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OPEN Global conservation prioritization

areas in three dimensions
of crocodilian diversity
Ricardo Lourenço‑de‑Moraes 1*, Felipe S. Campos 2,3,4*, Pedro Cabral 2,
Thiago Silva‑Soares 5,6, Yhuri C. Nobrega 7,8, Amanda C. Covre 9 & Frederico G. R. França 1

Crocodilians are a taxonomic group of large predators with important ecological and evolutionary
benefits for ecosystem functioning in the face of global change. Anthropogenic actions affect
negatively crocodilians’ survival and more than half of the species are threatened with extinction
worldwide. Here, we map and explore three dimensions of crocodilian diversity on a global scale. To
highlight the ecological importance of crocodilians, we correlate the spatial distribution of species
with the ecosystem services of nutrient retention in the world. We calculate the effectiveness of global
protected networks in safeguarding crocodilian species and provide three prioritization models for
conservation planning. Our results show the main hotspots of ecological and evolutionary values are in
southern North, Central and South America, west-central Africa, northeastern India, and southeastern
Asia. African species have the highest correlation to nutrient retention patterns. Twenty-five percent
of the world’s crocodilian species are not significantly represented in the existing protected area
networks. The most alarming cases are reported in northeastern India, eastern China, and west-central
Africa, which include threatened species with low or non-significant representation in the protected
area networks. Our highest conservation prioritization model targets southern North America, east-
central Central America, northern South America, west-central Africa, northeastern India, eastern
China, southern Laos, Cambodia, and some points in southeastern Asia. Our research provides a global
prioritization scheme to protect multiple dimensions of crocodilian diversity for achieving effective
conservation outcomes.

Carrying important evolutionary information, the Order Crocodylia appeared in the Late Cretaceous period and
among the extant Archosauria, crocodilians remain as the closest sister group of ­birds1. Their long evolution-
ary history (i.e. over 200 my) has been driving the ecology and evolution of an enormous variety of species on
­Earth2. Crocodilians are the largest inhabitants of freshwater ecosystems and are highly exposed to anthropogenic
pressures, mainly due to habitat ­loss3, with half of the living species threatened with ­extinction4. Despite limited
empirical knowledge, they have been globally identified as potential bioindicators due to their sensitivity to
pollution, and dependence on aquatic ­habitats5–8. Crocodilians are semiaquatic predators and may be of crucial
importance in aquatic and terrestrial ­ecosystems2,9. These iconic animals have varied roles in the aquatic and
terrestrial ecosystems as top-order predators, influence the nutrient cycle, and cross-ecosystem engineering
­processes2,10,12. Crocodilian species differ from other vertebrates by their demographic characteristics and can
generally be categorized as K-selected, characterized by presenting a long life, often large size, and few offspring;
or R-selected, characterized by presenting a short life span, many offspring, and usually small s­ ize11.

1
Programa de Pós‑graduação em Ecologia e Monitoramento Ambiental (PPGEMA), Universidade Federal da
Paraíba, Rio Tinto, PB 58297‐000, Brazil. 2NOVA Information Management School (NOVA IMS), Universidade
Nova de Lisboa, Campus de Campolide, 1070‑312 Lisbon, Portugal. 3Universitat Autònoma de Barcelona,
08193 Cerdanyola del Vallès, Catalunya, Spain. 4Centre de Recerca Ecològica i Aplicacions Forestals (CREAF),
08193 Cerdanyola del Vallès, Catalunya, Spain. 5Herpeto Capixaba project, Instituto Biodiversidade Neotropical,
Nova Guarapari, Guarapari, ES 29206‑400, Brazil. 6Museu de História Natural do Sul do Estado do Espírito Santo,
Universidade Federal do Espírito Santo, Jerônimo Monteiro, ES 29550‑000, Brazil. 7Projeto Caiman, Instituto
Marcos Daniel, Vitória, ES 29055‑290, Brazil. 8Departamento de Medicina Veterinária, Centro Universitário FAESA,
Vitória, ES 29053‑360, Brazil. 9Programa de Pós‑graduacão em Ecologia de Ambientes Aquáticos Continentais
(PEA), Universidade Estadual de Maringá, Maringá, PR 87020‑900, Brazil. *email: [email protected];
[email protected]

