J. Paleont., 80(2), 2006, pp. 245±263 Copyright ᭧ 2006, The Paleontological Society 0022-3360/06/0080-245$03.00
NEOGENE CUPULADRIIDAE OF TROPICAL AMERICA. I: TAXONOMY OF RECENT CUPULADRIA FROM OPPOSITE SIDES OF THE ISTHMUS OF PANAMA
AMALIA HERRERA-CUBILLA,1 MATTHEW H. DICK,2 JOANN SANNER,3 AND JEREMY B. C. JACKSON1,4 1Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Research Institute, Box 2072, Balboa, Republic of Panama, Ͻ[email protected]Ͼ, 2COE Program on Neo-Science of Natural History, Graduate School of Science, Hokkaido University, Sapporo 060±0810 Japan, Ͻ[email protected]Ͼ, 3Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, Ͻ[email protected]Ͼ, and 4Scripps Institution of Oceanography, University of California-San Diego, La Jolla 92093-0244, Ͻ[email protected]Ͼ
ABSTRACTÐWe used up to 28 morphological characters to discriminate and describe species of the genus Cupuladria based on entire colony specimens collected from both coasts of the Isthmus of Panama. The characters included a combination of zooidal features traditionally used in cheilostome taxonomy and nontraditional characters such as colony size, shape, and an index of calci®cation of the colony, as well as the size of the basal sectors and their number of pores. Species were discriminated by a series of repeated multivariate cluster and discriminant analyses until the majority of specimens were assigned to their putative species with high statistical con®dence. Nontraditional characters contributed signi®cantly to the power of the analyses. Colonies fell into two highly distinct groups most clearly recognized by the presence or absence of vicarious avicularia, which agrees well with previous molecular genetic analyses. Further analyses of each of these two groups considered separately resulted in the discrimination of eight species. These include two previously described Caribbean species, C. biporosa Canu and Bassler, 1919 and C. surinamensis CadeÂe, 1975, and six new species: C. multesima, C. incognita, C. cheethami, and C. panamensis from the Caribbean, and C. paci®ciensis and C. exfragminis from the eastern Paci®c. There was also good correspondence between major clades within these morphologically de®ned groups and the previous molecular analysis, although 20% of the specimens could not be distinguished from their cognate (``geminate'') species from the opposite ocean. The high ratio of undescribed to described species and higher diversity in the Caribbean than eastern Paci®c agree well with newly described patterns from other cheilostome genera based on similar analyses. Quantitative morphometric studies are essential to study biologically meaningful patterns of cheilostome speciation and macroevolution in the fossil record.
INTRODUCTION of both genera reproduce asexually by fragmentation of colonies, UPULADRIID BRYOZOANS are among the most abundant chei- with subsequent regeneration of surviving fragments (Cook, C lostomes in Neogene to Recent sediments throughout trop- 1965a; McKinney and Jackson, 1989; Thomsen and HaÊkansson, ical and subtropical seas (Cook and Chimonides, 1983; McKinney 1995; HaÊkansson and Thomsen, 2001; O'Dea et al., 2004). In and Jackson, 1989). Cupuladriids dominate the very extensive addition fragmentation, in some Discoporella species, is enhanced Miocene through Pleistocene collections of the Panama Paleon- by the growth of ``zoarial buds'' along the colony periphery (Mar- tology Project from the Isthmus of Panama and the Dominican cus and Marcus, 1962). Republic (Cheetham et al., 1999; Cheetham and Jackson, 2000) The family Cupuladriidae was ®rst de®ned by Lagaaij (1952) to include only the genus Cupuladria based on specimens in the and are the most common bryozoans from extensive dredge sam- Busk collection at the British Museum (Cook, 1965a, 1965b). ples from both sides of the Isthmus (O'Dea et al., 2004). Cupu- Cook (1965a) subsequently expanded the de®nition of the family ladriids have the most complete fossil record of any bryozoans in to include both Cupuladria and Discoporella. Within this frame- tropical America, occurring in greater abundance and more sam- work, however, signi®cant taxonomic problems remain. For ex- ples than any other bryozoan clade (Cheetham and Jackson, ample, a classic monograph by Lagaaij (1963) treated Cupuladria 2000). canariensis (Busk, 1859) as a single species distributed in the The family Cupuladriidae (Lagaaij, 1952) conventionally in- tropical Atlantic and eastern Paci®c, yet Lagaaij's Cupuladria cludes the two genera Cupuladria (Canu and Bassler, 1919) and canariensis actually comprises at least two species or species Discoporella (d'Orbigny, 1852). Both genera are free-living on complexes: Cupuladria canariensis and C. biporosa Canu and or just below the sediment surface (Cook, 1965b; McKinney and Bassler, 1923. There is also confusion over generic boundaries Jackson, 1989). Sexually produced larvae settle onto small sand within the family. Cupuladria and Discoporella have been delin- grains and shell fragments that they soon overgrow, after which eated morphologically by the degree of development of the cryp- they maintain their position on the bottom using the long setae tocyst and the presence or absence of basal sectors, kenozooidal of the peripheral and subperipheral autozooidal vibracula (Mc- chambers, and vicarious avicularia (Cook, 1965a, 1965b; Cook Kinney and Jackson, 1989). The normal life position is with the and Chimonides, 1994). In general, Cupuladria have well-de®ned convex, frontal surface upwards (Fig. 1.3, 1.4). Vibracular setae basal sectors and internal kenozooidal chambers, vicarious avi- on the frontal surface sweep away sediment particles and help cularia are common, and the cryptocyst is poorly developed (Fig. colonies to reach the surface after sudden burial. 1.5±1.8). In contrast, Discoporella lack basal sectors, vicarious Cupuladriids are colonial animals that grow by budding of avicularia, and kenozooidal chambers, and the cryptocyst is well modular zooids, but growth of the colony is semideterminate as developed (see Cook, 1965b, p.196, ®g. 2). However, intermediate with solitary animals. Cupuladria and Discoporella exhibit the morphologies exist, especially in the variable development of the same general pattern of development and internal structure and cryptocyst that allowed Boardman et al. (1970) to suggest that overlap broadly in colony size, shape, and life history (HaÊkans- the family probably includes three generic groups. Baluk and son, 1973). Colonies of both genera range in size from about 3 Radwanski (1984) subsequently described a third cupuladriid ge- to 23 mm and in shape from small thimble-shaped cones to large nus Reussirella, from the Vienna basin (middle Miocene Baden- ¯attened disks. Besides sexual reproduction of larvae that settle ian), based on the incomplete development of the cryptocyst in- and metamorphose to develop into new colonies, many species termediate between that of Cupuladria and Discoporella. 245 246 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006 HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 247
