Regional Studies in Marine Science 48 (2021) 102046

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Assessment of the stock status of two penaeid shrimps in the

Northeastern Brazil Marine Ecoregion and implications for their
management
∗
Matheus Souza Ferreira de Barros a , , Cícero Diogo Lins de Oliveira b ,
Taciana Kramer Pinto c , Igor da Mata-Oliveira d , Nidia Noemi Fabré a ,
Vandick da Silva Batista b
a
Laboratório de Ecologia, Peixes e Pesca (LaEPP) da Universidade Federal de Alagoas, Instituto de Ciências Biológicas e da Saúde, Brazil
b
Laboratório de Conservação e Manejo de Recursos Naturais Renováveis (LACOM) da Universidade Federal de Alagoas, Instituto de Ciências
Biológicas e da Saúde, Brazil
c
Laboratório de Ecologia Bentônica (LEB), Universidade Federal de Alagoas, Unidade Penedo, Brazil
d
Laboratório de Investigação e Manejo da Pesca (IMAP), Universidade Federal de Alagoas, Unidade Penedo, Brazil

article info a b s t r a c t

Article history: Shrimp fisheries is one of the most profitable fishery activities in tropical regions, highlighting the
Received 28 July 2021 need of assessing the status of those resources more thoroughly. Then, this study aimed to provide
Received in revised form 15 September 2021 a comprehensible stock assessment of two highly exploited marine penaeid shrimps (Xiphopenaeus
Accepted 5 October 2021
kroyeri and Penaeus schmitti) in two important fishing grounds within the Northeastern Brazilian Ma-
Available online 12 October 2021
rine Ecoregion (NBME) in the state of Alagoas. In addition, the hypothesis of different stocks between
Keywords: areas is also tested by checking for possible between-area heterogeneity in population parameters.
Xiphopenaeus kroyeri We found remarkably similar patterns of growth and mortality between the two fishing grounds for
Penaeus schmitti both species, with homogeneous parameters indicating an absence of regional structuration. Then,
Trawling the two fishing grounds contain a single stock for both species, which will respond similarly to the
Prawn
same fishing pressures and management scenarios. We also indicate that the seabob shrimp is close
Growth
to the limit of full exploitation in both regions based on Yield per Recruit analysis. Meanwhile, the
Mortality
white shrimp is overexploited in one of them. Potential management tools to allow sustainable and
productive exploitation in these fisheries are effort control and spatial restrictions to conserve nursery
habitats and maintain sustainable rates of population growth.
© 2021 Elsevier B.V. All rights reserved.

1. Introduction
Exploitable wild shrimps are one of the most internationally
important fishing resources, with roughly 3.4 million tons being
caught every year and accounting for about 18 percent of the
total value of fisheries worldwide. This resource is also socially
vital, being source of subsistence and jobs. Indeed, tropical shrimp
fisheries are one of the most worldwide growing activities in
tropical regions, where they are mainly performed by artisanal
fleets (FAO, 2017; Gillett, 2008). Brazil is one of the greatest
shrimp harvesters, catching an average of more than 30 thousand
tons annually since the late 90s (FAO, 2019; Lopes, 2008; Teixeira
et al., 2020).
Tropical marine shrimp fisheries are mainly targeted to catch
penaeid shrimps (Garcia, 1988). In fact, the fisheries in the tropics
∗ Corresponding author.
E-mail address: matheus.barrosteu@gmail.com (M.S.F. de Barros).
have the Atlantic seabob shrimp Xiphopenaeus kroyeri and the
white shrimp Penaeus schmittii as one of the main target species
(Santos, 2010a). The seabob shrimp is distributed in the Western
Atlantic from the south-eastern USA to southern Brazil, inhabiting
soft mud bottom substrates in shallow waters of up to 25 ∼ 30 m
of depth (Brazil Rogerio Costa et al., 2007). It is one of the top ten
most caught penaeid species concerning biomass worldwide and
the first in Brazil (MPA, 2013). The white shrimp is distributed in
the Western Atlantic from Cuba to southern Brazil (Ferrari, 1999)
in soft bottoms of up to 50 m deep (Bochini et al., 2014) and
was recorded as the fourth most caught species in the Brazilian
last published fisheries statistics (MPA, 2013). The remarkable
densities and considerable populations presented by both species
in easily accessible waters are the main factors increasing their
catchability (de Carvalho et al., 2016; Silva et al., 2013).
The two species present remarkably different life cycles due
to physiological processes linked to saline regulation. The seabob
shrimp presents a type 3 life cycle, characterized by preferring

