Chapter 4
Echinoderm Diversity in Panama:
144 Years of Research Across the Isthmus
Simon E. Coppard and Juan Jos? Alvarado
4.1 Introduction
The Republic of Panama is the southernmost country in Central America between
07000?10000 north and 77000?83000 west and is located between Costa Rica to
the north and Colombia to the south. The country runs from east to west with a
length of 772 km and a width that varies from 60 to 177 km (Meditz and Hanratty
1987). Panama has both Caribbean and Pacific coastlines that total some 2,857 km
and which incorporate a vast diversity of marine habitats and ecosystems. The
80 km Panama Canal bisects the country and although this is theoretically a
freshwater barrier, it provides a link between the Atlantic and Pacific Oceans.
Approximately one hundred and fifty rivers flow into the Caribbean, while over
three hundred rivers flow into the eastern Pacific.
Panama?s weather is governed by the Inter-Tropical Convergence Zone which
dictates the seasonal patterns of wind and rainfall in the region. The dry season
(mid-December to mid-April) is characterised by low precipitation but strong
winds as a result of the northeast trade winds (Forsbergh 1969; Amador et al.
2006). The rainy season (May to November) has light winds with heavy rainfall
S. E. Coppard (&)
Smithsonian Tropical Research Institute, PO BOX 0843-03092Balboa, Anc?n,
Panam?
e-mail: CoppardS@si.edu
J. J. Alvarado
Centro de Investigaci?n en Ciencias del Mar y Limnolog?a (CIMAR),
Universidad de Costa Rica, San Pedro, 11501-2060, San Jos?, Costa Rica
e-mail: juanalva76@yahoo.com
J. J. Alvarado
Posgrado en Ciencias Marinas y Costeras,
Universidad Aut?noma de Baja California Sur, La Paz, M?xico
J. J. Alvarado and F. A. Sol?s-Mar?n (eds.), Echinoderm Research and Diversity
in Latin America, DOI: 10.1007/978-3-642-20051-9_4,
 Springer-Verlag Berlin Heidelberg 2013
107
which varies regionally from less than 1.3 m to more than 3 m per year, with
rainfall on the Caribbean side typically being heavier than on the Pacific side of the
continental divide (Meditz and Hanratty 1987).
The formation of the Isthmus of Panama is considered to be one of the most
important geologic events of the past 60 million years as it had an enormous
impact on Earth?s climate and environment. It occurred due to the gradual collision
of the Pacific, Cocos, Nazca and Caribbean plates which led to uplift of the sea
floor and the formation of volcanic islands. Over the next 12 million years vast
quantities of sediment from North and South America were deposited in between
the newly emerging islands, with final closure of the straits occurring in the late
Pliocene, 2.8 million years ago (mya) (Coates et al. 2005). This formation blocked
the North Equatorial Current which had previously flowed westward through the
Central American Seaway and forced the current northwards forming the Gulf
Stream of today (Berggren and Hollister 1974; Burton et al. 1997). With the
Pacific and Atlantic no longer mixing, there were significant changes in temper-
ature, salinity and primary productivity. This resulted in both species extinctions
and species radiations as environments changed (Jackson et al. 1993). Sister
species that were isolated on either side of the isthmus and that subsequently
diverged are referred to as geminates (Jordan 1908). These represent initially
similar genomes that were isolated and diverged over the last 3 million years
(Lessios 2008) and provide insights into evolutionary adaptations in response to
the changing environments.
Today the Caribbean coast of Panama incorporates coral reefs, seagrass beds,
rocky shores, mud-flats and mangroves and has a narrow continental shelf.
It continues to be influenced by the Atlantic North Equatorial Current which flows
through the Lesser Antilles (Kinder et al. 1985). The coast of the south-western
Caribbean including Panama is also affected by a cyclonic gyre that develops from
this current (Gordon 1967; Kinder et al. 1985; G?mez et al. 2005). For an in-depth
review of the Caribbean habitats of Panama, see G?mez et al. (2005). The
Caribbean experiences very small tidal ranges (less than 0.5 m) and has relatively
stable conditions. Its waters are clear and nutrient poor (D?Croz and Robertson
1997; D?Croz et al. 2005; Collin et al. 2009) and unlike the north coast of
Colombia there is no upwelling. These conditions are suitable for growth of
extensive coral reefs which date back to the early Pleistocene (Glynn 1982; Cort?s
1993). Surface waters of the Caribbean have an upper 200 m layer of warm water
heated by solar radiation, which has a correspondingly high salinity. Surface water
temperatures vary from 27 C in the dry season to 30 C in the rainy season, while
salinity varies from 36 psu in the dry season to 32 psu in the rainy season (D?Croz
and Robertson 1997). Two archipelagos are present off the Caribbean coast of
Panama, the San Blas (Kuna Yala) Archipelago which has a very narrow conti-
nental shelf and is subject to strong ocean influence with an oligotrophic coastal
area (D?Croz and Robertson 1997) and the Bocas del Toro Archipelago, with a
larger continental shelf, and greater influence from continental run-off (D?Croz
et al. 2005). Five national parks have been created along the Caribbean coast of
108 S. E. Coppard and J. J. Alvarado
Panama: Bastimentos Island National Marine Park, Portobelo, Soberania, Galeta,
Chagres, and the wetlands of San San Pond Sank (G?mez et al. 2005).
The Pacific coast of Panama is comprised of two gulfs; the Gulf of Chiriqu? and
the Gulf of Panama which are separated by the Azuero Peninsula (Fig. 4.1). These
regions experience broad semi-diurnal tides with a range of up to 6 m (Glynn 1972).
Despite their close proximity, they experience very different hydrological condi-
tions. The Gulf of Panama includes the Gulf of San Miguel, the Gulf of Parita and
Panama Bay, as well as the Pearl Islands Archipelago which is a Marine Special
Management Zone (Guzman et al. 2008). The gulf is broad and shallow, with much
of it being less than 40 m deep due to the extension of the continental shelf. The
coastal environments consist of muddy and sandy beaches with extensive mangrove
forests, which receive large amounts of freshwater runoff from rivers such as the Rio
Chepo and Rio Chico as well as the discharge from the Panama Canal. Coral reefs
are only moderately developed and are associated with the Pearl Islands Archi-
pelago and the inshore island of Taboga. Throughout the rainy season the surface
water temperature ranges from 26?28 C, while salinity is typically below 30 psu
(D?Croz et al. 1991). During the dry season (December to April) the Gulf of Panama
experiences wind-driven, seasonal upwelling of colder, more saline, nutrient-rich
water (Forsberg 1963; Forsbergh 1969; D?Croz et al. 1991; D?Croz and Robertson
1997; G?mez et al. 2005; Pennington et al. 2006), which results in significantly
increased primary productivity. This occurs due to the displacement of the surface
water by northern winds and can result in a surface water temperature decrease of
12 C within 24 h (Glynn 1972). The Gulf of Panama is also subjected to the effects
of the El Ni?o-Southern Oscillation (ENSO) every two to seven years (Guzman and
Cortes 2007) resulting in the warming of the water up to 31 C (Glynn 1985a).
Fig. 4.1 Distribution of coral reefs and mangrove forests along the coasts of Panama (adapted
from G?mez et al. 2005). Black stars: coral reefs; grey shading: mangroves
4 Echinoderm Diversity in Panama 109
In contrast, the Gulf of Chiriqu? has a narrower continental shelf and less
freshwater input from continental runoff. It contains Chiriqu? National Park and
Coiba Nacional Park which has World Heritage Site status. Several island com-
plexes are present, including the islands of Boca Brava, Los Ladrones, Islas Secas,
Parilla, Isla Palenque, Montuosa, and Isla Jicaron, with Isla Jicarita being the
island furthest south of the Panama mainland. In the northwest of the gulf, water
depth gradually increases down the continental shelf. However, in the east, water
depth sharply drops to 160 m before plunging down the continental slope and
reaching a depth of 1,000 m less than a 1 km south of the Azuero Peninsula. The
Gulf of Chiriqu? is shielded from the trade winds out of the North by the Central
Cordillera and therefore experiences no seasonal upwelling. The Gulf of Chiriqu?
contains some of the most developed coral reefs on the continental shelf in the
eastern Pacific. These are predominantly formed of a loose Pocillopora spp.
framework (Fig. 4.2) that originated in the Holocene (Glynn 1976; Cort?s 1993).
4.2 Research
The first records of the echinoderm fauna of Panama date back to the late 19th and
early 20th century and are the result of the expeditions of the U.S. Fish Commission
Steamer Albatross. Addison Emery Verrill (Fig. 4.3a) wrote the first paper in 1867
that included echinoderms from Panama. It contained descriptions of many new
genera and species. In 1891 Alexander Agassiz (Fig. 4.3b), onboard the Albatross
collected specimens from the intermediate depths of the eastern Pacific and the
Caribbean Sea to study the relationship between forms of marine life on either side
Fig. 4.2 Pocillopora spp. framework on Uva Reef, Gulf of Chiriqu?, 2010
110 S. E. Coppard and J. J. Alvarado
of the Isthmus of Panama. The collections from this expedition were used by many
authors to describe new echinoderm species (e.g. Agassiz 1892, 1898, 1904;
Ludwig 1894, 1905; L?tken and Mortensen 1899, (Fig. 4.3c, d), Clark 1917).
In the 1930?s and 1940?s expeditions to the eastern Pacific were undertaken by
the New York Zoological Society onboard the Arcturus 1925 and Zaca
1937?1938, and by the Allan Hancock Foundation onboard the Velero III
1937?1941. As a result of these expeditions, a significant amount of echinoderm
research was published (e.g. Clark 1939; Clark 1940, 1948; Ziesenhenne 1940,
Fig. 4.3 a Addison Emery Verrill, b Alexander Agassiz, c Christian Frederik L?tken,
d Theodore Mortensen (photos courtesy of the Smithsonian National Museum of Natural History)
4 Echinoderm Diversity in Panama 111
1942, 1955; Deichmann 1941, 1958). In 1915 Mortensen spent several months
collecting echinoderms and other invertebrates in the Gulf of Panama, including
from St. Elmo in the Pearl Islands Archipelago and the islands of Taboga and
Taboguilla in Panama Bay. His findings were later included in a broader work on
larval development (Mortensen 1921) and as part of his monumental monograph
on echinoids (Mortensen 1928, 1935, 1940, 1943a, b, 1948a, b, 1950, 1951). Other
researchers in the 1920?s, 30?s and 40?s made collection trips to specific regions in
Panama (e.g. Boone 1928, Clark 1946) focusing more on specific taxa. In later
years echinoderms were collected from the Caribbean Sea off Panama as part of
general benthic sampling expeditions undertaken by the RV Oregon in 1962, the
RV Pelican in 1963, the RV Oregon II in 1970, the RV Pillsbury in 1971 and the
RV Alpha Helix in 1977.
The Smithsonian Tropical Research Institute (STRI) established its first field
station on Barro Colorado Island in the Panama Canal Zone in 1923. The marine
program at STRI began fifty-one years ago, in 1961. Today STRI runs two field
stations on the Caribbean Coast (Galeta Marine Laboratory in Col?n and Bocas del
Toro Research Station) and two in the Pacific (Naos Island Laboratories complex and
a Field Station on Rancher?a Island, Coibita). The first research vessel was acquired
by STRI in 1970, the 65-ft RV Tethys (1970?1972), followed by the 45-foot RV
Stenella in 1972 (1972?1978) and the 63-foot RV Benjamin in 1978 (1978?1994).
These research vessels allowed STRI scientists to collect and document the shallow
water echinoderm fauna. In 1994 STRI purchased the 96-foot RV Urraca
(1994?2008) that had an A-frame and oceanographic winch which finally provided
the means to trawl and dredge to depths of 250 m. In 1995 the submersible DSRV
Johnson Sea Link was used to collected samples from the Gulf of Chiriqu? at depths
over 1,000 m, providing a further insight into the deep water species present off
Panama?s Pacific coast. STRI researchers who worked on echinoderms in the 70?s
and 80?s included Peter Glynn, Gordon Hendler and Harilaos Lessios. For just
over 30 years Lessios has worked at STRI on the life histories and evolution of
echinoderms in Panama. His research has focused primarily on echinoids, including
work on speciation, molecular biogeography and the evolution of reproductive
isolation. Lessios (2005a) published a review of the echinoids of the Pacific waters of
Panama, providing information on the species and new records of their distributions.
4.3 Ecology
Ecological research in Panama has included work on all classes of echinoderms,
but with fewer studies on crinoids. Eleven species of echinoderms were recorded
in the seagrass meadows of Thalassia testudinum Banks and Sol. ex K.D. Koenig
(1805) in the Canal Zone off the Caribbean coast of Panama (Heck 1977). Species
richness of echinoderms correlated with proximity to well developed reefs and was
found to be stable throughout the study period (July 1974 to May 1975), without
any major decrease in population numbers during periods of reduced salinity.
112 S. E. Coppard and J. J. Alvarado
Mortality of sea urchins on the fringing reef-flat off Galeta Island has been
reported to occur twice yearly as the result of physical stress generated by
extended aerial exposure of the reef platform (Glynn 1968; Hendler 1977; Cubit
et al. 1986). Tripneustes ventricosus (Lamarck, 1816), Lytechinus variegatus
(Lamarck, 1816) and Diadema antillarum Philippi, 1845 were found to be less
tolerant to high temperature than either Echinometra lucunter (Linnaeus, 1758)
(Fig. 4.4a) or Echinometra viridis Agassiz, 1863 (Fig. 4.4b), and are therefore
more likely to die during the periods of exposure.