Moreover, a recent molecular phylogeny (Dick et al., 2003) did TABLE 1ÐThe morphological characters used to discriminate Cupuladria not clearly separate Cupuladria and Discoporella into distinct morphospecies. clades, but instead showed Cupuladria surinamensis (CadeÂe, 1975), which lacks vicarious avicularia, as the basal node of a Abbreviation Character name Discoporella clade. This suggests that characters other than the Cw Colony diameter Ch Colony height condition of the cryptocyst may be diagnostic at the generic level. Rahw Colony height±diameter ratio Further molecular studies, and cladistic analyses of the full range Ci Calci®cation index of morphologies of Recent and fossil species included in the Cu- RaZV AutozooidÐVicarious avicularia ratio and mode of repro- puladriidae, will be necessary to delineate genera within the fam- duction: fraction of the eight units, from the ®rst gen- eration of the colony, that are autozooids. In the ab- ily. sence of an ancestrula (e.g., origin by fragmentation) The taxonomy and systematics of tropical American cupulad- we scored as the integer 2 (see text). riids have usually been studied piecemeal from small geographic Zl Autozooid length areas or limited geological horizons. Moreover, the same species Zw Autozooid width Ol Opesia length names are commonly applied to specimens ranging over 10 to 15 Ow Opesia width million years and often from both the Atlantic and Paci®c. How- Al Autozooid vibracula length ever, detailed morphometric, cladistic, and molecular analyses of Aw Autozooid vibracula width the cheilostome genera Metrarabdotos Canu, 1914, Stylopoma RaOlZl Ratio opesia length±autozooid length RaOwZw Ratio opesia width±autozooid width Levinsen, 1909, Celleporella Gray, 1848, and Adeonellopsis RaAlZl Ratio autozooid vibracula length±autozooid length MacGillivray, 1886 have shown that most such widespread spe- RaAwZw Ratio autozooid vibracula width±autozooid width cies are actually complexes of cryptic species, i.e., species that NV Number of Vicarious avicularia* are genetically distinct, but extremely similar in their morphology Vl Length of Vicarious avicularia Vw Width of Vicarious avicularia and ecology (Brown and Lomolino, 1998, p. 245); that the true VOl Length of the Vicarious avicularia opesia species diversity is at least three to ®ve times greater than that VOw Width of the Vicarious avicularia opesia recognized by traditional descriptive taxonomy (Cheetham, 1986; VAl Vicarious avicularia vibracula length Jackson and Cheetham, 1990, 1994; Lidgard and Buckley, 1994; VAw Vicarious avicularia vibracula width RaVOlVl Ratio Vicarious avicularia opesia length±Vicarious avicu- Cheetham and Jackson 1996, 2000; Cheetham et al., 1999; laria length Hughes et al., 2004). Similar suites of cryptic species have been RaVOwVw Ratio Vicarious avicularia opesia width±Vicarious avicu- discovered for the great majority of marine invertebrates (Knowl- laria width ton, 1993; Knowlton and Jackson, 1994). RaVAlVl Ratio Vicarious avicularia vibracula length±Vicarious avic- ularia length In a previous paper, Dick et al. (2003) conducted an analysis RaVAwVw Ratio Vicarious avicularia vibracula width±Vicarious avic- based on DNA sequences to examine species boundaries and phy- ularia width logenetic relationships among cupuladriid bryozoans from tropi- Asec Basal sector's area cal America. The present paper is the ®rst in a series to apply Psec Number of pores per sector morphologically based methodologies to the taxonomy and sys- * We use here the term Vicarious avicularia after Cook and Chimonides, tematics of cupuladriid bryozoans from tropical America. We be- 1994. gin here with a morphometric analysis of the taxonomy of Cu- puladria from both sides of the Isthmus of Panama. The next two papers will include the morphometrically based taxonomy of Dis- coporella from the same region, followed by a cladistic analysis voucher specimens, collected separately from both sides of Pan- of the entire Recent fauna, in order to de®ne clades independent ama, which had been identi®ed genetically by sequencing a frag- of the traditional Cupuladria±Discoporella dichotomy. Only then ment of the 16S mtrRNA gene (Dick et al., 2003). These are will we have the systematic framework necessary to address the referred to hereafter as the VOUCHER specimens. fossil record and the phylogeny of the abundant Neogene cupu- Taxonomic characters.We used a combination of traditional ladriids from tropical America. zooidal characters and additional characters based on the size, shape, and weight of entire colonies as well as the shape and size MATERIAL AND METHODS of basal sectors and their numbers of pores (Table 1, Fig. 1). Collections.Specimens of Cupuladria were obtained by Similar characters based on the morphology of the entire colony dredging along both coasts of Panama during cruises of the RV have contributed signi®cantly to the power of discrimination of Urraca between 1995 and 1998 (O'Dea et al., 2004). Specimens scleractinian coral species, as well as studies of their life histories were separated from the substrate by sieving on deck with a 2 and ecology (Budd et al., 1994; Johnson et al., 1995; Knowlton mm mesh screen, and were placed in bags for subsequent wash- and Budd, 2001). Colonial characters should be particularly valu- ing, drying, and sorting into major taxa in the laboratory. Speci- able for cupuladriid bryozoans that exhibit semideterminate mens used in our analyses came from 30 of the dredge samples, growth. which included samples from the Gulf of Panama and Gulf of All observations and measurements were made using a Leica Chiriqui on the Paci®c side, and from the Bocas del Toro region MZ12 microscope and SigmaScan and SigmaScan Pro image eastward to central Panama and the San Blas archipelago on the measurement and automated image analysis software (Jandel Sci- Caribbean side. These specimens are referred to hereafter as the enti®c, 1993±1995). Weights of colonies for calculation of the SURVEY specimens. In addition, we included in our analyses calci®cation index (see O'Dea et al., 2004, p. 151) were made
←
FIGURE 1ÐMorphological characters used for discrimination of Cupuladria morphospecies. 1±3, Colonies of different shapes and mode of repro- duction; 1, C. biporosa Canu and Bassler, 1923 and 3, C. panamensis n. sp. are colonies that originated by sexual reproduction; 2, colony of C. biporosa regenerated from fragmentation. 4±8, C. biporosa, 4, size of the colony, 5, ancestrula and early astogeny (outlined); 6, 7, characters of autozooid and vicarious avicularium; 8, basal sectors (outlined) and pores. All these characters as well as ratio characters are de®ned in Table 1. 248 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
TABLE 2ÐResults for 110 Cupuladria SURVEY colonies entered as TABLE 3ÐResults of Discriminant Analysis based on 28 characters; for SUR- ``groups'' in a Direct Discriminant Analysis based on 28 characters. All VEY colonies of Cupuladria with vicarious avicularia (VA group). All characters were transformed like this: log10 (1 ϩ variable), see Methods, characters were transformed like this: log10 (1 ϩ variable), see Methods, and refer to Table 1 for character names. Difference between groups: N ϭ and refer to Table 1 for character names. Difference between groups: N ϭ 110, Wilks' Lambda ϭ 0.000, Chi-square ϭ 12,418.95, P ϭ 0.0000. 66, Wilks' Lambda ϭ 0.000, Approx. F ϭ 8.989, P ϭ 0.0000.
Cumulative Characters with % cases correctly Cumulative Characters with % cases correctly DF Eigen value % variance largest coef®cient classi®ed DF Eigen value % variance largest coef®cient classi®ed 1 14,227.60 0.543 V1 1 59.565 0.703 VAl RaVOlVl Vl Vw Vw VOl RaVAlVl 2 8,113.89 0.853 Vw 100 2 14.264 0.871 RaAlZl 100 Vl Zl RaVAwVw Al VAw RaHD 3 3,819.41 0.999 Vl 3 5.814 0.94 Zl RaVOlVl Zw Vw Ol VOl Aw Jackknifed classi®cation 98.3%. Jackknifed classi®cation 90%.
