Cenozoic Diversification and Extinction Patterns in Caribbean Reef Corals a Review
Sci Adv. 2018 Apr; iv(four): eaaq1508.
Differences in extinction rates drove modern biogeographic patterns of tropical marine biodiversity
Emanuela Di Martino
1Department of Globe Sciences, Natural History Museum, Cromwell Route, SW7 5BD London, UK.
Jeremy B. C. Jackson
twoDepartment of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013–7012, United states.
Paul D. Taylor
iDepartment of Earth Sciences, Natural History Museum, Cromwell Route, SW7 5BD London, United kingdom.
Kenneth G. Johnson
iDepartment of Earth Sciences, Natural History Museum, Cromwell Route, SW7 5BD London, United kingdom of great britain and northern ireland.
Received 2017 Oct vi; Accepted 2018 Feb fifteen.
- Supplementary Materials
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http://advances.sciencemag.org/cgi/content/total/four/iv/eaaq1508/DC1
GUID: CA1F4560-B854-4857-B468-B23C77490D93
GUID: 8FDD9148-B6D1-4709-B8D7-0F6457E272CF
GUID: 6A07CA63-FE1B-40F5-9454-45207A917A65
Supplementary fabric for this commodity is available at http://advances.sciencemag.org/cgi/content/total/4/4/eaaq1508/DC1
fig. S1. Diversity of Caribbean cheilostome bryozoan species for iv time intervals from the early Miocene to the Pleistocene.
fig. S2. Stratigraphic ranges of the 285 Neogene Caribbean cheilostome bryozoan species included in our information sets.
data gear up S1. Diversity and abundance of cheilostome bryozoans in the Miocene Chipola Formation and the DR.
information ready S2. TU and DR Miocene samples.
data set S3. Diversity and abundance of cheilostome bryozoans in the Miocene of Panama.
data set S4. PPP Miocene samples.
data set S5. Diversity and affluence of cheilostome bryozoans in the Pliocene of Panama.
data set up S6. PPP Pliocene samples.
data set S7. Diversity and abundance of cheilostome bryozoans in the Pleistocene of Panama.
data fix S8. PPP Pleistocene samples.
information set S9. Multifariousness and abundance of cheilostome bryozoans in the Miocene of East Kalimantan, Indonesia.
data set S10. Miocene samples from East Kalimantan.
data set up S11. Extant species.
Abstract
Marine biodiversity in the Coral Triangle is several times higher than anywhere else, only why this is true is unknown because of poor historical information. To accost this, we compared the first bachelor record of fossil cheilostome bryozoans from Indonesia with the previously sampled splendid record from the Caribbean. These ii regions differ several-fold in species richness today, but cheilostome multifariousness was strikingly similar until the end of the Miocene five.3 1000000 years ago so that the modern disparity must have developed more recently. However, the Miocene faunas were ecologically very different, with a greater proportion of erect and free-living species in the Caribbean area compared to the less well-known Coral Triangle. Our results back up the hypothesis that modern differences in diversity arose primarily from differential extinction of Caribbean cock and gratis-living species concomitant with oceanographic changes due to the uplift of the Isthmus of Panama, rather than exceptional rates of diversification in the Indo-Pacific.
INTRODUCTION
Marine species richness in the Coral Triangle region of Southeast Asia, commonly referred to equally the Coral Triangle, is ii to several times greater than in the tropical western Atlantic (1). Almost well-studied marine groups exhibit the same pattern. The greatest reported differences are for reef fishes (3689 versus 891 species) (2); reef corals (627 versus 73 species) (3); and coral reef–associated crustaceans, which are about x times more diverse in the Indo-Due west Pacific than in the Caribbean (four). The same pattern applies to bivalves and gastropods (v), and larger benthic foraminifera (6). A like multifariousness contrast has been suggested for less well-studied cheilostome bryozoans. More than 500 species take been reported from Republic of indonesia (vii), and more than 300 from the Philippines (8), whereas only 221 and 232 species are estimated to be nowadays in the Recent cheilostome fauna of the Caribbean (nine) and the Gulf of United mexican states (10), respectively. The data are based on extensive regional surveys in both regions but almost certainly underestimate total regional diversity considering they are based on old taxonomy. More disquisitional recent morphometric and genetic analyses of a limited number of Caribbean genera take revealed numerous complexes of cryptic species (11), and the same is likely for the Indo-W Pacific (12).
