Received: 22 November 2018 Revised: 15 July 2019 Accepted: 6 October 2019

DOI: 10.1111/jwas.12662

REVIEW ARTICLE

History, impact, and status of infectious diseases

of the Pacific white shrimp Penaeus vannamei
(Bonne, 1831) cultivated in Mexico

Norma A. López-Téllez1,2 | Juan A. Corbalá-Bermejo3 |

Marco L. Bustamante-Unzueta4 | Laura P. Silva-Ledesma1 |
Víctor M. Vidal-Martínez2 | Rossanna Rodriguez-Canul2
1
Centro Regional de Investigación Pesquera y
Acuacultura de Lerma, Campeche, Instituto Abstract
Nacional de Pesca y Acuacultura, Campeche, The Pacific white shrimp Penaeus vannamei is cultivated
Campeche, Mexico
2 worldwide and is an important economic resource in Mexico.
Departamento de Recursos del Mar, Centro
de Investigación y de Estudios Avanzados, del Despite continuous development of shrimp aquaculture in
Instituto Politécnico Nacional (CINVESTAV—
Mexico, this activity has exhibited variable production rates
Mérida), Mérida, Yucatán, Mexico
3
Escuela Superior de Ciencias Agropecuarias, because of health-related problems. Most of the health
Universidad Autónoma de Campeche, problems have been caused by viruses, such as IHHNV
Escárcega, Campeche, Mexico
4
[syn = penstyldensovirus (PstDV1)], TSV, and WSSV, and
Instituto de Acuacultura del Estado de
Sonora O.P.D., Hermosillo, Sonora, Mexico diseases caused by different species of the genus Vibrio,
such as Vibrio parahaemolyticus (Vp AHPND), which contain
Correspondence
Norma A. López-Téllez, INAPESCA CRIP- a plasmid with genes that encode for the toxins PirA and
Lerma, Km 5 Carretera Campeche-Lerma 200,
PirB. Even with the losses caused by these pathogens, the
Campeche, Campeche CP 24500, México.
Email: [email protected] production of shrimp continues, and the number of hectares
used for production increases year after year. This article
Funding information
CONACyT, Grant/Award Number: 165190 presents a review of the history of shrimp farming in Mexico,
the predominating health problems, and the estimated eco-
nomic impact on shrimp culture. The implementation of
good management practices in aquaculture production is
urgently needed to improve the production on shrimp farms.

KEYWORDS
bacteria, diseases, Penaeus vannamei, shrimp, virus

Significance statement: Data were analyzed from the official records as a set of settlement and the production of shrimp farms in Mexico from 1995 to
2014. The main features include the records of inland farms and their economic value and productivity, as well as major health issues related to shrimp
aquaculture. To our knowledge, this is the first comprehensive overview of the economic impact associated with shrimp diseases in the Mexican shrimp
industry.

© Copyright by the World Aquaculture Society 2019

J World Aquacult Soc. 2019;1–12. wileyonlinelibrary.com/journal/jwas 1

2 LÓPEZ-TÉLLEZ ET AL.

1 | I N T RO D UC T I O N

In terms of economic impact, the most important diseases affecting the penaeid shrimp aquaculture in Mexico are of
infectious origin. In this review, an outline of the historical development of shrimp farming and the presence of the
major outbreaks associated with the shrimp industry are presented using official statistical data and available litera-
ture. The social and economic impact of pandemics caused by pathogens associated with shrimp farming has been
profound, and the attempts to counteract their adverse effects are discussed herein.

1.1 | History of shrimp aquaculture

The shrimp production activities in Mexico are ancient; fishing and the culture of shrimp using enclosures dates back
to the pre-Hispanic period (Cifuentes-Lemus, Torres-García, & Frías-Mondragón, 1997).
According to Sánchez and Soto (1986), there are three relevant species of commercial penaeid shrimp on the
Mexican Pacific coast: the Pacific white shrimp Penaeus vannamei, the western blue shrimp Penaeus stylirostris, and
the brown shrimp Penaeus californiensis. Among them, the most important species is P. vannamei, which has been

