Courtship and mating behavior in the Pycnogonida (Chelicerata: Class Pycnogonida): A summary

Article (PDF Available)inInvertebrate Reproduction and Development 46(1):63-79 · December 2004with 155 Reads
DOI: 10.1080/07924259.2004.9652607
Abstract
The few published observations on pycnogonid courtship and mating behavior are widely scattered in the literature and there are no recent summaries available. Consequentially, the exclusively paternal care which is characteristic of this little-known group of marine invertebrates remains understudied by modern behavioral biologists. The current paper provides a comprehensive introduction to pycnogonid morphology with emphasis on the structures required for reproduction and then summarizes all of the available information on courtship and mating behavior in pycnogonids. The summary of reproductive behaviors is divided into categories based on the type of ovigerous leg structure present and the three most common types of ovi-gerous legs (complete ovigerous leg, modified phoxichilid ovigerous leg, modified ammotheid ovigerous leg) are described and named. The role of sexual selection in both the evolution of paternal care within this group and also the evolution of several different kinds of ovigerous legs is discussed and the gradual accumulation of a series of misinterpretations by non-pycnogonid specialists in the recent behavioral literature on paternal care is examined.
*Corresponding author. Present address for both authors: Department of Biological Sciences, Northern Arizona University,
Flagstaff, Arizona 86011-5640, USA. Tel. +1 (928) 523-0502; Fax: +1 (928) 523-7500; bonnie.bain@nau.edu; and
fredric.govedich@nau.edu.
P R O O F
IRD 649
Invertebrate Reproduction and Development, xx:x (2004) x–x 1
Balaban, Philadelphia/Rehovot
0168-8170/04/$05.00 © 2004 Balaban
Courtship and mating behavior in the Pycnogonida
(Chelicerata: Class Pycnogonida): a summary
BONNIE A. BAIN* and FREDRIC R. GOVEDICH
School of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia
email: Bonnie.Bain@sci.monash.edu.au
Received 14 July 2004; Accepted 13 December 2004
Summary
The few published observations on pycnogonid courtship and mating behavior are widely
scattered in the literature and there are no recent summaries available. Consequentially, the
exclusively paternal care which is characteristic of this little-known group of marine inverte-
brates remains understudied by modern behavioral biologists. The current paper provides a com-
prehensive introduction to pycnogonid morphology with emphasis on the structures required for
reproduction and then summarizes all of the available information on courtship and mating
behavior in pycnogonids. The summary of reproductive behaviors is divided into categories
based on the type of ovigerous leg structure present and the three most common types of ovi-
gerous legs (complete ovigerous leg, modified phoxichilid ovigerous leg, modified ammotheid
ovigerous leg) are described and named. The role of sexual selection in both the evolution of
paternal care within this group and also the evolution of several different kinds of ovigerous legs
is discussed and the gradual accumulation of a series of misinterpretations by non-pycnogonid
specialists in the recent behavioral literature on paternal care is examined.
Key words: Pycnogonids, mating behavior, paternal care, ovigerous leg
Introduction
Pycnogonids or sea spiders (subphylum Cheli-
cerata, Class Pycnogonida) are a fairly large group
(1200+ species) of marine chelicerates which have
been overlooked by many recent behavioral studies.
One of the major reasons for this is that most of the
recent pycnogonid literature consists mainly of species
descriptions with few papers published on any other
aspects of pycnogonid biology. As such, unlike most
other groups of organisms, the pycnogonids have not
been included in many discussions on behavior even
though they have some unique characteristics not
shared with other taxa. The purpose of this paper is to
provide a complete summary of all that is currently
known about pycnogonid courtship and mating
behavior, which will then lay the foundation for future
studies on the evolution of the exclusively paternal
care found within this group.
In general, the sexes are separate in pycnogonids
(but see below for exceptions) and they have a series
of courtship and mating behaviors during which the
female lays the eggs and then transfers them over to
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the male. The male then fertilizes the eggs and glues
them on to his ovigerous legs. He then carries the eggs
around until they hatch. Care consists of ventilating the
eggs (by moving the ovigerous legs back and forth)
and providing protection from predators. In most cases,
when the eggs hatch, the protonymphon larvae leave
the male and either take up a free-living existence
(Typical Protonymphon), form a cyst in a hydroid or
other cnidarian (Encysted Larva), or live in or on
another marine invertebrate (Atypical Protonymphon)
(Bain, 2003a, 2003b). In all species of the Calli-
pallenidae and some species of the Nymphonidae, the
eggs hatch into an Attaching Larva which reattaches
itself to the male and remains there for the first several
molts after which it then leaves the parent and takes up
a free-living existence (Bain 2003a, 2003b).
Although parental care is exclusively paternal in
the pycnogonids, there are a few scattered observations
of females carrying egg masses (summarized in Stock,
1954): Pycnogonum planum Stock, 1954; Nymphon
brevicaudatum Miers, 1875; Pycnogonum cataphrac-
tum Möbius, 1902; Pycnogonum portus Barnard, 1946;
Bathyzetes virago (Loman, 1908) (as Eurycyde
virago); and Phoxichilidium tubulariae Lebour, 1945
(as P. femoratum Rathke, 1799). In all of these species,
it is normally the male which carries the eggs. How-
ever, an observation by Loman (1907) provides one
possible explanation as to why the females would carry
the eggs instead of the males in these rare cases.
Loman (1907) observed that, during mating, if the
male of Phoxichilidium tubulariae was prevented from
taking over the eggs (by removing him), then the
female herself took over caring for the brood.
Summary of Pycnogonid Biology
External morphology
In nearly all pycnogonid species, the sexes are
separate (Figs. 1 and 2) and the sex ratio is approxi-
mately 50:50 (Bain and Gillespie, unpub. data). While
there is very little sexual dimorphism in most groups
(families Nymphonidae, Callipallenidae, Colossen-
deidae), there are very pronounced differences in
others (families Ammotheidae, Phoxichilidiidae, Pyc-
nogonidae) (Tables 1 and 2). Two instances of herma-
phroditism and several records of gynandromorphs
have been reported for four otherwise sexually dimor-
phic species, and a fifth species, Ascorhynchus cor-
deroi Marcus, 1952 may be the only truly herma-
phroditic pycnogonid (Table 3) but these abnormalities
are extremely rare among the Pycnogonida.
The sexes can readily be distinguished by several
different characteristics including gonopore structure
Fig. 1. Side view, whole pycnogonid (Ammothea hilgendorfi
female); legs removed for clarity.
and location, presence or absence of cement glands,
presence or absence of ovigerous legs, and ovigerous
leg structure. Both male and female gonopores
(Fig. 2c–f) are located on the ventral surface of the
second coxal segment (but see Table 1 for several
exceptions) on some or all legs depending on sex and
species (Table 1). Male gonopores are very tiny circu-
lar openings (Fig. 2c, e) which may or may not be
covered by an operculum while female gonopores are
very large, oval in shape and always covered by an
operculum (Fig. 2d, f). In several families (Ammo-
theidae, Phoxichilidiidae), males of some species have
the gonopore located at the tip of an elevated mound or
spike. Female gonopores are usually flush with the
surface of the leg, but in some species, the gonopore is
located on a small mound (Fig. 2d).
The cement gland, found only on the male, pro-
vides the glue used to attach the eggs to his ovigerous
legs during the latter phase of the mating ritual. These
glands are located on the femur (or rarely on both the
femur and first tibia) and come in a variety of shapes
and sizes, ranging anywhere from a series of slits to a
single large tube (Fig. 3a). Structure and exact location
of the cement gland vary according to phylogenetic
position.
