Behavioral Ecology Vol. 13 No. 2: 232–238
An experimental approach to altering mating
tactics in male horseshoe crabs (Limulus
polyphemus)
H. Jane Brockmann
Department of Zoology, University of Florida, Gainesville, FL 32611-8525, USA
Alternative reproductive tactics are often correlated with phenotype, density, environment, or social context. Male horseshoe
crabs (Limulus polyphemus) have two mating tactics that are associated with phenotype. Males in good condition arrive at the
nesting beach and spawn while attached to females, whereas those in poorer condition come ashore unattached and crowd
around the nesting couples as satellites, fertilizing eggs through sperm competition. The correlation between mating tactic and
phenotype may be due to males choosing tactics based on condition, or it may be that males that have not found a female
choose to come ashore as satellites. To distinguish between these two possibilities, I conducted an experiment on male horseshoe
crabs in the field at Seahorse Key on the northern Gulf coast of Florida. I prevented males from attaching to females by placing
small plastic bags over the claws they use to attach. The results showed that males in poor condition came ashore as satellites,
whereas males in good condition remained at sea. This means that mating tactics are cued by information about the male’s
condition and not about whether he found a female. The evolution of phenotype-correlated mating tactics can be represented
by a model in which the fitness of each tactic changes with condition and fitness curves cross. I hypothesize that male horseshoe
crabs in good condition have higher fitness when attached and that males in poorer condition do better when unattached. Key
words: alternative mating tactics, alternative reproductive behavior, alternative strategies, conditional strategies, frequency-dependent selection, horseshoe crabs, Limulus polyphemus. [Behav Ecol 13:232–238 (2002)]
A
nimals as different as bees (Alcock, 1979, 1996a,b, 1997;
Alcock et al., 1976, 1977; Danforth and Desjardins, 1999;
Starks and Reeve, 1999), elephant seals (Le Boeuf, 1974), and
sunfish (Gross, 1984; Gross and Charnov, 1980; Phillip and
Gross, 1994) show discrete patterns of male mating behavior
that are associated with differences in phenotype (Arak, 1983;
Campanella and Wolf, 1974; Gadgil, 1972; Hews et al., 1997;
Johnson et al., 2000, Maynard Smith, 1982; Moore et al., 1998;
Parker, 1982; Rubenstein, 1980; Thornhill, 1981; West-Eberhard, 1979). For example, in the beewolf (Philanthus pulcher,
a sphecid wasp), large males are territorial, whereas small individuals are not, and size is significantly correlated both with
the ability to defend a territory and with the probability of
mating (O’Neill, 1983). To understand and model such alternative tactics, we need to know both the cues used in making
decisions and the fitness associated with those decisions. For
example, in the beewolf, do males base their territorial decisions on size or on the ability to defend? Does fitness decline
if individuals choose a different tactic for their phenotype? To
acquire such information, one cannot rely on a correlation
using normally occurring behavior. Instead, one needs to
know how the animal behaves and its resulting success when
it cannot follow the usual tactic for its phenotype. This requires an experimental manipulation.
Male horseshoe crabs show variable mating tactics correlated with phenotype. Some search for females offshore (Barlow
et al., 1986) and come to the nesting beach in amplexus (attached), fertilizing their mates’ eggs as they are being laid in
the sand (external fertilization). Others come ashore without
females (unattached) and crowd around the nesting couples
as satellites (Brockmann, 1996). Satellite males fertilize signif-
Address correspondence to H.J. Brockmann. E-mail: [email protected].
edu.
Received 12 July 2000; revised 10 May 2001; accepted 23 May 2001.
2002 International Society for Behavioral Ecology
icant numbers of eggs through sperm competition (Brockmann et al., 1994). Attached males are, on average, lighter in
color, less worn, and have fewer fouling organisms than unattached individuals, all suggesting that they are, on average,
younger (Brockmann, 1996; Brockmann and Penn, 1992).
Unattached males are more likely to be overturned when they
come ashore (Penn and Brockmann, 1995), which may lead
to desiccation or predation (Botton and Loveland, 1989). Behavioral tests have demonstrated that many unattached males
will pair with females given the opportunity, but they are less
likely to find females, slower to attach, and more likely to let
go once attached (Brockmann and Penn, 1992).
A correlation between phenotype and behavioral tactic
could result from several different decisions. To demonstrate
whether males use information about their condition to
switch their behavior from one tactic to the other, I conducted
an experimental manipulation in which I prevented males
from attaching to females. If their behavioral tactics are the
result of a phenotype-cued decision rule, then males prevented from attaching that are in poor condition should come
ashore as satellites, whereas those in good condition should
remain at sea. Alternatively, if failure to attach is the cue, then
all males prevented from attaching should come ashore as
satellites regardless of condition.
METHODS
Study sites and times of study
This study was conducted on a wild population of horseshoe
crabs as they nested and mated on a 1-km stretch of sandy
beach on Seahorse Key (Penn and Brockmann, 1994). This
island is part of the Lower Suwannee National Wildlife Refuge
and is located 4 km southwest of Cedar Key (Levy County,
Florida, USA). With the help of field assistants, I conducted
observations on all high tides associated with the new and full
moons (high tides are especially high from 2 days before to
5 days after the new or full moon, and Florida horseshoe crabs
Brockmann • Mating tactics in Limulus
are particularly likely to nest during these times) for 7 weeks
between 6 March and 8 June 1993.
