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Note that a Preprint of this article also exists, first published June 12, 2015.

Introduction

The live aquarium fish trade faces a multitude of potential threats, including incidences of reduced biodiversity from over-extraction, habitat destruction in some source countries (Francis-Floyd & Klinger, 2003; Gopakumar & Ignatius, 2006), and negative impacts of species invasions in the US and elsewhere (Chucholl, 2013; García-Berthou, 2007; Holmberg et al., 2015; Padilla & Williams, 2004). Despite these threats, the aquarium trade can be a unique and significant positive force in reef-side communities (Rhyne, Tlusty & Kaufman, 2014). Benefits include but are not limited to saving threatened species from the brink of extinction through the development of captive breeding programs (Tlusty, 2002) and catalyzing habitat preservation through sustainable supply-side practices (Firchau, Dowd & Tlusty, 2013). These sustainable practices include stewardship, mechanisms for sustainable livelihoods via poverty alleviation, and the protection of threatened ecosystems (Rhyne, Tlusty & Kaufman, 2014). Finally, consumer education of aquarium trade sustainability can promote widespread public appreciation for the world’s aquatic ecosystems, with the ultimate goal of minimizing negative impacts of this trade (Tlusty et al., 2013). While a proactive stance can transform a large consumer base into a powerful agent for biodiversity conservation, increased sustainability, and human well-being, inaction will likely amplify the deleterious threats currently faced by the trade. Currently, the lack of oversight leading to a poor concept of trade volume and subsequent regulatory inefficiency has greatly hampered the development of a sustainable industry. Increasing the sustainability of the marine aquarium animal industry should be considered a primary initiative for the entire aquarium industry transport chain (Tlusty et al., 2013). Increasing the sustainability of the transport chain of marine aquarium animals is achieved through a more thorough understanding of the magnitude of the trade (Fujita et al., 2014), which begins by assessing the scale of imports into the US (the primary destination) (Rhyne et al., 2012). Once the annual volume of US imports is gauged, other relevant issues that lead to environmental and economic benefits can then be tackled, including animal quality and shipping survival.

There is no clear picture of the number of live marine fish and invertebrate species or individuals involved in the aquarium trade, primarily due to insufficient global tracking of the import and export of these animals (Bruckner, 2001; Fujita et al., 2014; Green, 2003; Lunn & Moreau, 2004; Tissot et al., 2010; Wabnitz et al., 2003). Multiple sources of data have been used to monitor this trade (Green, 2003; Smith et al., 2008; Wabnitz et al., 2003; Wood, 2001). However, not all of these data systems are sufficient for, or were even intended for, monitoring the aquarium trade. For example, compulsory data are maintained under federal mandates for species listed by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). However, previous studies found that CITES records were inaccurate, incomplete, or insufficient (Bickford et al., 2011; Blundell & Mascia, 2005; Rhyne et al., 2012). Furthermore, CITES-listed species (namely stony corals, giant clams, and seahorses) account for only a fraction of the total trade in live aquatic animals. Only a handful of studies (Rhyne et al., 2012; Smith et al., 2009; Smith et al., 2008) have attempted to quantify the movement of non-CITES-listed aquarium species from source to market. The Global Marine Aquarium Database (GMAD) encouraged companies to provide data on the marine aquarium trade (Green, 2003) and, until now, GMAD was the only source for aquarium trade data recorded at a species-specific level. While GMAD contains trade data from 1988 to 2003, some years and countries (e.g., Haiti) are missing, and values reported in GMAD were found to be drastically fewer than other estimates of trade data (Murray et al., 2012). Furthermore, the aquarium trade has been transformed by new technologies and husbandry breakthroughs since 2003 (Rhyne & Tlusty, 2012) which may dilute the relevance of this data set. In addition to CITES and GMAD, the Law Enforcement Management Information System (LEMIS) database has been used to better understand the aquarium trade. The United States Fish and Wildlife Service (USFWS) inspects wildlife shipments and, through LEMIS, maintains species-specific data in the case of transporting CITES-listed species per CITES requirements. However, non-CITES-listed species are recorded with general codes (e.g., marine aquarium tropical fish, regardless of species, are coded MATF). Recording data in this generalized manner eliminates specific information regarding the diversity and volumes of species traded (Smith et al., 2009). While the need for accurate accounts of aquarium trade flow continually increases, the current monitoring methods remain static (Bickford et al., 2011). The lack of specific data systems for recording all species exported and imported for the marine aquarium trade raises two main concerns: (1) because of the lack of trade data, it is unclear how importing and exporting governments can monitor this industry effectively; (2) it is also unclear how sustainability should be encouraged given the paucity of data.

To date, Balboa (2003), Wabnitz et al. (2003) and Rhyne et al. (2012), have catalogued species-specific information provided on trade invoices. Rhyne et al. (2012) further compared invoice information to associated shipment declarations. It was this effort that led to the development of the Marine Aquarium Biodiversity and Trade Flow online database (https://www.aquariumtradedata.org/), a public portal offering anonymized live marine animal trade data collected through trade invoices. Here we describe three years (2008, 2009, 2011) of fish and invertebrate invoice-based data from US imports that were analyzed for country of origin, port of entry, and quantity of species and individuals associated with each port. We also relate the findings from these three years of complete trade data to previously existing invoice-based trade data from the LEMIS database. Specifically, Rhyne et al. (2012) described one contiguous year of import data, based on a 12-month period from June 2004 (seven months) until May 2005 (five months), and Balboa (2003) described one month (October) of data from 2000. To address the missing months of data from these years and to increase the scope of the dataset, we modeled data for the missing months based on the monthly volume patterns analyzed from the three complete years of data available (2008, 2009, 2011). This work provides an enlarged snapshot of the volume, biodiversity, and trade pathways for live marine aquarium fish and invertebrate species beyond the information provided by other reporting systems (Wabnitz et al., 2003). Further, this work demonstrates that LEMIS, while well-designed for import/export compliance and management of USFWS staffing needs, is not designed to monitor the species-level activity of the live marine aquarium trade. Finally, we present two case studies (the Banggai cardinalfish, Pterapogon kauderni, and the common/orange clownfish, Amphiprion ocellaris/percula) to demonstrate the use of these data for better understanding the trade in marine species: a first step toward advancing industry sustainability.

Methods

The goal of this project was to evaluate the number of live marine aquarium species imported into the US, and to create a trade path analysis of the diversity of animals involved in the trade. The methods used to analyze trade invoices were described by Rhyne et al. (2012) and are briefly summarized here. We reviewed all USFWS shipment declarations and the attached commercial invoices coded as Marine Aquarium Tropical Fish (MATF) for 2008, 2009 and 2011 as indicated in the LEMIS database. While about 22,000 invoices were marked as containing MATF in the LEMIS database, we received approximately 20,000 shipment declarations and their attached invoices. CITES data are specially coded on import declarations, and thus are not integrated into this database.

Invoices were considered a true statement of shipping contents, as we were not able to assess the veracity of the information contained on the invoice. Shipment information (date, port of origin, and destination port) was collected from the declaration page, and species and quantity information was tabulated from the associated invoices and catalogued into a database. Within the trade of live marine organisms, re-export information is not recorded, and thus could not be assessed here. Both manual entry and automated optical character recognition (OCR) software (ABBYY FlexiCapture 9.0) customized for wildlife shipments (Fig. 1) were utilized to retrieve the above information from these documents. The input method varied with invoice quality and length. Manual entry was utilized when invoices were of poor quality (blurry, speckled, darkened, fonts less than six point, handwritten) or brief (less than 1/2 page), whereas all others were read using the OCR software. Once all necessary data were captured, species names were verified using World Register of Marine Species (WoRMS Editorial Board, 2015), FishBase (Froese & Pauly, 2015), and the primary literature (Appeltans et al., 2011; Froese & Pauly, 2011). We corrected species information only when species names were misspelled, listed under a junior synonym, or listed by only a common name. Species were identified to the greatest taxonomic detail available. Occasionally, genera were listed without species (e.g., ‘Chrysiptera sp.’), or the species was otherwise ambiguous (e.g., ‘hybrid Acanthurus tang’). In these cases the genus (and all higher-level taxonomic information) would be recorded, and the species would be recorded as unknown. Genus and species were recorded as unknown when listed only by an ambiguous common name (e.g., ‘colorful damsel,’ ‘unknown damsel,’ ‘assorted damsels’).