Pycnogonids are characterized by having an extra
set of legs, known as ovigers or ovigerous legs, located
between the pedipalps and the first pair of walking legs
(Figs. 1, 4). This extra pair of legs has a variety of
functions: grooming, food handling (both sexes),
courtship and mating (possibly used by the male to
stimulate egg-laying in the female), transfer of eggs
from female to male after eggs have been laid, and
transport of developing eggs (and in some cases,
larvae) by the male [see Bain (2003a) for summary]. In
the less derived pycnogonids, male and female ovi-
gerous legs are identical in both size and structure
(Fig. 4a), and the last four segments of the ovigerous
leg have either single or multiple rows of species-
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Fig. 2. Achelia pribilofensis. a. male (arrow indicates egg mass on ovigerous leg) and b. female (arrow indicates mature eggs
in pedal ovary); c and e: Male gonopore of Phoxichilidium tubulariae (arrow indicates gonopore); d and f: female gonopore
of Ammothea hilgendorfi (arrow indicates gonopore).
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Table 1. Comparison of male and female differences in Pycnogonids
Structure Male Female
Body size Smaller than female Larger than male
Gonopore location Second coxal segment, ventral side;
depending on genus, the gonopore is found
either on all four pairs of legs, pairs 2–4
only, pairs
3–4 only, or only on last pair
Second coxal segment, ventral side, on
all four pairs of walking legs.
Exceptions: in some (all?) Endeis and
Pycnogonum species, gonopore is on
second coxal segment, last pair of legs
only, and on the dorsal side
Gonopore structure Tiny circular opening, usually with an
operculum, in more derived genera, can
be at the tip of a raised mound or spike
Large oval opening, covered with an
operculum, opening flush with leg
surface or on a slightly elevated mound
Cement gland location Found on femur or femur and tibia 1. Exact
location varies depending on genus and
species
Absent
Cement gland structure Depending on genus and species, ranges
from one or more pores with openings flush
with the surface to pore(s) located at the tip
of a long tube or spike
Absent
Alar processes Absent A pair of winglike structures of
unknown function found on the ventral
side of the proboscis of some species of
Anoplodactylus
Pedipalps Always present (except in taxa which lack
pedipalps entirely)
Present in most except for certain
callipallenids. In these taxa, the male
only has a pedipalp.
Ovigerous legs Always present (except in one subgenus
(Nulloviger) of Pycnogonum
Usually present, lacking entirely in some
taxa (the genus Pycnogonum, all
members of the Phoxichilidiidae)
specific compound spines and often a single terminal
claw (Bain, 1992, 2003a, 2003b). This “complete” ovi-
gerous leg is found in the families Colossendeidae,
Nymphonidae, and Callipallenidae (Table 2).
More derived pycnogonids either have ovigerous
legs in which the structure of the last four segments
has been highly modified (Fig. 4b) or in which they
have lost some or all of these terminal segments or in
extreme cases, they have lost the entire ovigerous leg
(Fig. 4c, d) (Bain, 1992, 2003a). In all cases, those
pycnogonids with modified ovigerous legs show a high
degree of sexual dimorphism in these structures. For
instance, in the family Ammotheidae, although both
sexes retain the ten segments in the ovigerous leg, each
sex has modified these segments differently (Figs. 1,
4b). The female ovigerous leg (Fig. 1) is smaller in size
than the male ovigerous leg and it has no special
modifications except that in most cases, the female
ovigerous leg has two compound spines located at the
distal end of segment ten. The male ovigerous leg, in
contrast, has become highly modified with the last four
segments twisted into a club-shaped structure (Fig. 4b)
and in many cases, the compound spines have
disappeared.
A more extreme modification of the ovigerous legs
(Fig. 4c, d) can be found among members of both the
families Phoxichilidiidae and Pycnogonidae. In all
cases, the female ovigerous leg has disappeared
(Fig. 4d) and the male ovigerous leg (Fig. 4c) has lost
some or all of its segments and all of its compound
spines and other specialized structures (Table 2). In the
most extreme case, found among members of the
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Table 2. Comparison of ovigerous leg structure by family (family names from Stock, 1994). For details on observations of
mating behavior, see Tables 4 and 5
Family Observations of mating behavior Ovigerous leg structure
Ammotheidae No Male and female ovigerous legs quite different: both with 10
segments, but last 4 segments of male in many cases are
formed into a club-shaped structure (Fig. 4b)
Austrodecidae No Male and female ovigerous legs quite different, in both
sexes, they are very reduced in size and segment number
Callipallenidae Yes Male and female ovigerous legs nearly identical (Fig. 4a):
each 10 segmented, last 4 segments with single row of
compound spines, terminal claw may be present depending
on genus and species; in some genera, the male has a very
pronounced apophysis present at the distal end of the fifth
segment
Colossendeidae No Male and female ovigerous legs identical: each 10
segmented, last 4 segments with multiple rows of compound
spines, terminal claw may be present depending on genus
and species
Nymphonidae Yes Male and female ovigerous legs nearly identical: each 10
segmented, last 4 segments with single row of compound
spines, terminal claw may be present depending on genus
and species
Phoxichilidiidae Yes Ovigerous legs present in male only; depending on genus,
male ovigerous leg may be seven-segmented (Endeis); six-
segmented (Anoplodactylus); or five-segmented
(Phoxichilidium) (Fig. 4c, d)
Pycnogonidae Yes Ovigerous legs present in male only; in one subgenus of
Pycnogonum, P. (Nulloviger), the male also lacks ovigerous
legs and carries the egg masses cemented to his ventral
surface
Rhynchothoracidae No Male and female ovigerous legs nearly identical: each 10
segmented, some or all of the last 4 segments with paired
simple spines, terminal claw present
Pycnogonum subgenus Nulloviger, the male also has
completely lost the ovigerous leg and carries the eggs
attached to his ventral surface (Stock, 1968).
Internal morphology
In both sexes, the gonad is a U-shaped structure
located in the main trunk of the body, just above the
gut and sandwiched in between the two layers of the
horizontal septum (Miyazaki and Makioka, 1991).
Diverticula extend from the trunk region out into each
walking leg, usually to the end of the femur (ovary) or
the second coxa (testis). The gonadal structures in the
trunk are referred to as the “trunk” ovary or testis and
the diverticula in the legs are called pedal ovaries or
testes (Dohrn, 1879; Hoek, 1881; Thompson, 1909;
Helfer and Schlottke, 1935; Fage, 1949; Sanchez,
1959; King and Jarvis, 1970; Jarvis and King, 1975;
El-Hawawi and King, 1978; King and El-Hawawi,
1978; Arnaud and Bamber, 1987; Miyazaki and
Makioka, 1991, 1992). In one genus, Pycnogonum, the
two arms of the ovarian U are connected by one (Jarvis
and King, 1972) or two (Miyazaki and Makioka, 1992)
“ovarian junctions” and in another genus, Phoxichili-
dium, the ovary forms a continuous sheet of tissue
above the gut (Jarvis and King, 1972; Miyazaki and
Makioka, 1992). The pycnogonid testis is also U-
shaped in most genera, but in the genus Pycnogonum,
the testis is a continuous sheet of tissue above the gut
(El-Hawawi and King, 1978; King and El-Hawawi,
1978; Arnaud and Bamber, 1987).
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Fig. 3. Ammothea hilgendorfi. a: cement gland (arrow) on
male femur; b: mature eggs (e) in pedal ovary, female femur.
In general, the previtellogenic eggs or the immature
sperm are located in the main trunk of the body and
mature eggs/sperm are found in the pedal ovaries/testes
(King and Jarvis, 1970; Jarvis and King, 1972; Jarvis
and King, 1975; see Miyazaki and Makioka, 1991,
1992 for details). Mature sperm or vitellogenic eggs
are stored in the femur (Fig. 3b) and when copulation
begins, the eggs or sperm move back towards the
gonopores, located on the second coxal segment (King
and Jarvis, 1970; Nakamura and Sekiguchi, 1980). The
eggs exit the leg through a short oviduct which con-
nects the ovarian lumen with the gonopore (Bain,
1982; Miyazaki and Makioka, 1991, 1992). One
exception to this pattern is found in the genus Pycno-
gonum in which vitellogenic eggs are located in both
the trunk and leg diverticula (Jarvis and King, 1972;
Miyazaki and Makioka, 1992).