In the Caribbean D. antillarum has been shown to be the dominant herbivore on
coral reefs that have been subjected to heavy human fishing pressure, while
herbivorous fishes dominate in more pristine conditions where urchin populations
are kept in check by fish predators (Hay et al. 1983; Harborne et al. 2009). Off
Galeta Island, where human fishing pressure is reported to be low (Hay 1984),
almost all grazing on bioassays of T. testudinum was attributed to herbivorous
fishes (Hay 1984). Off the San Blas Islands of Panama, the grazing activity of
D. antillarum has been shown to be the primary determinant of fleshy algal
biomass on shallow reefs (\3 m) (Foster 1987a). At the time of Foster?s study
(pre-mass mortality of D. antillarum, see Sect. 4.6) this was particularly true in the
back reef environment, where D. antillarum occurred at densities three times
higher (*6 ind m-2) than in Elkhorn coral habitats (\2 ind m-2) (Foster 1987a).
Chemical defence by coral reef macroalgae has been shown to have an import role
in deterring grazers (Hay et al. 1987). Extracted terpenoid compounds (naturally
occurring in macroalgal species of Dictyota, Dilophus, Laurencia and Stypopodium)
were applied to assays of T. testudinum and shown to deter grazing by herbivorous
fishes and D. antillarum at Galeta (Hay et al. 1987). However, Cymopol, a terpenoid
bromohydroquinone from the green alga Cymopolia barbata (Linnaeus) Lamouroux,
1816, significantly reduced feeding by reeffishes but significantly stimulated feeding
in D. antillarum.
The ability of the damselfish Stegastes dorsopunicans (Poey, 1868) to exclude
and therefore reduce the grazing impacts of D. antillarum from their territories was
studied by Foster (1987b) in San Blas. Despite the major negative impact of
Fig. 4.4 a Echinometra lucunter, b Echinometra viridis at Galeta Point Panama
4 Echinoderm Diversity in Panama 113
D. antillarum on the algal biomass in damselfish territories, this damselfish species
was found to rarely defend its feeding areas against D. antillarum and therefore
had little effect on its distribution.
On the Pacific coast of Panama grazing by D. mexicanum results in the
bioerosion of the predominantly Pocillopora spp. coral reefs (Glynn 1988).
This species contributes 78 % of the overall bioerosion 13 kg m-2 y-1 produced
by benthic eroders (Glynn 1988; Eakin 1991). Analysis of faecal pellets has
revealed that the diet of D. mexicanum consists of 75.2 ? 11.03 % coral and
only 23.0 ? 11.4 % of crustose coralline algae (CCA). In contrast the diet of
Toxopneustes roseus (A. Agassiz, 1863) is composed of approximately 20 %
coral and 80 % of CCA (Glynn 1988). This highlights the potential damage
D. mexicanum poses to reef structures, particularly when present in large numbers.
Such a threat was realised following the 1982?83 El Ni?o Southern Oscillation
event (ENSO). This resulted in mass coral bleaching and a 50 % reduction of live
coral cover on Uva Reef (Glynn 1985a), which was followed by a dramatic
increase in the population size of D. mexicanum from 2?5 ind m-2 pre 1983 to
60?100 ind m-2 post 1982-83 ENSO (Glynn 1988, 1990; Eakin 1991, 1992). Such
large numbers of D. mexicanum resulted in high rates of reef framework erosion,
shifting the reef environment into a state of near accretionary stasis (Eakin 1992;
Glynn 1997). Low predation pressure (with the removal of potentially important
fish predators as a result of over-fishing), increased habitat availability, and the
increased abundance of benthic algae as a result of the newly dead coral sub-
stratum allowed D. mexicanum to attain high population densities (Glynn 1988).
However, such a large population of D. mexicanum could not be sustained and
in the year 2000 the population of D. mexicanum dropped to near 1974 levels
([10 ind m-2) (Eakin 2001).
The ability of damselfish in the eastern Pacific to exclude Diadema from their
territories appears to be a very different situation to that reported in the Caribbean.
The territorial action of Stegastes acapulcoensis (Fowler, 1944) on Uva Reef
results in few sea urchins being present in their territories (Glynn 1990), with
consequently lower levels of erosion (6.3 mm y-1) than elsewhere on the reef
(21.8 mm y-1) (Eakin 1992).
Ecological studies on irregular echinoids in Panama have focused on sand
dollars. Seilacher (1979) studied the distribution of Mellita quinquiesperforata
(Leske, 1778) (as Mellita lata Clark, 1940), a subjective junior synonym of M.
quinquiesperforata) at Maria Chiquita on the Caribbean coast of Panama. This
species lives partially buried in the sand (with some of the apical surface exposed)
and is restricted to a 4 m wide region of the surf-zone that runs parallel to the
beach (Seilacher 1979). This species was observed feeding along this zone, but
migrated to deeper water when the intensity of the wave action increased.
The behavioural ecology of a population of Mellitella stokesii (L. Agassiz,
1841) (as Encope stokesi L. Agassiz, 1841 [sic]) was studied over a year at Venado
Beach, on the eastern Pacific coast of Panama by Dexter (1977). Densities of this
species were reported to vary from a low of 19 ind m-2 in the rainy season to a
114 S. E. Coppard and J. J. Alvarado
high of 65 ind m-2 in the dry season, with numbers concentrated in the mid-
intertidal zone where the median sediment grain size was between 170 and
200 lm. No sand dollars were found in the muddy sand bar which had a high silt
and clay fraction. Migrations towards the substrate surface were observed at low
tide which correlated with the appearance of an organic film on the substrate,
composed of a combination of diatoms and fine detrital material. Observations by
one of the authors (SEC) at Venado Beach (see Fig. 4.5a, b) agree with Dexter?s
findings. During high tide this species typically remains buried in the substrate,
perhaps to avoid predation, and only migrates to the surface at low tide, where it
moves through the upper sediment layer in the shallow tide pools ingesting small
particulate mater (Fig. 4.3b). Water temperatures in these pools regularly gets in
excess of 40 C (Coppard unpublished data), demonstrating that M. stokesii has
a tolerance for high water temperatures. Dexter (1977) reports that this species has
a high growth rate, in conjunction with a small maximum size (she recorded a
maximum horizontal diameter of 57 mm) and a short life expectancy of typically
Fig. 4.5 Mellitella stokesii
at Venado beach, a aboral
view, b feeding during low
tide
4 Echinoderm Diversity in Panama 115
less than 1 year. Recruitment of the population was reported to occur throughout
the year, but with a peak in settlement during February, in the middle of the
Panamanian dry season. This is the season of increased food availability for
planktotrophic larvae, due to the upwelling of nutrients and subsequent increase in
phytoplankton (Martin et al. 1970).
Two species of pinnotherid crab (pea crab), Dissodactylus nitidis Smith, 1870
and Dissodactylus xantusi Glassell, 1936 were found associated with M. stokesii
(Dexter 1977). These species remove the spines near the lunules or marginal slits
on the oral surface, creating a wound in which they live (see Fig. 4.6a, b). Dexter
questioned whether this relationship is really commensal, as she found that these
crabs in aquaria removed larger numbers of spines on the oral surface, which
decreased the ability of the sand dollar to feed and move, ultimately resulting in
the death of the host.
Fig. 4.6 Mellitella stokesii
(oral views) on Venado beach
with Dissodactylus spp.,
a multiple wounds, b a single
wound
116 S. E. Coppard and J. J. Alvarado
Telford (1982) described the feeding habits of four species of Dissodactylus and
found that all of them feed extensively upon their sand dollar hosts, with
50?100 % of their food intake coming from their host?s tissues. This is supported
by the fact that some M. stokesii often have multiple wounds with only a single
crab present (Fig. 4.6a).
Ecological work on ophiuroids in Panama is primarily the result of research by
Gordon Hendler. Hendler and Meyer (1982) reported the presence of the poly-
chaete Branchiosyllis exilis (Gravier, 1900) associated with Ophiocoma echinata
(Lamarck, 1816) on the Caribbean coast of Panama. This association has only been
reported from Panama, despite the fact that both species? distributions are over-
lapping and widespread. The polychaete displays active recognition of its host and
seeks out O. echinata in preference to other species of the same genus. They
consistently found one polychaete per host, indicating that B. exilis is aggressive to
member of its own species, and concluded that B. exilis is parasitic on O. echinata.
An interesting association between juvenile and adult Ophiocoma aethiops
L?tken, 1859, from Punta Paitilla in Panama was documented by Hendler et al.
(1999). Juveniles were found in the bursae (respiratory structures that in brooding
and viviparous ophiuroids also serve as brood chambers) of adults that live
intertidally at Punta Paitilla but not those that live subtidally at Isla Taboguilla.
They proposed this association helped protect juveniles against desiccation and
predators. No similar association was found in other species of Ophiocoma form
either the Pacific (O. alexandri Lyman, 1860) or from the Caribbean (O. echinata,
O. wendtii M?ller and Troschel, 1842) of Panama.
Much of the ecological work on starfish in Panama has focused on Acanthaster
planci (Linnaeus, 1758) (e.g. Glynn 1973, 1974, 1976, 1977, 1981? 1985a,b,
1990). Glynn (1973) assessed the possible effect of A. planci on the coral species
on Uva Reef in the Gulf of Chiriqu?. He reported an average density of 25?36 ind
ha-1, with a disc diameter of 17?19 cm and a size frequency that had a unimodal
distribution. Population densities of A. planci remained fairly stable on Uva Reef
from 1970 to 1980, ranging from 7 to 30 ind ha-1 (Glynn 1981). At that time these
densities were comparable to population sizes in the Indo-Pacific that were not
considered to have a serious impact on coral communities (Glynn 1974). However,
prey preference data (Glynn 1974) indicate that A. planci selectively eats rarer
non-branching corals (e.g. species of Pavona, Gardineroseris, Porites, Millepora,
Fig. 4.7), which are replaced by faster-growing species (e.g. Pocillopora spp.),
resulting in A. planci having a negative effect on species diversity (Glynn 1976).
Such a preference can partly be explained by the presence of crustacean symbionts
(Trapezia sp. and Alpheus sp.) in large branching pocilloporid colonies which
repulse A. planci by nipping at its vulnerable oral surface (particularly the sensory
tube feet) as it attempts to mount the coral to feed (Glynn 1976).
Between 1982 and 1983 a strong El Ni?o-Southern Oscillation had a dramatic
impact on the coral reefs of the Eastern Tropical Pacific, causing a die off of
between 70?95 % of coral on Pacific Panamanian reefs (Glynn 1985a, b). How-
ever, population densities of A. planci before and after the 1983 event were not
statistically different (Glynn 1990), with A. planci continuing to feed on the
4 Echinoderm Diversity in Panama 117
dispersed, surviving coral. As the reefs recovered the relative effect of predation by
A. planci intensified due to the loss of the crustacean guards (Trapezia and
Alpheus), therefore reducing local coral species diversity (Glynn 1985b).
Fong and Glynn (1998) modelled the impacts of predation by A. planci and that
of the El Ni?o-Southern Oscillation (ENSO) on the structure of a population of the
massive coral Gardineroseris planulata (Dana, 1846) on Uva Reef. The results of
the simulations suggested that predation was far more important than the ENSO in
controlling the size structure of the coral G. planulata in the eastern Pacific.
Although A. planci has few predators, it has been observed in Panama being
attacked by the Harlequin shrimp Hymenocera picta Dana, 1852 and by the
polychaete Pherecardia striata (Kingberg, 1857) (Glynn 1981). The shrimp
attacks the aboral surface of the starfish, eventually amputating the arms and using
its chelae to expose and feed on the internal soft parts. However, the harlequin
shrimp typically prefers other starfish species such as Phataria unifacialis (Gray,
1840), Pharia piramidatus (Gray, 1840) and Nidorellia armata (Gray, 1840)
(Glynn 1977). The wounds created by the harlequin shrimp are used also by the
polychaete P. striata to enter A. planci and feed on the internal tissues. Glynn
(1981) calculated that 5?6 % of the A. planci population is under attack by
H. picta and about half of these starfish are killed over a 3-week period.
Guzman and Guevara (2002a) studied the spatial distribution, abundance, and
size structure of Oreaster reticulatus (Linnaeus, 1758) (Fig. 4.8) in the Bocas del
Toro Archipelago. They found a mean density of 149.7 ind ha-1 and estimated the
population size to be over seven million. Approximately 45 % of the population
was found at a density of 308.3 ? 50.9 ind ha-1, in areas dominated by the
Fig. 4.7 Acanthaster planci
feeding on Millepora
intricata Milne-Edwards and
Haime, 1860, Coiba National
Park, Gulf of Chiriqu? (photo
courtesy of Angel Chiriboga)
118 S. E. Coppard and J. J. Alvarado
seagrass T. testudinum, with a substratum that consisted of coarse, calcareous sand.
The lowest density (5.6 ind ha-1) was observed in coral reef habitats.
Feeding patterns of O. reticulatus off the San Blas Islands were studied by
Wulff (1995). She found that 61.4 % of the starfish were eating sponges; however,
this depended on their availability. Oreaster reticulatus fed upon sixteen of twenty
species that normally grow only on the reefs, but surprisingly only one of fourteen
species that live in the seagrass meadows and rubble flats surrounding the reefs.
Therefore O. reticulatus actively searches for and consumes edible sponges that
wash into the seagrass beds from reefs, or off mangrove roots (Wulff 1995, 2006).
