- Email: [email protected]
Regeneration, predatory–prey interaction, and evolutionary history of articulate crinoids
Accepted Manuscript Title: Regeneration, predatory-prey interaction, and evolutionary history of articulate crinoids Author: Tatsuo Oji PII: DOI: Reference:
S1871-174X(15)00047-5 http://dx.doi.org/doi:10.1016/j.palwor.2015.06.001 PALWOR 312
To appear in:
Palaeoworld
Received date: Revised date: Accepted date:
30-12-2014 12-2-2015 4-6-2015
Please cite this article as: Oji, T.,Regeneration, predatory-prey interaction, and evolutionary history of articulate crinoids, Palaeoworld (2015), http://dx.doi.org/10.1016/j.palwor.2015.06.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Regeneration, predatory-prey interaction, and evolutionary history of articulate
ip t
crinoids
Tatsuo Oji
cr
Nagoya University Museum, Nagoya University, Nagoya 464-8601, Japan
us
E-mail address: [email protected]
an
Abstract
Regeneration and predatory-prey interaction of crinoids are reviewed. Crinoids have
crinoids.
M
strong powers of regeneration, and arm regeneration is common in fossil and Recent Regenerated arms commonly start from the ligamentary articulation called Therefore,
d
syzygy or cryptosyzygy, where crinoids can autotomize their arms.
te
regenerated arms can be formed after loss of arms by autotomy of arms, and such autotomy is commonly the response to predatory attacks.
Ac ce p
be used as the clue to estimate the predatory frequencies.
Thus, regenerated arms can Regeneration of “correct”
skeletal morphology as in the original depends on the existence of adoral nerve center. A stalk without the adoral nerve center cannot regenerate the “correct” morphology of the original skeleton, but forms of “callus” as skeletal overgrowth. The strong ability of regeneration is a key factor of the success of articulate crinoids in the geologic history since the Triassic onward.
Keywords: Crinoidea; isocrinine; regeneration; predation; ontogeny
Page 1 of 11
1. Introduction Echinoderms have a strong ability to regenerate body parts after injury or Generally, crinoids have
ip t
autotomy, and crinoids are no exception (Wilkie, 2001).
many regenerated arms, and many have lost the visceral mass, whose regeneration is This paper reviews previous studies on autotomy and
cr
known in comatulid crinoids.
predators.
us
regeneration of crinoids, and discusses ecologic relationship of crinoids to their An excellent review on the crinoid regeneration was done by Gahn and
an
Baumiller (2010), and therefore, this paper focuses on the strong ability of autotomy and regeneration in articulate crinoids, the only survivors after the end-Permian mass
M
extinction, and also on the existence of programmed autotomy in comatulid crinoids,
d
which was not well documented in the ontogeny.
te
2. Regeneration in articulate crinoids
Regenerated skeletal parts are common in crinoids.
They are most commonly
Ac ce p
found in the arms (Oji, 2001), but also other body parts such as the visceral mass which can regenerate after autotomy (Reichensperger, 1912; Meyer, 1985, 1988).
During the
growth of regenerated arms, there is a clear boundary between the original and the regenerated parts with an abrupt diameter change, or color difference (for extant crinoids) (Fig. 1). Examples of regenerated arms in fossil crinoids are summarized in Oji (2001).
The position where regenerated arms begin tends to be random, but for
articulate crinoids, they are commonly at the ligamentary articulation called syzygy (or cryptosyzygy) where crinoids can autotomize their distal arms.
Syzygy consists of a
tightly connected pair of brachials (arm plates) called epizygal and hypozagal, the epizygal being the distal and the hypozygal being the proximal brachials among the pair.
