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Received: 27 October 2019    Revised: 20 August 2020    Accepted: 28 August 2020

DOI: 10.1111/jbi.13985

RE SE ARCH PAPER

Marine fish diversity in Tropical America associated with both

past and present environmental conditions

Andrea Polanco F.1  | Fabian Fopp2,3 | Camille Albouy4 | Philipp Brun3  |

Lydian Boschman2,3  | Loïc Pellissier2,3

1
Programa de Biodiversidad y Ecosistemas
Marinos, Museo de Historia Natural
Marina de Colombia (MHNMC), Instituto
de Investigaciones Marinas y Costeras –
INVEMAR, Santa Marta, Colombia
2
Landscape Ecology, Institute of Terrestrial
Ecosystems, Department of Environmental
Systems Science, ETH Zürich, Zürich,
Switzerland
3
Swiss Federal Institute for Forest, Snow
and Landscape Research WSL, Birmensdorf,
Switzerland
4
unité Écologie et Modèles pour
l'Halieutique, Institut Français de Recherche
pour l'Exploitation de la Mer IFREMER,
Nantes, France
Correspondence
Andrea Polanco F., Programa de
Biodiversidad y Ecosistemas Marinos, Museo
de Historia Natural Marina de Colombia
(MHNMC), Instituto de Investigaciones
Marinas y Costeras – INVEMAR, Calle 25
No. 2–55 Playa Salguero, Santa Marta,
Colombia.
Email: andrea.polanco@invemar.org.co
Funding information
ETH Global; Monaco Explorations
Foundation; INVEMAR; Swiss National
Science Foundation, Grant/Award Number:
310030E, - and 164294; Research Council of
Norway, Grant/Award Number: 268310
Handling Editor: Sergio Floeter
Abstract
Aim: Tropical America, including the Tropical Eastern Pacific and the Caribbean Sea,
presents a high level of marine biodiversity, but its fish fauna has been poorly docu-
mented. In early studies marine species distributions were interpreted based on tec-
tonic activity during the late Cenozoic, while more recent studies have highlighted a
link with the present-day environment. Here, we described the assemblage richness
and composition of fishes in Tropical America and related these properties to both
the past evolution of marine environmental conditions and current environmental
gradients.
Location: Tropical America.
Taxon: Demersal and benthic fishes.
Methods: We mapped the distribution of 2,216 demersal and benthic fish species of
Tropical America using existing occurrence data. We computed three assemblage in-
dicators: species richness, composition and nestedness, which we explained by envi-
ronmental gradients. We linked compositional distance to environmental differences
using distance-based redundancy analysis, species richness and nestedness using a
generalized linear model. We ran simulations of a mechanistic model in which three
processes determine the spatial dynamics of biodiversity: speciation, dispersal and
extinction. This model yielded estimates for species assemblage properties follow-
ing palaeogeographic changes in the region that shaped the current coastal habitat
configuration.
Results: Fish species richness in Tropical America peaks around the Florida Peninsula,
Bahamas and Greater Antilles. Fish composition varies along a depth gradient, be-
tween the Tropical Eastern Pacific and the Caribbean Sea, and forms distinct do-
mains within the Caribbean region. The nestedness component of β-diversity is lower
in shallower assemblages, especially those along the outer section of the Greater
Caribbean. Species richness and nestedness are partly explained by current environ-
mental conditions, but model simulations illustrate how this may be further explained
by the tectonic history of the region.
Main conclusions: Species richness peaks in the Greater Caribbean, coinciding with
generally favourable current environmental conditions for demersal and benthic

Journal of Biogeography. 2020;00:1–14. wileyonlinelibrary.com/journal/jbi © 2020 John Wiley & Sons Ltd     1 |
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2       POLANCO F. et al.

fishes. The high species richness and the low nestedness of fish assemblages in the
Cuba region are compatible with the results of palaeo-environmental changes that
have occurred in that area. Effects of the plate tectonic history might still be present
in the organization of fish fauna in this region.