FlexiCapture 9.0 verification screen used to capture shipping data for the www.aquariumtradedata.org database.

Figure 1: FlexiCapture 9.0 verification screen used to capture shipping data for the www.aquariumtradedata.org database.

(A) Shipping declaration; (B) shipping invoice; (C) invoice table produced from Optimal Character Recognition (OCR) software. Note: grey shaded cells indicate autocorrected fields and red flags within cells indicate errors for user to correct manually.

To determine if the volume of captive-bred P. kauderni imported into the US has increased in recent years, we reviewed invoice data from Los Angeles-based importer Quality Marine for two additional recent years of imports. Quality Marine sourced fish from Thailand, and these were known to have been captive-bred given that Thailand lies outside the native range of P. kauderni. At our request, all shipments of MATF from Thailand to Quality Marine over the period of March 2012 to July 2014 were supplied and reviewed.

In accordance with Rhyne et al. (2012), this report focused on major geographic trade flows, the frequency of invoice detail to species-level, and how invoice data compared to LEMIS data. Invoice data for both fishes and invertebrates were retrieved concurrently. To help organize and visualize the trade data, a publically accessible representation of the trade data was created: the Marine Aquarium Biodiversity and Trade Flow online database (https://www.aquariumtradedata.org/). This web-based graphical user interface, powered by the open source JavaScript library D3 (http://d3js.org/), is data-rich, visually appealing, and allows users to query more than 28,000 invoices containing over 2.7 million lines of invoice data from 2000, 2004, 2005, 2008, 2009, and 2011.

To back-calculate the estimated total annual imports of marine animals during years with incomplete data sets (years 2000, 2004, 2005), we first determined the proportion of individuals imported during the time interval (one month for 2000, seven months for 2004, and five months for 2005) based on the three years for which we had a complete 12-month dataset (2008, 2009, and 2011). For these three years, there was variation between months, but the intra-month variation was less than that of the inter-month variation, suggesting that monthly import volumes were proportionally consistent. This proportion was then used to calculate the number of individuals for the unknown months using the following relation:

n P r ̄ n

where n is the known number of imports per year for 1 (2000), 5 (2004) or 7 (2005) months, and Pr is the average proportion of known imports from corresponding months from 2008, 2009 and 2011. This estimated number of animals was then allocated across the unknown months proportionally for 2000, 2004 and 2005. This method appears robust given the consistency of the most voluminous species across years (see results). We also generated estimates for the source countries and ports of entry. The database user can select the type of data to view, and within the selection tool, can select to view actual data or whether estimates should be included. Even though these numbers are estimates, we present them as numbers so that they coalesce with the complete database.

Results

All data presented in this report are available at the Marine Aquarium Biodiversity and Trade Flow online database (https://www.aquariumtradedata.org/). This site was developed to allow users to generate database queries using dropdown menus. On the “Home” tab, initial queries can be filtered through large-scale source areas such as ocean basins or countries of origin for a defined time period (Fig. 2). Following user selections, the software compiles detailed information in the form of maps, timeline charts, and other data charts that allow users to access data at a depth uncommon in user interfaces for the wildlife or seafood trades. On further analysis, it is possible, using the “Species” tab, to query a single taxonomic family, genus, or species for one or more countries and/or ports of entry. The user-friendly dropdown menus are tree-based and progressive. Figure 3 demonstrates successive screens where the user has successively selected the family Pomacentridae, the genus Amphiprion, and the species complex Amphiprion percula/ocellaris. The dashboard displays (A) a distribution map depicting the relative geographic importance using proportionally-sized red dots, and (B, C) two graphs displaying export country- and port of entry-specific volumes for the selected query. To enhance the utility of the website and promote the dissemination of the data, the user can download charts and graphs of data queries. Users can also share these charts directly to Facebook and Twitter (Fig. 4). Further, to ensure the data within the invoice-based database is an accurate representation of the trade, users can report possible errors in data or features on the website. If users find species that are likely incorrect in distribution or taxa, we can examine the invoice record, verify its contents, and update the database if needed. This system also logs how users interact with the database, which provides feedback on the number and types of queries users generated.

Main dashboard page of www.aquariumtradedata.org.

Figure 2: Main dashboard page of www.aquariumtradedata.org.

(A) Interactive trade flow map depicting exporting countries (blue circles) and ports of entry in the US (green circles); (B) Timeline chart of fishes and invertebrates imported into the US based on user-selected dates.
Drop down menus for user-generated queries in www.aquariumtradedata.org.

Figure 3: Drop down menus for user-generated queries in www.aquariumtradedata.org.

(A) Main tab with Exporting Countries/Ocean and Ports of Entry inputs; (B) Species tab with taxa selection displaying “Top 20 Species” chart; (C) “Countries of Origin” and “Ports of Entry” charts generated by the query.
Exported chart from user-generated query: countries of origin for A. percula and A. ocellaris in www.aquariumtradedata.org.

Figure 4: Exported chart from user-generated query: countries of origin for A. percula and A. ocellaris in www.aquariumtradedata.org.

Export header includes query details and export footer includes data attributes and date of last database update.

General trends

In 2008, a total of 8,299,467 individual fishes (97.4% identified to species-level) representing 1,788 species were imported into the US. The total number of fishes imported decreased to 7,102,246 in 2009 and to 6,892,960 in 2011. However, the number of species imported increased to 1,798 by 2011. While no more than 1,800 species were imported in a single year, 2,278 unique species were imported across the three-year span (Table 1).

A similar trend in the overall trade was observed for non-CITES-listed invertebrates during this time period, although the invertebrate data were less voluminous and specious compared to the fish data. A total of 4.3 million invertebrates representing 545 species were imported into the US in 2008. The total number of invertebrates imported decreased to about 3.7 million in 2009 and 2011 (Table 2). A total of 724 species were imported over the three-year span. Compared to fishes, relatively fewer invertebrates were identified to species-level (72.9%).

Export countries

Forty-five countries in total exported marine fishes to the US during the three years (Table 1), with 41, 37, and 36 countries noted in 2008, 2009, and 2011, respectively. The Philippines exported 56% of the cumulative total volume (12.7 million fishes, Fig. 5). The overall volume of fishes traded decreased by 17% between 2008 and 2011, with commensurate export decreases from the Philippines and Indonesia. Third-ranked Sri Lanka exported consistently across the three years. Exports from fourth-ranked Haiti decreased by nearly 50% between 2008 and 2011, likely due to earthquake activity in 2010.