https://doi.org/10.1016/j.rsma.2021.102046
2352-4855/© 2021 Elsevier B.V. All rights reserved.
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al.
high salinities and thus being fully marine, spawning, recruiting
and growing at sea. Inversely, the white shrimp presents a type
2 life cycle: it spawns at sea, but their larvae are taken to es-
tuaries by local currents and diel vertical migration processes,
where they develop before coming back to the sea as subadults
(Dall et al., 1990). This allows the white shrimp to be classified
as estuarine-dependent (Gamba and Rodríguez, 1987; Kutkuhn,
1966).
The high commercial, social and ecological significance of
these species points out the necessity of adequately assessing
their stock status towards designing more effective management
strategies that can cope with the intense harvest along the Brazil-
ian coast (Lopes, 2008). In fact, studies determined that some
stocks of these shrimps are above or near the full exploitation
level (de Carvalho et al., 2021; Lopes et al., 2014; Miazaki et al.,
2021; Silva et al., 2019). Additionally, the white shrimp can be
considered data-deficient in Brazil, considering that it is exploited
virtually along all its coast, but few stock assessments report data
on the current level of exploitation (de Carvalho et al., 2021; Silva
et al., 2019). Facing this facts, these species were placed under
the insufficient data (I.D.) category in the Red Book of Brazilian
Crustaceans (Boos et al., 2010).
Short-lived species such as shrimps tend to exhibit a remark-
able dependence upon environmental variability in their pop-
ulation dynamics, with many regional patterns of population
structure being explained by environmental heterogeneity rather
than biogeographical or intrinsic genetic factors (Miazaki et al.,
2021). Numerous research established that abiotic variables such
as salinity, precipitation, temperature, currents and local hydrog-
raphy are capable of modifying populational parameters such
as recruitment/reproduction and growth or mortality patterns of
marine shrimps on a regional scale (Heras et al., 2019; Jónsdóttir
et al., 2013; Lopes et al., 2017; Milton et al., 2016; Wieland, 2005).
Indeed, determining if a population of an exploited resource
comprises small subunits is particularly important to fisheries
management, as these metapopulations (stocks) may exhibit dif-
ferent parameters and therefore different levels of sustainably
exploitable biomass, which may mean that local patterns of fish-
ing pressure will be able to determine the species ability to thrive
even in face of harvesting (Fogarty and Botsford, 2006). For that,
life history parameters such as growth, mortality and morphome-
tric relationships have been extensively used and were proven to
be reliable, given that they are mainly subject to environmental
control within a species (Begg et al., 1999; Du Pontavice et al.,
2018; McBride, 2013; Tzeng, 2004).
Additionally, using the appropriate methods to improve pa-
rameter estimation of data-poor resources is crucial towards
avoiding wrong interpretations and consequent misleading man-
agement recommendations. Length-frequency data analysis
(LFDA) is mandatory to species without durable hard structures
(King, 2013; Punt et al., 2013), facilitating data collection in
developing countries, where laboratory and financial conditions
are usually reduced and the vast majority of stocks are not being
fully monitored (Costello et al., 2012). Recently, a significant
emergence of new algorithms based on the response surface
analysis (RSA) allows refined estimation of parameters along with
estimates of variance, becoming exceptionally reliable to short-
lived species such as most crustaceans (Schwamborn et al., 2019;
Taylor and Mildenberger, 2017).
The Northeastern Brazil Marine Ecoregion (NBME) (Spalding
et al., 2007) harbors a narrow continental shelf, where warm and
nutrient-poor waters from the North Equatorial current flows.
Even so, the coastal ecosystems in Northeast Brazil are produc-
tive systems, mainly due to the intense nutrient input from the
estuaries and reef formations (Knoppers et al., 1999; Passos et al.,
2016). Therefore, it supports various fishing activities, including
2
Regional Studies in Marine Science 48 (2021) 102046
shrimp trawling in soft-bottom substrates, allowing harvesting
tens of thousands of tons annually (Costa and dos Santos, 2016).
Two of the most important Brazilian shrimp fishing grounds
are located southward of the NBME, with distinct environmental
conditions due to coastal profile. The Pontal do Peba fishing
ground is associated with the São Francisco River estuary, the
second-largest river in Brazil (Knoppers et al., 2005) and the
Jaraguá fishing ground is associated with the Mundaú-Manguaba
estuarine complex (one of the most extensive Brazil’s lagoon sys-
tems). Both coastal areas are highly influenced by seasonal pre-
cipitation patterns that affect the variations in discharge
(Da De Cunha et al., 2021; Lessa et al., 2018; Oliveira and Kjerfve,
1993). Even though, the São Francisco River Estuary is a particular
case, as a dam constructed decades ago highly affects the patterns
of nutrient-rich freshwater discharge and modifies the charac-
teristic seasonality of the estuarine plume extension, as well as
spatial patterns in water salinity (Cavalcante et al., 2020)
Based on the current information regarding the study areas,
we intended to address the following questions: are the stocks
of the seabob and white shrimps comprised of different sub-
populational units? How is that relevant to the local management
strategies, and what should be changed or improved? For that, we
used advanced traditional stock assessment methods to calculate
populational parameters such as growth, mortality and longevity
and compared them between the two areas. Our hypothesis of
the existence of different stocks for both species was based on
the fact that the two regions possess different environmental
characteristics driven by their main estuaries, mainly because of
the modified dynamics imposed by the dam construction and
consequently limited discharge in the São Francisco River Estu-
ary. Here, we utilize the definition of a stock by Cadrin et al.
(2013), in which a populational unit with homogeneous vital
rates within a certain area may be considered a stock for manage-
ment purposes, considering that between-area heterogeneity in
populational parameters urges different management measures
because of potentially diverging responses to fishing pressure.
Also, considering the urgent need for more comprehensible stock
assessments of marine shrimps due to the lack of data in many
fishing grounds (Boos et al., 2010), we addressed the current level
of exploitation and the amount of fishing mortality that may be
implied to maximize both sustainability and yield for both species
in the two fishing grounds, which may subsidize local policies.
2. Material and methods
2.1. Sampling and fishing grounds
Sampling was executed monthly (from May/19 to April/20)
by one-hour trawls using double rig trawling nets around 12 m
width and 14–20 mm bag mesh size, operated with a motorized
winch in an 8–12 m long boat with MWM diesel engines from 3
to 4 cylinders. Traditional fishing grounds in the Pontal do Peba
and Jaraguá were sampled (Fig. 1) in depths from 10 to 30 m.
The Pontal do Peba fishing ground (10◦ 23′ 51.0′′ S 36◦ 16′ 51.4′′ W)
is mainly influenced by the dynamics of the São Francisco River
estuary, with a drainage area of roughly 64 000 km2 and sediment
plumes extending up to 10 km from the shoreline (Knoppers
et al., 2005, 1999). On the other hand, the Jaraguá fishing ground
(9◦ 43′ 29.6′′ S 35◦ 46′ 05.3′′ W) is heavily influenced by the Mundaú-
Manguaba Estuarine System, which is of Northeastern Brazil’s
largest lagoon complexes and bears two lagoons with more than
23 000 km2 and sediment plumes that can reach up to 12 km
in the shallow waters of the continental shelf (Melo-Magalhães
et al., 2009). The fleet is artisanal with low to medium technolog-
ical improvements (sensu Batista et al., 2014), target mainly the
seabob shrimp Xiphopenaeus kroyeri, the white shrimp Penaeus
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al. Regional Studies in Marine Science 48 (2021) 102046

