple matings. Similarly, Schneider et al. (2001) found no
evidence for broken pedipalp parts preventing female remating in a congener of our study species, Nephila plumipes.
Perhaps the clearest evidence reported so far for broken
copulatory organs acting as mating plugs exists for the spider
L. hasselti, where males break off a small part of the embolus,
the apical sclerite, inside the female tract (Snow and Andrade,
2005; Snow et al., 2005). Although the apical sclerite in
L. hasselti does not prevent other males from copulating into
the same genital opening, it does affect paternity by interfering with sperm transfer from the copulatory duct to the
spermatheca (Snow et al., 2005; see also Berendonck and
Greven, 2002).
In the present study, the number of conductors lost by the
first male negatively predicted the number of pedipalp insertions achieved by the second male. Because paternity in
N. fenestrata is determined by the relative number of insertions
of each male (Fromhage and Schneider, 2005a), this finding
suggests that pedipalp damage protects the paternity of first
males. However, female remating might be prevented either
because pedipalp fragments physically obstruct her openings
(the mating plug hypothesis) or because they reveal her
mating status to the successor who then refrains from mating
(the nonvirginity cue hypothesis). In the former case, PCs
performed by second males could be unsuccessful copulation
attempts. This interpretation is supported by a positive relationship between pedipalp damage of first males and PCduration of second males, as would be expected if more
mating plugs make subsequent copulations increasingly
difficult.
Alternatively, if pedipalp fragments are nonvirginity cues,
PCs may be a mechanism of mate assessment (cf. Suter,
1990). However, this interpretation is inconsistent with the
pattern of pseudocopulatory activity observed in our study:
although assessment of female mating status should be relatively easy when pedipalp fragments are visibly protruding
from both of her genital openings (see Figure 2), second
males’ PCs were particularly protracted in such cases. We conclude that pedipalp fragments are more likely mating plugs
than nonvirginity cues, and PCs are unsuccessful copulation
attempts rather than a mechanism of mate assessment.
While pedipalp damage of first males substantially reduced
mating success of second males (Figure 3), the presence of
more than one embolus inside the same insemination duct in
a proportion of females shows that the effectiveness of these
mating plugs was nevertheless limited. This may reflect constraints on male morphology or may be the result of opposing
selection acting on females: if females can benefit from poly-
andry (see Jennions and Petrie, 2000, for a review), then their
genitalia might evolve to counteract monopolization by their
first mate. In addition, if the frequent occurrence of mating
plugs in N. fenestrata generates a selective advantage for males
able to copulate with a female despite the presence of a rival’s
plugs, then this might further limit the effectiveness of plugging over evolutionary time.
Males will only benefit from placing mating plugs if the
advantage in terms of paternity protection outweighs the
associated costs. The extent to which N. fenestrata males incur
costs of pedipalp damage, however, is unclear. Intuitively one
might expect these costs to be high because the simultaneous
loss of the anchoring structure (the conductor) and the
sperm-transferring structure (the embolus) almost certainly
rules out any future use of the pedipalp. On the other hand,
the loss of these structures may not be costly once a pedipalp’s
sperm content has been transferred. In L. hasselti, for example, sperm transfer with a given pedipalp is ruled out by a prior
copulation with that pedipalp (Andrade and Banta, 2002) but
not by experimentally induced pedipalp damage (Snow et al.,
2005). This suggests that postmating male sterility in L. hasselti
is more likely a consequence of sperm depletion than of pedipalp damage and that pedipalp damage has negligible costs
(Snow et al., 2005). Similarly, sperm depletion has been reported in a congener of our study species, Nephila clavipes,
where the male’s pedipalps are rarely damaged, but are used
for multiple copulations with the same female (Christenson,
1989; Christenson et al., 1985). Although we do not know if
sperm depletion occurs in N. fenestrata, we note that we have
never seen N. fenestrata males copulating with a previously
used pedipalp—even if no physical damage of the pedipalp
was evident (Fromhage L, personal observation; see also
Fromhage and Schneider, 2005b).
It is worth noting that, under natural conditions, mating
plugs in N. fenestrata back up the effect of postcopulatory mate
guarding (Fromhage and Schneider, 2005a,b), which operates
before a rival can even reach the female. Mate guarding and
mating plugs are hence complementary mechanisms by which
N. fenestrata males can maximize their paternity with a single
female. Fromhage et al. (2005) have shown theoretically that
such a (monogynous) mating strategy can evolve only under
certain conditions, one of which is a male-biased sex ratio.
The present study highlights N. fenestrata as an ideal model
organism to test this prediction and thus sets the stage for
further research in this field.
We thank G. Uhl for assistance with electron microscopy. S. Nessler,
M. Plath, and G. Uhl provided helpful comments on the manuscript.
This research was supported by a DFG grant to J.M.S.
Fromhage and Schneider • Emasculation in spiders
REFERENCES
Andrade MCB, 1996. Sexual selection for male sacrifice in the
Australian redback spider. Science 271:70–72.
Andrade MCB, Banta EM, 2002. Value of male remating and functional sterility in redback spiders. Anim Behav 63:857–870.
Bateman AJ, 1948. Intra-sexual selection in Drosophila. Heredity 2:
349–368.
Berendonck B, Greven H, 2002. Morphology of female and male
genitalia of Latrodetus revivensis Shulov, 1948 (Araneae, Theridiidae)
with regard to sperm priority patterns. In: European Arachnology
2000, Proceedings of the 19th European Colloquium of Arachnology, Aarthus, Denmark, 17–22 July 2000 (Toft S, Scharff N, eds).