Table 1:
Countries that exported live aquarium fishes to the US.
Data include the number of identifiable species, number of species exported in quantities greater than 1,000 individuals (>1,000 (No.)), number of individuals exported across species, and the proportion of individuals identifiable to species-level (Known (%)) by country and year.
Export Country 2008 2009 2011 2008–2011
Species Individuals Species Individuals Species Individuals Species Individuals
Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%)
Australia 115 3 12,877 100.0 162 2 8,773 100.0 199 1 9,573 99.6 298 6 31,224 99.9
Belize 49 4 9,472 99.9 45 3 8,846 99.4 39 4 14,976 99.6 63 6 33,351 99.6
Brazil 71 3 8,742 99.4 61 0 3,349 98.5 45 0 2,005 99.5 87 2 14,147 99.2
Canada 2 0 52 100.0 2 0 3 100.0 1 0 26 42.3 5 0 81 81.5
Cook Islands 23 2 4,763 100.0 27 2 3,317 100.0 34 2 8,080 100
Costa Rica 22 2 7,903 100.0 46 0 3,538 100.0 28 2 6,139 88.1 53 4 17,580 95.8
Curaçao 15 0 529 100.0 26 0 1,383 100.0 34 1 3,367 99.7 47 1 5,279 99.8
Dominican Republic 26 3 22,121 86.3 19 4 28,944 77.2 48 8 34,272 96.7 52 8 93,872 86.5
Egypt 20 0 953 92.1 20 0 953 92.1
Eritrea 52 2 9,506 99.6 44 0 3,986 99.3 62 2 13,519 99.5
Fed. States of Micronesia 131 0 5,550 97.4 131 0 5,550 97.4
Fiji 187 28 115,520 98.9 228 19 88,289 97.8 311 25 156,680 97.6 363 44 362,444 98.1
French Polynesia (Tahiti) 106 6 42,846 99.9 101 3 30,187 99.5 73 3 29,011 99 144 7 102,182 99.5
Ghana 19 0 509 99.8 19 0 686 96.1 22 0 708 95.5 33 0 1,931 96.8
Guatemala 3 0 1,055 100 3 0 343 100.0 3 0 1,398 100.0
Haiti 99 23 240,552 97.7 114 23 215,909 97.6 89 19 126,799 99 133 30 588,516 97.9
Hong Kong 9 0 262 99.2 4 0 5 100 1 0 16,510 0.3 14 0 16,777 1.9
Indonesia 973 214 2,402,733 97.2 1,009 186 1,998,195 96.9 992 181 1,867,946 97.3 1,284 234 6,331,781 97.2
Israel 7 0 666 100.0 10 2 21,985 100.0 10 0 22,651 100.0
Japan 44 0 1,133 100.0 92 0 1,137 100.0 62 0 569 92.4 132 0 2,839 98.5
Kenya 173 27 144,211 97.7 210 24 139,129 97.8 186 21 101,910 99 249 39 388,376 98.1
Kiribati 67 6 122,971 99.1 52 7 78,812 98.2 72 6 105,679 97.6 103 8 308,889 98.4
Malaysia 11 0 622 99.8 1 0 13 100.0 12 0 635 99.8
Mauritius 63 0 823 93.4 41 0 680 98.2 81 0 1,503 95.6
Mexico 90 1 5,174 99.4 40 2 12,688 96.2 62 3 15,135 98.6 118 5 33,504 97.8
Netherlands Antilles 9 0 319 100.0 9 0 319 100.0
New Caledonia 2 0 84 100.0 2 0 75 100.0 17 0 387 99.7 17 0 546 99.8
Nicaragua 72 2 8,986 98.0 31 0 1,847 93.2 83 1 10,833 97.2
Papua New Guinea 132 2 6,816 99.8 111 2 8,313 98.6 176 2 15,243 99.1
Philippines 980 255 4,694,961 97.5 1,053 248 4,024,693 97.3 1,016 258 3,901,058 97.3 1,320 315 12,732,212 97.4
Rep. of Maldives 141 5 24,574 96.4 109 4 22,093 98.9 67 11 34,360 100 174 19 81,275 98.6
Rep. of the Marshall Isl 96 6 37,972 94.0 138 9 115,686 75.1 139 13 142,068 78.7 227 19 334,174 78.8
Saudi Arabia 16 0 326 100.0 4 0 19 100.0 20 0 345 100.0
Singapore 36 1 2,606 100.0 14 1 2,520 99.8 42 4 13,949 99.5 71 3 19,081 99.6
Solomon Islands 134 8 47,262 96.5 133 6 34,773 94.9 138 10 41,673 92.5 180 15 125,588 94.7
Sri Lanka 419 30 202,632 98.0 468 34 217,116 97.1 461 28 212,407 96.7 633 57 638,606 97.2
Taiwan 33 0 1,511 98.1 29 0 897 85.3 26 1 2,444 100.0 63 0 5,007 96.3
Thailand 10 3 39,887 100.0 3 1 8,310 100.0 10 0 48,197 100.0
The Bahamas 85 0 951 100.0 45 0 432 99.8 8 0 297 100.0 98 0 1,681 99.9
Tonga 207 6 27,857 89.5 92 2 8,047 92.3 82 0 2,676 91 227 8 39,253 90.2
United Arab Emirates 7 0 77 85.7 7 0 77 85.7
United Kingdom 32 1 3,710 98.6 32 0 3,710 98.6
Vanuatu 190 3 19,704 97.2 123 1 12,671 96.8 183 0 14,405 94.1 240 11 47,195 96.2
Vietnam 146 1 14,593 99.8 112 1 6,545 99.1 102 0 4,826 99.5 183 6 26,022 99.6
Yemen 10 3 10,340 100 14 3 11,871 100.0 16 3 22,211 100.0
Total 1,788 443 8,299,467 97.4 1,780 411 7,102,246 96.7 1,798 413 6,892,960 96.7 2,278 518 22,538,637 97.0
DOI: 10.7717/peerj.2949/table-1
Table 2:
Countries that exported live aquarium invertebrates to the US.
Data include the number of identifiable species, number of species exported in quantities greater than 1,000 individuals (>1,000 (No.)), number of individuals exported across species, and the proportion of individuals identifiable to the species-level (Known (%)) by country and year.
Export Country 2008 2009 2011 2008–2011
Species Individuals Species Individuals Species Individuals Species Individuals
Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%) Total (No.) >1,000 (No.) Total (No.) Known (%)
Australia 3 0 231 37.2 16 0 1,881 99.8 34 0 1,020 90.6 43 1 3,132 92.2
Belize 8 2 49,515 56.1 7 3 83,922 57.3 12 6 292,176 58.2 17 7 425,613 57.8
Brazil 1 0.0 1 0.0
Canada 1 0 2 100.0 28 0.0 1 0 30 6.7
China 3 0 1,260 100.0 3 0 1,260 100
Costa Rica 3 0 64 100.0 3 0 64 100
Curaçao 1 0 15 100.0 4 0 911 89.1 5 0 926 89.3
Dominican Republic 6 2 93,781 99.9 5 2 133,056 100.0 18 4 107,103 96.3 19 4 333,940 98.8
Federated States of Micronesia 1 0.0 1 0.0
Fiji 6 2 52,228 15.4 9 1 25,502 20.5 23 3 28,462 22.4 29 4 106,192 18.5
French Polynesia (Tahiti) 766 0.0 3 0.0 48 47.9 3 0 814 2.8
Ghana 3 0 2,395 12.2 3 0 135 100.0 3 0 768 53.5 5 0 3,298 25.4
Guatemala 3,000 0.0 3,000 0.0
Haiti 55 24 1,409,841 92.5 63 24 1,011,683 93.3 47 26 676,134 94.4 79 34 3,097,658 93.2
Hong Kong 1 1 1,520 100.0 1 1 23,255 100.0 1 1 24,775 100.0
Indonesia 323 57 709,736 61.2 317 51 610,264 64.9 301 48 575,657 68.6 413 90 1,895,657 64.6
Japan 8 0 425 76.5 17 0 556 64 12 0 168 91.1 25 0 1,149 72.6
Kenya 18 2 13,955 57.0 17 2 44,426 26.1 22 1 14,750 53.7 30 6 73,131 37.6
Kiribati 6 0.0 18 0.0 1 0 80 15 1 0 104 11.5
Mauritius 1 0 198 100.0 1 0 198 100.0
Mexico 24 1 1,429 99.4 8 2 4,035 97.6 17 2 17,678 53.3 38 5 23,142 63.9
New Caledonia 4 0.0 4 0.0
Nicaragua 30 8 58,918 83.8 19 3 31,052 74.5 41 11 89,970 80.6
Papua New Guinea 23 0 2,323 90.5 21 2 6,336 83.9 34 3 8,659 85.6
Philippines 259 65 1,111,002 71.5 294 67 1,154,255 65.6 284 75 1,380,014 68.2 395 118 3,645,271 68.4
Rep. of Maldives 3 0 95 21.1 2 0 686 2.6 890 0.0 4 0 1,671 2.3
Rep. of the Marshall Islands 3 2 47,362 100.0 7 5 200,088 42.1 24 3 39,588 68.8 29 6 287,038 55.4
Saudi Arabia 5 0.0 5 0.0
Singapore 15 0 2,654 45.9 11 0 2,063 64.7 11 1 7,017 56.7 21 2 11,734 55.7
Solomon Islands 17 2 12,521 51.4 10 1 4,084 67.4 8 2 16,753 43.7 21 3 33,358 49.5
Sri Lanka 63 11 251,373 90.2 60 9 309,053 91.9 54 11 261,004 88.1 87 17 821,430 90.2
Thailand 1 0 250 100.0 1 0 250 100.0
The Bahamas 9 0 92 97.8 6 0 28 78.6 13 0 120 93.3
Tonga 18 3 135,089 65.6 8 2 31,214 61.0 8 1 81,918 52.6 23 3 248,221 60.7
United Arab Emirates 2 0.0 2 0.0
United Kingdom 2 0 4 100.0 2 0 4 100.0
Vanuatu 8 0 672 99.9 4 0 96 97.9 5 0 132 79.5 11 0 900 96.7
Vietnam 25 6 293,733 8.1 23 5 108,699 27.2 24 4 106,411 12.2 38 8 508,843 13.1
Total 545 137 4,256,372 73.4 537 126 3,732,213 73.1 535 138 3,662,980 72.2 724 220 11,651,565 72.9
DOI: 10.7717/peerj.2949/table-2

The US imported marine invertebrates from a total of 38 countries during the three years (Fig. 5, Table 2), although only 27 (2008, 2009) or 28 (2011) countries were noted per year. The number of individuals exported per year decreased 14% between 2008 and 2011, a rate similar to that of fishes. The countries exporting the greatest volume over the three years were the Philippines (3.6 million invertebrates) and Haiti (3.1 million invertebrates). The number of individual invertebrates exported from the Philippines increased by 24% between 2008 and 2011. This was likely a response to the decrease in volume from Haiti (52% decline from 2008 to 2011). Third-ranked Indonesia (1.8 million invertebrates) exported a consistent volume across the three years. Even though Indonesia ranked third in volume, it exported the most species (413) during the three years. The Philippines (395) and Sri Lanka (87) were second and third respectively in terms of the number of species exported to the US.