Fig. 1. Fishing areas within the study two fishing grounds.

Table 1 issues and consequent low reliability of approaches based on the

Length–weight relationships for both sexes of the seabob and white shrimps in Powel–Wetheral method to estimate the asymptotic length, we
the two fishing grounds. TL stands for total length and W for weight.
chose not to estimate it previously. After that, we executed a re-
Seabob shrimp
fined ELEFAN (Electronic Length Frequency Analysis) version that
Sex Region Equation Allometry uses a simulated annealing optimization algorithm with boot-
2.66
M Peba TL = 0.29*W (−) strapping (ELEFAN_SA_boot function of the ‘‘fishboot’’ package)
F Peba TL = 0.013*W3.3 (+) (Schwamborn et al., 2018). It searches for von Bertalanffy Growth
M Jaraguá TL = 0.29*W2.71 (−)
Function (VBGF) parameters such as K, L∞ and t_anchor and
F Jaraguá TL = 0.045*W3.16 (+)
its respective confidence intervals by finding a local maximum
White shrimp
(i.e., the growth curve that best performs with the given LFD)
M Peba TL = 0.363W2.19 (−) within a range of input parameters (Schwamborn et al., 2019;
F Peba TL = 0.146*W2.89 (−)
Taylor and Mildenberger, 2017). We used a moving average (MA)
M Jaraguá TL = 0.53*W2.62 (−)
F Jaraguá TL = 0.124*W2.9 (−) of 5 for the restructured LFD because it is more appropriate for
the low bin resolution relative to the asymptotic length, follow-
ing the general rule of thumb as recommended by Taylor and
Mildenberger (2017). Additionally, we also verified that setting
schmitti and the pink shrimp Farfantepenaeus subtilis (Santos et al., MA = 5 maximizes the relative fit value in prior testing. The
2016; Santos, 2010a). input parameters were based on biologically reasonable estimates
In the laboratory, the shrimps were identified according to sex (Minte-Vera et al., 2017), always using the same search space,
by verifying the petasma and thelycum in males and females, re- regardless of sex (K = 1 to 3, t_anchor = 0 to 1, L∞ = 100 to
spectively, according to Fransozo et al. (2011) and Pérez-Farfante 140 mm for the seabob shrimp and L∞ = 180 to 230 mm for the
(1998). We measured total length (TL) in mm, defined from the white shrimp). We resampled data 500 times with 500 maximum
tip of the telson to the end of the postorbital margin of the iterations following a reliable approach for data-limited fisheries
carapace, and wet weight (WW) in grams. assessment of short-lived species and depleted populations that
exhibit changes in size structure (Wang et al., 2021).
2.2. Data analysis The length at first capture (average length at which an indi-
vidual has a 50% probability of being captured) was calculated
Monthly length-frequency data (LFD) with a bin size of 4 by determining the cumulative frequency of each size class with
and 6 for the seabob and white shrimp, respectively, using the 2 mm intervals in the total TL LFD, assuming a knife-edge se-
rule of thumb approach to reach an approximately optimal value lection model. Next, the data were fitted to a logistic model
as recommended by Wang et al. (2020), were analyzed using determined by the following formula:
the R package ‘‘TropFishR’’ (Mildenberger et al., 2017). As rec- 1
ommended by Schwamborn (2018), because of autocorrelation P =
1 + exp (− (a + b ∗ TL))
3
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al. Regional Studies in Marine Science 48 (2021) 102046