KEYWORDS

environment, Greater Caribbean, marine fish diversity, tectonics

1 |  I NTRO D U C TI O N
Tropical America, including the Greater Caribbean and the Tropical
Eastern Pacific, contains several marine hotspots of biodiversity
(Roberts et  al.,  2002). In comparison to other tropical zones, this
region remains less documented as regards to the diversity and
composition of fish assemblages, because it contains a mosaic
of countries and high geographic complexity (Fautin et  al.,  2010;
Miloslavich et al., 2010). The fish fauna of the Greater Caribbean in-
cludes a diverse tropical assemblage with many reef-associated fish
species distributed along the continental coast of Central America
and near the Caribbean islands (Bahamas, Antilles and the islands
and atolls of the western Caribbean and Bermuda). These areas are
associated with habitats including mangroves, seagrasses, soft bot-
toms, coral reefs and rocky shorelines (Robertson & Cramer, 2014).
A first attempt to compile distribution maps for the most common
fish species of the Greater Caribbean indicated a higher species di-
versity around southern Florida, the eastern Bahamas and northern
Cuba (Smith et al., 2002). As regard to species composition, fish as-
semblages are structured into three major provinces: (a) a central,
tropical province; (b) a southern province spanning the continental
shelf of northern South America and (c) a northern province covering
the Gulf of Mexico (Robertson & Cramer,  2014). The fauna of the
Greater Caribbean shares many lineages with that of the Tropical
Eastern Pacific (Robertson & Cramer,  2009), which was separated
from the Greater Caribbean (~15–3  Ma) during the formation of
the isthmus of Panama (Hoorn & Flantua, 2015; Leigh et al., 2014;
Lessios, 2008; Montes et al., 2015; O'Dea et al., 2016). In the Tropical
Eastern Pacific, fish assemblages are structured into three major
provinces: (a) a northern province, the Cortez (Gulf of California and
lower Pacific Baja); (b) a southern province, the Panamian and (c) the
Ocean Island Province, formed by the five oceanic islands/archipela-
gos (Robertson & Cramer, 2009). Although general knowledge about
these faunas has been established (Robertson & Cramer,  2009;
Zapata & Robertson, 2007), a more detailed understanding of the
organization and origins of the gradients in fish species richness and
composition in Tropical America could be obtained by a data syn-
thesis effort.
The global spatial distribution of marine fishes has been demon-
strated to be associated with various environmental variables re-
lated to contemporary physical conditions or habitat structure
(Arias-González et al., 2008; Mora, 2015), but we lack a high-resolu-
tion description of the diversity of Tropical America to uncover the
main gradients. Global studies have partly documented the diversity
in Tropical America in comparison with other regions (Parravicini
et  al.,  2013; Tittensor et  al.,  2010), but have generally lacked de-
tails on the more subtle variations within this region (but see Alzate
et  al.,  2019, for the Tropical Eastern Pacific region). Studies of the
regional fauna have shown an association between species rich-
ness and reef cover (Galaiduk et al., 2017; Komyakova et al., 2013),
water depth (Baldwin et  al.,  2018; Costello & Chaudhary,  2017;
Semmler et al., 2017), the type and complexity of the substrate
(Bouchon-Navaro et  al.,  2005; Graham & Nash,  2013; Gratwicke
& Speight,  2005; McEachran,  2009) and geomorphology (e.g. reef
lagoons, fronts, slopes and terraces; Arias-González et  al.,  2008).
Moreover, variation in physical parameters, including temperature
(Mora, 2015), surface currents (McEachran, 2009) and local upwell-
ing systems (Jury, 2011; Rueda-Roa et al., 2018; Rueda-Roa & Muller-
Karger, 2013), have been found to be associated with differences in
fish composition. For example, the lower sea temperatures and reef
cover in the temperate northern Gulf of Mexico compared with con-
ditions in the southern Gulf and tropical Caribbean Sea align with a
difference in species richness and composition (Fautin et al., 2010;
Ward, 2017). On a smaller scale, Andradi-Brown et al. (2016) showed
that reef fish species richness, abundance and biomass declined with
water depth. Such studies indicate that extant environmental con-
ditions play a role in the composition of demersal fish assemblages
in Tropical America, but these relationships remain to be tested at a
larger scale.
Besides current environmental conditions, the spatial organiza-
tion of marine assemblages is expected to be related to variability in
these environments through geological time due to plate tectonics
(Briggs, 1974; Leprieur et al., 2016; Rosen, 1975; Rosenblatt, 1967)
or paste climate change (Pellissier et al., 2014). In a first attempt to
understand marine biogeographic provinces of the global ocean
in relationship to the movement of tectonic plates, Ekman (1953)
compared the faunal composition in different regions. Many stud-
ies have followed focusing on, for example, classical monographies
(Briggs,  1974; Ekman,  1953), fossil records (Renema et al., 2008),
phylogenies (e.g. Cowman et al., 2017; Floeter et al., 2008) and sim-
ulations (Gaboriau et al., 2019; Leprieur et al., 2016). Nonetheless,
linking the extant spatial distribution of marine organisms with
deep-time processes has thus far been limited by: (a) the availability
of a palaeogeographic reconstruction that can be used numerically;
(b) methods that allow the transformation of such a palaeogeo-
graphic reconstruction to a set of biological expectations that can be
POLANCO F. et al.
compared with data (Rangel et al., 2018) and (c) the complete doc-
umentation of the biological organization of a region at sufficient
resolution, enabling the description of small-scale empirical patterns
(Tyberghein et al., 2012). Recently, remote sensing of habitat char-
acteristics (Mumby et  al.,  2004), climate mapping (Frölicher et al.,
2018), detailed quantitative reconstructions of plate tectonic mo-
tions (Boschman et al., 2014), process-based simulations of biodiver-
sity (Descombes et al., 2018) and large databases compiling species
distributions have facilitated the study of the historical and environ-
mental context that led to the extant spatial organization of marine
life in Tropical America.
Species assemblage properties are general indicators of the pro-
cesses that shape biodiversity, which can be associated with both
current environmental conditions and palaeo-environmental con-
ditions (Pellissier et  al.,  2018). Variation in both ⍺- and β-diversity
in fishes has been related to contemporary processes, such as abi-
otic filtering (Tittensor et al., 2010), dispersal (Stier et al., 2014) and
trophic-level interactions (Jacquet et al., 2017). While local studies
have suggested an associations between fish biodiversity and en-
vironmental gradients (Arias-González et  al.,  2008; Costello &
Chaudhary, 2017), this was never investigated at the scale of Tropical
America as a whole. Moreover, biodiversity gradients can result
from historical dynamics (Cowman et al., 2017; Leprieur et al., 2016;
Pellissier et  al.,  2014), but the association between biodiversity
and plate tectonics has never been tested quantitatively. Here, we
mapped the species richness, composition and nestedness of marine
fish biodiversity in Tropical America to document the main spatial
gradients in species richness and composition in the region. The dis-
tribution and structure of assemblages of shore fishes are relatively
well documented, but knowledge diminishes with water depth and
distance to the shore (Fautin et al., 2010; Miloslavich et al., 2010). We
therefore did not focus only on shorefishes, but rather included all
demersal species that have tight connections with their shelfal envi-
ronmental conditions. Next, we related ⍺- and β-diversity properties
of benthic and demersal fishes to present-day environmental condi-
tions and the deep-time evolution of the region to understand their
potential origin. To this end, we first generated a detailed synthesis
of the regional biodiversity using species occurrence data compila-
tion combined with species spatial mapping (Albouy et al., 2019). We
tested whether reconstructed ⍺- and β-diversity properties of fish
assemblages for shallow- and deep-water fauna are associated with
present-day environmental conditions, and/or are reflected in the
historical palaeogeographic dynamics.
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Study area
The Greater Caribbean marine realm comprises the tropical and
subtropical waters between Cape Hatteras in North Carolina,
USA (35°N), and northern Guyana (5°S) in South America, and sur-
rounding the islands of Bermuda, the Bahamas, the Greater and
|
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Lesser Antilles, and the islands and atolls of the western Caribbean
(Figure  1). This heterogeneous region includes deep ocean basins
separated by relatively shallow rises, many island platforms and
continental shelves (Robertson & Van Tassell, 2015). The centre of
the region is mainly influenced by the Gulf Stream, with seasonally
mixing waters on the inshore side and fluctuating waters subject to
cool-water upwelling events and warm Gulf Stream intrusions on
the offshore side (Blanton et  al.,  1981). The Caribbean Sea is bor-
dered by the eastern coast of Central America, the northern coast
of South America and the Greater and Lesser Antilles, and connects
to the Gulf of Mexico via the Yucatan channel. Water depth in the
Caribbean Sea ranges from shallow to very deep in the Cayman
Trough (7,686 m), and averages at ~2,400 m. The Gulf of Mexico, ex-
tending from the Yucatan Peninsula to the Straits of Florida, is influ-
enced by temperate warm waters in the north, as well as by tropical
Caribbean waters in the south (Ward, 2017). Freshwater coastal in-
puts (Chérubin & Richardson, 2007; Restrepo et al., 2016; Restrepo
& Syvitski,  2006), eddies and meanders (Andrade & Barton,  2005)
and an upwelling system in the southern Caribbean Sea (Rueda-Roa
& Muller-Karger, 2013) are the sources of nutrient fluctuations in the
area. The Tropical Eastern Pacific extends from Magdalena Bay in
Baja California (25°N) to Cabo Blanco in Peru (4°S), and includes the
islands of Revillagigedos, Clipperton, Cocos, Malpelo and Galápagos
(Robertson & Cramer, 2009). It is characterized by a variety of eco-
systems including mangroves (Castellanos-Galindo et al., 2013;
Cortés et al., 2017), rocky shores and soft bottoms, which are distrib-
uted along the Central American coast and on the available shelves
of the surrounding islands. The Tropical Eastern Pacific has a patchy
coral reef distribution caused by frequent disturbances, intense bio-
erosion and extremely slow rates of recovery (Cortés, 1997; Glynn
et al., 2016). Trade winds blowing from the north sustain upwelling
systems and high productivity levels in central Panama, the Gulf of
Papagayo and the Isthmus of Tehuantepec (Amador et  al.,  2006;
Fiedler & Lavín, 2017).
2.2 | Plate tectonic history
The Caribbean region consists of a large number of (micro-)plates
and tectonic terranes that move or have moved with different tec-
tonic motions and speeds throughout geological time. The region
is underlain by: (a) the westward moving North American Plate in
the north, hosting the North American continent, Cuba and the
Yucatan Basin south of Cuba, and part of the Atlantic Ocean; (b)
the westward moving South American Plate, hosting the South
American continent and part of the Atlantic Ocean; (c) the rela-
tively stationary Caribbean Plate, hosting all the Caribbean islands
(except Cuba), the Central American land bridge and the Caribbean
Sea; and (d) the eastward moving Cocos and Nazca plates that are
located east of the Central American subduction zone that borders
the western coast of the Central American land bridge (Figure  1).
The Caribbean Plate, with the Greater Antilles (Cuba [which became
part of the North American Plate ~45 Ma], Jamaica, Hispaniola and
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4       POLANCO F. et al.