Trade flow of marine aquarium fishes and invertebrates from source nations into the US during 2008, 2009 and 2011.

Figure 5: Trade flow of marine aquarium fishes and invertebrates from source nations into the US during 2008, 2009 and 2011.

Numbers within circles denote percent contribution to total imports. Pie chart within US represents Ports of Entry (with the Midwest starting at 0 degrees, and clockwise, NE, SE, SW and NW).
Table 3:
Top 20 live aquarium fish and invertebrate species imported into the US by year.
Data include proportion of import volume (individuals as % Total) and number of export countries (Countries (No.)) for each.
Rank 2008 2009 2011
Species % Total Countries (No.) Species % Total Countries (No.) Species % Total Countries (No.)
Fishes
1 Chromis viridis 10.2% 13 Chromis viridis 10.5% 16 Chromis viridis 11.6% 13
2 Chrysiptera cyanea 5.6% 8 Chrysiptera cyanea 5.0% 8 Chrysiptera parasema 4.7% 6
3 Dascyllus trimaculatus 5.0% 11 Dascyllus trimaculatus 4.4% 12 Chrysiptera cyanea 4.4% 7
4 Dascyllus aruanus 3.7% 9 Chrysiptera parasema 3.6% 4 Dascyllus trimaculatus 3.7% 10
5 Chrysiptera parasema 3.5% 3 Dascyllus aruanus 3.3% 9 Dascyllus aruanus 3.6% 8
6 Amphiprion ocellaris 3.2% 10 Amphiprion ocellaris 3.0% 10 Nemateleotris magnifica 3.0% 8
7 Nemateleotris magnifica 2.7% 12 Nemateleotris magnifica 2.4% 12 Amphiprion ocellaris 3.0% 10
8 Chrysiptera hemicyanea 2.6% 2 Chrysiptera hemicyanea 2.4% 3 Pterapogon kauderni 1.9% 5
9 Dascyllus melanurus 1.8% 3 Dascyllus melanurus 2.0% 6 Centropyge loricula 1.9% 9
10 Pterapogon kauderni 1.8% 3 Paracanthurus hepatus 1.7% 14 Pseudocheilinus hexataenia 1.6% 9
11 Pseudocheilinus hexataenia 1.4% 13 Pterapogon kauderni 1.7% 4 Dascyllus melanurus 1.6% 3
12 Paracanthurus hepatus 1.3% 16 Centropyge loricula 1.6% 7 Sphaeramia nematoptera 1.5% 7
13 Synchiropus splendidus 1.3% 3 Pseudocheilinus hexataenia 1.6% 12 Chrysiptera hemicyanea 1.5% 3
14 Centropyge loricula 1.3% 8 Valenciennea puellaris 1.4% 10 Synchiropus splendidus 1.5% 5
15 Labroides dimidiatus 1.3% 13 Synchiropus splendidus 1.4% 5 Valenciennea puellaris 1.4% 7
16 Salarias fasciatus 1.3% 8 Gramma loreto 1.3% 6 Paracanthurus hepatus 1.3% 15
17 Gramma loreto 1.2% 6 Salarias fasciatus 1.3% 10 Salarias fasciatus 1.2% 11
18 Valenciennea puellaris 1.1% 9 Sphaeramia nematoptera 1.3% 6 Centropyge bispinosa 1.2% 14
19 Centropyge bispinosa 1.1% 12 Labroides dimidiatus 1.1% 13 Labroides dimidiatus 1.1% 11
20 Sphaeramia nematoptera 1.0% 7 Centropyge bispinosa 1.1% 12 Valenciennea strigata 0.9% 10
Invertebrates
1 Paguristes cadenati 22.0% 3 Paguristes cadenati 20.9% 2 Paguristes cadenati 14.0% 4
2 Lysmata amboinensis 10.2% 6 Lysmata amboinensis 13.5% 8 Lysmata amboinensis 12.3% 8
3 Clibanarius tricolor 8.0% 1 Clibanarius tricolor 5.7% 2 Mithraculus sculptus 7.3% 3
4 Mithraculus sculptus 5.1% 3 Mithraculus sculptus 4.2% 2 Trochus maculatus 4.6% 3
5 Stenopus hispidus 2.9% 11 Lysmata debelius 3.0% 5 Condylactis gigantea 3.3% 4
6 Trochus maculatus 2.7% 1 Calcinus elegans 2.8% 4 Clibanarius tricolor 2.7% 2
7 Nassarius venustus 2.6% 1 Trochus maculatus 2.8% 2 Stenopus hispidus 2.6% 10
8 Tectus fenestratus 2.5% 2 Stenopus hispidus 2.7% 12 Lysmata debelius 2.5% 3
9 Dardanus megistos 2.4% 5 Tectus fenestratus 2.5% 3 Entacmaea quadricolor 2.4% 12
10 Percnon gibbesi 2.3% 5 Tectus pyramis 2.4% 4 Dardanus megistos 2.4% 6
11 Tectus pyramis 2.1% 2 Percnon gibbesi 2.3% 3 Protoreaster nodosus 2.3% 5
12 Lysmata ankeri 2.0% 1 Condylactis gigantea 2.1% 5 Nassarius dorsatus 2.2% 1
13 Lysmata debelius 2.0% 5 Sabellastarte spectabilis 1.7% 5 Percnon gibbesi 1.8% 5
14 Condylactis gigantea 1.9% 5 Heteractis malu 1.5% 6 Nassarius venustus 1.6% 1
15 Sabellastarte spectabilis 1.8% 4 Lysmata ankeri 1.5% 1 Sabellastarte spectabilis 1.6% 4
16 Heteractis malu 1.4% 6 Protoreaster nodosus 1.3% 4 Nassarius distortus 1.6% 1
17 Calcinus elegans 1.3% 3 Engina mendicaria 1.2% 2 Heteractis malu 1.5% 4
18 Archaster typicus 1.3% 6 Entacmaea quadricolor 1.1% 12 Lysmata ankeri 1.5% 1
19 Engina mendicaria 1.2% 2 Nassarius distortus 1.1% 1 Pusiostoma mendicaria 1.4% 2
20 Stenorhynchus seticornis 1.1% 5 Archaster typicus 1.1% 4 Archaster typicus 1.4% 6
DOI: 10.7717/peerj.2949/table-3

Species

More than half (52%) of the total fishes imported into the US (identified to species-level, Table 3) were represented by 20 species. There was a great deal of consistency within these top 20 species among the years of this study. The species ranking was identical between 2008 and 2009, and only the 20th ranked fish was different in 2011 (the blueband goby, Valenciennea strigata, replaced the royal gramma, Gramma loreto). The order of the top seven fish species was consistent across the years, and represented nearly 33% of total fish imports. The green chromis, Chromis viridis, was the most popular fish species across all three years (>10% of total fish imports) and was exported by 13–16 different countries, depending on the year. This Chromis species was unique in being collected from a large number of countries. The only other fish that was equally sourced from a large number of countries (an average of 15 per year) was the blue tang, Paracanthurus hepatus, (Table 3).

