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Aquarium trade as a pathway for the introduction of invasive species into Mexico

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The total ornamental fish industry worldwide (including dry goods) is valued at approximately US $15 billion dollars and it has been estimated that approximately one billion ornamental fish are commercialized every year with a value in the order of US $6 billion dollars. Freshwater species constitute the bulk of the trade; 90 percent of these are obtained from aquaculture and only 10 percent are wild captured. Around 800 to 1000 species and varieties are traded worldwide. Ornamental fish trade has been recognized as an important pathway for the introduction of non native species in several countries and present trends indicate that this pathway may turn into the main source of exotic invasive species in North America. Invasive species are characterized by posing different threats to the environment, the economy and human health. Among the main impacts provoked in the aquatic environment by invasive species are: competition with native species, hybridization, predation, introduction of diseases, habitat disruption and trophic webs modification. The introduction of exotic species has been related to the extinction of 54 percent of aquatic native species worldwide. Overall, 70 percent of the extinctions of North American fishes and 60 percent of those from Mexico are related to non native species, totally or partially. Aquarium trade has shown an accelerated increase during the last decade with a trade value of US $160 million dollars. This increase parallels the boost of exotic species in the country. In fact, in the 80's only 55 non native fish species were registered in Mexico and by 2004 the number raised to l l 8, of which 67 (58.26 percent) have turned invasive. Several facts contribute to explain this: i) The low amount of varieties cultured in Mexico (61 varieties pertaining to 19 species), compared to the huge number of varieties imported (more than 700 from l l7 families), ii) The number of fish imported in Mexico; 40 million ornamental fish are traded annually, of which 45 percent are imported (nearly 18 million fish were imported in 2006) while 55 percent are captive bred iii) there is a lack of official regulations for the establishment and operation of farms producing ornamental fish and for the translocation of ornamental fish within the country. As a result, ornamental fish species have been established in 9 out of 10 continental aquatic regions of Mexico. Some of these species have already severely impacted the environment and the economy in most regions of the country.
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Aquarium Trade as a Pathway
for the Introduction of
Invasive Species into Mexico
Roberto Mendoza Alfaro
Carlos Ramírez Martínez
Salvador Contreras Balderas
Patricia Koleff Osorio
Porfirio Alvarez Torres
In: "Freshwater Ecosystems and
Aquaculture Research"
Editor: F. De Carlo and A. Bassano
ISBN: 978-1-Ó0741-707-1 2010
In: Freshwater Ecosystems and Aquaculture Research IS BN: 978-1-60741-707-1
Editors: F. De Carlo and A. Bassano, pp. 209-224 © 2010 Nova Science Publishers, Inc.
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Chapter 8
AQUARIUM TRADE AS A PATHWAY FOR THE
INTRODUCTION OF INVASIVE SPECIES INTO M EXICO
Roberto Mendoza Alfaro, Carlos Ramírez Martínez,
Salvador Contreras Balderas, Patricia Koleff Osorio
and Porfirio Alvarez Torres
Facultad de Ciencias Biológicas de la UANL, Monterrey,
Nuevo León, México
Abstract
The total ornamental fish industry worldwide (including dry goods) is valued at approximately
US $15 billion dollars and it has been estimated that approximately one billion ornamental
fish are commercialized every year with a value in the order of US $6 billion dollars.
Freshwater species constitute the bulk of the trade; 90 percent of these are obtained from
aquaculture and only 10 percent are wild captured. Around 800 to 1000 species and varieties
are traded worldwide. Ornamental fish trade has been recognized as an important pathway for
the introduction of non native species in several countries and present trends indicate that this
pathway may turn into the main source of exotic invasive species in North America. Invasive
species are characterized by posing different threats to the environment, the economy and
human health. Among the main impacts provoked in the aquatic environment by invasive
species are: competition with native species, hybridization, predation, introduction of diseases,
habitat disruption and trophic webs modification. The introduction of exotic species has been
related to the extinction of 54 percent of aquatic native species worldwide. Overall, 70 percent
of the extinctions of North American fishes and 60 percent of those from Mexico are related
to non native species, totally or partially. Aquarium trade has shown an accelerated increase
during the last decade with a trade value of US $160 million dollars. This increase parallels
the boost of exotic species in the country. In fact, in the 80's only 55 non native fish species
were registered in Mexico and by 2004 the number raised to l l 8, of which 67 (58.26 percent)
have turned invasive. Several facts contribute to explain this: i) The low amount of varieties
cultured in Mexico (61 varieties pertaining to 19 species), compared to the huge number of
varieties imported (more than 700 from l l7 families), ii) The number of fish imported in
Mexico; 40 million ornamental fish are traded annually, of which 45 percent are imported
(nearly 18 million fish were imported in 2006) while 55 percent are captive bred iii) there is a
lack of official regulations for the establishment and operation of farms producing ornamental
fish and for the translocation of ornamental fish w ithin the country. A s a result, ornamental
210 R. Mendoza Alfaro, C. Ramírez Marnez, S. Contreras Balderas et al.
fish species have been established in 9 out of 10 continental aquatic regions of Mexico. Some
of these species have already severely impacted the environment and the economy in most
regions of the country.