Vitellogenesis has recently been examined in detail
in the following species: Achelia echinata Hodge,
1864 (by Jarvis and King, 1978), Endeis laevis (Grube,
1871) (by Jarvis and King, 1975, 1978), Endeis nodosa
Hilton, 1942 (by Miyazaki and Makioka, 1991),
Nymphon gracile Leach, 1814 (by King and Jarvis,
1970; Jarvis and King, 1978), and Pycnogonum lito-
rale (Ström, 1762) (by Jarvis and King, 1972, 1978;
Miyazaki and Makioka, 1992). Mature eggs come in
many different sizes, but in general callipallenids
(family Callipallenidae) tend to have the largest eggs,
followed by the Nymphonidae (medium to large eggs),
Table 3. Hermaphrodites and gynandromorphs
Species Sexual abnormality References
Ascorhynchus abyssi Sars, 1877 One specimen with male characters on one side and
female characters on other side. All other specimens
sexually dimorphic
Losina-Losinsky
(1964)
Ascorhynchus corderoi Marcus, 1952 A true morphological hermaphrodite-all specimens
collected had both male and female characters
Marcus (1952);
Stock (1965);
Arnaud and
Bamber (1987)
Anoplodactylus gestiens (Ortmann, 1891) One out of 598 specimens examined had both male and
female characters. All other specimens were either male
or female
Child and
Nakamura (1982)
Anoplodactylus jonesi Child, 1974 Child (1974) found one female with eggs (in ovaries)
and which also has ovigerous legs (found in males only
in this family); Child (1979) found 2 more females like
this (6% of the adults collected)
Child (1974, 1979)
Anoplodactylus portus Calman, 1927 Child (1978) examined several different populations of
this species from the Pacific terminus of the Panama
Canal Zone and found that gynandromorphs and other
sexual mosaics made up from 7–24% of the population
Child (1978)
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Fig. 4. a. Terminal segments (each with a single row of compound spines) of Austropallene sp. ovigerous leg; b. terminal
segments of male Ammothea hilgendorfi ovigerous leg with eggs and newly hatched protonymphon larvae; c. and d. Phoxi-
chilidium tubulariae, ventral view; c, male with ovigerous legs (arrow) and d, female showing lack of ovigerous legs. Note:
male has a deformed right walking leg.
Ammotheidae (small to medium eggs), Pycnogonidae
and Phoxichilidiidae (smallest eggs). No eggs (or
sperm) have yet been described for members of the
Colossendeidae (Hoek, 1881; Hedgpeth, 1964; King,
1973).
Spermiogenesis has been described for the follow-
ing species: Nymphon gracile (by El-Hawawi and
King, 1978); Nymphon leptocheles Sars, 1891 and
Nymphon rubrum Hodge, 1862 (by van Deurs, 1974a);
and Pycnogonum litorale (by King and El-Hawawi,
1978) and pycnogonid sperm structure and ultra-
structure have been described in: Nymphon gracile
(examined by El-Hawawi and King, 1978); Nymphon
leptocheles and Nymphon rubrum (examined by van
Deurs, 1973, 1974a, 1974b), and Pycnogonum litorale
(examined by van Deurs, 1974a; King and El-Hawawi,
1978) and summarized by Franzén (1987). Sperm from
the three species of Nymphon are all flagellated but
with different axoneme patterns (Nymphon gracile
18 + 0; Nymphon leptocheles 12 + 0; Nymphon rubrum
9 + 0) while sperm from Pycnogonum litorale is afla-
gellate. All three species of Nymphon have motile
sperm of the type usually associated with external
fertilization in water while the very aberrant non-
motile sperm of Pycnogonum litorale implies a very
“modified fertilization biology” (van Deurs, 1974a;
El-Hawawi and King, 1978).
Summary of Courtship and Mating Behavior
Observations on courtship and mating behavior in
pycnogonids are few and far between (Tables 2, 4, 5),
but an examination of these few instances will give us
some insight into the broader picture and clearly
highlight the gaps in our current knowledge which can
be filled in by more focused research on this group in
the future.
All of the recorded observations can be divided into
two groups: the more primitive pycnogonids with the
complete ovigerous leg (Fig. 4a) (Table 4) and the
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Table 4. Observations on pycnogonid mating behavior (complete ovigerous leg)
Species No. of matings observed Duration of mating References
Nymphon gracile ? 1–2 h King and Jarvis (1970); Jarvis and King (1972)
Parapallene avida 2 4.5 h Hooper (1980)
Propallene longiceps 30+ “Several hours” Nakamura and Sekiguchi (1980)
Table 5. Observations on pycnogonid mating behavior (phoxichilid type, modified ovigerous leg)
Species No. of matings observed Duration of mating References
Anoplodactylus lentus 1 5 min Cole (1901, 1906)
Phoxichilus laevis Grube
[now known as Endeis laevis]
1 30 min Hoek (1881)
Phoxichilidium femoratum
[now known as P. tubulariae]
? ? Loman (1907)
Pycnogonum aurilineatum 1 (?) ? Staples (1999)
Pycnogonum litorale Many, by several different
authors
Up to 5 weeks Prell (1910)
Jarvis and King (1972, 1978)
King and El-Hawawi (1978)
Tomaschko et al. (1997)
Wilhelm et al. (1997)
more derived ones with the phoxichilid type of
modified ovigerous leg (Fig. 4c, d) (Table 5). For a
very large and speciose third group of pycnogonids
(family Ammotheidae) with the ammotheid type of
modified ovigerous leg (Fig. 4b), as well as all of the
other families, there are no recorded observations of
courtship and mating behavior. However, some
information on the ammotheid type can be gleaned
from a very complete description of the number,
arrangement, and developmental states of the egg
masses found on a female of Tanystylum brevipes
(Hoek, 1881) by Cole (1901b) which is discussed
below.
Mating behavior (complete ovigerous leg)
Courtship and mating behavior in pycnogonids with
this type of ovigerous leg has been observed in three
species from two different families: Nymphon gracile
Leach, 1814 (family Nymphonidae); Parapallene
avida Stock, 1973 and Propallene longiceps (Böhm,
1879) (family Callipallenidae). Since the observations
on P. longiceps are the most complete record of pycno-
gonid courtship and mating behavior in the literature,
they will form the basis for the following discussion,
with information on the other two species added where
possible.
Courtship or precopulatory behavior
According to Hooper (1980), the male Parapallene
avida spends approximately 30 min closely following
a female and occasionally, he approaches her with his
anterior pair of legs raised, and uses these to touch her
last pair of legs. After being touched, the female
usually moves away. After several such approaches,
the male grasps the female and places her into the
copulatory position. Precopulatory behavior was not
described by Nakamura and Sekiguchi (1980) except
to say that the male probably initiates copulation since
they observed several cases of male–male coupling and
one case of adult male–subadult female coupling
which led them to conclude that the male initiates the
copulation in this species.
More recent evidence (Bain and Govedich, 2004)
indicates that precopulatory behavior in this group may
also include intense female competition for males in
some species. For instance, in the callipallenid species,
Propallene saengeri Staples, 1979, courtship was ini-
tiated by the female and consisted of dance-like move-
ments and physical contact between the legs of each
partner. This went on for several hours and during this
time, a second female became interested in the court-
ing pair and intervened. This intervention provoked an
aggressive response from the first female and even-
tually led to physical combat between the two females,
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resulting in physical damage to both and ultimately,
the death of one of the two combatants (Bain and
Govedich, 2004).
Pseudo-copulation or close pairing
The behaviors described in this section are not a
true copulation since pycnogonids have external rather
than internal fertilization and so the terms pseudo-
copulation or close pairing will be used instead of
copulation (Jarvis and King, 1978).
In this phase, the male grasps the female and
assumes the pseudo-copulatory position. In P. longi-
ceps, they are oriented head to head, the male positions
both himself and the female so that he is laying on his
back, legs extended, and holding the female on top of
him (her legs are folded up against her body) and his
ventral body surface is in contact with her dorsal body
surface. He does this by using his chelicerae and the
terminal segments (segments 7–10) of his ovigerous
legs to grasp and hold the female. His chelicerae are
fastened on to the base of her chelicerae and his
ovigerous legs hold on to her second pair of walking
legs [see Fig. 2.1 in Nakamura and Sekiguchi (1980)].