using a Sartorious Basic Balance (Model B1205-⌽UR) at a pre- cision of 0.001g. For zooidal measurements we chose haphazardly this second set of measurements, we used only a single fragment three to ®ve autozooids from the zone of astogenetic repetition to per colony to reconstruct the diameter, height, and weight of the maximize consistency of the results (Boardman et al., 1970; Jack- original entire colony. The procedure involved making drawings son and Cheetham, 1990, 1994). When vicarious avicularia were of the fragment using a camera lucida to determine the diameter, present, they occurred outside the zone of astogenetic repetition, and mounting it onto a reconstructed base of modeling clay to either in the central part of the colony or scattered in the zone of determinate the height, according to the assumption of a regular astogenetic change. To minimize effects of variation in early de- morphology for the colony. Using a camera lucida drawing, we velopment, data for vicarious avicularia were transformed like calculated the area of the fragment as a fraction of total colony this: log10 (1ϩvariable), as were all characters for colony char- area; then weighing the fragment, we estimated the weight of the acteristics including height, diameter, the ratio between these two original colony. Estimates of whole-colony values based on these dimensions, Autozooid±Vicarious avicularia ratio (in the central reconstructions were not signi®cantly different from the original part of the colony, see Fig. 1), mode of reproduction, index of measurements based on entire, unbroken colonies (t-tests; diam- ϭϪ ϭ ϭ ϭ ϭ calci®cation, and ®nally all characters related to autozooids and eter: t 0.784, df 58, P 0.436; height: t 0.985, df ϭ ϭ ϭ ϭ the basal sectors. 58.0, P 0.329; weight: t 0.875, df 56.6, P 0.385). Colonies derived through sexual reproduction and the subse- These methods were then applied to the VOUCHER specimens quent settlement and metamorphosis of a larva have an ancestrula to obtain a full suite of the 28 characters for the analyses. and pattern of early astogeny that are absent in colonies regen- Discrimination of morphospecies. We used a modi®cation of erated from fragments. Recent studies have shown that in sexually the methodologies developed previously for discriminating spe- produced colonies, the ancestrula of Cupuladria species is typi- cies of Metrarabdotos and Stylopoma (Cheetham, 1986; Jackson cally a triplet of zooids developed simultaneously during meta- and Cheetham, 1990, 1994; Cheetham et al., 2001). In the ®rst morphosis (Winston, 1988; Cook and Chimonides, 1994). This phase using the statistical program SPSS Inc., 2002; 110 SUR- ancestrula is directly connected to ``the primary circle (or ®rst VEY colonies were entered as ``groups'' into a Linear Discrimi- generation) of zooecia budded from it'' which altogether comprise nant Analysis based on the 28 morphological characters (Chee- what Cook (1965a, p. 155) termed the ``ancestrular area,'' char- tham et al., 2001). Colonies were entered independently without acteristically located in the central area of the colony. Although being preassigned to any putative group. This analysis resulted in it seems that only autozooids can occur in early astogeny, the two well-de®ned groups of colonies most readily distinguished by proportions of Autozooids and Vicarious avicularia formed during the presence or absence of vicarious avicularia. These groups the subsequent development of the colony could be systematically were designated VA and NVA, respectively, and subsequently relevant. We call this character the Autozooid±Vicarious avicu- analyzed separately from one another. laria ratio scored as the fraction of the eight units, from the ®rst In the second phase of the analysis, we submitted each of these generation of the colony, that are autozooids (e.g., for C. biporosa two groups separately to a Hierarchical Cluster Analysis using the the range of values of this character is ®ve-eighths to seven- nearest neighbor method based on squared Euclidean distance eighths). Colonies regenerated from fragments were arbitrarily (SPSS Inc., 2002). We used 28 characters to cluster 66 colonies scored as the integer 2. of the VA group (two colonies were discarded because of missing Measurements of colony dimensions and weights of entire col- data). This analysis produced 14 discrete groups with a similarity onies were not made for the VOUCHER specimens before they coef®cient of Ͻ0.04, with 12 outlier colonies (18%) which in- were broken apart to homogenize parts of the colonies for genetic cluded colonies that split between clusters. In contrast, we used analysis. We therefore exploited the relatively simple colony mor- only 17 characters to cluster 42 colonies of the NVA group, be- phology of Cupuladria to design a modeling approach to estimate cause all the characters related to vicarious avicularia were absent colony characters for the vouchers. We ®rst randomly picked 30 (see above). This analysis produced 12 discrete groups with a additional Cupuladria colonies not otherwise used for the dis- similarity coef®cient of Ͻ0.02, with eight outlier colonies (19%). crimination of morphospecies, and measured their height, diam- In the third phase of the analysis, the 14 discrete groups of VA eter, and weight. We then broke these 30 colonies into fragments colonies and the 12 discrete groups of NVA colonies were tested of different size and shape and then measured the fragments. For for stability in a series of Linear Discriminant Analyses (Jackson HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 249
FIGURE 2ÐThe Canonical Discriminant Plot for all 110 SURVEY col- onies entered as ``groups'' based on 28 characters. Each point repre- sents a colony. The groups were identi®ed qualitatively, before quan- titative analyses: A±E (above), VA group; F±H (below), NVA group. and Cheetham, 1994) using the same 28 and 17 characters, re- spectively. The purpose was to determine whether the clusters were signi®cantly different from each other and whether each colony was correctly assigned to its cluster. In the ®rst of these analyses, colonies were assigned to clusters only if they were unambiguously included in their respective groups. All other col- onies, including outliers and intermediate colonies, were left un- assigned. The highest probability cluster for each colony, includ- ing previously assigned and unassigned colonies, was determined by the classi®cation function of the discriminant analysis, based on colony mean values (Jackson and Cheetham, 1994). In each succeeding analysis, we combined clusters not different at P Ͻ 0.001 and reassigned colonies to their highest probability clusters. For the cross-validation we used standard ®rst-order jackkni®ng when only a single original colony was excluded, or higher-order jackkni®ng when more than one original colony was excluded (SPSS Inc., 1999, p. 321). After 23 discriminant analyses, the 14 clusters of the 66 colo- nies with vicarious avicularia (VA colonies) were reduced to six putative morphospecies (Fig. 3), and after 18 discriminant anal- yses the 12 clusters of the 42 colonies without vicarious avicularia (NVA colonies) were reduced to two putative morphospecies. All FIGURE 3ÐCanonical Discriminant Plot based on 28 skeletal morpholog- morphospecies in both groups were different from one another at ical characters used for the discrimination of SURVEY Cupuladria P Ͻ 0.001 (Fig. 3, Table 4). colonies of the VA group. The morphospecies discriminated are: C. Only 28 VOUCHER specimens were suitable for morphometric multesima n. sp. (⌬), C. incognita n. sp. (᭡), C. cheethami n. sp. (Ⅲ), analysis. Of these, 24 were in the group with vicarious avicularia C. paci®ciensis n. sp. (⅙), C. biporosa (▫), C. exfragminis n. sp. (●). (VA colonies) and four were in the group without vicarious avi- Ellipses represent 95% con®dence limits of group centroids for the two cularia (NVA). We added the 24 VOUCHER specimens with vi- discriminant function plots. carious avicularia (VA VOUCHER) to the original 66 VA SUR- VEY colonies that had been grouped into six putative species based on the 28 characters. The VOUCHER specimens were left NVA SURVEY colonies that had been grouped into two putative unassigned. We then repeated the discriminant analysis to deter- species based on 17 characters. As above, these VOUCHER col- mine how the voucher specimens were classi®ed based on the onies were not assigned to groups and we then repeated the dis- morphological characters. Similarly, we added the four specimens criminant analysis to determine how the voucher specimens were without vicarious avicularia (NVA colonies) to the original 42 classi®ed based on morphological characters. 250 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
FIGURE 4ÐCupuladria multesima n. sp.,USNM523158, Bocas del Toro. 1, Colony, bar scale ϭ 1 mm; 2, ancestrula and central vicarious avicularia; 3, autozooid and autozooid vibracula; 4, basal radial sectors; 5, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony up). 2±5 bar scales ϭ 100 m.
