Agroforest Syst
https://doi.org/10.1007/s10457-021-00702-x (0123456789().,-volV)
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89().,-volV)
Parameters associated with sexual precocity of Nellore
heifers in integrated systems
Kássila Fernanda Bertogna . Paulo Sérgio Andrade Moreira . Fagner Júnior Gomes .
Fernando Barbosa Kachiyama . Andressa Groth . Marcelo Oster Rezende .
Ciro Augusto de Souza Magalhães . Luciano Bastos Lopes
Received: 24 June 2021 / Accepted: 5 October 2021
Ó The Author(s), under exclusive licence to Springer Nature B.V. 2021
Abstract This study evaluated how integrated crop–
livestock–forestry systems affected the expression of
sexual traits in Nellore heifers. The serum concentra-
tion of insulin-like growth factor type-I (IGF-I),
follicular diameter, rump fat thickness (RFT), and
weight gain were assessed in 48 prepubertal Nellore
heifers (14–16 months old, initial average live weight
of 270 ± 36 kg). Calf birth weight was assessed after
parturition. Heifers were distributed into four produc-
tion systems following a completely randomized
block design, with 12 animals in each treatment: open
pasture (OP); two silvopastoral systems (SPSs—single
rows or SPSt—triple rows), and crop-livestock system
(CL). Thermal comfort was evaluated using the black
globe, as well as humidity index (BGHI) and radiant
thermal load (RTL). Animals in all treatments were
K. F. Bertogna  P. S. A. Moreira  F.
B. Kachiyama  A. Groth  M. O. Rezende
Federal University of Mato Grosso, UFMT, Campus,
Sinop, Brazil
e-mail: kassilafernanda@hotmail.com
P. S. A. Moreira
e-mail: paulomoreira@ufmt.br
F. B. Kachiyama
e-mail: f.kachiyama@live.com
A. Groth
e-mail: andressagroth@hotmail.com
M. O. Rezende
e-mail: marceloosterrezende@gmail.com
exposed for long periods to heat stress; however,
thermal indexes got lesser values in the SPS treat-
ments. Heifers from the SPSt achieved the greatest
serum concentration of IGF-I, but the follicular
diameter did not differ among systems, as initially
expected. The greatest weight gain and RFT standards
were found in heifers of the CL system. Calves born
from females of exclusive livestock (OP) showed the
smallest weight at birth. Therefore, we suggested the
adoption of the SPS and CL systems for livestock beef
ranches as Nellore heifers reached better zootechnical
and physiologic parameters associated with sexual
precocity.
Keywords Agrosilvopastoral  Thermal comfort 
Livestock  Prepuberal
F. J. Gomes
Department of Animal Science, ‘‘Luiz de Queiroz’’
College of Agriculture, University of São Paulo, Pádua
Dias Av., 11, Piracicaba, SP 13.418-900, Brazil
e-mail: fagner_junior@usp.br
C. A. de Souza Magalhães  L. B. Lopes (&)
Embrapa Agrosilvopastoral, Embaúbas Av, 567,
PO Box 343, Sinop, Mato Grosso 78.550-970, Brazil
e-mail: luciano.lopes@embrapa.br
C. A. de Souza Magalhães
e-mail: ciro.magalhaes@embrapa.br
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Introduction
Brazilian livestock stands out internationally due to
several reasons. The nations’ herd consists of 214.7
million animals, and the State of Mato Grosso stands
out as the most representative in terms of livestock
numbers, with approximately 32 million heads regis-
tered in 2019 (IBGE 2020). Also, most of this
livestock shows non-dependence on grains and other
inputs as food resources. Historically, beef cattle
ranches are predominantly constituted by Zebu breeds
(Bos indicus indicus), mainly due to their rusticity and
adaptability to the tropical climate and extensive
management (Latawiec et al. 2014). Although the
most usual system among the Brazilian livestock
farmers is the open pasture, the importance of
agroforestry systems has grown steadily over the last
years and it is one of the suggested actions to reduce
carbon emissions in Brazil, advancing the concept of
carbon–neutral livestock farming (Government of
Brazil 2013).
