Aquacultural Engineering 58 (2014) 107112

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Aquacultural Engineering
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Short communication

Mass balances of nitrogen and phosphorus in an integrated culture of

shrimp (Litopenaeus vannamei) and tomato (Lycopersicon esculentum
Mill) with low salinity groundwater: A short communication
M. Martin Mariscal-Lagarda a , Federico Pez-Osuna b,c,
a

Universidad Estatal de Sonora, Calle Independencia y 5 de Mayo, Benito Jurez, Sonora, Mexico
Instituto de Ciencias del Mar y Limnologa, Universidad Nacional Autnoma de Mxico, Joel Montes Camarena s/n, Mazatln 82040, Sinaloa, Mexico
c
Miembro de El Colegio de Sinaloa, Mexico
b

a r t i c l e

i n f o

Article history:
Received 11 May 2013
Accepted 19 December 2013
Keywords:
Shrimp-tomato culture
Nitrogen
Phosphorus
Groundwater
Sonora, Mexico

a b s t r a c t
This study re-examines the performance of an integrated shrimp-tomato system using the nutrients mass
balance approach. A budget was calculated based on nutrients analysis, water management, feeding,
fertilization, stocking, harvest and sludge removal. Nitrogen and P content in the input water (groundwater) were low, contributing 33.5% and 0.5%, of the total inputs, respectively. Most of the N (43.6%)
and P (98.8%) entered to the system as shrimp food. Likewise, 15.2% and 2.5% of the input N, and 8.9%
and 4.3% of the input P, were converted to harvested shrimp and tomato plants, respectively; 4.1% N and
24.6% P remained in the organic sludge, while the environmental losses expressed per unit of production were relatively low, 57 kg N ton1 and 7.1 kg P ton1 of product harvested. About 13.4% of input N
was unaccounted for, and was assumed to be lost to the atmosphere via denitrication and volatilization. Comparison between these results and previous studies indicate that the shrimp-tomato system
produces a relatively low recovery of N and P as harvested products, however, the main progress reached
with this system is the reduction of the environmental losses of N and P in terms of kg of each nutrient
per ton of the product harvested.
2014 Elsevier B.V. All rights reserved.

1. Introduction
The integrated aquacultureagriculture system emerge as a
means to decrease dependency of chemical fertilizers (Fernando
and Halwart, 2000), optimize the use of limited water resources
(McIntosch and Fitzsimmons, 2003) and increase economic return
per unit of water (Stevenson et al., 2010). This strategy it is particularly pertinent in those regions where water resources are limited;
arid and semi-arid lands where agriculture is difcult of operate at
recurrent droughts and where the continue application of chemical fertilizers affects quality of groundwater and surface waters.
Another additional advantage of integrated systems is the decrease
of the environmental cost that implies individually to such cultures; each culture separately imposes an environmental impact in
terms of water use and the amounts of nutrients discharged, which
may be signicantly reduced when two cultures are appropriately
integrated (Mariscal-Lagarda et al., 2012).

Corresponding author at: Instituto de Ciencias del Mar y Limnologa, Universidad

Nacional Autnoma de Mxico, Joel Montes Camarena s/n, Mazatln 82040, Sinaloa,
Mexico. Tel.: +52 669 9852845; fax: +52 669 9826133.
E-mail address: paezos@ola.icmyl.unam.mx (F. Pez-Osuna).
0144-8609/$ see front matter 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquaeng.2013.12.003

In the specic case of inland aquaculture, efuents have been

utilized for a number of agricultural products. For example, freshwater from sh cultures has been used traditionally for the
irrigation of rice and various vegetables (Phong et al., 2011).
Similarly, moderately saline groundwater from shrimp farming
in Arizona, has been used for irrigate cotton, sorghum, wheat
and barley (McIntosch and Fitzsimmons, 2003; Stevenson et al.,
2010).
The prerequisites to achieving a reduction in nitrogen and phosphorus waste include a quantitative understanding of the nutrients
mass balances, and an understanding of the uxes associated with
the distinct components of the culture systems. The strategy of
nitrogen and phosphorus budget allows a comparison of nutrient
loading from shrimp systems operated traditionally and with the
integrated shrimp-tomato system, and permit an assessment of
progress in achieving waste reduction. The objective of the present
study was to expand the information presented in Mariscal-Lagarda
et al. (2012, 2013) on the nutrients mass balance budget of the
shrimp (Litopenaeus vannamei)-tomato (Lycopersicon esculentum
Mill) system. We use the mass balances to assess the performance
identifying the proportion of nutrients in each compartment of
the shrimp-tomato system, and to demonstrate the reduction of
nutrient losses in comparison to shrimp monoculture.