RESULTS Clustering and the ®nal series of discriminant analyses of col- The ®rst discriminant analyses neatly separated the two groups onies with vicarious avicularia (VA colonies) based on 28 char- distinguished by the presence or absence of vicarious avicularia acters resulted in six putative morphospecies (Fig. 3, Table 3). at very high con®dence (Fig. 2, Table 2). All of the specimens Ranks of the canonical discriminant function scores for the ®rst were correctly classi®ed by the classi®cation function of the dis- two functions are presented in Appendix. All of the groups were criminant analysis and 98.3% by jackknife analysis. The most different at P ϭ 0.0000 with 100% of cases correctly classi®ed highly signi®cant character for discrimination of the two groups by the classi®cation function of the discriminant analysis versus was the size of the vicarious avicularia, although many other char- 90% by jackknife analysis. Most colonies were assigned to their acters contributed signi®cantly. cluster at P Ͼ 0.999 although two colonies (3%) could not be HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 251
TABLE 4ÐResults of Discriminant Analysis based on 17 characters; for SUR- classi®ed. The four species from the Caribbean include Cupulad- VEY colonies of Cupuladria without vicarious avicularia (NVA group). All characters are transformed like this: log10 (1 ϩ variable), see Methods, ria biporosa (Fig. 6) as well as the three new species Cupuladria and refer to Table 1 for characters names. Difference between groups: N multesima (Fig. 4), Cupuladria incognita (Fig. 5), and Cupuladria ϭ 42, Wilks' Lambda ϭ 0.081, Approx. F ϭ 15.526, P ϭ 0.0000. cheethami (Fig. 7). The two species from the tropical eastern Pa- ci®c are both new: Cupuladria paci®ciensis (Fig. 8) and Cupu- Cumulative Characters with % cases correctly ladria exfragminis (Fig. 9). DF Eigen value % variance largest coef®cient classi®ed Comparable clustering and discriminant analyses, for colonies 1 11.292 1.000 Zw without vicarious avicularia (NVA) based upon 17 characters, re- Ow 100 sulted in just two putative morphospecies (Table 4). The ranks of Zl RaOwZw the canonical discriminant function scores are given in Appendix. The two groups were different at P ϭ 0.0000 with 100% of the Jackknifed classi®cation 100%. cases classi®ed correctly by both the classi®cation function and by jackkni®ng. As above, most of the colonies were correctly classi®ed to their cluster at P Ͼ 0.999 and no colonies were left unassigned. The two Caribbean species are Cupuladria surina- mensis (Fig. 10) and Cupuladria panamensis n. sp. (Fig. 11).
FIGURE 5ÐCupuladria incognita n. sp., USNM523161, Bocas del Toro. 1, Colony, bar scale ϭ 1 mm; 2, ancestrula and central vicarious avicularia; 3, autozooid and autozooid vibracula; 4, basal radial sectors; 5, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony up). 2±5 bar scales ϭ 100 m. 252 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
Four of the 24 VOUCHER colonies with vicarious avicularia had missing data for at least one colony character and were dis- carded from the analysis. Sixteen of the remaining 20 colonies (80%) were classi®ed correctly according to their classi®cation based upon molecular data (Dick et al., 2003). Cupuladria bipo- diam.: 0.13 mm max. diam.: 0.10 mm diam.: 0.13 mm diam.: 0.06 mm diam.: 0.10 mm diam.: 0.10 mm diam.: 0.16 mm diam.: 0.27 mm rosa corresponds to Cupuladria 4 of Dick et al. (2003), while the eastern Paci®c species Cupuladria exfragminis corresponds to species Cupuladria 5 of Dick et al. (2003). The four incorrectly classi®ed colonies were assigned to their cognate species from the opposite ocean: two colonies from the Paci®c were classi®ed as Thinner 0.70 3±4 layers Thin 0.54 1±20.34 layers max. 1±2 layers max. C. biporosa from the Caribbean; while one of the Caribbean col- 0.440.47 1±2 layers max. 0.57 1±2 layers max. 1 layer max. onies was classi®ed as C. exfragminis and the other as C. paci- ®ciensis from the Paci®c. The four VOUCHER colonies without vicarious avicularia (NVA) were all classi®ed correctly according to their classi®cation based upon molecular data as Cupuladria surinamensis, which corresponds to Cupuladria species 6 of Dick et al. (2003). gular 12±16 pores times irregular 1±6 pores times irregular 3±6 pores times irregular 4±6 pores times irregular 4±6 pores pores Radial 6±18 pores Thick 0.80Radial and rectan- 5±6 layers max. Rectangular some- Rectangular some- Rectangular some- Radial 14±24 Radial 8±23 pores 0.57 1 layer max. DISCUSSION
Morphometric analysis and extensive new collecting increased C. C. the number of Cupuladria species from three to eight species, of C. suri- which only C. biporosa and C. suranamensis were previously C. incog- described. This increase in diversity mirrors that for Metrarab- cryptocyst Basal sectors Wall (mm) Kenozooids dotos and Stylopoma, the only other tropical American cheilos- Autozooid nita multesima thickened by sec- ondary calci®cation thickened by sec- ondary calci®cation thickened by sec- ondary calci®cation panamensis tome genera subjected to such detailed morphometric analysis namensis (Jackson and Cheetham, 1994; Cheetham and Jackson, 1996, Wider than Narrower than 2000). The strong morphological differentiation in the ®rst phase of the discriminant analyses between colonies with and without vi-
carious avicularia agrees well with the molecular results in which shape wider than long wider than long Cupuladria haplotypes 4 and 5 (corresponding to our C. biporosa Autozooid Hexagonal Hexagonal Hexagonal InHexagonal ancestrular area In ancestrular area not and C. exfragminis n. sp.) are sister clades, whereas Cupuladria Hexagonal InHexagonal ancestrular area not Ð Rectangular some- haplotype 6 is the sister clade to Discoporella (Dick et al., 2003). The six species with vicarious avicularia probably include two or three distinct clades whose resolution requires cladistic anal- ysis. Cupuladria multesima n. sp. and C. incognita n. sp. are very different from the rest; and some of their features resemble rather Vicarious those of C. canariensis. However, Cupuladria multesima has ra- avicularia dial basal sectors while C. incognita has a combination of radial or 3rd generation or 5th generation netic change some- times absent netic change netic change netic change and elongated rectangles, and in both species the sectors present morphospecies described. large numbers of pores; but only the long rectangular sectors of C. incognita resemble somewhat those of C. canariensis. Both Cupuladria multesima and C. incognita also have abundant vi- Cupuladria carious avicularia exclusively in the central part of the colony ratio Vicarious Avicularia (Table 5), like C. canariensis, but the shape of vicarious avicularia Autozooid more closely resembles C. biporosa (see Cook, 1965b, p. 202, ®g. i; Cook and Chimonides, 1994, p. 255, ®g. 8). Moreover, C. multesima and C. incognita are both smaller than about 8 mm in diameter, whereas C. canariensis commonly grows larger than 20 diameter mm (Cook and Chimonides, 1994). Finally, both C. multesima Zooarium Max.: 4.3 mm 0 Central area up to 2nd Max.: 6.8 mmMax.: 9.9 mm 0 5:8±7:8Max.: 9.1 mm Central area Scattered up zone to astoge- 5:8±7:8 4th Scattered zone astoge- Max.: 6.3 mm 5:8±7:8 Scattered zone astoge- and C. incognita have several layers of basal kenozooids, al- Max.: 9.3 mmMax.: 9.6 Ð mmMax.: 8.8 mm Scattered1 zone astoge- 1 Absent Absent Hexagonal Hexagonal Narrower than in Wider than in though the number of layers of kenozooidal chambers in C. can- ariensis is unknown. We therefore agree with CadeÂe (1975, 1979) that, despite numerous previous reports, C. canariensis appears to be absent from the tropical western Atlantic. shape
The other four species with vicarious avicularia are probably Zooarium high-narrow h/d ratio 0.6 h/d ratio 0.5 h/d ratio 0.3 h/d ratio 0.25 h/d ratio 0.25 cognate species that show similar morphological features includ- h/d ratio 0.2 h/d ratio 1:3 and narrow h/d ratio 0.3 Dome shape Cone shape Cone shape Cone shape Cone shape ing: rectangular basal sectors with mostly four to six pores, one Irregular cone shape Cone shape Dome shape high to two kenozooidal chambers, vicarious avicularia of the same
shape and scattered throughout the zone of astogenetic change n. sp. n. sp. n. sp. n. sp. n. sp.