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Crocodilians are considered one of the twenty groups most charismatic in the w ­ orld12, attracting the public
attention because of their morphological features, thus promoting marketing for financial resources for conserva-
tion ­plans13. Due to the need for good protection across a large number of different habitats, crocodilians can be
considered flagship-umbrella species; act as flagship species because they are c­ harismatic13 and act as an umbrella
species because their conservation protects a large number of species that coexist in the same e­ nvironment14.
Despite the increased conservation efforts, there is a gap in the literature that integrates ecological and evolu-
tionary interactions that assess crocodilian species as mediators of cross-ecosystem linkages in the ­landscapes2.
Effective conservation planning must protect taxonomic, functional and phylogenetic diversity, to ensure the
persistence of all biodiversity ­components15. Taxonomic diversity (TD) is the number of species in a determinate
area. Functional diversity (FD) is a dimension of diversity that represents the extent of ecological differences
between species based on the distinction of their morphological, physiological, and life-history ­features16. Phy-
logenetic diversity (PD) adds value to theoretical and applied ecology studies, distinguishes species according to
their evolutionary histories, and quantifies how much of the Tree of Life is represented ­locally17. Therefore, for
any effective conservation plan, TD, FD and PD components should be considered as a central issue beyond the
detailed knowledge of the species’ d ­ istribution18. Finding areas with multiple biodiversity components can be
essential for the effectiveness and achievement of conservation ­goals19. Thus, prioritize areas covering a minimum
area with more chances of success in maximizing biodiversity conservation.
Protected areas (PA) typically figure as the cornerstone of conservation strategies worldwide, covering about
15% of the Earth’s s­ urface20,21. The current protected network is particularly helpful in safeguarding biodiversity,
although far from enough in the face of habitat ­loss22–24. For improved conservation outcomes, mapping ecologi-
cal and evolutionary values of different species pools may be key in determining the establishment of new PA
in aquatic and terrestrial e­ cosystems18,25.
Given the ecological importance of crocodilians for cross-ecosystem fluxes, here we explore how their biodi-
versity components are distributed on Earth, and how they are correlated to nutrient retention patterns. For this,
we calculate three dimensions of crocodilian diversity, and evaluate the effectiveness of the global PA networks
in conserving species, thus suggesting three scenarios of conservation prioritization models. These three sce-
narios differ in the values of the different dimensions of diversity (TD, FD and PD) and the distribution range of
threatened species. This work aims to contribute to conservation strategies focusing on the role of crocodilian
species in ecosystem functioning worldwide.

Results
As they are ectothermic, crocodilians have distribution patterns related to elevated temperatures, which corre-
sponds to a latitudinal range between − 30° and 20°. On the three dimensions of crocodilian diversity on Earth,
our results show high values of TD (i.e. number of species per cell, see materials and methods), FD and PD in
tropical and subtropical regions, at latitudes between − 15° and 20°. High TD and FD values are distributed in
the north to central South America, central Central America, and southern North America. In Africa, high TD,
FD and PD values are concentrated in the west-central region (Fig. 1a–c). In Asia, the main regions are located
in northeastern India, Sri Lanka, Malaysia, western Indonesia, Borneo and New Guinea, northern and southern
Philippines, and northern Oceania (Fig. 1a–c). The highest TD is in South America, mainly in the Amazon Basin
(Fig. 1a) where occur five species in sympatry. The higher values of FD in the Americas are in extreme southern
North America, central Central America, and extreme northern South America; in Africa, higher FD values
are in the west-central and it is a small portion in the direction south of the west-central region (see Fig. 1c).
The highest values of PD are distributed in the extreme southern North America and extreme northern South
America, where in sympatry species of subfamily Alligatorinae (e.g. Alligator, Caiman) and Crocodylinae (e.g.
Crocodylus) occur, with distinct evolutionary lineages (Fig. S2a).
The highest FD is in northeastern India, where occurs the Gavialis gangeticus, a species functionally distinct
from the other crocodilian species (Fig. S2b). Higher values of TD, FD and PD are in Malaysia and Indonesia
mainly in Borneo, Sumatra, north of Java, and New Guinea, and northern Oceania (Fig. 1). The null models for
FD and PD show different values than expected by chance (p < 0.001), indicating a non-random pattern of FD
and PD. The distribution of the three dimensions of crocodilian diversity through different landscape patterns
on Earth shows a high spatial correlation between TD, FD and PD values (R = 0.90 to 1, p < 0.0001; Fig. 1d),
highlighting their interaction of ecological and evolutionary scales, and the effects of these interactions on
ecosystem-level processes.
Our results show that Africa has the highest values of the positive interaction between TD and nutrient reten-
tion (35%), followed by the Americas (29%) and Asia and Oceania (11%) (Fig. 2). The mean percentage overlap
(MPO) demonstrates that the PA networks cover an average of 57.1% of the species’ ranges currently protected
(individual species ranging from 3.3 to 9.7%, SD ± 1.72%, Fig. 3, Table 1). In 17.8% of the species, the level of
protection is not significantly different from that expected by chance. In 25% of the species (e.g. A. mississippi-
ensis, A.sinensis, Ca. latirostris, Ca. yacare, Cr. halli, and G. gangeticus), the distribution patterns are significantly
higher than expected by chance (Fig. 3, Table 1), with the lowest level of representativeness in the PA networks.
The regions prioritized by Model 1(see Fig. 4, Table 2) hold values of FD, PD and TD higher than 90% of
the total observed in the world and the presence of Critically Endangered (CR) species. The main conservation
areas indicated by Model 1 (Fig. 4, Table 2) are southern North and east-central Central America, with one CR
species (Cr. rhombifer) and high values of FD and PD; northern South America, with one CR species (Cr. inter-
medius), and in the Amazon basin with the highest values of TD and higher values of FD and PD; west-central
Africa, with one CR species (Mecistops cataphractus), and high values of TD, FD and PD, having three species
(Me. cataphractus, Osteolaemus tetraspis, O. osborni) not significantly protected in the PA networks (see Fig. 3).
Northeastern India, southern Nepal, and Bangladesh also can be considered an important region for crocodilian