F I G U R E 1   Geography of the study area, including the main geographic features of the Greater Caribbean between Cape Hatteras in
North Carolina, USA and northern Guyana in South America, and surrounding the islands of Bermuda, the Bahamas, the Greater and Lesser
Antilles and the islands and atolls of the western Caribbean. The Tropical Eastern Pacific extends from Magdalena Bay in Baja California
to Cabo Blanco in Peru and includes the islands of Revillagigedos, Clipperton, Cocos, Malpelo and Galápagos. The limits of the tectonic
plates of Tropical America are presented as dashed lines. Coordinates are given in WGS84 projection

Puerto Rico) at its leading edge, drifted towards its current position
between the American continents from the eastern Pacific, where it
was positioned in Jurassic-Cretaceous times (Boschman et al., 2014;
Burke,  1988; Pindell et  al.,  1988; Pindell & Kennan,  2009). In con-
trast, the northern part of the Greater Caribbean region (Mexico and
the southern coast of the USA) is part of the North American Plate,
which has tectonically been much more stable. Around 45 Ma, Cuba
collided with the Bahamas platform, which then formed the south-
ern end of the North American Plate, which led to the formation of
the current plate boundary at the Cayman Trough and the merging of
Cuba and the Yucatan Basin to the North American Plate (Boschman
et  al.,  2014; Iturralde-Vinent,  1997; Iturralde-Vinent et  al.,  2008).
Both the Caribbean and the North American plates contain exten-
sive areas of shallow water, providing habitat for marine benthic and
demersal species. Moving crustal terranes are believed to transport
their associated fauna (Valentine & Moores,  1970; Zaffos et al.,
2017), and consequently, due to the highly dynamic tectonic history
of the Caribbean region, the spatial distribution of habitats has been
highly variable throughout geological time.
2.3 | Compilation of environmental maps
To summarize the environmental variability across Tropical America,
we gathered data on bathymetry, mean annual seabed tempera-
ture, mean annual sea surface temperature, mean annual chloro-
phyll-a productivity and dissolved oxygen from the Global Marine
Environment Dataset (Basher et  al.,  2018; available from www.
gmed.auckl​and.ac.nz). In addition, we computed the reef cover from
Reef Cover (https://www.wri.org/publi​catio​n/reefs​-risk-revis​ited),
by summing the reef cover present within one geographic cell of
0.16 × 0.16 degree (Figure S1).
2.4 | Establishment of species lists and occurrence
data collection
We cross-referenced various regional species lists to establish a
list including all known benthic and demersal fish species of the
Greater Caribbean and the Tropical Eastern Pacific. For the Greater
POLANCO F. et al.
Caribbean, we extracted species names from a compiled distribution
database (https://bioge​odb.stri.si.edu/carib​bean/) based on data from
Robertson and Van Tassell (2015) for shorefishes, McEachran (2009),
Quattrini et al. (2017) and unpublished data for slope species. For the
Tropical Eastern Pacific, a list of species names was extracted from a
compiled distribution database of demersal species (https://bioge​odb.
stri.si.edu/) based on Robertson and Allen (2015) for shorefishes and
Robertson et al. (2017) for shelf edge and slope fishes. When available,
we extracted occurrences from the databases mentioned above, to-
gether with others compiled from the IDigBio portal search, the Ocean
Biogeographic Information System (OBIS; https://obis.org/) and the
Global Biodiversity Information Facility (GBIF) portal search. All the
records were mapped and checked for outlying single occurrences: we
excluded occurrences for which the bathymetry was largely out of the
bathymetry range established by FishBase (Froese & Pauly, 2019).
2.5 | Species range mapping
To generate the species ranges from the occurrences, we developed
a range mapping algorithm that combines convex-hull polygons with
modelled species ecological niche projections. For each species, we
excluded outliers that are more than 10° away from the next cluster
(>2) of presence points. We generated polygons in each of the four
main bioregions per species (the Gulf of Mexico, the Caribbean Sea,
the Carolinian region and the Tropical Eastern Pacific). This step pro-
vided the flexibility to generate disjunct species distribution ranges
if necessary. In each bioregion, we applied a convex-hull polygon
with a buffer of 3° around the occurrences to define the geographic
range polygons of the species. We then joined all separate polygons
to delimit the full geographic domain of each species.
Next, we generated maps of species ecological suitability using
species distribution models (Guisan & Zimmermann, 2000). To com-
plement species presences, we generated 8,000 pseudo-absences,
of which 80% were sampled with the geographic approach (Phillips
et al., 2009) and 20% were sampled in an environmentally stratified
manner. Environmentally stratified random samples were added in
order to ensure that the models were trained along all environmen-
tal gradients considered, and thus no extrapolations beyond train-
ing ranges were necessary (Mesgaran et al., 2014). In order to relax
spatial biases in the presence observations, we randomly removed
one observation from each point pair with less than 5 km separation.
By applying this 5 km threshold, we removed biases from repeated
local measurements without discarding too many observations of
sparsely sampled species. We related species presences and pseu-
do-absences to environmental conditions using generalized linear
models (McCullagh & Nelder, 1983) and generalized additive models
(Hastie & Tibshirani, 1990). For both algorithms, we applied a sim-
ple parameterization as defined by Brun et al. (2020). We fitted dif-
ferent models for fish species occurring in shallow and deep water,
classified by applying a threshold of 200 m for the typical depth of
the species' occurrence. The number of predictors considered in the
algorithms was constrained by the available occurrence data. For
|
      5
shallow-water species, if 10–19 filtered occurrence observations
were available for a species, we fitted univariate models based on
sea surface temperature; for species with >20 occurrences, we fit-
ted bivariate models also considering bathymetry. For deep-water
species, if 10–19 filtered occurrence observations were available for
a species, we fitted univariate models based on bathymetry; for spe-
cies with >20 occurrences, we fitted bivariate models also consider-
ing seabed temperature. Model-based projections were converted
into binary presence/absence using the threshold of maximum TSS
(true skill statistic; Allouche et al., 2006). We then stacked them and
considered the species to be present in areas where both models
predicted presence. In a last step, we combined the range maps and
the species distribution projections to obtain the final distribution
map for each species, which was the intersection of the presence/
absence predictions from both approaches. The distribution maps
were compared with existing maps from the atlases of Robertson
and Van Tassell (2015) and Robertson and Allen (2015). We analysed
the species distribution maps and grouped species and genera into
general distribution patterns, and we described general species dis-
tribution types. Range-mapping analyses were run in the R environ-
ment (R Core Team, 2019).
2.6 | Computation of assemblage properties
From the compiled species distribution maps, we computed ⍺- and
β-diversity of the assemblage properties for each grid cell of 0.25°:
(a) species richness, (b) species composition and (c) the first axis of