Introduction
The Ornamental Fish Industry Worldwide
The global ornamental fish industry (including dry goods) is valued at approximately US
$15 billion dollars (Bartley, 2000) and currently about one billion ornamental fish are traded
anually (Whittington and Chong, 2007), with a value of US $6 billion dollars (Holthus and
Gamain, 2007) of which Asia provides 78 percent of such exportations worldwide (UNEP,
2008).
The main trading countries obtain most of their product &om developing countries such
as Philippines, Colombia, Peru, Brazil and Sri Lanka to later be re-exported to the rest of the
world. However, the ornamental fish trade is not just important in terms of its share in
international trade. The sector is frequently a welcome provider of employment opportunities
(Wijkstrom, 2002) and an important source of income for these economically depressed rural,
coastal and insular communities where this industry manage to account under the proper
developmental scenario, up to 60 percent of the local economy as in the case of the Amazon
(Chao and Prang, 1997; Dowd and Tlusty, 2000; Huanqui-Canto, 2002).
Most of the production of cultured ornamental fish focuses on &eshwater species.
Approximately 90 percent of freshwater ornamental fish are captively bred, compared to only
10 percent collected in the wild (Dawes, 1998, Chao and Prang, 2002; Wabnitz et al., 2003).
This contrasts with marine ornamental species which are mostly (99 percent) collected in the
wild and just 1 percent are reared (Hershberger, W.K., 2003).
The variety of fish involved in this industry is very significant. The estimated number of
species artificially reared in the freshwater ornamental trade range from 800 to more than
1,000 species, despite the scarce studies existing concerning their culture (Hernández, 2002;
Tlusty, 2002). This is an important figure when it is compared to the total number of finfish
species used for food or stock enhancement in commercial aquaculture which is estimated to
be only about 180 (Williams 1997). In contrast, it is estimated that a total of about 2,600
species are harvested in industrial and artisanal fisheries. (Hershberger, 2003)
The Ornamental Fish Industry as a Pathway for Aquatic Invasive Species
There is a clear and direct relationship between international trade and the spread of
invasive alien species (Burgiel., et al., 2006) and the most important pathway for non
indigenous introductions into N orth America has been intentional or unintentional
importations of organisms associated with international trade (Rixon et al., 2005). In this
regard, at the international level, aquarium trade has been widely recognized as an important
pathway for the introduction of alien aquatic species into new environments (Taylor et al.,
1984; Welcomme, 1992) and the current trends indicate that it may become soon the main
source of introductions of invasive exotic species in North America (Courtenay, 1995;
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 211
Courtenay and Williams, 1992). Following the criteria Burgiel and co-workers (Burgiel., et
al. 2006), several facts support this contention:
~ The rate of introductions of invasive alien species likely correlates with the volume
of trade. More than one billion ornamental fish are traded every year (Whittington
and Chong, 2007)
~ More introductions lead to a greater probability that an invasive alien species will
become established. The rat e of movement of species between countries has
accelerated since 1900 (Welcomme, 1992). From approximately 100 species of
ornamental fish that have been recorded as introduced into USA and Canada natural
waters via the aquarium trade, 40 have established populations (Rixon et al., 2004),
while in the case of Mexico &om l 15 introduced exotic species 67 have become
established (Contreras, In Press).
~ An increasing variety of goods and means of transport increases both the potential
array of species that may be moved and their pathways for transfer. Only the state of
Florida in the US produces 800 varieties of freshwater fish (Tlusty, 2002) and it has
been stated the high potential risk posed by the tremendous taxonomic diversity of
the ornamental fish industry (Weigle et al., 2005). On the other hand, ornamental fish
are transported by planes, ships and trucks all over the world.
~ More &equent delivery of goods &om and to a wider range of countries and habitats
increases the rate and variety of potential introductions. Data &om the last decade
show that 133 countries imported ornamental fish, while 146 countries exported them
(Huanqui-Canto, G, 2002).