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M.M. Mariscal-Lagarda, F. Pez-Osuna / Aquacultural Engineering 58 (2014) 107112

2. Materials and methods

2.1. Production system, stocking, feeding, planting and harvest
The production system and experimental design, stocking, fertilization and feeding of the shrimp tanks, planting and harvest of
tomato were described previously (Mariscal-Lagarda et al., 2012,
2013), here is included only a synthesis. A 19-week eld study
was developed in Sonora State, NW Mexico during August 4 to
December 12 2008. Three circular tanks (31.1 m3 ) covered with
liner were used. Three water types were tested on the basis for
3 treatments: efuent water from shrimp culture tanks (treatment
A), hydroponic nutrient solution prepared for tomatoes (treatment
B), and water directly from the well (treatment C). Each module contained 3 rows of 15 individually potted tomato plants, and
each row was randomly assigned to one of the 3 treatments. However, here only are presented the results from treatment A. The
tomato plant in each pot was placed in a zeolite base. Aeration in
shrimp tanks was maintained with a blower of HP. Water from
the shrimp tanks was discharged by gravity and dripped into pots
through a hydraulic pipe (3.4 L plant1 day1 ). The efuent not consumed by the plants was recollected and returned to the shrimp
tanks.
The tanks were lled with groundwater (electrical conductivity,
1074 S cm1 ) and supplemented with KCl and MgNO3 to the level
where K and Mg reached the theoretical concentrations equivalent for the salinity of seawater diluted (Roy et al., 2010). Shrimp
postlarvae were stocked into the tanks at a density of 50 PL m2 .
A commercially formulated feed (NassaTM #1 pellets of 0.635 mm:
protein 40%) (Animalnutri Mxico, S.A. de C.V.) was used in the
rsts 7 weeks; 3.0 0.1 kg of feed per tank was used during the
cycle. From week 8 until week 19, feed with a second formulated
feed (NassaTM #2 pellets of 0.794 mm: protein 35%) was used;
15.0 0.2 kg of feed per tank was added during the cycle. The feeding supplied during the complete cycle was: 17.9 kg for tank 1,
18.2 kg for tank 2, and 18.3 kg for tank 3. The daily ration was
adjusted according to the strategy described by Casillas-Hernndez
et al. (2006).
The seed tomato plants (L. esculentum Mill) were stocked in
polystyrene seed recipients with 200 cavities utilizing a substrate
of peat-mossperlite. After of 30 days, tomato plants were transferred to pots. A total of 135 plants were transplanted at a density
of 4.9 plants m2 . The separation between plants was 0.30 m and
between the adjacent rows was 1.0 m. Plants were vertically supported by nylon cord guides. The harvest of tomatoes was initiated
when the rst red coloration of the fruit appeared (13 weeks).
For the growth of shrimp samples of 100 shrimp from each tank
were weighed (0.1 g) weekly throughout the cycle. The nal survival and biomass were determined by individually measuring the
weight of the shrimp at harvest. For the plants, these were weighed
at harvest and the fruits were also weighed and counted.
2.2. Sampling and chemical analysis
Weekly water samples were taken directly from the tanks and
the output of pots (from recovery channels); between 12:00 and
13:00 h. Filtered (Whatman GF/F) and unltered water samples
were stored in plastic bottles and transported to the laboratory after
collection. Dissolved oxygen, temperature, salinity and pH were
measured in situ twice a day (6:00 and 18:00 h) with a dissolved
oxygen meter (YSI model 58, USA) and a pH meter. Filtered water
samples were used to determine dissolved nutrients. The nutrient
analyses were performed by procedures outlined in Grasshoff et al.
(1990). The groundwater used in this trial was analyzed in duplicate
for major ions with standard techniques (APHA, 2012). The analysis total-N and total-P in waters, sludge, plants and shrimp were