Page 2 of 11
If mechanical or chemical stimuli are applied to the distal arms, or a predatory attack such as a bite occurs in the distal arms of comatulid criniods, the break occurs at the
ip t
proximal syzygy that is closest to the location of stimuli, attacks or bites. The correspondence of the start of regenerations at syzygies in most museum specimens
cr
suggests that most of the regenerated arms in articulates were the result of autotomy Articulate crinoids
us
(and probably non-lethal predatory attacks) to crinoid arms.
generally possess numerous syzygies or cryptosyzygies in the arms, and thus they
an
probably have more ability in autotomizing and regenerating arms than most of the Paleozoic crinoids. Gahn and Baumiller (2010) noted that crinoids have always had
M
the ability to regenerate lost arms, and such ability has been maintained through the history of crinoids. Regeneration of lost arms is a common phenomenon through the
d
crinoid history; but since the evolution of articulate crinoids, chances of autotomy and
te
regeneration should be increased.
The most basal place for autotomy in the crown (arms plus theca) is between
Ac ce p
the basal and radial plates in isocrinines. cryptosyzygial.
In Metacrinus, this facet is flat and
Even if Metacrinus loses its entire body above the basals, including
the visceral mass, it can regenerate its entire arms (and radials) and its visceral mass within several months in aquarium (Amemiya and Oji, 1992).
Thus, crinoids are
thought to possess very strong ability of regeneration.
3. Correct and incorrect regenerations after autotomy Crinoids tend to regenerate the lost body parts exactly the same as or similar to the original one. However, sometimes they regenerate a very different morphology, such as callus.
Whether crinoids regenerate their lost body parts correctly (i.e.,
Page 3 of 11
morphology similar to the previous one) or not seems to depend on the existence of the adoral nerve center (or the entoneural nerve center (chambered organ), Gahn and
ip t
Baumiller, 2010) located in the basal part of theca. After “decapitation” below the basal circlet, stalks cannot regenerate the
These examples were reported from both extant (Donovan and Pawson, 1997)
us
stalk.
cr
original morphology, but tend to produce an irregular “callus” above the non-damaged
and fossil (Ausich and Baumiller, 1993; Donovan and Schmidt, 2007) crinoids.
an
Experiments with extant crinoids in a tank (Nakano et al., 2004) demonstrated that Metacrinus rotundus, after the most of the stalk was cut below the basals but
M
retained the aboral nerve center, could regenerate the entire crown, but the stalk cut below the basals cannot regenerate the lost part of stalk (but continues to live at least for
d
a year, and probably more years). Therefore, the adoral nerve center housed in the
lost body parts.
te
basal part of theca (near the basal circlet) is necessary for the “correct” regeneration of Instead, if the adoral nerve center is missing, the crinoid either cannot
Ac ce p
regenerate the lost body parts, or they reproduce skeletal parts with different morphology from the original (“incorrect regeneration”, or “overgrowth” in the sense of Oji and Amemiya, 1998b).
The adoral nerve center located in the basal part of theca is thought to be
crucial for the correct regeneration of the body parts.
However, even with the
existence of the adoral nerve center, the number of brachials, when regenerated, tends to change from the original number (Oji, 1986 for Metacrinus and Saracrinus), thus leading to incorrect regeneration. In Metacrinus the number of primibrachials tends to be reduced from the original seven, whereas in Saracrinus the number tends to increase from the original four. Also aberrant arm branching can be formed in the regenerated
Page 4 of 11
part of the arms (Gahn and Baumiller, 2010).
Autotomy also occurs in isocrinine stalks.
ip t
4. Autotomy of stalk Autotomy occurs only at an
After autotomy of the distal stalk, crinoids can temporally move and change the
locations (Baumiller and Messing, 2007).
us
nodal.
cr
articulation called cryptosymplexy, which is located at the distal articulation of the
The discarded stalk can continue to stand
an
for a while on the sea floor (Fujita et al., 1987). In a tank experiment, stalk fragments of Metacrinus rotundus left on the bottom of the tank can live more than a year after
M
they were detached, but there was no regeneration or overgrowth afterwards from the detached stalk (Oji and Amemiya, 1998a).
d
If this stalk autotomy is caused by the response of crinoids to escaping from
te
predators such as sea urchins (Baumiller et al., 2008), the growth rate of stalk and the frequency of stalk autotomy should depend on the rate of encounter of predators: high
Ac ce p
growth speed in the environment with frequent predation, and vice versa. In
some
isocrinines
such
as
Endoxocrinus
parrae
or
Annacrinus
wyvillethomsoni, calcification occurs on the distal facet of stalk, sealing the axial canal (Roux, 1977).