Invertebrates demonstrated a similar but more extreme trend. The top 20 species of invertebrates imported into the US were responsible for approximately 75% of total imports (identified to species-level, Table 3), yet there was more variability in the invertebrate top 20 species list compared to the fish list. Only the top two species (the scarlet hermit crab, Paguristes cadenati, and the scarlet skunk cleaner shrimp, Lysmata amboinensis) were consistently ranked across the three years. Overall, 25 invertebrate species were represented on the three yearly top 20 lists (Table 3).

Each country could be represented by a single most exported species. Overall, the single most imported species averaged 37% (fishes) or 63% (invertebrates) of total species volume exported from that country (Tables 4 and 5). In general, countries that exported greater quantities of marine animals relied less on the contribution of the single most important species to export volume (Fig. 6).

Table 4: Top live aquarium fish species exported to the US from each exporting country (1°) with proportion of country’s export volume (individuals) (% Total) by year.
Export Country 2008 2009 2011
1°Species % Total 1°Species % Total 1°Species % Total
Australia Amphiprion ocellaris 42.3% Choerodon fasciatus 14.7% Choerodon fasciatus 16.9%
Belize Gramma loreto 22.4% Gramma loreto 27.0% Holacanthus ciliaris 25.8%
Brazil Holacanthus ciliaris 23.0% Holacanthus ciliaris 28.6% Holacanthus ciliaris 44.5%
Canada Eumicrotremus orbis 76.9% Rhinoptera jayakari 66.7% Eptatretus stoutii 42.3%
Cook Islands Pseudanthias ventralis 45.0% Pseudanthias ventralis 46.0%
Costa Rica Thalassoma lucasanum 31.1% Thalassoma lucasanum 28.0% Elacatinus puncticulatus 28.1%
Curaçao Elacatinus genie 28.0% Liopropoma carmabi 18.6% Gramma loreto 31.2%
Dominican Republic Gramma loreto 59.8% Gramma loreto 60.4% Gramma loreto 36.0%
Egypt Zebrasoma xanthurum 31.7%
Eritrea Zebrasoma xanthurum 23.2% Zebrasoma xanthurum 24.6%
Fed. States of Micronesia Pseudanthias bartlettorum 12.3%
Fiji Pseudanthias squamipinnis 9.6% Pseudanthias squamipinnis 12.2% Chromis viridis 20.3%
French Polynesia (Tahiti) Neocirrhites armatus 43.9% Neocirrhites armatus 64.6% Neocirrhites armatus 68.0%
Ghana Balistes punctatus 20.2% Balistes punctatus 36.3% Holacanthus africanus 41.4%
Guatemala Selene brevoortii 58.8% Selene brevoortii 64.7%
Haiti Gramma loreto 33.8% Gramma loreto 31.2% Gramma loreto 32.9%
Hong Kong Zebrasoma flavescens 76.3% Dascyllus trimaculatus 40.0% Chordata 99.7%
Indonesia Chromis viridis 10.5% Chromis viridis 8.9% Chromis viridis 10.8%
Israel Premnas biaculeatus 34.7% Amphiprion ocellaris 88.7%
Japan Parapriacanthus ransonneti 66.2% Parapriacanthus ransonneti 13.5% Paracentropogon rubripinnis 14.2%
Kenya Labroides dimidiatus 15.5% Labroides dimidiatus 14.2% Labroides dimidiatus 12.0%
Kiribati Centropyge loricula 70.1% Centropyge loricula 63.2% Centropyge loricula 65.1%
Malaysia Amphiprion ocellaris 35.7% Paracanthurus hepatus 100.0%
Mauritius Amphiprion chrysogaster 12.0% Macropharyngodon bipartitus 13.2%
Mexico Holacanthus passer 49.5% Holacanthus passer 35.8% Holacanthus passer 39.0%
Netherlands Antilles Elacatinus genie 58.9%
New Caledonia Chaetodontoplus conspicillatus 84.5% Chaetodontoplus conspicillatus 85.3% Cirrhilabrus laboutei 40.3%
Nicaragua Apogon retrosella 22.4% Acanthemblemaria hancocki 39.5%
Papua New Guinea Amphiprion percula 29.7% Paracanthurus hepatus 23.4%
Philippines Chromis viridis 11.7% Chromis viridis 13.3% Chromis viridis 13.6%
Rep. of Maldives Acanthurus leucosternon 12.9% Acanthurus leucosternon 12.7% Acanthurus leucosternon 14.7%
Rep. of the Marshall Islands Centropyge loricula 53.7% Centropyge loricula 41.9% Centropyge loricula 40.1%
Saudi Arabia Dascyllus marginatus 30.7% Anampses caeruleopunctatus 36.8%
Singapore Amphiprion ocellaris 42.3% Amphiprion ocellaris 73.0% Amphiprion percula 31.6%
Solomon Islands Paracanthurus hepatus 19.4% Paracanthurus hepatus 33.7% Paracanthurus hepatus 20.4%
Sri Lanka Valenciennea puellaris 22.5% Valenciennea puellaris 21.1% Valenciennea puellaris 26.8%
Taiwan Pomacanthus maculosus 24.8% Pomacanthus maculosus 19.4% Amphiprion ocellaris 55.2%
Thailand Amphiprion ocellaris 87.8% Amphiprion ocellaris 90.5%
The Bahamas Haemulon sciurus 17.5% Chromis cyanea 11.5% Haemulon flavolineatum 88.9%
Tonga Centropyge bispinosa 14.8% Centropyge bispinosa 12.7% Meiacanthus atrodorsalis 9.6%
United Arab Emirates Zebrasoma xanthurum 63.6%
United Kingdom Amphiprion ocellaris 76.5%
Vanuatu Centropyge loricula 9.4% Chrysiptera rollandi 12.8% Chromis viridis 6.9%
Vietnam Nemateleotris magnifica 8.3% Nemateleotris magnifica 16.7% Chaetodontoplus septentrionalis 12.3%
Yemen Zebrasoma xanthurum 48.2% Zebrasoma xanthurum 47.6%
Total Chromis viridis 10.0% Chromis viridis 10.2% Chromis viridis 11.2%
DOI: 10.7717/peerj.2949/table-4
Table 5: Top live aquarium invertebrate species exported to the US from each exporting country (1°) with proportion of country’s export volume (individuals) (% Total) by year.
Export country 2008 2009 2011
1°Species % Total 1°Species % Total 1°Species % Total
Australia Pseudocolochirus violaceus 75.6% Actinia tenebrosa 46.1% Actinia tenebrosa 37.2%
Belize Mithraculus sculptus 72.5% Mithraculus sculptus 51.9% Mithraculus sculptus 65.3%
Canada Enteroctopus dofleini 100.0%
China Actinia equina 70.5%
Costa Rica Lysmata wurdemanni 78.1%
Curaçao Lysmata wurdemanni 100.0% Paguristes cadenati 94.7%
Dominican Republic Paguristes cadenati 92.2% Paguristes cadenati 95.1% Paguristes cadenati 88.0%
Fiji Linckia laevigata 78.0% Linckia laevigata 87.0% Linckia laevigata 36.5%
French Polynesia (Tahiti) Holothuria (Halodeima) atra 52.2%
Ghana Actinia tenebrosa 85.3% Actinia equina 94.8% Lysmata grabhami 99.5%
Haiti Paguristes cadenati 46.3% Paguristes cadenati 47.1% Paguristes cadenati 43.6%
Hong Kong Entacmaea quadricolor 100.0% Entacmaea quadricolor 100.0%
Indonesia Trochus maculatus 19.3% Trochus maculatus 19.1% Trochus maculatus 30.3%
Japan Aurelia aurita 52.9% Aurelia aurita 58.7% Catostylus mosaicus 29.4%
Kenya Lysmata amboinensis 56.0% Lysmata amboinensis 69.0% Lysmata amboinensis 48.9%
Kiribati Panulirus versicolor 100.0%
Mauritius Heteractis magnifica 100.0%
Mexico Pentaceraster cumingi 74.9% Turbo fluctuosus 40.1% Dardanus megistos 59.7%
Nicaragua Turbo fluctuosus 49.2% Coenobita clypeatus 52.3%
Papua New Guinea Archaster typicus 45.7% Archaster typicus 36.5%
Philippines Lysmata amboinensis 15.9% Lysmata amboinensis 18.8% Lysmata amboinensis 16.3%
Rep. of Maldives Echinaster (Echinaster) sepositus 50.0% Echinaster (Echinaster) sepositus 83.3% Pusiostoma mendicaria 45.9%
Rep. of the Marshall Islands Engina mendicaria 70.8% Calcinus elegans 45.2%
Singapore Tectus niloticus 41.1% Entacmaea quadricolor 34.7% Sabellastarte spectabilis 54.0%
Solomon Islands Archaster typicus 46.4% Archaster typicus 65.8% Archaster typicus 66.7%
Sri Lanka Lysmata amboinensis 61.9% Lysmata amboinensis 63.7% Lysmata amboinensis 60.7%
Thailand Gecarcoidea natalis 100.0%
The Bahamas Ophiocoma alexandri 46.7% Ancylomenes pedersoni 22.7%
Tonga Nassarius venustus 92.0% Nassarius venustus 77.6% Nassarius venustus 99.2%
United Kingdom Chrysaora quinquecirrha 50.0%
Vanuatu Linckia multifora 28.2% Entacmaea quadricolor 56.4% Entacmaea quadricolor 54.3%
Vietnam Macrodactyla doreensis 34.1% Macrodactyla doreensis 36.5% Entacmaea quadricolor 40.1%
Total Paguristes cadenati 22.1% Paguristes cadenati 20.9% Paguristes cadenati 14.3%
DOI: 10.7717/peerj.2949/table-5