Meyer (1973) described the feeding behaviour, microgeographic distribution,
population size, bathymetric distribution and adaptive skeletal morphology of
eight species of Caribbean crinoids from four main study areas, including San Blas
and Galeta, in Panama. Based on his findings he divided the species into two
categories: 1) those forming a filtration fan (Nemaster grandis Clark, 1909,
Tropiometra carinata (Lamarck, 1816), Comactinia echinoptera (M?ller, 1840),
Analcidometra caribbea (A. H. Clark, 1908) and Neocomatella pulchella (Pour-
tal?s, 1878)) and 2) those with a radian posture (Davidaster rubiginosus (Pourtal?s,
1869), Davidaster discoidea (Carpenter, 1888) and Ctenantedon kinziei Meyer,
1972). Species diversity and population size of shallow-water comatulids was
found to be greatest in Panama (seven species). Meyer (1973) proposed that the
diversity and abundance of comatulid crinoids can be correlated to increased
primary productivity which occurs close to continental land masses.
Ecological studies on holothuroids in Panama have been carried out by Guzman
and Guevara (2002b). They studied the population structure, distribution and
abundance of the sea cucumbers Isostichopus badionotus (Selenka, 1867),
Holothuria (Halodeima) mexicana Ludwig, 1875 and Astichopus multifidus
(Sluter, 1910) in the Bocas del Toro Archipelago. Holothuria (Halodeima)
mexicana was found to be more abundant in seagrass, I. baniodotus occurred at
higher densities in interspersed areas, while A. multifudus showed no specific
habitat preference. For the Bocas del Toro Archipelago Guzman and Guevara
Fig. 4.8 Oreaster reticulatus
in the Thalassia testudinum
seagrass bed, Bocas del Toro
(photo courtesy of Edgardo
Ochoa)
4 Echinoderm Diversity in Panama 119
(2002b) estimated populations of 7,630,164 individuals for H. (H.) mexicana,
5,536,349 for I. badionotus, and 231,074 for A. multifidus. However, the densities
of these sea cucumbers in Panama were 50 times lower than those measured at
other Caribbean sites (Guzman and Guevara 2002b).
4.3.1 Physiology
Lawrence and Glynn (1984) studied the diet of the sea urchin Eucidaris thouarsii
(Valenciennes, 1846) through the absorption of nutrients from the predation on the
coral Pocillopora damicornis (Linnaeus, 1758) in the Gulf of Panama. The
absorption efficiency was determined to be 44.7 % for carbohydrates, 85.3 % for
protein and 69.3 % for lipids. The urchin absorbs 0.402 mg carbohydrate,
2.814 mg protein and 1.108 mg lipid for each gram of P. damicornis ingested;
0.201 mg carbohydrate, 1.407 mg protein and 0.554 mg lipid per individual per
day; and absorbs 0.824 9 10-3 kcal carbohydrate, 7.950 9 10-3 kcal protein and
235 9 10-3 kcal lipid per individual per day. The authors concluded that despite
the high efficiency of digestive absorption of organic constituents of the coral
ingested, E. thouarsii needs to consume large quantities to meet its nutritional
requirements.
Work by Hendler and Byrne (1987) on Ophiocoma wendtii collected in Galeta,
Panama Caribbean, Belize and Florida, resulted in the identification and descrip-
tion of three structures in the dorsal arm plate (DAP) that comprise a photoreceptor
system. The upper surface of the DAP bears transparent microscopic structures
which are expanded peripheral trabeculae of the calcite stereom. These structure
are part of the photoreceptor system and can facilitate light transmission through
the DAP by decreasing light refraction, reflection and absorption that occur at
stereom/stroma interfaces. Bundles of nerve fibres located below the expanded
peripheral trabeculae function as primary photoreceptors. The third elements of the
system are the chromatophores that regulate the intensity of light impinging on the
sensory tissue are regulated by the diurnal activity cycle. During the day
the chromatophores cover the expanded peripheral trabeculae and thereby shade
the nerve fibres. At night they retract into inter-trabecular channels, uncovering the
expanded peripheral trabeculae and thereby exposing the nerve fibres to trans-
mitted light. Thus, the transparent stereom may play a role in photoreception, in
addition to its generally recognized skeletal function. Although ciliated cells that
may be sensory are present in the epidermis of O. wendti, they do not appear to be
photoreceptors (Hendler and Byrne 1987).
120 S. E. Coppard and J. J. Alvarado
4.3.2 Reproduction
Reproductive cycles of echinoids on both sides of the Panama Isthmus have been
studied by Lessios (1981a, 1984, 1985a, 1991). Populations of D. mexicanum and
E. vanbrunti from Punta Paitilla, Isla Urab? and Culebra Island in the seasonal
Gulf of Panama have well-defined, synchronous, reproductive cycles (Lessios
1981a). The majority of individuals reached a peak gonad size in September, with
spawning predicted to occur from September to October. This would allow the
newly metamorphosed sea urchins, rather than the larvae, to benefit from the
increased food production as a result of the dry season upwelling (Lessios 1981a).
Populations of D. antillarum and E. lucunter from Maria Chiquita and Fort
Randolph in the less seasonal Caribbean demonstrated only slight, if any syn-
chrony between individuals. However, E. viridis which is rarer at these locations
had a well defined, population wide cycle. Based on these data Lessios (1981a)
proposed that in a constant environment the intensity of selection for synchrony
between individual gametogenic cycles may be inversely proportional to popula-
tion density. Later work by Lessios (1985a) on Caribbean echinoids did not
directly support this hypothesis. However, Lessios (1985a) suggested that popu-
lation density may be one of the factors determining the degree of synchronicity.
This study (1985a) revealed that E. viridis, L. williamsi, Clypeaster rosaceus
(Linnaeus, 1758) and Leodia sexiesperforata (Leske, 1778) are reproductively
active during Panama?s rainy season from May to November, but quiescent during
the dry season (Lessios 1985a), while L. variegatus, T. ventricosus, and Clypeaster
subdepressus (Gray, 1825) have ripe gonads throughout the year. Only E. lucunter
showed non-periodic fluctuations in readiness to spawn.
Lessios (1984, 1991) also worked on lunar spawning periodicity in Panamanian
echinoids. Diadema mexicanum was found to spawn on the third quarter of the
lunar cycle, with a peak three to four days after full moon, while its allopatric
congener D. antillarum, spawned during the first lunar quarter, one to two days
after new moon. Lessios (1984) wrote that it is therefore possible that geminate
species of Diadema have acquired a prezygotic isolating mechanism while in
allopatry and therefore reproductive isolation need not be the product of natural
selection against hybridization, thus casting doubt on the speciation by rein-
forcement theory.
Lunar spawning rhythms were not found in T. ventricosus, E. viridis,
L. sexiesperforata, C. rosaceus or L. williamsi (Lessios 1991). Eucidaris tribu-
loides and D. antillarum were found to have a distinct lunar rhythm spawning at
different lunar phases, while L. variegatus has a semilunar rhythm spawning
every new and full moon (Lessios 1991). Such spawning rhythms are unlikely to
be cued by tides as the Atlantic coast experiences only small tidal ranges
(\0.5 m) where water level is determined as much by meteorological conditions
as by tides. Lunar periodicity was therefore shown to not be a lineage specific
trait inherited from a common ancestor, but has evolved independently in dif-
ferent echinoid taxa (Lessios 1991).
4 Echinoderm Diversity in Panama 121
Temporal and spatial variation in egg size of thirteen Panamanian echinoids was
studied by Lessios (1987). His results showed that mean egg size from different
females collected from the same locality on the same day were significantly different
in all species studied. However, daily (within-month) variation in egg size was only
significant in E. tribuloides, D. antillarum, and L. variegatus, while no significant
differences were found in the daily means of egg volume in D. mexicanum and E.
viridis. Monthly means of egg volume were different in L. variegatus, L. williamsi,
T. ventricosus, E. viridis, E. vanbrunti, C. rosaceus and C. subdepressus. Between-
years variation was also significant in all of these species except L. variegatus. All
Caribbean species showed a decline in egg size after September, however, this could
not be explained by any obvious environmental fluctuation. Echinometra lucunter
showed no significant variation between months of the same year but exhibited
differences between years. No significant monthly or annual variation was observed
in E. tribuloides, E. thousarii (Valenciennes, 1846), D. antillarum, D. mexicanum or
Leodia sexiesperforata. Correlations between size of eggs collected at a particular
time and the intensity of spawning by the population at that time was not significant,
suggesting that size of mature eggs is not determined by the reproductive state of the
parental population (Lessios 1987).
Lessios (1990) looked at adaptation and phylogeny as determinants of egg size
in twenty-two species of echinoids and two species of asteroids from the Carib-
bean and Pacific coasts of Panama. Lessios (1990) identified four trends: (1)
species have eggs that are significantly different from those of other congeneric
species; (2) species evolving for three million years in separate environments have
accumulated differences in their egg sizes and the direction of these differences is
not random; (3) egg size of congeneric species is similar where developmental
modes are similar (n.b. the volume of Clypeaster rosaceus eggs is eight times
greater than that of its congener C. subdepressus, an adaptation that reflects
developmental mode as the larvae of C. rosaceus are facultative planktotrophs,
while those of C. subdepressus are obligate planktotrophs); (4) there is no simi-
larity between the egg sizes of species belonging to the same family or higher
taxonomic category, even if these species inhabit the same ocean. He concluded
that because the phenomena of smaller eggs in the Pacific (a pattern attributed to
higher levels of primary productivity in the eastern Pacific) holds for lineages that
have not shared a common ancestor for a long time, it is likely that independent
adaptation by the members of each pair has occurred due to the environments of
the two oceans during the last three million years.
McAlister (2008) studied the plasticity of larval feeding arms for geminate
species pairs to determine how food availability can influence growth and the arm
length of the larvae. No plasticity in arm length was found in either Caribbean or
Pacific species, however, arm length was significantly longer in Caribbbean spe-
cies (including in D. antillarum). McAlister (2008) suggests that historical changes
in food levels led to the development of longer feeding arms in Caribbean species,
while plasticity may be limited by egg size or the timing of reproduction.
The evolution of gametic incompatibility in neotropical Echinometra was
investigated by Lessios and Cunningham (1993). They used fertilization
122 S. E. Coppard and J. J. Alvarado
experiments to determine the degree of reproductive isolation both between the
sympatric E. lucunter and E. viridis, in the Caribbean, and with the allopatric
E. vanbrunti from the eastern Pacific. They reported that, contrary to the predic-
tions of the ?speciation by reinforcement hypothesis?, the degree of incompatibility
between the allopatric E. lucunter and E. vanbrunti is higher than between the
sympatric E. lucunter and E. viridis. Crosses between E. viridis and E. vanbrunti
produced rates of fertilization almost equal to those of homogamic crosses, while
sperm of E. lucunter were found to be able to fertilize eggs of the other two
species. However, few E. lucunter eggs are fertilized by heterospecific sperm
(Lessios and Cunningham 1993). In the wild E. lucunter and E. viridis maintain
their genetic integrities despite having this unidirectional gamete isolation.
Allozyme data placed the speciation event of the sympatric species after the rise of
the isthmus. Thus there is no correlation between genetic divergence and strength
of reproductive isolation (Lessios and Cunningham 1993).
Later work by McCartney and Lessios (2002) confirmed these findings and
demonstrated a much stronger block to cross-species fertilization of E. lucunter
eggs than was previously shown. They reported that gamete incompatibility in
these species is weaker in sympatry than in allopatry, and based on the mtDNA
data in McCartney et al. (2000), such gamete incompatibility in these species arose
in the last 1.5 million years.
Zigler et al. (2008) looked at egg energetics, fertilization kinetics, and popu-
lation structure in echinoids with facultatively feeding larvae. This work included
C. rosaceus, one of only two echinoid species known to have facultatively
planktotrophic larvae. The eggs of C. rosaceus resemble those of echinoid species
with obligately feeding larvae in egg energetic density, egg buoyancy and fertil-
ization kinetics, but resemble non feeding larvae in time to metamorphosis, the
early formation of the coelom and the reduced allocation to larval feeding struc-
tures (Zigler et al. 2008).
Cross-fertilization experiments between C. rosaceus and C. subdepressus by
Zigler et al. (2008) revealed that bidirectional gametic incompatibility has evolved
between the two species. These species are commonly found together or within close
proximity to one another in the shallow waters of the Caribbean in Panama (both
species live in the sand, but C. rosaceus is typically more common in turtle grass
beds). These species have no temporal reproductive isolation, as both have ripe
gonads for much of the year, but with peaks from July to October (Lessios 1984).
The results of Zigler et al. (2008) indicate that the small eggs of C. subdepressus
are particularly resistant to fertilization by C. rosaceus sperm, while the larger
C. rosaceus eggs are slightly more vulnerable to fertilization by C. subdepressus
sperm, but at levels that are unlikely to results in conspecific fertilizations in nature.
Research on the sea urchin sperm protein bindin in sea urchin species found off
the coasts of Panama has been conducted by Zigler and Lessios (2003a, b, 2004),
McCartney and Lessios (2004), Zigler et al. (2005), and Geyer and Lessios (2009).
Bindin is a sea urchin sperm protein that mediates sperm-egg attachment and
membrane fusion. Across echinoid genera, its divergence has been shown to be
correlated with heterospecific incompatibility in fertilization (Zigler et al. 2005).