a nestedness ordination. We computed species richness by stacking
the single species distribution maps. We performed a principal com-
ponents analysis on the presence/absence data using the Jaccard
distance to describe the main composition axes with the function
dudi.pco in the R package ‘ade4’ (Dray & Dufour,  2007). We com-
puted the ordinated value of nestedness as in Leprieur et al. (2016).
We used the NODF index based on paired overlap and decreasing fill
to measure the extent to which species present in species-poor cells
constitute representative subsets of those present in species-rich
cells. We related the grid cell species richness of fish assemblages
to bathymetry, productivity and reef cover when considering the en-
tire study area, using a generalized linear model with a quasi-Poisson
distribution. We considered sea surface temperature, productivity
and reef cover when investigating the species richness of the coastal
area. We related nestedness to environmental variables using a
linear model. We related compositional distance to environmental
differences using distance-based redundancy analysis using the cap-
scale function of the R package ‘vegan’ (Oksanen et al., 2007).
2.7 | Tectonic evolution and diversification
simulations
We used the plate tectonic reconstruction of Boschman
et  al.  (2014), which describes the tectonic motions of (micro-)
 |
6       POLANCO F. et al.
plates and tectonic blocks or terranes of the Caribbean region. We
developed this reconstruction with the GPlates plate reconstruc-
tion software (Boyden et al., 2011), incorporating an update to ac-
count for the large-scale rotations of the continental Chortis Block
(Garza et  al.,  2019). To convert this two-dimensional reconstruc-
tion of plate motions into a palaeogeographic reconstruction, we
used the present-day location and distribution of the shoreline and
shallow and deep water and reconstructed them back in time. We
made adjustments in line with geological data: (a) subareal regions
underlain by oceanic crust that consist largely of volcanic mate-
rial (volcanic islands or, e.g. the Costa Rica–Panama arc) were re-
constructed back towards the age of onset of volcanism, and were
not present in the reconstruction before that time (e.g. the Lesser
Antilles islands do not exist prior to 40 Ma); and (b) the now deeply
submerged Aves ridge was considered to be a shallow-water envi-
ronment during arc volcanism (between ~80 and 45 Ma; Iturralde-
Vinent & MacPhee,  1999). The palaeogeographic reconstruction
did not include the changes in water depth through time, and there-
fore this process was not considered in our analysis. From the re-
construction, we extracted the distribution of shallow marine and
land areas per million-year time step, which we used as input for the
model developed by Descombes et al. (2018). In this model, three
processes determine the spatial dynamics of biodiversity: specia-
tion, dispersal and extinction. The model assumes that speciation is
driven by dispersal-driven isolation only. If two habitat patches are
isolated by a distance larger than a threshold ds, populations of spe-
cies in these isolated geographic clusters will speciate. Species can
disperse to connected cells at a distance smaller than a threshold
distance d. We explored a range of values for ds and d between 50
and 240 km per time step, selecting values that best matched the
regional number of species (dispersal d ∈ {1°:15°}) and speciation
(ds ∈ {1°:15°}). This neutral parsimonious model generates expecta-
tions of the effects of palaeogeography on biodiversity. We started
the simulations at 80 Ma, corresponding to the crown age of many
of the fish clades considered in our study (Rabosky et  al.,  2018),
which implies that for the majority of the simulated time, there is no
geographic barrier between the Greater Caribbean and the Tropical
Eastern Pacific. We ran the model at a temporal resolution of 1 Myr
and spatial resolution of 0.16°. We selected the best simulation by
performing a Pearson's correlation test between the species rich-
ness obtained from the stacked range maps and the simulations.
We further mapped the simulated species composition and nested-
ness for the final time steps of the simulation, following the same
procedure as for the mapped data.
3 |   R E S U LT S
3.1 | Description of species and genera distribution
patterns
The mapping of richness at both the species and genus level in
the Greater Caribbean indicated four distribution types: north,
central, south and Caribbean wide (Figure 2a, Figures S2–S5). The
northern distribution includes species in the Gulf of Mexico and
along the south-eastern coast of the USA, and contains genera
such as Fundulus (Figure  S4a). The central distribution includes
all species present in the waters surrounding the carbonate
platforms offshore Belize, the Greater and Lesser Antilles, the
south-eastern Caribbean and along the east coast of the Florida
Peninsula (e.g. genus Emblemariopsis). The southern distribu-
tion includes the entire continental shelf and slope of the north-
ern coast of South America, from Colombia to northern Guyana,
and reaches north to Belize and the Lesser Antilles (e.g. Ariidae:
Notarius, Sciades; Batrachoididae: Amphichthys). The Caribbean-
wide distribution covers almost the entire Greater Caribbean re-
gion (e.g. Acanthuridae: Acanthurus; Monacanthidae: Cantherhines;
Chaetodontidae: Chaetodon).
Similarly, the mapping of richness at both the species and
genus level in the Tropical Eastern Pacific revealed four distribu-
tions: Mexican, central, offshore islands and eastern Pacific wide
(Figure 2a, Figures S2–S5). The Mexican region is a northern distri-
bution unit including species present in the Gulf of California and
the surrounding waters (e.g. genera Fundulus, Gillichthys). Some
species are restricted to the northern part of the Gulf while oth-
ers are present within the Gulf and along the west coast of the
Baja California Peninsula, and some reach farther south along the
coast of central/southern Mexico. The central distribution contains
all species present in the waters surrounding Central America.
Most species are present along the entire stretch of coast from
Guatemala to southern Ecuador, although some species are present
in only a segment of this area (e.g. genus Batrachoides). The off-
shore islands distribution includes a potential assemblage of fishes
restricted to the islands and archipelagos of the Tropical Eastern
Pacific (e.g. genera Xenocys, Taeniurops). The eastern Pacific-wide
unit contains species present in almost the entire Tropical Eastern
Pacific (e.g. genus Abudefduf).
3.2 | Species richness distribution
The mean stacked species richness per cell in the Greater Caribbean
(μGC  =  68.3  ±  139.8; maxGC  =  795) is significantly higher than in
the Tropical Eastern Pacific (μTEP  = 27.1 ±  66.3; maxTEP  = 497; t
test, t  =  89.46, p  <  0.001), but species richness gradients exist in
each region (Figure 2, Figure S3). Species richness is highest on the
continental shelves of the eastern Florida Peninsula around Palm
Bay, including the Florida Keys coral reefs, Grand Bahama, the
north-western side of the Bahamas and the Cay Sal Bank. Other
regions of relatively high species richness are as follows: (a) the
continental shelf of south-eastern Florida and the south-eastern
Bahamas; (b) the northern Gulf of Mexico offshore Campeche and
Yucatan; (c) the coastal areas around Quintana Roo, Belize and
Honduras; (d) offshore Nicaragua and Colombia (including all the
western Caribbean islands and banks) and (e) the continental shelf
area of northern South America (Figure 2). In the Tropical Eastern
POLANCO F. et al. |
      7