commercially cultured on both the Mexican Pacific and Mexican Gulf coastlines since the 1980s (Alvarez-Torres,
Hernández-Martínez, Díaz-Luna, Romero-Beltrán, & Lyle-Fritch, 2000; Arredondo-Figueroa, 2002).
Shrimp culture for research purposes was initiated in the 1970s in the Gulf of California, specifically in Sonora
State (northwestern Mexico), where pioneering work was conducted by the University of Sonora and The University
of Arizona in Puerto Peñasco with controlled cultivation of P. californiensis and P. stylirostris (Lightner, Williams, Bell,
Redman, & Pérez, 1992).
Subsequently, by the end of 1980, commercial cultivation of the blue shrimp P. stylirostris, started in the state of
Nayarit. During this period, the Mexican government also encouraged the social sector to construct and operate the
first commercial aquaculture production units in Sinaloa and Sonora, and by 1990, the production was of 4,371 T
(CONAPESCA, 2014). This initiative provided significant profits; however, the national production of shrimp was still
supported by offshore fishing until the 1990s. In 1981, there were four shrimp farms located on the Pacific coast:
two in Nayarit, one in Sinaloa, and another one in Sonora with a covered inland area of more than 60 ha in total

(Alvarez-Torres et al., 2000). However, it was not until 1999 that the shrimp farming sector was necessary to supply
the commercial demand that was impossible to sustain by offshore fishing alone (FAO, 2016). Despite the marked
growth of shrimp aquaculture in the area, there were factors that contributed to the inconsistent increase in produc-
tion which highlight some questions:

• What factor or factors explain improvements in the trend of shrimp aquaculture growth in Mexico?
• What was the impact of this change in the aquaculture sector within the country?
• What actions have been implemented and what are their scopes?

1.2 | Shrimp production and health problems

Shrimp aquaculture, like most agricultural activities, is bound by various factors; however, the most important are
physical factors such as the availability of water and suitable areas. For this review, the shrimp industry in Mexico
was analyzed based on the official production (CONAPESCA, 2014) and productivity, measured in shrimp weight
production per unit area (Equation 1):

Productioni
Productivityi = , ð1Þ
Cultured areai
LÓPEZ-TÉLLEZ ET AL. 3

where Productivityi is the national productivity during year i, Productioni is the national production of shrimp in
aquaculture systems during year i, Cultured areai is the area of the national territory designated to the commercial
cultivation of shrimp during year i.
Official records of commercial shrimp aquaculture recorded from 1995 to 2014 are shown in Figure 1. Since the
beginning, production (T) (bars) has displayed a positive exponential growth; however, in the period of 2005–2013,
the production showed an asymptotic trend. In 1996, the production was 13,114 T in an area of 18,188 Ha, whereas
in 2013, the production increased 4.6 times (60,191 T), with an area that increased 4.7 times (86,438 ha). Thus, in a
period of 17 years, the culture area increased by 68,250 ha (solid line). However, the average annual productivity in
1996 was 0.72 T/ha and in 2013 it was 0.70 T/ha (discontinuous line), corresponding to the lowest registered pro-
ductivity values in the studied period.
During this period, the water supply was adequate, as well as feed and technical knowledge on shrimp aquacul-
ture. Moreover, health issues were the most important biotic variables explaining the decrease in productivity. For
instance, in 1995, there were 231 shrimp farms with 14,302 ha of cultured area with a productivity of 1.11 T/ha,
whereas in 2014, there were 1,447 farms, with a production of 86,438 T, and a productivity of 1 T/ha (Figure 1).

2 | VIRUSES: THE MAIN PROBLEM

Outbreaks caused by viral infections have caused a reduction in production and increased economic cost. Apart from
this, to avoid the risk of further infections, there is an extra cost for the disposal of dead organisms.

2.1 | Infectious hypodermal and hematopoietic necrosis virus, IHHNV

[Syn = penstyldensovirus (PstDV1)]
Penaeid shrimp either collected from the Gulf of California or from culture facilities in the region tested negative for
IHHNV (PstDV1) until 1987. Farms relied on wild broodstock collected nearby and from seed from three hatcheries
reported at the time (Lightner et al., 1992). This changed in 1987 with the introduction and spread of IHHNV
(PstDV1) with imported stocks of penaeid shrimps. The first outbreak of IHHNV (PstDV1) occurred on a shrimp farm
of P. stylirostris located in La Paz, Baja California Sur (Galaviz-Silva & Molina-Garza, 2014), which in turn caused seri-
ous epizootic problems in the shrimp farms of Sonora and Sinaloa.