Observational procedures
During each high tide, my field assistants and I walked along
the 100 m beach shoreline from 1 h before each predicted
maximum high tide to 2–3 h after. This is the period during
which female–male pairs of horseshoe crabs arrive at the
shoreline and nest. Once the tide has receded, the pairs return to sea and await the next high tide. As males came to
shore, we picked them up, recorded their attachment status
(whether unattached or attached to a female), tagged them
with numbered embossing tape (Cohen and Brockmann,
1983), and placed them in plastic wading pools. We placed
these pools (1.2 m diameter, 20 cm high) at 25–50 m intervals
along the shoreline and filled them with 15 cm of fresh seawater before each tide. Before picking up a crab, we detached
attached males by carefully pushing their claws off the females’ terminal spines. Attached and unattached males were
picked up alternately and placed in pools so that equal numbers of each type were collected without respect to their condition. We measured (see below) the crabs 1–5 h after the
tide receded and released them at sea (still detached or unattached).
On the high tides after release, we searched the beach for
returning marked individuals and recorded their attachment
status. If an individual was seen more than once during a tide,
only the first encounter was used. Males were given consecutively numbered tags, so observers could not tell if the animal
had originally come to the beach attached or unattached.
When males were seen on three or more days, I characterized
them as following the attached tactic if seen attached more
than 75% of the time, as unattached if seen unattached more
than 75% of the time, or as following a mixture of tactics.
Experimental procedures
Males were prevented from attaching by placing small plastic
bags over the claws they use for attaching to females. This
experiment was conducted during the periods 5–8 April, 21–
23 April, and 3–4 May. We measured each male (see below),
marked him with a red tag (indicating that he was a part of
the experiment) and attached a pair of bags. To put on the
bags, the male was turned ventral side up, half a soft foam
plug was placed in each claw (between the basipodite and
epipodite), and a plastic bag was placed over each claw and
secured with a 4-cm twist tie around the base of the claw. The
twist tie was placed far enough up on the bag so that the bag
flared out slightly and was held in place and excess twist tie
was clipped off with scissors; the foam plugs, normally used
as Drosophila vial stoppers, were necessary to reduce shredding of the plastic bags with the claws. The male was then
released at the shoreline to return to sea. Equal numbers of
attached (males whose original attachment status had been
attached) and unattached (males whose original status had
been unattached) males were given bags over their claws. We
made the bags from 2-mil plastic (Kapak Scotchpak heat-sealable pouches) by cutting out two 3.5 ⫻ 6 cm plastic strips and
sealing them together along three sides with a heated rod
(Scotchpak brand Pouch Sealer; excess plastic was trimmed
off with scissors). This resulted in a rectangular-shaped bag
that just fit over the male’s claw (the bags were made in pairs
before the tide in slightly different sizes; during the tide we
tried on a few bags to get a good fit). With a foam stopper in
and bags over his claws, a male was unable to attach (unless
the bag became shredded, which happened after 1–2 weeks).
At the same time, we conducted a second experiment in
233
which attached and unattached males received just the twist
ties on the bases of their claws, but were otherwise treated in
the same way as the males with bags (the two experiments
were conducted on alternate males as they were taken from
the pools, so the two experiments were conducted at random
with respect to male condition). The males were marked,
measured, and turned on their dorsal surface; twist ties were
placed around the base of their claws (without the bags), and
they were released at the shoreline just like males with bags.
All data points were independent because no male was included in an experiment more than once.
We collected data on the return rates of males with bags
(so they cannot attach) and normal (males with twist ties that
can attach) crabs on the 3–5 tides after release. When we
found a male with a red tag, we recorded whether he was
attached or unattached and then we checked to see whether
the bags or ties were present (we simply lifted on edge of the
carapace and looked, which could be done without disturbing
the nesting crabs). If present, we picked up the male, untwisted the ties, and removed the bags or ties. We saw a large
portion of the males at least once after release, so most of the
males had their ties and bags removed by us. The twist ties
were made of thin metal wire with a paper covering, and they
rusted through after a few weeks.
Condition index and measurements
I estimated the condition of the males by constructing a simple index made up of five measures. (1) The dorsal prosomal
surface of Limulus changes color from a light tan in newly
molted animals to black, as the surface of the carapace erodes
over years (Brockmann and Penn, 1992). The surface color
was evaluated by visual examination and classified on a scale
of 1–5 (5 ⫽ no black anywhere; 4 ⫽ a few black scratches; 3
⫽ ⬍10% of surface black; 2 ⫽ 25–49% black; 1 ⫽ ⱖ50%
black). (2) As the carapace ages, it also shows changes in surface quality from completely smooth and covered with mucus
(on a scale of 1–5, a score of 5), to patches of mucus with no
pitting on the surface (score of 4), to no mucus and a few
pits (score of 3), to no mucus and ⬍10% of the surface pitted
(score of 2) to seriously eroded and pitted by chitinoclastic
bacteria and algae (score of 1). (3) Crabs also differed in the
condition of the eyes (both eyes in good condition ⫽ score
of 5; one eye soft or covered with epibiotic organisms ⫽ 3;
both eyes soft or covered ⫽ 1). (4) Males attach to the terminal spines of females, but males also hold on to the terminal spines of other males when in satellite groups, and
these may become worn or broken (both in perfect condition
⫽ score of 5; one of the terminal spines worn ⫽ 3, both worn
or broken ⫽ 1). (5) Males also differed in the percentage of
the dorsal surface covered with epibionts, such as barnacles,
slipper shells, and algae (Shuster, 1982; Sydlik and Turner,
1989; Turner et al., 1988). We estimated the percent of the
surface that was covered by epibiotic organisms, categorized
on a scale of 1–5 (5 ⫽ 0–4%, 4 ⫽ 5–9%; 3 ⫽ 10–19%; 2 ⫽
20–50%; 1 ⫽ ⬎50%; the scale was adjusted so that at least 10
individuals fell into each category).