Table 2
Parameters of the seabob shrimp with 95% CIs for both fishing grounds.
Pontal do Peba Landing Port
Males Females Pooled sexes
Max dens Upper limit Lower limit Max dens Upper limit Lower limit Max dens Upper limit Lower limit
K 1.57 2.15 1.36 1.3 1.79 0.93 1.39 1.62 1.06
L∞ 110.59 117.54 110.06 123.24 136.19 119.18 117.45 128.21 114.75
tmax 1.91 1.39 2.20 2.34 1.67 3.22 2.13 1.82 2.79
Z 5.49 7.50 4.76 3.92 8.6 2.50 4.21 4.95 3.16
M 2.74 3.63 2.4 2.22 3.06 1.68 2.45 2.88 1.91
F 2.75 3.86 2.35 1.70 5.54 0.82 1.81 1.38 2.35
E 0.50 0.52 0.49 0.43 0.64 0.33 0.43 0.32 0.55
Lc 80.5 – – 89.78 – – – – –
Jaraguá Landing Port
Males Females Pooled sexes
Max dens Upper limit Lower limit Max dens Upper limit Lower limit Max dens Upper limit Lower limit
K 1.58 1.98 1.42 1.28 1.68 1.06 1.4 1.65 1.05
L∞ 115.28 118.07 110.89 121.41 134.8 117.82 118.12 129.3 115.38
tmax 1.90 1.51 2.11 2.34 1.78 2.83 2.12 1.8 2.82
Z 5.72 7.84 4.90 4.23 8.87 2.74 4.13 5.41 3.44
M 2.75 3.37 2.5 2.28 2.91 1.92 2.47 2.88 2.87
F 2.96 4.46 2.40 1.95 5.96 0.81 1.66 2.53 1.25
E 0.52 0.57 0.49 0.46 0.67 0.30 0.4 0.47 0.3
Lc 81.33 – – 90.14 – – – – –

Table 3
Parameters of the white shrimp with 95% CIs for both fishing grounds.
Pontal do Peba Landing Port
Males Females Pooled sexes
Max dens Upper limit Lower limit Max dens Upper limit Lower limit Max dens Upper limit Lower limit
K 1.16 2.1 0.92 1.05 1.85 0.93 1.08 1.78 0.9
L∞ 168.03 178.43 158.16 192.47 215.04 186.99 193.42 217.12 185.33
tmax 2.58 1.54 3.26 2.72 1.62 3.22 2.77 1.68 3.33
Z 6.86 14.35 3.76 4.64 15.24 5.07 5.93 14.44 5.17
M 2.08 3.31 1.69 1.99 3.17 1.71 1.92 3.04 1.63
F 4.77 11.04 2.06 2.65 12.06 3.36 4.01 12.52 3.54
E 0.70 0.77 0.55 0.57 0.79 0.66 0.68 0.87 0.69
Lc 134.3 – – 149.5 – – – – –
Jaraguá Landing Port
Males Females Pooled sexes
Max dens Upper limit Lower limit Max dens Upper limit Lower limit Max dens Upper limit Lower limit
K 1.3 1.95 0.9 1.08 1.94 0.9 1.12 1.81 0.93
L∞ 162.65 190.32 157.7 194.37 212.62 187.18 194.35 215.8 186.2
tmax 2.3 1.6 3.26 2.77 1.54 3.33 2.67 1.66 3.22
Z 5.98 17.37 3.3 4.32 17.4 3.27 4.86 13.2 3.29
M 2.31 3.2 1.69 1.95 3.31 1.66 1.99 3.09 1.68
F 3.67 14.16 1.6 2.36 14.09 1.62 2.87 10.11 1.61
E 0.61 0.82 0.49 0.55 0.81 0.49 0.59 0.77 0.49
Lc 135.7 – – 148.80 – – – – –