Sometimes the male will use the terminal claws of his
first and second walking legs to fasten on to the pro-
podi of her first and second walking legs (Nakamura
and Sekiguchi, 1980).
In Parapallene avida, the positioning is somewhat
different. In this species, the male gets on top of the
female, they are also oriented head to head, and the
male holds her first pair of legs and trunk with his first
and second pairs of legs, respectively (Hooper, 1980).
In both species, once the pseudocopulatory position
has been achieved, the pair remain in this position for
some time (1+ h in P. longiceps; 3.5 h in P. avida) and
the male (of Propallene longiceps) periodically folds
and stretches his ovigerous legs in a rhythmic fashion
(Hooper, 1980; Nakamura and Sekiguchi, 1980). The
male of Parapallene avida was seen to often bring his
walking legs into contact with the female’s legs during
this time period (Hooper, 1980).
Egg-laying
In P. longiceps, the female releases two mature
eggs from each ovary (one ovary per walking leg; eight
walking legs; total of 16 eggs released per mating).
Each egg, upon release, travels from the mature ovary
located in the femur, back two segments towards the
gonopore, located on the ventral surface of the second
coxal segment. Egg movement is probably due to
peristaltic movements of the underlying gut diver-
ticula. Once it arrives at the gonopore, the egg is
forced out through the pore (by peristalsis again?) and,
when first laid, the egg is deformed and nearly flat, but
becomes spherical again within an hour. The eggs are
released from the ovary one by one and the timing is
quite variable (depends on rate of peristalsis?). From
initial release of the first egg to its emergence from the
gonopore takes between 10–25 min. Once the first egg
begins to move, it then takes 3 min to travel down the
leg and emerge from the gonopore. The second egg
emerges from the gonopore 3 to 5 min later (Nakamura
and Sekiguchi, 1980).
Fertilization and egg transfer from female to male
The P. longiceps female, using her ovigerous legs,
collects and holds the eggs as they are being laid. She
is still in the same position as before, but with her
walking legs unfolded now. Once she has collected all
of the eggs, the male, also still in the same position,
bends his fourth pair of walking legs so that his
gonopores (on the second coxal segments) are close to
the eggs. He maintains this position for 5–10 min and
all the while, his ovigerous legs are actively moving
(Nakamura and Sekiguchi, 1980). Presumably this is
where fertilization occurs since Nakamura and Seki-
guchi (1980) removed eggs during this time and these
eggs went on to develop normally.
The P. longiceps male then releases his hold on the
female’s chelicerae and pushes her backwards with all
of his walking legs. He then brings his ovigerous legs
close to the female’s and the eggs are transferred.
During this time, the female actively moves the last
four segments of her ovigerous legs [no other details
given] and the eggs are transferred to the base of the
male’s ovigerous legs. At some point during this pro-
cess, the male turns the female upside down so that
they are both facing each other. After the eggs are
transferred, male and female separate (Nakamura and
Sekiguchi, 1980).
Once they have separated, the P. longiceps male
then begins to form the eggs into egg “bracelets” for
attachment to his ovigerous legs. In order to form the
egg bracelet, the male secretes mucus from the femoral
cement glands and covers the eggs in a pool of mucus.
At this time, he is temporarily holding all of the eggs at
the base of his ovigerous legs. Then, using the last four
segments of the ovigerous leg, he pulls one egg at a
time out of the pool and assembles them into two
bracelet-like egg masses, eight eggs per bracelet (two
eggs per femur × four legs = eight eggs total). The
mucus, which forms the eggshell (outermost covering),
egg stalk (which attaches to the bracelet) and the
bracelet itself, solidifies within 24 h. Usually, eggs
from the left side of the female form one egg bracelet
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–00010
and those from the right form the other. The eggs from
the left side usually end up on the male’s left ovigerous
leg and vice versa. At the end of copulation, the male
has one egg bracelet on each ovigerous leg. When
multiple matings occur, the newest egg bracelets are
always placed at the base of the male’s ovigerous leg
and subsequently, the more distal the egg bracelet, the
further developed the eggs with the most distal egg
bracelets hatching first (Nakamura and Sekiguchi,
1980).
Fewer details of these activities are known for
Parapallene avida. Once the pair is in the pseudo-
copulatory position, the female lays the eggs and the
male, using his ovigerous legs, collects the eggs from
the female after they are laid (5–8 eggs per femur; total
of 52–60 eggs per mating). The male holds onto the
eggs by curling his ovigerous legs towards his ventral
surface and at the end of egg transfer, nearly all
segments of his ovigerous legs are covered with eggs.
The female leaves and the male then forms the eggs
into two egg clusters (30 eggs per cluster), one on each
ovigerous leg. While doing this, he remains in the
pseudo-copulatory position (for 25–31 min) and moves
the egg-covered ovigerous legs so that they frequently
come in contact with one or more walking legs
(coating the eggs with glue from the cement glands?)
(Hooper, 1980).
Pseudo-copulation in Nymphon gracile was briefly
described by King and Jarvis (1970). They observed a
female N. gracile release all of the eggs from only her
last pair of legs, the eggs were gathered up by the
ovigerous legs of the male and he then used one
ovigerous leg to push a ball of eggs into position on
the other ovigerous leg. At the end, the male had two
balls of eggs, one on each ovigerous leg. Eggs
removed from the ovigerous legs at this point in time
failed to develop further.
Mating behavior (phoxichilid type of modified ovi-
gerous leg)
Observations on courtship and mating behavior in
pycnogonids with this type of ovigerous leg are known
for the following four species from two different
families: Anoplodactylus lentus Wilson, 1878, Endeis
laevis (Grube, 1871), and Phoxichilidium tubulariae
(as P. femoratum) (family Phoxichilidiidae); and
Pycnogonum litorale (Ström, 1762) (family Pycno-
gonidae). Of these four species, the most complete
descriptions of courtship and mating are from Cole
(1901a, 1906) for Anoplodactylus lentus and from
various authors (see below) for Pycnogonum litorale.
Courtship or precopulatory behavior
Anoplodactylus lentus and Phoxichilidium tubu-
lariae are very closely related and differ mainly in the
number of male ovigerous leg segments (six in Anoplo-
dactylus and five in Phoxichilidium). Consequentially,
mating in both species is quite similar (Cole, 1901a,
1906; Loman, 1907; King and Jarvis, 1970). There is
no published information on precopulatory behaviors
in these species, but unpublished observations on Ano-
plodactylus sp. from Port Philip Bay, Victoria,
Australia (H. Crisp, pers. obs.) and Phoxichilidium sp.
from Friday Harbor, Washington, USA (B. Bain, pers.
obs.), indicate that the female approaches the male first
in both of these species and may possibly be the sole
initiator of copulation in Anoplodactylus sp.
Pseudo-copulation or close pairing
According to Cole (1901a), the male Anoplo-
dactylus lentus holds on to the dorsal surface of the
female and both of them face in the same direction.
Gradually, the male moves forward and eventually
goes down over the anterior end of the female and
comes to lie underneath her. He is now upside down
relative to her, their ventral surfaces are opposed, and
they are headed in opposite directions. At this point in
time, the female has already laid a single large mass of
eggs and is holding them underneath her. As the male
moves into position below her, his hook-shaped ovi-
gerous legs fasten into the egg mass, and then, as the
two separate, the ovigerous legs pull away, carrying
most of the egg mass with them. Some of the eggs are
lost during this process, but the male ends up with
most of them stuck onto his ovigerous legs. “For some
time after they separated the male was observed to
work the ovigerous legs slowly, the effect seeming to
be to get the eggs more firmly upon them and into a
more compact shape. The time from when the animals
were first observed until they had separated was only
about five minutes” (Cole, 1901a, p. 206). Males of
this species were observed to have either one or two
large egg masses on the ovigerous legs, with two egg
masses being more common than one. Cole (1901a)
observed that, for those males with two large egg
masses, since the eggs were all in the same stage of
development, both egg masses had probably been
acquired at the same time from a single female. Cole
(1906) observed that the mating behavior of A. lentus
was very uniform except in one respect: occasionally,
the male attached the eggs to his ovigerous legs while
he was still on the dorsal side of the female rather than
waiting until he had moved around to the ventral side.