When and why these hit differences arose and how they have been maintained are controversial questions. Biologists have long invoked v conflicting theoretical mechanisms equally explanatory models of high Coral Triangle diversity, variously viewing the region as a (i) center of origin, (2) eye of overlap, (iii) middle of accumulation, (iv) centre of survival, or (v) centre of mid-domain overlap (xiii). Depending on the target group investigated and whether or not both fossil and nowadays-day data are analyzed, results are more consistent with different mechanisms, suggesting that a single theory solitary is inadequate to explain the high diversity in the region (13, xiv).
Fourth dimension-calibrated molecular phylogenies for reef-associated tetraodontiform fishes (15) and gastropods (16) suggest that their main species diversification in the Coral Triangle region occurred around xx to 25 million years (Ma) agone. Withal, the paleontological record has been too trivial studied, and there are no comparative information for fossil species to provide a definitive quantitative test (17). In contrast, the Caribbean is besides a major middle of Cenozoic tropical marine biodiversity with extensive paleontological data on species richness of corals, mollusks, bryozoans, and foraminifera from the Oligocene to today (eighteen). Variety in most groups has generally increased over the past 25 Ma until a regional mass extinction about 2 Ma ago (nineteen, twenty).
Although still limited, we now accept some comparative paleontological data from Indonesia to compare with the splendid Caribbean record. A detailed report of Miocene corals from Indonesia demonstrated species richness of about 100 species for each stage of the Miocene, which is but about 25% greater than contemporaneous faunas from the Caribbean (nineteen). In addition, preliminary analyses of ostracods from the tropical western Pacific showed that species richness has increased over the by 25 Ma, with a big jump to approximately modern values beginning nearly 5 Ma ago (21). However, comparable data for Caribbean ostracods are sparse.
Nosotros used all-encompassing paleontological collections of Caribbean and Indonesian cheilostome bryozoans (22) to address the timing of the divergence in species richness betwixt the two regions and to evaluate the relative contributions of differential rates of origination and extinction to the patterns nosotros notice today. Cheilostome bryozoans offer a model organisation because they are arable, small-scale, and well-preserved components of Cenozoic tropical shelf sediments (23). Moreover, their skeletal complication provides a wealth of morphological characters enabling a precise species-level taxonomy (24), whereas variations in their life history and ecology are readily apparent from differences in colony course. Caribbean area faunas are well documented from the early on Miocene (approximately eighteen Ma ago) to the Contempo in Florida, the Dominican Republic (DR), and Panama (25, 26). Indonesian collections are from East Kalimantan and extend from 17.5 to 5.3 Ma ago (22). The fossil samples analyzed are provisionally assumed to be representative of the two regions every bit a whole. We reanalyzed all available fossil collections to develop a new, taxonomically standardized Caribbean database to compare with the Indonesian fabric (data sets S1 to S11).
RESULTS
Cheilostome origination and extinction in the Caribbean
Caribbean cheilostome species richness increased nearly threefold from the early on to the center-belatedly Miocene (18.3 to five.three Ma ago) and changed piddling afterward (Fig. 1 and fig. S1). The generally strong agreement between the observed and estimated patterns of variety suggests that these patterns are highly robust. Notwithstanding, trends in diversity for iii major categories of colony course—encrusting, cock, and free-living—are strikingly different. Encrusting species diversity increases throughout the time series. In contrast, erect and free-living species diverseness increased from the early to middle-late Miocene (18.three to 5.iii Ma ago) just after declined steadily. These patterns become even more striking when categories of colony grade are expressed as percentages of the entire fauna within each time interval (Fig. 2). The proportions remained stable until five.3 Ma ago when erect species precipitously declined, whereas free-living species peaked before declining over the by ii Ma in favor of encrusting species.
Changes in Caribbean cheilostome species richness over the by 18 Ma.
Observed counts (black squares), Chao2 estimates (blue triangles), and resampled estimates (greenish dots) of cheilostome species diversity over geological fourth dimension for all colony growth forms combined and for encrusting, erect, and free-living only.
Neogene-Recent histories of Caribbean cheilostome bryozoan colony growth forms.
Results are shown as proportional abundances. "Recent" refers to the proportions of species present in our fossil data sets that are notwithstanding living today.