5. Regenerated arms as a response to nonlethal predatory attack Except for the juvenile stage during which crinoids tend to increase the number of arms, they do not autotomize their arms.
However, crinoids have many incidences
of regenerated arms, mostly from the facet of syzygy or cryptosyzygy where crinoids can autotomize their arms.
Therefore, it is highly probable that the regenerated arms
Page 5 of 11
are formed after loss of arms by a non-lethal attack of predators. If so, regenerated arms can be a good indicator of the frequency at which crinoids are attacked and
ip t
autotomize their arms. Frequency of regenerated arms is a function of predatory attacks.
If the
cr
crinoids are subjected to higher incidences of predatory attacks, they tend to have high
Meyer (1985) examined the frequency of regenerated
us
frequency of regenerated arms.
arms in exposed and nocturnal species of comatulids, and found that the former has Regeneration frequency also
an
higher frequency of regenerated arms than the latter. differs between shallow and deeper water crinoids.
Oji (1996) demonstrated that
M
Endoxocrinus parrae living in shallow water tends to have more frequently regenerated arms than deep water inhabitants. Baumiller (2013) also found that specimens of
d
Florometra serratissima living off the Pacific coast of United States have higher
te
frequency of regeneration in shallower populations than in deeper populations. Thus, these data clearly show that there are fewer incidences of non-lethal attacks to crinoids
Ac ce p
in deep water, supporting the hypothesis that crinoids were eliminated from shallow water by expansion of predators in shallow water. There are also studies of temporal change in the frequency of regeneration in
crinoid arms.
Gahn and Baumiller (2005) and Baumiller and Gahn (2004) showed that
there is a high frequency of regenerated arms in the Paleozoic. They think that the increase of predators should be attributed to the diversification of durophagous predators. The number of cryptosyzygies per individual of isocrinines has increased through time.
Before the middle Cretaceous, most isocrinines possessed synarthrial
articulations in the primibrachials (the first arm branching series) and also in
Page 6 of 11
secundibrachials, and after the middle Cretaceous, many isocrinines had replaced these synarthries with cryptosyzygies (Oji, 1985; Hess and Messing, 2011). Synarthry is a
ip t
kind of ligamentary articulation as is a cryptosyzygy, but synarthry is not an articulation for autotomy, whereas cryptosyzygy is a specialized articulation for autotomy.
Thus,
cr
there is an evolutionary trend in isocrinines for the number of articulations for autotomy
us
to increase over time. The advantage of possessing more numerous cryptosyzygies is still unknown, but modern Metacrinus kept in aquaria often autotomize their arms at
an
primibrachials when the water temperature rises or when kept for months in the tank. Therefore, autotomy at the cryptosyzygy in the primibrachials should possess some
M
defensive/adaptive meaning acquired in the evolutionary history of Isocrinina.
te
comatulids
d
6. Regenerated arms after a “programmed” autotomy during ontogeny of
Shibata and Oji (2005) demonstrated that the number of arms (originally ten)
Ac ce p
of juvenile comatulid (Oxycomanthus japonicus) increases by autotomizing one arm (secundibrachials; second series of arm branching after the first axillary).
Individuals
tend to autotomize an arm and produce another new axillary plate to hold two new arms. Then another arm (usually positioned at the opposite side of the ray from the original autotomy/regeneration) autotomizes.