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Figure 1.  Spatial distribution of crocodilians worldwide. (a) Taxonomic diversity (TD); (b) functional diversity
(FD); (c) phylogenetic diversity (PD); and (d) relationships between TD, FD and PD. The maps were created in
ArcGIS Pro s­ oftware60.

conservation efforts, with one CR species (G. gangeticus), the highest values of FD, and high values of TD and
PD. The eastern China also covers one CR species (A. sinensis), which is highly threatened with extinction, with
their distribution patterns not represented in the PA networks (MPO = 0.00; Fig. 3, Table 1). In southeastern
Asia, a little portion of southern Vietnam and south-central Thailand, southern Laos, Cambodia, northern and
southern Philippines, and Borneo also cover two CR species (Cr. mindorensis and Cr. siamensis), with higher
values of FD and high values of TD and PD.
The regions prioritized by Model 2 (Fig. 4) hold values of FD, PD and TD higher than 70% of the total
observed in the world and the presence of Endangered (EN) species. Model 2 prioritizes west-central Central
America, north and central South America; west-central Africa with two EN species (Me. leptorhynchus and O.
aftezelli). The regions prioritized by Model 3 (Fig. 4) hold values of FD, PD and TD higher than 50% of the total
observed in the world and the presence of Vulnerable (VU) species. Model 3 shows important areas for croco-
dilian conservation in northern Central America and little portions of east-central Central America, southern
North America, and north and south-central South America, with one VU species (Cr. acutus); west-central
Africa and a little portions of northern Ethiopia, with three VU species (Cr. suchus, O. osborni, and O. tetraspis);
a little portions of southeastern Iran, southern Pakistan, India, Sri Lanka, a little portions of southern Nepal,
parts of Malaysia and Indonesia, and northern Oceania, with two VU species (Cr. palustris and T. schlengelii).

Discussion
Our results show different patterns of TD, FD and PD around the world and show the importance of using the
three dimensions of diversity for conservation strategies by aggregating the evolutionary history and ecology
of species. South America showed the highest TD values, and southern North America and northern South
America had the highest PD values. This pattern is probably due to the evolutionary history of crocodilians in
the Americas with two lineages of phylogenetically distinct origins (i.e. Alligatoroidea and Gavialoidea). The
species with Alligatoroidea form has a robust body, broad head and skulls, and low saltwater tolerance, the species
that evolved in North America (genus Alligator is extant) dispersed from North to Central and South America
­diversifying26. Three genera are currently extant in South America (Caiman, Melanosuchus, and Paleosuchus26).
Currently, two basal species of the subfamily Alligatorinae live in colder areas in southern North America (A.
mississippiensis), and eastern China (A. sinensis). The other group is species with Gavialoidea forms that pos-
sibly arrived from the African continent and diversified from Central America to northern South A ­ merica27.
The Gavialoidea forms have a skull elongated and greater saltwater ­tolerance27, currently in America only the
genus Crocodylus is extant. These two evolutionary lineages that diversified in the Americas showed the highest
TD and PD values, and higher FD values.
Asia had the highest FD values, despite being concentrated in a small area in northeastern India. Although
previously occurring over a wide geographic area, today the G. gangeticus occurs in small and fragmented areas
in northeastern India, Nepal, and B ­ angladesh4. It is a species with distinctive functional traits (Fig. S2b), with a
long thin skull, a large size as an adult, an aquatic life, and high functional v­ alue28,29. Another species that occurs
in sympatry with the G. gangeticus in a small area in northeastern India is the Cr. porosus, a species with a high
saltwater tolerance and one of the largest species at its adult size. These two species living in sympatry, together

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Figure 2.  Spatial distribution on the global-scale of Nutrient Retention (Map). (a) Relationship between
Nutrient Retention and Crocodilians’ TD in North, Central and South America; (b) relationship between
Nutrient Retention and Crocodilians’ TD in Africa and the Middle East; (c) relationship between Nutrient
Retention and Crocodilians’ TD in Asia and Oceania. The maps were created in ArcGIS Pro s­ oftware60.

with Cr. palustris, provide the highest FD values in the world. In central Borneo where the species T. schlegelii
with distinct functional characteristics, such as the long and thin skull, occurs in sympatry with Cr. porosus and
Cr. siamensis promoting higher FD values. High values of PD occur in areas where the two of the most basal
species of the subfamily Gavialinae live in northeastern India (G. gangeticus) and southeastern Asia (T. schlegelii)
in sympatry with species of genus Crocodylus (subfamily Crocodylinae). In Africa, Gavialoidea forms have
diversified, and currently, three distinct extant genera occur, Crocodylus, Mecistops, and Osteolaemus (subfamily
Crocodylinae). Areas with higher PD and FD values comprise species with long thin/broad skulls, small/very
large species when adults, fairly terrestrial species/highly ­aquatic28,29, living in sympatry in west-central Africa.
Despite the same evolutionary lineages, morphological differences and habits make African species one of the
higher FD values found in this study.
Crocodilians may play a key role as contributors to nutrient and energy cycling through cross-ecosystem
movements worldwide, but there is a lack of research in this a­ rea2. Our exploratory findings show that the spatial
distribution of crocodilians is positively correlated to nutrient retention, suggesting some competing hypotheses
for the correlations found. These spatial patterns are better observed in Africa and the Americas, where higher
values of FD are found in this study. Crocodilians of Asia and Oceania have a less spatial contribution (observed
in our preliminary study) as ecological indicators of nutrient fluxes. However, they can play an important role in
cross-ecosystem linkages through their food habits and dietary intakes, mainly in northeastern India, southeast-
ern Asia, and northern Oceania which showed higher FD values. The interaction of crocodilians and nutrient
retention is a preliminary investigation, and more complex causal mechanisms should also be considered in
future studies.
Conservation practices ideally need evidence-based planning, but the fact that the species occurs in a PA,
or whether their range has a good representation in the PA networks, does not imply the conservation of this
individual species for example. Despite the distribution of half of the crocodilian species being well represented
in the global PA networks, CR species do not have a good representation in the PA networks. Crocodilian
management programs are also key in determining whether conservation efforts can be s­ ustained2. Therefore,
land use planning efforts prioritizing the establishment and maintenance of protected areas for crocodilian