These five measures of condition were combined in a simple index: if the animal showed the poorest condition in all
5 categories, he received a rank of 5; the highest rank in all
5 categories received a score of 25 (a middle rank in all five
categories received a score of 15). For some analyses this condition index was reduced to four categories (⬍15; 15–19; 20–
24; 25) to maintain adequate sample sizes for chi-square analyses. In addition, we measured the size of each crab by the
distance between its lateral eyes (IO, measured on the dorsal
surface between the eye spines using a tape measure; Brockmann and Penn, 1992). For crabs that were not involved in
234
Figure 1
The percentage of males with bags covering their claws (unable to
attach to females) in each condition index category that returned
to the nesting beach as satellites during the first week after the
manipulation. Sample sizes are given above each bar.
the bags/ties experiments, we also measured the lengths of
their telsons (from the dorsal process of the telson to the tip
using a tape measure), their carapace widths (CW; measured
on the ventral surface with a tape measure at the widest
point), the heights of their telsons at the highest point (using
a caliper), and their weights (WT, crab placed in a Styrofoam
bucket and weighed with a hand-held Pesola scale).
All analyses were conducted with Statview (SAS Institute,
1998). Descriptive data are presented as means ⫾ SEs.
RESULTS
Experimental
When males were released without a female and prevented
from attaching to females (with bags over their claws), 41%
(N ⫽ 93 of 225) returned to the nesting beach as satellites
on a subsequent tide during the same week. These returning
males were in significantly worse condition (but not different
in size) than those that did not return and remained at sea
(Figure 1; average condition index for those returning in the
first week is 20.3 ⫾ 0.43 and for those not 22.2 ⫾ 0.29; MannWhitney U test, N1 ⫽ 132, N2 ⫽ 93, Z ⫽ ⫺4.012, p ⬍ .0001).
If all males with bags are included, regardless of when they
returned, then 59% of males were seen again, and those that
were in worse condition were significantly more likely to be
seen (average condition index for those returning ⫽ 20.9 ⫾
0.35; for those not returning ⫽ 22.2 ⫾ 0.35; Mann-Whitney
U test, N1 ⫽ 90, N2 ⫽ 135, Z ⫽ ⫺2.665, p ⬍ .007). The original
attachment status of the males with bags significantly affected
their likelihood of returning: 33% of attached males (n ⫽
117) returned and 50% (n ⫽ 108) of unattached males returned within one week (␹2 ⫽ 6.8, df ⫽ 1, p ⫽ .01). This may
be because unattached males were in worse condition, on average, than attached males (Mann-Whitney U test, N1 ⫽ 225,
N2 ⫽ 171, Z ⫽ ⫺2.073, p ⫽ .038). Both condition and original
attachment status (but not size) played a role in whether
males with bags returned, regardless of whether their first return was during the first week after treatment (logistic regression, N ⫽ 225, ␹2 ⫽ 5.55, p ⫽ .01; for condition ␹2 ⫽
10.59, p ⫽ .001; for original status ␹2 ⫽ 5.07, p ⫽ .02) or any
Behavioral Ecology Vol. 13 No. 2
week (N ⫽ 225, ␹2 ⫽ 4.16, p ⫽ .04; for condition ␹2 ⫽ 4.6, p
⫽ .03; for original status ␹2 ⫽ 11.37, p ⫽ .0007).
The normal males (released with twist ties at the base of
their claws but otherwise treated like males with bags) behaved in much the same way. In this experiment 50% (N ⫽
86 of 172) of males returned within the first week. Males in
poor condition were significantly more likely to return than
those in good condition (average condition for returning
males ⫽ 20.5 ⫾ 0.41; for non-returning males ⫽ 22.0 ⫾ 0.31;
Mann-Whitney U test, N1 ⫽ 86, N2 ⫽ 86, Z ⫽ ⫺2.58, p ⫽
.009). Eventually, 57% of these males were seen again, with
males in poor condition being more likely to return than
males in good condition (Mann-Whitney U test, N1 ⫽ 74, N2
⫽ 98, Z ⫽ ⫺2.56, p ⫽ .01). About half (47%) of these males
returned attached, and the original attachment status had a
significant effect on whether they returned or not (␹2 test, ␹2
⫽ 11.4, df ⫽ 1, p ⫽ .0007) and on whether they returned
attached or not (70% of former attached males return attached, whereas only 35% of former unattached males returned attached; ␹2 test, ␹2 ⫽ 10.6, df ⫽ 1, p ⫽ .001). Like
the males with bags, both condition and original attachment
status (but not size) significantly affected whether these males
returned in the first week (logistic regression, N ⫽ 172, ␹2 ⫽
4.38, p ⫽ .04; for condition ␹2 ⫽ 6.22, p ⫽ .01; for original
status ␹2 ⫽ 9.08, p ⫽ .003) or in subsequent weeks (logistic
regression, N ⫽ 172, ␹2 ⫽ 4.89, p ⫽ .02; for condition ␹2 ⫽
5.5, p ⫽ .019; for original status ␹2 ⫽ 8.6, p ⫽ .0034).