Aarhus, Denmark: Aarhus University Press; 157–167.
Brotherton PNM, Rhodes A, 1996. Monogamy without biparental care
in a dwarf antelope. Proc. R. Soc. Lond. B 263:23–29.
Christenson TE, 1989. Sperm depletion in the orb-weaving spider
Nephila clavipes (Araneae, Araneidae). J Arachnol 17:115–118.
Christenson TE, Brown SG, Wenzl PA, Hill EM, Goist KC, 1985. Mating behaviour of the golden-orb-weaving spider, Nephila clavipes: I.
Female receptivity and male courtship. J Comp Psychol 99:160–166.
Clutton-Brock T, Vincent ACJ, 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60.
Foelix RF, 1996. Biology of spiders, 2nd ed. Oxford: Oxford University
Press.
Foellmer MW, Fairbairn DJ, 2003. Spontaneous male death during
copulation in an orb-weaving spider. Proc R Soc Lond B
270(Suppl.):183–185.
Fromhage L, Elgar MA, Schneider JM, 2005. Faithful without care: the
evolution of monogyny. Evolution 59:1400–1405.
Fromhage L, Schneider JM, 2005a. Safer sex with feeding females:
sexual conflict in a cannibalistic spider. Behav Ecol 16:377–382.
Fromhage L, Schneider JM, 2005b. Virgin doves and mated hawks:
contest behavior in a spider. Anim Behav 70:1099–1104.
Gomendio M, Harcourt AH, Roldán ERS, 1998. Sperm competition in
mammals. In: Sperm competition and sexual selection (Moller AP,
Birkhead TR, eds). San Diego: Academic Press; 667–752.
Jennions MD, Petrie M, 2000. Why do females mate multiply? A review
of the genetic benefits. Biol Rev 75:21–64.
Kamimura Y, Matsuo Y, 2001. A ‘‘spare’’ compensates for the risk of
destruction of the elongated penis of earwigs (Insecta: Dermaptera). Naturwissenschaften 88:468–471.
Knoflach B, 2002. Copulation and emasculation in Echinotheridion
gibberosum (Kulczynski, 1899) (Araneae, Theridiidae). In: European
Arachnology 2000, Proceedings of the 19th European Colloquium
of Arachnology, Aarhus, Denmark, 17–22 July 2000 (Toft S, Scharff
N, eds). Aarhus, Denmark: Aarhus University Press; 139–144.
357
Knoflach B, van Harten A, 2001. Tidarren argo sp. nov. (Araneae:
Theridiidae) and its exceptional copulatory behaviour: emasculation, male palpal organ as a mating plug and sexual cannibalism.
J Zool 254:449–459.
Monnin T, Peeters C, 1998. Monogyny and regulation of worker
mating in the queenless ant Dinoponera quadriceps. Anim Behav 55:
299–306.
Moritz RFA, Southwick EE, 1992. Bees as superorganisms: an evolutionary reality. Heidelberg: Springer.
Roth VD, Roth BM, 1984. A review of appendotomy in spiders and
other arachnids. Bull Br Arachnol Soc 6:137–146.
Sall J, Creighton L, Lehmann A, 2005. JMP Start Statistics—a guide to
statistics and data analysis using JMP and JMP IN Software. Toronto,
Canada: SAS Institute Inc.
Sauter A, Brown MJF, Baer B, Schmid-Hempel P, 2001. Males of social
insects can prevent queens from multiple mating. Proc R Soc Lond
B 268:1449–1454.
Schneider JM, Fromhage L, Uhl G, 2005. Copulation patterns in the
golden orb-web spider Nephila madagascariensis. J Ethol 23:51–55.
Schneider JM, Thomas ML, Elgar MA, 2001. Ectomised conductors in
the golden orb-web spider, Nephila plumipes (Araneoidea): a male
adaptation to sexual conflict? Behav Ecol Sociobiol 49:410–415.
Snow LSE, Abdel-Mesih A, Andrade MCB, 2005. Broken copulatory
organs are low-cost adaptations to sperm competition in redback
spiders. Ethology (in press).
Snow LSE, Andrade MCB, 2005. Multiple sperm storage organs facilitate female control of paternity. Proc R Soc Lond B 272:1139–1144.
Suhm M, Thaler K, Alberti G, 1996. Glands in the male palpal organ
and the origin of the mating plug in Amaurobius species (Araneae:
Amaurobiidae). Zool Anz 234:191–199.
Suter RB, 1990. Courtship and assessment of virginity by male bowl
and doily spiders. Anim Behav 39:307–313.
Thornhill R, Alcock J, 1983. The evolution of insect mating systems.
Cambridge, Massachusetts: Harvard University Press.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual
selection and the descent of man (Campbell B, ed). Chicago:
Aldine; 1871–1971.
van Veen JW, Sommeijer MJ, 2000. Observations on gynes and drones
around nuptial flights in the stingless bees Tetragonisca angustula
and Melipona beecheii (Hymenoptera, Apidae, Meliponinae). Apidologie 31:47–54.
Vollrath F, 1998. Dwarf males. Trends Ecol Evol 13:159–163.
Winston ML, 1987. The biology of the honey bee. Cambridge,
Massachusetts: Harvard University Press.
Yamamura N, Tsuji N, 1989. Postcopulatory guarding strategy in a
finite mating period. Theor Popul Biol 35:36–50.