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Figure 3.  Representation of distribution of crocodilian species and spatial relationship of the Mean Percentage
Overlap (MPO) between each species range and the global PA networks. Results of null models: green dots
denote values significantly higher than expected by chance, red dots denote values significantly lower than
expected by chance, and yellow (above mean) and orange (below mean) dots denote non-significant (p < 0.05)
values. (a) Crocodilian species in North, Central and South America (Amis = Alligator mississippiensis,
Cyac = Caiman yacare, Clat = Ca. latirostris, Ccro = Ca. crocodilus, Cacu = Crocodylus acutus, Cint = Cr.
intermedius, Cmor = Cr. moreletii, Crho = Cr. rhombifer, Mnig = Melanosuchus niger, Ppal = Paleosuchus
palpebrosus, Ptri = P. trigonatus). (b) Crocodilian species in Africa and the Middle East (Cnil = Cr. niloticus,
Csuc = Cr. suchus, Mcat = Mecistops cataphractus, Mlep = Me. leptorhynchus, Otet = Osteolaemus tetraspis,
Oaft = O. aftezelli, Oosb = O. osborni). (c) Crocodilian species in Asia and Oceania (Asin = A. sinensis, Chal = Cr.
halli, Cjoh = Cr. johnsoni, Cmin = Cr. mindorensis, Cnov = Cr. novaeguineae, Cpal = Cr. palustris, Cpor = Cr.
porosus, Csia = Cr. siamensis, Ggan = Gavialis gangeticus, Tsch = Tomistoma schlegelii). Dashed lines indicate the
mean percentage overlap from 1,000 randomizations, and the light blue surface represents the random range,
with 95% confidence interval. The maps were created in ArcGIS Pro ­software60 and the illustrations of species
were created by L-d-M, Lia.

conservation, require private and governmental efforts to address the degradation of the natural environment
and climate global changes.
Because of habitat loss, several crocodilian species are being h ­ ybridized30. The hybridization can result in
30
decreased fitness of hybrids and distinctive genetic l­ ineages . Because of extensive hunting pressures from the
middle of the nineteenth century, the population decline of crocodiles increased in Central and North A ­ merica31.
The crocodilian species like Cr. rhombifer and Cr. moreletii are suffering from these declines and hybridization
processes in the Caribbean ­islands11. The species Cr. acutus is a marine species and co-occurs with these two
species (i.e. Cr. rhombifer and Cr. moreletii), and if hybridized with these ­species30,32. Few populations of parental
(non-admixed) Cr. moreletii remain in the ­wild33 and Cr. rhombifer, an endemic species in Cuba, is classified as
CR by the IUCN Red L ­ ist4, which is on the verge of extinction as a result of hybridization with Cr. acutus, both
enhanced by human a­ ctivities32. Our data show that the species Cr. moreletii, despite not being a threatened
species, does not have a significant representation in the PA networks. Effective conservation and manage-
ment strategies for crocodilians are crucial to maintaining their ecological and evolutionary values in land use
­planning9,34. We suggest that the establishment of new PA with a wide spatial range covering the species, and
molecular efforts throughout its distribution are necessary for the conservation of this species.
In the Americas, three species do not have a good representation in the PA networks (A. mississippiensis, Ca
yacare, and Ca. latirostris). These species are classified as Least Concern (LC) by the IUCN Red L ­ ist4. Empirical
evidence on the A. mississippiensis in Florida demonstrated its ecosystem engineering role in creating microhabi-
tats and foraging opportunities for plants and a­ nimals35. In the case of Ca. latirostris in South America, despite
they have developed ability to colonize human-made habitats (e.g. small swamps in grasslands and secondary
woodlands), is suffering continuous anthropogenic pressures in the Atlantic F ­ orest36,37, one of the most threat-
38,39
ened hotspots of the ­world . Due to habitat loss, this species is increasingly isolated in small fragments, and
many individuals that enter urban areas are exposed to various threats, such as hunting, climate change, invasive
species, and ­pollution37,40. The species Ca. yacare occurs in the Pantanal biome in Brazil, which suffered one

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Species MPO observed MPO randomized Representativeness IUCN