Effect of condition on the behavior of unmanipulated males
Condition was associated with many aspects of the behavior
of nonexperimental males. Of the 1319 males that were
marked and measured in this study, 26% were unattached and
74% were attached when they were initially found on the
beach. The attached males were in significantly better condition than unattached individuals (22% of attached males and
12% of unattached males had a condition index of 25, whereas 9% of attached males and 14% of unattached males had a
condition index of ⬍15; Mann-Whitney U test: Z ⫽ ⫺4.88, p
⬍ .0001). We saw 702 males (53% of those marked) again at
the nesting beach from 1 to 12 times. The males that were
seen most often were in the poorest condition (for males in
the poorest condition category, 9% were seen once and 21%
were seen 4⫹ times; for males in the best condition category,
22% were seen once and 12% were seen 4⫹ times; KruskalWallis test: H ⫽ 12.8, df ⫽ 3, p ⫽ .003). Of the returning
males, 44% came back attached and 56% (N ⫽ 702) unattached, and the attached males were in better condition than
the unattached males (Mann-Whitney U test: Z ⫽ ⫺3.12, p ⫽
.0016). Males that had originally come in attached were more
likely to return attached (␹2 test: ␹2 ⫽ 40.1, df ⫽ 1, p ⬍ .0001).
Of the 252 males that were seen three times or more, 26%
were attached (75% or more of the time), 39% were unattached (75% or more of the time), and 35% showed a mixture
of behavioral tactics. The three categories of behavior differed
in original attachment status (␹2 test: ␹2 ⫽ 43, df ⫽ 2, p ⬍
.0001) and condition: of the animals in the highest condition
category, 40% were attached and 24% were unattached,
whereas in the lowest condition category 7% were attached
and 61% were unattached (␹2 test: ␹2 ⫽ 26.9, df ⫽ 6, p ⬍
.002). When original attachment status and condition were
considered together, only condition significantly affected
whether males spent most of their time unattached (ANOVA;
original status: F ⫽ .016, df ⫽ 1, p ⫽ .9, condition: F ⫽ 12.8,
df ⫽ 1, p ⫽ .0004, original status by condition F ⫽ 2.9, df ⫽
1, p ⫽ .09).
With the larger sample size of the unmanipulated group,
and where additional measurements were made, some addi-
Brockmann • Mating tactics in Limulus
235
Figure 2
Frequency distribution of nonexperimental males of different
condition index categories that returned to the nesting beach three
or more times (N ⫽ 252) as unattached (more than 75% of the
time), as attached (more than 75% of the time), or as a mixture of
tactics. Sample sizes are given above each bar.
Figure 3
Threshold or switch model for the evolution of a phenotypecorrelated decision mechanism for mating tactics in horseshoe
crabs. The downward arrow shows the threshold below which males
show unattached, satellite behavior and above which males show
attached behavior. Reproductive success and male condition are
given in arbitrary units.
tional relationships were found. Smaller animals were in better condition than larger animals (CW: rs ⫽ ⫺.14, Z ⫽ ⫺3.8,
p ⬍ .0001, N ⫽ 751; IO: rs ⫽ ⫺.213, Z ⫽ ⫺7.7, p ⬍ .0001, N
⫽ 1312; WT: rs ⫽ ⫺.309, Z ⫽ ⫺8.5, p ⬍ .0001, N ⫽ 751).
None of the measures (CW, IO, WT, tail height, tail length)
was significantly associated with the original attachment status,
with attachment status upon return, or with the percentage
of times that a male returned as a satellite. Size, however, was
significantly associated with whether the animals returned
(unpaired t test, CW: t ⫽ ⫺2.3, df ⫽ 749, p ⫽ .02; IO: t ⫽
⫺3.4, df ⫽ 1310, p ⫽ .0007) and with the number of times
they returned (Kruskal-Wallis test, CW: H ⫽ 12.1, df ⫽ 4, p
⫽ .02, IO: H ⫽ 12.5, df ⫽ 4, p ⫽ .01; i.e. the larger animals
that were in poorer condition and that were originally unattached returned more often). When all three variables were
considered together, only condition and original attachment
status (not size) affected whether the male returned attached
or as a satellite (logistic regression, condition: ␹2 ⫽ 7.51, p ⬍
.0061, original attachment status: ␹2 ⫽ 58.2, p ⬍ .0001, N ⫽
697); original attachment status and size (but not condition)
significantly affected whether the animal returned (logistic regression, IO: ␹2 ⫽ 9.5, p ⬍ .002, original attachment status:
␹2 ⫽ 36.5, p ⬍ .0001, N ⫽ 1312); and all three variables affected the number of times that males returned (logistic regression, condition: ␹2 ⫽ 13.75, p ⬍ .0002, original attachment status: ␹2 ⫽ 29.6, p ⬍ .0001, and IO: ␹2 ⫽ 4.6, p ⬍ .03,
N ⫽ 1137).
ellites are in significantly worse condition than those that remain at sea (Figure 1). In fact, the behavior of males that can
attach (i.e., no bags; Figure 2) is quite similar to the behavior
of those that cannot attach (i.e., with bags; males in the two
experiments did not differ in the likelihood that they will return: ␹2 test, return in the first week: ␹2 ⫽ 2.6, df ⫽ 1, p ⫽
.11; all returns: ␹2 ⫽ 0.5, df ⫽ 1, p ⫽ .47), except, of course,
that about half of those that can attach will return to the
nesting beach with females.