Comparison to LEMIS data

The LEMIS database contains information regarding non-CITES-listed species recorded on declarations under general codes. LEMIS data is produced by US-based importers from shipment declarations, where importers input shipment data into the required 3-177 declaration form and present the completed shipment declaration with corresponding invoice to USFWS prior to shipment clearance. We have demonstrated elsewhere (Rhyne et al., 2012) that this method of gathering import data is fraught with errors; first, importers commonly mislabel shipments as containing marine aquarium species when they only contain freshwater fish, non-marine species, or non-aquarium fish (all increasing the total number of fish reported in the LEMIS database); second, the data do not appear to be updated if shipments are canceled or modified (there is sometimes a significant mismatch between the number of individuals on the declaration and the corresponding values on the invoices); third, importers commonly misrepresent the country of origin and source (wild-caught/captive-bred) of species in shipments. As previously discussed (Rhyne & Tlusty, 2012), LEMIS is a tool designed for internal use by USFWS, primarily relating to volume of boxes arriving at ports and CITES compliance. Shipments of non-CITES-listed species and/or unregulated species are not held to any data integrity standards. We propose that the invoice-based method of data collection presented here can rectify many of the data deficiency issues that currently exist within the marine aquarium trade. Through this work, it was observed that the numbers of fishes imported into the US were routinely 60%–72% fewer than the import volumes reported by the LEMIS database (Fig. 7). A large proportion of the declaration form overestimate was a result of importers misclassifying shipments as MATF when they only contained freshwater species. Occasionally, entire freshwater shipments were erroneously listed as MATF. A second unknown portion of this error was missing invoices. Not all invoices were recovered from the LEMIS system. Several hundred records were either missing the invoice or exhibited invoice/declaration mismatch, making the data impossible to verify. Similarly, invoice-based data reported a total of 45 countries exporting MATF, which was only 60% of the 76 export countries reported by the LEMIS database (Table 6). These countries represented 5%, 6%, and 11% of the total volume of MATF imported into the US according to the LEMIS database during 2008, 2009, and 2011, respectively (Table 6). Third is that the declaration is typically completed days before the order is packed, which invites variation between estimated and actual order volume. Finally, there was a lack of adherence to differentiating “wild-caught” and “captive-bred” animals (Rhyne, Tlusty & Kaufman, 2012). The case studies presented below use the invoice-based dataset to shed light on this discrepancy.

The cumulative summation of the number of (A) fishes and (B) invertebrates exported per country by rank order of species.

Figure 6: The cumulative summation of the number of (A) fishes and (B) invertebrates exported per country by rank order of species.

The most-exported species represents a significant proportion of the total individuals exported per country, and this importance decreases as a country exports a greater number of species.
Comparison of total number of marine aquarium fish imports into the US.

Figure 7: Comparison of total number of marine aquarium fish imports into the US.

Comparison of total number of marine aquarium fish imports into the US according to the Law Enforcement Management Information System (LEMIS) and The Marine Aquarium Biodiversity and Trade Flow (MABTF) online database across 4 years. Data from 2008, 2009, and 2011 is from the dataset presented here, and data from 2005 was presented in Rhyne et al. (2012).

Estimated fish

In October of 2000, 810,705 fishes and 124,308 invertebrates were imported. During the years 2008, 2009 and 2011, October represented on average 8.7% of fish and 8.6% of invertebrate imports into the US. Thus, it can be estimated that 9,327,754 fish and 1,442,859 invertebrates were imported into the US during calendar year 2000. Following this example, 10,766,706 and 11,229,443 fish were imported into the US in 2004 and 2005 respectively, no invertebrate data was available for 2004 and 2005 data.

Table 6:
Countries reported in LEMIS database that export live aquarium fishes to the US.
Data include number of individuals exported (LEMIS (No.)) and proportion of LEMIS invoices recovered in the present study (Invoice (%)). Shaded countries are those represented in the invoice-based assessment of fish imports to the US.
Country 2008 2009 2011 2008–2011
LEMIS (No.) Invoice (%) LEMIS (No.) Invoice (%) LEMIS (No.) Invoice (%) LEMIS (No.) Invoice (%)
Antarctica 49 49
Australia 16,908 76.2 13,973 62.8 10,545 90.8 41,426 75.4
Barbados 82 82
Belgium 266 266
Belize 19,957 47.5 18,214 48.6 27,840 53.8 66,011 50.5
Brazil 61,247 14.3 15,342 21.8 3,179 63.1 79,768 17.7
Canada 53 98.1 119 2.5 56 46.4 228 35.5
Cayman Islands 14 14
China 354,093 126,218 44,151 524,462
Christmas Island 1,712 1,712
Colombia 24,386 12,594 36,980
Dem. Rep. of the Gongo 185 185
Cook Islands 4,793 99.4 3,330 99.6 8,123 99.5
Costa Rica 38,904 20.3 15,770 22.4 6,220 98.7 60,894 28.9
Cuba 20 20
Curacao 2,992 112.5 2,992 176.4
Czech Republic 1,154 428,022 80,500 509,676
Dominican Republic 58,497 37.8 64,254 45 39,687 86.4 162,438 57.8
Ecuador 5,990 5,990
Egypt 755 126.2 755 126.2
Eritrea 2,796 340.0 3,046 130.9 5,842 231.4
Fed. States of Micronesia 5,515 100.6 5,515 100.6
Fiji 13,8801 83.2 119,535 73.9 171,364 91.4 429,700 84.3
French Polynesia (Tahiti) 50,261 85.2 30,789 98.0 30,914 93.8 111,964 91.3
Ghana 1,119 45.5 982 69.9 808 87.6 2,909 66.4
Guatemala 7,755 13.6 343 100.0 8,098 17.3
Guinea 357 357
Haiti 306,084 78.6 280,196 77.1 135,890 93.3 722,170 81.5
Hong Kong 205,408 0.1 25,806 0 141,888 11.6 373,102 4.5
India 5,374 4,932 10,306
Indonesia 3,044,574 78.9 2,743,170 72.8 2,228,446 83.8 8,016,190 79.0
Israel 22 818 81.4 25,990 84.6 26,830 84.4
Japan 1,911 59.3 1,790 63.5 820 69.4 4,521 62.8
Kenya 175,607 82.1 178,715 77.8 123,248 82.7 477,570 81.3
Kiribati 143,615 85.6 93,586 84.2 118,164 89.4 355,365 86.9
Republic of Korea 6 6
Malaysia 6,516 9.5 11,937 15,255 0.1 33,708 1.9
Mauritania 184 184
Mauritius 6,465 12.7 681 99.9 7,146 21.0
Mexico 5,147 100.5 15,805 80.3 22,331 67.8 43,283 77.4
Morocco 141 141
Netherlands 87 175 262
Netherlands Antilles 2,178 14.6 1,558 628 4,364 7.3
New Caledonia 317 26.5 86 87.2 617 62.7 1,020 53.5
New Zealand 1 1
Nicaragua 15,647 57.4 2,120 87.1 17,767 61.0
Nigeria 4,005 4,249 9,446 17,700
Norway 196 2,853 2,903 5,952
Papua New Guinea 11,899 57.3 13,167 63.1 25,066 60.8
Peru 80,963 67,609 10,395 158,967
Philippines 5,504,928 85.3 4,815,066 83.6 4,545,933 85.8 14,865,927 85.6
Rep. of Maldives 27,215 90.3 23,572 93.7 37,423 91.8 88,210 92.1
Rep. of the Marshall Isl 50,143 75.7 163,433 70.8 152,000 93.5 365,576 91.4
Saudi Arabia 7,304 4.5 2,131 0.9 9,435 3.7
Sierra Leone 244 244
Singapore 310,090 0.8 279,794 0.9 325,715 4.3 915,599 2.1
Slovakia 119 119
Solomon Islands 66,057 71.5 58,397 59.5 42,562 97.9 167,016 75.2
Sri Lanka 337,521 60.0 1,807,583 12 1,981,399 10.7 4,126,503 15.5
Suriname 214 214
Taiwan 54,623 2.8 47,430 1.9 6,950 35.2 109,003 4.6
United Republic of Tanzania 253 253
Thailand 207,582 19.2 115,952 7.2 1,117,626 1,441,160 3.3
The Bahamas 1,557 61.1 1,524 28.3 1,397 21.3 4,478 37.5
Tonga 57,120 48.8 13,787 58.4 2,474 108.2 73,381 53.5
Trinidad and Tobago 107,805 46,360 154,165
Tunisia 558 558
Ukraine 93 93
United Arab Emirates 79 97.5 79 97.5
United Kingdom 3,721 99.7 583 4 4,308 86.1
United States 828 87 45 960
Vanuatu 22,850 86.2 15,538 81.5 15,924 90.5 54,312 86.9
Various States 31,771 13,369 23,350 68,490
Vietnam 26,621 54.8 10,832 60.4 9,597 50.3 47,050 55.3
Yemen 20,230 51.1 13,114 90.5 33,344 66.6
Zambia 1,286 1,286
Total (No Invoice Data) 50,5041 776,984 1,350,027 1,499,694
Total (All Countries) 11,529,062 72.0 11,783,973 60.3 11,586,805 59.5 34,899,840 64.6
DOI: 10.7717/peerj.2949/table-6

