Research Article |
Corresponding author: Haleigh A. Ray ( haray@stetson.edu ) Academic editor: Michael McKinney
© 2024 Haleigh A. Ray, Elizabeth P. Tristano, Kirsten A. Work.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ray HA, Tristano EP, Work KA (2024) Exotic species swapping: Reciprocal movement of animal species among regions of the Americas. NeoBiota 94: 289-310. https://doi.org/10.3897/neobiota.94.124500
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The movement of exotic species, both intentional and unintentional, is among the top threats to global biodiversity and native taxa. Research has frequently explored species movement between the eastern and western hemispheres, focusing on the number of species moving from east to west. Here we use qualitative and quantitative information from a compiled exotic species compendium (CABI Digital Library) to produce a conservative picture of the exchange of nonnative animal species, trends in movement of various taxa among regions, and the trade relationships that could contribute to species’ movements strictly within four major regions of the western hemisphere (North America, South America, Central America, and the Caribbean). Species exchange between regions in the western hemisphere (285) were higher than documented invasions from all regions of the eastern hemisphere with the exception of Asia, the largest region in the study (348). Among the broad taxonomic categories, arthropods and fish dominated the counts of exchanged species in every region, largely due to trade related to food production, aesthetics, or sport. Perhaps due to the importance of trade-related movement vectors for the dominant taxa, country GDP was positively related to export of exotic species. Therefore, the magnitude and importance of species exchanges among countries in the western hemisphere has been underestimated, with factors like proximity and economic trade connections likely leading to more species translocations.
Economic activity, exotic species, international trade, species translocation, vectors
The long history of global colonization by European powers has resulted in transport of species around the world and produced historical records of species’ movements. These records include domesticated animals such as pigs, game species, or species introduced by Acclimatization Societies, which released animals with the express purpose of having them naturalize in colonized regions. From the 900s to 1900s, explorers and colonists released these species explicitly to become naturalized for food and aesthetic enjoyment, a phenomenon coined “ecological imperialism” (
The origins and directions of these modern invasions may correlate with national GDP (
In these exchanges, the presence of movement vectors, the specific characteristics of individual species, and the characteristics of the receiving sites all can contribute to successful species invasions. In general, species that are linked in some way to human activity are more likely to move between continents and countries (
Of course, intentional movement of attractive species or hitchhiking on such species does not ensure a successful invasion; plasticity of behavior, lifestyle, and physiology as well as high productivity greatly increase, although do not guarantee, the likelihood of invasion success. The ability to change investment in reproduction, such as crabs that may produce more or fewer broods with changing resource availability, can allow populations in new habitats to persist in lean, and grow under, flush conditions. Omnivory can reinforce the ability to capitalize on variable resources to support population growth and expansion (
Movement and establishment of invasive species ranks high, along with habitat loss/degradation and climate change, in the threats to the world’s biodiversity (
To evaluate the movement of nonnative species within regions of the Americas, we collected lists of exotic species for each country in North, Central, and South America and in the Caribbean from the CABI Invasive Species Compendium (
To put the western hemisphere data into context, we plotted the total number of species that have invaded the western hemisphere from other countries in the western hemisphere (the Americas), but also from Australia and New Zealand, Asia, Europe, Middle East, and Africa. When the origin information was broad or not clear, we assigned them to a Not Specified category.