Encrusting colony forms make up the largest proportion (80%) of the 124 extant species in our fossil data set that are still extant. Only twenty% of the 42 erect and 15 free-living species in the data prepare are still living today, confirming earlier results based on less complete data (27–29). Loftier rates of extinction of erect species are epitomized past the genus Metrarabdotos, with only ii of xiv species recorded in our data prepare extant (30), and for free-living species by the genus Discoporella, with three of xi species still extant (29).
Patterns of diversity change were examined by counting the numbers of species inside each 1-Ma time interval. The results signal significant species origination at 18.three Ma ago (Fig. 3). The Chipola Formation contains the oldest occurrences for all the cheilostome bryozoan species recorded in its fauna with the sole exception of Nellia tenella, which first appeared seventy to 65 Ma agone and has been considered a "living fossil." 30 of the 54 first occurrences were restricted to the Chipola Formation, and their subsequent demise produced the first tiptop of extinction at 18 Ma ago. The remaining 24 species were also found in younger units, with the bulk extant (fig. S2). Diversification peaked effectually 7 Ma agone and afterwards effectually four Ma ago.
Measures of cheilostome taxonomic turnover and sampling intensity in the Caribbean for 1-Ma time intervals for the by xviii Ma.
(A) Range-through species richness (in green, the number of species effectively constitute in each 1-Ma time interval) and numbers of samples, (B) numbers of beginning and last occurrences in each sampled million year interval, (C) origination, and (D) extinction rates per colony growth form (black, encrusting; red, erect; bluish, gratuitous-living) per million year subinterval.
Patterns of extinction show two clear peaks at 5 Ma ago (Miocene-Pliocene boundary) and 2 to 1 Ma ago, driven mainly by erect and gratis-living taxa. The majority of species responsible for the extinction peak at v Ma ranges dorsum to xviii to xv Ma ago, whereas the two-Ma extinction peak is caused by the disappearance of species that range back to 10 to viii Ma agone.
Comparing of Caribbean and Indonesian diversity
Cheilostome species richness, which is dominated by encrusting species, is similar in the ii regions over the range represented by the Indonesian collections, which cover the heart-belatedly Miocene (xvi to v Ma ago) (Fig. 4). Although there are fewer species in the Indonesian collections than in the Caribbean (107 and 151 species, respectively) due to less intensive sampling (65 collections versus 111 collections), estimates of diversity based on Chao2 and resampling are non significantly dissimilar. This effect is further supported by the like shapes of the private-based cumulative collecting curves for the two regions being compared, which advise that the differences in total numbers of cheilostome species reverberate real differences in truthful variety (Fig. 5).
Observed, Chao2, and resampled estimated measures of cheilostome species diversity in the middle-tardily Miocene (sixteen to 5 Ma ago) in Republic of indonesia (IND) and the Caribbean area (CAR).
Results are presented for all colony growth forms combined and for encrusting, erect, and free-living only.
Diversity of cheilostome bryozoan species for the middle-late Miocene for Indonesia and the Caribbean area.
Cumulative drove curves are for the middle-late Miocene for all colony growth forms combined and for encrusting, erect, and gratuitous-living just.
In add-on to gauge of regional diversities determined by pooling samples together and bold them to exist representative of the two regions every bit a whole, we besides calculated species richness for each site. In Indonesia, local species richness ranges from 1 to 32 (median, 7.5; mean, 9); no pattern of distribution can be recognized according to facies type, surroundings, or age of the sample (22). In the Caribbean, local species richness ranges from 1 to 44 (median, 18; mean, xviii.half dozen), with the variability in credible diversity partly a role of preservation (25). These differences are statistically significant (t test, P = 6.213 × ten−xiv).
The two faunas are ecologically very different because of the greater proportion of cock (28% versus 24%) and free-living (12% versus 5%) species in the Caribbean compared to Indonesia. Equally it is apparent from the shapes of the cumulative collecting curves (Fig. 5), not all the growth forms are sampled with the same completeness. All the collecting curves for the Caribbean level out, suggesting that the sampling is saturated, whereas collecting curves for Indonesia differ greatly depending on the colony form. The collecting bend for erect species rises steeply before leveling out, the collecting curve for encrusting species shows a slight trend toward flattening, simply the collecting curve for free-living species suggests that the sampling was non saturated.