conducted using procedures from Grasshoff et al. (1990). With the

exception of ammonia, for which the coefcient of variation was
between 9 and 15%, the precision of these determinations was <10%.
2.3. Mass balances and environmental nutrient loads
Field records were used to quantify total amounts of commercial feed and fertilizer added to tanks and individual tank yields.
The volume of water exchange in tanks was estimated from eld
records; evaporation rates were from historical registers mean
monthly rates (CNA, 2008). Tank water uxes were calculated from
water exchanges, evaporation rates and measurements of levels in
tanks. Inputs of nutrients through atmospheric precipitation, rainfall, nitrication and nitrogen xation by blue-green algae were
considered negligible (Briggs and Funge-Smith, 1994; Pez-Osuna
et al., 1997; Jackson et al., 2003; Casillas-Hernndez et al., 2006).
Concentrations of nitrogen and phosphorus were multiplied
by water ows to determine the total mass of each parameter in
irrigation water, return water, and discharged water. Similarly, the
mass ux of each parameter which entered ponds from the groundwater was calculated from the nutrients data of water input. From
the sum of input and output uxes, the equations used for the
mass balances of nitrogen and phosphorus were (Pez-Osuna et al.,
1997):
FCFN + fCfN + ICIN + PLCPLN = HCHN + ZCZN + SCSN + OCON + A

(1)

FCFP + fCfP + ICIP + PLCPLP = HCHP + ZCZP + SCSP + OCOP

(2)

where CF , Cf , CI , CPL , CH , CZ , CS and CO are referred to the content

(at dry weight basis) of P or N in the dry feed pellets (F), fertilizer
(f), input water (I), postlarvae (PL), the shrimp and tomato harvest
(H), zeolite (Z), sludge (S) and output water (O), respectively. The
ux of nitrogen via atmosphere (A) by the processes of volatilization of ammonia and/or denitrication was estimated by difference.
Considering the gross nutrient mass balance, the environmental
losses for phosphorus (LP ) and nitrogen (LN ) were calculated from
the nutrients lost to the environment via the net output water
(discharged at harvest-input water), denitrication, volatilization
and sedimentation. Pruning of plants, and the nutrients associated
to zeolite and organic sludge were included also within losses of
nutrients. The equations used were:
L N = ZCZN + SCSN + OCON ICIN + A

(3)

L P = ZCZP + SCSP + OCOP ICIP + surplus

(4)

3. Results
The composition of groundwater used to ll the tanks and that
resulting after the addition of fertilizers at the rst week was (in
mg L1 ): Cl , 50 and 50; Mg2+ , 5.7 and 24.6; K+ , 7.8 and 11.0; Ca+2 ,
73.0 and 67.5; Na+ , 175 and 170; pH, 7.9 and 9.0; and electrical
conductivity, 1074 and 1285 S cm1 , respectively. The water tank
used for the shrimp culture and for the irrigation of tomato plants
was a mean concentration (mg L1 ) of nutrients along the culture
cycle: phosphate, 0.11 0.16; total ammonia, 0.20 0.15; nitrite,
0.58 0.89; and nitrate, 419 77. Table 1 summarizes the production results for both shrimp and tomato. The discussion on the
production, management and the water quality variables (nutrients
and major components) is presented elsewhere (Mariscal-Lagarda
et al., 2012, 2013).
For the feed CFN supplemented during the rsts 7 weeks, this
was 6.25% N, and the amount F for the tank 1, 2 and 3 was 2.98,
3.04 and 3.0 kg; i.e., 186.2, 190.0 and 187.5 g N, respectively. While
for week 819 (nal of cycle) CFN was 5.76% N, and F was 14.87,