4 Echinoderm Diversity in Panama 123
In sympatric species, a region of the bindin molecule reportedly evolves at high
rates under strong positive selection (Metz and Palumbi 1996), whereas in allo-
patric species (e.g. T. ventricosus in the Caribbean and T. depressus in the eastern
Pacific), bindin variation was reported to be low, with no evidence of positive
selection. However, this does not appear to be the case for all sea urchin species.
Lytechinus williamsi and L. variegatus, which have overlapping distributions in
the Caribbean, show no clear evidence of selection (Zigler and Lessios 2004).
While in spatially overlapping E. lucunter and E. viridis, positive selection was
only found to have accumulated along the bindin lineage of E. lucunter
(McCartney and Lessios 2004). Further, Geyer and Lessios (2009) found no evi-
dence to suggest that the source of selection on bindin in E. lucunter is
reinforcement, as bindin showed no evidence of stronger selection in areas of
sympatry relative to areas of allopatry. Geyer and Lessios (2009) propose that the
evolution of this molecule is a result of the processes acting within species, such as
sexual selection and sperm competition.
The reproductive cycle of the starfish O. reticulatus in Isla Solarte, Bocas del
Toro Archipelago, was studied from February 2000 to February 2001 by Guzman
and Guevara (2002a). Males and females with ripe gonads were observed almost
every month, however, the gonad index revealed peaks in reproductive activity,
during July, November, and January. Gonad maturation was not triggered by
changes in water temperature (these ranged from 27 C to 30 C), but may have
responded to chemical cues in the water (e.g. nutrients, salinity) (Guzman and
Guevara 2002a).
Guzman et al. (2003) assessed the reproductive status of two commercial
species of sea cucumber, I. badionotus and H. (H.) mexicana in the Caribbean of
Panama. They reported that for both species the minimum reproductive length was
13?20 cm with a weight of 150 g. Both species were gonochoric with a 1:1 sex
ratio. Gametogenesis and spawning occurred throughout the year; however there
were periods of peak reproductive activity, between July and November for
I. badionotus and from February to July for H. (H.) mexicana (Guzman et al.
2003).
4.3.3 Evolution
Molecular work on echinoids in Panama started with Lessios (1979), who used
geminate species of Panama (E. tribuloides and E. thouarsii, D. antillarum and D.
mexicanum, E. viridis, E. lucunter and E. vanbrunti) to test the molecular clock
hypothesis. This hypothesis predicts that each protein changes at a constant rate, so
that the degree of divergence between two species is linearly related to the time for
which their lineages have remained separate (Wilson et al. 1977). Lessios (1979)
found that this does not hold for Panamanian echinoids, as very different rates of
divergence were found in the enzymatic proteins between geminates in the
different genera. Eucidaris and Echinometra exhibited transisthmian distances
124 S. E. Coppard and J. J. Alvarado
sixteen and thirty-seven times greater than intraspecific ones respectively, while
the trans-isthmian distance in Diadema was twenty times smaller than for the
Echinometra. Lessios (1979) proposed that the most plausible explanation was that
the molecules used in this investigation were evolving under the influence of
natural selection.
In 1981(b) Lessios combined this molecular work with morphometric data
using twenty morphological measurements. The morphometric data showed that
differentiation between members of each geminate pair are not significantly dif-
ferent from local variation within each species. However, the ratio of inter to
intraspecific Mahalanobis distance was congruent with the molecular data, being
lowest in Diadema, intermediate in Eucidaris, and highest in Echinometra.
Morphological rates of divergence were found to be more rapid in sympatric
species, possibly due to habitat separation between congeners (Lessios 1981b).
Bermingham and Lessios (1993) used mitochondrial DNA (mtDNA) and
isozymes in these sea urchin species to measure the degree of divergence. Trans-
isthmian isozyme divergence in the geminate pairs differed by an order of mag-
nitute, while mtDNA divergence was equivalent in all pairs demonstrating that
mtDNA can provide accurate estimates of time since separation (Bermingham and
Lessios 1993).
After the mass mortality of D. antillarum in the Caribbean (see Sect. 4.6.
Threats to echinoderms), Lessios (1985b) looked at the genetic consequences of
the restriction in the genetic structure of populations. His results showed no loss of
genetic variability to that recorded in the same populations of D. antillarum in
1977. Lessios suggested that organisms with planktonic larvae are likely to recover
from local extinction events without significant losses of their genetic variability,
as larval exchange allows re-seeding of affected areas by recruits not exposed to
the bottleneck.
A phylogenetic survey of sea urchin retroviral-like (SURL) retrotransposable
elements in 33 species of echinoid (regular sea urchins, sand dollars, and heart
urchins) was conducted by Gonzalez and Lessios (1999). High ratios of synony-
mous to nonsynonymous substitutions suggest that the reverse transcriptase of the
elements is under strong purifying selection (Gonzalez and Lessios 1999). They
report that despite the predominance of vertical transmission, sequence similarity
of 83?94 % for SURL elements from hosts that have been separated for 200 Myr
suggests four cases of apparent horizontal transfer between the ancestors of the
extant echinoid species. In three additional cases, elements with identical RT
sequences were found in sea urchin species separated for a minimum of 3 Myr.
Thus, horizontal transfer plays a role in the evolution of this retrotransposon
family (Gonzalez and Lessios 1999).
Cytochrome oxidase I (COI) divergence was assessed in Atlantic and eastern
Pacific Echinometra by McCartney et al. (2000), using the closure of the Isthmus
of Panama to date cladogenic events. They reported that the Atlantic species
E. lucunter and E. viridis diverged 1.27?1.62 mya at a time in the Pleistocene
when sea levels fell and Caribbean coral speciation and extinction rates were high.
The fact that these species split so recently, yet do not hybridize, demonstrates that
4 Echinoderm Diversity in Panama 125
reproductive barriers between marine species can occur in less than 1.6 million
years (McCartney et al. 2000).
A global molecular phylogeny of Diadema (including D. antillarum and
D. mexicanum from Panama) was published by Lessios (2001) and Lessios et al.
(2001). This molecular study showed that Diadema is composed of reciprocally
monophyletic mtDNA clades, and that the eastern Atlantic D. antillarum
(D. antillarum-b) from Madeira, Canary Islands, Cape Verde and Sao Tome is
genetically distinct from the western Atlantic D. antillarum. These species are
separated by the long stretch of deep water separating the eastern from the western
Atlantic. Diadema antillarum ascensionis Mortensen, 1909 from the central
Atlantic islands of Ascension and St. Helena was found to be genetically isolated,
but nested within the Brazilian clade of the western Atlantic D. antillarum. Lessios
suggests that the biogeographic barrier between the Caribbean and Brazil may be
caused by the outflow from the Amazon and Orinoco Rivers. High levels of gene
flow were reported among populations of D. mexicanum in the eastern Pacific,
with D. mexicanum from the Galapagos and Cocos Island belonging to the same
population as sea urchins from Panama and Mexico (Lessios et al. 2001).
A study of the phylogeography of the pantropical sea urchin Tripneustes by
Lessios et al. (2003) showed that based on morphology, COI, and bindin data,
T. depressus A. Agassiz, 1863 from the eastern Pacific is in fact the same species
as T. gratilla (Linnaeus, 1758) from the western Pacific. The formation of the
Isthmus of Panama, the deep water separating the eastern and western Atlantic,
and the freshwater plume of the Orinoco and Amazon rivers between the
Carribbean and the coast of Brazil were shown to be important barriers to the
evolution of Tripneustes. However, the Eastern Pacific Barrier (5,000 km of deep
water) between the central and eastern Pacific was unimportant in the subdivision
in the genus.
A phylogeographic study of the genus Lytechinus by Zigler and Lessios (2004)
using mitochondrial COI, and the entire molecule of nuclear bindin shows that the
genus Lytechinus is paraphyletic (using Toxopneustes and Tripneustes as out-
groups), with Sphaerechinus granularis (Lamarck, 1816) coming out as the sister
species to L. euerces Clark, 1912 . The authors propose that L. euerces should be
moved into the monotypic Sphaerechinus, rather than placing Sphaerechinus in
Lytechinus which would increase the range of the genus to the temperate eastern
Atlantic and Mediterranean (Mortensen 1943a). Lytechinus semituberculatus
(Valenciennes in L. Agassiz, 1846) and L. panamensis formed a clade with no
distinction between the two species, while L. anamesus and L. pictus were also
phylogenetically indistinguishable. A well supported Atlantic clade was formed of
L. williamsi and the three subspecies of L. variegatus (L. variegatus variegatus,
L. variegatus atlanticus, L. variegatus carolinus). Lytechinus williamsi from the
Caribbean was found to share mtDNA haplotypes with L. variegatus variegatus,
however, their bindin was shown to be distinct and to coalesce within each
morphospecies. A small private clade of mtDNA was found in some L. williamsi
from Panama and Belize. Zigler and Lessios (2004) suggest that this may be
126 S. E. Coppard and J. J. Alvarado
indicative of former differentiation in the process of being swamped by intro-
gression, or of recent speciation.
Molecular work on the starfish A. planci, including specimens from Panama,
revealed that it is not in fact a single species, but a pan-Indo-Pacific species
complex consisting of four deeply diverged clades (Pacific, Red Sea, Northern
Indian Ocean, and Southern Indian Ocean) (Vogler et al. 2008). These clades
reportedly diverged between 1.95 and 3.65 mya (Pliocene to early Pleistocene)
and have genetic distances (8.8?10.6 %) equivalent to the distances between other
sibling species of starfish (Waters et al. 2004). Vogler et al. (2008) propose that
this speciation process was driven by sea level changes (Pillans et al. 1998) that
isolated populations.
Zulliger and Lessios (2010) published a global phylogeny of the genus
Astropecten based on 117 specimens belonging to 40 species. This genus is one of
the most species-rich genera among starfish containing over 150 described species
with six species recorded from Panama: A. armatus Gray, 1840, A. articulatus (Say,
1825), A. cingulatus Sladen, 1883, A. exiguus Ludwig, 1905, A. fragilis Verrill,
1870 and A. regalis Gray, 1840. Such diversity is remarkable, because most species
of Astropecten have a long-lived planktotrophic larval stage. Consequently one
would expect this to lead to a low speciation rate (Zulliger and Lessios 2010).
Zulliger and Lessios (2010) compared their molecular phylogeny to D?derlein?s
(1917) morphological phylogeny. They found high levels of congruence on the
whole, but many discrepancies on a local scale. Phylogentic inference from their
data reveals that that morphological and ecological convergence has taken place in
Astropecten, resulting in allopatric non-sister taxa with similar morphologies and
habitat preferences. Varieties of several species were also shown to exhibit genetic
distances large enough to justify recognizing them as separate species.
Reviews on speciation in organisms separated by the Isthmus of Panama have
been written by Lessios (1998, 2008). Lessios (1998) wrote a chapter in ??Endless
Forms: Species and Speciation?? on the first stage of speciation as seen in organ-
isms separated by the Isthmus of Panama. Lessios points out that although gem-
inate species have had a long history of contributing evidence relevant to
speciation, they remain an underutilised tool for understanding vicariant specia-
tion. Lessios?s (2008) review showed that a total of 38 regions of DNA have been
sequenced in nine clades of echinoids, 38 clades of crustaceans, 42 clades of fishes,
and 26 clades of molluscs with amphi-isthmian subclades. Of these, 34 clades are
likely to have been separated at the final stages of Isthmus completion, 73 clades
split earlier and eight clades maintained post-closure genetic contact (e.g. via a
circumglobal route or through the Panama Canal). As no vicariant event is better
dated than that of the Isthmus of Panama, molecular divergence between species
pairs remains to be of great interest, particularly as adaptive divergence can be
seen in species life history parameters.
4 Echinoderm Diversity in Panama 127
4.4 Diversity and Distribution of Echinoderms
Chesher (1972) published a list of Pacific and Caribbean echinoids and identified
potential geminate species pairs. Maluf (1988) synthesised and tabulated the
composition and distribution of central eastern Pacific echinoderms from the
literature, which has proved to be a valuable resource for researchers. Lessios
(2005a) updated the records of echinoids found in the Pacific waters of Panama,
and distinguished species that have been documented for Panama from those that
have collection records that straddle Panama, but with no published records of
actual presence in Panama. In the latter category Lessios (2005a) lists Kamptosoma
asterias (Agassiz, 1881), Plesiodiadema horridum (Agassiz, 1898), Cystocrepis
setigera (Agassiz, 1898), Pourtalesia tanneri Agassiz, 1898, Homolampas fulva
Agassiz, 1879, Echinometra oblonga (Blainville, 1825) and Encope perspectiva
Agassiz, 1841. The inclusion of E. perspectiva in this category is a mistake as it
was collected in Panama from Playa Grande, on San Jose Island, Pearl Islands
Archipelago by Clark (1946) and more recently by Coppard (2010) from the same
location. Plesiodiadema horridum is listed in the Smithsonian, National Museum of
Natural History collections as collected off Panama (USNM 21050). However, the
coordinates of the collection site (309.000N, 8208.000W) indicate that it was
collected off Colombia. Lessios (2005a) gives details of why the subtropical
Centrostephanus coronatus (Verrill, 1867) and central and western Pacific species
E. oblonga are unlikely to occur in Panama, and that the record of Caenocentrotus
gibbosus (Agassiz, in Agassiz and Desor, 1846) in Panama is a mistake in the
literature.