140,000 2.00
1.80
120,000
1.60
100,000 1.40
Productivity (T/Ha)
Cultured area (Ha)

1.20
Production (T)

80,000
1.00
60,000
0.80

40,000 0.60
0.40
20,000
0.20
0 0.00

Time (Years)
Production (T) Cultured area (Ha) Productivity (T/Ha)

F I G U R E 1 National production of shrimp in culture systems. Area designated for the culture of the species and
the productivity during the period 1995–2014 (CONAPESCA, 2014)
4 LÓPEZ-TÉLLEZ ET AL.

IHHNV (PstDV1) was characterized in 1990 and determined to be related to the parvoviruses (Bonami &
Lightner, 1991; Bonami, Trumper, Mari, Brehelin, & Lightner, 1990). Age and species differences in susceptibility to
the IHHN (PstDV1) virus were later reported (Bell & Lightner, 1984, 1987). According to Lightner et al. (1992),
IHHNV (PstDV1) was introduced to Mexico, because the demand far exceeded the available seed supply. As a result,
postlarval P. vannamei, P. stylirostris, and infected tiger shrimp Penaeus monodon stocks were imported by commercial
shrimp farming cooperatives from commercial sources in the United States, Hawaii, Panama, and Ecuador (Lightner,
1996; Lightner, 2005; Lightner, 2011; Lightner et al., 2012; Tang & Ligthner, 2002). Although IHHNV (PstDV1) is
lethal to P. stylirostris, it does not cause mortality in P. vannamei; instead it causes deformity and dwarfism syndrome
(RDS) (Bell & Lightner, 1984).
Shrimp that survive the acute phase chronically suffer from RDS and transmit the infection vertically (paternally
from parent to offspring), and horizontally (between organisms) (Dhar, Roux, & Klimpel, 2001). The gradual change in
cultivation from P. stylirostris to the white shrimp P. vannamei was probably motivated by the success in the manage-
ment and survival of this species in addition to its tolerance to IHHNV (PstDV1).

2.2 | Baculovirus penaei

The first report of Baculovirus penaei (BP) was in P. stylirostris larvae cultivated in Guaymas, Sonora, and its reported
mortality was up to 100% (Lightner, Redman, & Ruíz, 1989). Tetrahedral baculovirosis is the name given to the disease
caused by infection with BP. The ICTV name for the virus is PvSNPV (singly enveloped nucleopolyhedrovirus from
P. vannamei) (Overstreet, Stuck, Krol, & Hawkins, 1988). BP infections are most serious in the larval stages and the dis-
ease can be diagnosed by simple wet-mount squashes that show the pathognomonic tetrahedral viral occlusion bodies
in the hepatopancreas or midgut, which are the target organs of the virus (Wang, Hong, & Lotz, 1996). The disease is
transmitted from parents to offspring by fecal contamination of the spawned eggs. The application of routine disinfec-
tion methods to eggs and nauplii in penaeid shrimp hatcheries has significantly reduced the occurrence and impor-
tance of this disease.

2.3 | Taura syndrome viruses

The first outbreak of Taura syndrome viruses (TSV) was recorded in the state of Sinaloa in 1995 (Zarain-Herzberg &
Asencio-Valle, 2001). TSV is one of the most economically significant viruses infecting penaeid shrimp in the western
hemisphere (Brock, Gose, Lightner, & Hasson, 1995; Hasson et al., 1995). TSV epizootics in Sinaloa, Mexico, reached
a peak during 1996, followed by a steady decline, and by 1998, shrimp production in Sinaloa appeared to have stabi-
lized. This decrease in TSV outbreaks was attributed to the farming of TSV-tolerant P. stylirostris instead of TSV-
susceptible P. vannamei (Zarain-Herzberg & Asencio-Valle, 2001). The replacement of P. vannamei with P. stylirostris
in shrimp farms might have contributed to the development of a new strain (s) of TSV in Mexico because the virus
has the ability to adapt to new host species (Robles-Sikisaka et al., 2002).
The most susceptible species to TSV is the white shrimp P. vannamei, which has a mortality rate of up to 90%
(Briggs, Funge-Smith, Subasinghe, & Phillips, 2005). It has also been estimated that TSV caused a mortality of up to
80% in farms in Nayarit and Sonora (FAO, 2016).
Animals that survive acute infection might carry the virus for life and can transmit it horizontally and potentially
vertically (Flegel, 2006).
TSV is rapidly spread locally from farm to farm. Some authors have reported that the excrement of marine birds,
such as seagulls, can transport the virus mechanically (Garza et al., 1997).
LÓPEZ-TÉLLEZ ET AL. 5