where P is the proportion of individuals retained by each size
class and a and b are constants given by the model output. Then,
we obtained the constants by fitting a linear regression to the
logged P as explanatory variable and TL as a response variable
and calculated Lc by the ratio between -a and b (King, 2007).
Nextly, we utilized the Beverton and Holt empirical approach
to estimate the instantaneous rate of total mortality (Z ), defined
by the following formula:
( )
K L∞ − L′
Z =
L′ − Lc
In which K is the growth rate, L∞ is the previously obtained
asymptotic length, L′ is the mean of all lengths equal to or greater
than Lc, and Lc is the length at first capture corresponding to
the highest mode in the total length frequency distribution (Then
et al., 2015a,b).
Finally, the instantaneous rate of natural mortality (M) was
calculated by the adaptation of Hoenig’s empirical formula
(Hoenig, 2013) by Then et al. (2015a,b), defined by M = 4.899
4
(tmax−0.916 ), where tmax is the longevity or maximum age es-
timated by the inverse von Bertalanffy growth equation. Then,
the fishing mortality (F ) was estimated by subtracting M from Z,
while the exploitation rate was calculated by the ratio between F
and Z. Values of E > 0.5 were considered to denote overfishing.
All procedures were repeated for each species, both sexes and
fishing grounds. Additionally, we calculated CIs for mortality and
longevity parameters utilizing the lower and upper bounds of
the bootstrapped VBGF parameters to address the uncertainty
commonly associated with data-poor stocks.
To compare VBGF parameters between the two fishing
grounds and test the hypothesis of populational geographical
structuring, we conducted a permutational multivariate analysis
of variance (PERMANOVA) because the data did not fit multi-
dimensional normality assumptions using the output from the
bootstrapping ELEFAN method, which includes measures of vari-
ability for K, L∞ and t_anchor. We previously verified if the
data meets the assumption of multivariate homogeneity of group
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al.
Fig. 2. Length-frequency distributions for males and females of X. kroyeri (left) and P. schmitti (right). The dashed line represents the length at which 50% of the
shrimps are retained by the net (Lc ).
dispersions utilizing the ‘‘betadisper’’ function in the ‘‘vegan’’ R
package.
Finally, we utilized the relative yield per recruit (YPR) model
from Beverton and Holt (1993) to determine fishing mortality
at specific reference levels: the highest biomass per recruit or
maximum exploitable biomass (Fmax), the level of exploitation
that reduces the population at 50% of its exploitable biomass
(F0.5 ) and the fishing mortality at 10% of the slope in the origin
of the YPR curve (Fmsy). In addition, we obtained parameters of
the length–weight relationship (slope and intercept) by the least-
squares method. Parameters from pooled sexes were utilized for
running the YPR analysis. All data were analyzed in the R software
version 4.0.5.
3. Results
Both species had similar size structure in both regions. Males
of the seabob shrimp showed mean total lengths of 83.59 (±10.5)
in the Jaraguá Landing Port, and 82.13 (±9.44) mm in the Pontal
do Peba Landing Port, while females had total lengths of 89.47
(±12.54) and 88.86 (±14.5) mm in the Jaraguá and Pontal do
Peba regions, respectively. Males of the white shrimp had mean
TL of 130.34 (±10.19) in Pontal do Peba and 135.71 in Jaraguá,
while females had 149.15 (±20.67) and 147.62 (±16.7) in the
Jaraguá and Pontal do Peba, respectively. No differences in mean
lengths were detected between regions for both species and
sexes (t-test, p = 0.64), but females were always larger than
males (t-test, p = 0.03). The mean length at first capture (Lc)
was practically the same for both regions. Males of the seabob
shrimp had an Lc of 83.5 and females of 90.3, while the white
shrimp exhibited Lc values of 129.7 and 147.8, respectively for
males and females (Fig. 2). The length–weight relationships were
remarkably similar between regions (p = 0.31), but again showed
differences between sexes in both regions (p = 0.008) (Table 1).
The refined ELEFAN with simulated annealing routine detected
remarkably similar values of VBGF parameters between the two
regions in both sexes and species. More specifically, the values of
5
Regional Studies in Marine Science 48 (2021) 102046
asymptotic length, growth rates, natural/total mortality and ex-
ploitation rate in the Jaraguá fishing ground were slightly greater
for the seabob shrimp, while the same parameters were slightly
higher in the Pontal do Peba fishing ground for the white shrimp.
Values of the exploitation rate for the seabob shrimp were very
close to the limit of 50% in both regions. Even though, we detected
more alarming exploitation rates for the white shrimp in the
Pontal do Peba fishing ground, while in Jaraguá they always ex-
hibited smaller values, although above the limit of 50%. Values of
growth and mortality were consistently higher in males, whereas
the females appear to grow slower and attain higher sizes and
maximum ages (Tables 1 and 2, Figs. 3 and 4).
Cohorts with considerably similar patterns of modal class pro-
gression were detected for both species, with only males of the
seabob shrimp exhibiting three cohorts only and the remaining
exhibiting four. Females of the seabob shrimp exhibited the high-
est modal peaks (> 115 mm TL) in December and January in
both regions. Similarly, females of the white shrimp exhibited
the highest modes (> 195 mm TL) at the end of the year also
for both regions (Figs. 4 and 5). Differences were not found
in the growth curves between regions for both species using
PERMANOVA, except for the white shrimp males. Nonetheless,
differences between the sexes were found for both species in both
regions (Table 4).
The YPR analysis returned similar reference yield values for
both species, with the current values of fishing mortality being
higher than F0.5 but smaller than the maximum sustainable yield
(FMSY ) (Table 4). For the seabob shrimp, the data suggest that
increases in the fishing effort and, therefore, fishing mortality
may only lead to minor gains in yield, regardless of the length
at first capture, while some decrease may be necessary to reach
an optimum value. It also suggests that the white shrimp is very
close to the limit of maximum sustainable yield in Jaraguá and
significantly above the Peba region, allowing us to consider this
shrimp to be overexploited (Fig. 5) (see Table 5).
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al. Regional Studies in Marine Science 48 (2021) 102046

Fig. 3. Restructured length-frequency distributions and growth curves for males and females of the seabob shrimp on the Peba (a) and Jaraguá (b) fishing grounds.

Fig. 4. Restructured length-frequency distributions and growth curves for males and females of the white shrimp on the Peba (a) and Jaraguá (b) fishing grounds.

4. Discussion Despite the apparent environmental heterogeneity imposed

The results presented herein are the first in the studied regions
to present a comprehensive stock assessment of two highly ex-
ploited shrimp species. Our study indicated that the two fishing
grounds contain a single and reasonably homogeneous stock,
with remarkably similar parameters and significant implications
for future management measures. In addition, we found that
the seabob shrimp in the two regions is close to the maximum
recommended limit, with E values very close to 0.5. The white
shrimp appears to be similarly fully exploited in the Jaraguá
fishing grounds but is significantly overexploited in the Pontal do
Peba fishing ground.
6
by the estuaries, it can be considered that the two fishing grounds
harbor a single populational unit for both species, with highly
similar population dynamics such as the patterns of growth and
mortality. The answer for why this happens may lie in decapod
larval ecology, genetics and the reasonably homogeneous soft
bottoms between the two studied fishing grounds (Cristóvão,
2019; Manso et al., 1997). Firstly, larval drifting either by passive
or active processes is the main dispersal mechanism in crus-
taceans and may play a vital role in the genetic interchange
between populational units (Fogarty and Botsford, 2006). In this
specific case, it seems that the proximity between the two fishing
grounds allows a mutual homogenizing larvae interchange.
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al. Regional Studies in Marine Science 48 (2021) 102046

Fig. 5. Relative yield per recruit curves for the seabob (a) and white shrimp (b), with three different values of Lc.