M.M. Mariscal-Lagarda, F. Pez-Osuna / Aquacultural Engineering 58 (2014) 107112

Table 1
Harvest size, yield, factor of conversion (FC) and survival of shrimp and tomato
(mean standard deviation) in the experimental shrimp-tomato culture.
Variable

Shrimp mean SD

Harvest size (g)

Yield (ton ha1 )
FC
Growth rate (g week1 )
Survival (%)

13.9
3.9
1.61
0.73
56.3

0.4
0.2
0.03
0.04
0.9

Tomato fruit mean SD

110.6 22.5
36.1 2.3

100

15.17, and 15.27 kg for the tanks 1, 2 and 3, respectively; i.e., 856.5,
873.8 and 879.6 g N, respectively. From these amounts the nitrogen
input through of food was 1042.7, 1063.8, and 1067.1 g N cycle1
for tank 1, 2 and 3, respectively. From P concentrations of feed
supplemented (1.14% for weeks 17 and 0.94% for weeks 819)
and amounts of feed consumed were obtained 174.7, 177.5, and
177.7 g P cycle1 for tank 1, 2 and 3, respectively. The fertilizer
applied (f) 5 kg tank1 cycle1 was MgNO3 with a nitrogen content
(CfN ) of 11.0%, and a phosphorus content (CfP ) of <0.02%, therefore
the ux of nitrogen for this via was 550 g N tank1 cycle1 , and of
phosphorus <1.0 g P tank1 cycle1 .
The ux of nitrogen and phosphorus associated to lling
water was calculated from concentration of the nutrients in
groundwater (CIN = 15.4 mg N L1 ; CIP = 0.017 mg P L1 ), and the
volume of tanks (31.1 m3 ) which was 478.9 g N tank1 cycle1 and
0.5 g P tank1 cycle1 . Similarly, the ux associated to replacement
of water (by evaporation) was estimated from the volume registered through of cycle (21.8 m3 ) and the concentration of each
nutrient, were 335.7 g N tank1 cycle1 and 0.37 g P tank1 cycle1 .
The ux of nutrients associated to outlet water (discharge) was
calculated considering the volume of each tank (31.1 m3 ) and the
concentration of each nutrient in the last week of culture; 53.4, 50.7
and 52.4 mg N L1 for tank 1, 2 and 3, respectively. From this route
were discharged 1659.9, 1576.7 and 1629.6 g N per cycle for the
tank 1, 2 and 3, respectively. Similarly, for phosphorus were considered the concentrations of the last week of culture; 0.67, 1.47
and 1.16 mg P L1 for tank 1, 2 and 3, respectively. Then the ux of
phosphorus estimated via the discharge of tanks was 18.8, 46.6 and
36.0 g P per cycle for tank 1, 2 and 3, respectively.
The input of nitrogen and phosphorus in the postlarvae was
estimated from their content (CPLN = 11.02% N; CPLP = 0.57% P), the
postlarvae stocked per tank (1414 individuals), their wet (82.0 mg)
and dry weight. For the tank 1, the dry weight of the 1414 postlarvae was 30.3 g and their CPLN 11.02% N, then the nitrogen associated
was of 3.3 g N per cycle. For the tank 2, the dry weight of the 1414
postlarvae stocked was 27.2 g and their CPLN 10.7% N, then the nitrogen input was of 2.9 g N per cycle. For the tank 3, the dry weight
of the 1414 postlarvae stocked was 27.4 g and their CPLN 10.9% N,
then the nitrogen input was 3.0 g N per cycle. Similarly, in the case
of phosphorus, the CPLP for tank 1, 2 and 3 were 0.57, 0.74 and 0.63%
P, which gives 0.18, 0.20 and 0.17 g P per cycle for tank 1, 2 and 3,
respectively.
The nutrients associated to harvest were calculated from the
corresponding concentrations and biomass of shrimp and of tomato
plants. At tank 1, the shrimp harvest was 11.3 kg, equivalent in dry
weight to 2955.3 g and the content of nitrogen (CHN ) and phosphorus (CHP ) was 11.0% and 0.53%, respectively; consequently, the
uxes were 325.1 g N per cycle and 15.7 g P per cycle. Similarly,
in tanks 2 and 3 were made the same calculus obtaining 303.0
and 330.5 g per cycle for nitrogen, and 16.5 and 15.2 g per cycle
for phosphorus, respectively. For the tomato plants were considered the weights (wet and dry) of each fraction (roots, leaves, stem
and fruit) and their nitrogen and phosphorus contents. Roots, stem,
leaves and fruit were a content of 1.63, 1.68, 2.60 and 1.70% of N,
and 0.208, 0.250, 0.217 and 0.302% P, respectively. The mean ux
associated to tomato harvest was nally the result of the sum of

