Introduction
The global ornamental fish trade is a multibillion-dollar industry involving > 125 countries, with > 2,500 species traded, 60% of which are from freshwater (Dey, Reference Dey2016). One major challenge of managing the ornamental fish trade is the difficulty of quantifying fish populations because of limited application of conventional fish stock assessment approaches for ornamental fisheries (Dee et al., Reference Dee, Horii and Thornhill2014; Fujita et al., Reference Fujita, Thornhill, Karr, Cooper and Dee2014; Leal et al., Reference Leal, Vaz, Puga, Rocha, Brown, Rosa and Calado2016). In addition, most global ornamental fish production statistics are based on inaccurate historical estimates of the value of exports (Watson & Roberts, Reference Watson and Roberts2015; Biondo & Burki, Reference Biondo and Burki2020). These challenges affect both freshwater and marine ornamental fisheries, and therefore it can be difficult to conserve and manage ornamental fish species effectively (Monteiro-Neto et al., Reference Monteiro-Neto, de Andrade Cunha, Nottingham, Araujo, Rosa and Barros2003; Maceda-Veiga et al., Reference Maceda-Veiga, Domínguez- Domínguez, Escribano-Alacid and Lyons2016; Evers et al., Reference Evers, Pinnegar and Taylor2019).
The export of ornamental fishes from Malawi, which affects > 700 wild taxa, predominantly cichlid fishes (Msukwa, Reference Msukwa2020; Msukwa et al., Reference Msukwa, Cowx and Harvey2021, Reference Msukwa, Cowx and Harvey2022), also faces some of these management challenges. This trade started operating in Malawi in the early 1970s, and since then the number of licensed fish exporters has fluctuated between one and four. All four current exporters are based in Salima District, a lakeshore district in the Central Region (nearly all ornamental fish exported are from Lake Malawi, with only a small per cent from the inlet and outlet streams and rivers of the lake; Msukwa et al., Reference Msukwa, Cowx and Harvey2022). The exporters employ SCUBA diving teams to capture ornamental fishes using small nets. Individual exporters have close connections with their regular clients in importing countries and export fish based on the species and quantities specified by their clients. The exploited ornamental fish species have varying abundance and distribution patterns in Lake Malawi (Konings, Reference Konings2016), and most are also targeted by commercial and artisanal fisheries for food, increasing their vulnerability to overexploitation (Msukwa et al., Reference Msukwa, Cowx and Harvey2021, Reference Msukwa, Cowx and Harvey2022). For every ornamental fish export consignment, the exporters submit details of the exported fish (including a species list, quantities exported and invoices specifying the selling price and total value of the consignment) to the Government of Malawi through the Department of Fisheries (Msukwa, Reference Msukwa2020). However, the Department has never undertaken a detailed analysis of this information, nor used it for the management of the ornamental fishery.
Sayer et al. (Reference Sayer, Palmer-Newton and Darwall2019) highlighted the need to devise a system for monitoring the collection and export of live ornamental fishes from Malawi to prevent the overcollection of popular species with restricted distribution ranges. Such a strategy could involve monitoring the exploited ornamental fish populations and/or the quantities of individual ornamental fish species exported, which could facilitate the identification of species that have been overexploited so that appropriate management actions can be taken. Msukwa et al. (Reference Msukwa, Cowx and Harvey2022) reported increasing volumes of ornamental fish exports during 2008–2019. In addition, ornamental fish exporters have reported that the fishes their clients demand are becoming scarcer and more difficult to catch (Msukwa, Reference Msukwa2020; Msukwa et al., Reference Msukwa, Cowx and Harvey2022). One unique characteristic of global ornamental fisheries is that exporters target both abundant and rare fish species (Rhyne et al., Reference Rhyne, Tlusty, Schofield, Kaufman, Morris and Brukner2012b).
Here we examine export trends of individual ornamental fish species from Malawi, taking into account temporal variation in fish prices and the number of fish exporters. We also examine any potential correlation between export trends and the IUCN Red List status of the fishes (IUCN, 2024). We anticipate that our findings will provide insights into the status of the exploited ornamental fish species and be a guide for remedial action for species that show evidence of overexploitation. In addition, our findings could contribute to the development of an appropriate strategy for the management of the ornamental fishery in Malawi, which is not yet included in the Fisheries and Aquaculture Policy (Msukwa et al., Reference Msukwa, Cowx and Harvey2022).