We used the R package circlize (
To visualize patterns in the origin and end movement of invasive species, we constructed webs of species movement using the R package bipartite version 2.19 (
To evaluate whether the regions differed in the number of nonindigenous species that arrived within their borders, we compared the numbers of these species that entered the four different regions to a null hypothesis of equal movement among regions with chi-square tests. To evaluate whether some taxa were more likely to move, we compared the number of nonindigenous species among the different taxa in the database to a null hypothesis of equal movement among taxa with a chi-square test. A country or region with a lot of international trade or traffic might be expected to both import and export more species, so we compared the total number of species exported from one region to the next (e.g., from North America to Central America) with its reciprocal (e.g., from Central America to North America) with linear regression. However, species at different taxonomic levels might move using different vectors, so we repeated this regression analysis using the different phyla or classes for which there were sufficient numbers of species in a taxonomic category for analysis. These analyses were performed in RStudio (
To understand how the regions differed in the types of species that they were receiving, we used nonmetric multidimensional scaling (nMDS) ordination of fourth root-transformed variables that represented the counts of species in each taxonomic group in each country of the Americas. This ordination was based on a resemblance matrix of Euclidean distances between countries (
Finally, we examined whether trade might have affected species movement. We compared the number of species that moved by different vectors to a null hypothesis of equal movement by all vector types using chi-square tests. To evaluate the potential effect of trade activity on species movement, we collected the national Gross Domestic Product (GDP) from The
For species coming into North America, South America, Central America, and the Caribbean, Asia contributed the greatest number of imported species (348 invasions). However, nearly as many of the species imported into these western regions originated within the Americas (285 invasions, Fig.
Origin of exotic animal species found in four regions of the Americas. North America has been the largest recipient of exotic species (453), followed by South America (214), Caribbean (172), and Central America (115).
The proportion of invertebrate and vertebrate species indigenous to one of the countries in the Americas or indigenous to a country outside of the Americas (Eurasia, Africa, or Oceania) that have moved into a country within the Americas outside of their original range.
Across all taxa, the number of species that were exported from a region was comparable to the number of species imported to that region (Regression: r2 = 0.57, F1,4 = 7.76, p = 0.05, Fig.
Reciprocal swaps of animal species in aggregate. Solid line is the regression line, whereas the dotted line is the 1:1 line, indicating equal numbers of species swapped between regions (North America - NA, South America - SA, Central America - CA, Caribbean - Carib).
All regions traded species, but regions differed in the number of species that they contributed to the database (Chi-square: X2 = 228.33, df = 3, p = 2.7×10-12). North and South America contributed the largest number of exported species, and the number of species in the database that originated in these two regions were roughly equal (116 vs. 112). Compared to the large continents to the north and south, the Caribbean exported approximately half the number of species (52) and Central America approximately one quarter (27) of the number of species exported by their neighboring regions (Fig.
Exchange of animal species between North America, South America, Central America, and the Caribbean. The largest exchanges were between North and South America, with South America being the highest exporter of exotic species.
Of the four countries highlighted in our analysis, all exported species widely, sending species to 24–44 countries. This export was lopsided; for example, the US sent the largest number of species to the rest of North America (Canada and Mexico), but it was the largest receiver of species from Cuba, Costa Rica, and Brazil by far (Fig.
Largest animal species-exporting countries in each of our four major regions A United States B Cuba C Costa Rica, and D Brazil Bars with color represent interactions with at least five species sent to the receiving country. All three of the non-North American countries sent the most species to the United States.
The taxa differed in their representation in the database (Chi-square: X2 = 2410.4, df = 8, p = 5.9×10-48) with a greater number of arthropods and fish than other taxa in the countries’ nonindigenous species lists (Fig.
Invasion abundance of different animal taxa into each of the four regions of the Americas (North America - NA, South America - SA, Central America - CA, Caribbean - Carib).
nMDS plot of the differences in taxon composition of invading animal species in different regions of the Americas (North America - NA, South America - SA, Central America - CA, Caribbean - Carib).
The largest number of arthropod exchanges occurred between North America and South America, although both regions contributed large numbers of species to Central America and the Caribbean (Fig.
The recorded exchanges of A arthropods (n = 79) B molluscs (n = 19) C fish (n = 72) D reptiles and amphibians (n = 34) E birds (n = 7), and F mammals (n = 10) between regions of the Americas. Green bars show the regions that exported the taxa, whereas blue bars show the region that imported the taxa (North America - NA, South America - SA, Central America - CA, Caribbean - Carib).