Despite the potentialities, high temperatures in the
tropics can negatively affect the performance of some
cattle breeds, translating into low weight gains caused,
for instance, by the decrease in forage intake (Kumar
et al. 2019). Heifers exposed to high temperatures also
show fluctuations in hormonal production and follic-
ular development, contributing to puberty delay and,
consequently, to the first calving (Nogueira 2004). In
addition, previous studies (e.g., Silva et al. 2020a, b)
detected low oocyte competence in Nellore heifers
exposed to intense heat stress. Likewise, other phys-
iological events also depend upon environmental,
nutritional, and genetic factors, such as the secretion of
type I insulin-like growth factor (IGF-I) (Webb et al.
2004). Giraldo-Arana (2019) recently measured serum
IGF-I concentrations, weight gain, and rump fat
thickness (RFT), associating these characteristics as
predictors of sexual precocity in Nellore heifers. The
RFT has also been associated with reproductive
maturity and nutritional status in heifers (Yokoo
et al. 2010), with evident effects on follicular devel-
opment and steroidogenesis (Moore et al. 2003).
In this regard, crop–livestock–forest integration
systems can promote better reproductive rates due to
increased cattle weight gain (Domiciano et al. 2016)
and improved thermal comfort (Magalhães et al.
2020). Reasons for this advantage include better
microclimatic conditions promoted by the
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afforestation of pastures. This study aimed to examine
the effects of different strategies of integrated systems
on parameters associated with sexual precocity in
prepuberal Nellore heifers, such as serum concentra-
tion of IGF-I, follicular diameter, RFT, and weight
gain. Besides, the study recorded the birth weight of
calves immediately after parturition.
Material and methods
Study area
The experiment was carried out from May to Novem-
ber 2019 (210 days) at Embrapa Agrosilvopastoral,
Sinop, MT, Brazil (118 51 S, 558 35 W, 370 m a.s.l.).
The soil is a Rhodic Hapludox (Staff 2014), and the
climate was classified according to Köppen as Trop-
ical wet and dry (Aw), with rainfall concentrated in the
summer/autumn and the dry season in winter/spring
(Alvares et al. 2014). The average annual temperature
is 25.5 °C, with 20.2 °C minimum and 33.0 °C
maximum temperatures. The mean annual relative
air humidity is 70%, with annual precipitation of
2250 mm.
The study was conducted according to ethical
standards and approved by the local Committee on
Ethics in Animal Use (Protocol 001/2020).
Production systems and experimental design
A long-term experiment was established in 2011, as
described by Magalhães et al. (2019). The experimen-
tal design was a randomized complete block, com-
posed of four systems and four replicates (blocks).
Nellore heifers were distributed into the systems as
(a) livestock in an open pasture (OP) with Marandu
palisade grass [Brachiaria (syn. Urochloa) brizan-
tha (Hochst. ex A. Rich.) Stapf.]; (b) silvopastoral
system (single|SPSs), with eucalyptus trees (Eucalyp-
tus urograndis, H13 clone) disposed into a single row
(east–west direction with 3.0 m intra-row spacing
trees) spaced 37 m apart, mixed with Marandu
palisade grass, and overall density of 90 trees ha-1;
(c) silvopastoral system (triple | SPSt), also with
eucalyptus trees (H13 clone) disposed into triple rows
(east–west direction, 3.0 m intra-row and 3.5 m inter-
row spacing) spaced 30 m apart, mixed with Marandu
palisade grass, with an overall density of 135 trees
Agroforest Syst
ha-1. This density was achieved after selective
thinning removal of 50% of trees in 2016; and
(d) crop-livestock system (CL), where both compo-
nents were rotated every two years.
Before we begun the herd assessments, soybean
[Glycine max (L.) Merr.] was cultivated from October
2018 to February 2019 and then harvested according
to cropping recommendations. All systems were
installed and evaluated in experimental plots of two
hectares (100 9 200 m). Palisade grass was adopted
in all systems due to its abundance as a monoculture
pasture within the tropical climate region (Carvalho
et al. 2019).