2.4 | White spot syndrome virus

White spot syndrome virus (WSSV) has a history of causing catastrophic economic losses on shrimp farms world-
wide. The devastating effect occurs in a short period of time (from 3 to 10 days) with mortalities of approximately
100% (Dhar et al., 2001). In Mexico, WSSV caused a major outbreak in 1999 in farms located in northwestern
Mexico (Esparza-Leal et al., 2010).
In Mexico, WSSV was first reported in 1999 and soon caused severe losses, first in the culturing of Penaeus
stilyrostris and later for P. vannamei (Galaviz-Silva & Molina-Garza, 2014; Esparza-Leal et al., 2010). Apparently,
WSSV-contaminated postlarvae were introduced in areas where BP and IHHNV (PstDV1) were endemic (COSAES,
2014). Despite the increase in the cultivated hectares in Mexico, the production of shrimp stagnated as a result of a
decline in productivity in the years 1999, 2002, and 2012 compared to the previous year. The reason for this drop
might be related to the economic loss related to the presence of pathogens.
In addition to the first report of WSSV in 1999, this viral infection reappeared during the years 2005, 2010, and
2012. For example, in 2005 alone, the official sheet records reported that WSSV caused a loss of approximately
100 million of dollars on farms in Sonora, Sinaloa, and Nayarit (Esparza-Leal et al., 2010).
In this sense, WSSV is a recurrent health problem that is difficult to eradicate. For instance, it has more than
100 host vectors and affects crustaceans that live in fresh, brackish, and marine waters, as well as polychaetes,
bivalves, rotifers, larvae of insects, and microalgae that can accumulate high viral loads, acting as mechanical vectors
(Liu, Yu, Song, & Guan, 2007).

3 | T H E P R O B L E M O F B A C T E R I A L OR I G EN

3.1 | Acute hepatopancreatic necrosis disease

Acute hepatopancreatic necrosis disease (AHPND), previously referred to as early mortality syndrome, initially emerged
as a destructive disease of cultured shrimp species in Asia in 2009. The pathogen associated with the disease, Vibrio
parahaemolyticus, also called VpAHPND, emerged in Mexico in early 2013. In all countries where VpAHPND was reported,
massive economic loses were also reported, and Mexico was not the exception. According to Nunan, Lightner, Pantoja,
and Gomez-Jimenez (2014), a large economic loss occurred in Sonora, Sinaloa, and Nayarit states. For instance, Nunan
et al. (2014) reported significant losses of −0.45 T/Ha in the Mexican aquaculture industry in 2013. In the same year,
VpAHPND reduced the total production of cultivated shrimp to 60,292 m.t. This was 40,000 m.t. less than the total pro-
duction recorded during the previous year (100,321 m.t.) (CONAPESCA, 2014). VpAHPND can cause serious losses when
the culture conditions are suboptimal. This pathogenic bacterium harbors a 69-kb plasmid that contains two genes
homologous to the Photorhabdus insect-related (Pir) toxin genes, pirA and pirB (Han, Tang, Pantoja, White, & Lightner,
2015). The bacterium VpAHPND can either be transmitted horizontally through cannibalism or through bird feces, or by
the consumption of detritus found in the water column and the bottom of the pond. After ingestion, the bacteria colo-
nize the digestive tract and if the conditions are suitable, the pirA and pirB genes result in the expression of toxins that
cause damage to hepatopancreatic cells during the acute phase (FAO, 2013).