109

each nutrient in each fraction of the plant; 51.7 6.3 g N cycle1

and 7.7 1.5 g P cycle1 .
About the ux of nutrients associated to sludge and zeolite, these
were calculated from the corresponding weights (wet and dry) and
concentrations of the materials. In tank 1, were recollected in the
nal of the cycle 16.3 kg of sludge (water content, 76.9%), which
was 3.7% N and 1.12% P, therefore the uxes were 139.3 g N cycle1
and 42.2 g P cycle1 . In tank 2, were recollected 15.5 kg of sludge
(water content, 70.5%), which was 1.01% N and 1.16% P, then the
uxes were 46.2 g N cycle1 and 53.0 g P cycle1 . In tank 3, were
recollected 13.7 kg of sludge (water content of 76.6%), which was
2.28% N and 1.12% P, then the uxes were 73.1 g N cycle1 and
35.9 g P cycle1 . For the zeolite, the 15 pots were lled with 3.1 kg of
zeolite (humidity 24.1%) each one, i.e., 46.5 kg per tank. The initial
and nal concentration of nitrogen of a replicated of six aliquots
of zeolite was 0.030 0.011% and 0.081 0.010% N, respectively,
i.e., a mean difference of 0.051% for nitrogen, which indicates that
zeolite retained nitrogen; similarly, for phosphorus was estimated
a nal retention of 0.03% P of zeolite. Then the retention estimated of nutrients by zeolite was 22.1 1.2 g N tank1 cycle1 and
15.8 0.6 g P tank1 cycle1 .
Considering each component of the shrimp-tomato culture system was elaborated a synthesis of the uxes and percentages, which
are represented in Fig. 1. Nitrogen input to the shrimp-tomato system was derived primarily from addition of feed (43.6%), followed
by fertilizer (22.7%), lling water (19.7%) and replacement of water
levels (13.8%). Postlarvae represented only a very low proportion
(0.1%). Nitrogen losses occurred primarily through of the water
of discharge during harvest (tank drainage) (77.2%), to the atmosphere (13.4%) and organic sludge (4.1%). Removal of shrimp and
tomato plants at harvest represented a 15.2 and 2.5%, respectively
(Fig. 1). The uncertainty estimated in the sum of inputs and outputs
of nitrogen expressed in percentage was of 5.4%.
Phosphorus input to the shrimp-tomato system was derived
principally from addition of feed (98.8%). Inlet water contributed
with 0.5% (lling water, 0.3% and replacement of water levels, 0.2%)
and postlarvae with 0.1%. Phosphorus outputs from the entire system occurred primarily by accumulation of organic sludge (24.6%)
and the surplus (34.3%). The surplus (61.9 29.4 g P cycle1 ) probably is associated to residues of materials in the walls of the
tanks and implicit errors of the methodology. Therefore, here was
considered that the sum of these two processes was via the accumulation. Removal of shrimp and tomato plants at harvest represented
8.9% and 4.3%, respectively. Water discharge during the harvest
accounted for 19.0% (Fig. 1). The uncertainty global in the sum of
inputs and outputs of phosphorus was estimated in 16.5%.