Both condition and original attachment status significantly
affect the likelihood that males will become satellites. When
males are unable to attach, the condition index is the more
important component, and when males can attach, previous
attachment status is the better predictor of male tactics. The
fact that both condition and original attachment status are
significantly associated with differences in male behavior
could be explained in several ways. First, it could mean that
there are additional condition factors associated with attached
or satellite behavior that I am not detecting with my condition
index. In fact, over the years I have added measures to the
study, such as the number of gill parasites, which also correlate with attached and satellite behavior (Brockmann, in preparation). Second, it could mean that both condition and attachment status are associated with another variable that I am
not measuring. The most obvious possibility is age. Horseshoe
crabs do not molt as adults, and so it seems reasonable that
the darkening and eroding of the carapace (darker color, pits,
damaged eyes and spines) and the accumulating epibiotic organisms are correlated with time since the last molt and thus
with adult age (Brockmann, 1996; Penn and Brockmann,
1995). So far, however, no one has developed a reliable way
of determining the age of horseshoe crabs (Botton and Ropes,
1988). Third, it could mean that the animals learn from previous experience and that this information is a part of the
decision to become a satellite. Finally, it could mean that
males use previous experience to evaluate variables that I am
not measuring in this study, such as the availability of females,
which I am detecting through differences in original attachment status.
Alternative tactics are often modeled as the success associated with two or more tactics across a set of phenotypes or
conditions (Figure 3; Barnard and Sibley, 1981; Charnov,
DISCUSSION
Male horseshoe crabs gain reproductive success in two ways:
attached to females and as unattached satellites of nesting
pairs. Depending on their position, the number of other
males present, and other factors, either attached or satellite
males can fertilize a majority of a female’s eggs (Brockmann
et al., 1994, 2000). Attached and unattached mating tactics
are correlated with differences in phenotype: attached males
are in better condition than unattached (Brockmann and
Penn, 1992). The results of this study show that attached and
satellite tactics are based on cues related to male condition
rather than on the ability of males to find females. When
males are prevented from attaching, those that become sat-
Behavioral Ecology Vol. 13 No. 2
236
1982; Dominey, 1984; Gross, 1984; Henson and Warner, 1997;
Hutchings and Myers, 1994; Koprowski, 1993; Oster and Wilson, 1978; Reeve, 1998; Roff, 1996; Taborsky, 1999; Walker,
1986; Waltz, 1982; West Eberhard, 1979). If the fitness curves
do not cross, then the tactics are maintained in the population
only when it is not possible for all individuals to perform the
more successful behavior. If the fitness curves cross, then
there exists a threshold size, age, or condition, T, below which
the behavior of unattachment is followed (Figure 3) and
above which the behavior attachment is followed (Parker,
1982, 1984a). In the case of horseshoe crabs, the model predicts that males in good condition should have higher fitness
when attached and those in poor condition should have higher fitness when unattached. The model predicts that males
will switch from one tactic to the other at the age or condition
that maximizes fitness; in other words, they will use information about phenotype when it increases fitness. As long as the
fitness curves for the tactics cross (at T ), both tactics will be
maintained in the population (Brockmann, 2001), and their
success will be equal at the switch point (Gross, 1996; West
Eberhard, 1979). Frequency-dependent selection can alter the
threshold age or condition at which an animal switches from
one tactic to the other (Gross and Repka, 1998a; Parker,
1984a,b; Repka and Gross, 1995). In horseshoe crabs, for example, females will not lay eggs without an attached male,
satellites reduce attached male success, and when there are
more than two satellites, they reduce the success of other satellites (Brockmann et al., 2000). This means that the unattached mating tactic is more successful when it is rare (Brockmann, 2001). Gross and Repka (1995, 1998a,b) demonstrated
a unique, stable equilibrium switch-point for state-dependent
tactics even when the tactics have unequal average fitnesses.
Switch models of condition-dependent alternative tactics
have been tested experimentally in a few cases (Arak, 1988;
Basolo, 1994; Bull and Schwarz, 1996; Conover and Voorhees,
1990; Eadie and Fryxell, 1992; Emlen, 1997; Foote et al., 1997;
Perrill et al., 1982; Tomkins and Simmons, 1996; Waltz and
Wolf, 1988; Wolf and Waltz, 1993). For example, Radwan
(1993) describes two phenotype-correlated mating tactics in
an acarid mite: fighters that develop only at low population
densities and nonfighters that develop in dense colonies. He
tested the model by evaluating whether the fitness curves
cross. One can also evaluate models by changing conditions
(such as altering density) or by altering the state of the individuals and determining whether they change their behavior
in the predicted directions (Brockmann, 2001; Gross, 1991,
1996; Hutchinson and McNamara, 2000).