~ Faster modes of transport may improve an organism's chance of survival while in
transit. Fuller (In press) points out that aquarium trade has become the most
important pathway in the introduction of invasive species in the Gulf of Mexico and
South Atlantic region and that potential invasive species are more likely to survive
their journey now than in the past because the increased speed of travel and better
packaging techniques.
Also, internationally, ornamental fish farms constitute one of the main pathways for the
introduction of exotic species into the natural environment. This is in part due to the high
number of continuous changing species and varieties of fish produced and the closeness to
natural freshwater bodies (Copp et al., 2005). Fish are known to have escaped or were
purposefully released from aquarium fish culture facilities, and others were introduced by
well-meaning but misguided aquarists. The escape or release of aquarium fishes into open
waters has never resulted in beneficial introductions. In many such instances, there have been
negative impacts on native fishes and habitats (Contreras-Balderas and Escalante, 1984;
Courtenay and Stauffer, 1990).
The Ornamental Fish Industry in Mexico: History, Size and Scope
The ornamental fish industry in Mexico initiated in the 50's, when ornamental fish were
reared for the first time and important exhibitions in public aquaria were mounted. It is also at
212 R. Mendoza Alfaro, C. Ramírez Martínez, S. Contreras Balderas et al.
this time, that the first ornamental fish production and commercialization association was
established (Ortiz, 1997).
However, the development of the industry through the time was incipient, as stated by the
fact that during the 70's there were only 5 producers and 100 retailers. This industry started
culturing cyprinids, brought from Asia by the federal government, as an alternative to
agriculture. The value of the industry at the time was US $500,000 dollars, while the
importations, represented only US $21,000 dollars (INP, 1974). It is worthy to point out that
during the 70's there were severe restrictions to import exotic species from Asia and Africa
and the availability of equipment for tanks was minimal.
The effort to culture ornamental fish continued and during the 80's several fish farms,
originally created to culture tilapias and &eshwater prawns, were reconverted to culture
ornamental fish due to former cultured species low yields. However, the growth of the
industry kept on being low not only because the government stopped subsidizing the
production, but also due to the lack of experience and technical skills, together with the poor
existing sanitary control measures at that time. (SEPESCA, 1984).
During the early 90's the demand increased and the federal government began providing
proper financial support to establish farms. How ever, the most important contribution to the
industry development and expansion was the nation economic crisis during the mid 90's,
which limited the importers and pushed local producers to sustain the market with fish
accessible to consumers.
In the same sense, &om the official records of imported fish and those of registered
farmers in the states of Morelos, Yucatán, Hidalgo and Puebla, it can be assessed that
ornamental fish commerce grew more than 100 percent in the past decade (Fig. 1) responding
to the continuous growing demand, particularly in the three main large cities (México City,
Guadalajara and Monterrey), where owing to urbanization and lack of space fish rapidly
became the preferred pets.
4 0, 0 0 0
35 ,0 DD
3 0, 0 0 0
o
o25,000
2 0, 0 0 0
l15,00D
10.000
5,0 00
199 4 1995 19 96 19 97 1998 19 99 20 00 200 1 20D2 20 03 200 4 20 05 20 06
Yaar
~ Im porra ~ Nari onalPro duclion T OTAL
Source: INEGI 1994-2006 and Annual Fisheries Statistics 1994-2004.
Figure 1. Sales of ornamental fish in México in the period of 1994-2006.
According to information on the Annual Statistical Reports from Foreign Commerce of
Mexico (1994-2007), and the Annual Fisheries Statistics (1994-2003) the fresh water
aquarium fish trade in México, increased more than 100 percent, going &om approximately
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 213
13 million fish to nearly 37.5 million &om 1994-2006, representing thus an annual growth
rate of 8 percent (Fig. 1).
However, accordingly to a spoken statement from five of the main aquarium fish traders
from M éxico City, it is a common practice to declare less than the amount of fish specimens
than are actually received in shipments, leading to the inaccuracy of official reports. In this
way, importations may be underestimated by almost 25 percent. This situation may indicate
that the number of freshwater fish species traded in México may actually be a bit above 40
million individuals a year (Fig. 2).
45, 000
40„0 00
35„0 00
30 a OOO
25,000
20,000
1 5 , 0 0 0
'10,00 0
5,0 00
1 99 4 19 9 5 1 99 6 199 7 1 99 8 1 999 200 0 2 0 01 2 00 2 2 00 3 2 004 2 00 5 2 00 6
Tea r
~ Es um al od im porl s ~ N al ionai Pro duo uo n TOT AL
Figure 2. Estimated sales of fresh water aquarium fishes in México, during 1994-2006.