Therefore, this is an example of “augmentative
autotomy” by Gislén (1924). Oxycomanthus japonicus tends to maintain maximum feeding capability by keeping as many arms as possible, by changing the places of autotomy in a distant place from the former place of autotomy.
Therefore, at least
these comatulid crinoids, and probably many comatulids, have this type of “programmed autotomy” and regeneration afterwards in their ontogenetic stage.
Page 7 of 11
7. Conclusions
ip t
Regeneration is one of the most conspicuous characteristics of crinoids. Regenerations can be formed after non-lethal predatory attacks, but also can be formed
cr
during ontogeny as a programmed autotomy for increasing the number of arms.
us
Crinoid regeneration is important for estimating non-lethal predation; and therefore this will be used for estimating local predation pressure where crinoids live. Existence of a
an
strong ability of regeneration in articulate crinoids is a key factor of their success in the
M
geologic history since their appearance and diversification from the Triassic onward.
Acknowledgments
He also
d
T.O. thanks Jih-Pai (Alex) Lin for inviting me to contribute to this volume.
Ac ce p
te
thanks comments and the improvements of English text by D.L. Meyer and W.I. Ausich.
References
Amemiya, S., Oji, T., 1992. Regeneration in sea lilies. Nature 357, 546-547. Ausich, W.I., Baumiller, T.K., 1993. Column regeneration in an Ordovician crinoid (Echinodermata): Paleobiologic implications. Journal of Paleontology 67, 1068-1070. Baumiller, T.K., 2013. Arm regeneration frequencies in Florometra serratissima (Crinoidea, Echinodermata): impact of depth of habitat on rates of arm loss. Cahiers de Biologie Marine 54, 571-576.
Page 8 of 11
Baumiller, T.K., Gahn, F.J., 2004. Testing predation-driven evolution using mid-Paleozoic crinoid arm regeneration. Science 305, 1453-1455.
evolutionary
implications.
Palaeonntologia
ip t
Baumiller, T.K., Messing, C.G., 2007. Stalked crinoid locomotion, and its ecological and Electronica
10
(2A),
cr
http://palaeo-electronica.org/paleo/2007_1/crinoid/index.html
us
Baumiller, T.K., Mooi, R., Messing, C.G., 2008. Urchins in the meadow: paleobiological and evolutionary implications of cidaroid predation on
an
crinoids. Paleobiology 34, 22-34.
Donovan, S.K., Pawson, D.L., 1997. Proximal growth of the column in bathycrinid
M
crinoids (Echinodermata) following decapitation. Bulletin of Marine Science 61, 571-579.
d
Donovan, S.K., Schmidt, D.A., 2007. Survival of crinoid stems following decapitation:
263-270.
te
evidence from the Ordovician and palaeobiological implications. Lethaia 34,
Ac ce p
Fujita, T., Ohta, S., Oji, T., 1987. Photographic observations of the stalked criniod Metacrinus rotundus Carpenter in Suruga Bay, central Japan. Journal of the
Oceanograhical Society of Japan 43, 333-343.
Gahn, F.J., Baumiller, T.K., 2005. Arm regeneration in Mississippian crinoids: Evidence of intense predation pressure in the Paleozoic. Paleobiology 31, 151-164.
Gahn, F.J., Baumiller, T.K., 2010. Evolutionary history of regeneration in crinoids (Echinodermata). Integrative and Comparative Biology 50, 514a-514m. Gislén, T., 1924. Echinoderm studies. Zoologiska Bidrag från Uppsala 9, 1-330. Hess, H., Messing, C.G., 2011. Revised Crinoidea, Vol. 3. In: Ausich, W.I. (Ed.), Treatise on Invertebrate Paleontology. Part T, Echinodermata 2, Vol. 3.