4 | E F F E C T O F P A T H O G E N S ON P R O D U C T I ON

During the study period (1995–2014), the diseases recorded in Mexico were TSV, WSSV, IHHNV (PstDV1), and
VpAHPND and negative changes were observed during the years 1996, 2010, 2012, and 2013 regarding the national
production levels of cultivated shrimp (Figure 2). These diseases cause mortality, and they probably constitute at
least one reason why the national production decreased during these years. In 2002, there was also a negative
change in production; however, it might have been due to a reduction in the cultivation area from 52,648 to
6 LÓPEZ-TÉLLEZ ET AL.

1999 2003 2005

30,000 WSSV 2007 2011 3.00
WSSV TVS
17,372 TSV 2009 PstDV1
5,313 16,553
20,000 908 PstDV1 8,483 2.50
3,091

Changes in productivity (T/Ha)

10,000 2.00
Changes in production (T)

0 1.50

-10,000 1996 2002 1.00

TSV Decrease culture
2012
-2,753 area
-20,000 WSSV 0.50
-2,314
-9,496
-30,000 0.00

-40,000 2010 2013 -0.50

WSSV VpAHPND
-50,000 -32,652 -39,284 -1.00

Time (Years)
Changes in production (T) Changes in productivity (T/Ha)

F I G U R E 2 Changes in production and productivity of shrimp in aquaculture systems during the period of
1996–2014. In the figure, the years in which any disease was reported and the change in the production during that year
are indicated. The values of change in productivity, marked with a triangle, indicate negative values (CONAPESCA, 2014)

49,689 ha (Figure 1). In the data evaluated herein, total shrimp cultivation showed increases and decreases
(Figure 1); therefore, losses in production cannot be explained by the effects generated by the disease alone. The cal-
culation of productivity (production/cultivated area) allows the elimination of this effect, and the calculation of the
change in productivity (Equation (2)) allows the determination of whether productivity decreased during the disease
years, which would indicate, on average, fewer shrimp produced per unit area of culture.

cProductivityi = Productivityi − Productivityi −1 , ð2Þ

where cProductivityi is the change in productivity, Productivityi is the change during year i, Productivityi − 1 is the
productivity during year i−1.
Figure 2 shows that in 1996, when TSV was recorded, a negative change in production occurred. In that year, there
were 18,188 ha under production, with a productivity of 0.72 m.t./ha. In 1999, the production increased to 28,288 m.t.,
and the productivity increased to 1.08 m.t./ha, over 26,291 ha. In 1999, the first outbreak of WSSV occurred in Mexico,
and although a positive change in the production was observed, there was a concurrent negative change in productivity.
In 2001, the water surface area for production increased by 49% compared to the previous year; however, the
productivity was 0.90 m.t./ha, which was a decrease of −30 m.t./ha in comparison to 2000. During that year, no viral
disease was reported, which supports the hypothesis that, despite the federal government having recorded an
increase in the number of farms, those farms did not begin working until the following year. Additionally, the hect-
ares of intensive cultivation decreased from 3.05% to 0.71% on the national level in 2001. In 2002, the total produc-
tive surface decreased from 52,648 to 49,689 ha, and the national productivity was 0.91 m.t./ha. In 2003, the
production increased to 61,704 m.t.; however, this could be because of the number of productive hectares increas-
ing to 15,396. Additionally, in 2003, the presence of TSV was detected for the second time.
Low productivity is masked when the cultured surface increases, because this apparently increases production;
however, in a detailed analysis it was observed that an increase in the productive surface area did not correspond to
an increase in biomass. This situation is more noticeable after the detection of WSSV in 2005, and TSV in 2007. The
viruses appeared on alternate years, for instance, TSV in 1996, 2003, and 2007, and WSSV in 1999, 2005, 2010, and
2012. Importantly, during these years, the highest productivity was 1.38 m.t./ha, obtained in 2010. In comparison,
IHHNV (PstDV1) was detected in 2009, and 2011, when the productivity was 1.81 and 1.53, respectively (Figure 2).
LÓPEZ-TÉLLEZ ET AL. 7

Likewise, as mentioned above, an important outbreak occurred in 2013 and most of the affected farms recorded
up to 100% mortality rates, VpAHPND was reported as the causal agent (Nunan et al., 2014). However, it is still
unknown whether the illegal introduction of larvae or broodstock carrying the bacteria was the causal agent.
VpAHPND caused a significant loss of −0.45 m.t./ha during 2013, and the highest losses caused by WSSV were
−0.42 m.t./ha. In 2013, with the emergence of VpAHPND, there were losses of 39,284 m.t. compared to 2012, and
the productivity was 0.7 m.t./ha (Figure 2).
The negative productivity values indicate the quantity of shrimp that was not produced per unit area in 1 year
compared to the previous year. Of the data analyzed, the change in productivity has been negative only for the years
when a disease was reported (1996, 2010, 2012, and 2013), with the exception of 2002, in which the negative value
was a consequence of a decrease in the cultivated area of intensive farms, from 52,648 to 49,689 ha.