4. Discussion
Different criteria had been used for report nutrient loads.
According to Jackson et al. (2003) only net discharge should be utilized; that is, any introduction of nutrients in incoming pond water
should be subtracted from the gross discharge quantity. However,
their study does not include emission of nutrients into the atmosphere (denitrication and volatilization of nitrogen compounds)
and deposition via sedimentation; both processes are of environmental concern. Losses of nitrogen to the atmosphere do not affect
directly receiving waters, although they should be included because
they are added to the environment and ultimately contribute to
nonpoint loads into estuaries and coastal waters. From the atmosphere, nitrogen can reach the waters either by direct leaching or
by runoff from drainage basins, or indirectly through the atmosphere (Howarth et al., 2000). On the other hand, the inuence
of sequestered phosphorus and nitrogen could vary signicantly
depending on whether sediments are removed or not during

110

M.M. Mariscal-Lagarda, F. Pez-Osuna / Aquacultural Engineering 58 (2014) 107112

Fig. 1. Nitrogen and phosphorus mass balance in the integrated shrimp-tomato system. Values represent the mean standard deviation in g tank1 cycle1 ; percentages are
respect to total nutrient input to system. Dashed arrows represent routes deduced by difference among inputs and outputs.

post-harvest. In Mexican farms, a common procedure for preparing pond soils before stocking consists of natural drying, raking,
and nally, liming (Lyle-Fritch et al., 2006). Eventually, some farms
remove sediments. The tendency in areas where shrimp farming is
developing is that sediments and their associated materials constitute an environmental concern and should be considered potential
waste (Casillas-Hernndez et al., 2006).
Table 2 was elaborated with three different units for intensive shrimp culture systems. For nitrogen, the environmental
losses from our study were intermediate or higher when the
loads are expressed in kg N ha1 cycle1 , and as net N discharged
only in efuents (kg N ton1 ). But when is expressed as kg N per
ton of shrimp harvested (without tomato fruit) also is higher
than those reported for other intensive shrimp ponds; however, when are considered the two products, shrimp and tomato,
the shrimp-tomato system produced a lower environmental loss
(57 kg N ton1 ). Similarly, for phosphorus, the environmental load
expressed as kg P ha1 cycle1 found in our work, including only
shrimp and shrimp + tomato, were high in comparison to the lower
value reported in the Tailake region, China (Xia et al., 2004). In

the case of environmental losses of phosphorus expressed in kg

P per ton of shrimp harvested or per ton of shrimp + tomato, our
values (14.6 and 7.1 kg P ton1 , respectively) are lower than those
calculated from literature, which the loads varied from 23 to 41 kg
P per ton for intensive shrimp ponds. The case of the net P discharged only through of efuents, our values are among the higher.
Xia et al. (2004) reported in their budgets for the water pumped
83.6 kg N ha1 and 8.48 kg P ha1 , and for the drainage and seepage, 40.1 kg N ha1 and 6.3 kg P ha1 in ponds stocked with 50 L.
vannamei postlarvae per m2 ; these values give a negative net load of
both, nitrogen and phosphorus. However, for the most of nutrients
measures, the net discharges and environmental losses from the
semi-intensive ponds (Pez-Osuna et al., 1997; Casillas-Hernndez
et al., 2006) were lower or closed to the minimum reported for
intensive ponds; which is expected, to higher intensity, greater is
the impact.
The chemical uxes are indispensable to estimate nutrient
budgets and modeling the dynamics of materials in culture systems.
Among the main sources potential of error associated with these
calculations are: (a) the estimates for quantifying the uxes of input

M.M. Mariscal-Lagarda, F. Pez-Osuna / Aquacultural Engineering 58 (2014) 107112

111

Table 2
Environmental losses of nutrients from intensive monoculture shrimp and from the shrimp-tomato culture.
Species

kg N ha1 cycle1

kg N ton1

Net N discharged in
efuents kg N ton1

kg P ha1 cycle1

kg P ton1

Net P discharged in
efuents kg N ton1

Refs.