Alvarado et al. (2008) assessed the diversity of echinoderms in the Caribbean of
Central America and gave faunal lists for each country. Panama had the greatest
species richness, with 154 species listed, comprised of 15 species of crinoids, 23
species of asteroids, 56 species of ophiuroids, 30 species of echinoids and 30
species of holothuroids. Among the crinoids they included both Davidaster
insolitus Clark 1917 and Davidaster discoideus (Carpenter, 1888). The number of
species of crinoids should be reduced to 14 because D. insolitus is currently
considered a junior synonym of D. discoideus (Messing 2010). Among the
asteroids, two species are missing from their list for Panama. These are Echinaster
(Othilia) echinophorus (Lamarck, 1816) collected from Limon Bay (Smithsonian
National Museum of Natural History, USNM 38235) and Fort Randolph (USNM E
26417, USNM E 26418), and Persephonaster patagiatus (Sladen, 1889) collected
from the Gulf of Mosquitos (USNM E 31501). The number of ophiuroid species is
incorrect as Amphiodia riisei (L?tken, 1869) [sic] is a junior synonym of
Ophiophragmus riisei (L?tken in: Lyman 1860) (St?hr 2010). Among the holo-
thuroids they list Thyone deichmannae Madsen, 1941 and Thyone inermis Heller,
1868 which are junior synonyms of Havelockia inermis (Heller, 1868) (Hansson
2011). Although Alvarado et al. (2008) state that there are 30 echinoid species
recorded from off the Caribbean coast of Panama they only list 29 species which
agrees with more recent work by Coppard (2010).
128 S. E. Coppard and J. J. Alvarado
Alvarado et al. (2010) documented the echinoderm diversity in the Pacific coast
of Central America, again providing faunal lists for each country. Although
Alvarado et al. (2010) included the paper by Lessios (2005a) in their bibliography
they unfortunately ignored Lessios?s comments and tables. These indicate echinoid
species that have distributions in the eastern Pacific that straddle Panama (but have
not been recorded from Panama), those unlikely to occur in Panama, and errors in
the literature. Alvarado et al. (2010) also incorrectly listed Encope grandis
Agassiz, 1841 in Guatemala, El Salvador, Honduras, Nicaragua and Panama. This
species is endemic to the Gulf of Mexico; Encope michelini Agassiz, 1841 in
Costa Rica (this is an Atlantic species that occurs off Florida), Dendraster
excentricus (Eschscholtz, 1829) in Panama (this temperate species has a distri-
bution range from Alaska to Baja California), as well as including many junior and
senior synonyms as separate taxa (e.g. Ophionereis annulata (Le Conte, 1851) and
Ophionereis dictyota Ziesenhenne 1940; Sclerasterias alexandri (Ludwig 1905)
and Hydrasterias diomediae Ludwig 1905; Lissothuria ornata Verrill 1867 and
Thyonepsolus beebei Deichmann, 1937). Alvarado et al. (2010) list 253 species of
echinoderms from Panama, the country with the highest species richness in Central
America. This is explained by the long coastline (1,690 km) of Panama which
incorporates high levels of coastal heterogeneity and reflects the greater echino-
derm research effort than in other Central America countries (Alvarado et al.
2010).
A web-based project by Coppard (2010) (??The Echinoderms of Panama??) has
documented 414 species of echinoderms that occur off the Caribbean and Pacific
coasts of Panama (Table 4.1 and Appendix). This work was carried out in con-
junction with the Encyclopaedia of Life and contains images (including type
material), diagnostic descriptions and references with links to nomenclators,
GenBank, Barcode of Life, and depth, distribution and specimen data. All species
names were checked with the World Register of Marine Species and lists of junior
synonyms are given. Where physical specimens were not found in museum col-
lections, records from the literature were used.
Since the final closure of the Panama Isthmus unequal rates of speciation,
extinction and migration have occurred in the Caribbean and Pacific, resulting in
very different levels of biodiversity seen on either side of the isthmus today
(Vermeij 1978; Jackson et al. 1996; Budd 2000). Among invertebrates, greater
levels of diversity have been reported in the Caribbean than in the Pacific for
Table 4.1 Number of echinoderm species recorded from Panamanian waters
Pacific Caribbean Both pacific and caribbean Total
Crinoidea 7 14 0 21
Ophiuroidea 75 51 4 130
Asteroidea 56 25 2 83
Echinoidea 49 27 2 78
Holothuroidea 73 27 2 102
Total 260 144 10 414
4 Echinoderm Diversity in Panama 129
corals (Glynn 1982), sponges (Van Soest 1994), benthic foraminiferans (Collins
1999), cheilostome bryozoans (Cheetham et al. 2001) and cupuladriid bryozoans
(O?Dea et al. 2004). With the exception of crinoids, the diversity of echinoderms
off Panama shows a very different trend, with a far greater diversity in the Pacific
(270 species) than in the Caribbean (154 species). The high diversity of crinoids in
the Caribbean is most likely a consequence of greater coral reef development,
which provides a broad range of suitable habitats for species such as Nemaster
grandis (Fig. 4.9).
For the other classes of echinoderms, the greater number of species in the
Pacific of Panama can partially be explained by a number of species having
crossed the Eastern Pacific Barrier (e.g. Toxopneustes roseus, Tripneustes
depressus, Acanthaster planci) and thus have a West Pacific origin, with no sister
species in the Caribbean. However, in many genera, particularly those that contain
mud and sand dwelling species, a genus in the Caribbean often contain one or two
species, while in the Pacific the same genus will often have more than double the
number of species (e.g. in Panama the genus Luidia has three species recorded
from the Caribbean, but nine species from the eastern Pacific; Astropecten, two
species from the Caribbean, four species from the Pacific; Encope, one species
from the Caribbean, five species from the Pacific). The different hydrological
conditions in the Gulf of Chiriqu? and the Gulf of Panama have created high levels
of coastal heterogeneity providing a diverse range of habitats. However, such
morphological variation that has given rise to authors erecting many species names
in the Pacific may simply reflect ecophenotypic varriation within a species.
Sampling the sharp drop down the continental slope to a depth over 1,000 m
just south of the Azuero Peninsula has resulted in a number of deep water species
being recorded from the Pacific of Panama, such as sea lilies (e.g. Calamocrinus
diomedae Agassiz, 1890, depth 1,430 m), brittle stars (e.g. Astrodia plana (L?tken
and Mortensen 1899), depth 3,058 m; Asteronyx loveni M?ller and Troschel, 1842,
Fig. 4.9 Nemaster grandis
with arms spread for feeding,
Bocas del Toro, Caribbean
Sea (photo courtesy of
Edgardo Ochoa)
130 S. E. Coppard and J. J. Alvarado
depth 1,866 m, Fig. 4.10), starfish (e.g. Dytaster gilberti Fisher, 1905, depth
2,690 m; Pectinaster agassizi Ludwig 1905, depth 2,323 m), sea urchins (e.g.
Salenocidaris miliaris (Agassiz 1898), depth 3,058 m; Caenopedina diomedeae
Mortensen, 1939, depth 850 m; Araeosoma leptaleum Agassiz and Clark, 1909,
1,062 m) and sea cucumbers (e.g. Molpadia spinosa (Ludwig, 1893), depth
3,279 m; Protankyra brychia (Verrill, 1885), depth 4,000 m).
Ten species have collection records from both sides of the Panama Isthmus.
These are the ophiuroid species Hemipholis elongata (Say, 1825), Ophiactis
savignyi (M?ller and Troschel, 1842), Ophioderma panamensis L?tken, 1859 and
Amphipholis squamata (Delle Chiaje, 1828); the asteroid species Linckia guil-
dingii Gray, 1840, Ctenodiscus crispatus (Retzius, 1805); the echinoid species
Moira atropos (Lamarck, 1816) (the subspecies Moira atropos clotho Michelin,
1855 is recorded from the Pacific), Meoma ventricosa (Lamarck, 1816) (the
subspecies Meoma ventricosa grandis Gray, 1851 is recorded from the Pacific);
and the holothuroids Holothuria (Thymiosycia) arenicola Semper, 1868 and
Holothuria (Thymiosycia) impatiens (Forsk?l, 1775). With the final closure of the
isthmus (2.8 mya) there has been no gene flow between populations in the Pacific
and Caribbean. However, the opening of the freshwater Panama Canal in 1914
provided a means for echinoderms to cross the isthmus, either as larvae in the
ballast tanks of ships or associated with fouling organisms on the hulls of ships.
Roy and Sponer (2002) found identical mtDNA haplotypes of Ophiactis savignyi
in the Caribbean and Pacific. This led them to suggest that these sponge-dwelling
brittle stars have been recently transported between oceans on the hulls of ships.
Global phylogenies have also shown that genes of certain species have travelled
around the world during the last 3 million years providing a connection between
tropical species on the two sides of tropical America (Bowen et al. 2001, 2006;
Lessios et al. 2001; Rocha et al. 2005).
Fig. 4.10 Deep water ophiuroids, a Astrodia plana and b Asteronyx loveni
4 Echinoderm Diversity in Panama 131
Some echinoderm species have records in Panama that may represent transient
populations. Arbacia spatuligera (Valenciennes, 1846) is recorded (specimen not
examined) from the reef off French Fort (USNM 1017377), in Panama Bay. This
may be a misidentification or represent a transient population of this species, with
larvae carried up from Ecuador into the Gulf of Panama but with insufficient
recruitment to establish a viable population. This species has therefore not been
included in the Pacific data for Panama, since to the best of our knowledge it is the
only record of this species in Panama. Records of Lytechinus pictus in Panama are
probably erroneous. Mortensen (1921) described L. panamensis based on speci-
mens he obtained from Taboga Island. Clark (1948) collected one specimen from
Bahia Honda as well as one specimen from Gorgona Island, Colombia. However,
Clark (1948) states that these may be specimens of L. panamensis, a view sup-
ported by Zigler and Lessios (2004) and Lessios (2005a). Lessios (2005a) reports
that he has only seen two specimens of this species collected off Isla Saboga in the
Perlas Archipelago (8380N, 79030W). Clark (1925) and Mortensen (1928?1951)
speculated that Lytechinus from Peru and Ecuador may not be L. semituberculatus
but L. panamensis, with the larvae of this species occasionally settling in the Gulf
of Panama.
Panama is the type locality of 82 species of echinoderms (nine Caribbean, 73
eastern Pacific, one of these species occurs in both the Caribbean and Pacific).
However, four of these species (starfish) are now considered subjective junior
synonyms of other species. The majority of the Pacific species were established
from Panamanian specimens in the late 1800s and early 1900s by authors such as
L?tken and Mortensen (1899) and Ludwig (1894, 1905), as a result of the material
collected on expeditions by the Albatross. The majority of new Caribbean species
were discovered much later in the 1960s, 1970s and 1980s by authors such as
Chesher (1968, 1970, 1972) and Hendler (1995 2005), as a result of the labora-
tories of the Smithsonian Tropical Research Institute in Panama. In recognition of
this, Hendler (2005) named the ophiuroid species Ophiothrix stri Hendler 2005.
4.5 Aquaculture and Fisheries
The sustainable aquaculture of echinoderms in Panama has not been developed. In
1997 the Panamanian government granted a permit for the harvesting and
processing of b?che-de-mer (sea cucumbers) in Bocas del Toro. However, this
exploitation was short lived, with the permit being revoked 30 days later.
Nevertheless, in that short time period Guzman and Guevara (2002b) estimate that
750,000 sea cucumbers were harvested (based on 25 fishermen extracting an
average of 1,000 and a maximum of up to 1,500 cucumbers day-1). This consisted
primarily of three species Holothuria (Halodeima) mexicana, Isostichopus
badionotus and Astichopus multifidus. This quantity represents a biomass of ca.
180 tons (based on average body wet weight of 240 g). If such fishing pressure
was permitted, Guzman and Guevara (2002b) estimate that stocks of the three
132 S. E. Coppard and J. J. Alvarado
species of holothuroids would collapse within a very short period of time
(305 days for H. (H.) mexicana, 221 days I. badionotus and only 9 days for
A. multifidus), based on a catch effort of 25,000 ind day-1 (Fig. 4.11)
Commercial b?che-de-mer fishing currently is banned in all Panamanian waters
under Decree 157?2003. However, there are reports of illegal fishing activities,
with five species being commercially exploited in Panama: Actinopyga agassizi
(Selenka, 1867) H. (H.) mexicana, A. multifidus, I. badionatus (Caribbean) and
I. fuscus (eastern Pacific) (Toral-Granda 2008). In Parque Nacional Marino Isla
Bastimentos, H. (H.) mexicana showed a maximum density of 956 ind ha-1 in
480 ha representing only 10 % of the shallow water protected area, while
I. badionotus and A. multifidus were strikingly absent in 95 % of the protected
insular area around Cayos Zapatillas. This indicates that that illegal fishing has
taken place inside the park (Guzman and Guevara 2002b). Data from the statistics
department in Hong Kong, revealed that 281 kg (dry weight) of b?che-de-mer
were imported from Panama in 2004 and 408 kg (dry weight) in 2005 (Toral-
Granda 2008).