Approximately 45 percent of these fish are imported, while the remaining 55 percent are
raised in ornamental fish farms located around several states of the country. These farms are
the source of employment to more than 1,250 persons (Ramírez and Mendoza, 2005).
According to the last economical census there are 5,126 aquarium stores (INEGI, 2005),
however unofficial figures point to the existence of 20,000 aquarium stores, employing
around 41,000 persons.
$18 0
B$16 0
hi $ 1 4 0
JS $ 1 Z O
$10 0
$80
$60
$40
$20
$0
a i m p o r ls aa N a l io n a i p ro d uo Li o n Q T O T A L
Figure 3. Retail amount of sales from ornamental freshwater fish inxico during the period 1994
2006.
214 R. Mendoza Alfaro, C. Ramírez M artínez, S. Contreras Balderas et al.
Ornamental freshwater fishes generate sales accounting to US $161,500,000 dollars at
retail prices, of which 51 percent comes from importations and 49 percent were provided by
national production, with an average annual increase of 18 percent in the last 12 years (Fig. 3)
As a consequence of &eshwater ornamental fish industry rapid growth, diverse risks have
also increased. Unfortunately, a large amount of those exotic organisms accidentally and/or
intentionally have been released to natural aquatic environments and many of them became
invasive.
National Production
The bulk of the national production is concentrated in the state of Morelos, which would
be the equivalent of the State of Florida in the USA .
The number of ornamental fish farms at the national level is uncertain, but it is estimated
to be around 250. To find official figures a request to the National Institute of A ccess to
Information (IFAI) was done, and the National Commission of Aquaculture and Fisheries
answered that "...according to the Law of Transparency there is not a systematized register of
ornamental fish production or producers, however there would be a gross estimate of 128
farms in the state of Morelos..." Nevertheless according to the SAGARPA Coordinator of
Fisheries Promotion at Morelos State there would be at least 200 farms. Moreover, from a
survey made at the national level there are farms located in other 20 states (Fig.4), but these
would not surpass 50. Most of these farms are rustic and are operated at the family level.
+~II/
Figure 4. Mexican states where facilities for the culture of ornamental freshwater fish are located
(marked in black).
The state of Morelos produces around 17 million individuals/year (CONAPESCA, 2005).
These farms are concentrated in 17 of the 33 municipalities of the State and their size varies
from 2,000 m to 1.5 has. Most of them (85 percent) are considered small (between 2,000 to
40,000 m ). The majority of the ponds are concrete made, but the larger ones are rustic
earthen ponds (Fig. 5). The bulk of these fish production is sold mainly in Mexico City,
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 215
Jalisco, Nuevo León, Baja California and Guanajuato States. Fish are sold directly in the
farms or sent to the wholesalers market in Mexico City (SAGARPA, 2005).
Figure 5. Typical ornamental fish farm in the state of Morelos, Mexico.
Nearly all the producers are organized in two main associations. Of the 128 farms
officially registered, 45 belong to the APPOEM Ornamental Fish Farmers Association of
Morelos (Asociación de Productores de Peces de Ornato del Estado de Morelos) and 54 to
"La Perla" (Productores de Peces de Ornato "La Perla" de Morelos A.C) however there are 29
independent farms. The first of these associations was created under an initiative of
ornamental farmers, while the second was created as a request &om the state government, so
the producers could benefit from the different government support programs and economic
subsidies. Ornamental fish farmers have benefited from government official programs not
only by obtaining significant tax discounts, but also by being eligible to financial support and
subsidies of up to US $7,000 dollars, only if their farms are officially registered. Nowadays,
besides representing the producers they serve as a discussion forum to deal with different
problems such as the adaptation of their facilities to new regulations, and homogeneity of
prices to face intermediaries. The greatest part of the production takes place from M arch to
November, as the winter temperatures are rather low for the production of goldfish which
have the highest demand. One of the producers' associations (La Perla) has been looking for
technical assistance of the Morelos State University to increase their production levels. The
main problem faced by producers is the supply of good quality broodstock and the control of
genetic quality of the different varieties of fishes produced.
The recent success of the ornamental fish industry has attracted the interest of several
entrepeneurs &om other sectors, willing to invest on this activity, which will be reflected in
its growth, in the short term.
The variety of ornamental fish produced in Mexico can be considered low when
compared to the international standard, as there are only 61 varieties &om 19 species
216 R. Mendoza Alfaro, C. Ramírez Marnez, S. Contreras Balderas et al.
currently reared. In contrast, it has been estimated that nearly 700 varieties pertaining to l l7
families are imported each year into the country (Alvarez-Jasso, 2004). However, the
economic accessibility to these varieties is restricted and contributes to explain the drop in
consumption during the times of economical crisis.