Evaluating the model (Figure 3) in horseshoe crabs requires measuring the success of good-condition males that
take up the satellite tactic and poor-condition males that attach. When good-condition males are experimentally prevented from attaching (by putting bags over their claws), they
do not become satellites. This result is consistent with the hypothesis that males in good condition have lower success as
satellites than when attached. Reduced fitness for males in
good condition that take up the satellite tactic may be due to
differences in sperm competition abilities (for which there is
no evidence; Brockmann et al., 2000) or to differences in
their willingness to come ashore. Unattached males that return to the nesting beach as satellites are at a greater risk of
being overturned and preyed upon than are attached males
(Penn and Brockmann, 1995). Dynamic models (Clark and
Mangel, 2000; Houston et al., 1988; Houston and McNamara,
1999; Lucas and Howard, 1995; Lucas et al., 1996; Mangel and
Clark, 1988) demonstrate that risk can be an important factor
influencing age-related behavior, with young animals being
less likely to run risks than older individuals (Godin, 1995;
Jeanne, 1991). To provide a robust test of the model in Figure
3, however, one needs to measure the fitness of males that
differ in condition when forced to be satellites.
Switch models predict a threshold condition at which individuals should change from one tactic to another, but the
models do not predict the common observation that individuals of intermediate condition change back and forth, as with
attached and satellite behavior in horseshoe crabs (Figure 2).
Such variation could occur because of additional variables not
captured in my analysis, such as an interaction between operational sex ratio and phenotypic condition. In a series of
experiments using sailfin mollies (Poecilia latipinna), for example, Travis and Woodward (1989) showed that large males
always court females, small males never court, and males of
intermediate size switch from one behavior to the other depending on context. Prior experience, age, and condition, as
well as size and genetic differences, may affect the flexible
behavior of intermediate-sized males. Tomkins (1999) found
considerable variation in the region over which male earwigs
switch from a phenotype with long forceps to one with short
forceps. He defines a switch zone rather than a switch point.
Phenotype-correlated switches in tactics allow animals to track
changes in environmental, social, or age-related conditions
that affect fitness (Moran, 1992).
I thank my field assistants Susan Wineriter, Blaine Biedermann, Christian Solaré, Carlos Iudica, Eric Botsford, Andy Rothfusz, and Salomé
Dussan. The research was conducted under a special use permit from
the Lower Suwannee National Wildlife Refuge, Ken Litzenberger, refuge manager. I thank Frank Maturo and Henry Coulter of the UF
Marine Laboratory at Seahorse Key for their help with logistics. The
research was supported by the National Science Foundation (OCE9006392), the University of Florida Division of Sponsored Research, the
University of Florida Foundation, the Department of Zoology, and the
UF Marine Laboratory at Seahorse Key.
REFERENCES
Alcock J, 1979. The evolution of intraspecific diversity in male reproductive patterns in some bees and wasps. In: Sexual selection and
reproductive competition in insects (Blum MS, Blum NA, eds). New
York: Academic Press; 381–402.
Alcock J, 1996a. Provisional rejection of three alternative hypotheses
on the maintenance of a size dichotomy in males of Dawson’s burrowing bee, Amegilla dawsoni (Apidae, Apinae, Anthophorini). Behav Ecol Sociobiol 39:181–188.
Alcock J, 1996b. The relation between male body size, fighting, and
mating success in Dawson’s burrowing bee, Amegilla dawsoni (Apidae, Apinae, Anthophorini). J Zool (Lond) 239:663–674.
Alcock J, 1997. Small males emerge earlier than large males in Dawson’s burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini). J Zool 242:453–462.
Alcock J, Jones CE, Buchmann SL, 1976. Location before emergence
of the female bee, Centris pallida, by its male (Hymenoptera: Anthophoridae). J Zool 179:189–199.
Alcock J, Jones CE, Buchmann SL, 1977. Male mating strategies in
the bee Centris pallida, Fox (Anthophoridae: Hymenoptera). Am
Nat 111:145–155.
Arak A, 1983. Male-male competition and mate choice in anuran amphibians. In: Mate choice (Bateson PPG, ed). Cambridge: Cambridge University Press; 181–210.
Arak A, 1988. Callers and satellites in the natterjack toad: evolutionarily stable decision rules. Anim Behav 36:416–432.
Barlow RB Jr, Powers MK, Howard H, Kass L, 1986. Migration of Limulus for mating: relation to lunar phase, tide height, and sunlight.
Biol Bull 171:310–329.
Barnard CJ, Sibly RM, 1981. Producers and scroungers: a general
model and its applications to captive flocks of house sparrows. Anim
Behav 29:543–550.
Basolo AL, 1994. The dynamics of fisherian sex-ratio evolution: theoretical and experimental investigations. Am Nat 144:473–490.
Botton ML, Loveland RE, 1989. Reproductive risk: high mortality as-
Brockmann • Mating tactics in Limulus
sociated with spawning by horseshoe crabs (Limulus polyphemus) in
Delaware Bay, USA. Mar Biol 101:143–151.
Botton ML, Ropes JW, 1988. An indirect method for estimating longevity of the horseshoe crab (Limulus polyphemus) based on epifaunal slipper shells (Crepidula fornicata). J Shellfish Res 7:407–412.
Brockmann HJ, 1996. Satellite male groups in horseshoe crabs, Limulus polyphemus. Ethology 102:1–21.
Brockmann HJ, 2001. The evolution of alternative strategies and tactics. Adv Study Behavior 30:1–51.
Brockmann HJ, Colson T, Potts W, 1994. Sperm competition in horseshoe crabs (Limulus polyphemus). Behav Ecol Sociobiol 35:153–160.
Brockmann HJ, Nguyen C, Potts W, 2000. Paternity in horseshoe crabs
when spawning in multiple male groups. Anim Behav 60:837–849.