(Figs. 6±9, Table 5), and with the exception of C. exfragminis,an n. sp. Autozooid-Vicarious avicularia ratio of 5:8±7:8 (Table 5). Of ÐComparison of morphological characters for the eight 5 these, Cupuladria paci®ciensis n. sp. and C. exfragminis from the Species Paci®c have smaller autozooids than any of the cognate species multesima incognita biporosa cheethami paci®ciensis exfragminis surinamensis panamensis ABLE T Cupuladria Cupuladria Cupuladria Cupuladria Cupuladria from the Caribbean. However, C. exfragminis is most distinct in Cupuladria Cupuladria Cupuladria HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 253
FIGURE 6ÐCupuladria biporosa. 1±5, USNM523164 Bocas del Toro; 1, colony, bar scale ϭ 1 mm; 2, ancestrula, autozooids, and vicarious avicularia in the central area of the colony, showing secondary calci®cation; 3, autozooid and autozooid vibracula; 4, vicarious avicularia and vicarious avicularia vibracula; 5, basal sectors; 6, USNM523166, San Blas, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony down). 2±6 bar scales ϭ 100 m. the discriminant analyses because it has the largest ratio of au- C. exfragminis across the isthmus. However, this does not account tozooid vibracular length to autozooid length (Tables 3 and 6, Fig. for the misidenti®cation of the fourth VOUCHER specimen as C. 9); and its autozooid vibracula is more than the half the length of paci®ciensis. the autozooid. The two species without vicarious avicularia include C. suri- The misidenti®cation of three of the four VOUCHER specimens namensis, that ranges throughout the wider Caribbean, and the with vicarious avicularia is due to confusion with their morpholog- new species C. panamensis so far known only from the central ically extremely similar cognate species such as C. biporosa and Caribbean coast of Panama. No Cupuladria species without 254 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006 n. sp. Cupuladria exfragminis N Mean SD n. sp. n. sp. Cupuladria paci®ciensis Cupuladria panamensis N Mean SD N Mean SD Cupuladria biporosa N Mean SD Morphospecies n. sp. Cupuladria cheethami N Mean SD n. sp. Cupuladria surinamensis Cupuladria incognita N Mean SD N Mean SD n. sp. Cupuladria multesima N Mean SD ÐMeasurements in mm of zoarial and zooidal characters for the eight morphospecies described. Refer to Table 1 for character names. 6 hw 9 0.589 0.175 15 0.523 0.172 6hw 0.253 0.043 14 0.288 23 0.075 8 0.261 0.027 0.356 9 0.215 0.074 0.084 16 0.644 0.146 CwChRa Zl 9Zw 9Ol 3.558Ow 9Al 2.128 9Aw 0.408 9Vl 9 0.384 0.759 0.306Vw 9VAl 15 9 0.270 0.142 0.025VAw 15 0.027 9 9 0.205 4.553 0.015 0.174 9 0.013 9 15 2.261 15 0.351 0.025 0.254 1.205 0.022 15 0.148 0.384 15 0.122 0.576 0.318 0.024 0.024 15Cw 0.245 6 0.017 15 0.148 0.026Ch 0.014 0.038 6 15Ra 0.214 15 0.020 0.183Zl 7.008 15 0.015 15 6Zw 1.758 0.370 6 0.025 0.278Ol 0.020 1.736 0.159 6Ow 0.135 6 0.555 0.483 0.030Al 0.331 0.024 6Aw 0.018 14 6 0.415 0.014 0.200 0.049 14 0.022 6 6 0.213 7.133 0.045 0.166 6 0.033 23 6 14 2.100 14 0.511 23 0.018 0.312 1.272 0.020 14 0.198 0.447 14 0.155 0.822 0.317 0.070 23 0.027 23 14 0.321 8 0.018 14 0.180 0.034 0.015 23 0.038 8 23 14 0.214 14 0.026 0.161 5.441 23 14 0.016 22 14 8 1.419 0.426 8 0.020 0.300 0.016 0.780 0.188 8 0.149 6.339 8 0.435 0.251 0.059 0.294 0.029 2.280 8 0.024 8 0.319 9 0.017 0.175 0.039 0.014 0.547 9 8 0.371 8 0.201 0.027 0.165 8 7.333 0.012 0.406 8 9 0.219 1.544 0.368 9 0.014 0.246 0.015 0.235 1.376 0.169 9 0.165 0.138 9 0.423 0.544 0.035 0.294 0.032 9 0.017 9 0.330 1.714 0.010 0.181 0.042 0.023 0.830 9 9 0.218 0.027 0.173 9 0.015 9 0.058 0.408 0.048 0.019 0.297 0.020 0.202 0.036 0.163 0.031 0.047 0.028 0.030 0.018 0.018 0.012 16 16 16 16 16 16 16 16 6.255 3.891 0.586 0.414 0.415 0.248 0.259 0.198 1.199 0.582 0.071 0.045 0.052 0.012 0.028 0.021 logical ABLE Morpho- characters T Morphospecies with Vicarious avicularia (VA group) Morphospecies without Vicarious avicularia (NVA group) HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 255
FIGURE 7ÐCupuladria cheethami n. sp. 1, 2, USNM523168 Laguna de Chiriqui, Bocas del Toro; 1, colony, bar scale ϭ 1 mm; 2, ancestrula, autozooids, and vicarious avicularia in the central area of the colony; 3±5, USNM523167, Laguna de Chiriqui, Bocas del Toro; 3, autozooid and autozooid vibracula; 4, vicarious avicularia and vicarious avicularia vibracula; 5, basal sectors; 6, USNM523169, Laguna de Chiriqui, Bocas del Toro, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony up). 2±6 bar scales ϭ 100 m. vicarious avicularia are known from the tropical eastern Paci®c. highly restricted distributions, such as C. cheethami n. sp., that Their absence helps to explain the much greater diversity of Cu- was found only in the Chiriqui Lagoon from depths 20±23 m, puladria species in the Caribbean compared to the tropical eastern and from the Gulf of San Blas from 67 m to 100 m that was not Paci®c. sampled during the cruises to collect living colonies. Moreover, The much larger number of species found in this study com- most of the specimens of C. incognita, C. paci®ciensis, and C. pared with the molecular study stems from the far greater sam- panamensis n. sp. occurred as dead colonies in the dredge samples pling effort employed. Several of the new species appear to have (80%, 90%, and 97%, respectively). Lastly, C. multesima and C. 256 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006 panamensis that correspond to Cupuladria 1 and Cupuladria 9, Occurrence.From the western San Blas archipelago to Bocas respectively, in the life history study of cupuladriids from the del Toro. Isthmus of Panama done by O'Dea et al. (2004), were found in Discussion.In comparison to C. multesima, the zoarium is fewer samples, only 5.4% and 1.6%, respectively, than the other approximately as wide as high, and although both species have species. autozooids wider than long, the cryptocyst C. incognita is nar- rower than in C. multesima. SYSTEMATIC PALEONTOLOGY