Page 9 of 11
University of Kansas and Paleontological Institute, Lawrence, Kansas, pp. 1-261.
from the Great Barrier Reef. Paleobiology 11, 154-164.
ip t
Meyer, D.L., 1985. Evolutionary implications of predation on Recent comatulid crinoids
cr
Meyer, D.L., 1988. Crinoids as renewable resources: rapid regeneration of the visceral
us
mass in a tropical reef-dwelling crinoid from Australia. In: Burke, R.D., Mladenov, P.D., Lambert, P., Parsley, R.L. (Eds.), Echinoderm Biology.
an
Rotterdam, Balkema, pp. 519-522.
Moore, R., Vokes, H.E., 1953. Lower Tertiary crinoids from northwestern Oregon.
M
United States Geological Survey Professional Paper 233-E, 113-148. Nakano, H., Hibino, T., Hara, Y., Oji, T., Amemiya, S., 2004. Regrowth of the stalk of
d
the sea lily Metacrinus rotundus (Echinodermata: Crinoidea). Journal of
te
Experimental Zoology 301A, 464-471. Oji, T., 1985. Early Cretaceous Isocrinus from Northeast Japan. Palaeontology 28,
Ac ce p
661-674.
Oji, T., 1986. Skeletal variation related to arm regeneration in Metacrinus and Saracrinus, Recent stalked crinoids. Lethaia 19, 355-360.
Oji, T., 1996. Is predation intensity reduced with increasing depth? Evidence from the west Atlantic stalked crinoid Endoxocrinus parrae (Gervais) and
implications for the Mesozoic marine revolution. Paleobiology 22, 339-351.
Oji, T., 2001. Fossil record of echinoderm regeneration with special regard to crinoids. Microscopy Research and Technique 55 (6), 397-402. Oji, T., Amemiya, S., 1998a. Survival of crinoid stalk fragments and its taphonomic implications. Paleontological Research 2, 67-70.
Page 10 of 11
Oji, T., Amemiya, S., 1998b. Survival of crinoid stalk fragments and its taphonomic implications: additional discussion. Paleontological Research 2, 285-286.
ip t
Reichensperger, A., 1912. Beiträge zur Histologic und zum Verlauf der Regeneration bei Crinoiden. Zeitschrift für wissenschaftliche Zoologie 101, 1-69.
cr
Roux, M., 1977. The stalk joints of Recent Isocrinidae (Crinoidea). Bulletin of the
us
British Museum (Natural History), Zoology 32 (3), 45-64.
Shibata, T.F., Oji, T., 2005. Autotomy and arm number increase in Oxycomanthus
an
japonicus (Echinodermata, Crinoidea). Invertebrate Biology 122 (4), 375-379.
M
Wilkie, I.C., 2001. Autotomy as a prelude to regeneration in echinoderms. Microscopy
te
d
Research and Technique 55, 369-396.
Ac ce p
Explanations for figure
Figure 1. Regenerated arm of Isocrinus oregonensis (Moore and Vokes, 1953). Note that a small regenerated arm (arrow) extends from the upper surface of hypozygal (lower pair of brachials with a syzygial articulation), where autotomy preferentially occurs. Photo by J. Schneider.
Page 11 of 11
S1871-174X(15)00047-5 http://dx.doi.org/doi:10.1016/j.palwor.2015.06.001 PALWOR 312
To appear in:
Palaeoworld
Received date: Revised date: Accepted date:
30-12-2014 12-2-2015 4-6-2015
Please cite this article as: Oji, T.,Regeneration, predatory-prey interaction, and evolutionary history of articulate crinoids, Palaeoworld (2015), http://dx.doi.org/10.1016/j.palwor.2015.06.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Regeneration, predatory-prey interaction, and evolutionary history of articulate
ip t
crinoids
Tatsuo Oji
cr
Nagoya University Museum, Nagoya University, Nagoya 464-8601, Japan
us
E-mail address: [email protected]
an
Abstract
Regeneration and predatory-prey interaction of crinoids are reviewed. Crinoids have
crinoids.