The remaining two species, Endeis laevis and P.
litorale, have more in common with each other than
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–000 11
they do with the previous two species. Both lack
chelicerae and pedipalps, but more interestingly for the
current discussion, the females of both species have
their gonopores located on the dorsal rather than the
ventral side of the second coxal segments (all other
female pycnogonids have gonopores on the ventral
side of these same segments). The female of E. laevis
has gonopores on all pairs of legs (Jarvis and King,
1975) while the female of P. litorale has gonopores
located only on the last pair of legs (Jarvis and King,
1972). This switch in the location of the female gono-
pore should subsequently be reflected in a modification
of the copulatory position in these two species. This
can be clearly seen in the various descriptions of
copulatory behavior for P. litorale, but unfortunately,
the early description of these same behaviors in E.
laevis does not provide the same level of detail and
confirmation of this will have to await further
observation.
The short description (Hoek, 1881, p. 131) of
mating behavior in Endeis laevis is as follows: “The
eggs are fecundated the moment they are laid, and the
copulation, therefore, is quite external, brought about
by the genital openings of the two sexes being placed
against each other. Half an hour after the beginning of
copulation, the male had a large white egg mass on one
of his ovigerous legs, and about one hour later both
masses were present.”
Courtship and mating behavior in P. litorale, a
common shallow water European species, has been
described by a number of authors (Prell, 1910; Schmidt
and Bückmann, 1971; Jarvis and King, 1972, 1978;
King and El-Hawawi, 1978; Wilhelm et al., 1997). All
of the accounts are very similar and differ mainly in
the number of days in which the male “rides” on top of
the female (24 d, Schmidt and Bückmann, 1971;
5 weeks, Jarvis and King, 1972; 6–80 d, Wilhelm et
al., 1997).
Mating behavior in P. litorale is as follows: “The
male clings to the back of the female with the terminal
claws of its walking legs. The coxae of the fourth pair
of walking legs are in such a position that their genital
pores are exactly aligned with the female’s genital
openings, which are located dorsally on the coxae of
the fourth pair of walking legs. Both animals remain in
this position between 6 and 80 d. At the end of this
time, the female releases her eggs. The freshly laid
eggs stick together forming a ball, which becomes
attached to the ovigers of the male. Thereafter, the
male carries the eggs on its ventral side until hatching”
(Wilhelm et al., 1997, p. 605). P. litorale adults can
live for up to 9 years under laboratory conditions, and
Tomaschko et al. (1997) kept a number of mated pairs
together for long periods of time. They observed that
over a 4-year time span, the same pairs mated up to
seven times, although it is not clear whether this was
seven single mating bouts over a 4-year period or
multiple bouts of mating within one (or several)
reproductive season(s).
According to Jarvis and King (1972), the female
lays all of her mature eggs during one mating bout and
the male does not mate again while carrying the single
large mass of eggs obtained from the original mating.
In contrast to this, males of a different species of
Pycnogonum, P. stearnsi Ives, 1892, were collected
while carrying two large egg masses (Cole, 1904),
although since mating was not observed in this species,
it is not known if this condition resulted from one or
two matings.
Mating behavior (ammotheid type of modified ovi-
gerous leg)
There are no records of observations on courtship
and mating behavior of species with this type of
ovigerous leg despite the fact that these pycnogonids
are quite common in many localities worldwide. How-
ever, Cole (1901b) thoroughly described the condition
and exact locations of a number of egg masses on the
ovigerous legs of a male Tanystylum brevipes (Hoek,
1881) and this description differs radically from the
conditions found in either of the ovigerous leg types
discussed above. According to Cole (1901b), there
were eight outermost egg masses on the ovigerous legs
in which the eggs were in “the later cleavage stages”
and underneath these were two older egg masses in
which most of the eggs had already hatched and the
“small pantopod-larvae” were clinging to the remains
of the egg mass by their chelae. The two different sets
of egg masses probably came from two different
females and Cole (1901b) goes on to speculate that the
eight newer egg masses may correspond to the eight
gonopores of a single female, each egg mass coming
from one gonopore (and consequentially, from one
ovary).
Multiple matings
Male pycnogonids have repeatedly been shown to
mate more than once during the breeding season,
mainly by direct observation of the number and
condition of the egg masses/larvae carried by the males
when collected. Usually these males carry several
batches of eggs, each of which are at different stages of
development indicating that the different egg masses
were obtained through more than one mating. In a
simple experiment, Nakamura and Sekiguchi (1980)
demonstrated that males of Propallene longiceps
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–00012
Table 6. Typos/misconceptions in the literature
Reference Typos/Misconceptions Correct word/Explanation
Jarvis and King
(1972)
p. 148 – they state that ovigerous legs in
Pycnogonum littorale are present only in
juvenile males.
p. 150 –they state that, for both sexes, the
gonopores of Nymphon gracile are present
on all legs.
Ovigerous legs are present only in males in this
species and they first appear (as tiny limb buds) after
the molt to the 2nd juvenile instar (Tomaschko et al.
1997).
In the female, the gonopores are present on all legs,
but in the male, they are found only on legs 2,3,4.
They state this correctly in King and Jarvis (1970).
Jarvis and King
(1978)
p. 114:
Relatively few eggs are produced by
pycnogonids and they are carried by the male
for varying periods of time before larvae (in the
Nymphonidae and Pallenidae), or eggs (in the
Ammotheidae, Endeidae, Phoxichilidiidae and
Pycnogonidae) are deposited amongst
hydroids to complete their development.”
p. 114:
“It must be noted that males of Achelia echinata
(Hodge), Phoxichilidium femoratum (Rathke)
and P. littorale have all been observed
carrying larvae, but this is not usual and the
majority tend to release the eggs before they
have hatched.”
Number of eggs produced varies depending on egg
size and phylogenetic position–see text for details.
In all cases, under normal conditions, the males carry
the eggs until they hatch. In two families
(Nymphonidae and Callipallenidae), the males carry
the Attaching Larvae for several more molts.
Note: Pallenidae is an older name for the
Callipallenidae.
When males with eggs or larvae become stressed
(usually the first few days in an aquarium after being
collected), they have a tendency to dump their egg
masses or larvae. These fall to the bottom of the
aquarium and fail to develop further. This has been
observed for many different species in the families
Ammotheidae, Callipallenidae, Nymphonidae, and
Phoxichilidiidae (B. Bain pers. observ.) and is
probably what Jarvis and King (1978) saw.
All of these species carry the eggs until they hatch.
Shortly after hatching, the protonymphon larvae
leave the male. Releasing the eggs before they have
hatched may refer back to the egg dumping
mentioned above.
Ridley, 1978 p. 904:
“At fertilization the male inserts his ovigerous
legs into the female’s gonads and extracts the
eggs.”
“While mating the two sexes have their genital
pores closely opposed.”
p. 905:
“It is not possible to give a list of the species in
which males have been observed carrying eggs.
This is because it is rarely made explicit
whether males have been observed carrying
eggs or whether they are assumed to carry them,
by analogy with related species.”
Fertilization is external and the female lays the eggs,
then hands them over to the male. Details vary
depending on family and ovigerous leg type. See text
for more information.
See text for details of the different matings which
have been observed. This condition (closely opposed
genital pores) does not always occur.
All male pycnogonids carry the eggs and in some
cases, also carry the early larval instars (Attaching
Larvae). The only exception is that, to date, none of
the Colossendeidae have been observed to do this.
They may also carry eggs but only for a short time,
or they may have a different strategy altogether.
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–000 13
Table 6, continued
Ridley (1978) “Females have never been observed carrying
eggs in any pycnogonid”
“[Callipallenid] eggs are big and are only
rarely produced.”