Alligator mississippiensis 1.432 2.983 − LC
A. sinensis 0.000 2.037 − CR
Caiman crocodilus 6.071 2.993 + LC
Ca. latirostris 0.946 2.992 − LC
Ca. yacare 2.107 2.993 − LC
Crocodylus acutus 4.166 2.990 + VU
Cr. halli 0.350 2.066 − LC
Cr. intermedius 5.658 2.990 + CR
Cr. johnsoni 3.745 2.078 + LC
Cr. mindorensis 4.631 2.040 * CR
Cr. moreletii 2.519 3.006 * LC
Cr. niloticus 4.120 2.410 + LC
Cr. novaeguineae 3.230 2.042 + LC
Cr. palustris 0.685 2.061 − VU
Cr. porosus 3.527 2.055 + LC
Cr. rhombifer 6.109 2.968 + CR
Cr. siamensis 9.692 2.050 + CR
Cr. suchus 3.376 2.396 + VU
Gavialis gangeticus 0.515 2.052 − CR
Mecistops cataphractus 2.057 2.413 * CR
Me. leptorhynchus 3.467 2.398 + EN
Melanosuchus niger 5.206 2.995 + NT
Osteolaemus aftezelli 3.294 2.393 + EN
O. osborni 2.913 2.419 * VU
O. tetraspis 2.618 2.403 * VU
Paleosuchus palpebrosus 4.543 2.992 + LC
P. trigonatus 6.793 2.983 + LC
Tomistoma schlegelii 4.095 2.059 + VU

Table 1.  Mean percentage of spatial overlap (MPO) between the range of crocodilian species and protected
areas networks (IUCN Red List categories I to ­IV4) of the World. Results of null models describing the
representativeness of the species in protected areas: (−) denotes values significantly lower than expected by
chance, (+) denotes values significantly higher than expected by chance, and (*) denotes non-significant
(p < 0.05) values. IUCN Red List categories for all 28 crocodilian species: CR – Critically Endangered, EN
– Endangered, LC – Least Concern, NT – Near Threatened, VU – Vulnerable.

recent environmental disaster of anthropic origin (i.e. an intentional fire that reached huge ­proportions41). In
addition to the death of animals in this biome, the catastrophic event triggered negative hydrological ­effects42,
with many populations of Ca. yacare suffering from dehydration and infectious diseases in the worst affected
areas, which raised the species’ mortality rate in this ­region42 (see Fig. S1). The loss of Ca. yacare in this region
can disproportionately disrupt the ecosystem structure and ­function43, which may cause an ecological problem
termed ‘trophic downgrading’ induced by lower-order ­consumers44,45. Although these species are not considered
threatened, the low representation in the PA networks in areas so altered by human actions, makes them possibly
threatened in the future due to climate changes associated with environmental degradation. Therefore, improving
conservation actions for crocodilians in human-induced landscapes can avoid the extinction or decline in the
population of crocodilian species with further impacts on food web dynamics and ecosystem stability.
In Asia and Oceania, the most alarming cases concern G. gangeticus, Cr. palustris, A. sinensis, and Cr. halli
(see Fig. 3). The species A. sinensis is classified as CR by the IUCN Red L ­ ist4. Because of decreasing of the popu-
lation of A. sinensis, strategies for the conservation of this species are fundamental, thus some implications for
the management of captive breeding have been ­implemented46. However, these individuals in captivity decrease
the genetic diversity, resulting in a bottleneck e­ ffect47. It appears that isolated habitats may provide an environ-
ment with low exposure to pathogens, and genes have no motivation to change, causing an increase in similar
genes across captive p ­ opulations47. Our findings showed that A. sinensis has a representation non-existent in
the PA networks, the establishment of protected areas in its range is essential for its conservation. In the case of
the gharial (G. gangeticus—classified as CR by the IUCN Red List)4, the bottleneck effect occurs because habitat
fragmentation isolated the populations, decreasing genetic d ­ iversity48. Previous conservation efforts in India
concerning the threatened G. gangeticus benefit numerous other species at regional s­ cales49–51. This suggests that
for success in conserving crocodilians, the populations should be maintained in large PA networks, maximizing
the representation of catchments and linear riparian systems, and maintaining their evolutionary history, genetic
variability, and ecological functions.

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Figure 4.  Spatial distribution of the conservation prioritization models on a global scale, based on the three
dimensions of crocodilian diversity (TD, FD and PD) and spatial distribution of threatened species. The maps
were created in ArcGIS Pro ­software60 and the illustrations of species were created by L-d-M. Lia.