Order CHEILOSTOMATIDA Busk, 1852 CUPULADRIA BIPOROSA Canu and Bassler, 1923 Suborder FLUSTRINA Smitt, 1867 Figure 6 Superfamily CALLOPOROIDEA Norman, 1903 Family CUPULADRIIDAE Lagaiij, 1952 Cupuladria biporosa CANU AND BASSLER, 1923, p. 29, pl. 47, ®gs. 1, 2, Genus CUPULADRIA Canu and Bassler, 1919 Miocene, Santo Domingo. CUPULADRIA MULTESIMA new species Cupuladria biporosa CANU AND BASSLER, 1923. COOK, 1965b, p. 203, Figure 4 pl. 1, ®gs. 2, 4, 6. Diagnosis.The colony is dome-shaped, small, and compact, very densely calci®ed, with a height-diameter ratio of about 0.6 Description. The zoarium has a height-diameter ratio of about and vicarious avicularia occupying the central area. 0.3 with a maximum diameter of 9.9 mm. The central area of the Description.The zoarium is dome shaped, high, narrow, and colony is formed mostly by autozooids; the cryptocyst of these compact with a maximum observed diameter of 4.3 mm. The autozooids and vicarious avicularia are thickened by secondary entire central area of the colony consists of vicarious avicularia calci®cation. The vicarious avicularia are frequent and scattered up to the second or third astogenetic generation. The autozooids throughout the zone of astogenetic change, but occasionally ab- have a hexagonal shape, wider than long. The basal sectors are sent. The autozooids have a hexagonal shape approximately as radial, with 6±18 pores per basal sector. The colony wall is thick; wide as long. The basal sectors are mostly rectangular but some- in transversal section it has a maximum width of 0.80 mm, with times irregular in shape with one to six pores per sector (mostly ®ve to six layers of basal kenozooecial chambers (max. diam. 0.13 three to four). The colony wall has in transversal section a max- mm). imum width of 0.54 mm, with one to two layers of basal keno- Etymology.The name multesima is Latin for ``very small,'' zooecial chambers (max. diam. 0.13 mm). with reference to its smaller zoarium size in comparison with the Material examined.USNM523164, USNM523165, BT99± other species studied. 130, Bocas del Toro; September 1999, H. Fortunato coll., 9.47Њ Types.Holotype, USNM523158, BT98±36, Bocas del Toro; Lat., 82.33Њ Long., 22 m depth. USNM523166, SB95±11, San October 1998, H. Fortunato coll., 9.23Њ Lat., 81.88Њ Long., 50 m Blas; October 1995, H. Fortunato coll., 9.50Њ Lat., 78.92Њ Long., depth, coarse sandy mud. Paratypes, USNM523159, BT98±36, 40 m depth, black sandy mud. Bocas del Toro; October 1998, H. Fortunato coll., 9.23Њ Lat., Measurements.See Table 6 for morphological measurements. 81.88Њ Long., 50 m depth, coarse sandy mud. USNM523160, Occurrence.Throughout the wider Caribbean from Florida to SB95±20, San Blas; October 1995, H. Fortunato coll., 9.62Њ Lat., Guyana. 78.99Њ Long., 70 m depth, coarse sand. Measurements.See Table 6 for morphological measurements. CUPULADRIA CHEETHAMI new species Occurrence.From the western San Blas archipelago to Bocas Figure 7 del Toro. Diagnosis.The autozooids as well as the vicarious avicularia CUPULADRIA INCOGNITA new species are long and slender. The autozooids and vicarious avicularia in Figure 5 the central area of the colony lack secondary calci®cation. Diagnosis.The colony has a height-diameter ratio of about Description. The zoarium has a height-diameter ratio of about 0.5, also with vicarious avicularia occupying the central area. 0.25 with a maximum observed diameter of 9.1 mm. The central Description.The zoarium is cone-shaped, with a maximum area of the colony is formed mostly by autozooids; the cryptocyst observed diameter of 6.8 mm. As in Cupuladria multesima n. sp., of these autozooids and vicarious avicularia are not thickened by the entire central area of the colony consists of vicarious avicu- secondary calci®cation. The vicarious avicularia are frequent and laria up to the fourth or ®fth astogenetic generation. The auto- scattered throughout the zone of astogenetic change. The auto- zooids have a hexagonal shape and are wider than long. The ope- zooids are hexagonal in shape, and both the autozooids and vicar- sia narrows in the middle. The basal sectors are radial and ious avicularia are markedly longer than wide. The basal sectors rectangular, but sometimes irregular, in shape with 12±16 pores are rectangular with three to six pores per sector, similar, to C. per basal sector (irregular sectors with three to ®ve pores). The biporosa. The colony wall has in transversal section a maximum colony wall has in transversal section a maximum width of 0.70 width of 0.34 mm, with one to two layers of basal kenozooecial mm, with three to four layers of basal kenozooecial chambers chambers (max. diam. 0.06 mm). (max. diam. 0.10 mm). Etymology.The name cheethami is in honor of Dr. Alan Etymology.The name incognita is from Latin for ``unrecog- Cheetham, bryozoologist extraordinaire. nized, unexamined,'' since it has not been described before. Types.Holotype, USNM523167, LC98±13, Laguna de Chi- Types.Holotype, USNM523161, BT98±5, Bocas del Toro; riqui, Bocas del Toro; October 1998, H. Fortunato coll., 9.13Њ October 1998, H. Fortunato coll., 9.51Њ Lat., 82.33Њ Long., 100 Lat., 82.22Њ Long., 20 m depth. Paratypes, USNM523168, m depth, black, ®ne, sandy mud. Paratypes, USNM523162, USNM523169, LC98±13, Laguna de Chiriqui, Bocas del Toro; BT98±5, Bocas del Toro; October 1998, H. Fortunato coll., 9.51Њ October 1998, H. Fortunato coll., 9.13Њ Lat., 82.22Њ Long., 20 m Lat., 82.33Њ Long., 100 m depth, black ®ne sandy mud. depth. USNM523163, BA98±125; Bahia Almirante, Bocas del Toro, Oc- Measurements.See Table 6 for morphological measurements. tober 1998, H. Fortunato coll., 9.42Њ Lat., 82.34Њ Long., 23 m Occurrence.From the Caribbean coast of Panama in the Gulf depth, greenish smelly mud. of San Blas in the east, and Laguna de Chiriqui (Bocas del Toro) Measurements.See Table 6 for morphological measurements. in the west. HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 257
FIGURE 8ÐCupuladria paci®ciensis n. sp. 1±5, USNM523170, Gulf of Chiriqui; 1, colony, bar scale ϭ 1 mm; 2, ancestrula, autozooids, and vicarious avicularia in the central area of the colony; 3, autozooid and autozooid vibracula; 4, vicarious avicularia and vicarious avicularia vibracula; 5, basal sectors; 6, USNM523172, Gulf of Panama, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony up). 2±6 bar scales ϭ 100 m.