Brockmann HJ, Penn D, 1992. Male mating tactics in the horseshoe
crab, Limulus polyphemus. Anim Behav 44:653–665.
Bull NJ, Schwarz MP, 1996. The habitat saturation hypothesis and
sociality in an allodapine bee: cooperative nesting is not ‘‘making
the best of a bad situation.’’ Behav Ecol Sociobiol 39:267–274.
Campanella PJ, Wolf LL, 1974. Temporal leks as a mating system in
a temperate zone dragonfly (Odonata: Libellulidae). I. Plathemis
lydia. Behaviour 51:49–87.
Charnov E, 1982. The theory of sex allocation. Princeton, New Jersey:
Princeton University Press.
Clark CW, Mangel M, 2000. Dynamic state variable models in ecology.
methods and applications. Oxford: Oxford University Press.
Cohen JA, Brockmann HJ, 1983. Breeding activity and mate selection
in the horseshoe crab, Limulus polyphemus. Bull Mar Sci 33:274–
281.
Conover D, Van Voorhees D, 1990. Evolution of a balanced sex ratio
by frequency-dependent selection in a fish. Science 250:1556–1558.
Danforth BN, Desjardins CA, 1999. Male dimorphism in Perdita portalis (Hymenoptera, Andrenidae) has arisen from preexisting allometric patterns. Insectes Soc 46:18–28.
Dominey WJ, 1984. Alternative mating tactics and evolutionarily stable
strategies. Am Zool 24:385–396.
Eadie JM, Fryxell JM, 1992. Density dependence, frequency dependence, and alternative nesting strategies in goldeneyes. Am Nat 140:
621–641.
Emlen DJ, 1997. Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera:
Scarabaeidae). Behav Ecol. Sociobiol 41:335–341.
Foote CJ, Brown GS, Wood CC, 1997. Spawning success of males using
alternative mating tactics in sockeye salmon, Oncorhynchus nerka.
Can J Fish Aquat Sci 54:1785–1795.
Gadgil M, 1972. Male dimorphism as a consequence of sexual selection. Am Nat 106:574–579.
Godin JG, 1995. Predation risk and alternative mating tactics in male
Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229.
Gross MR, 1984. Sunfish, salmon, and the evolution of alternative
reproductive strategies and tactics in fishes. In: Fish reproduction:
strategies and tactics (Wooton R, Potts G, eds). London: Academic
Press; 55–75.
Gross MR, 1991. Salmon breeding behavior and life history evolution
in changing environments. Ecology 72:1180–1186.
Gross MR, 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–97.
Gross MR, Charnov EL, 1980. Alternative male life histories in bluegill
sunfish. Proc Natl Acad Sci USA 77:6937–6940.
Gross MR, Repka J, 1995. Inheritance and the conditional strategy.
Am Zool 24:385–396.
Gross MR, Repka J, 1998a. Game theory and inheritance in the conditional strategy. In: Game theory and animal behavior (Dugatkin
L, Reeve HK, eds). Oxford: Oxford University Press; 168–187.
Gross MR, Repka J, 1998b. Stability with inheritance in the conditional strategy. J Theor Biol 192:445–453.
Henson SA, Warner RR, 1997. Male and female alternative reproductive behaviors in fishes: a new approach using intersexual dynamics.
Annu Rev Ecol Syst 28:571–592.
Hews DK, Thompson CW, Moore IT, Moore MC, 1997. Population
frequencies of alternative male phenotypes in tree lizards: geographic variation and common-garden rearing studies. Behav Ecol
Sociobiol 41:371–380.
Houston A, Clark C, McNamara J, Mangel M, 1988. Dynamic models
in behavioural and evolutionary ecology. Nature 332:29–34.
237
Houston AI, McNamara JM, 1999. Models of adaptive behavior: an
approach based on state. Cambridge: Cambridge University Press.
Hutchings JA, Myers RA, 1994. The evolution of alternative mating
strategies in variable environments. Evol Ecol 8:256–268.
Hutchinson JMC, McNamara JM, 2000. Ways to test stochastic dynamic programming models empirically. Anim Behav 59:665–676.
Jeanne RL, 1991. Polyethism. In: The social biology of wasps (Ross
KG, Matthews RW, eds). Ithaca, New York: Cornell University Press;
389–425.
Johnson K, DuVal E, Kielt M, Hughes C, 2000. Male mating strategies
and the mating system of great-tailed grackles. Behav Ecol 11:132–
141.
Koprowski JL, 1993. Alternative reproductive tactics in male eastern
gray squirrels: ‘‘making the best of a bad job.’’ Behav Ecol 4:165–
171.
Le Boeuf BJ, 1974. Male-male competition and reproductive success
in elephant seals. Am Zool 14:163–177.
Lucas JR, Howard RD, 1995. On alternative reproductive tactics in
anurans. Dynamic games with density and frequency dependence.
Am Nat 146:365–397.
Lucas JR, Howard RD, Palmer JG, 1996. Callers and satellites: chorus
behavior in anurans as a stochastic dynamic game. Anim Behav 51:
501–518.
Mangel M, Clark CW, 1988. Dynamic modeling in behavioral ecology.
Princeton, New Jersey: Princeton University Press.
Maynard Smith J, 1982. Evolution and the theory of games. Cambridge: Cambridge University Press.