4.6 Threats to Echinoderms
Between 1983 and 1984, D. antillarum suffered one of the most extensive and
severe mass mortality events ever recorded for a marine animal. This was probably
caused by a waterborne pathogen transported by ocean currents, since plots of
surface currents in the Caribbean Sea coincided with the spread of the die-off
(Lessios 1988; Miller et al. 2003). The mass mortality of D. antillarum has been a
major factor leading to a shift from coral-dominated to algae-dominated com-
munities on many Caribbean reefs during the past 20 years (Lessios 1988). The
die-off was first observed in January 1983 at Galeta Point, near the entrance of the
Panama Canal. In approximately three months it had extended to the San Blas
Archipelago, before reaching the Panama-Colombia border by the end of June. By
Fig. 4.11 Astichopus
multifidus photographed in
Bocas del Toro (photo
courtesy of Juan Sanchez)
4 Echinoderm Diversity in Panama 133
January 1984 the die-off had spread throughout the rest of the Caribbean with
population densities in Panama reduced to 5.8 % of their previous levels (Lessios
et al. 1984a). The first symptom of the presumed disease was accumulation of
sediment on the spines and sloughing off of the spine ectoderm. This was followed
by loss of pigmentation in the skin covering the spine muscles, the peristome, and
in the periproctal cone. Spines became brittle and broke, while others fell off
completely, exposing areoles and tubercules. Tube feet became flaccid, no longer
retracted fully upon stimulation, and were unable to cling to the substrate. Many
individuals at this stage were found on their sides or being moved to and fro by the
surge. In advanced stages large patches of skin pealed off the test, the peristome
and the anal cone lost practically all pigmentation, and the spines could be pulled
off with little force (Lessios et al. 1984b).
Before the mass mortality, mean densities of D. antillarum on reefs at Punta
Galeta and San Blas where 1.82 and 1.91 ind m-2, respectively (Lessios et al.
1984b). After the mass mortality the densities dropped to an average of 0.05 ind
m-2 in San Blas, and to 0.004 ind m-2 in Punta Galeta. This density reduction was
not observed in other species of echinoids (E. lucunter, E. viridis, Echinoneus
cyclostomus (Leske, 1758), E. tribuloides, L. variegatus and T. ventricosus (La-
marck 1816)) on the same reefs. In San Blas, the mean sizes were reduced from
48.6 mm to 25.0 mm (Lessios et al. 1984b). However, this mass reduction on the
population did not have any consequence on its genetic variability (Lessios
1985b).
Five years after the event, Lessios (1988) did not observe any recovery of the
populations on the San Blas reefs, with little influx of juveniles and no increase in
population densities of other sea urchins species (E. viridis, E. lucunter, E. tribuloides,
T. ventricosus, or L. variegatus). He reported no alteration in the reproductive
behaviour of D. antillarum, proposing that the low recruitment success could be an
effect of low populations densities and low adult numbers.
Fig. 4.12 Diadema
antillarum on a reef in San
Blas, depth 2 m, June 2010
134 S. E. Coppard and J. J. Alvarado
Ten years after the mass mortality densities remained at less than 3.5 % of their
pre-mortality levels, with D. antillarum being absent in its preferred habits in San
Blas (Lessios 1995). Moreover, the mean size of individuals remained low
(17.3?35.2 mm). This was thought to be a direct result of the disease, as food
availability was not a limiting factor (Lessios 1995).
Twenty years after the mass mortality populations remained at less than 6.5 %
of their pre-mortality levels in San Blas (Lessios 2005b). Some successful
recruitment events have been observed on a few reefs. However, these have not
been sustained over time (Lessios 2005b). The lack of apparent recruitment could
have been caused by too few adults in upstream areas to reproduce at a rate that
would overcome the normal sources of mortality (the Allee effect) or by the
continuing presence of the pathogen that devastated the populations in 1983?1984.
Recent observations (2010) on some San Blas reefs indicate a slight recovery
(Fig. 4.12), however, it remains to be seen if these populations will be sustained.
On 27 April 1986 more than 8 million liters of crude oil spilled into a complex
region of mangroves, seagrassses, and coral reefs east of the Caribbean entrance to
the Panama Canal (Jackson et al. 1989). At the seaward edge, numbers of the most
abundant sea urchin E. lucunter was reduced by 80 % within a few days of the
spill, and the reef flat was littered with its skeletons (Jackson et al. 1989). How-
ever, further inshore no such mortality of E. lucunter was reported (Jackson et al.
1989).
During 2008?2009 Coppard (unpub. obs.) found large numbers of dead and
dying sand dollars of the genera Encope and Mellita washed up on beaches from
Punta Abreojos, Baja California Sur, Mexico, to Santa Elena Bay, La Libertad in
Ecuador in the eastern Pacific and off Costa Rica and Belize in the Caribbean. In
Panama dead mellitid sand dollars were found at Playa Las Lajas in the Gulf of
Chiriqui, but not on beaches in the Gulf of Panama. These dead sand dollars were
unusual in that they appeared to have an infection that originated at one or more
circular denuded regions on the aboral surface of the test (Fig. 4.13a). The cause of
such scars is most likely the result of attacks by gastropods from species such as
Fig. 4.13 Mellitid sand dollars showing varying degrees of predation and secondary infection,
a M. longifissa, collected alive (sublethal predation), b E. laevis (lethal predation, no secondary
infection), c M. kanakoffi, found dead (probable death from secondary infection due to the large
amount of necrotised tissue)
4 Echinoderm Diversity in Panama 135
Northia pristis (Deshayes in Lamarck, 1844) and Polinicies sp. in the Pacific and
Cassis tuberosa (Linneaus, 1758) in the Caribbean which have been reported to
attack, and bore into the tests of mellitid sand dollars (McClintock and Marion
1993; Sonnenholzner and Lawrence 1998). Attacks always occurred on the aboral
surface, and in the majority of cases centred over one or more petals. When the
gastropods managed to bore through the test into the coelom (Fig. 4.13b), death of
the sand dollar resulted. However, the presence of multiple scars of varying size
indicates that such attacks are not always lethal. Following such attacks bacteria
infected the majority of wounds which became dark green or black as a result of
necrosis (Fig. 4.13c).
In many instances where the coelom had not been penetrated, the bacteria in the
wound spread and caused the death of the sand dollar. Such pathogenic bacteria
may be similar to that reported in Meoma ventricosa in Cura?ao by Nagelkerken
et al. (1999). In this instance a tetradotoxin-producing bacterial strain of the genus
Pseudoalteromonas was found in the sediment and was ingested by M. ventricosa.
The density of such strains of bacteria may have increased as a result of the
outflow of polluted water from the harbour.
In Bocas del Toro, only 2.8 % of the shallow habitats in the archipelago are
within the protected area (Guzman and Guevara 2002a). Since 1997, coastal
environments in Bocas del Toro have changed, as infrastructure such as roads,
marinas, and hotels have developed. Destruction of these seagrass habitats is
resulting in an increase in runoff and sedimentation in the coastal zone (Guzman
and Guevara 1998). This has already started to affect the coral reefs (Guzman and
Guevara 2001), and could potentially modify the function of the remaining coastal
ecosystems.
The illegal harvesting of sea cucumbers continues to put pressure on the
remaining populations particularly on the Caribbean coast of Panama, along the
coastal perimeter of Laguna de Chiriqu?, from the point of Pen?nsula Valiente
through the southern section of Isla Popa and Cayo Agua (Cruz 2000; Guzman and
Guevara 2002a).
4.7 Conclusions and Recommendations
Echinoderm diversity in Panama is reported to be greater on both the Caribbean
(Alvarado et al. 2008) and eastern Pacific coasts (Alvarado et al. 2010) than in
other Central American countries. The length of coastline, with high levels of
coastal heterogeneity may explain high levels of species richness. However, this
diversity relative to other Central American countries is probably more of a
reflection of the research effort that has taken place in Panama. The first phase of
echinoderm research in Panama began in the late 1800?s with the collections made
by the U.S. Fish Commission Steamer Albatross in the eastern Pacific. This period
of exploration resulted in many new species being described. The second phase of
echinoderm research in Panama in the 1930?s and 1940?s continued to explore the
136 S. E. Coppard and J. J. Alvarado
diversity of species and was the result of expedition by the New York Zoological
Society and the Allan Hancock Foundation. These expeditions resulted in the
collection of a vast number of specimens (some 28,835 echinoids alone from
eastern Pacific of the Americas) with the description of many new species. The
third phase of echinoderm research in Panama began with the inception of the
marine program at STRI in 1961. This has resulted in extensive ecological and
evolutionary echinoderm research, which has increased knowledge of echinoderms
not only in Panama, but in many countries in tropical America, and other regions
in the Atlantic and Pacific. Most of this knowledge concerns the ecology, repro-
duction and evolution in echinoids and certain species of asteroids (e.g. A. planci
and O. reticulatus). However, less is known about holothuroids, ophiuroids and
crinoids, particularly on a molecular and ecological level, highlighting a need for
more research in these classes of echinoderm.
The continued monitoring of populations of Diadema antillarum needs to be
maintained to determine whether the recently observed population increase is
sustained, while the monitoring of sea cucumber populations, particularly in Bocas
del Toro is needed to protect against illegal fishing. Guzman and Guevara (2002b)
have proposed that protected areas should be established allowing the monitoring
of natural populations. These could be part of the Parque Nacional Marino Isla
Bastimentos (PNMIB) or may be located close to fishing communities willing to
protect the resource.
Acknowledgments Simon Coppard thanks SENACYT (La Secretar?a Nacional de Educaci?n
Superior Ciencia Tecnolog?a e Innovaci?n) (Panama) who helped fund this project as part of
project COL08-002 and David M. Rubenstein who funded Simon through a Smithsonian
Rubenstein fellowship. Juan Jos? Alvarado thanks Consejo Nacional de Ciencia y Tecnolog?a
(CONACYT; Mexico) and Consejo Nacional para Investigaciones Cient?ficas y Tecnol?gicas
(CONICIT; Costa Rica). We are grateful to Edgardo Ochoa, Juan S?nchez, Angel Chiriboga and
Dave Pawson for providing us with photographs. We appreciate the comments made by J. Cort?s,
J. Lawrence and H.A. Lessios that improved this paper.
References
Agassiz A (1892) Reports on an exploration off the west Coast of Mexico, Central and South
America, and off Gal?pagos Island, in Charge of Alexander Agassiz by the U.S. Fish
Commission Steamer ??Albatross?? during 1891, Lieut. Commander Tanner ZL, U. S. N.
Commanding. I. Calamocrinus diomedae Agassiz A new stalked crinoid. With notes on the
apical system and the homologies of echinoderms.Mem Mus Comp Zool Harvard Coll 17:1?95
Agassiz A (1898) Preliminary report on the echini. Dredging operations of the Albatross. Bull
Mus Comp Zool 32:71?86
Agassiz A (1904) The Panamic deep sea Echini. Report XXXII on an exploration off the west
coasts of Mexico, Central and South America, and off the Galapagos Islands. Mem Mus Comp
Zool Harvard Coll 31:1?243
Alvarado JJ, Solis-Marin FA, Ahearn C (2008) Equinodermos (Echinodermata) del Caribe
Centroamericano. Rev Biol Trop 56(Suppl 3):37?55
4 Echinoderm Diversity in Panama 137
Alvarado JJ, Solis-Marin FA, Ahearn C (2010) Echinoderms (Echinodermata) diversity off
Central America Pacific. Mar Biodiv 40:45?56
Amador JA, Alfaro EJ, Lizano OG, Maga?a VO (2006) Atmospheric forcing of the eastern
tropical Pacific: a review. Prog Oceanogr 69(2?4):101?142
Berggren WA, Hollister CD (1974) Paleogeography, paleobiogeograph and the history of
circulation in the Atlantic ocean, in Studies in paleo-oceanography. Soc Econ Paleontol
Mineral Spec Publ 20:126?186
Bermingham E, Lessios HA (1993) Rate variation of protein and mitochondrial DNA evolution
as revealed by sea urchins separated by the Isthmus of Panama. Proc Nat Acad Sci USA
90:2734?2738
Boone L (1928) Echinoderms from the Gulf of California and the Perlas Islands. Bull Bingham
Oceanogr Coll Yale Univ 2:1?14
Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the
trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029?1039
Bowen BW, Muss A, Rocha LA, Grant WS (2006) Shallow mtDNA coalescence in Atlantic
pygmy angelfishes (Genus Centropyge) indicates a recent invasion from the Indian Ocean.
J Hered 97:1?12
Budd AF (2000) Diversity and extinction in the cenozoic history of Caribbean reefs. Coral Reefs
19:25?35
Burton KW, Ling HF, O?Nions RK (1997) Closure of the Central American Isthmus and its effect
on deepwater formation in the North Atlantic. Nature 386:382?385
Cheetham AH, Jackson JBC, Sanner J (2001) Evolutionary significance of sexual and asexual
modes of propagation in neogene species of the bryozoan Metrarabdotos in tropical America.
J Paleontol 75:564?577
Chesher RH (1972) The status of knowledge of Panamanian echinoids, 1971, with comments on
other echinoderms. Bull Biol Soc Wash 2:139?157
Clark AH (1939) Echinoderms (other than Holothurians) collected on the presidential cruise of
1938. Smithson Miscell Collec 98:1?22
Clark AH (1946) Echinoderms from the Pearl Islands, Bay of Panama with a revision of the
Pacific species of the genus Encope. Smithson Miscell Collec 106:1?11
Clark HL (1917) Ophiuroidea. Report XVIII and XXX on the scientific results of the expedition
of the ??Albatross?? to the tropical Pacific 1899?1900 and 1904?1905. Bull Mus Comp Zool
Harvard Univ 61:429?453
Clark HL (1940) Eastern Pacific expeditions of the New York Zoological Society. XXI. Notes on
echinoderms from the West Coast of Central America. Zoology 25:331?352
Clark HL (1948) A report on the Echini of the warmer eastern Pacific, based on the collections of
the Velero III. Allan Hancock Pac Exp 8:225?352
Coates AG, McNeill DF, Aubry MP, Berggren WA, Collins LS (2005) An introduction to the
geology of the Bocas del Toro archipelago, Panama. Carib J Sci 41:374?391
Chesher RH (1968) The systematics of sympatric species in West Indian spatangoids. Studies
Tropic Oceanogr 7:1-168, pls 1?35
Chesher RH (1970) Evolution in the genus Meoma (Echinoidea: Spatangoida) and a description
of a new species from Panama. Bull Marine Sci 20:731?761
Clark HL (1925) A catalogue of the recent sea urchins (Echinoidea) in the collection of the
British Museum (Natural History). Oxford Univ. Press, London. 250 p
Collin R, D?Croz L, Gondola P, Del Rosario JB (2009) Climate and hydrological factors affecting
variation in chlorophyll concentration and water clarity in the Bahia Almirante, Panama.