F I G U R E 2   Predicted fish species richness (a) obtained by stacking all reconstructed species distribution maps and (b) from the
statistical model linking species richness to environmental variables. Coordinates are given in WGS84 projection. We found the richest fish
assemblages in the area of the Florida Keys, northern Bahamas and northern margin of Cuba. The statistical model generally reproduced the
gradient in species richness with depth, but was less able to explain variation at similar depths and in particular the hotspot of the eastern
Florida Peninsula around Palm Bay, including the Florida Keys coral reefs, Grand Bahama, the north-western side of the Bahamas and the
Cay Sal Bank

TA B L E 1   (a) Statistical relationships from the generalized linear
model linking species richness to environmental variables with a
quasi-Poisson distribution and considering a linear term for each
of the explanatory variables. The species richness is related to
bathymetry, reef cover and log10 of primary productivity. The total
explained variance is D2 = 0.9. (b) Statistical relationship of the
generalized linear model linking species richness to environmental
variables with a quasi-Poisson distribution, focusing only on shallow
cells. The species richness is related to sea surface temperature,
reef cover and primary productivity. The total explained deviance
of the model is lower (D2 = 0.34)
waters with high reef cover and decreases with increasing primary
production (Table  1a,b). The species richness model including the
entire benthic and demersal fish fauna showed high explanatory
power (D2 = 0.9, Table 1a), while the model focusing only on shal-
low areas had a comparatively lower explanatory power (D2 = 0.34,
Table 1b, Figure S3b). Families with the largest number of species
(e.g. Gobiidae and Labrisomidae) contribute most to the biodiver-
sity gradients (Figure S5a,c).