Females of 6 different species have been seen
carrying egg masses. In all cases, it is normally the
male which carries the eggs in these species. See text
for details
Currently there is no information available on how
often females of any pycnogonid species produce
eggs. In this same paragraph, Ridley uses the family
name, Pallenidae, which has been replaced by
Callipallenidae. Also, he cites King (1974) in this
paragraph which is a typo. The actual citation should
be King (1973).
Hooper (1980) When describing mating in Parapallene avida,
Hooper assumes that the female gonopores of P.
avida are in the same location as those of
Pycnogonum litorale females, but they are not.
Gonopores of P. avida females are located on the
ventral surface of the second coxal segment of all
legs; those of P. litorale are located on the dorsal
surface of the second coxal segment, last pair of legs
only.
Nakamura and
Sekiguchi (1980)
When paraphrasing Cole (1901) on p. 167, they
state that, after the male hooks into the egg
mass on the female Anoplodactylus and pulls
away, some eggs remain on the female’s
ovigerous legs.
Since females of this species do not have ovigerous
legs, they probably meant to say that some eggs
remain on the female’s ventral surface rather than on
her ovigerous legs.
Ghiselin (1987) P. 656: “In pycnogonids (Jarvis and King 1970,
1972) the females live ectoparasitically and
evidently generate large numbers of eggs,
producing a number of batches in rapid
succession. The males are more motile, and
gather eggs - usually several batches from a
series of females. They then carry their
progeny and deliver them to new hosts.”
Male and female pycnogonids have similar habits
and there are no records of one sex doing something
(like living ectoparasitically) while the other sex is
free-living. The two references (Jarvis and King
1970, 1972) cited by Ghiselin (1987) cover the
reproductive biology of Nymphon gracile and
Pycnogonum litorale, both of which are discussed in
more detail elsewhere in the current paper.
Giese and Kanatani
(1987)
p. 274: “...the male attaches the fertilized eggs
to cement glands on his ovigerous legs...”
p. 274: “In a few species the females carry the
fertilized eggs in brood chambers on their
legs, for example in Ascorhynchus castelli
(Hedgpeth and Haderlie 1980).”
The cement glands are located on the femur and the
glue from these glands is used by the male to attach
the eggs to his ovigerous legs.
There are no brood chambers in the legs. Rather, the
mature eggs are stored in the femurs (and rarely,
third coxal segments) of the walking legs and since
these legs are transparent, it might be possible to
mistake the mature eggs (which are still inside the
ovary) for brooded embryos.
Clutton-Brock
(1991)
p. 109: “Among marine invertebrates,
uniparental male care predominates among the
sea spiders, Pycnogonidae, where males carry
eggs attached to a pair of specialized ovigerous
legs in seven out of ten families (Jarvis and
King 1972, 1975; R. E. [sic] King 1973; Ridley
1978).
P. 109: At fertilization, which is believed to be
external, the male extracts the eggs from the
female’s gonads with these [ovigerous] legs.”
In nearly all known cases, care is exclusively
paternal. This covers pycnogonids from all families
except the Colossendeidae (no recorded observations
of eggs or young from members of this family). The
few records of females carrying a brood (see text)
appear to be anomalies and not the normal condition
for this group.
Fertilization IS external and the female lays the eggs,
then hands them over to the male. Details vary
depending on family and ovigerous leg type. See text
for more information.
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–00014
mated multiple times with different females by staining
females with mature eggs either red (neutral red) or
blue (Nile blue) and then placing several of the colored
females in with an unstained male. Each time, the male
mated with both red and blue females and ended up
with red and blue egg bracelets on his ovigerous legs.
Eggs within one bracelet were all of the same color
(either red or blue) indicating that they had come from
the same female.
There is currently no definitive published infor-
mation on whether or not female pycnogonids mate
multiple times. Several authors (Sanchez, 1959; King
and Jarvis, 1970) have observed female pycnogonids
laying some, but not all of their eggs during any one
particular mating bout, but none of this is proof that
females mate multiple times, only an indicator that
they could. For instance, Sanchez (1959) observed that
“Females of Endeis spinosa release a mass of eggs at
each mating which represents the contents of a single
femur; Nymphon gracile release the contents of two
femurs and Callipallene, which produces only one or
two eggs in each femur, releases the contents of all
femurs at the same time.” King and Jarvis (1970)
observed that a Nymphon gracile female only laid the
eggs from her last (fourth) pair of legs during a mating
bout.
Unpublished observations on a female Phoxichili-
dium sp. with mature eggs in all femurs (collected from
Friday Harbor, Washington, USA) is further proof that
female multiple matings are quite possible, at least in
some species. The female Phoxichilidium collected
from Friday Harbor was placed into a container with a
male of the same species, which initially was not
carrying any egg masses, and after several days
together, the male was observed one morning to have
one egg mass on his right ovigerous leg and the
female’s femurs still appeared to be fully packed with
mature eggs, indicating that she could have easily
mated more than once given additional time and/or
more mates (B. Bain, unpub. data).
Discussion
Pycnogonids (sea spiders) are a good group for
studying paternal care in arthropods. They have a
nearly equal sex ratio, exclusive paternal care and
external fertilization, allowing us to examine how
paternal care may have evolved and also allowing us to
test evolutionary models such as those proposed by
Eberhard (1985), Queller (1997), Tallamy (2000),
Wade and Shuster (2002), and Shuster and Wade
(2003).
Our current knowledge of pycnogonid precopu-
latory behavior is incomplete at best and information
on competition for mates is nonexistent for this group,
but it has long been assumed that only the male pycno-
gonid initiates courtship. This may be true for some
but not all pycnogonid species. For instance, female
Propallene saengeri have been observed initiating
courtship (Bain and Govedich, 2004) as have female
Anoplodactylus sp. (Bain and Crisp, pers. obs.) and
female Phoxichilidium sp. (B. Bain, pers. obs.).
Pycnogonids have external fertilization in which
the male fertilizes the eggs once they have been placed
into his care. This allows the male to insure that
offspring that he carries are his and not those of
another male, keeping the probability of parentage
equal to that of the female. In addition, sea spiders are
iteroparous with both males and females potentially
mating multiple times (polyandry and polygamy)
during a breeding season and males alone caring for
the ensuing multiple broods. Assuming that parentage
is assured for both the male and the female and that the
sex ratio is equal (50:50), the sex that incurs the
smallest cost should then be selected to become the
care giver (Queller, 1997). The female in this case
probably incurs the greatest cost because she must
invest more energy into egg production whereas the
male will probably have a much lower cost since
sperm production is relatively cheap.
Sexual selection may also help explain why males
care and females do not. Tallamy (2000) suggested that
paternal care could be seen as a nuptial gift and the
males which offer this gift would then greatly increase
their chances of being selected by the female over
males unwilling or unable to offer it. Thus freed from
the care-giving role, the female could then invest much
more energy into egg production, greatly increasing
her mating opportunities and as a result of this,
markedly increasing her fitness.
The single most important feature of pycnogonid
morphology which has allowed the evolution of
exclusively paternal care within this group has been
the possession of the ovigerous legs, structures which
have allowed the pycnogonids to keep the eggs/young
securely tucked away under the body, safe from roam-
ing scavengers and egg predators while at the same
time allowing the parent the freedom to continue his
daily activities (hunting, feeding) relatively unbur-
dened. During mating season, the males can and do
continue to mate more than once since the eggs are
securely stashed away on the ovigerous legs after each
mating bout, leaving the male free to mate again.
Realistically, however, there will be an upper limit to
the number of matings any one male can engage in and
this limit will depend on the amount of space available
for eggs/larvae on the male’s ovigerous legs. This limit
B.A. Bain and F.R. Govedich / IRD 4x (200x) 000–000 15
will vary depending on species and phylogenetic
position since both egg/larva size and ovigerous leg
size and structure can vary considerably.