DISCUSSION
The similarity in Indonesian and Caribbean Miocene cheilostome multifariousness is statistically robust despite differences in the mode and density of sampling, the latter being far more express in Indonesia. Thus, the mod differences in cheilostome variety must have arisen within just the last 5 Ma. New collections from the Coral Triangle are needed to determine when the regional differences arose. Notwithstanding, our results clearly negate the hypothesis that high cheilostome diversity in the Coral Triangle today is the result of exceptionally high diversification over tens of millions of years (31).
The newly integrated Caribbean tape too demonstrates that Caribbean cheilostome diversity increased throughout the Miocene until stalling in the Pliocene due to mass extinction of cock and costless-living species associated with the collapse in Caribbean planktonic productivity following the final closure of the Central American Seaway (32). Full cheilostome diversity did non reject, nevertheless, because of the continued diversification of encrusting species that make up most of the faunas in both regions. Caribbean extinction exhibited two peaks at the start of the Pliocene and Pleistocene epochs roughly 5 and 2 Ma ago. The Pliocene extinction is confounded with a shift in the primary sampling locations from the DR in the Miocene to Panama in the Pliocene, but the records of uncommonly well-studied genera with collections from throughout the Caribbean propose that the pattern is robust (27, 30).
The Caribbean extinction of erect and free-living cheilostomes coincided with the closure of the Isthmus of Panama. Morphological evidence for clonal propagation strongly supports the hypothesis of a causal mechanism between the extinction of free-living species and the collapse in main productivity due to oceanographic changes (29, 33). The uncommonly low affluence and diversity of Indonesian erect and free-living species is a mystery, particularly because these colony forms are generally more robust, better preserved, more conspicuous, and therefore more probable to attract attention than frail, generally smaller, and hands disregarded encrusting species (34). However, in terms of the proportions of species classified co-ordinate to major colony forms, the Indonesian diversity in the middle-late Miocene reflects modernistic tropical bryozoan faunas, which, on average, incorporate 78% of encrusting species, 19% of erect species, and 3% of costless-living species (34). Cryptic encrusters are the most common bryozoans in modern tropical reefs pantropically.
The history of cheilostome diversity in the Caribbean is very similar to that of reef corals, mollusks, and fishes in that progressively higher diversity was halted, and in the case of corals reversed, from about 5 to 2 Ma ago (35). Similar mass extinction of highly diverse coral and cheilostome faunas occurred approximately 6 Ma ago when the Mediterranean was isolated from the Atlantic during the Messinian salinity crisis from which variety never fully recovered. Nosotros conclude that the infrequent diverseness of the Coral Triangle today reflects the absence of mass extinction as much equally any exceptional rates of diversification compared to more peripheral regions.
MATERIALS AND METHODS
Cheilostome bryozoans from standardized majority sediment samples in existing museum collections were used to determine species diversity from Indonesia and the Caribbean area. Collections from Indonesia are from East Kalimantan and are housed at the Natural History Museum, London (NHMUK). Collections from the Caribbean area include (i) early Miocene samples from the Chipola Formation in Florida, deposited at the Florida Museum of Natural History (FLMNH) in Gainesville; (ii) middle-late Miocene samples from the Baitoa, Gurabo, and Cercado formations in the DR and the Gatun Formation in Panama; and (iii) Pliocene and Pleistocene samples from several formations in the Bocas del Toro and Limon basins in Panama. All the DR and Panama specimens are housed at the National Museum of Natural History (NMNH), Smithsonian Institution, Washington, DC.
To sympathize the furnishings of sampling on diversity estimates, nosotros compared observed richness with Chao2 multifariousness and resampled richness (Figs. i and 4). Chao2 is a nonparametric estimator of the number of undetected species calculated by calculation a correction factor to the observed species richness that corresponds to the square of the number of uniques (species occurring in one sample) divided by two times the number of duplicates (species occurring in two samples), with 95% confidence interval (36, 37). This figurer is based on incidence data and provides a nonparametric lower leap of true species richness nether the assumption of homogeneity among samples. Resampled-based species richness was estimated by private-based collecting curves every bit the median of 100 random draws of taxon occurrences without replacement (Fig. v and fig. S1). This approach attempts to normalize variation in sampling completeness between the two sets of collections by drawing random subsamples to reduce the number of samples considered in each set of collections. A randomization distribution of species richness for each prepare of collections is obtained by repeated resampling followed by counting the number of species in each selection of samples (nineteen). Confidence intervals are provided past the 5th and 95th percentiles of permutation distributions.