The varieties currently reared are: Livebearers (mollies, guppies, platies and swordtails)
constituting the bulk of the production, however many usual oviparous fish such as cichlids
(angels and different A&ican cichlids), anabantids (gouramies and betas), characins (tetras),
silurids (catfish, corys and plecos) and chiefly a vast array of goldfish and other cyprinids
(barbs, rasboras, sharks) are also cultured.
Importations
The ornamental fish industry in Mexico has been operating for more than 50 years and
although at the beginning, this industry depended mostly on species captured &om the natural
environment and some imported from Central and South America, imports, for year 2006
have been estimated in nearly 18 million fish.
The main reasons to import fish into Mexico are:
~ The high retailers' price of several alien species
~ The quality of many imported species, that can't be attained by national producers
~ The variety of organisms, which is a fundamental aspect, since the demand in the
ornamental fish industry is fashion-based
~ The availability of many species during the whole year, while in Mexico some
species are just available during a part of the year (e.g. goldfish)
~ The support of the academic sector &om exporting countries
6 , 0 0 0
H5 , Q D D
4 , 0 0 0
3 , 0 0 0
2 , 0 0 0
1, O D D
Yea r
E Co l o m b i a a P e r a Brea ii
Figure 6. Importations of ornamental freshwater fish from South America to México during 1994-2006.
In the case of importations coming from South America, especially from the Amazons
region pertaining to Brazil, Colombia and Peru, a significant change in the volume of fish
exported has been noticed during the last five years. Not only has the total number of
individuals increased in an important way, but also the participation of Colombia over those
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 217
of Brazil and Peru has increased over time. This is in great part due to the Treaty on Free
Trade Between the Republic of Colombia, the Republic of Venezuela and Mexico also known
as G3. In particular, this treaty not only cases the importations of goods coming from
Colombia, but also gives this country an important advantage over the rest due to the tariff
elimination (Fig. 6)
On the other hand, Almenara (2001) points out a disadvantage between importers in
relation to the NAFTA (North American Free Trade Agreement), signed between Mexico,
Canada and the United States of America. According to this agreement, aquatic ornamental
organisms whose origin is either Canada or the USA are duty free, in comparison with 23
percent import duty from other countries; this also applies to the duty on &eight and packing
paid to transport them. As all fishes coming from Asia pass through the USA, this allows
some cheating importers to turn China goldfish into 'American bred' goldfish and, thus end up
paying less than US $15.00 dollars in customs fee per shipment, compared to the more than
US $2,500.00 dollars per shipment with legal papers that honest importers pay. The lack of
professional staff at the Customs Department cannot control this tax and duty evasion that is
harmful to the country. Since it is virtually impossible to determine the precise origin of tank
bred species of fish, the Customs authorities rely only on the exporter's paperwork.
Within this context, in spite of the substantial increase in commercial exchange between
Mexico and the USA after the NAFTA treaty establishment, more than ten years ago, it is
interesting to note that ornamental fish importations follow a cyclic pattern in which every six
years when the federal government changes (1994, 2000, 2006) there is an economic
constriction, which coincides with the drop of importations. Notwithstanding, importations
remain to be the second source of ornamental fish in Mexico
The more frequent imported &eshwater fish families are:
Table 1. Imported families of ornamental fish according to the number of species and
number of individuals.
I l
Cichlidae 107 Characidae l, l 87,788
Characiidae 64 Cyprinidae 1,092,506
Cyprinidae 27 Osphoronemidae 689,776
Callichthyidae 24 Poeciliidae 456,563
Loricariidae 20 Cichlidae 161,276
Conaitidae 15 Ambassidae 133,003
Aplocheilidae 13 Callicthyidae 130,385
Anabantidae 12 Pangasiidae l l 8,739
Pimelodidae I l Loricariidae 102,743
The importance of these families changes when the number of individuals per family is
taken into account. This shows that in some cases, such as the cichlids, a relatively high
number of species, but a small number of individuals is imported, which contrasts with
characids in which a high number of individuals and a low number of species is imported,
obeying to the market demand.
It has been suggested that the risk of establishment largely depends on the biogeographic
origin of the organisms (Ramírez y Mendoza, 2005). Thus, many fish imported from Asia,
Europe and the USA are actually captively bred and consequently are less prone to survive in
218 R. Mendoza Alfaro, C. Ramírez Martínez, S. Contreras Balderas et al.
the wild; however the threat associated to the introduction of these organisms are diseases
caused by exotic pathogens and parasites. In contrast, most of those organisms imported from
South America, particularly from the Amazons, are captured in the wild and consequently
represent a high risk of establishment in a similar environment, as has been the case with
some cichlids and fish of the Loricariidae family. In relation to this, it should be noticed that
ornamental fish importations from South America have been increasing, while those &om
Florida are decreasing, due to import substitutions made by domestic breeders (Almenara,
2001). However, a large amount of fish has been historically imported &om the USA.