Explained 3.3 | Spatial distribution of species composition

Variable name Estimate p-value variance

(a) Global species richness In the first ordination of the principal coordinates analysis, which
(intercept) 7.35 <0.001 included benthic and demersal species across all depths, the first
Bathymetry −0.0012 <0.001 0.896 axis discriminated the fauna of the Greater Caribbean from the
Primary production −0.44 <0.001 0.156 fauna of the Tropical Eastern Pacific (Figure 3a,c). The second axis

Reef cover 2.11 <0.001 0.03

highlighted compositional variation along a depth gradient across
Tropical America (Figure  3a,c). The second ordination, performed
(b) Coastal species richness
on benthic and demersal species on shallow reefs only, yielded a
(Intercept) 6.1 <0.001
contrast between the fauna of the Greater Caribbean and the fauna
Sea surface 0.075 <0.001 0.19
of the Tropical Eastern Pacific, as well as between the upper and
temperature
lower part of the Greater Caribbean (Figure S3c,d). Using the cap-
Primary production −0.73 <0.001 0.18
scale analysis relating composition to environmental variables, we
Reef cover 0.94 <0.001 0.03
found that the composition of all benthic and demersal fish species
was primarily associated with depth (Table S1a). When focusing on
Pacific, overall species richness is lower, but peaks exist along the shallow assemblages only, compositional differences were mostly
coast of Nicaragua, Costa Rica and Panama. Areas of lower spe- associated with sea surface temperature (Table S1a). The associa-
cies richness include the continental shelves of southern Mexico, tion between composition and environmental variables was weaker
Guatemala and Ecuador, and the Galapagos Archipelago. The statis- for shallow assemblages than when the entire depth gradient was
tical model indicated that fish species richness is higher in shallower considered.
 |
8       POLANCO F. et al.

F I G U R E 3   Assemblage dissimilarity of marine fish species in Tropical America computed using a principal coordinate analysis (PCoA) on
a Jaccard distance matrix obtained from the species range maps for (a) all depths and (b) coastal areas. Each colour represents an individual
cell present in the PCoA space. According to these colour gradients, we mapped each cell (c) across depth and (d) in coastal areas. In the first
PCoA (a, c), the first axis mainly discriminates the fauna of the Greater Caribbean from the fauna of the Tropical Eastern Pacific. The second
axis highlights compositional differences along a depth gradient across Tropical America. The second ordination (b, d) shows a contrast
between the fauna of the Greater Caribbean and the fauna of the Tropical Eastern Pacific, and between the upper and lower Caribbean.
Coordinates in (c) and (d) are given in WGS84 projection

3.4 | Nestedness of species assemblages
The nestedness ranking across Tropical America indicated that as-
semblages in deeper waters are generally composed of nested sub-
sets of shallower assemblages (Figure  S6a). The statistical model
relating the nestedness of all benthic and demersal fish species
showed a predominant correlation with sea surface temperature
(Table 2a). In shallow water, the least nested assemblages are found
along the arc from the Florida Keys to Grenada via the Bahamas,
British Virgin Islands and Antigua and Barbuda, as well as along the
coast of Venezuela (Figure S6a). The most nested assemblages are
found in the inner part of the Caribbean. The statistical model con-
sidering only the shallow coastal area showed a weaker association
between nestedness and environmental variables and a lower ex-
plained deviance (R 2 = 0.37; Table 2b) compared with the model con-
sidering the entire bathymetric gradient (R 2 = 0.70; Table 2a).
3.5 | Tectonic evolution and diversification
simulations
The mechanistic model reproduced the extant species richness gra-
dient in tropical american fish (Figure 2) and the simulation with the
best fit to the data used d = 5 and ds = 10 (Pearson correlation coeffi-
cient: r = 0.50; t = 11.01, p < 0.001). This simulation also reproduced
the pattern of nestedness (Pearson correlation coefficient: r = 0.49;
POLANCO F. et al. |
      9

TA B L E 2   (a) Statistical relationships from the linear model to Venezuela via the Greater and Lesser Antilles, and relative lows
linking nestedness reconstructed from data to environmental in the Gulf of Mexico and along the Central American land bridge.
variables. The nestedness is related to bathymetry, primary
production and reef cover. The total explained variance is R 2 = 0.7.
(b) Statistical relationship of the linear model linking reconstructed
nestedness to environmental variables, considering only shallow 4 | D I S CU S S I O N
cells. The nestedness is related to bathymetry, primary production
and sea surface temperature (R 2 = 0.37) We have provided the first detailed biogeographic analysis of the

Explained potential assemblages of the benthic and demersal ichthyofauna

Variable name Estimate p value variance of Tropical America by jointly investigating the effects of present-