5 | E S T I M A T E D EC ON O M I C I M P A C T

In economic terms, if productivity decreases, it is possible that the economic value generated per ha (economic pro-
ductivity) will also decrease depending on the price per unit of shrimp (with the exchange rate being considered as
the average exchange rate of that year). If the productivity decreases, there is an economic value that is not gener-
ated per unit area, compared to the previous year. If productivity increases, there is an additional economic value
generated compared to the previous year.
The economic value is calculated depending on the change in productivity (VcP, Equation (3)). Negative values
indicate an economic value not generated per hectare in a year because of low productivity compared to the previ-
ous year. Positive values indicate that the economic value generated per hectare was higher than the previous year.

VcPi = ðcProductivityi ÞðuPricei Þ, ð3Þ

where VcPi is the economic value because of the change in productivity, cProductivityi is the change in productivity
during year i compared to year i−1, uPricei is the Unitary price during the year i.
The impact of a disease is more evident in the economic value because of the change in productivity (VcPi) than
the impact shown only by the change in production, but is similar to that shown by productivity. It can be observed
that, per hectare (ha) and compared to the previous year, in 1996, 1999, 2007, 2010, 2012, and 2013, a certain eco-
nomic value was not produced (Figure 3). The least effect was caused by TVS in 2007 when, compared to the previ-
ous year, the production per hectare reached a value of 230 USD/ha. VpAHPND was the disease that had the greatest
effect because an economic value of 2,320 USD/ha was not produced.
At a national level, the economic value because of the change in productivity has varied, and with the exception
of 2001, every year in which the economic value was negative, a disease was also reported. However, the economic
value was positive in 2003, 2005, 2009, and 2011, in which there were reports of TVS, WSSV, IHHNV (PstDV1),
and IHHNV (PstDV1), respectively.
Table 1 displays the years from 1996 to 2014, the diseases that were recorded during those years, and the eco-
nomic values that were not produced each year (compared to the previous year) at a national level. VpAHPND reduced
the economic production by $200,632,180.25 USD in 2013, and the economic loss that occurred in 2013 attributed
to VpAHPND alone surpassed the reduced economic production.

6 | A C T I O N S T H A T H A V E B E E N I M P L E M E N T E D TO M I T I G A T E T H E
IMPACT

The first and only action that was taken during the IHHNV (PstDV1) outbreak in 1987 was to replace the blue shrimp
P. stylirostris with the white shrimp P. vannamei because it is more tolerant of or less susceptible to the disease.
8 LÓPEZ-TÉLLEZ ET AL.

Thousands
$3.00 2005 $8.00

Economic value due to change in

WSSV 2011
$2.00 2003 $0.62
2009
PstDV1 $7.00
productivity (USD/Ha)
TSV $0.47
PstDV1
$1.00 $0.15 $0.07
$6.00
$-

Price (USD)
2007
$5.00
$(1.00) TSV
$(0.23) $4.00
$(2.00) 1999
1996 WSSV 2001
TSV 2010 2012
$(3.00) $(1.22) Decrease 2013 $3.00
$(1.91) of intensive WSSV WSSV VpAHPND
farms $(1.36) $(1.36) $(2.32)
$(4.00) $(1.84) $2.00

Time (Years)
Economic value due to changes in productivity (USD/Ha) Price (USD/kg)

F I G U R E 3 Estimation of economic values because of the change in productivity and price per kg of shrimp
produced in aquaculture systems during the period 1996–2014. The figure displays the years in which a disease was
reported and the economic value because of the change in productivity in that year. Negative economic values
because of the change in productivity indicate the economic amount that was not produced in that year compared
to the previous year (CONAPESCA, 2014)