Methods
Data sources
From packing lists of species and quantities of ornamental fish export consignments from Malawi during 1998–2021, we extracted data on ornamental fish exports. Consignments are inspected and certified by the Department of Fisheries before export. One copy of the packing list for each consignment is submitted to the Department of Fisheries, and the other accompanies the consignment to the importing countries (Msukwa et al., Reference Msukwa, Cowx and Harvey2021). We extracted data from the packing lists for > 700 species but analysed export trends only for the 135 most commonly exported species (i.e. those with > 500 specimens each exported during 1998–2021), with 113 described by their full scientific names and 22 only known by their informal trade names (Tables 1 & 2, Supplementary Table 1). The extracted data include the numbers exported by species, date of export, the unit price of each species and the number of licensed fish exporters in each year. We estimated the mean annual unit price for each fish species by dividing the total export value for all individuals of a particular species by the total number exported each year. We did this after converting the value of various export currencies into the USD equivalent using historical annual average currency exchange rates (OFX, 2024) and adjusting the USD values to purchasing power in 2021 using an inflation calculator (CoinNews, 2024). We based the total export value only on the price of fish, without the freight, insurance and other charges as some exporters did not provide this information in the export returns they submitted to the Department of Fisheries.
Table 1 Ornamental fish species from Lake Malawi showing increasing export volume trends during 1998–2021, adjusted for the price of fish and the number of exporters, with the negative binomial regression model coefficients ± SE for year, price and number of exporters, and IUCN Red List status of assessed species (IUCN, 2024). The two species without a Red List status have not been fully scientifically named and are known only by their informal trade names.
* P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001.
1 DD, Data Deficient; LC, Least Concern; CR, Critically Endangered.
Table 2 Ornamental fish species from Lake Malawi showing decreasing export volume trends during 1998–2021, adjusted for the price of fish and the number of fish exporters, with the negative binomial regression model coefficients ± SE for year, price and number of exporters, and IUCN Red List status of assessed species (IUCN, 2024). The three species without a Red List status have not been fully scientifically named and are known only by their informal trade names.
* P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001.
1NT, Near Threatened; LC, Least Concern; CR, Critically Endangered.
Compilation of species names and conservation status
The exporters of ornamental fish use either trade or scientific names (A.V. Msukwa, pers. obs., 2017). The exporters and the SCUBA divers employed to catch the fish are experienced in identification, having handled the same species for many years (A.V. Msukwa, pers. obs., 2018). Moreover, owners of two of the exporting companies formerly worked for the first established export company before establishing their own ornamental fish export companies (D. Nkhwazi, pers. comm., 2018), and most of the SCUBA divers commonly move between exporters (H. Ngwira, pers. comm., 2018). We validated the scientific names of the exported fish species using Konings (Reference Konings2016, pp. 422–431), which provides detailed information of both the trade and scientific names of the fish species of Lake Malawi. We extracted information on the conservation status of the fish species from the IUCN Red List of Threatened Species (IUCN, 2024).
Data analysis
Export trends
We first employed a Poisson regression to model the fish export trend data for each fish species by fitting the number of exported ornamental fish as a response variable and year as an explanatory variable, with price and the number of exporters as covariates. We considered this model appropriate because ornamental fish export data involved counts that cannot have a negative value, have increasing variance as the mean increases and have errors that are not normally distributed (Crawley, Reference Crawley2007). However, the overdispersion parameter of the Poisson regression was > 1, and therefore we used a negative binomial regression model instead to fit the relationship between the number of exported ornamental fish of each species as a response variable and year of fish export as an explanatory variable, adjusting for average price of fish and number of exporters each year. We fitted the negative binomial regression model using the glm.nb function in the package MASS (Venables & Ripley, Reference Venables and Ripley2002) in R 4.3.1 (R Core Team, 2023).
Correlation between export trends and conservation status
We coded the conservation status and export trend values for the 111 fully named ornamental fish species in an ordinal scale to determine their relationship using Kendall's rank correlation tau, in R. We excluded two of the 113 fully named species (Chiloglanis neumanni and Copadichromis mloto) from this analysis because they are categorized as Data Deficient on the IUCN Red List. The conservation status codes were 1 for species of Least Concern, 2 for Near Threatened species and 3 for threatened species (i.e. categorized as Vulnerable, Endangered or Critically Endangered). The export trend codes were −1 for decreasing, 0 for no trend and 1 for increasing. We used Kendall's rank correlation because, in addition to offering a distribution-free test of independence and a measure of the strength of dependence between two variables, it is easier to interpret than Spearman's correlation (Dalgaard, Reference Dalgaard2008). We determined the significance of the Kendall's rank correlation analysis at an α level of 0.05.