Confusion Between “Wild” and “Cultured” Production

The Banggai cardinalfish, Pterapogon kauderni, is a popular marine fish in the aquarium trade (ranked the 10th, 11th, and 8th most imported fish into the US during 2008, 2009, and 2011, Table 5). It was one of the original marine aquarium aquaculture success stories (Talbot et al., 2013; Tlusty, 2002), which was supposed to reduce the need for wild-caught fishes. While aquaculture should dominate the source of the fish, all P. kauderni imported during this three-year span were reported as wild-caught fish. Yet import records from Sri Lanka in 2009 and 2011, and Thailand in 2013 (both outside the natural geographic range of P. kauderni) suggest this is not the case (Fig. 8).

Annual volume of Bangaii cardinalfish (Pterapogon kauderni) into the US by top export countries.

Figure 8: Annual volume of Bangaii cardinalfish (Pterapogon kauderni) into the US by top export countries.

Exports from Sri Lanka (2009, 2011) and Thailand (2013) illustrate the likely prevalence of previously unrecognized captive-bred P. kauderni in the trade.

The export volume of P. kauderni from Thailand followed the typical aquarium trade pattern of lower volumes exported in the summer months (June–August) and in December (Fig. 9). Interestingly in 2013, the only year with a 12-month data set starting in January and ending in December, the volume of P. kauderni (∼120,000 individuals/year) was approximately 75% of the average total import volume of this species recorded per year for 2008, 2009 or 2011. Further, these fish were listed on import declarations as ranging in size from 1 to 1.5 inches. A 1-inch fish is smaller than the average wild-caught fish (A Rhyne, pers. obs., 2013) and instead represents the typical shipping size of a captive-bred fish. Shipment manifests also list the number of Dead On Arrival (DOA) from previous shipments, which were extremely low (<0.5%) for wild-caught P. kauderni.

Temporal variability of the volume of captive-bred Bangaii cardinalfish (Pterapogon kauderni) imported into the US.

Figure 9: Temporal variability of the volume of captive-bred Bangaii cardinalfish (Pterapogon kauderni) imported into the US.

Temporal variability of the volume of assumed captive-bred Bangaii cardinalfish (Pterapogon kauderni) imported into Los Angeles, California, US. This seasonal variability is consistent with the import of wild fish.

The shipment manifests have common errors that can be observed on the 3–177 USFWS declarations. On several occasions the importer incorrectly indicated that shipments were wild-caught animals (“W”). After examining the invoices and associated documents, (i.e., health and aquaculture certificates), we determined that all shipments of P. kauderni from Thailand to Quality Marine during the period examined were captive-bred (“C”), and the importer erroneously selected “W” in the Source box (Box 18B, 3–177 form). Given the current Endangered Species Act (ESA) listing for P. kauderni (NOAA, 2014), accurate and timely trade data are crucial to the sustainable management of this species.

Misidentification and Unknown Trade

Similar to the Banggai cardinalfish, clownfishes exported from Southeast Asia are commonly labeled as wild-caught while many are in fact captive-bred. This inaccuracy is compounded by the misidentification of clownfishes on export invoices, especially among species with similar morphological appearances (e.g., the orange clownfish, Amphiprion percula, and the common clownfish, A. ocellaris). Use of http://www.aquariumtradedata.org not only sheds light on source-errors (as seen in the Banggai cardinalfish case study) but also on potential species misidentifications.

Recently, the orange clownfish (A. percula) was proposed to be listed as threatened or endangered under the ESA, mainly due to its small geographic distribution and obligate relationship with giant sea anemones prone to bleaching events in the Coral Triangle. However, the proposition was also based on the assumption that out of the 400,000 individuals from the percula/ocellaris complex imported into the US in 2005 (Rhyne et al., 2012), (a) all specimens were wild-caught, and (b) A. percula and A. ocellaris were equally traded, with 200,000 individuals of each species being harvested. Utilization of http://www.aquariumtradedata.org can help clarify issues regarding origination of these species. While in 2008, 2009 and 2011, 831,398 individual clownfishes of the percula/ocellaris complex were imported into the US (Fig. 10), only 163,547 individuals were A. percula (24.5%, Fig. 10). These data suggest that the original assumptions of trade volume used to petition for ESA listing were strongly overestimated.

Imports of orange clownfish (Amphiprion ocellaris/A. percula) into the US aggregated over 2008, 2009, and 2011.

Figure 10: Imports of orange clownfish (Amphiprion ocellaris/A. percula) into the US aggregated over 2008, 2009, and 2011.

Export countries were grouped based on the documented geographic range of each species. All non-native individuals are either actually native (but of an unknown distribution), captive-bred, or misidentified as to origin on the shipping invoice.

Further, the Countries of Origin feature of the database revealed that of the ten export countries of A. percula, seven countries (41% of all individuals) fall outside the natural geographic range of this species (Fautin & Allen, 1997; Froese & Pauly, 2015). Furthermore, five of the seven non-native locations are established producers of captive-bred A. percula. Based on this, 7% of the non-native individuals are likely captive-bred specimens. The remaining two non-native countries (Singapore and the Philippines) account for the residual 93% of the non-native individuals and are likely misidentifications. Interestingly, both Singapore and the Philippines fall within the natural geographic range of A. ocellaris, which is commonly confused with A. percula. While these individuals may be misidentified, it is also important to note that Singapore is a known trans-shipping country, and could have imported their specimens from another country, making the true origin of these specimens unattainable. Furthermore, Singapore is a leader in captive-bred production of aquarium fish, and thus many clownfish could be of captive-bred origin.

In summary, 41% of A. percula imported into the US over the three-year span (a) were misidentified as to species or export country, (b) were misidentified as to source (wild-caught versus captive-bred), or (c) represent a recently expanded home range not yet noted within the scientific literature (unlikely). Regardless of the reason, the contribution of A. percula imports to the percula/ocellaris complex is not only substantially less than assumed, but also is likely even lower based on the high percent of geographic anomalies reported here. Ultimately, this case study confirms the need for more accurate and detailed trade data, such as that provided via http://www.aquariumtradedata.org, for any potential ESA listing activity.