(a) Global nestedness day environmental conditions and palaeogeographic evolution. The
Caribbean is a geographically complex region and its western part
(Intercept) 6.59 0.07
has long been considered one of the hotspots of biodiversity in the
Bathymetry −0.0137 <0.001 0.699
tropics (Roberts et  al.,  2002). In the largest mapping effort so far,
Primary production 1.64 <0.01 0.29
we have documented the potential species ranges of 2,216 benthic
Reef cover −59.67 <0.001 0.028
and demersal fish species and showed that their assemblages are
(b) Coastal nestedness
structured along clear geographic gradients of species richness and
(Intercept) 70 <0.001 composition, which are primarily linked to present environmental
Sea surface −3.84 <0.001 0.30 factors. The main environmental gradient structuring assemblage
temperature
properties of benthic and demersal fishes is water depth (Arias-
Primary production 22.28 <0.001 0.16 González et al., 2008; Brown, 2014; Tables 1 and 2). Deeper habitats
Reef cover −65.1 <0.001 0.044 are generally less productive (Sigman & Hain, 2012) and physically
more demanding to live in (Helfman et  al.,  2009), and therefore
t  =  10.48, p  <  0.001; Figure  S6) and composition differentiations require appropriate adaptation in fishes (Bone & Moore, 2008).
among cells (Pearson correlation coefficient; r  = 0.44; t  =  566.6, Independent of water depth, our analysis indicates a contrast in spe-
p < 0.001). The simulations showed the most taxonomically nested cies richness between the Caribbean Sea and the south-western
(highest) assemblage values occurring in the Gulf of Mexico, inner Gulf of Mexico, the latter of which shows poorer assemblages. We
Caribbean Sea and Tropical Eastern Pacific, while the lowest values explain this contrast by a difference in temperature, as well as dif-
were found along the Greater and Lesser Antilles. At the start of ferences in substrate. These correlations suggest that warmer areas
the simulation, 80  Ma, the Greater Antilles island arc was located that are also more complex in terms of habitat host richer benthic
between southern Mexico and Colombia (Figure  4), creating great and demersal fish assemblages (Parravicini et al., 2013).
complexity of habitat patches in the eastern Caribbean region. In The spatial variations in assemblage properties reconstructed
contrast, the “proto-Caribbean Sea” did not contain extensive areas from data were further associated with the palaeogeographic dy-
of shallow water. North-eastward migration of the Caribbean Plate namics of the region. In particular, the shallow areas along the east-
relative to the North and South American continents also resulted ern arc of the Caribbean, stretching from the Floridian Keys to the
in the eastward migration of the southern part of the leading edge coast of Venezuela, including the Antillean islands, are characterized
of the Caribbean Plate along the South American margin. According by high values of species richness and low nestedness, correspond-
to the best-fitting simulation, there was an accumulation of diver- ing to the simulation outputs. Our simulations of the in situ origin of
sity following the collisions, and a subsequent interaction between the regional biodiversity agree with the species richness estimated
the leading edge of the Caribbean Plate, hosting the Aves ridge, from data and support the idea that this region has the highest evo-
the Leeward Antilles and Tobago and the South American margin. lutionary species accumulation in the Caribbean Province (Briggs
In contrast, the trailing edge of the Caribbean Plate, hosting the & Bowen, 2013). The simulated dynamics illustrate how this fauna
Costa Rica–Panama arc, was more isolated and therefore did not might have originated and/or moved with the north-eastward–shift-
accumulate as many species through dispersal or speciation. Even ing Caribbean Plate. In particular, the fauna of the leading edge of
after the formation of the Panama isthmus around 15–3  Ma and the Caribbean Plate (Greater Antilles) merged with the fauna of the
the connection of the North and South American continents, the ancestral southern end of the North American Plate, resulting in in-
simulation resulted in a generally lower species richness in the Costa creased species accumulation. Furthermore, the high species rich-
Rica–Panama region compared with the Greater Antilles. From a tec- ness in the relatively young Lesser Antilles island arc and along the
tonic point of view, the Gulf of California region has little interaction coast of Venezuela may be explained by southward migration of a
with the Caribbean, and the simulation shows the Gulf of Mexico fraction of the Cuba/Bahamas region fauna after formation of the
maintaining a species composition that is quite different from that Lesser Antilles volcanic islands. The simulations further predicted
of the Caribbean region, supporting the isolation of the Gulf of less-nested assemblages northeast of the Antillean arc and along
Mexico through geological time. The simulations predicted diversity the coast of Venezuela (Figure S6), in line with the patterns recon-
highs along the outer arc of the Caribbean stretching from Florida structed from data. Nestedness is an especially useful property
 |
10       POLANCO F. et al.

F I G U R E 4   Diversification simulation for fish species in Tropical America including the palaeogeographic reconstruction, based on
Boschman et al. (2014), of time steps (a) 50, (b) 40, (c) 20, (d) 10, (e) 5 and (f) 3 Ma for the simulation ds = 10 and d = 5. The leading edge of
the Caribbean Plate hosting the proto-Greater Antilles and the Aves ridge is located between Mexico and Colombia. Around 50 Ma, the
proto-Greater Antilles migrated further to the northwest relative to North America and approached the Bahamas platform and southern
Florida. Around 40 Ma, the collision of Cuba with the Bahamas platform was finalized and motion of the Caribbean Plate relative to North
America was eastwards. The volcanic islands of the Lesser Antilles started forming. Around 20–10 Ma, the Panama isthmus was formed,
separating the Caribbean Sea from the Pacific. The Lesser Antilles arc continued to move eastward along the coast of South America.
Coordinates in all panels are given in WGS84 projection