The herd was composed of Nellore heifers (Bos
indicus indicus) with an initial mean weight of
270 ± 36 kg (SD), between 14 and 16 months old.
In each system, weight gain was recorded every 28 d
on 12 tester animals (i.e., replicates), weighing three
heifers per block. The individual weighing was
performed after 16 h of fasting, including liquids,
and the average daily weight gain was expressed in kg
d-1. Calves born from tester heifers were weighed just
after their birth, before first nursing, using a hanging
scale. Three extra pastures were used as a reserve area,
where animals (regulators) used only for adjustments
in the stocking rate were kept throughout the
experiment.
The animals were managed in continuous stoking
with variable stocking rates, maintaining the canopy
height at 30 ± 5 cm (Gomes et al. 2020). In February
2019, 50 kg N ha-1, 50 kg K2O, and 40 kg ha-1
P2O5 ha-1 in the form of urea, potassium chloride,
and superphosphate, respectively, were applied to all
pastures. The animals had free access to water
(ad libitum) and mineral supplements, set at 0.2% of
body weight (mix for the dry season: NDT (min.)
530 g kg-1; protein min. 300 g kg-1 | mix for the
rainy season: NDT min. 720 g kg-1; protein min.
200 g kg-1); both formulas used were from Fortuna
Nutrição AnimalTM. During the dry season, starting in
June was provided 15 kg animal-1 d-1 of corn silage,
terminating the offer on the first week of October.
Microclimate and estimation of thermal comfort
indices
Meteorological stations were installed in one exper-
imental unit (block) per system. In OP and CL
systems, only one station was placed at the central
point of the pasture. In the SPS units, we set five
stations in a transect, all perpendicular to the rows: one
placed in the middle of the grove, two on the north (7.5
and 15 m from edge row in SPSt; 11 and 18.5 m from
edge row in SPSs), and two others on the south face of
the central grove of trees (also at 7.5 and 15 m in SPSt;
11 and 18.5 m in SPSs).
To assess the radiant thermal load (RTL) and the
black globe and humidity index (BGHI), we moni-
tored the following variables: temperature (8C), black
globe temperature (°C), relative humidity (%), wind
speed (m s-1), and photosynthetically active radiation
(PAR; lmol photons m-2 s-1). The following sensors
were used: thermo-hygrometers (HC2—S3, Rotronic,
Bassersdorf, Swiss accuracy: ± 0.8% RH, ± 0.1 °C),
installed on multiple plates, thermocouples copper-
constantan (accuracy: 0, 4%) inside a black metallic
hollow globe, PQS-1 quantum sensor (Kipp & Zonen,
Delft, Netherlands—accuracy: ± 4 nm), ultrasonic
anemometers (Windsonic, Gill, Lymington, Hamp-
shire, UK—accuracy: ± 2% of reading). These sen-
sors were installed at 1.7 m (thermo-hygrometers and
black globe), 1.9 m (PAR), and 2 m (wind speed)
above the soil surface. The sensors were connected to
a CR3000 datalogger (Campbell Scientific, Logan,
Utah, USA) programmed to record readings every 5 s
and register the hourly average values. BGHI and RTL
(W m-2) indices were calculated using the following
equations:
BGHI ¼ Tg þ 0; 36Tdp þ 41:5
where Tg is the globe temperature (°C), and Tdp is the
dew point temperature (°C) (Buffington et al. 1981).
RTL ¼ rðTr Þ4
   4 !
p ffi 0:5 Tg
Tr ¼ 100 4 2:51Vv ðTg  TaÞ
100
where Ta is the air temperature (K), Tg is the black
globe temperature (K), Vv is the wind speed (m s-1),
and r is the Stefan-Boltzmann constant (5.6703 108
8 W m-2 K-4) (Esmay 1969).
We generated space–time maps using ArcGisTM
10.2, in which the values of BGHI and RTL were
interpolated by the Spline method to represent the
average of these indices between 7 and 18 h for each
month. The rows were represented at the bottom and
top edges, providing a better view of trees’ influence.