The orange clownfish case study demonstrates the effect that species-level nomenclature confusion can have on trade data. Users of http://www.aquariumtradedata.org have illuminated other examples of species misidentification, such as Centropyge argi, an Atlantic species (Froese & Pauly, 2015) with a significant volume of reported exports from Indonesia. While species-level confusion may be common for specious genera of fishes such as Centropyge and Amphiprion, it is important to recognize instances of more blatant misidentification. For example, the iconic yellow tang, Zebrasoma flavescens, although a Hawaiian endemic, appears in this database as being exported from 13 countries; it is difficult to imagine this fish being confused with anything else. Continuous biogeographical filtering of invoice data by website users will help to minimize misidentification errors. One of the egregious cases of identification error is invoice items listed as “unknown”. These must find a home in the database, and at this point in time, are ultimately listed as “Chordata.” This lack of identification of fishes raises the issue that different countries have various reporting requirements that can create data deficiencies within the database. If one queries exports from Hong Kong, there are no reporting requirements, and thus all fish are entered into the database as the generic category “Chordata.” A deficiency of reporting requirements for this database is the lack of between-country agreement.

Discussion

The deficiency of comprehensive and overarching data relating to the global marine aquarium trade hinders progress toward its effective management (Foster, Wiswedel & Vincent, 2016; Fujita et al., 2014; Rhyne et al., 2012). We believe that access to more accurate data will allow for increased public engagement in trade sustainability and guide responsible trade management. These data can stimulate action toward consumer education, address challenges such as misidentification, and better manage species. Ideally these will result in greater sustainability (Tlusty et al., 2013). Currently, there is no overarching system for tracking species-level import/export data for the marine aquarium trade. This is exacerbated by the lack of standard recordkeeping between different countries (Green, 2003). Coupled with this is the fact that present data systems are either overly general, based on declaration forms (LEMIS), or specific to the trade of rare and threatened species (CITES, Foster, Wiswedel & Vincent, 2016). The Global Marine Aquarium Database (Green, 2003) attempted to make sense of some of these discrepancies, but can be difficult to use due to its data structures and relational databases. These complications and data limitations promote misinterpretation, as evidenced by the trade volume under- and over-estimates discussed here. Changes to and standardization of the way live animal trade data are recorded are necessary to accurately assess trade pathways and data inaccuracies. This will avoid misinterpretations with potentially costly consequences of social, economic, and ecological proportions (e.g., the use of such data to affect ESA listing status). Such costs will only be exacerbated as the aquarium industry continues to grow.

Capturing invoice-based data can waylay many of the deficiencies of the extant databases and should prove useful to both conservation organizations and government agencies by helping to address the aquarium trade data deficiency that currently exists. The benefit of the more detailed invoice data we focused on here is that it allowed for a truer estimate of aquatic wildlife trade. The recent ESA petitions for both the Banggai cardinalfish (NOAA, 2014) and the orange clownfish (Maison & Graham, 2015) were proposed based on incorrect trade data and, in each of these cases, we demonstrated that increased knowledge of production areas and modalities do not support the underlining trade assumptions of these petitions. The assumptions of these ESA listings were demonstrated to be erroneous in part due to reported source (wild-caught, captive-bred, farmed) inaccuracies of shipped animals. For example, exporters will often mark farmed corals as wild corals, even when they have proper CITES permits for the export of farmed corals (Rhyne, Tlusty & Kaufman, 2014). Many exporters do not have the appropriate paperwork or government support needed to accurately mark corals as captive-bred or farmed on CITES documents, often because of the onerous process required to certify that corals are of farmed origin. While improved analysis of invoices will help limit some of this misreporting, it will not be totally unabated until a full fishery/farm to retail traceability program is initiated.

Further issues with the clownfish ESA listing occurred because of demonstrated geographic misidentification. Seven of the ten export countries of the orange clownfish fell outside the natural geographic range of this species. Even though these can be indicated as erroneous data, correcting these anomalies is outside the purview of http://www.aquariumtradedata.org, as it was deemed important to record data as indicated on the invoice. Further discussion of discrepancy can occur through in-depth analysis of these data and such efforts are welcomed. As this database develops, it will be important to identify the commonly misidentified species, and to help the entire trade improve its species documentation. Ideally, lists of ‘look-alike’ species can be created, and machine learning can be used to derive biogeographically edited species lists. One of the critical assumptions of this work is that the invoice represents the true contents of the shipment. There are a number of reasons this may not be the case, including but not limited to miscounting, misidentification, and intentional substitution. The question of invoice veracity has been highlighted by others (Jones, 2008; Wabnitz et al., 2003), and without a study directly comparing invoice to box contents, the exact correlation will remain unknown. If it is assumed that the trade is based on above-board honest business practices, then the invoice should be an accurate representation of the trade. However, the greater the dishonesty in the trade (e.g., invoicing a shipment of corals as MATF), the greater the disconnect between invoice and box contents. This project was recently named a Grand Prize Winner of the Wildlife Crime Tech Challenge (www.wildlifecrimetech.org), which will spur continued development of this project, with an emphasis on increasing honest business practices by more easily identifying and enforcing illegal and inaccurate trade activity.

The development of http://www.aquariumtradedata.org is a first step toward improving the data, which will allow for better management and oversight of the trade in marine aquatic animals. However, the invoice analysis was developed from a post-import standpoint. The shipments were accepted at import, the paperwork processed, and the invoices stored, only to be recovered from storage and delivered for analysis within this program. However, the OCR data processing has the potential to be utilized in real time. This would allow for shipment diagnostics to be conducted, which could potentially identify misidentified or even illegal shipments. Such an import risk-based screen tool exists under the FDA’s Predictive Risk-based Evaluation for Dynamic Import Compliance Targeting program (http://www.fda.gov/ForIndustry/ImportProgram/ucm172743.htm), and we propose that a similar model would be effective for the aquatic wildlife trade. Ultimately, such an analysis would provide support to port agents to help them more effectively monitor the trade.

Aquaculture is a significant means of fish production (Tlusty, 2002). This will present a challenge because the lack of reporting for domestic sales will obscure patterns in the trade. Murray & Watson (2014) observed clownfish to be the most popular species kept by aquarists, although they were not the most popular species imported in our database. The US domestic production will obscure the relationship between fishes imported, and those actually being kept by hobbyists. However, we need to step towards greater recordkeeping on species in the trade, and while we focus on international trade, it would be ideal if records of domestic production could additionally be kept.

While it was not implicitly necessary to estimate the number of individuals imported for years of incomplete data (2000, 2004 and 2005), incomplete data in 2004 and 2005 compared to complete data in the later years could give the impression the trade was increasing. A common query without the estimated number of fish would result in a figure where the total number of indivudals in 2000 was 8% while 2004 and 2005 data would be approximately half that of 2008, 2009 and 2011. Therefore, the estimated fish numbers were calculated to create a more cohesive visual presentation of data, and to avoid the incorrect analysis that numbers of US imports of marine aquarium fishes and invertebrates are increasing. Prior analysis indicated the trade has decreased from its peak in 2005 following the economic recession and a shift to smaller tank sizes (Rhyne & Tlusty, 2012; Rhyne, Tlusty & Kaufman, 2012). Estimated data should be treated with caution given their (by definition) degree of error. We encourage users of this database to determine if more sufficient methods to estimate unknown data can be validated.

In summary, wildlife data tracking systems require improvement (Chan et al., 2015; Foster, Wiswedel & Vincent, 2016); we are beyond the age of tracking animal shipment volume solely for the purpose of assessing port agent staffing needs. The systems currently in place for tracking non-CITES-listed aquarium animals have proven ineffective in producing meaningful data that can move the trade toward sustainability and conservation (Vincent et al., 2014). The invoice-based dataset presented here, while set up as a post-import assessment tool, could be easily modified into a real-time aquarium trade data monitoring system. Ideally this can have a positive impact on increasing the veracity of the LEMIS system. It behooves the largest aquatic wildlife importer in the world to showcase real constructive intent to foster sustainability in the trade and to create positive change in an important industry. This proof that the trade can be passivily monitored (Wallace et al., 2014) is a huge step toward driving positive change in the trade. The next step will be to monitor aquarium trade pathways in real-time, as this is crucial to effectively assist the management of the trade of marine aquarium wildlife for the home aquarium industry. A goal for real-time, simultaenous monitoring of exports and imports is now within reach.