Our results show that two threatened species that occur in India, have low representation in protected areas;
CR species G. gangeticus with MPO = 0.515%, and VU species Cr. palustris with MPO = 0.685%. Unfortunately,
we did not have access to PA networks in India which do not provide data to UNEP, WCMC & ­IUCN52. However,
according to the Wild Life Institute of India (https://​wii.​gov.​in/​nwdc_​about​us), India has a PA network with 990
areas covering 5.27% of the country’s geographical area, with 106 National Parks and 565 Wildlife Sanctuaries, so
the MPO results may be better for these species. Anyway, India enters Model 1(covering 20.45% of the priority
area, see Table 2) and Model 3 (see Fig. 4) of conservation as one of the main areas for the establishment and
maintenance of PA.
Our results show important patterns for the evaluation of species to be considered: (i) species threatened and
not represented (A. sinensis, Cr. palustris, G. gangeticus) or with non-significant results (Cr. mindorensis, Me.
cataphractus, O. osborni, O. tetraspis) in the current coverage of PA networks. These are the most alarming cases,
the establishment or maintenance of PA is extremely important, and these species may be at serious risk of extinc-
tion; (ii) species not considered threatened by the IUCN, but threatened by anthropic actions in which our data
show that they are not well represented or with non-significant results in the PA networks (A. mississippiensis,
Ca. yacare, Ca. latirostris, Cr. halli, Cr. morelleti). These species can be considered as indicators for priority areas
for the establishment of PA, to avoid a drastic decrease in their populations; (iii) threatened species with good
representation in the PA networks (Cr. acutus, Cr. suchus, Me. leptorhyncus, O. aftzelli, T. schlegelii). The MPO
analysis is based on the total area of occurrence of the species and their occurrence in the PA network, most of
these species have a representativeness percentage with their coverage lower than 5% of MPO, recommending
the establishment of new PA in their areas of occurrence connecting populations. In the case of Cr. intermedius,
Cr. rhombifer, and Cr. siamensis have coverage above 5.5%, and almost all of their distribution is in PA, which
denotes the importance of these PA and the connections between them are extremely important for the conserva-
tion of these CR species; and (iv) species not threatened and well represented in the network of protected areas
(Ca. crocodilus, Cr. johnsoni, Cr. niloticus, Cr. novaeguineae, Cr. porosus, Melanosuchus niger, P. palpebrosus, P.
trigonatus). These are the species of the least concern. However, it is important to clarify that our analysis for
these species were based on the ­IUCN4 distribution data (i.e. polygons) and did not analyze their population
size. Therefore, being well-represented does not exclude the possibility of being threatened by anthropic actions.
In addition, they strongly contribute to the values of TD, FD and PD, and should be considered when choosing
and maintaining priority areas.
We argue for the use of Model 1 as the main ecological indicator for crocodilian conservation on Earth (see
details in Fig. 4, Table 2). However, Models 2 and 3 also show important areas for crocodilian conservation such
as Central America, South America, west-central Africa, India, Sri Lanka, southeastern Asia, and northern Oce-
ania (see Fig. 4). Model 2 and 3 also shows important areas for crocodilian conservation in Pantanal and Atlantic
Forest biomes, in Brazil (Fig. 4), comprising two species of the genus Caiman (Ca. yacare and Ca. latirostris) that
are not well represented in the PA networks. Another priority area for conservation in New Guinea and Papua
New Guinea, where there the recently described species of the crocodile (Cr. halli) is not well represented in

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Country Area ­(km2) Relative percentage (%)

Bangladesh 234,963.48 69.41
Benin 117,057.68 61.91
Bolivia 143,981.29 12.40
Brazil 618,214.55 6.98
Burkina Faso 12,068.24 4.01
Cambodia 258,627.70 82.64
Cameroon 509,056.90 84.55
Central African Republic 232,748.66 24.13
Chad 36,499.10 2.87
China 254,398.23 2.82
Colombia 640,940.08 56.50
Cuba 107,415.63 100.00
Democratic Republic of the Congo 36,859.72 1.61
Ghana 228,481.86 95.58
Guinea 317,132.00 92.96
Guinea-Bissau 19,072.10 100.00
Guyana 32,564.25 15.47
India 644,551.70 20.45
Indonesia 120,355.71 6.41
Ivory Coast 423,054.19 100.00
Laos 47,367.70 20.60
Liberia 120,610.98 100.00
Myanmar 35,114.95 5.26
Nepal 10,850.34 7.37
Niger 60,123.45 5.09
Nigeria 600,591.30 66.10
Peru 96,233.90 7.45
Philippines 105,439.76 36.06
Republic of the Gambia 110,856.15 65.31
Thailand 78,055.34 15.24
United States 62,452.63 0.85
Venezuela 493,966.75 54.45
Vietnam 49,391.12 15.23

Table 2.  Areas with the highest priority for crocodilian conservation worldwide and their relative percentage
by country. Areas denote regions selected by Model 1 (i.e. FD, PD and TD higher than 90% of the total
observed and with the presence of CR ­species4).

the PA networks. Global challenges for conserving the three dimensions of crocodilian diversity require more
research and practical recommendations. However, the existing global PA networks have extreme importance
for the conservation of the ecological and evolutionary values of crocodilians in the world.
It is important to emphasize that our model followed the distribution of species from the most recent literature
or database found, and species such as Me. catapractus may be considered extinct or unconfirmed in some areas
such as Benin and Nigeria. These unconfirmed areas can be critical areas for study focus and the establishment
of protected areas for crocodilian species and should be considered. For species that occur in India such as Cr.
palustris and China (A. sinensis), further confirmation of their distribution is needed as well as their presence
in the PA networks.
Our models represent new conservation areas with a maximum relevance of evolutionary and ecological
values for crocodilians and can help in the choice for the establishment or expansion of protected areas at dif-
ferent scales. We suggest the following steps in the application of the models: (i) choice of the model; (ii) pres-
ence of threatened species; (iii) confirmation of the presence of the species in the area; and (iv) ensuring that
areas contain suitable environments for the species (i.e. maximizing the representation of catchments and linear
riparian systems).
In the present study, we report key conservation areas that incorporate the three dimensions of crocodilian
diversity (i.e. TD, FD and PD) under an integrative landscape plan. Our results emphasize global priority areas
for crocodilian conservation, using evidence-based planning with multiple crocodilian diversity components.
However, these findings demand political will and applied environmental actions in balance with social interests
to reduce extinction risk and avoid species loss. In addition, maintenance and efforts in the PA networks may
help prevent catastrophic encounters with crocodilians and humans. By using crocodilians as umbrella species

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for conservation, many species that co-occur with crocodilian species will benefit. Therefore, using multiple
biodiversity components in balance with the landscape and their potential threats is essential to improve future
strategies in designing effective conservation models.