To compare regional diverseness of the Caribbean during the Neogene, we divided the information set up into four intervals with a like sample size: early on Miocene, eye-late Miocene, Pliocene, and Pleistocene. The Indonesian data prepare is limited to a unmarried interval, the heart-tardily Miocene, so it is for the comparison with the Caribbean area. Ages of localities were taken from several sources (22, 25, 26).
Collections used for the comparison of the two regions are from a similar range of habitats including shallow nearshore environments with seagrass meadows and patch reefs (inferred paleodepth of <five m) to deeper shelf border reefs (inferred paleodepth of 60 to 100 m) (38, 39). In both regions, samples are from a single sedimentary basin. DR collections are from sites little more than 100 km across in the Cibao region of the northern DR (25). Indonesian collections are from sites extending most 200 km across in the Kutai Basin (22).
Stratigraphic ranges of each taxon were estimated as extending from the lower boundary of the age of the sample in which the taxon first occurred to the upper boundary of the age assigned to the sample in which the taxon last occurred (fig. S2). Taxonomic turnover was estimated within a set of stratigraphic intervals that were one Ma in duration (Fig. three). Per-interval richness was estimated both by the number of species that occurred in each bin and by counting range-through taxa that were not recovered from the bin but occurred in both earlier and after bins. Numbers of species that showtime or last occurred in each bin were counted and divided by full within-bin richness to produce rates of origination and extinction.
Diverseness and taxonomic turnover were estimated for the full fauna and also after dividing the assemblages into iii major colony growth forms following the study of Cheetham et al. (25): encrusting, erect, and free-living. Affluence of individuals was measured equally minimum numbers on an gauge scale that codes the number of specimens in each species in a drove as one for one to ix specimens, 10 for 10 to 99 specimens, and 100 for 100 or more than specimens. All analyses were conducted in R Statistical Environment (forty). All faunal data sets necessary for reproducing figures are available in the Supplementary Materials.
Supplementary Material
http://advances.sciencemag.org/cgi/content/full/4/4/eaaq1508/DC1:
Acknowledgments
We thank R. Portell (FLMNH) and J. Sanner (NMNH) for providing access to the fossil bryozoan collections in their care. This work is funded by a Leverhulme Trust Research Project Grant (RPG-2015-036: Origin of loftier tropical diversity: A test using bryozoans). Collections from Indonesia were made as office of the Throughflow Project, a Marie Curie Initial Training Network supported under Framework Package 7 of the European Spousal relationship. Author contributions: Due east.D.M., J.B.C.J., and P.D.T. conceived, designed, and coordinated the study; E.D.Thou. identified and revised the cheilostome bryozoan faunas, built the data sets, and drafted the manuscript; One thousand.G.J. carried out the statistical analyses. All authors discussed results and interpretations, commented on the drafts of the manuscript, and gave terminal approval for publication. Competing interests: The authors declare that they accept no competing interests. Data and materials availability: All data sets are provided with the Supplementary Materials and published on the NHMUK data portal. All the East Kalimantan material is housed in the fossil collections of the NHMUK; the DR and Panama Paleontology Projection textile is housed in the collection of the Department of Paleobiology at NMNH; Chipola material is housed in the collections of the FLMNH.
SUPPLEMENTARY MATERIALS
Supplementary material for this commodity is available at http://advances.sciencemag.org/cgi/content/total/4/iv/eaaq1508/DC1
fig. S1. Diversity of Caribbean cheilostome bryozoan species for four time intervals from the early Miocene to the Pleistocene.
fig. S2. Stratigraphic ranges of the 285 Neogene Caribbean cheilostome bryozoan species included in our data sets.
data fix S1. Diversity and abundance of cheilostome bryozoans in the Miocene Chipola Formation and the DR.
data set S2. TU and DR Miocene samples.
data set S3. Variety and abundance of cheilostome bryozoans in the Miocene of Panama.
information set S4. PPP Miocene samples.
data set S5. Multifariousness and abundance of cheilostome bryozoans in the Pliocene of Panama.
data set S6. PPP Pliocene samples.
data set S7. Diversity and abundance of cheilostome bryozoans in the Pleistocene of Panama.
information set S8. PPP Pleistocene samples.
data set S9. Diversity and abundance of cheilostome bryozoans in the Miocene of E Borneo, Indonesia.
data set S10. Miocene samples from East Kalimantan.
data set S11. Extant species.
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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5938229/
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