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In addition, the relative contribution of each range of
values was attained, for each index, to quantify the
zones of greater or lesser thermal comfort in the
systems.
Gynecological assessment
From April to November of 2019, all tester heifers
were submitted to ultrasound inspections using a
Honda Electronics HS-2000 (VET) ultrasound device,
equipped with a 7.5 MHz transrectal linear transducer
with a 10-d interval, to identify some corpus luteum as
a criterion for the first ovulation and to measure the
diameter of the largest follicle.
Serum sampling to IGF-I serum analysis
Simultaneously to the gynecological evaluation, we
collected 10 mL of a blood sample from each tester
animal, directly from the coccygeal vein, using a
25 9 8 mm needle in vacutainer tubes and then
centrifuged 3500 RPM to separate the serum. Serum
samples were aliquoted in duplicate and stored in
1.5 mL microtubes at -80 °C. The samples were sent
into a Styrofoam box containing dry ice and sent to the
Veterinary Endocrinology Laboratory of the Veteri-
nary Medicine Institute of UNESP (Araçatuba, SP;
Brazil). A standardized competitive enzyme
immunoassay (cELISA) was used for the hormonal
dosage to determine the total IGF-I concentrations
(Maioli and Nogueira 2017).
Rump fat thickness
The rump fat thickness (RFT) assessments were
carried out on three occasions: July, August, and
October 2019, when heifers were 18 and 20 months
old. The images were obtained using the Aquila-PRO
ultrasound (Esaote Piemedical) with a 3.5 MHz fre-
quency transducer. Vegetable oil was used on the
heifers’ skin, and the transducer was positioned
between the ilium and the ischium in the region of
Gluteus medius and then moved to the Biceps femoris.
The images were stored in the ultrasound for later
metric analysis.
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Statistical analysis
The data were analyzed with a parametric structure
using general linear mixed models (PROC MIXED|-
SASÒ version 9.4|Institute Inc., Cary, NC, USA).
Treatments (OP, CL, SPSs or SPSt), cycle (repeated
measurement), and interactions were considered fixed
effects. The repetition (block) was considered a
random effect.
Plots of linear predictors and quantile–quantile of
the residuals were used to examine the heteroscedas-
ticity of variances and error. The variance and
covariance matrix were selected using the Akaike
information criterion (Wolfinger and O’Connell
1993). The correction of degrees of freedom was
performed by the ‘‘Kenwardroger’’ method (Kenward
and Roger 1997), treatment averages were estimated
by least square means and multiple comparisons were
made by the probability of difference (PDIFF) using a
t-test (P \ 0.05).
Results
Regarding environmental conditions on the study site,
the greatest BGHI was 83–84 in September, stamping
the transition between the dry and the rainy seasons. In
OP, BGHI reached marks over 84, with lesser values
ranging between 81 and 82 only in July. As expected,
slighter BGHI were observed in both SPS systems
(Fig. 1), even during a critical period of the dry season
(June to July). However, the SPSt conferred better
microclimatic conditions throughout that risky period
than the other three systems, reaching values below
78.