For instance, a male Nymphon aequidigitatum
Clark, 1963 (Family Nymphonidae) collected from
Westernport Bay, Melbourne, Australia, seems to be
limited to two broods at any one time, since when it
was collected, all the space on the ovigerous legs was
taken up by two distinct clusters. The most distal
cluster consisted of 8–10 fifth instars which were
nearly ready to leave the parent while the inner brood
consisted of two newly laid egg masses (B. Bain, pers.
obs.). On the other hand, Achelia pribilofensis (Cole,
1904) males (Family Ammotheidae) (Fig. 2a) can
easily carry 6–8 egg masses and could potentially carry
even more since there are many reports of other
ammotheid (and phoxichilid) males heavily over-
burdened with egg masses to the point where the male
himself is barely visible (Cole, 1904; Stock, 1954;
B. Bain, pers. obs.).
Since the male pycnogonid can so easily care for
the eggs/larvae without much interference in his daily
activities, this frees up the female to increase her
fitness by potentially giving her many more oppor-
tunities for additional matings, opportunities usually
unavailable to females in most other groups of
organisms. Multiple matings in female pycnogonids
have yet to be documented, but there are some tanta-
lizing indicators that these matings could potentially
happen (Sanchez, 1959; King and Jarvis, 1970).
For instance, Sanchez (1959) observed female
Endeis spinosa release eggs from only a single femur
at any one time and both Sanchez (1959) and King and
Jarvis (1970) observed that females of Nymphon
gracile release eggs from two femurs at any one time.
Unfortunately, no other observations were published
by either, so it is unknown whether or not any of these
females engaged in additional matings, but conceiv-
ably, female pycnogonids could engage in a strategy in
which they only give the male one fourth of their
mature eggs during any one mating, thereby increasing
their potential fitness. Alternatively, females may have
evolved a strategy in which they can produce several
sets of mature eggs in a relatively short period of time,
thus allowing for multiple matings within one mating
season. One variation on this is the condition found in
some female callipallenids, such as Propallene longi-
ceps, in which the female has lots of immature eggs
present in the femur during the mating season and at
any one time, she only has 1–2 mature eggs per femur.
During a mating bout, the female will lay all of her
mature eggs at one time and could possibly mate again
relatively quickly depending on how long it takes her
to form more mature eggs.
Misconceptions and Misunderstandings
in the Literature
A nearly complete lack of information on many
different aspects of pycnogonid parental care at this
point in time quickly hampers any serious attempts to
investigate this topic in more detail. Since most
behavioral biologists are not well versed in pycno-
gonid biology, a number of misconceptions have
appeared in the parental care literature when attempt-
ing to extract specific information about pycnogonids
and insert this information into summaries of parental
care in invertebrate groups. Another, perhaps more
serious set of misunderstandings/typos has been slowly
accumulating in the pycnogonid literature itself in the
past few years. While many of these misconstrued
points in both sets of literature are relatively minor by
themselves, when taken together they can potentially
lead to serious errors when used as the basis for further
observations. In an attempt to correct these minor
problems, we have listed them in Table 6 along with
the correct words and/or explanations.
Acknowledgments
Thanks to Heike Bock for translating Schmidt and
Bückmann (1971), Helen Crisp for behavioral obser-
vations on several different Australian pycnogonids,
Avi Waksberg for reading and commenting on an
earlier draft of this paper, Jay Gillespie for sex ratio
information, and Steve Shuster for lots of helpful
discussion on this topic.
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  • ... The proboscis is flanked by the first limb pair, the generally three-articled and raptorial cheliphores (Fig. 1band e), being followed by the sensory palps and the ovigers, both limb pairs displaying various article numbers in different taxa (Fig. 1b, d and e). The ovigers are used by the males to carry developing eggs (Fig. 1b–d) and sometimes also hatched postembryonic instars (Fig. 1e ) – a rare example of paternal brood care in invertebrates – but in some taxa also for grooming and/or other functions (see [46]). Notably, not all pycnogonids retain the complete set of these three anterior limb pairs in the adult: with the exception of the ovigers in males, all of them can be partially or completely reduced in a taxon-and sexspecific pattern (e.g., Fig. 1aand d). ...
    ... During mating, fertilized eggs are transferred from the female to the ovigers of the male, where they are glued into packages with secretions of cement glands located in the male's femora (see [46] for review). The egg packages are carried on the ovigers at least until hatching of the first postembryonic instar (Figs. ...
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  • ... Hermaphroditic and gynandromorphic specimens may occur among the pycnogonids, but are quite uncommon. Ascorhynchus corderoi Du Bois-Reymond Marcus (1952) is the only recorded case of true hermaphroditism (Corrêa, 1987; Bain & Govedich, 2004). Some individuals of A. corderoi were collected with ovigers covered with egg masses, and in these individuals ovaries and testicles were found on all legs (Du Bois-Reymond Marcus, 1952). ...
    ... Some individuals of A. corderoi were collected with ovigers covered with egg masses, and in these individuals ovaries and testicles were found on all legs (Du Bois-Reymond Marcus, 1952). Cases of gynandromorphism in sexually dimorphic species have been recorded occasionally in Pycnogonida (Bain & Govedich, 2004). Ascorhynchus abyssi Sars 1877 was the first example of gynandromorphism known for the group. ...
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    A new species of Anoplodactylus was discovered in coral reefs from the State of Paraíba, northeastern Brazil. A. mirim sp. nov. is very small and is characterized for having 3 teeth on the cheliphores and a very small cement gland. It belongs to the A. pygmaeus complex, which contains very small species. A. batangensis is recorded for the first time along the Brazilian coast, and A. eroticus is recorded for the first time in the South Atlantic. We record the fifth known case of gynandromorphism, the fourth for Anoplodactylus, based on two specimens of A. eroticus.
  • ... In fact, mate choice is likely to be influenced not only by parental investment and potential reproductive rates, but also by the relative costs and benefits of choosiness, the mating history of the individuals , mate encounter rates, sex-specific mortalities, and variation in mate quality (Bonduriansky 2001; Kokko and Mappes 2005; Barry and Kokko 2010; Edward and Chapman 2011). The list of species in which males heavily invest in nuptial gifts or in parental care has quickly increased in the last decades, revealing cases of female–female competition for access to males and even exclusive male mate choice (e.g., Wilson et al. 2003; Bain and Govedich 2004a; Wells 2007; Gwynne 2008). Among arthropods, exclusive paternal care has evolved independently in at least 17 lineages (Tallamy 2001; Machado and Macías-Ordóñez 2007; Requena et al. 2010; Proud et al. 2011; Villareal-Manzanilla and Machado 2011), but detailed descriptions of reproductive interactions between males and females are available only for a few species belonging to distantly related taxa: the harvestman Zygopachylus albomarginis (Mora 1990), some giant water bugs of the family Belostomatidae (Smith 1997; Kight et al. 2011), and a few sea spiders of the class Pycnogonida (Bain and Govedich 2004a). ...
    ... The list of species in which males heavily invest in nuptial gifts or in parental care has quickly increased in the last decades, revealing cases of female–female competition for access to males and even exclusive male mate choice (e.g., Wilson et al. 2003; Bain and Govedich 2004a; Wells 2007; Gwynne 2008). Among arthropods, exclusive paternal care has evolved independently in at least 17 lineages (Tallamy 2001; Machado and Macías-Ordóñez 2007; Requena et al. 2010; Proud et al. 2011; Villareal-Manzanilla and Machado 2011), but detailed descriptions of reproductive interactions between males and females are available only for a few species belonging to distantly related taxa: the harvestman Zygopachylus albomarginis (Mora 1990), some giant water bugs of the family Belostomatidae (Smith 1997; Kight et al. 2011), and a few sea spiders of the class Pycnogonida (Bain and Govedich 2004a). These species show different degrees of sex role reversal (sensu Vincent et al. 1992), with evidence of female exclusive initiation of courtship behavior reported for Z. albomarginis and the sea spider Propallene saengeri (Bain and Govedich 2004b). ...