Table 4 but are very similar to others (Table 6). More specifically, the
Probability values for the pairwise comparisons of VBGF parameters between values obtained here for the seabob shrimp are considerably close
fishing grounds and sexes for both species.
to other studies in the NBME such as Lopes et al. (2014) and Reis
Seabob shrimp
et al. (2019) and below the values obtained in southern Brazil
Pairwise M Jaraguá F Jaraguá F Peba M Peba (Grabowski et al., 2014; Heckler et al., 2013a,b). Similarly, the
M Jaraguá – <0.0001 <0.0001 >0.05 same pattern was also found for the white shrimp (de Carvalho
F Jaraguá <0.0001 – >0.05 <0.0001 et al., 2021; Miazaki et al., 2018; Silva et al., 2019). Against
F Peba <0.0001 >0.05 – <0.0001
M Peba >0.05 <0.0001 <0.0001 – the ‘‘latitudinal paradigm’’, which states that shrimps tend to
grow faster, live less and attain smaller maximum sizes in lower
White shrimp
latitudes mainly due to the warmer climates (Bauer, 1992), we
Pairwise F Jaraguá F Peba M Jaraguá M Peba
must highlight the increasing body of evidence suggesting that
F Jaraguá – >0.05 <0.001 <0.05 the influence of environmental variability in a regional scale
F Peba >0.05 – >0.05 <0.05
M Jaraguá <0.01 <0.05 – <0.05 may strongly influence population parameters in penaeid shrimps
M Peba <0.05 <0.05 <0.05 – (Heckler et al., 2014; Lopes et al., 2017; Pérez-Castañeda and
Defeo, 2005; Zink et al., 2017), which considerably distorts the
proposed relationship proposed by the paradigm and reinforces
Table 5
the increasing importance of considering environmental factors
Values for the Economic (E0.1 ), optimum (E0.5 ) and maximum (EMSY ) yields for
the two studied species. Values refer to currents Lcs and both fishing areas. The that are key to penaeid life cycle when analyzing population
reader is referred to the Materials and Methods section for the definitions of structures. In fact, Miazaki et al. (2021), which studied growth
each yield reference values. dynamics of the seabob shrimp in several regions of southeast-
Seabob shrimp White shrimp ern Brazil, instead of finding a consistent latitudinal gradient,
E0.1 0.35 0.30 observed that the population parameters are in accordance with
E0.5 0.44 0.38 the patterns of environmental variation.
EMSY 0.63 0.62
The discrepancy of VBGF parameters between sexes in both
species is a common feature of penaeid shrimps due to specific
evolutionary pressures that selected characteristics that maxi-
Moreover, movements patterns may also exert some influence. mized individual and reproductive fitness. Males usually tend to
More specifically, as the shrimps reach late life stages, they be- grow faster, achieve smaller maximum lengths/ages and there-
come substantially more mobile, which may result in individuals fore exhibit higher values of natural mortality than females. This
from relatively distant regions having higher probability of ex- is a result of larger females having a significantly higher fecun-
changing genes (Fogarty and Botsford, 2006). This is also possible dity and afterward being positively selected, while males with
because in most areas of the continental shelf between the two faster growth being more reproductively successful because they
fishing grounds, the depths where the shrimps are usually caught mature faster (Dall et al., 1990; Hartnoll, 2001). Indeed, most
are composed of suitable habitats for shrimps such as mud, fine or studies detected this same pattern of sexual dimorphism in both
coarse sand (Manso et al., 1997). Then, the apparent differences seabob (Branco, 2005; Da Silva et al., 2019; Grabowski et al.,
between the two regions in the seasonal estuarine runoff imposed 2014; Heckler et al., 2013a,b; Miazaki et al., 2021) and white
by the flow control in the São Francisco River Estuary may not be shrimp (Miazaki et al., 2018), although some also detected higher
enough to cause modifications in specific relevant parameters to growth coefficient and asymptotic lengths for females of the
management such as growth and mortality patterns. Therefore, white shrimp (de Carvalho et al., 2021; Silva et al., 2019). Never-
it is clear that the two areas appear to contain a single and theless, the different parameters and mean sizes between sexes,
homogeneous stock of both species of shrimp, to which the same and spatial segregation (Capparelli et al., 2012; Castrejón et al.,
set of rules such as effort control and closed seasons may apply. 2005; Cezar et al., 2016), imply different mean lengths at first
The VBGF parameters for both species in this study presented capture for both species. Consequently, due to the small mesh size
marked differences from those obtained in some other studies, in the fisheries studied here, males appeared to be proportionally
7
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al. Regional Studies in Marine Science 48 (2021) 102046