Slighter RTL were observed in the SPSt compared
to SPSs, CL system, and OP. A possible explanation is
the greater density of trees, which led to values not
surpassing 610–640 W*m-2 and reaching values as
low as 550 W*m-2, between May and July 2019
(Fig. 2). The lowest RTL values were found in the
SPSs between May and July 2019, with 550–580 (W*
m-2) on the southern Eucalyptus rows due to the
greater shade projection. Despite the presence of trees,
there were critical sites regarding radiation over
640 W*m-2 on the north face due to lesser shade
projections from the rows (Fig. 2). These values were
registered between May and September of 2019,
which locally indicated the dry season. In the OP, RTL
Agroforest Syst

Fig. 1 Time and space dynamics of the BGHI for SPSt, SPSs,
and OP. Monthly averages between 7:00 am and 6:00 pm, from
April to November 2019
Fig. 2 Time and space dynamics of the RTL for SPSs, SPSs,
and OP. Monthly averages between 7:00 am and 6:00 pm, from
-2
values remained reasonably high (over 640 W*m ) April to November 2019
during most of the period between early May and
September, reaching reduced values (580 to Table 1 Means of IGF-I (ng ml-1) serum levels and follicular
610 W*m-2) only in October (Fig. 2) when the rainy diameter (mm) of Nellore heifers reared on OP, CL, SPSt, and
season typically begins in this area. SPSs systems in Sinop, Brazil
Concerning hormone balance, heifers submitted to Variable OP CL SPSt SPSs SE* P-
the SPSt exhibited higher serum IGF-I levels con- value
firming our initial hypothesis (Table 1). Besides, the IGF-I (ng ml-1) 476b 490b 547a 509ab 22 0.049
mean IGF-I values per treatment gradually increased
FA (mm) 8.9 9.3 9.0 9.3 0.22 0.35
over the period (P = 0.049), and the bottom levels of
IGF-I occurred during the dry season (Fig. 3) when the FA (mm): follicular diameter
harsher weather conditions usually occur in the study t-test post hoc for differences among means | Lower case letters
compare systems (P \ .05)
site.
*Standard error
There was a strong correlation (R2 = 0.909)
between serum IGF-I levels and BGHI in July, and
as mentioned before, it is a critical period for the
animals due to the lack of rain. Despite the negative follicle (Table 1). Concerning the physiological
influence of microclimate, we observed greater levels responses, we found the highest average weight gain
of IGF-I due to better conditions in the SPSt and SPSs and average daily gain in heifers reared in the CL
systems, even though all 48 heifers received the same system (Table 2) compared to OP or both SPS systems.
food resources (corn silage ? mineral ? forage). There was no variation in the RFT among systems
Regardless of better climatic conditions and greater (P = 0.269) in the initial set of measurements per-
serum levels of IGF-I, no differences were observed formed in July (Table 3). However, the same mea-
among treatments for the mean diameter of the largest surements when taken in August and October

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Fig. 3 IGF-I (mg ml-1) serum levels of Nellore heifers raised in OP, CL, SPSt, and SPSs, from April to November 2019

exhibited greater values in the CL system Table 2 Means of daily weight gain and total weight gain (kg)
(5.5 ± 1.4 mm and 6.5 ± 1.6 mm, respectively) in Nellore heifers reared in OP, CL, SPSt, and SPSs
compared to OP and SPS (Fig. 4). Calf birth weight Variable OP CL SPSt SPSs SE* P-
did not differ among intercropped systems (CL 36 kg; value
SPSs 35 kg; SPSt 35 kg); however, calves from
TWG (kg) 279b 306a 290c 288bc 3.1 0.041
heifers reared in OP showed lesser weight (28 kg | -1 b a b
AWG (kg d ) 0.28 0.48 0.30 0.34b 0.02 0.048
P = 0.0493).
TWG (kg): total weight gain; AWG (kg d-1): average weight
gain
Discussion t-test post hoc for differences among means | Lower case letters
compare systems (P \ .05)
*Standard error
Cattle are frequently exposed to adverse climatic
conditions in the tropics and 81.4% of the Brazilian
territory is located in the tropical zone (Alvares et al.
2014). Therefore, as Navarini et al. (2009) suggested, there were no previous records of beef animals
these heifers are dangerously exposed to heat stress regarding BGHI, so that index may not be suitable for
during most of the studied time based on the BGHI beef cattle under tropical climate conditions, including
gradient (79–84) as shown in our results. These data, the state of Mato Grosso.
however, should be interpreted with caution due to Despite the lack of consistent information on Zebu
limitations of criteria since there are some livestock cattle in the tropical zone, Pezzopane et al. (2019)
research boundaries. Furthermore, unlike dairy cattle, recently reported better environmental conditions in a

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Table 3 Means of RFT (mm) in Nellore heifers reared in OP, animal performance among systems, partially explain-
CL, SPSt, and SPSs ing greater Zebu adaptability to the tropical climate.