Moore MC, Hews DK, Knapp R, 1998. Hormonal control and evolution of alternative male phenotypes: generalizations of models for
sexual differentiation. Am Zool 38:133–151.
Moran N, 1992. The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989.
O’Neill KM, 1983. The significance of body size in territorial interactions of male beewolves (Hymenoptera: Sphecidae, Philanthus).
Anim Behav 31:404–411.
Oster GF, Wilson EO, 1978. Caste and ecology in the social insects.
Princeton, New Jersey: Princeton University Press.
Parker GA, 1982. Phenotype-limited evolutionarily stable strategies.
In: Current problems in sociobiology (King’s College Sociobiology
Group, eds). Cambridge: Cambridge University Press; 173–201.
Parker GA, 1984a. Evolutionarily stable strategies. In: Behavioural
ecology: an evolutionary approach (Krebs JR, Davies NB, eds). Oxford: Blackwell; 30–61.
Parker GA, 1984b. The producer-scrounger model and its relevance
to sexuality. In: Producers and scroungers: strategies for exploitation and parasitism (Barnard CJ, ed). London: Croom Helm; 127–
153.
Penn D, Brockmann HJ, 1994. Nest-site selection in the horseshoe
crab, Limulus polyphemus. Biol Bull 187:373–384.
Penn D, Brockmann HJ, 1995. Age-biased stranding and righting in
male horseshoe crabs, Limulus polyphemus. Anim Behav 49:1531–
1539.
Perrill SA, Gerhardt HC, Daniel R, 1982. Mating strategy shifts in male
green treefrogs, Hyla cinerea: an experimental study. Anim Behav
30:43–48.
Phillip DP, Gross MR, 1994. Genetic evidence for cuckoldry in bluegill
Lepomis macrochirus. Mol Ecol 3:563–569.
Radwan J, 1993. The adaptive significance of male polymorphism in
the acarid mite Caloglyphus berlesei. Behav Ecol Sociobiol 33:201–
208.
Reeve HK, 1998. Game theory, reproductive skew, and nepotism. In:
Game theory and animal behavior (Dugatkin L, Reeve HK, eds).
Oxford: Oxford University Press; 118–145.
Repka J, Gross MR, 1995. The evolutionarily stable strategy under
individual condition and tactic frequency. J Theor Biol 176:27–31.
Roff DA, 1996. The evolution of threshold traits in animals. Q Rev
Biol 71:3–35.
Rubenstein DI, 1980. On the evolution of alternative mating strategies. In: Limits to action: the allocation of individual behavior (Staddon JER, ed). New York: Academic Press; 65–100.
SAS Institute, 1998. Statview. Cary, North Carolina: SAS Institute.
Shuster CN, Jr., 1982. A pictorial review of the natural history and
ecology of the horseshoe crab Limulus polyphemus, with reference
to other Limulidae. In: Physiology and biology of horseshoe crabs:
studies on normal and environmentally stressed animals (Bonav-
238
entura J, Bonaventura C, Tesh S, eds). New York: Alan R. Liss; 1–
52.
Starks PT, Reeve HK, 1999. Condition-based alternative reproductive
tactics in the wool-carder bee, Anthidium manicatum. Ethol Ecol
Evol 11:71–75.
Sydlik MA, Turner LL, 1989. Temporal variation in the composition
of epibiotic assemblages found on horseshoe crab carapaces. Am
Zool 29:37A.
Taborsky M, 1999. Conflict or cooperation: what determines optimal
solutions to competition in fish reproduction? In: Behaviour and
conservation of littoral fishes (Almada VC, Oliveira R, Goncalves
EJ, eds). Lisboa, Portugal: Instituto Superior de Psicologia Aplicada;
1–47.
Thornhill R, 1981. Panorpa (Mecoptera: Panorpidae) scorpionflies:
systems for understanding resource-defense polygyny and alternative reproductive efforts. Annu Rev Ecol Syst 12:355–386.
Tomkins JL, 1999. Environmental and genetic determinants of the
male forceps length dimorphism in the European earwig Forficula
auricularia L. Behav Ecol Sociobiol 47:1–8.
Behavioral Ecology Vol. 13 No. 2
Tomkins JL, Simmons LW, 1996. Dimorphisms and fluctuating asymmetry in the forceps of male earwigs. J Evol Biol 9:753–770.
Travis J, Woodward BD, 1989. Social context and courtship flexibility
in male sailfin mollies, Poecilia latipinna (Pisces: Poeciliidae). Anim
Behav 38:1001–1011.
Turner LL, Kammire C, Sydlik MA, 1988. Preliminary report: composition of communities resident on Limulus carapaces. Biol Bull
175:312.
Walker TJ, 1986. Stochastic polyphenism: coping with uncertainty. Fla
Entomol 69:46–62.
Waltz EC, 1982. Alternative mating tactics and the law of diminishing
returns: the satellite threshold model. Behav Ecol Sociobiol 10:75–
83.
Waltz EC, Wolf LL, 1988. Alternative mating tactics in male whitefaced dragonflies (Leucorhinia intacta): plasticity of tactical options
and consequences for reproductive success. Evol Ecol 2:205–231.
West Eberhard MJ, 1979. Sexual selection, social competition, and
evolution. Proc Am Philos Soc 123:222–234.
Wolf LL, Waltz EC, 1993. Alternative mating tactics in male whitefaced dragonflies: experimental evidence for a behavioural assessment ESS. Anim Behav 46:325–334.