Problems of the Industry
During the last decade the culture and commercialization sectors of the ornamental fish
industry have been experiencing some difficulties due to the following aspects:
~ Lack of promotion
~ No research support
~ La ck of internal organization
~ La ck of an efficient regulation
The industry lacks a real and reliable organization due to fierce competition between and
among producers, importers, wholesalers and retailers ("changarreros"). To this should be
added the scarce research on different aspects of ornamental fish species (particularly on
reproduction, nutrition, pathology and genetics), the lack of communication (only a minority
gathers in an annual congress), lack of training or information within the context of
sustainability and responsibility towards the environment (there are very few national
aquarium magazines). The official figures and statistics concerning the sector (number of
producers, arcas of production, volume and origin of imports or countries where fish are
exported) are inaccurate and o&en non trustworthy.
As a consequence of the above mentioned problems, a continuous negative impact to the
environment has been registered, particularly due to the absence of a specific and efficient
legal &amework. Indeed, the absence of regulatory measures requesting farmer owners to
have an adequate infrastructure has originated the continuous escapes of native or exotic
species into the wild. An example is the state of Morelos, where most of ornamental fish
farms are concentrated. In the rivers of this state there are a total of 22 species registered, 8 of
which are native while 14 are exotic (Contreras-MacBeath, 1998).
In addition, several voids in the environmental laws together with the lack of necessary
enforcement have given place to illegal trade (importation and exportation) and translocation
within the country of these species. In fact, despite the existence of a seven day quarantine
period prior to selling the product a&er importation, in many cases the law is not observed by
non-ethical people whose businesses are based on just moving their fishe rapidly without
caring for quality. The results of these improper practices are disastrous to those importers
who have been investing their money, effort and time in order to offer healthy organisms
according to the prevailing rules. They are at a total disadvantage against those people who
keep on cheating the law and doing whatever possible to keep giving away their products
without any consideration. An undesirable, yet expected consequence is that all importers are
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 219
pushed to ignore the quarantine period as well. Even though the authorities know that the law
is not being properly observed (or not observed at all), they cannot act, due to the lack of
resources to enforce the law. In consequence, this leaves the legal importers sector abandoned
at the mercy of unscrupulous merchants (Almenara, 2001). To this should be added the
difficulty to obtain the permits, the frequency to get them (every three months), the strict
specificity of permits (which increase the price with each new species) and the geographical
distance from Mexico City to Mazatlan city (1,085 Km) to obtain the permit where fisheries
authorities are based.
Ecological Risks
In Mexico, fish are commonly released by farmers when prices drop or when a disease is
detected, because due to the cost of antibiotics they will not obtain the desired commercial
value. This situation implies a high risk of escapes generating important problems, such as
competition for food resources and space, predation, native species displacement and
alteration of communities' trophic structure, hybridization, incidence of diseases and parasites
and habitat alteration, (Contreras-Balderas, 1969, Contreras-Balderas and Escalante, 1984,
Lassuy, 2000; MIT Sea Grant, 2002; Goldburg, 2001; Hopkins, 2001)
At the national level, most of the ornamental fish farms lack of adequate biosecurity
systems, implying the risk of disease propagation and escapes of native and non-native
species. In general, operating farms use extensive culture systems, with low or non-existent
technology and are operated by untrained personnel (Ramírez, 1999).
Furthermore, most of the farms are not constructed under the official standards and
regulations established by the environmental authority, such as conducting environmental
impact assessments to demonstrating that the farm w il l not pose any threats to the
environment, as stated by the environmental law (DOF, 2000) and oflen farms do not adopt
current sanitary regulations, (NOM-010-PESC-1993, NOM-011-PESC-1994). As a result,
many farms are located in places where they represent a high ecological risk and are
operating with production systems far from being adequate.
This situation is critical as M exico is one of the five most diverse countries in the world
and among the 12 considered as megadiverse (CONABIO, 2006), that hosts 60 and 70
percent of the known biological diversity in the planet. This high biodiversity is due in part to
the biogeographic conditions of the country, in a transitional zone between the two large
neotropical and neartic regions. As a result, Mexico has a rich source of flora and fauna and
particularly a high species diversity of freshwater fish. There are more than 47 families,
composed by approximately 506 species, 375 of which are exclusively restricted to
freshwater environments (Contreras-Balderas, et al., 2008; Torres-Orozco, y Kobelkowsky,
1991). Additionally to this high diversity, the important variety and isolation of the different
basins has given place to several endemic species which ecological importance is even higher.