Month OP CL SPSt SPSs SE* P-Value Indeed, we witnessed better daily weight gain in the
OP where there were no trees at all, reinforcing the
July 4.1 4.6 4.9 4.3 0.06 0.269 excellent adaptability of Nellore under Brazilian
b a ab ab
August 3.9 5.5 5.0 4.6 0.13 0.009 climate conditions. Lopes et al. (2009) assessed an
b a
October 4.8 6.5 5.8ab 5.5ab 0.15 0.012 eight-year dataset (1841 cows), including variables
t-test post hoc for differences among means | Lower case letters such as temperature and humidity index (THI). The
compare systems (P \ .05) authors could not demonstrate a relationship between
*Standard error pregnancy rate and THI.
Nevertheless, pregnancy rates had high despite
adverse thermal conditions strengthen the Zebu adap-
SPS, achieving BGHI values frequently under 79 due tation to the tropical climate, even under extensive
to the reduction of direct radiation. In our study, management. In fact, Gaughan et al. (2010) suggested
differences of 22% were found between the SPS and that the lack of heat-resistant breeds is a major
the OP systems regarding BGHI values. Furthermore, limitation to livestock worldwide, emphasizing the
Magalhães et al. (2020) mentioned in their study that, need to identify breeds adapted to heat stress and
as shading increases, the mean values of BGHI and resistant animals within a nonresistant breed. Further-
RTL decrease naturally, promoting better environ- more, acclimatization would be another issue and may
mental conditions for the animals. Aranha (2019) also be considered in temperate climate zone. According to
reported similar trends in a tropical climate when Thornton et al. (2009), the lack of prior conditioning to
evaluating shading conditions during summer and a sudden change in weather often results in catas-
autumn. trophic losses to the livestock industry; however, the
Our data showed greater BGHI in OP (88), weather conditions in Mato Grosso are relatively
exposing animals to critical conditions, and lesser constant in terms of temperature.
values of BGHI (82) in the SPS composed of three Concerning RTL, lesser values were observed in
rows of eucalyptus trees. Despite these differences and the SPSt treatment compared to the other three
high BGHI, Aranha (2019) found no differences in treatments. The RTL is related to the thermal swap

Fig. 4 Means deviation of weight and RFT from heifers reared in OP, CL, SPSt, and SPSs: (means | black dot; raw data |red dots)

123

among animals and their environment, and conse-
quently, low values of RTL can mitigate heat stress
(Silva 2000). Domiciano et al. (2018) assessing cattle
welfare in the same long-term study and same study
site got greater averages of RTL 713 (W m-2) in OP,
while the highest value recorded in SPS systems was
663 (W m-2), a reduction that certainly promotes
better conditions of thermal comfort to animals reared
in the SPS.
Independent of the index, as Wolfenson et al.
(2000) mentioned, heifers exposed to thermal stress
might suffer alterations in follicular development as
well as hormonal levels imbalance. Some authors
propose that IGF-I is an important hormone in the
onset of puberty (e.g., Giraldo-Arana 2019; Heslin
et al. 2020), stimulating the follicular response to LH,
and then the proliferation of granulosa cells improving
the production of 17b-estradiol (Webb et al. 2004).
Although Nellore heifers have greater tolerance to
thermal stress and adaptation to the tropical climate,
our results show that better conditions provided by
shading in SPS systems contributed to greater IGF-I
serum levels (Table 1). Independent of differences
detected among systems, the levels of IGF-I here
reported were greater than other results previously
published. Peres (2016) found higher serum IGF-I
concentration (191 ± 6.8 ng mL-1) in cyclical Nel-
lore heifers after hormonal therapy, much lesser than
the lowest mean value we observed at the OP
treatment (4770 ± 230). However, according to Hes-
lin et al. (2020), serum concentrations of IGF-I above
334 ng mL-1 are enough to stimulate Nellore heifers
to reach puberty.