Table 6
Population parameters for both species in diverse locations. Note that SC = Santa Catarina, SP = São Paulo, PE = Pernambuco, RJ = Rio de Janeiro, SE = Sergipe.
Note that some studies utilized carapace length (CL) and others utilized total length (TL).
Species Sex Size range k (yr−1 ) L∞ (mm) Method Area Study
M 8–27 3.14 27.73 (CL) PEAKFIT + Solver (excel) SC Grabowski et al. (2014)
F 8–31 2.56 31.41 (CL) PEAKFIT + Solver (excel) SC Grabowski et al. (2014)
M 3–26 3.28 26.38 (CL) PEAKFIT + Solver (excel) SP Heckler et al. (2013a,b)
F 6–31 2.19 30.54 (CL) PEAKFIT + Solver (excel) SP Heckler et al. (2013a,b)
M 25–134 1.93 134.4 (TL) PEAKFIT + Solver (excel) RJ Jardim et al. (2011)
F 33–146 1.65 148.8 (TL) PEAKFIT + Solver (excel) RJ Jardim et al. (2011)
Seabob shrimp
M 40–110 1.25 115 (TL) ELEFAN I (FISAT II) PE Lopes et al. (2017)
F 45–135 1.5 141.8 (TL) ELEFAN I (FISAT II) PE Lopes et al. (2017)
M 7.3–25.1 1.7 31 (CL) ELEFAN in R SE Reis et al. (2019)
F 5.9–30.2 1.5 33 (CL) ELEFAN in R SE Reis et al. (2019)
M 40–110 1.52 110.5 (TL) Length-at-age (FISAT II) PE Lopes et al. (2014)
F 45–135 1.99 147.9 (TL) Length-at-age (FISAT II) PE Lopes et al. (2014)
M 4.4–53 2.19 43.23 (CL) PEAKFIT + Solver (excel) SP Miazaki et al. (2018)
F 4.1–52 1.82 53.1 (CL) PEAKFIT + Solver (excel) SP Miazaki et al. (2018)
M 11.4–37.9 1.86 46 (CL) PEAKFIT + Solver (excel) RJ de Carvalho et al. (2021)
F 9.4–53.5 1.99 54 (CL) PEAKFIT + Solver (excel) RJ de Carvalho et al. (2021)
M 15.8–33.1 2.4 32.5 (CL) PEAKFIT + Solver (excel) SE Santos et al. (2020)
White shrimp
F 11.4–39.3 2.01 38.8 (CL) PEAKFIT + Solver (excel) SE Silva et al. (2018)
M 17–42 1 43.0 (CL) ELEFAN I (FISAT II) PE Silva et al. (2018)
F 18–49 1.2 51.6 (CL) ELEFAN I (FISAT II) PE Silva et al. (2018)
M 17–42 1.02 42.5 (CL) Length-at-age (FISAT II) PE Silva et al. (2018)
F 18–49 1.26 50.0 (CL) Length-at-age (FISAT II) PE Silva et al. (2018)