One of the reasons why the impact of alien invasive species has passed inadvertently in
Mexico is the high biological diversity of the country. In this regard, it has been stated that
because some ecosystems are richer in number of species than are others, it is likely that such
ecosystems would be less hospitable to establishment and invasion by nonnative species
through species packing over time (Courtenay, 1990). In the same sense Moyle and Light
(1996) mentioned that major community effects of invasions are most often observed where
220 R. Mendoza Alfaro, C. Ramírez Martínez, S. Contreras Balderas et al.
the number of species is low and that invaders are most likely to extirpate native species in
aquatic systems with extremely low variability.
Unfortunately, it should be pointed out that according to the National Fishery Chart (DOF
2004) 9 of the 10 aquatic provinces of the country host several species that have been
introduced due to aquarium trade.
Some of these exotic species have reached critical arcas such as Mexico's Natural
Protected Arcas, characterized by a high endemism, e.g. A&ican jewel cichlid in Cuatro
Cienegas Basin (Contreras-Balderas and Ludlow, 2003). Unfortunately, according to
Contreras-Balderas, (1971) and Hamilton (2001) native species, especially indigenous species
that evolved in isolated ecosystems are o&en very poorly equipped to survive once invasive
alien species are introduced. Additionally, most of the endemic fishes are small and therefore,
subject to more adverse impacts through introductions of small bait or ornamental fishes than
with larger fishes (Courtenay and Deacon, 1982). The prediction of an invasion by non-native
fishes in Cuatro Cienegas and its consequences was reported since 1983 (Courtenay, 1983).
There are two reasons to expect invasion threats &om the aquarium industry to increase
with time. Firstly, the pool of potential invaders is ever expanding as the industry searches for
new, potentially popular species to market. Secondly, because most aquarium species are of
tropical and subtropical origin, the probability of their establishment in North America will
increase with climatic warming (Rixon et al., 2004).
Finally, it should be noted the tight relationship existing between a highly deteriorated
aquatic ecosystems, as those of the state of Morelos, and the establishment of invasive species
as the plecos or the convict cichlid. With this regard, it is difficult to estimate to which extent
the severe pollution was the direct cause of extinction of native species and what role was
played by the invasive species. Anyhow, it has been reported that most impacts, to date, have
been in arcas where habitats modification has already stressed fish populations (Minckley and
Deacon 1968; Deacon 1979; Courtenay, et al, 1985; Welcomme, 1988; Courtenay and
Robins, 1989). Moreover, the environmental tolerance of non-indigenous fish combined with
increasing habitat disruption in streams and lakes assures their continued dispersal into
formerly unoccupied arcas (Boydstun, et al, 1995). This is also true regarding their
establishment, as in aquatic systems with intermediate levels of human disturbance, any
species with the right physiological and morphological characteristics can become established
and long-term success (integration) of an invading species is much more likely in an aquatic
system permanently altered by human activity than in a lightly disturbed system (Moyle and
Light, 1996).
Conclusion
Several aspects in the aquarium trade industry in Mexico need urgently to be reviewed
and modified &om current trade and farming practices to those related to norms, standards
and regulations applicable to the industry. Among these the need to adequately regulate
importations and adopt preventive measures such as risk analysis and the elaboration of white
and black lists. In the case of production there is a strong need of biosecurity standards and
preventive measures such as HACCP (Hazard Analysis to Control Critical Points) plans for
each farm. While in the case of commercialization international measures such as those
proposed by the Ornamental Aquatic Trade Association should be adopted.
Aquarium Trade as a Pathway for the Introduction of Invasive Species into Mexico 221
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... La importación de peces ornamentales es considerada como otra vía de gran importancia para la introducción de especies (Mendoza et al., 2010), la cual depende del número de operaciones de cultivo (Mendoza, com. pers). ...
... La segunda actividad con mayor relevancia en la introducción y dispersión del pangasius en Colombia depende de su cría en acuarios para uso ornamental. De acuerdo con Mendoza-Alfaro et al. (2010), Colombia se encuentra entre los países con mayor comercialización de peces ornamentales. A esto se suman los reportes de mercadeo ilegal de juveniles de la especie en el país (Valderrama et al., 2016) y se ha evidenciado que su tenencia para fines ornamentales también es frecuente en otras latitudes (Jayaneththi, 2015;Khamees et al., 2013;Singh y Lakra, 2012;Lakra y Singh, 2010;Ma et al., 2003;Ng et al., 1993). ...