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    Paternal care has independently evolved in several arthropod lineages, but mating interactions have been described in detail for only a few species. Here, we describe the mating behavior of Iporangaia pustulosa, a Neotropical harvestman with exclusive paternal care. We obtained the data under natural conditions, and the results are based on 51 mating interactions. Females performed mate searching exclusively, locating and approaching stationary caring males on the vegetation. Upon arrival, nearly 33 % of the visiting females were promptly attacked and repelled by the males without copulating. We did not observe pre-copulatory courtship, and males, exclusively, performed copulatory courtship. Nearly 30 % of the females that copulated with caring males left the clutches without laying any egg. Finally, several behavioral actions reported here are remarkably similar to those observed in the sex-role-reversed harvestman Zygopachylus albomarginis, for which there is strong evidence of both male and female mate choice. In conclusion, our results provide evidence of male aggressive rejection of mates and female abandonment of clutches without ovipositing, suggesting that individuals of both sexes may evaluate and select mating partners.
  • ... Popular topics in the literature centered around molecular systematics and evolution, but over the past 15 years several publications have examined aspects of the development, biology, anatomy and morphology of shallowwater pycnogonids (e.g. Bain and Govedich, 2004; Brenneis et al., 2011a; Fornshell, 2014; Lehmann et al., 2011; Sánchez and López- González, 2010, 2013; Vilpoux and Waloszek, 2003). Pycnogonids are considered relatively rare, although there are regions around the world where they can be locally abundant (Schmidt and Buckmann , 1971) suggesting that these marine invertebrates could play an important role in marine ecosystems despite their small biomass (Arnaud and Bamber, 1987). ...
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  • ... Aggregated across trees, this reversal will be reconstructed with a high degree of uncertainty. We note also that there are no known reversals from male care in the Belostomatidae (giant water bugs, Smith 1997) or in Pycnogonids (sea spiders, Bain and Goveditch 2004), an order of arthropods related to insects—two large, speciose and exclusively male-caring groups. Three male-caring species of assassin bug (Rhinocoris spp.) that are morphologically almost identical probably also form a monophyletic clade (R. tristis, R. albopilosus, R. albopunctatus;). ...
  • ... One of the noteworthy behaviours observed were the pycnogonids bouncing up and down on top of each other. This kind of ‘dancing’ or ‘pumping’ behaviour in females is recognised as (an initiation to) mating behaviour [44]. No negative interactions were observed between pycnogonids and tubeworms on the video imagery, more precisely, pycnogonids did not invariably cause retraction of tubeworm plumes, nor were they observed to attack or nibble on tubeworm individuals. ...
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    The NEPTUNE cabled observatory network hosts an ecological module called TEMPO-mini that focuses on hydrothermal vent ecology and time series, granting us real-time access to data originating from the deep sea. In 2011-2012, during TEMPO-mini's first deployment on the NEPTUNE network, the module recorded high-resolution imagery, temperature, iron (Fe) and oxygen on a hydrothermal assemblage at 2186 m depth at Main Endeavour Field (North East Pacific). 23 days of continuous imagery were analysed with an hourly frequency. Community dynamics were analysed in detail for Ridgeia piscesae tubeworms, Polynoidae, Pycnogonida and Buccinidae, documenting faunal variations, natural change and biotic interactions in the filmed tubeworm assemblage as well as links with the local environment. Semi-diurnal and diurnal periods were identified both in fauna and environment, revealing the influence of tidal cycles. Species interactions were described and distribution patterns were indicative of possible microhabitat preference. The importance of high-resolution frequencies (<1 h) to fully comprehend rhythms in fauna and environment was emphasised, as well as the need for the development of automated or semi-automated imagery analysis tools.
  • ... Then, the eggs are fertilized and glued together, forming compact egg masses. They are carried until they hatch as protonymphon (characterized by a proboscis and three pairs of larval appendages), but in some cases, hatching stages (as protonymphon or other structural forms) remain on the male's ovigers, developing into different postlarval stages (Wilhelm et al. 1997; Bain and Govedich 2004). Although eggs usually hatch asLarva (Nakamura 1981; Bain 2003a, b; Bogomolova and Malakhov 2003, 2004 ). ...
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    In this paper, new data on larval and postlarval stages after newly collected and museum-deposited material of six Ammothea species is provided and compared with previously known information. Different developmental stages attached to the ovigerous legs of adult males for each species were found: four stages [protonymphon (Ptn), postlarval instar 1 (PL-1), postlarval instar 2 (PL-2), and postlarval instar 3 (PL-3)] for A. carolinensis; just one (Ptn) for A. clausi and A. minor; three stages (Ptn, PL-1, PL-2) for A. bicorniculata and A. spinosa; and other three (Ptn, PL-2, PL-3) for A. longispina. In the present contribution, the external morphology of each larval and postlarval instar is described, illustrated, and discussed. The larval and postlarval development of Ammothea bicorniculata, A. carolinensis, A. longispina, and A. spinosa is characterized by (1) the eggs hatch as a protonymphon larva; (2) the larvae and subsequent postlarval stages have yolk reserves and a relatively large size (0.5–0.85 mm in length for the protonymphon); (3) the postlarvae remain on the ovigerous legs of males during several moults; (4) the spinning spine is absent; and (5) the development of walking legs is sequential. The protonymphon larva of A. clausi and A. minor is the only stage on the ovigerous legs of males, and this stage is characterized by: (1) there is no yolk reserve and it has a relatively small size (0.22–0.3 mm in length); (2) the spinning spine is present; and (3) all larval appendages have a relatively large size.
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    For sexual selection to act on a given sex, there must exist variation in the reproductive success of that sex as a result of differential access to mates or fertilisations. The mechanisms and consequences of sexual selection acting on male animals are well documented, but research on sexual selection acting on females has only recently received attention. Controversy still exists over whether sexual selection acts on females in the traditional sense, and over whether to modify the existing definition of sexual selection (to include resource competition) or to invoke alternative mechanisms (usually social selection) to explain selection acting on females in connection with reproduction. However, substantial evidence exists of females bearing characters or exhibiting behaviours that result in differential reproductive success that are analogous to those attributed to sexual selection in males. Here we summarise the literature and provide substantial evidence of female intrasexual competition for access to mates, female intersexual signalling to potential mates, and postcopulatory mechanisms such as competition between eggs for access to sperm and cryptic male allocation. Our review makes clear that sexual selection acts on females and males in similar ways but sometimes to differing extents: the ceiling for the elaboration of costly traits may be lower in females than in males. We predict that current and future research on female sexual selection will provide increasing support for the parsimony and utility of the existing definition of sexual selection.
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    Since Darwin’s conception of sexual selection theory, scientists have struggled to identify the evolutionary forces underlying the pervasive differences between male and female behavior, morphology, and physiology. The Darwin- Bateman paradigm predicts that anisogamy imposes stronger sexual selection on males, which, in turn, drives the evolution of conventional sex roles in terms of female-biased parental care and male-biased sexual dimorphism. Al- though this paradigm forms the cornerstone of modern sexual selection theory, it still remains untested across the animal tree of life. This lack of evidence has promoted the rise of alternative hypotheses arguing that sex differences are entirely driven by environmental factors or chance. We demonstrate that, across the animal kingdom, sexual selection, as captured by standard Bateman metrics, is indeed stronger in males than in females and that it is evolution- arily tied to sex biases in parental care and sexual dimorphism. Our findings provide the first comprehensive evidence that Darwin’s concept of conventional sex roles is accurate and refute recent criticism of sexual selection theory.
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    Which sex should care for offspring is a fundamental question in evolution. Invertebrates, and insects in particular, show some of the most diverse kinds of parental care of all animals, but to date there has been no broad comparative study of the evolution of parental care in this group. Here, we test existing hypotheses of insect parental care evolution using a literature-compiled phylogeny of over 2000 species. To address substantial uncertainty in the insect phylogeny, we use a brute force approach based on multiple random resolutions of uncertain nodes. The main transitions were between no care (the probable ancestral state) and female care. Male care evolved exclusively from no care, supporting models where mating opportunity costs for caring males are reduced - e.g. by caring for multiple broods - but rejecting the "enhanced fecundity" hypothesis that male care is favoured because it allows females to avoid care costs. Biparental care largely arose by males joining caring females, and was more labile in Holometabola than in Hemimetabola. Insect care evolution most closely resembled amphibian care in general trajectory. Integrating these findings with the wealth of life history and ecological data in insects will allow testing of a rich vein of existing hypotheses.I This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.