Smith Contr Mar Sci 38:323?334
Collins LS (1999) The miocene to recent diversity of Caribbean benthic foraminifera from the
Central American Isthmus. Bull Am Paleontol 357:91?107
Coppard SE (2010) The Echinoderms of Panama. Accessed online at http://echinoderms.
lifedesks.org/ on 30 May 2011
Cort?s J (1993) Comparison between Caribbean and eastern Pacific coral reefs. Rev Biol Trop
41:19?21
138 S. E. Coppard and J. J. Alvarado
Cruz LG (2000) Campa?a de educaci?n ambiental para la conservaci?n y protecci?n del pepino
de mar (Echinodermata: Holothuroidea) en 15 comunidades del Archipi?lago de Bocas del
Toro y Pen?nsula Valiente. MSc Thesis, Universidad Santa Mar?a La Antig?a, Panama
Cubit JD, Windsor DM, Thompson RC, Burgett JM (1986) Water-level fluctuations, emersion
regimes, and variations of echinoid populations on a Caribbean reef flat. Estuar Coast Shelf
Sci 22:719?737
D?Croz L, Robertson R (1997) Coastal oceanographic conditions affecting coral reefs on both
sides of the Isthmus of Panama. Proceedings of 8th international coral reef symposium,
Panama 2:2053?2058
D?Croz L, Del Rosario JB, G?mez JA (1991) Upwelling and phytoplankton in the Bay of
Panama. Rev Biol Trop 39:233?241
D?Croz L, Del Rosario JB, G?ndola P (2005) The effect of fresh water runoff on the distribution
and dissolved inorganic nutrients and plankton in the Bocas del Toro Archipelago, Caribbean
Panama. Carib J Sci 41:414?429
Deichmann E (1941) The Holothurioidea collected by the Velero III during the years 1932?1938.
Part I. Dendrochirota. Allan Hancock Pac Exp 8:61?195
Deichmann E (1958) The Holothurioidea collected by theVelero III and IV during the years 1932
to 1954. Part II Aspidochirota. Allan Hancock Pac Exp 11:253?349
Dexter D (1977) A natural history of the sand dollar Encope stokesi L Agassiz in Panama. Bull
Mar Sci 27:544?551
D?derlein L (1917) Die Asteriden der Siboga-Expedition. I. Die Gattung Astropecten und ihre
Stammesgeschichte. In:Brill EJ (ed) Siboga-Expeditie. Uitkomsten op zo?logisch, botanisch,
ozeanographisch en geologisch gebied verzameld in Nederlandsch Oost-Indie 1899 - 1900
aan boord H.M. ??Siboga??, 46 (a), Leiden, pp 191
Eakin CM (1991)The damselfish-algal lawn symbiosis and its influenced on the bioerosion of an
El Ni?o impacted coral reef, Uva Island, pacific Panama. PhD dissertation, University of
Miami, Florida
Eakin CM (1992) Post-El Ni?o Panamanian reefs: less accretion, more erosion and damselfish
protection. Proceedings of 7th International Coral Reef Symposium, Guam 1:387?396
Eakin CM (2001) A tale of two ENSO events: carbonate budgets and the influence of two
warming disturbances and intervening variability, Uva Island, Panama. Bull Mar Sci
69:171?186
Fong P, Glynn PW (1998) A dynamic size-structured population model: does disturbance control
size structure of a population of the massive coral Gardineroseris planulata in the Eastern
Pacific? Mar Biol 130:663?674
Forsberg ED (1963) Some relationships of meteorological, hydrographic and biological variables
in the Gulf of Panama. Bull Inter Amer Trop Tuna Comm 7:1109
Forsbergh ED (1969) On the climatology, oceanography and fisheries of the Panama Bight. Bull
Inter Amer Trop Tuna Comm 14:49?385
Foster SA (1987a) The relative impacts of grazing by Caribbean coral reef fishes and Diadema:
effects of habitat and surge. J Exp Mar Biol Eco 105:1?20
Foster SA (1987b) Territoriality of the dusky damselfish: influence on algal biomass and on the
relative impacts of grazing by fishes and Diadema. Oikos 50:153?160
Geyer LB, Lessios HA (2009) Lack of character displacement on the male recognition molecule,
bindin, in Atlantic sea urchins of the genus Echinometra. Mol BiolEvol 26:2135?2146
Glynn PW (1968) Mass mortalities of echinoids and other reef flat organisms coincident with
midday, low water exposures in Puerto Rico. Mar Biol 1:226?243
Glynn PW (1972) Observations on the ecology of the Caribbean and Pacific coasts of Panama.
Bull Biol Soc Wash 2:13?30
Glynn PW (1973) Acanthaster: effect on coral reef growth in Panama. Science 180:504?506
Glynn PW (1974) The impact of Acanthaster on corals and coral reefs in the eastern Pacific.
Environ Conser 1:295?304
Glynn PW (1976) Some physical and biological determinants of coral community structure in the
Eastern Pacific. Ecol Monogr 46:431?456
4 Echinoderm Diversity in Panama 139
Glynn PW (1977) Interaccions between Acanthaster and Himenoceras in the field and laboraroty.
Proceedings of 3rd international coral reef symposium, Florida 2: 209?215
Glynn PW (1981) Acanthaster population regulation by a shrimp and a worm. Proceedings of 5th
international coral reef symposium, Manila 2:607?612
Glynn PW (1982) Indiviual recognition and phenotypic variability in Acanthaster planci
(Echinodermata: Asteroidea). Coral Reefs 1:89?94
Glynn PW (1983) Crustacean symbionts and the defense of corals: coevolution on the reef. In:
Nitecki MH (ed) Coevolution. University Chicago Press, Chicago, pp 111?178
Glynn PW (1984) An amphinomid worm predator of the crown-of-thorns sea star and general
predation on asteroids in Eastern and Western Pacific corals. Bull Mar Sci 35:54?71
Glynn PW (1985a) El Ni?o associated disturbance to coral reefs and post disturbance mortality
by Acanthaster planci. Mar Ecol Prog Ser 26:295?300
Glynn PW (1985b) Corallivore population size and feeding effects following El Ni?o (1982?83)
associated coral mortality in Panama. Proceedings of 5th international coral reef symposium,
Tahiti 4:183?188
Glynn PW (1988) El Ni?o warming, coral mortality and reef framework destruction by echinoid
bioerosion in the eastern Pacific. Galaxea 7:129?160
Glynn PW (1990) Coral mortality and disturbances to coral reef in the Tropical Eastern Pacific.
In: Glynn PW (ed) Global Ecological Consequences of the 1982?83 El Ni?o-Southern
Oscillation. Elsevier, Amsterdam, pp 55?126
Glynn PW (1997) Assessment of the present health of coral reefs in the eastern Pacific. In: Grigg
RW, Birkeland C (eds) Status of coral reefs in the Pacific. Univ Hawaii Sea Grant Coll Progr,
Hawaii, pp 31?40
G?mez JA, Villalaz JR, D?Croz L (2005) Panama. In: Miloslavich P, Klein E (eds) Caribbean
Marine Biodiversity: the Known and the Unknown. DEStech Publications, Lancaster,
pp 157?168
Gonzalez P, Lessios HA (1999) Molecular evolution of the sea urchin retroviral-like (SURL)
family of transposable elements. Mol Biol Evol 16:938?952
Gordon AL (1967) Circulation of the Caribbean sea. J Geophys Res 72:6207?6223
Guzman HM, Cortes J (2007) Reef recovery 20 years after the 1982?1983 El Ni?o massive
mortality. Mar Biol 151:401?411
Guzman HM, Guevara CA (1998) Arrecifes coralinos de Bocas del Toro, Panama. I. Distribuci?n,
estructura y estado de conservaci?n de los arrecifes continentales de la Laguna de Chiriqu? y
la Bah?a Almirante. Rev Biol Trop 46:601?622
Guzman HM, Guevara CA (2001) Arrecifes coralinos de Bocas del Toro, Panam?: IV.
Distribuci?n, estructura y estado de conservaci?n de los arrecifes continentales de Pen?nsula
Valiente. Rev Biol Trop 49:53?66
Guzman HM, Guevara CA (2002a) Annual reproductive cycle, spatial distribution, abundance,
and size structure of Oreaster reticulatus (Echinodermata: Asteroidea) in Bocas del Toro,
Panama. Mar Biol 141:1077?1084
Guzman HM, Guevara CA (2002b) Population structure, distribution and abundance of three
commercial species of sea cucumber (Echinodermata) in Panama. Carib J Sci 38:230?238
Guzman HM, Guevara CA, Hernandez IC (2003) Reproductive cycle of two commercial species
of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama. Mar Biol 142:
271?279
Guzman HM, Benfield S, Breedy O, Mair JM (2008) Broadening reef protection acroos the
marine conservation corridor of the Eastern Tropical Pacific: distribution and diversity of
reefs in Las Perlas Archipelago, Panama. Environ Conser 35:46?54
Hansson H (2011) Havelockia inermis (Heller, 1868). Accessed. World Register of Marine
Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=124634 on 2011-06-04
Harborne AR, Renaud PG, Tyler EHM, Mumby PJ (2009) Reduced density of the herbivorous
urchin Diadema antillarum inside a Caribbean marine reserve linked to increased predation
pressure by fishes. Coral Reefs 28:783?791
140 S. E. Coppard and J. J. Alvarado
Hay ME, Colbum T, Downing D (1983) Spatial and temporal patterns in herbivory on a
Caribbean fringing reef: the effects on plant distribution. oecologia 58:299?308
Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results
typical? Ecology 65: 446?454
Hay ME, Fenical W, Gustafsson K (1987) Chemical defense against diverse coral reef herbivores.
Ecology 68:1581?1591
Heck KLJr (1977) Comparative species richness, composition, and abundance of invertebrates in
Caribbean seagraa (Thalassia testudinum) meadows (Panam?). Mar Biol 41:335?348
Hendler G (1977) The differential effects of seasonal stress and predation on the stability of reef-
flat echinoid populations. Proceedings of 3rd international Coral Reef Symposium, Miami
1:217?223
Hendler G (1995) New species of brittle stars from the western Atlantic, Ophionereis vittata,
Amphioplus sepultus, and Ophiostigma siva, and the designation of a neotype for
Ophiostigma isocanthum (Say) (Echinodermata: Ophiuroidea). Contrib Sci, Natural History
Museum of Los Angeles County 458:1-19
Hendler G (2005) Two new brittle star species of the genus Ophiothrix (Echinodermata:
Ophiuroidea: Ophiotrichidae) from coral reefs in the Southern Caribbean Sea, with notes on
their biology. Carib J Sci 41:583?599
Hendler G, Meyer DL (1982) An association of a polychaete, Branchiosyllis exilis with an
ophiuroid, Ophiocoma echinata, in Panama. Bull Mar Sci 32:736?744
Hendler G, Byrne M (1987) Fine structure of the dorsal arm plate of Ophiocoma wendti:
Evidence for a photoreceptor system (Echinodermata, Ophiuroidea). Zoomorphology
107:261?272
Hendler G, Grygier MJ, Maldonado E, Denton J (1999) Babysitting brittle stars: heterospecific
symbiosis between ophiuroids (Echinodermata). Invert Biol 118:190?201
Jackson JBC, Cubit JD, Keller BD, Batista V, Burns K, Caffey HM, Caldwell RL, Garrity SD,
Getter CD, Gonzalez C, Guzman HM, Kaufmann KW, Knap AH, Levings SC, Marshall MJ,
Sterger R, Thompson RC, Weil E (1989) Ecological effects of a major oil spill on Panamanian
coastal marine communities. Sci 243:37?44
Jackson JBC, Jung P, Coates AG, Collins LS (1993) Diversity and extinction of Tropical
American mollusks and emergence of the Isthmus of Panama. Sci 260:1624?1626
Jackson JBC, Jung P, Fortunato H (1996) Paciphillia revisited: transisthmian evolution of the
Strombina Group (Gastropoda: columbellidae). In: Jackson JBC, Budd AF, Coates AG (eds)
Evolution and environment in tropical America. Univ Chicago Press, Chicago, pp 234?270
Jordan DS (1908) The law of the geminate species. Am Nat 42:73?80
Kinder TH, Heburn GW, Green AW (1985) Some aspects of the Caribbean circulation. Mar Geol
68:25?52
Lawrence JM, Glynn PW (1984) Absorption of nutrients from the coral Pocillopora damicornis
(L.) by the echinoid Eucidaris thouarsii (VAL.). Comp Biochem Physiol A 77:111?112
Lessios HA (1979) Use of Panamanian sea urchins to test the molecular clock. Nature
280:599?601
Lessios HA (1981a) Reproductive periodicity of the echinoid Diadema and Echinometra on the
two coasts of Panama. J Exp Mar Biol Ecol 50:47?61
Lessios HA (1981b) Divergence in allopatry: molecular and morphological differentiation
between sea urchins separated by the Isthmus of Panama. Evolution 35:618?634
Lessios HA (1984) Possible prezygotic reproductive isolation in sea urchins separated by the
Isthmus of Panama. Evol 38:1144?1148
Lessios HA (1985a) Annual reproductive periodicity in eight echinoid species on the Caribbean
coast of Panama. In: Keegan B,F O?Connor BDS (eds) Echinodermata. Proceedings of 5th
international Echinoderm Conference, Balkema AA, Rotterdam, pp 303?312
Lessios HA (1985) Genetic consequences of mass mortality in the Caribbean sea urchin Diadema
antillarum. Proceedings of 5th International Coral Reef Symposium, Tahiti, 4:119?126
Lessios HA (1987) Temporal and spatial variation in egg size of 13 Panamanian echinoids. J Exp
Mar Biol Ecol 114:217?239
4 Echinoderm Diversity in Panama 141
Lessios HA (1988) Population dynamics of Diadema antillarum (Echinodermata: Echinoidea)
following mass mortality in Panama. Mar Biol 99:515?526
Lessios HA (1990) Adaptation and phylogeny as determinants of egg size in echinoderms from
the two sides of the Isthmus of Panama. Am Nat 135:1?13
Lessios HA (1991) Presence and absence of monthly reproductive rhythms among eight
Caribbean echinoids off the coast of Panama. J Exp Mar Biol Ecol 153:27?47
Lessios HA (1995) Diadema antillarum 10 years after mass mortality: still rare, despite help from
a competitor. Proc R Soc Lond B 259:331?337
Lessios HA (1998) The first stage of speciation as seen in organisms separated by the Isthmus of
Panama. In: Howard D, Berlocher S (eds) Endless forms: Species and Speciation. Oxford
University Press, Oxford, pp 186?201
Lessios HA (2001) Molecular phylogeny of Diadema: systematic implications.In: Barker M
(ed)Echinoderms 2000: Proceedings of 10th international Echinoderm Conference Swets and
Zeitinger, Lisse 487?495
Lessios HA (2005a) Echinoids of the Pacific waters of Panama: status of knowledge and new
records. Rev Biol Trop 53(Suppl 3):147?170
Lessios HA (2005b) Diadema antillarum populations in Panama twenty years following mass
mortality. Coral Reefs 24:125?127
Lessios HA (2007) Reproductive isolation between species of sea urchins. Bull Mar Sci
81:191?208
Lessios HA (2008) The Great American Schism: divergence of marine organisms after the rise of
the Central American Isthmus. An Rev Ecol Evol Syst 39:63?91
Lessios HA (2010) Speciation in sea urchins. In: Harris LG, B?ttger SA, Walker CW, Lesser MP
(eds) Echinoderms: Durham. Proceedimngs of 12th international echinoderm conference.