The American exchanges of animal genera that were represented by more than two species in the database. For molluscs, only one genus included more than two species: A Pomacea (n = 6). For fish, four genera included more than two species: B Pterygoplichthys (n = 3) C Cichlasoma (n = 6) D Poecilia (n = 3), and E Lepomis (n = 4). Amphibians and reptiles were each represented by one genus only: F Eleutherodactylus (n = 3) and G Anolis (n = 11). Areas colored red represent native ranges, whereas areas colored orange represent introduced ranges with arrows showing the direction of movement. Arrow color represents region of origin (green = South America, purple = North America, blue = Caribbean, teal = Central America).
For vertebrates, the directions of species’ movements also were variable. A disproportionate number of the fish species that moved between regions originated in North America, which also received the most fish. Most of these contributions were from either Central America or South America (Fig.
In contrast, the largest number of amphibian and reptile species that moved between regions originated from Caribbean islands (Fig.
Vectors differed in the number of species that they transported, both for different regions (Chi-square: X2 = 70.8, df = 21, p = 2.63×10-7) and for different taxa (Chi-square: X2 = 190.0, df = 64, p = 2.02×10-14). For North America, the most important vector moving species into the region was food production. Although this vector also was important for species’ movement into Central and South America, the pet and ornamental species trade moved more species into these regions. In the Caribbean, the pet and ornamental species trade also moved a lot of species, but many species also moved by hitchhiking (Fig.
Importance of different transport vectors in moving animal species into the four regions of the Americas (a) and in moving different taxa among regions (b) (North America - NA, South America - SA, Central America - CA, Caribbean - Carib).
The importance of different vectors also varied greatly among taxa (Fig.
For all countries that reported GDP, this symbol of economic activity significantly predicted the number of native species that have been moved from one country to another within the Americas (Regression: r2 = 0.51, F1,39 = 42.25, p = 1.05×10-7). Countries with a higher GDP exported more species (Fig.
The relationship between countries’ GDP and the number of animal species exports. Grey squares labeled “NA” represent North America, purple circles labeled “CA” represent Central America, green triangles labeled “C” represent the Caribbean, and blue diamonds labeled “SA” represent South America. The line is a regression line, with r2 = 0.51.
This study suggests that species have been swapped extensively among countries in the western hemisphere, particularly between countries in close proximity (e.g., Cuba and Jamaica) or with strong trade ties (e.g., the US and Brazil) (
While recognition of the problem is an important goal on its own, investigation of the vectors of transport point to possible avenues for reducing the problem. For North, Central, and South America, some of the most common exports were associated with food, sport, and ornamental trade, such as intentional transport for use in aquaculture/sport fishing/hunting or unintentional transport as hitchhikers with plants. On the other hand, for Central America, South America, and the Caribbean, transport of species as pets or for ornamental uses (or as ornamental hitchhikers) were the most common types of species movement. These vectors have been associated with exotic species’ movement globally (
The effect of global trade and travel on species transport may be a long story.
Of the 25 biodiversity hotspots identified by
The success and effect of invasions may depend on the condition of the habitat, including the level of disturbance and the presence of other exotic species (
Species invasions clearly are a world-wide problem, only increasing with global travel and transport (
We would like to thank the multitudes of researchers contributing research to the exotic species literature and to the CABI datasets. We also would like to thank Janardan Mainali for work in starting up the project.
The authors have declared that no competing interests exist.
No ethical statement was reported.
No funding was reported.
All authors have contributed equally.
Haleigh A. Ray https://orcid.org/0000-0003-2153-4813
Elizabeth P. Tristano https://orcid.org/0000-0002-3365-2123
Kirsten A. Work https://orcid.org/0000-0002-0116-1223
Data used are available with open access from the Exotic Species Compendium in the CABI Digital Library (https://www.cabi.org/isc/about).