Methods
Spatial data. We created an updated database with geographic distribution maps of the IUCN Red List, ver-
sion 2022-14 for all species of crocodilians distributed on a global scale, and Smolenski et al.53, Shirley et al.54,55,
Murray et al.56, Hekkala et al.57, Mobaraki et al.58, Cunninghan et al.59, and Platt et al.60 for actualized distribu-
tions of Osteolaemus, Mecistops, Crocodylus halli, Cr. novaguinae, Cr. palustris, Cr. niloticus, Cr. suchus, and Cr
siamensis respectively. We use the most up-to-date distribution of the species. Then, we created a presence/
absence matrix, superimposing the species distribution data on a grid system with a spatial resolution of 0.5
degrees, using ArcGIS Pro s­ oftware61. In total, we assessed the geographical ranges of 28 crocodilian species
covered by our grid system of 38,974 grid cells.

Calculating taxonomic, functional and phylogenetic diversity. We calculated and mapped taxo-
nomic diversity (TD) by summing the number of crocodile species in each cell of the world grid. We calculated
the FD of Crocodilians through a database of Griffith et al.28 and the present study totalized 13 functional traits
divided into five categories of morphology, life history, and behavior characteristics (e.g.25,28,62). The functional
traits were categorized as (1) body size (largest male size and female size at maturity); (2) habitat type (generality,
salt tolerance, and terrestriality); (3) tolerance to extreme climates (aestivation and brumation); (4) potential to
act as ecosystem engineers (ability to dig burrows); (5) activity (day, night, and both); (6) diet/foraging strategy
(diet generality, skull shape, bite force); (7) Reproduction (nest type, relative clutch mass). The skull shape was
combined as a single trait (see Griffith et al.28). For further details of specific functions and ecosystem-support-
ing services of each one of the functional traits assessed, see Griffith et al.28 and Supplementary Tables S1 and S2.
We followed the protocol proposed by Petchey and G ­ aston16 to calculate FD: (1) construction of a species-
trait matrix; (2) conversion of the species-trait matrix into a distance matrix; (3) clustering distance matrix into
a dendrogram (UPGMA); and (4) calculating functional diversity by summing dendrogram branch lengths of
species community. To create distance matrices, we used the method Gower d ­ istance63.
We based the phylogenetic distance on the phylogeny proposed by Colston et al.64 which contains 27 of the
species. We used the software ­R65 for the reconstruction of the phylogenetic tree using the package ‘ape’. For phy-
logenetic analysis, we used Faith’s PD ­index66 because has appropriate ways of accounting for relatedness between
taxa and evolutionary history in a conservation ­context67. Faith’s PD index comprises the sum of the branch
lengths of the phylogenetic tree of all species assessed and is often used in the assessment of phylogenetic diversity
of co-occurring species (e.g.68–70). The analyses were done for each grid cell of 0.5 degrees (38,974 grid cells).
We verified whether FD and PD were influenced by species r­ ichness71, using independent swap null m ­ odels72.
The values provided by such models are more sensitive to preserving both site diversity and species frequency
of occurrence while randomizing the pairs of species/sites, which ensures that patterns of trait assembly do not
simply reflect the differential occurrence of s­ pecies1,72. The null model is independent of the species richness
of an a­ ssemblage71, which provides expected values at different species richness l­ evels73. Hence, we tested if the
functional and phylogenetic diversity were higher, equal, or lower than expected by chance for each grid cell
(random or non-random pattern), assuming a random distribution in which every species could occupy any grid
cell in the biome. We computed 1000 replicates of random remaining PD and FD, allowing us to obtain a p-value
of predicted PD and FD as compared to the distribution of the random replicates. We correlated the values
obtained for TD, FD and PD in each grid cell using simple linear correlation models (normality was evaluated
using the Shapiro–Wilk test). All analyses were performed using the packages ‘ade4’, ‘picante’, ‘FD’, and ‘vegan’
through the R s­ oftware65. The Phylogenetic Tree and Functional Tree are available in Supplementary Fig. S2.

Estimating crocodilians vs nutrient retention relationships. To estimate the potential correlations

of crocodilians to ecosystem services of nutrient retention, we used the global data provided by Chaplin-Kramer
et al.74 and map it on our grid system under a spatial resolution of 0.5°. The nutrient retention data were provided
from the InVEST (Integrated Valuation of Ecosystem Services and Tradeoffs) nutrient delivery ­model75, which is
used to map nutrient sources from watersheds and their transport to the streams based on land cover. Nutrient
retention maps reflect the pollution avoided in water-related ecosystems and are assessed by subtracting nitro-
gen load and nitrogen export values for water purification services. For these analyses, we used correlation linear
models between TD, FD and PD vs. nutrient retention for Americas, Africa/Middle East, and Asia/Oceania,
through the package ‘vegan’, in the R ­software65.