Results
Export trends
Using the negative binomial regression model, we identified three export trends for the 135 fish species: increasing export volumes (Table 1), decreasing export volumes (Table 2) and no apparent export volume trend (Supplementary Table 1). Export price and the number of exporters significantly affected the annual export volumes of some of the fish species.
Species with increasing export volume trends
Sixteen species of 14 genera had significant increasing export volume trends (Table 1), with all but one genus (Chiloglanis, family Mochokidae) of the Cichlidae family. Three of these genera (Copadichromis, Metriaclima and Pseudotropheus) were represented in all three export volume trend types (Tables 1 & 2, Supplementary Table 1), and five genera (Chilotilapia, Chindongo, Cynotilapia, Labeotropheus and Placidochromis) were also common in the group with no apparent export volume trends. Fourteen of the species with increasing export volume trends are fully named, and two only have trade names (Table 1). Of the fully named species, Metriaclima koningsi is Critically Endangered, Chiloglanis neumanni is Data Deficient and the others are Least Concern (IUCN, 2024). Export volumes of five of the species in this group were positively influenced by fish prices, and export volumes of three and one fish species were positively and negatively influenced, respectively, by the number of exporters (Table 1).
Species with decreasing export volume trends
Sixteen species of seven genera (Aulonocara, Copadichromis, Dimidiochromis, Labidochromis, Melanochromis, Metriaclima and Pseudotropheus, all of the family Cichlidae) had significant decreasing export volume trends (Table 2). Four of the genera (Aulonocara, Dimidiochromis, Labidochromis and Melanochromis) were also common in the group with no apparent export volume trends (Supplementary Table 1). Thirteen of these species are fully named, and three only have trade names (Table 2). Of the fully named species, two are Critically Endangered, one is Near Threatened and 10 are Least Concern (IUCN, 2024). Export volumes of one and three species in this group were positively and negatively influenced, respectively, by fish prices, and export volumes of five species were positively influenced by the number of exporters (Table 2).
Species with insignificant export volume trends
One hundred and three species (86 fully named and 17 with only trade names) of 34 genera (32 of the family Cichlidae, Synodontis of the family Mochokidae and Mastacembelus of the family Mastacembelidae) did not have significant export trends (Supplementary Table 1). Of the fully named species, three are Critically Endangered, one Vulnerable, 10 Near Threatened and the others Least Concern (IUCN, 2024). Export volumes of eight and 16 species in this group were positively and negatively influenced, respectively, by fish prices, and 17 and two species were positively and negatively influenced, respectively, by the number of fish exporters (Supplementary Table 1).
Correlation between export trends and conservation status
Of the 111 fully named species, seven are categorized as threatened (six Critically Endangered, one Vulnerable), 11 as Near Threatened and 93 as Least Concern (Supplementary Table 1). Of the seven threatened species, two (29%) had decreasing export volume trends, one (14%) an increasing export volume trend and four (57%) no significant export volume trends. Of the 11 Near Threatened species, one (9%) had a decreasing export volume trend and 10 (91%) no significant export volume trend. Of the 93 Least Concern species, 10 (11%) had decreasing export volume trends, 12 (13%) increasing export volume trends and 71 (76%) no significant export volume trend (Fig. 1). Kendall's tau correlation analysis showed no statistically significant correlation between species conservation status and export trends (tau = −0.09848178, P = 0.2791).
Fig. 1 The number of Lake Malawi ornamental fish species exported, by IUCN Red List status and export volume trend type (see text for details), during 1998–2021. Threatened species included species categorized as Vulnerable, Endangered and Critically Endangered (IUCN, 2024).
Discussion
The objective of this study was to examine the export trends of ornamental fish species from Lake Malawi, taking into account the effect of the unit prices of the fish and the number of fish exporters, and to examine whether there was any association between export trends and the conservation status of the species. Such information can improve understanding of any overexploitation and be used as a basis for instituting appropriate actions for conservation and sustainable exploitation.