CUPULADRIA PACIFICIENSIS new species Description.The zoarium has a height-diameter ratio of about Figure 8 0.25, with a maximum observed diameter of 6.3 mm. The central area of the colony is formed mostly by autozooids, and the cryp- Cupuladria canariensis OSBURN, 1950, p. 33, pl. 3, ®gs. 2, 3 (in part?). tocyst of these autozooids and vicarious avicularia are not thick- Diagnosis.Small autozooids 0.44 mm in average (Table 6), ened by secondary calci®cation. The vicarious avicularia are fre- the ones in the central area of the colony lack secondary calci®- quent and scattered throughout the zone of astogenetic change. cation. The autozooids are hexagonal in shape and approximately as wide 258 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
FIGURE 9ÐCupuladria exfragminis n. sp. 1±5, USNM523173, Gulf of Chiriqui; 1, colony, bar scale ϭ 1 mm; 2, area of fragmentation/regeneration; 3, autozooid and autozooid vibracula; 4, vicarious avicularia and vicarious avicularia vibracula; 5, basal sectors; 6, USNM523175, Gulf of Chiriqui, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony up). 2±6 bar scales ϭ 100 m. as long. The basal sectors are rectangular with four to six pores depth, ®ne mud. Paratypes, USNM523171, GC97±65, Gulf of per sector. The colony wall has in transversal section a maximum Chiriqui; March 1997, H. Fortunato coll., 7.18Њ Lat., 81.67Њ width of 0.44 mm, with one to two layers of basal kenozooecial Long., 142 m depth, ®ne mud. USNM523172, GP97±1 1/8(1) chambers (max. diam. 0.10 mm). dredge, Gulf of Panama; February 1997, H. Fortunato coll., 8.60Њ Etymology.The name paci®ciensis refers to the Paci®c Lat., 78.58Њ Long., 6 m depth, black ®ne mud. Ocean, where it was found. Measurements.See Table 6 for morphological measurements. Types.Holotype, USNM523170, GC97±65, Gulf of Chiriqui; Occurrence.Off the Paci®c coast of Panama, in the Gulf of March 1997, H. Fortunato coll., 7.18Њ Lat., 81.67Њ Long., 142 m Panama and the Gulf of Chiriqui. HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 259
FIGURE 10ÐCupuladria surinamensis CadeÂe, 1975. 1, 2, USNM523177, San Blas; 1, colony, bar scale ϭ 1 mm; 2, ancestrula and autozooids in the central area of the colony; 3, 5, USNM523176, Bocas del Toro; 3, autozooid and autozooid vibracula; 4, USNM523178 San Blas, basal radial sectors; 5, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony down). 2±5 bar scales ϭ 100 m.
CUPULADRIA EXFRAGMINIS new species Description.All colonies examined originated from fragments. Figure 9 The zoarium has an irregular cone shape and a height-diameter ratio of about 0.2, with a maximum observed diameter of 9.3 mm. Cupuladria canariensis OSBURN, 1950, p. 33, pl. 3, ®gs. 2, 3 (in part?). The vicarious avicularia are frequent and scattered throughout the Diagnosis.Small autozooids 0.42 mm in average (Table 6), zone of astogenetic change. The autozooids are hexagonal in shape has the largest ratio of autozooid vibracula length-autozooid and approximately as wide as long. The basal sectors are rectan- length. gular with four to six pores per sector. The colony wall has in 260 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
FIGURE 11ÐCupuladria panamensis n. sp., USNM523180, Gulf of Mosquitos, Bocas del Toro; 1, colony, bar scale ϭ 1 mm; 2, ancestrula and autozooids in the central area of the colony; 3, autozooid and autozooid vibracula; 4, basal radial sectors; 5, transversal cut of the colony, showing kenozooidal chambers (basal side of the colony down). 2±5 bar scales ϭ 100 m.
transversal section a maximum width of 0.47 mm, with one to two depth, soft black mud with wooden remains. Paratypes, layers of basal kenozooecial chambers (max. diam. 0.10 mm). USNM523174, USNM523175, GC97±24, Gulf of Chiriqui; Etymology.The name exfragminis, Latin, for ``from frag- March 1997, H. Fortunato coll., 8.5Њ Lat., 79.75Њ Long., 10.6 m ments,'' with reference to the origin from fragments of all the depth, soft black mud with wooden remains. colonies examined. Measurements.See Table 6 for morphological measurements. Types.Holotype, USNM523173, GC97±24, Gulf of Chiriqui; Occurrence.Off the Paci®c coast of Panama, in the Gulf of March 1997, H. Fortunato coll., 8.5Њ Lat., 79.75Њ Long., 10.6 m Panama and the Gulf of Chiriqui. HERRERA-CUBILLA ET AL.ÐTAXONOMY OF RECENT CUPULADRIA FROM PANAMA 261
Discussion.Both C. paci®ciensis n. sp. and C. exfragminis Colony ¯atter; height/diameter ratio around 0.4 (range 0.2±0.5); have smaller autozooids than C. biporosa, but C. exfragminis has cryptocyst narrower ...... C. surinamensis the largest ratio of autozooid vibracula length-autozooid length. 3) Central area of the colony completely formed by vicarious avicu- laria ...... 4 CUPULADRIA SURINAMENSIS CadeÂe, 1975 Central area of the colony formed mostly by autozooids ...... 5 Figure 10 4) Colony a high dome; mean height/diameter ratio 0.6 (range 0.3± 0.8); mean zooarium diameter 3.6 mm (range 3±4 mm) 5±6 layers Cupuladria surinamensis CADEÂ E, 1975, p. 325, pls. 1, 2, 3c. of basal kenozooids ...... C. multesima n. sp. Cupuladria canariensis surinamensis CADEÂ E, 1979, p. 446, ®gs. 1h, 2c. Colony ¯atter, variable; mean height/diameter ratio 0.5 (range 0.3± 0.8); mean zooarium diameter 4.6 mm (range 3±7 mm) 3±4 layers Description.The zoarium has a height-diameter ratio of about of basal kenozooids ...... C. incognita n. sp. 0.3, with a maximum observed diameter of 9.6 mm. The central 5) Autozooids and vicarious avicularia longer in relation to width; more streamlined, autozooids more than 0.5 mm in length (range area of the colony is formed exclusively by autozooids. The vi- 0.5±0.6 mm) ...... C. cheethami n. sp. carious avicularia are absent. The autozooids have a hexagonal Autozooids and vicarious avicularia approximately as wide as long; shape as wide as long and are bigger than all the Cupuladria autozooids less than 0.5 mm in length (range 0.4±0.5 mm) .... 6 species examined here, except for C. cheethami n. sp. (Table 6). 