T A B L E 1 Estimation of the economic

Value (US) of lost production as
value because of the change in
Year Disease compared to previous year
productivity and price per kg of shrimp
1996 TSV −$34,752,492.52 produced in aquaculture systems during
1999 WSSV −$31,944,036.57 the period 1996–2014
2001 No disease −$96,964,276.74
report
2003 TVS $9,973,340.46
2005 WSSV $43,981,779.43
2007 TSV −$15,362,428.38
2009 IHHNV $5,277,798.47
(PstDV1)
2010 WSSV −$98,702,910.72
2011 IHHNV $33,459,614.17
(PstDV1)
2012 WSSV −$117,428,598.20
2013 VpAHPND −$200,632,180.25

Note: Negative values indicate the economic value that was not generated
per hectare in a year because of a low productivity compared to the
previous year.

In 1997, following the detection of TSV, the federal government took developmental actions such as: 1) optimizing the
existing laboratory infrastructure, 2) closing the culture cycle under controlled conditions, 3) implementing a large number
of laboratories for postlarvae production, 4) producing lines of genetically selected shrimp broodstock, 5) promoting good
management practices, and 6) because of the viral infections occurring during all the stages of the life cycle of shrimp, the

translocation of organisms of different ages (e.g. broodstock, postlarvae, etc.) was reduced (Alvarez-Torres et al., 2000).
In addition, the Mexican government created the Official Mexican Standard (Norma Oficial Mexicana, NOM)
including NOM-011-PESC-1993 (n.d.), NOM-020-PESC-1993 (n.d.), NOM-022-PESC-1994 (n.d.), and NOM-EM-
LÓPEZ-TÉLLEZ ET AL. 9

001-PESC-1999 (n.d.). These established the requirements and measures to prevent and control the introduction
and dispersion of viral diseases known as “white spot,” and “yellow head.” The Journal Official Federation (DOF,
2012) established health regulations for aquatic species, their products and subproducts. However, some of the reg-
ulations are hard to fulfill because the movement of animals is recurrent in the country.
In Puerto Vallarta, Jalisco, from July 24 to 28, 2000, the International Cross-border Movement of Aquatic Animal
Pathogens and the Standardization of Techniques in Aquaculture Health workshop was held with representatives from
four international organizations: OIE, FAO, NACA, and APEC. SENASICA produced a new fishing and aquaculture law
on October 22, 2007, resulting in the creation of aquaculture health committees of each state. Today, there are three
official laboratories that diagnose the diseases of aquatic organism, including the National Centre of Animal Health Ver-
ification Services (Centro Nacional de Servicios de Constatación en Salud Animal, CENAPA), the National Centre for
Animal Health Diagnosis Services (Centro Nacional de Servicios de Diagnostico de Salud Animal, SENASA), and the
Mexico-United States Commission for the Prevention of Foot-and-mouth Disease and other Exotic Animal Diseases
(Comisión México–Estados Unidos para la Prevención de la Fiebre Aftosa y otras Enfermedades Exóticas de los ani-
mals, CPA) which are responsible for epidemiological surveillance of the country's aquaculture units and three qualified
laboratories certified by a Mexican Agency (EMA = Entidad Mexicana de Acreditacion), that are authorized by the gov-
ernment to issue health certificates for importation and exportation of frozen commodities and live organisms.
In 2014, when the presence of VpAHPND was suspected, the federal government provided for the first time an
economic support of 600 million Mexican pesos (MP), of which 283.5 million was given to the shrimp farmers, 317.5
million MP was designated for insurance, and 140 million was used to support the acquisition of shrimp larvae for
seeding. A temporary suspension of shrimp imports from China, Malaysia, and Thailand was also implemented by
SENASICA in April 2014 (SAGARPA, 2014).