CRC Press, Taylor and Francis group, Balkema, pp 91?101
Lessios HA, Robertson DR, Cubit JD (1984a) Spread of Diadema mass mortality through the
Caribbean. Science 226:335?337
Lessios HA, Cubit JD, Robertson DR, Shulman MJ, Parker MR, Garrity SD, Levings SC (1984b)
Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs
3:173?182
Lessios HA, Cunningham CW (1993) The evolution of gametic incompatibility in neotropical
Echinometra: a reply to McClary. Evol 47:1883?1885
Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas:
global phylogeography of the sea urchin Diadema. Evolution 55:955?975
Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin
Tripneustes: contrasting patterns of population structure between oceans. Evolution
57:2026?2036
Ludwig H (1894) Reports on an exploration off the west coast of Mexico, Central America and
South America, and off the Gal?pagos Islands, in charge of Alexander Agassiz, by the U.S.
Fish Commission steamer ??Albatross??, during 1891. XII. The Holothurioidea. Mem Mus
Comp Zool XVII:1?183
Ludwig H (1905) Asteroidea in: explorations of ??Albatross?? in Tropical Pacific, 1891 and
1899?1900. Mem Mus Comp Zool XXII:1?290
L?tken CF, Mortensen T (1899) Reports on an exploration off the west coast of Mexico, Central
America and South America, and off the Gal?pagos Islands, in charge of A. Agassiz, during
1891 on the ??Albatross??. XXV. The Ophiuridae. Mem Mus Comp Zool XXIII:93?208
Maluf LY (1988) Composition and distribution of the Central eastern Pacific echinoderms. Nat
Hist Mus LA County Tech Rep 2:1?242
Martin WE, Duke A, Bloom SG, McGinnis JT (1970) Possible effects of a sealevel canal on the
marine ecology of the American Isthmian Region. Bioenvironmental and radiological-safety
feasibility studies, Atlantic-Pacific interoceanic canal. Battelle Mem Inst, Columbus, Ohio
McAlister JS (2008) Evolutionary responses to environmental heterogeneity in Central American
echinoid larvae: plastic versus constant phenotypes. Evolution 62:1358?1372
142 S. E. Coppard and J. J. Alvarado
McCartney MA, Lessios HA (2002) A quantitative analysis of gamete incompatibility between
closely related species of neotropical sea urchins. Biol Bull 202:166?181
McCartney MA, Lessios HA (2004) Adaptive evolution of sperm bindin tracks egg
incompatibility in neotropical sea urchins of the genus Echinometra. Mol Biol Evol 21:
732?745
McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation
in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391?1400
McClintock JB, Marion KR (1993) Predation by the king helmet (Cassis tuberose) on six-holed
sand dollars (Leodia sexiesperforata) at San Salvador, Bahamas. Bull Mar Sci 52:1013?1017
Meditz SW, Hanratty DM (1987) Panama: a country study. GPO for the Library of Congress,
Washington
Messing C (2010) Davidaster discoideus (Carpenter, 1888). In: Messing C (ed) World List of the
Crinoidea. Accessed. World Register of Marine Species at http://www.marinespecies.org/
aphia.php?p=taxdetails&id=246783 on 2011-06-04
Metz EC, Palumbi SR (1996) Positive selection and sequence rearrangements generate extensive
polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397?406
Meyer DL (1973) Feeding behavior and ecology of shallow-water unstalked crinoids
(Echinodermata) in the Caribbean Sea. Marine Biology, 22:105-130
Miller RJ, Adams AJ, Ogden NB, Ebersole JP (2003) Diadema antillarum 17 years after mass
mortality: is recovery beginning on St. Croix? Coral Reefs 22:181?187
Mortensen T (1921) Studies of the development and larval forms of echinoderms. CA Reitzel,
Copenhagen
Mortensen T (1928) A Monograph of the Echinoidea I. Cidaroidea. CA Reitzel, Copenhagen
Mortensen T (1935) A Monograph of the Echinoidea. II. Bothriocidaroidea, Melonechinoidea,
Lepidocentrotida and Stirodonta. CA Rietzel, Copenhagen
Mortensen T (1940) A Monograph of the Echinoidea. III. 1. Aulodonta. CA Rietzel, Copenhagen
Mortensen T (1943a) A Monograph of the Echinoidea. III. 2. Camarodonta. I. Orthop-
sid?,Glyphocyphid?, Temnopleurid? and Toxopneustid?. CA Rietzel, Copenhagen
Mortensen T (1943b) A Monograph of the Echinoidea. III. 3. Camarodonta. II. Echinid?,
Strongylocentrotid?, Parasaleniid?, Echinometrid?. CA Rietzel, Copenhagen
Mortensen T (1948a) A Monograph of the Echinoidea. IV. 1. Holectypoida, Cassiduloida. CA
Rietzel, Copenhagen
Mortensen T (1948b) A Monograph of the Echinoidea. IV. 1. Holectypoida, Cassiduloida. CA
Rietzel, Copenhagen
Mortensen T (1950) A Monograph of the Echinoidea, vol 1. Spatangoida, CA Rietzel,
Copenhagen
Mortensen T (1951) A Monograph of the Echinoidea, vol 2. Spatangoida, CA Rietzel,
Copenhagen
Nagelkerken I, Smith GW, Snelders E, Karel M, James S (1999) Sea urchin Meoma ventricosa
die-off in Cura?ao (Netherlands Antilles) associated with a pathogenic bacterium. Dis Aquat
Org 38:71?74
O?Dea A, Herrera-Cubilla A, Fortunato H, Jackson JBC (2004) Life history variation in
cupuladriid bryozoans from either side of the Isthmus of Panama. Mar Ecol Progr Ser
280:145?161
Pennington JT, Mahoney KL, Kuwahara VS, Kolber DD, Calienes R, Chavez FP (2006) Primary
production in the eastern tropical Pacific: a review. Prog Oceanogr 69:285?317
Pillans B, Chappell J, Naish TR (1998) A review of the Milankovitch climatic beat: template for
Plio-Peistocene sea-level changes and sequence stratigraphy. Sediment Geol 122:5?21
Rocha LA, Robertson DR, Rocha CR, Van Tassell JL, Craig MT, Bowen BW (2005) Recent
invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14:3921?3928
Roy MS, Sponer R (2002) Evidence of a human-mediated invasion of the tropical western
Atlantic by the ?world?s most common brittlestar?. Proc R Soc London Ser B 269:1017?1023
Seilacher A (1979) Constructional morphology of sand dollars. Paleobiology 5:191?221
4 Echinoderm Diversity in Panama 143
Sonnenholzner J, Lawrence JM (1998) Disease and predation in Encope micropora (Echinoidea:
Clypeasteroida) at Playas, Ecuador. In: Mooi R, Telford M (eds) Echinoderms: San Francisco.
Proceedings of9th international echinoderm conference, San Francisco. AA Balkema,
Rotterdam, pp 829?833
St?hr S (2010) Ophiophragmus riisei (L?tken in: Lyman 1860). In: St?hr S, O?Hara T (eds)
World Ophiuroidea database. Accessed. World Register of Marine Species at http://www.
marinespecies.org/aphia.php?p=taxdetails&id=246617 on 2011-06-04
Telford M (1982) Echinoderm spine structure, feeding and host relationships of four species of
Dissodactylus (Brachyura: Pinnotheridae). Bull Mar Sci 32:584?594
Toral-GrandaV (2008) Population status, fisheries and trade of sea cucumbers in Latin America
and the Caribbean. In: Toral-Granda V, Lovatelli A, Vasconcellos M (eds) Sea cucumbers.
A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper. No.
516. Rome, pp 213?229
Van Soest RWM (1994) Demosponge distribution patterns. In: Van Soest RWM, Kempen TMG,
Van Braekman JC (eds) Sponges in Space and Time. Biology, Chemistry, Paleontology.
Proceedings of 4th international Porifera Congress, Amsterdam. AA Balkema, Rotterdam,
pp 213?223
Vermeij GJ (1978) Biogeography And Adaptation: Patterns Of Marine Life. Harvard University
Press, Cambridge
Verrill AE (1867) Notes on the echinoderms of Panama and west coast of America, with
description of new genera and species. Trans Connect Acad Arts Sci 1:251?322
Vogler C, Benzie J, Lessios HA, Barber P, W?rheide G (2008) A threat to coral reefs multiplied?
Four species of crown-of-thorns starfish. Biol Lett 4:696?699
Waters JM, O?Loughlin PM, Roy MS (2004) Cladogenesis in a starfish species complex from
southern Australia: evidence for vicariant speciation? Mol Phylogen Evol 32:236?245
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. An RevBiochem 46:573?639
Wulff JL (1995) Sponge-feeding by the Caribbean starfish Oreaster reticulatus. Mar Biol
123:313?325
Wulff JL (2006) Sponge systematics by starfish: predators distinguish cryptic sympatric species
of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae,
Poecilosclerida). Biol Bull 211:83?94
Ziesenhenne FC (1940) New ophiurans of the allan hancock Pacific expeditions. Allan Hancock
Pac Exp 8:9?59
Ziesenhenne FC (1942) New eastern Pacific sea stars. Allan Hancock Pac Exp 8:197?223
Ziesenhenne FC (1955) A review of the genus Ophioderma. Essays in the Natural Sciences in
Honor of Captain Allan Hancock on the Occasion of his Birthday, July 26, University of
Southern California Press, Los Angeles, 1955
Zigler KS, Lessios HA (2003a) Evolution of bindin in the pantropical sea urchin Tripneustes:
comparisons to bindin of other genera. Mol Biol Evol 20:220?231
Zigler KS, Lessios HA (2003b) 250 million years of bindin evolution. Biol Bull 205:8?15
Zigler KS, Lessios HA (2004) Speciation on the coasts of the new world: phylogeography and the
evolution of bindin in the sea urchin genus Lytechinus. Evolution 58:1225?1241
Zigler KS, Raff E, Popodi E, Raff R, Lessios HA (2003) Adaptive evolution of bindin in the
genus Heliocidaris is correlated with the shift to direct development. Evolution 57:2293?2302
Zigler KS, McCartney MA, Levitan DR, Lessios HA (2005) Sea urchin bindin divergence
predicts gamete compatibility. Evolution 59:2399?2404
Zigler KS, Lessios HA, Raff RA (2008) Egg energetics, fertilization kinetics, and population
structure in echinoids with facultatively feeding larvae. Biol Bull 215:191?199
Zulliger DE, Lessios HA (2010) Phylogenetic relationships in the genus Astropecten (Paxillosida:
Asteroidea) on a global scale: molecular evidence for morphological convergence, occurrence
of species-complexes and possible cryptic speciation. Zootaxa 2504:1?19
144 S. E. Coppard and J. J. Alvarado