Monitoring fish production trends is one of the recommended actions for sustainable management of ornamental fisheries (Rhyne et al., Reference Rhyne, Tlusty and Kaufman2012a; Sayer et al., Reference Sayer, Palmer-Newton and Darwall2019; Biondo & Burki, Reference Biondo and Burki2020; Millington et al., Reference Millington, Holmes and Balcombe2022). Analysis of export/import trends of marine ornamental species has been used to monitor both exploitation and the challenges associated with supply (Rhyne et al., Reference Rhyne, Tlusty and Kaufman2012a; Leal et al., Reference Leal, Vaz, Puga, Rocha, Brown, Rosa and Calado2016). Such trend analyses have also been used for marine capture fisheries landing data in relation to environmental and fishery variables (Zuur et al., Reference Zuur, Tuck and Bailey2003; Zuur & Pierce, Reference Zuur and Pierce2004; Erzini, Reference Erzini2005), assessment of the status of the green sea turtle Chelonia mydas in New Caledonia (Fretey et al., Reference Fretey, Read, Carron, Fontfreyde, Fourdrain and Kerandel2023), analysis of the illegal harvest and trade of marine turtles (Lopes et al., Reference Lopes, Paulsch and Nuno2022) and assessment of the population of the olive ridley sea turtle Lepidochelys olivacea in Guatemala (Morales-Mérida et al., Reference Morales-Mérida, Muccio and Girondot2023). Our analysis of trends in ornamental fish exports, adjusted for fish prices and number of exporters, shares many similarities with the monitoring of marine ornamental fish exports.
Although data presented previously (Msukwa et al., Reference Msukwa, Cowx and Harvey2022) indicated an overall trend of increasing volumes of ornamental fish species exported from Malawi, we found no significant export volume trends for 103 of the 135 commonly exported fish species, an increasing trend for 16 species, and a decreasing trend for 16 species. The decreasing export volume trends for 16 species occurred despite an increase in the number of ornamental fish exporters, with 1–2 exporters during 1998–2009 and 3–4 exporters during 2010–2021 (except in 2011, when there was only one exporter; Msukwa et al., Reference Msukwa, Cowx and Harvey2022), potentially indicating unsustainable collection and consequent declines in the populations of these species.
Inclusion of fish export prices and the number of fish exporters as covariates in the negative binomial regression model indicated how these contributed to the significance of the export volume trends of the individual species. Of the 33 species for which there was a significant relationship between export volumes and price, 14 (42%) and 19 (58%) were positively and negatively influenced, respectively. Of the 28 fish species for which there was a significant relationship between export volumes and the number of exporters, 25 (89%) and three (11%) were positively and negatively influenced, respectively, by the number of exporters. The positive relationship between fish export volumes and the numbers of exporters for some species is consistent with the linkages between specific individual exporters and the importers of ornamental fish from Malawi (Msukwa et al., Reference Msukwa, Cowx and Harvey2022). These linkages are strong, and most importers would rather not import fish for a while than switch to a different exporter if they fail to renew their export licence (D. Nkhwazi, pers. comm., 2018).
Although increases in fish prices were mostly associated with a decrease in export volumes, there were positive relationships between price and export volume for some fish species. These findings could reflect two potential situations. Firstly, there could be other factors influencing fish export volumes that were not accounted for by the negative binomial regression model. Secondly, ornamental fish species in high demand, in particular newly discovered or rare species, could command higher prices compared to other species (Biondo, Reference Biondo2017; Msukwa et al., Reference Msukwa, Cowx and Harvey2022). Courchamp et al. (Reference Courchamp, Angulo, Rivalan, Hall, Signoret, Bull and Meinard2006) demonstrated how the rarity of exploited species can cause an increase in both demand and price, resulting in their exploitation remaining profitable and potentially driving species to extinction. The influence of the rarity of individual species on price has previously been hypothesized in the trade of coral reef species (Rhyne et al., Reference Rhyne, Tlusty and Kaufman2012a). As the value of the rare ornamental fish species of Lake Malawi increases, exporters may devote more time and resources to catching these species. This is evident for some exporters in Malawi, who pay bonuses to their fishers when they catch rare species (Msukwa, Reference Msukwa2020). In addition, most of the ornamental fish species of Malawi have limited distribution patterns within small, rocky outcrops (Ribbink et al., Reference Ribbink, Marsh, Marsh, Ribbink and Sharp1983; Reinthal, Reference Reinthal1993; Konings, Reference Konings2016), which makes them easy to catch even at low densities. However, the extent to which rarity influences the export prices of the Lake Malawi ornamental fish species cannot be determined without data on the abundance of these species. Ribbink et al. (Reference Ribbink, Marsh, Marsh, Ribbink and Sharp1983) conducted a comprehensive baseline study of the distribution and abundance of the rock-dwelling cichlid fishes of Lake Malawi, but although the study provided insights into the rarity of individual species, most of the information is now out of date because of subsequent taxonomic changes such as the splitting of some genera and species, the merging of some species and the description of new species (Hanssens & Snoeks, Reference Hanssens, Snoeks and Snoeks2003; Konings, Reference Konings2016). In addition, the populations of the targeted species could also have changed over time because of other anthropogenic factors such as subsistence fishing, localized water pollution, sedimentation and habitat destruction (IUCN, 2024). This demonstrates the need for a comprehensive resurvey of the status of exploited ornamental fish species as a basis for the management of this fishery.