M
strong powers of regeneration, and arm regeneration is common in fossil and Recent Regenerated arms commonly start from the ligamentary articulation called Therefore,
d
syzygy or cryptosyzygy, where crinoids can autotomize their arms.
te
regenerated arms can be formed after loss of arms by autotomy of arms, and such autotomy is commonly the response to predatory attacks.
Ac ce p
be used as the clue to estimate the predatory frequencies.
Thus, regenerated arms can Regeneration of “correct”
skeletal morphology as in the original depends on the existence of adoral nerve center. A stalk without the adoral nerve center cannot regenerate the “correct” morphology of the original skeleton, but forms of “callus” as skeletal overgrowth. The strong ability of regeneration is a key factor of the success of articulate crinoids in the geologic history since the Triassic onward.
Keywords: Crinoidea; isocrinine; regeneration; predation; ontogeny
Page 1 of 11
1. Introduction Echinoderms have a strong ability to regenerate body parts after injury or Generally, crinoids have
ip t
autotomy, and crinoids are no exception (Wilkie, 2001).
many regenerated arms, and many have lost the visceral mass, whose regeneration is This paper reviews previous studies on autotomy and
cr
known in comatulid crinoids.
predators.
us
regeneration of crinoids, and discusses ecologic relationship of crinoids to their An excellent review on the crinoid regeneration was done by Gahn and
an
Baumiller (2010), and therefore, this paper focuses on the strong ability of autotomy and regeneration in articulate crinoids, the only survivors after the end-Permian mass
M
extinction, and also on the existence of programmed autotomy in comatulid crinoids,
d
which was not well documented in the ontogeny.
te
2. Regeneration in articulate crinoids
Regenerated skeletal parts are common in crinoids.
They are most commonly
Ac ce p
found in the arms (Oji, 2001), but also other body parts such as the visceral mass which can regenerate after autotomy (Reichensperger, 1912; Meyer, 1985, 1988).
During the
growth of regenerated arms, there is a clear boundary between the original and the regenerated parts with an abrupt diameter change, or color difference (for extant crinoids) (Fig. 1). Examples of regenerated arms in fossil crinoids are summarized in Oji (2001).
The position where regenerated arms begin tends to be random, but for
articulate crinoids, they are commonly at the ligamentary articulation called syzygy (or cryptosyzygy) where crinoids can autotomize their distal arms.
Syzygy consists of a
tightly connected pair of brachials (arm plates) called epizygal and hypozagal, the epizygal being the distal and the hypozygal being the proximal brachials among the pair.
Page 2 of 11
If mechanical or chemical stimuli are applied to the distal arms, or a predatory attack such as a bite occurs in the distal arms of comatulid criniods, the break occurs at the
ip t
proximal syzygy that is closest to the location of stimuli, attacks or bites. The correspondence of the start of regenerations at syzygies in most museum specimens
cr
suggests that most of the regenerated arms in articulates were the result of autotomy Articulate crinoids
us
(and probably non-lethal predatory attacks) to crinoid arms.
generally possess numerous syzygies or cryptosyzygies in the arms, and thus they
an
probably have more ability in autotomizing and regenerating arms than most of the Paleozoic crinoids. Gahn and Baumiller (2010) noted that crinoids have always had
M
the ability to regenerate lost arms, and such ability has been maintained through the history of crinoids. Regeneration of lost arms is a common phenomenon through the
d
crinoid history; but since the evolution of articulate crinoids, chances of autotomy and
te
regeneration should be increased.
The most basal place for autotomy in the crown (arms plus theca) is between
Ac ce p
the basal and radial plates in isocrinines. cryptosyzygial.
In Metacrinus, this facet is flat and
Even if Metacrinus loses its entire body above the basals, including
the visceral mass, it can regenerate its entire arms (and radials) and its visceral mass within several months in aquarium (Amemiya and Oji, 1992).
Thus, crinoids are
thought to possess very strong ability of regeneration.
3. Correct and incorrect regenerations after autotomy Crinoids tend to regenerate the lost body parts exactly the same as or similar to the original one. However, sometimes they regenerate a very different morphology, such as callus.