7 | D I S C U S S I O N A N D C O N C L U S I ON S

Shrimp farming with a value annually of approximately US $711 million, is one of the most important primary activities
in Mexico. In 2014, the production of shrimp reached 158,123 m.t., 60.58% of which was produced by aquaculture
(CONAPESCA, 2014). Despite high profits, shrimp farming has been facing mass mortalities associated with pathogens
that have limited its development. The OIE define an epizootic event as an infectious disease that affects a high num-
ber of organisms of the same species or of different species at the same time and in the same place, and that propa-
gates rapidly. These characteristics have been displayed by IHHNV (PstDV1), TSV, WSSV, and the bacterium VpAHPND.
In 1987, the cultivation of P. vannamei instead of P. stylirostris was fundamental for the development of
P. vannamei aquaculture, which is now the most cultivated species worldwide (Lightner et al., 2012). Indeed, the
growth of shrimp farming in Mexico would not have been possible without the development of the Pacific white
shrimp P. vannamei aquaculture.
Despite the fluctuation in production observed over the three decades of shrimp aquaculture in Mexico, the
most devastating effect apart from WSSV (Esparza-Leal et al., 2010), was that of VpAHPND (Nunan et al., 2014).
Although it is still unknown what factors triggered this outbreak, it is necessary to evaluate whether the genetic lines
of shrimp that were tolerant to WSSV and imported from Asia, were the carriers of this pathogen. VpAHPND caused
high mortalities in China in 2009, in Vietnam 2010, in Malaysia 2011, and in Thailand in 2011 (Flegel, 2012). It is
likely either that postlarvae or broodstock of P. vannamei were irregularly introduced and/or that the diagnosis of
this disease was inefficient before shrimp importation.
The shrimp industry started in 1970 in the states of Sonora, Sinaloa, and Nayarit, and nowadays, this industry is
sustained by approximately 1,500 farms located in the same states (COSAES, 2014). The economic success of this
industry in the Gulf of California is high; however, the cost is high. From the data analyzed herein, it was observed
that an increase in the productive surface area did not correspond to an increase in biomass. Apart from the eco-
nomic losses associated with outbreaks, the safe and environmentally responsible disposal of animal carcasses,
10 LÓPEZ-TÉLLEZ ET AL.

whether an individual death or during significant mortality events, is an essential consideration. For instance, in
Mexico, native shrimp is a very important resource from ecological, social, and economic perspectives. As an exam-
ple, IHHNV (PstDV1) has become enzootic in wild shrimp from the Gulf of California (Robles-Sikisaka, Bohonak,
McClenaghan Jr., & Dhar, 2010). Although it is difficult to evaluate the effect of the pathogens in shrimp from natural
environments, it is necessary to be concerned that wild shrimp sustain regional fisheries. For the rest of the country,
the risk of disease transmission would be mitigated by planning inland farms with proper management procedures.
Additionally, the number of qualified laboratories must increase. Only certified laboratories should produce shrimp
postlarvae free of pathogens. Also, the implementation of sanitary checkpoints along the country would be useful
during transportation of live shrimps within the country.
Finally, the viral diseases described herein will continue, cyclically and recurrently, because of their nature. There-
fore, it is necessary to track their epidemiological characteristics and compile data that will allow us to predict their
recurrence. It is also necessary to generate, review and update local regulations with scientific criteria, and likewise
to comply with the OIE (2015) guidance regarding the transport of animals. Overall, it is fundamental to guarantee
the transparency of the procedures of all the intervening actors (government, producers, and academies), to avoid
the risks of introducing new pathogens.

ACKNOWLEDGMENTS

We would like to thank to Biol. Yuliana Zurita Moo (INAPESCA, CRIP-Lerma) and MSc. Juan Antonio Pérez-Vega
(CINVESTAV IPN Unidad Merida), for their technical support. We are grateful to Dr. Rodrigo Vichido Chávez
(SENASICA, CENAPA), for his comments to an earlier version of the manuscript. This manuscript is part of the PhD
thesis of N.A.L.-T. (CONACyT Scholarship No. 165190). Special thanks are conveyed to the anonymous reviewers.
The Instituto Nacional de Pesca y Acuacultura supported financially this review.

CONF LICT OF IN TE RE ST

The authors declare no potential conflict of interest.

AUTHOR CONTRIBUTIONS

The first author conceived the idea, the rest of the authors contributed to the redaction, discussion, and edition of
the ms.

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How to cite this article: López-Téllez NA, Corbalá-Bermejo JA, Bustamante-Unzueta ML, Silva-Ledesma LP,
Vidal-Martínez VM, Rodriguez-Canul R. History, impact, and status of infectious diseases of the Pacific white
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