P. monodon
P. monodon
P. monodon
L. vannamei
L. vannamei
L. vannamei + L. esculentum

327
596
1527
130
457
438

93.4
92
111
76
116
57

72
38
11

73
37

265
425
39
57
55

41
31
23
14.6
7.1

3.4
2.2

8.4
4.3

Jackson et al. (2003)

Briggs and Funge-Smith (1994)
Robertson and Phillips (1995)
Xia et al. (2004)
This study
This study

and output water; (b) seepage in the bottom and losses through
walls of reservoirs; (c) the estimating of evaporation and precipitation rates (dry and humid) of nutrients via atmosphere, runoff and
rainfall; (d) denitrication rates (for nitrogen); (e) volatilization
(for nitrogen); (f) nitrogen xation; and (g) accumulation of material adhered in the walls of the tanks. When calculating nitrogen
mass balances for shrimp reservoirs, denitrication and ammonia volatilization are two losses of nitrogen that are often not
quantied. Consequently, the ux of nitrogen involved in these
processes is estimated indirectly as the difference between the
sum of inputs and outputs (surplus). In our study, 13.4% of nitrogen was deduced as lost via these two processes (dashed arrows
in Fig. 1). Comparable values had been estimated by Martin et al.
(1998) (15%) and Briggs and Funge-Smith (1994) (13%). In contrast,
Jackson et al. (2003) found 3% in their study working densities of
3235 shrimp m2 with Penaeus monodon in NE Australia.
The mean ux of nitrogen exported via denitrication and
volatilization in our work was of 323.9 g cycle1 , taking into
account the variation between the three shrimp tanks, this amount
has an uncertainty (standard deviation) of 130.4 g cycle1 . Considering the high levels of nitrates (by addition of fertilizer), a source
of organic carbon available (from uneaten feed and others components of shrimp tank), and a management of tanks closed to
zero exchange, certain denitrication is expected, though anaerobic conditions are difcult by the continuous aeration in our tanks.
Burford and Longmore (2001) found in intensive shrimp ponds
<2% of available nitrogen denitried. Evidently, some potential
for denitrication did exist in our experimental shrimp tanks. On
other hand, ammonia volatilization is favored by various factors
(Jackson et al., 2003): those that promote the non-ionic ammonia
(NH3 ) side of the water column equilibrium NH4 + -NH3 (dependent of total ammonia concentration, high pH, high temperature
and salinity); and those factors stimulating the effective transfer
across the waterair interface (wind, aeration and temperature).
In our shrimp tanks, these conditions are met, therefore, some of
volatilization of ammonia is present.
Nitrogen xation was not considered in our work. The
levels of ammonia found were relatively low or moderated
(<0.0010.848 mg L1 ) during the culture cycle, and the general group composition of phytoplankton consisted mainly of
Chlorophyta and Bacilliariophyta. Cyanophyta constituted <3%
(Mariscal-Lagarda et al., 2012). From such phytoplankton community and ammonia concentrations, it is expected that the quantity
of nitrogen added by xation should be minimum. Other route
of exportation of nutrients in shrimp reservoirs is through accumulation of organic sludge and other materials in the bottom and
walls; in our work, the fraction of nitrogen and phosphorus associated to sludge was of 4.1% and 58.9%, respectively. Only few
studies have quantied directly this mechanism; Briggs and FungeSmith (1994) found proportions relatively highs, 31% and 84%,
respectively. Therefore, sediment accumulation was likely to be
responsible for a signicant proportion of the phosphorus which
was not accounted for.
Regarding the concentrations of nutrients found in the waters of
the shrimp tanks and the output from the module of tomato plants