We recognize that other variables should also be
taken into account to understand the results found. We
controlled, for example, the nutritional variables, age,
and initial weight and despite of that, our results about
thermal comfort indexes (BGHI 82–84; RTL
610–640) may significantly reduce IGF-I serum levels
in heifers reared in the CL and OP systems. According
to Rhoads et al. (2010), in cows kept under thermal
stress, there is a possible decoupling of the hepatic
Grow Hormone-IGF axis, mainly in lesser levels of
IGF-I. In addition, there is an impairment in follicular
development in these conditions, decreased frequency
and pulsatility of Luteinizing Hormone (LH), and the
retardation of ovulation (Diskin et al. 2003). Lakhani
et al. (2020) detected greater plasma concentrations of
IGF-I, increased forage intake, and weight gain in
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crossbred cows under better thermal comfort condi-
tions. Our results seem to be a significant variation
related to local conditions and variables, such as breed
and system. For example, Nellore heifers reached
better weight gain in the CL system but greater IGF-I
levels in SPSt (Table 2). Thus, the role of nutrition
seems to overlap the environment for adapted breeds.
Wolfenson and Roth (2019) observed a drop in
forage intake in cows under thermal stress. Because
the concentration of IGF-I is related to nutritional
status and considering its importance for ovarian
follicular development, low concentrations may be
associated with a reduction in the reproductive
performance of heifers during the warmer periods of
the yr.
In this study, the mean IGF-I concentration per
system gradually increased over the period
(P = 0.049). Thus, it is possible to check high levels
of IGF-I in the rainy season (Fig. 3), which would be
associated with restoring energy reserves, as Webb
et al. (2004) mentioned in their study. Domiciano et al.
(2016), in an experiment also conducted at Embrapa
Agrosilvopastoral found vigorous pastures and the
highest weight gains per area (Domiciano et al. 2018)
during the rainy season. Considering those results, we
controlled the height of grass’ dossel along the whole
period of study and fed the heifers with 15 kg of corn
silage per animal over the dry season. This reinforces
our hypothesis that, after controlling other variables,
microclimate by itself seems to influence the hormonal
balance in prepubertal heifers, even in beef cattle
breeds such as Nellore.
According to Silva et al. (2020a; b), forage
accumulation and animal performance were greater
in the CL systems than SPS, in the same study site as
well. Our results indicate better performance concern-
ing weight gain too. Based on those results, milder
microclimatic conditions seem to determine the Nel-
lore heifers’ IGF-I balance. However, this hormone
cannot be seen solely as a predictor of sexual
precocity. According to Giraldo-Arana (2019), IGF-I
acts as an indirect signal of reproduction and nutri-
tional conditions events, but it is also necessary to
consider other factors involved.
In prepubertal heifers, follicular dynamics are
limited to the growth phase, with variation in the
diameter of the follicles. As the animal approaches
puberty, it is possible to identify a follicle pattern with
diameters close to ovulatory capacity. However, the
Agroforest Syst
average follicular diameter in all systems was consid-
ered suitable for Zebu females based on our results, as
Nellore heifers get ovulatory capacity between 7.0 and
8.4 mm, responding to LH increase between 8.5 and
10.0 mm in diameter (Sartori et al. 2001; Gimenes
et al. 2008).
Gasser et al. (2006) reported that follicular diameter
is associated with plasma concentrations of growth
factors, with larger follicles associated with IGF-I
concentrations. However, we did not observe this
relationship between the serum concentration of IGF-I
and the follicle’s diameter. That possibly occurred
because the animals of all systems evaluated had large
follicles (8.2 ± 0.29 to 9.3 ± 0.29 mm) and high
levels of IGF-I. Thus, it was not possible to attribute
larger follicles due to the system that induced a greater
concentration of IGF-I (SPSt; 547 ± 23.2 ng mL-1).