Whether crinoids regenerate their lost body parts correctly (i.e.,
Page 3 of 11
morphology similar to the previous one) or not seems to depend on the existence of the adoral nerve center (or the entoneural nerve center (chambered organ), Gahn and
ip t
Baumiller, 2010) located in the basal part of theca. After “decapitation” below the basal circlet, stalks cannot regenerate the
These examples were reported from both extant (Donovan and Pawson, 1997)
us
stalk.
cr
original morphology, but tend to produce an irregular “callus” above the non-damaged
and fossil (Ausich and Baumiller, 1993; Donovan and Schmidt, 2007) crinoids.
an
Experiments with extant crinoids in a tank (Nakano et al., 2004) demonstrated that Metacrinus rotundus, after the most of the stalk was cut below the basals but
M
retained the aboral nerve center, could regenerate the entire crown, but the stalk cut below the basals cannot regenerate the lost part of stalk (but continues to live at least for
d
a year, and probably more years). Therefore, the adoral nerve center housed in the
lost body parts.
te
basal part of theca (near the basal circlet) is necessary for the “correct” regeneration of Instead, if the adoral nerve center is missing, the crinoid either cannot
Ac ce p
regenerate the lost body parts, or they reproduce skeletal parts with different morphology from the original (“incorrect regeneration”, or “overgrowth” in the sense of Oji and Amemiya, 1998b).
The adoral nerve center located in the basal part of theca is thought to be
crucial for the correct regeneration of the body parts.
However, even with the
existence of the adoral nerve center, the number of brachials, when regenerated, tends to change from the original number (Oji, 1986 for Metacrinus and Saracrinus), thus leading to incorrect regeneration. In Metacrinus the number of primibrachials tends to be reduced from the original seven, whereas in Saracrinus the number tends to increase from the original four. Also aberrant arm branching can be formed in the regenerated
Page 4 of 11
part of the arms (Gahn and Baumiller, 2010).
Autotomy also occurs in isocrinine stalks.
ip t
4. Autotomy of stalk Autotomy occurs only at an
After autotomy of the distal stalk, crinoids can temporally move and change the
locations (Baumiller and Messing, 2007).
us
nodal.
cr
articulation called cryptosymplexy, which is located at the distal articulation of the
The discarded stalk can continue to stand
an
for a while on the sea floor (Fujita et al., 1987). In a tank experiment, stalk fragments of Metacrinus rotundus left on the bottom of the tank can live more than a year after
M
they were detached, but there was no regeneration or overgrowth afterwards from the detached stalk (Oji and Amemiya, 1998a).
d
If this stalk autotomy is caused by the response of crinoids to escaping from
te
predators such as sea urchins (Baumiller et al., 2008), the growth rate of stalk and the frequency of stalk autotomy should depend on the rate of encounter of predators: high
Ac ce p
growth speed in the environment with frequent predation, and vice versa. In
some
isocrinines
such
as
Endoxocrinus
parrae
or
Annacrinus
wyvillethomsoni, calcification occurs on the distal facet of stalk, sealing the axial canal (Roux, 1977).
5. Regenerated arms as a response to nonlethal predatory attack Except for the juvenile stage during which crinoids tend to increase the number of arms, they do not autotomize their arms.
However, crinoids have many incidences
of regenerated arms, mostly from the facet of syzygy or cryptosyzygy where crinoids can autotomize their arms.
Therefore, it is highly probable that the regenerated arms
Page 5 of 11
are formed after loss of arms by a non-lethal attack of predators. If so, regenerated arms can be a good indicator of the frequency at which crinoids are attacked and
ip t
autotomize their arms. Frequency of regenerated arms is a function of predatory attacks.