Contrary to our expectation, we found no significant correlation between export volume trends and the conservation status of these ornamental fish species, suggesting that export volume trends alone are not a reflection of the population status of these fish species. All three export volume trend groups included threatened species. Exploitation of these threatened ornamental fish species, irrespective of their export trend, is a significant conservation concern (Raghavan et al., Reference Raghavan, Dahanukar, Tlusty, Rhyne, Krishna Kumar, Molur and Rosser2013). In addition to the 113 named fish species, 22 species known only by their trade names are also being exported and are represented within all three export trend groups. These species are potentially vulnerable to overexploitation and need to be fully named, to facilitate monitoring.
To ensure sustainability of the ornamental fishery of Lake Malawi, the Government of Malawi needs to incorporate aspects of ornamental fishery management when revising the Fisheries and Aquaculture Policy, which expired in 2021. The revised Policy should include strategies and measures such as encouragement of the preferential exploitation of ornamental fish species of Least Concern that have either increasing or no significant export volume trends, action to control overexploitation of the species with declining export trends, and a ban on the export of threatened ornamental species. Such a ban could be implemented both internationally and nationally. All threatened species should be included in the appendices of CITES, which regulates the international trade of species. Currently, none of the ornamental fish species exported from Malawi are included in the CITES appendices (CITES, 2024). Nationally, export bans could be enforced by the Department of Fisheries, which is responsible for the inspection and clearance of export consignments (Msukwa et al., Reference Msukwa, Cowx and Harvey2022). To be effective, such a ban would require training of Fisheries Department staff in the identification of exported fish species. Additionally, a clause could be included in the Fisheries and Aquaculture Policy to allow the export of threatened species only if they have been propagated in aquaculture facilities. This could reduce pressures on threatened wild ornamental fish stocks (Brummett, Reference Brummett2005), increase employment and encourage the production of new strains of ornamental fish species by selective breeding (Teletchea, Reference Teletchea2016). There is a general concern that breeding ornamental fish only benefits developed countries with the infrastructure to support aquaculture operations, at the expense of the countries from which the wild fish are sourced (Watson, Reference Watson2000; Wood, Reference Wood2001; Tlusty, Reference Tlusty2002) and with captive rearing away from the exporting country resulting in negative economic impacts for that country (Gerstner et al., Reference Gerstner, Ortega, Sanchez and Graham2006).
Finally, we recommend further research to establish the current status of the populations of the exploited ornamental fish species of Malawi and to identify any other factors that influence the observed export trends of individual ornamental fish species. Information from such research would be valuable for the development of suitable strategies for managing this ornamental fishery sustainably.
Acknowledgements
We thank the Department of Fisheries in Malawi for providing hard copy files of ornamental fish export lists and invoices from which we extracted the information presented in this study; all members of staff at the Department of Fisheries in Malawi, including Fisheries Headquarters, Salima District Fisheries Office and Senga Bay Fisheries Research Unit, who supported this study in many ways; and the editor and reviewers for their useful comments. Part of the information presented was collected using funding from the Commonwealth Scholarship Commission (Grant/Award Number: MWCS-2016-312) and part was funded from the authors' own resources.
Author contributions
Development of research concept, design of data collection tools: AVM; data collection and analysis, writing: both authors.
Conflicts of interest
None.
Ethical standards
This research was approved by the University of Hull (UK) Ethical Clearance Committee (SES Code 146 and Dept. Code H 79) and the Department of Fisheries in Malawi (Ref. No. 20/1/21, dated 13 September 2018). It did not involve working with live specimens of fish or human subjects, and abided by the Oryx guidelines on ethical standards.
Data availability
A summary of the data used is provided in the Supplementary Material, without details that could lead to the identification of individual fish exporters, for ethical reasons.
Open access