6) Ratio autozooid vibracula length-autozooid length Ͼ 0.5...... The cryptocyst is narrower than in C. panamensis n. sp. The basal ...... C. exfragminis n. sp. sectors are radial with 14±24 pores per sector. The colony wall Ratio autozooid vibracula length-autozooid length Ͻ 0.5 ...... 7 has in transversal section a maximum width of 0.57 mm, with 7) Autozooids and vicarious avicularia in the central area of the col- one layer of basal kenozooecial chambers (max. diam. 0.16 mm). ony are thickened by secondary calci®cation ...... C. biporosa Material examined.USNM523176, BA98±119, Bahia Almi- Autozooids and vicarious avicularia in the central area of the col- Њ ony are not thickened by secondary calci®cation ...... rante, Bocas del Toro; October 1998, H. Fortunato coll., 9.33 ...... C. paci®ciensis n. sp. Lat., 82.31Њ Long., 21 m depth, greenish smelly mud. USNM523177, USNM523178, SB95±4; October 1995, H. For- ACKNOWLEDGMENTS tunato coll., 9.57Њ Lat., 78.56Њ Long., 95 m depth. USNM523179, SB95±9, San Blas; October 1995, H. Fortunato coll., 9.52Њ Lat., H. Fortunato directed the dredging program that produced all 78.74Њ Long., 67 m depth, brown sandy mud. the specimens. The captain and crew of the R/V Urraca provided Measurements.See Table 6 for morphological measurements. logistical support. F. Rodriguez processed all the samples, picked Occurrence.Throughout the Caribbean from Florida to Guy- out the bryozoans, and helped to develop the modeling procedure ana. for estimating colony characters values for the VOUCHER spec- imens. A. O'Dea developed the method for calculation of the CUPULADRIA PANAMENSIS new species index of calci®cation of colonies and helped prepare Figure 1. A. Figure 11 Cheetham provided his customary insight and wisdom about Diagnosis.The zoarium is dome-shaped (high narrow), the bryozoans as well as critically reviewed the manuscript. S. Lao autozooids are bigger and have a wider cryptocyst than C. suri- geographically referred the distribution of the survey species. To namensis. all we are very grateful. Financial support was provided by the Description.The zoarium is dome shaped (high narrow), and Walcott Studies Grant to JBCJ and the NSF Grant EAR03±45471 has a height-diameter ratio of about 0.6, with a maximum ob- to JBCJ. served diameter of 8.8 mm. The central area of the colony is formed exclusively of autozooids. The vicarious avicularia are REFERENCES absent. The autozooids are hexagonal as wide as long. The cryp- BALUK,W.,AND A. RADWANSKI. 1984. Middle Miocene (Badenian) free tocyst is wide. The basal sectors are radial with 8±23 pores. The living Bryozoan from the Vienna Basin. Annalen Naturhistorisches colony wall has also in transversal section a maximum width of Museum Wien, 86A:13±40. 0.57 mm, with only one layer of basal kenozooecial chambers BOARDMAN, R. S., A. H. CHEETAM, AND P. L. COOK. 1970. Intracolony (max. diam. 0.2 mm). variation and the genus concept in Bryozoa. Proceedings of the North Etymology.The name panamensis refers to the Isthmus of American Paleontological Convention September 1969, Pt. C, p. 294± Panama, where it was found. 320. Types.Holotype, USNM523180, GM98±78, Gulf of Mosqui- BROWN, J. H., AND M. V. LOMOLINO. 1998. Biogeography (second edi- tion). Sinauer Associates, Inc., Sunderland, Massachusetts, 692 p. tos, Bocas del Toro; September 1998, H. Fortunato coll., 9.48Њ Њ BUDD, A. F., K. G. JOHNSON, AND D. C. POTTS. 1994. Recognizing mor- Lat., 80 Long., 79 m depth. Paratypes, USNM523181, GM98± phospecies in colonial reef corals: 1, Landmark-based methods. Paleo- 78, Gulf of Mosquitos, Bocas del Toro; September 1998, H. For- biology, 20:484±505. tunato coll., 9.48Њ Lat., 80Њ Long., 79 m depth. USNM523182, BUSK, G. 1852. Catalogue of Marine Polyzoa in the Collection of the GM98±90, Gulf of Mosquitos, Bocas del Toro; September 1998, British Museum, Pt. 1. British Museum, London, 54 p. H. 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Bulletin de la SocieÂteÂGeÂologique de France, series 4, 14:465± KEY TO SPECIES 474, pls. 14, 15. 1) Vicarious avicularia absent...... 2 CANU,F.,AND R. S. BASSLER. 1919. Fossil Bryozoa from the West In- Vicarious avicularia present ...... 3 dies. Contributions to the Geology and Paleontology of the West Indies. 2) Colony a high dome; height/diameter ratio around 0.6 (range 0.4± Publication of the Carnegie Institution of Washington, No. 291:73±102. 0.9); cryptocyst wider ...... C. panamensis n. sp. CANU,F.,AND R. S. BASSLER. 1923. North American Later Tertiary and 262 JOURNAL OF PALEONTOLOGY, V. 80, NO. 2, 2006
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APPENDIXÐAbsolute rank of the standardized canonical discriminant function coef®cients from the discrimination of SURVEY colonies of Cupuladria. All characters were transformed like this: log10 (1 ϩ variable), see Methods, and refer to Table 1 for character names. Values in bold indicate characters with highest coef®cients. Missing values indicate characters that were not used in the calculations or that were not present in the colonies.
VA group NVA group Morphological characters DF(1) Absolute rank DF(2) Absolute rank DF(3) Absolute rank DF(1) Absolute rank Cw 0.34 25 2.09 15 0.02 28 0.16 14 Ch Ϫ0.41 23 Ϫ5.11 7 1.36 19 Ϫ0.92 9 Rahw 1.42 9 6.01 4 Ϫ1.62 18 Ϫ0.97 8 Ci Ϫ0.92 15 Ϫ0.82 21 0.87 20 0.44 10 RaZV Ϫ1.36 11 0.94 20 Ϫ0.09 26 Ϫ0.23 13 Zl Ϫ0.54 22 Ϫ8.33 1 Ϫ13.91 1 Ϫ2.44 3 Zw Ϫ2.89 5 Ϫ2.87 13 13.18 2 6.40 1 Ol 0.85 17 2.38 14 8.60 3 1.87 6 Ow 2.76 6 5.40 6 Ϫ5.58 8 Ϫ4.18 2 Al Ϫ0.31 26 7.21 3 5.38 9 0.10 15 Aw Ϫ0.84 19 Ϫ4.29 10 Ϫ8.41 4 Ϫ2.08 5 RaAlZl 0.85 18 Ϫ8.19 2 Ϫ6.27 7 0.25 12 RaAwZw 0.97 14 4.62 8 7.81 5 0.50 10 RaOlZl Ϫ0.71 20 Ϫ1.06 18 Ϫ7.32 6 Ð Ð RaOwZw Ϫ2.80 7 Ϫ5.52 5 5.10 10 2.16 4 NV Ϫ0.25 27 1.64 16 Ϫ0.19 23 Ð Ð Vl 3.69 2 Ϫ1.18 17 0.22 22 Ð Ð Vw 3.63 3 Ϫ4.33 9 Ϫ4.0 13 Ð Ð VOl 0.91 16 1.05 19 1.87 17 Ð Ð VOw Ϫ1.30 12 3.73 12 4.52 12 Ð Ð VAl Ϫ5.11 1 0.20 26 Ϫ2.97 14 Ð Ð VAw Ϫ1.64 8 Ϫ0.29 25 0.11 25 Ð Ð RaVAlVl 3.27 4 Ϫ0.29 24 1.94 16 Ð Ð RaVAwVw 1.40 10 Ϫ0.35 23 0.39 21 Ð Ð RaVOlVl Ϫ0.62 21 Ϫ0.79 22 Ϫ2.58 15 Ð Ð RaVOwVw 1.21 13 Ϫ4.03 11 Ϫ4.80 11 Ð Ð Asec 0.04 28 Ϫ0.14 27 Ϫ0.14 24 Ϫ0.40 16 Psec 0.35 24 0.11 28 0.04 27 1.02 7