more caught because they presented higher exploitation rates
and fishing mortality values (Tables 1 and 2). Still, the length at
first capture found in this study is larger than others found for
the seabob shrimp (Lopes et al., 2014).
The fishing mortality (F ) found for the two species in both
fishing grounds was found to be close to the estimated 0.5 thresh-
old of maximum exploitation rate (Tables 2–4), except for the
white shrimp in the Pontal do Peba fishing ground. Indeed, this
species in that region appears to be significantly overexploited,
with reduced abundance of larger individuals (Figs. 2 and 4).
Furthermore, this species seems to be more vulnerable to such
high fishing pressure because of the slower growth rates, as
well as the higher time needed to reach the spawning age when
comparing to the seabob shrimp (Peixoto et al., 2018).
The E values for the seabob shrimp are close to the recom-
mended limit of 50%, while the same parameter for white shrimp
indicates overexploitation on the Peba stock and practically full
exploitation in Jaraguá. In fact, the Peba fishing fleet, where both
stocks exhibit higher values of fishing mortality, is responsible
for most of the shrimp yield in the state (Santos and Freitas,
2006), mainly due to the higher fleet horsepower and increased
fishing effort (Santos and Freitas, 2006). Nonetheless, the YPR
analysis suggests that decreases in the exploitation rate to E =
0.44 and 0.38 for the seabob and white shrimp, respectively,
will result in optimized yields. However, YPR curves for species
with high mortality and short life spans should be assessed with
caution. Generally, the output produces curves that suggests that
fishing mortality should be dramatically increased to reach the
maximum yield, which may be misleading because such high
exploitation rates may substantially reduce the spawning biomass
and cause recruitment overfishing.
It is essential to recognize the limitations of our study, the in-
trinsic uncertainty related to data-limited fisheries and the inher-
ent stochasticity due to environmental variability (Ae and Wolff,
2007). More specifically, our analyzes yielded substantially high
CIs for the VBGF parameters of both species, which also lead to
considerably large CIs for the other parameters such as mortality
rates and longevity (Tables 2 and 3). Indeed, values of total mor-
tality (Z) are strongly correlated to values of K and L∞, as well
as natural mortality (M) and maximum ages (Schwamborn et al.,
2021). Such high uncertainty is commonly associated with ‘‘type
3’’ LFDs, which are usually a result of substantial undersampling
8
that result in relatively poorly structured LFDs (see Schwamborn
et al., 2021). Veritably, length-based routines are extremely sensi-
tive to sample size due to the high importance of large individuals
(King, 2013; Schwamborn, 2018). Then, facing the global experi-
ence on vulnerable stocks, the concern on failure of the traditional
fisheries management on those cases (Hilborn and Ovando, 2014),
more precautionary and ‘‘hard-on’’ approaches are needed (Leen-
hardt et al., 2013). More specifically, the authors understand that
possible management measures must consider the upper limits
of the parameters and its possible outcomes for the produc-
tion of shrimp biomass. Close long-term monitoring must also
be implemented using both fishery-dependent and independent
surveys to obtain a comprehensive dataset to future parameter
adjustments (Lunn and Dearden, 2006; Moffett et al., 2011).
Taking into account that the fisheries of penaeid shrimps
along the Brazilian coast are intensely submitted to unmoni-
tored and acute harvest due to weak law enforcement (San-
tos, 2010b), many different management tools are available to
tackle these issues. They include closed seasons that cover re-
cruitment or spawning peaks, imposing limits on fleet/mesh size
(effort control), and protecting essential nursery areas (Dias-Neto,
2011; Gillett, 2008; Lira et al., 2021; Vandeperre et al., 2011),
with diverse success perception (Musiello-Fernandes et al., 2017).
For example, recent evidence from Lira et al. (2021), that used
ecotrophic modeling to project the outcomes of different man-
agement measures for similarly structured shrimp fisheries also
in the NBME , found that a reduction in effort of only 10% can
substantially improve landings of commercial species, including
the seabob and white shrimps, without adversely affecting the
ecosystem.
It is critical to highlight that the seabob shrimp, which spends
all its life within the ocean, can only be directly protected by
effort control and closed seasons. Contrarily, for the white shrimp,
which is dependent on estuaries to develop as post-larvae, other
options are available. For example, Baker et al. (2014) demon-
strated that the population growth rate is more proportionately
influenced by the growth and survival rates of juveniles than
adults of the shrimp Litopenaeus setiferus, which appears to use
salt marshes in estuarine habitats to grow before maturity (Baker
and Minello, 2010). Then, measures towards preserving nursery
areas such as maintaining aquatic vegetation (Taylor et al., 2017)
or reducing growth overfishing by protecting coastal shallow wa-
ters (i.e., following spawning peaks) may be a relatively neglected
shrimp management strategy.
M.S.F. de Barros, C.D. Lins de Oliveira, T.K. Pinto et al.
5. Conclusions
We recommend managers and stakeholders to be vigilant
and consider more thorough and comprehensive management
measures to protect the white shrimp stock, significantly overex-
ploited by the Peba fleet and dangerously close to the maximum
effort (MSY) in Jaraguá. The white shrimp is particularly vulner-
able to such high fishing pressure because of its slower growth
rates and more time needed to achieve optimum sizes comparing
to seabob shrimp, which clearly sets the priority for manage-
ment and conservation measures in the studied regions. We also
highlight that the productivity of this species may be enhanced
with the protection of estuaries – their nursery areas – leading
to possible reductions in juvenile mortality rates and higher
recruitment intensities.
In conclusion, our findings show that, within two of the main
NBME fishing grounds, both species (seabob and white shrimps)
exhibit similar and homogeneous size/age structure, recruitment
pattern and population parameters between fishing grounds,
which points out to the existence of a single stock for manage-
ment purposes. Consequently, we emphasize that any potential
change in fishing strategies, management rules, or environmental
impacts will affect equally both fishing grounds. Nevertheless,
our contribution does not provide any information about the
local genetic variability; therefore, the conservation practices
should be conservative to maintaining the genetic integrity of
both species. In this sense, future studies should unravel the
genetic discreteness or local adaptation of the sympatric stock
here described, improving effective management decisions.
CRediT authorship contribution statement
Matheus Souza Ferreira de Barros: Conceptualization, Data
curation, Formal Analysis, Investigation, Methodology, Validation,
Visualization, Writing – original draft, Writing – review & editing.
Cícero Diogo Lins de Oliveira: Conceptualization, Data curation,
Formal Analysis, Investigation, Methodology, Validation Writing
– original draft. Taciana Kramer Pinto: Data curation, Funding
acquisition, Resources, Supervision, Writing – review & editing.
Igor da Mata-Oliveira: Data curation, Methodology, Resources,
Writing – review & editing. Nidia Noemi Fabré: Data curation, In-
vestigation, Funding acquisition, Resources, Supervision, Writing
– review & editing. Vandick da Silva Batista: Data curation, In-
vestigation, Funding acquisition, Resources, Supervision, Writing
– review & editing.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
Acknowledgments
Thanks to all fellows from the Management and Conservation
of Renewable Resources Laboratory and Laboratory of Ecology,
Fish and Fisheries that continuously contributed to the data col-
lection and analysis, to the fishers from Pontal do Peba, and
Jaraguá, especially Samuel da Silva (Moa), José Adriano dos San-
tos (Didiu) and Edson Sabino da Silva for their kind collabora-
tion and support. Thanks to MPA (Brazilian Ministry of Fishing
and Aquaculture) and CNPQ (#445766/2015-8), which supported
the ‘‘Project Shrimp’’ NEN – ‘‘Cooperative Multidisciplinary Net-
work to subsidize the management of shrimp fishing in North
and Northeast Brazil, with ecosystem focus’’. CNPQ also provided
fellowships (VSB #311038/2017-4 and NNF #311785/2018-2).
9
Regional Studies in Marine Science 48 (2021) 102046
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