... They may have been introduced into adjacent waterways through a combination of failed containment structures, fl oods, and migration through existing channels (especially in the extensive network of artifi cial waterways in south Florida). Release by aquarists is a signifi cant source of introductions globally due to the ubiquity of the hobby and the size of the industry in the United States and Mexico(Alfaro et al. 2010). Suckermouth catfi shes are typically kept as solitary specimens by most hobbyists, but due to their famed " janitorial " skills, they are owned by a substantial number of aquarists. ...
... Finalmente, cabe señalar la existencia de una relación directa entre el Tratado de Libre Comercio y la dispersión de especies exóticas invasoras (Burgiel et al., 2006 ); la vía más importante de estas introducciones , intencionales o no, hacia Norteamérica sigue siendo el comercio de organismos (Rixon et al., 2005). En relación con esto, el acuarismo ha sido ampliamente reconocido en todo el mundo como una vía significativa de introducción de especies exóticas a nuevos ambientes (Welcomme, 1992; Courtenay, 1995; Padilla y Williams, 2004; Mendoza-Alfaro et al., 2010 ). Al respecto se ha reportado que las granjas de peces ornamentales representan una de las principales vías de introducción de especies exóticas en ambientes naturales , debido al continuo cambio de especies y variedades de peces producidos y a la proximidad a los cuerpos de agua naturales (Copp et al., 2005). ...
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Rogers Spring, Clark County, Nevada has been the recipient of at least 14 fish introductions since the 1950's. These included one clupeid, two (and possibly three) cyprinids, one clariid, six poeciliids and three cichlids. The known history of this introduced ichthyofauna is reviewed. Tilapia mariae and Poecilia reticulata were discovered in Rogers Spring in 1980. Since this spring has served as a transfer point for introductions elsewhere in Nevada, a consideration of the potential environmental impress of such introductions is included.
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México is the southernmost country in North America, and extends into Central America, south of the Isthmus of Tehuantepec. The northern half of México is located on the Temperate belt and is arid in character (Nearctic), while the rest is within the Tropical belt (Neotropical). Climate varies from extremely temperate desert in the north, to tropical humid in the south. México has more than 500 freshwater fish species, about 271 of them country endemics, and approximately 48 endemics from binational basins. There are still some 30–40 fish species not yet described. There are 563 fish species colonizing coastal flood plain species. In addition to the numbers of colonizing fishes, the burden of introduced exotics has also been growing. In 1904, only 4 species were recognized as exotics; by 1997 the number had increased to 94, and by 2008 to 115. The main fish collections in Mexico are at IPN, UNAM, and UANL and are the most representative, being national in scope, although concentrated in the tropics, central region, and general in coverage, respectively. The decline of the native fish fauna has been in focus in recent years, usually as trend-in-time comparisons, where the loss of native forms and increase of exotics and/or colonizer species is evident in many basins, mainly in Río Balsas, Río Grande, and Río Lerma-Santiago. As a result, the numbers of species reported at some degree of risk have been increasing also, from 17 in 1963 to 192 in 2005. The trends in colonizers, exotics, and species at risk among Mexican fishes are parallel. The Index of Biological Integrity (IBI), in either its geographical, or historical form (IBIh), has been applied to the Rio Grande/Río Bravo basin, USA and México. IBIh values go between 0–91 (average 31). Alien species are regarded as detrimental. Overall, the IBI trends have been similar in all regions, starting from 70–95% in upper reaches, decreasing to less than 0–35% in the lower reaches of West central basins, and then down to 15% or less near the Lower Rio Grande delta. Several alien species of plecos have been recognized in the rivers Balsas, Grijalva-Río Usumacinta complex, and, also, one in the Rio Grande. Mexican rivers are notoriously dewatered in the northern half of the country. Until 1962, the Rio Grande had an average runoff of 12,000+ millions of cubic meters/year; however by 2002 it was less than 2% of that value. The river went nearly dry along the Big Bend region and was dry for months in the delta region, both in 2002 and 2004. The Rio Grande is mostly dry north of the Río Conchos junction, its main Mexican tributary, and other tributaries provide now between 1% (Río San Juan) and 20% (Río Conchos) of pre-1960 runoff. A modified Index of Biological Integrity for Rio Grande resulted in grades from 70 to 95% of the baseline in upper reaches, less than 35% in lower reaches, to less than 15% near the coast. The Texan version of the IBI was not representative as it suppresses data on euryhaline fishes. The reports of total toxics were masked, since the sum should have included both organics and heavy metals exceeding USA regulations to the total count, but only one of the two was included.