Torres & Junior (2008) observed a deleterious
effect on ovarian follicular dynamics in Zebu cows
exposed to heat stress, characterized by follicular
codominance associated with an increase in FSH and a
reduction in the inhibin concentration compromising
the dominance of the follicle. The occurrence of
follicular codominance due to thermal stress was not
observed in our study, possibly due to the ten-day
interval among gynecological evaluations, perhaps not
characterizing codominance occurrence.
Among others, primary factors for early sexual
precocity in heifers are that weight gain associated
with body frames has been suggested as crucial
(Nogueira 2004). Furthermore, Nepomuceno et al.
(2017) reported that the increase in weight gain of
Nellore heifers after weaning (0.7 kg of weight gain
d-1) increased the percentage of pubescent heifers at
18 mos of age (31.7 vs. 13.3%), which is considered
excellent for zebu cattle.
We found the highest average weight gain and
average daily gain in heifers reared in CL systems
(Table 2) compared to OP and both SPS systems.
These results may be related to the more significant
forage accumulation in that system after two years of
grain crops, even though all heifers had received corn
silage. Previously, from the same long-term study,
Domiciano et al. (2016) found a greater forage leaf/
stem ratio in CL, indicating a higher protein content
and digestibility of the forage compared to the OP and
SPS. According to the authors, when evaluating the
performance of Nellore steers in integrated systems,
the weight gain per area (kg ha-1) was superior in the
CL system, 32 and 44% more than the OP and SPS,
respectively (Domiciano et al. 2016). Aranha (2019)
detected a greater rate of forage accumulation in the
OP (5190 kg ha-1) when compared to the SPSs and
SPSt (3950 and 4030 kg ha -1, respectively). The
lesser mass of forage SPS may result from a lesser
amount of radiation reaching the forage (Soares et al.
2009). Similarly, Nascimento et al. (2019) found
lesser (21%) rates of photosynthetically active radia-
tion reaching the canopy in some paddock spots than
OP.
The CL system exhibited greater weight gains
(P = 0.041) compared to the other three systems.
Considering that the RFT sample section is where fat
accumulation occurs earlier in bovine species (Schro-
der and Staufenbiel 2006), it is justifiable that the
animals raised in the CL system have greater values of
RFT due to the greater average weight (Fig. 4). Wertz-
Lutz et al. (2010) mentioned a reduction in muscle
growth as the cattle approach maturity, and fat
deposition begins. Based on that and our results, that
phenomenon, as expected, likely happened on the
animals from the CL system.
Calf birth weight is a vital attribute related to adult
performance, and the selection based on this feature
can promote genetic gains during the life cycle of
Nellore females (Boligon et al. 2009). As shown by
our data, OP had the worse calf birth weight according
to our results, while in the integrated systems, calves
got around eight kg more, independently of the
consortium. The results can be attributed to the
benefits of integration in weight gain (CL) and the
best thermal comfort conditions (SPS) for females,
especially in the last trimester of pregnancy, when
there is more remarkable fetal development.
There is an intersection point that must be high-
lighted regarding integrated systems and several
implementation strategies on farms. Based on our
results, farmers should consider the best system
according to animal necessity, as there are better
options of integration to reach different goals. The
importance of afforestation to heifers regarding IGF-I
production has been discussed, as clearly demon-
strated by our results. However, if the goal is weight
gain, the CL system shows better results. Therefore,
livestock ranches should consider the availability of
areas under different intercropping strategies to max-
imize results regarding the variable of interest.
123

Conclusions
The SPSt promoted better thermal conditions influ-
encing serum IGF-I concentrations in Nellore heifers.
On the other hand, there was a greater weight gain and
rump fat thickness in the animals raised in the CL
system. Therefore, it is suggested to consider the
adoption of integrated production systems as a man-
agement strategy for anticipating puberty in Nellore
heifers due to the greater weight gain and RFT
influenced by a previous soybean crop in the CL
system and the greater serum levels of IGF-I in SPS,
since those variables are known as physiological
predictors of bovine sexual precocity.
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