Calculating the effectiveness of the existing PA networks. To compile a list of species supported by
the PA networks available from UNEP-WCMC & ­IUCN52, we compiled spatial data on the distribution of PA
networks in the world within the IUCN Red List categories (i.e. I to IV)4, which represent the National, State,
and Municipal reserves, totaling 38,010 PA. We then superimposed the species distribution data on a gridded
representation of the PA separately according to region, Americas (included South, Central and North America,
8223 PA), Africa (included all Africa and the Middle East, 1217 PA), and Asia/Oceania (included all Asia and
Oceania, 28,579 PA) for each grid cell of resolution of 0.5 degrees. In preparation for the subsequent analyses,
we used ArcGIS Pro ­software60 to create a presence/absence matrix of species per grid cell Americas (11,358
grid cells), Africa/Middle East (12,753 grid cells), and Asia/Oceania (14,863 grid cells) a matrix describing the
percentage of the grid cell occupied by PA.

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To demonstrate the level of representativeness of crocodilian species in the existing PA networks in the world,
we calculated the Mean Percentage Overlap—MPO76,77. The MPO corresponds to the mean percentage of spatial
overlap between the units in which the species occurs in the studied area and the protected areas. We obtained
the spatial overlap (%) of each cell of the study area with the polygons of the PA networks. Then, we used null
models to test if the level of the MPO of each species was significantly different (lower or higher) than expected by
chance, considering the number of occupied cells of each species (i.e. range size). For that, we used the software
­R64 to compare the observed MPO value of each species with MPO values obtained from 1000 randomizations
using a significance level of p < 0.05.

Mapping the priority conservation areas. To map the priority conservation areas, we implemented
three dimensions of the crocodilian diversity (TD, PD and FD), and the presence of threatened species following
the IUCN Red List c­ riteria4. For the conservation status of threatened species, we used the three major catego-
ries of the Red List assessments (CR = Critically Endangered, EN = Endangered, and VU = Vulnerable)4. Then,
we run three prioritization models based on different levels of complementary scenarios adapted from Campos
et al.18, as follows:
  n 
Model1(90%) = FD ≥ (0.9(( FD)/N))/0.5 + PD
i=0
 n     n   
≥ 0.9 PD /N /0.5 + TD ≥ 0.9(( TD)/N) /0.5 + CR ,
i=0 i=0

  n   
Model2(70%) = FD ≥ 0.7 FD /N /0.7 + PD
i=0
 n     n    
≥ 0.7 PD /N /0.5 + TD ≥ 0.7 TD /N /0.5 + EN
i=0 i=0
− Model1(90%) ,
  n  
Model3(50%) = FD ≥ 0.5 FD /N + PD
i=0
 n     n   
≥ 0.5 PD /N + TD ≥ 0.5 TD /N + VU
i=0 i=0
− Model2(70%) .
Model 1 identifies areas that hold very high priority for conservation because of levels of per-cell FD, PD,
and TD ≥ 90% (0.9) of the total observed (N), and the presence of CR ­species4; Model 2 identifies areas that hold
high levels of per-cell FD, PD, and TD ≥ 70% (0.7) of the total observed (N), and the presence of EN ­species4;
Model 3 identifies areas that hold medium levels of per-cell FD, PD, and TD ≥ 50% (0.5) of the total observed
(N), and the presence of VU s­ pecies4.
The main reason for this modeling approach was to select areas from medium to very high priority, leaving out
low-priority regions. In this context, these models allow practical recommendations for crocodilian conservation
efforts and provide a spatial prioritization ranking worldwide.

Data availability
All data generated or analyzed during this study are included in this article and its Supplementary Information
files. No live animals were used in this study.

Received: 11 May 2022; Accepted: 18 January 2023

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Acknowledgements
The authors thank Lia Lourenço-de-Moraes for the illustrations. This work was supported by the Portu-
guese Foundation for Science and Technology (FCT) (PTDC/CTA-AMB/28438/2017), under the project—
UIDB/04152/2020—Information Management Research Center (MagIC/NOVA IMS), and the European Union-
Next Generation EU. This study was financed in part by the CAPES—Finance Code 001.

Author contributions
R.L-d-M.: conceived the ideas of the study; R.L-d-M.: wrote the manuscript with important contributions for
the other authors; R.L-d-M.: designed methodology with an important contribution by F.S.C. R.L-d-M., T.S.-S.,
Y.N., F.S.C., and A.C.: collected the data; R.L-d-M.: analyzed the data. R.L-d-M. and F.S.C.: created the figures
and tables. R.L-d-M., F.S.C., P.C., T.S.-S., Y.N., A.C., and F.G.R.F.: contributed critically to the drafts and gave
final approval for publication.

Competing interests
The authors declare no competing interests.

Additional information
Supplementary Information The online version contains supplementary material available at https://​doi.​org/​
10.​1038/​s41598-​023-​28413-6.
Correspondence and requests for materials should be addressed to R.L.-d.-M. or F.S.C.
Reprints and permissions information is available at www.nature.com/reprints.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and
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