(Mariscal-Lagarda et al., 2012), and from the mass balances of both

nitrogen and phosphorus it is evident that for these tanks (31.1 m3 ),
it is necessary to integrate a major number of tomato plants. The
recovery of nutrients as biomass of shrimp and tomato plants was
relatively low; for nitrogen, shrimp 15.2% and tomato plants 2.5%;
for phosphorus, shrimp 8.9% and tomato plants 4.3%. In traditional
shrimp monoculture, with L. vannamei under brackish or marine
conditions, the shrimp harvest biomass represents a 22.735.5%
and 6.114.3% for nitrogen and phosphorus, respectively (PezOsuna et al., 1997; Xia et al., 2004; Casillas-Hernndez et al., 2006).
In intensive shrimp monoculture with P. monodon under brackish
and marine conditions, the shrimp harvest represents 20.422.0%
and 5.76.5% for nitrogen and phosphorus, respectively (Briggs and
Funge-Smith, 1994; Jackson et al., 2003). In the particular case of
nitrogen, our recovery of biomass at harvest are below of the range
found, and for phosphorus, the values are closed of those calculated.
This indicates that the shrimp culture using low salinity groundwater under the conditions here examined was not the optimal in
terms of nutrients recovery; this can be due to a combination of
factors included the low salinities (EC 1505 S cm1 ), the composition of major ions (individual concentration and ratios) and the
relatively high levels of nitrates (Mariscal-Lagarda et al., 2012).
For the scenario studied here, presumably are required 4.9 g N
per plant in each pot (3.4 g N per plant + 1.5 g N per zeolite).
Considering the nitrogen discharged in efuents during harvest
(1622.1 g N tank1 cycle1 ), theoretically there is sufcient nitrogen for the fertilization of 331 plants more instead of 15 only. This
indicates that one tank could be coupled to 346 plants. However, in
the integrated shrimp-tomato culture managed under our conditions, the phosphorus was apparently the limiting nutrient rather
than nitrogen. The mean concentration of dissolved phosphorus
recorded as the fraction available for tomato plants was an average
of 0.11 0.16 mg P L1 in the shrimp tanks (Mariscal-Lagarda et al.,
2012). These levels are low and probably insufcient for the fertilization required either for the outeld soil culture or the soil-less
culture system. In the particular case of our trial (1 tank shrimp
culture: 15 tomato plants) (94 shrimp: 1 plant), the tomato plant
presented the following mean phosphorus content: fruit, 0.302;
stem, 0.250; root, 0.208; and leaf, 0.217% P that was perhaps sufcient for the nutrition of the plant here but probably not optimal.
After of harvest, the discharge of efuents contain sufcient phosphorus (33.8 g P tank1 cycle1 ) theoretically for the fertilization of
22 plants in addition to 15 coupled here, i.e., the system could
sustain 37 tomato plants. It is important to indicate that in the
nal after of harvest, the water of shrimp tanks can be utilized to
continue the tomato culture; or well as have been calculated here
couple more plants.

5. Conclusions
The results of the present study are the rst mass balance of
nutrients in shrimp culture in low-salinity waters integrating
tomato plants. From this mass balance, it is evident that the
amount of N and P generated in the system is sufcient to produce

112

M.M. Mariscal-Lagarda, F. Pez-Osuna / Aquacultural Engineering 58 (2014) 107112

without the use of agrochemical fertilizers a proportion of 94

shrimp: 1 tomato plant. Our results suggest that the shrimp
culture with low-salinity water produces a low percentage of
total nitrogen and phosphorus recovered as harvested shrimp
in comparison to traditional marine systems. Concurrently, this
coupled system produces an amount of tomato fruit that can
compensate the relatively low recovery in shrimp. However, the
main progress with this integrated system is the reduction of
the environmental losses of nitrogen and phosphorus reached to
contribute to minimize the eutrophication of receiving waters.
We have characterized the main attributes of the integrated
shrimp-tomato culture, which can assist future efforts toward
removing most effectively nutrients from shrimp farm efuent.
These results indicate there is a considerable potential to improve
the production and environmental performance of shrimp-tomato
system, in the following points: (a) increasing the proportion of
nitrogen and phosphorus inputs that are harvested as shrimp and
tomato fruit; (b) establish the optimal concentrations and ratios of
major components in the water to cultivate successfully the two
cultures; (c) it is required precise the amount of coupled tomato
plants with number of shrimp; and (d) nd the ideal conditions
for the shrimp-tomato culture consistent with the climate of the
region.
Acknowledgements
Project 26-2006-1031 supported by Fundacin Produce Sonora.
We thank H. Bojrquez-Leyva, C. Ramrez-Juregui and G.
Ramrez-Resndiz for your collaboration in the chemical analysis,
bibliographic services, and statistical support. To hatchery Maricultura del Pacco who provide the postlarvae for the trial. This
research forms part of the Ph.D. dissertation of MMML at Programa
Multidisciplinario de Posgrado, Universidad de Occidente.
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