to assess the role of historical changes, as it can provide informa-
tion on the effects of past colonization trails (Cook & Quinn, 1995;
Patterson,  1990) or faunal merging in focal regions (Leprieur
et  al., 2016). The simulations suggest that the movement of plates
both isolating and then bringing together previously separated fauna
may increase the diversity in the area of interaction, as previously
suggested (Cowman et al., 2017; Leprieur et al., 2016; Renema et al.,
2008). Despite these congruent patterns, the simulations only in-
clude contours of shorelines and of shallow-water areas and lack
more detailed depth gradients as well as palaeoclimate reconstruc-
tions, which also influence fish assemblage composition (Pellissier
et  al.,  2014). As a result, the simulations can generate predictions
of general geographic domains of species, but future improvement
of palaeo-environmental and climatic reconstructions is expected to
provide predictions that are more realistic.
While we provide a first high-resolution map of the fish diver-
sity in Tropical America, our study has several methodological lim-
itations. First, fish occurrence data are denser in some regions than
others, which generates spatial variability in our mapping confidence
(Figure S7). The geographic unbalance in the density of occurrences
argues for the use of geographic polygons and species distribution
modelling to reconstruct species ranges, as done in previous stud-
ies (Albouy et  al.,  2019; Pellissier et  al.,  2014). Our mapping relies
on geographic and environmental interpolations, which can lead to
overprediction of species in geographic cells (Pineda & Lobo, 2012).
While the species richness gradients reconstructed are expected to
reflect empirical gradients, mapped species richness values might be
higher than those of realized assemblages. Second, the reconstruc-
tion of species ranges based on their presence or absence could ig-
nore the representation of species that are difficult to detect, such
as rare species with few occurrences in the considered area, imply-
ing an underestimation of both species composition and richness.
With our approach, it is also possible that we did not detect the rapid
colonization over the greater Caribbean by some species, such as
Pterois volitans, the lionfish (Betancur-R et al., 2011). This under-rep-
resentation of, for example, rare species could affect the estimation
of nestedness. Third, because some environmental variables deter-
mine both species distributions and species richness (e.g. Smith &
Brown, 2002), we used some of the same variables in species distri-
bution reconstructions and richness analyses. However, the main re-
covered gradients of species richness are also detectable in the raw
occurrence data (Pearson correlation coefficient richness, per depth
POLANCO F. et al.
bin r = 0.68, per sea bottom temperature bin r = 0.8), which demon-
strates that these relationships are not the result of potential circu-
larity in the methodology. Fourth, the simulation model provides a
simple qualitative expectation from palaeo-environmental dynam-
ics. The geological reconstruction only provides an estimation of
plate movements, which are only a rough proxy of species habitats.
Finally, the model ignores important biological processes that can
shape current species richness, such as species interactions, which
cannot be entirely validated without fossil records (Descombes
et al., 2018). Nevertheless, the investigation of both present and his-
torical environments offers a broader perspective on the formation
of biodiversity gradients in this region.
5 | CO N C LU S I O N S
We linked patterns in species richness of benthic and demersal fish
assemblages in the Greater Caribbean and Tropical Eastern Pacific
to present-day environmental conditions, principally to gradients
of depth and sea surface temperature. Our results are in line with
previous estimations (Fautin et al., 2010; Miloslavich et al., 2010),
showing that the Straits of Florida and the Antilles have the rich-
est ichthyofauna in the Atlantic, which may further be explained
by the complexity of the tectonic history of the region compared
with the tectonically quiet Atlantic Ocean. Our model simulations
of tectonic evolution and of dispersal, speciation and extinction
illustrate how the Caribbean fish fauna evolved to become more
closely related to those of the Eastern Pacific than to those of
the Eastern Atlantic (Briggs & Bowen,  2013) and demonstrate
that greater tectonic complexity may explain why the Caribbean
is more diverse than other regions of the Atlantic. These findings
suggest that the current distribution and diversity are associated
with present environmental factors, but may also partly reflect a
legacy of historical events. In conclusion, our findings suggest that
interpretation of the current spatial distribution of biodiversity
is best achieved by considering both extant environmental con-
ditions and past historical dynamics, thereby taking into account
both spatial and temporal heterogeneity and habitat variability.
Our study leads to a better understanding of the distribution and
composition of benthic and demersal fishes in Tropical America.
Furthermore, it provides a detailed account of the extant diver-
sity, which may be used as a benchmark for studies on how global
change will shape future biodiversity.
AC K N OW L E D G E M E N T S
This project was supported by an ETH Global grant and the
Monaco Explorations Foundation. LP received funding from the
Swiss National Science Foundation for the project Reefish (grant
310030E-164294). The study was co-funded by the Instituto de
Investigaciones Marinas y Costeras (INVEMAR) through the project
“Investigación científica hacia la generación de información y cono-
cimiento de las zonas marinas y costeras de interes de la nación“,
BPIN Code 2017011000113.” We thank David Ross Robertson
|
      11
from the Smithsonian Tropical Research Institute for checking
the regional species lists and Claudia Correa Rojas (Information
Systems Laboratory of INVEMAR) for her support with cartogra-
phy. The manuscript corresponds to the contribution no. 1271 of
the Instituto de Investigaciones Marinas y Costeras – INVEMAR,
Colombia. The Research Council of Norway project DRIVEBANKS
(Project no. 268310) provided funding for a workshop that ad-
vanced this study.
DATA AVA I L A B I L I T Y S TAT E M E N T
All the occurrence data are available in the respective data portals
that we queried. We have published the cleaned occurrence dataset
on the Envidat data portal (https://www.envid​at.ch/datas​et/marin​
e-fish-occur​rence​s-of-tropi​cal-america). The code used to run the
mapping and analyses is available on github (link: https://github.
com/FFopp/​fish_ranges).
ORCID
Andrea Polanco F.  https://orcid.org/0000-0001-6121-5214
Philipp Brun  https://orcid.org/0000-0002-2750-9793
Lydian Boschman  https://orcid.org/0000-0002-1802-0187
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B I O S K E TC H
Andrea Polanco F. is a scientific researcher at the Institute of
Marine and Coastal Research INVEMAR, Curator of fish at the
MHNMC of INVEMAR. Her research interests are concentrated
on the distribution of marine fish biodiversity over time and
space. This study represents a collaboration between INVEMAR,
the Swiss Federal Institute of Technology in Zurich ETH, the
Swiss Federal Institute for Forest, Snow and Landscape Research
WSL et the French Research Institute for Exploitation of the Sea
IFREMER.
Author contributions: APF, LP, CA, jointly designed this study,
APF, LP, CA, FF, developed the analysis of the data; and all the au-
thors APF, LP, CA, FF, LB, PB contributed to write the manuscript.
S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found online in the
Supporting Information section.
How to cite this article: Polanco F. A, Fopp F, Albouy C, Brun
P, Boschman L, Pellissier L. Marine fish diversity in Tropical
America associated with both past and present
environmental conditions. J. Biogeogr. 2020;00:1–14.
https://doi.org/10.1111/jbi.13985