If the
cr
crinoids are subjected to higher incidences of predatory attacks, they tend to have high
Meyer (1985) examined the frequency of regenerated
us
frequency of regenerated arms.
arms in exposed and nocturnal species of comatulids, and found that the former has Regeneration frequency also
an
higher frequency of regenerated arms than the latter. differs between shallow and deeper water crinoids.
Oji (1996) demonstrated that
M
Endoxocrinus parrae living in shallow water tends to have more frequently regenerated arms than deep water inhabitants. Baumiller (2013) also found that specimens of
d
Florometra serratissima living off the Pacific coast of United States have higher
te
frequency of regeneration in shallower populations than in deeper populations. Thus, these data clearly show that there are fewer incidences of non-lethal attacks to crinoids
Ac ce p
in deep water, supporting the hypothesis that crinoids were eliminated from shallow water by expansion of predators in shallow water. There are also studies of temporal change in the frequency of regeneration in
crinoid arms.
Gahn and Baumiller (2005) and Baumiller and Gahn (2004) showed that
there is a high frequency of regenerated arms in the Paleozoic. They think that the increase of predators should be attributed to the diversification of durophagous predators. The number of cryptosyzygies per individual of isocrinines has increased through time.
Before the middle Cretaceous, most isocrinines possessed synarthrial
articulations in the primibrachials (the first arm branching series) and also in
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secundibrachials, and after the middle Cretaceous, many isocrinines had replaced these synarthries with cryptosyzygies (Oji, 1985; Hess and Messing, 2011). Synarthry is a
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kind of ligamentary articulation as is a cryptosyzygy, but synarthry is not an articulation for autotomy, whereas cryptosyzygy is a specialized articulation for autotomy.
Thus,
cr
there is an evolutionary trend in isocrinines for the number of articulations for autotomy
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to increase over time. The advantage of possessing more numerous cryptosyzygies is still unknown, but modern Metacrinus kept in aquaria often autotomize their arms at
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primibrachials when the water temperature rises or when kept for months in the tank. Therefore, autotomy at the cryptosyzygy in the primibrachials should possess some
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defensive/adaptive meaning acquired in the evolutionary history of Isocrinina.
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comatulids
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6. Regenerated arms after a “programmed” autotomy during ontogeny of
Shibata and Oji (2005) demonstrated that the number of arms (originally ten)
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of juvenile comatulid (Oxycomanthus japonicus) increases by autotomizing one arm (secundibrachials; second series of arm branching after the first axillary).
Individuals
tend to autotomize an arm and produce another new axillary plate to hold two new arms. Then another arm (usually positioned at the opposite side of the ray from the original autotomy/regeneration) autotomizes.
Therefore, this is an example of “augmentative
autotomy” by Gislén (1924). Oxycomanthus japonicus tends to maintain maximum feeding capability by keeping as many arms as possible, by changing the places of autotomy in a distant place from the former place of autotomy.
Therefore, at least
these comatulid crinoids, and probably many comatulids, have this type of “programmed autotomy” and regeneration afterwards in their ontogenetic stage.
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7. Conclusions
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Regeneration is one of the most conspicuous characteristics of crinoids. Regenerations can be formed after non-lethal predatory attacks, but also can be formed
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during ontogeny as a programmed autotomy for increasing the number of arms.
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Crinoid regeneration is important for estimating non-lethal predation; and therefore this will be used for estimating local predation pressure where crinoids live. Existence of a
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strong ability of regeneration in articulate crinoids is a key factor of their success in the
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geologic history since their appearance and diversification from the Triassic onward.
Acknowledgments
He also
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T.O. thanks Jih-Pai (Alex) Lin for inviting me to contribute to this volume.
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thanks comments and the improvements of English text by D.L. Meyer and W.I. Ausich.
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Explanations for figure
Figure 1. Regenerated arm of Isocrinus oregonensis (Moore and Vokes, 1953). Note that a small regenerated arm (arrow) extends from the upper surface of hypozygal (lower pair of brachials with a syzygial articulation), where autotomy preferentially occurs. Photo by J. Schneider.
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