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ABAH Bioflux, 2016, Volume 8, Issue 1.
http://www.abah.bioflux.com.ro 1
Follicular hierarchy evaluation of pateros ducks
(Anas platyrhynchos domestica) from semi free-
range farms of Zamboanga del Sur and Misamis
Occidental, Mindanao, Philippines
Leocris S. Batucan Jr., Bryan G. D. Belleza, Henry I. Rivero, Olga M.
Nuñeza
Department of Biological Sciences, Mindanao State University – Iligan Institute of
Technology, Tibanga, Iligan City, Philippines. Corresponding author: O. M. Nuñeza,
olgamnuneza@yahoo.com
Abstract. The egg-type pateros ducks, Anas platyrhynchos domestica, in the Philippines are raised in the
traditional semi free-range management system which allows farmers to keep the ducks in flocks as
extra activities in between their crop farming routines. This study assessed the follicular development in
ducks grown from farms in semi free-range system and evaluated the different conditions of the gonads
using the follicular ranks and the frequency of occurrence of follicular atresia. Nineteen ducks from
Zamboanga del Sur (9 aged 6-12 months; 10 aged 13-24 months) and 20 ducks from Misamis
Occidental (10 each for 6-12 and 13-24 months age group) were dissected and evaluated (n=39).
Results showed that the gonadosomatic index (GSI) of 6-12 month-old ducks from Zamboanga del Sur
(Group 1) was 0.367% while GSI of the 6-12 month-old ducks from Misamis Occidental (Group 2) was
0.323%. Lower GSI of 0.298% was observed for Group III (13-24 month-old ducks from Zamboanga del
Sur) and Group IV with 0.222% (13-24 month-old ducks from Misamis Occidental). Results also revealed
atretic, unresponsive, and undeveloped follicles in almost all of the ducks sampled which appear to be
affected by the type of feeding management by the farmers.
Key Words: Endocrine disruptor, feeding, follicles, gonads, gonadosomatic index, management.
Introduction. The Philippine duck industry is dominated by balut (partially hatched
embryos) production and by smallholder production that accounts for more than 75
percent of total duck output (Dagaas & Chang 2004). The demand for duck products in
the Philippines continually rises indicating that the duck industry can be a lucrative
enterprise. The pateros ducks, Anas platyrhynchos domestica, are raised under two farm
management systems – complete confinement and semi free-range system (Lambio et al
1988). In the latter, ducks are allowed to range freely the whole day usually in rice fields
and are then herded back to their shelter at night time or during severe weather. Semi
free-range management system allows the ducks to have varying food sources as
compared to the commercial management system wherein the food they eat depends on
the farmer’s choice. However, semi free-range management system exposes the ducks to
a number of ecological factors which could alter their egg-laying capacity. Data over a
10-year period (2003-2013) showed that there is stagnation, if not contraction, in the
duck inventory of five out of six regions of Mindanao (Philippine Statistics Authority
2014).
The low egg productivity must be taken into account in order to help the farmers
overcome decline in marketing as well as low-quality breeding stocks. One of the ways
duck egg production fitness can be assessed is by checking on its follicular hierarchy and
occurrences of follicular atresia on the ranks of rapidly growing follicles. Birds have
unique characteristic in their ovaries wherein follicles from all stages of development
exist at the same time once they reach egg-laying stage (Johnson & Woods 2007).
Examination of the preovulatory follicles (POF) may provide a viable method to estimate
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breeding probability in free-range mallard populations (Lindstrom 2005). POF belonging
to a clutch is a good tool for researchers to assess the egg-laying health of ducks and
thus draw conclusions for use, enforcement, and policy development by concerned
individuals.
The main goal of the study was to determine the state of the gonads of randomly
sampled ducks in two provinces in the Philippines. Documenting the growing follicles of
duck layers in varying stages of growth and development can give us a physiological
knowledge on the state of duck gonads in semi free-range farms of Mindanao.
Material and Method. Thirty-nine randomly selected 6–12 months (early laying, EL)
and 13–20 months old (late laying, LL) pateros ducks were sampled from semi free-
range farms located in Zamboanga del Sur (ZDS) and Misamis Occidental (MSO) (Figure
1). The birds were divided into four groups based on location and age. Group I consisted
of nine EL ducks from Zamboanga del Sur (EL-ZDS); Group II with 10 EL ducks from
Misamis Occidental (EL-MSO); Group III with 10 LL ducks from Pagadian City (LL-ZDS);
and Group IV with 10 LL ducks from Misamis Occidental (LL-MSO). Body weight of each
individual was recorded prior to dissection. After dissection, the gonads were carefully
isolated and imaged, weighed, and then stored in a freezer (-40C) for future use. Mature
follicles of follicular hierarchies were measured using ImageJ v1.46r.
Figure 1. (A) Ducks freely ranging in the streams of a farm in Misamis Occidental. (B)
Location of the sampling sites marked “x”. (C) A herd of Anas platyrhynchos domestica
from Misamis Occidental and the (D) shelter at night. (Photos A, C, D are original photos;
B, from www.mindanaomaps.com with modifications).
Results and Discussion. The mean live weights (LW) of groups I at 1,304 g and II at
1,326 g were more or less similar (Table 1) while ducks belonging to Group III were
heavier compared to Group IV with mean live weights of 1,472 g and 1,387 g,
respectively (Table 2). The mean gonadal weights (GW) and mean gonadosomatic index
(GSI) between groups I and II were of values close to each other but varied greatly
between Groups III and IV. The GWs of ducks with preovulatory follicles are indicated in
red; the ones colored black signify absence of preovulatory follicles.
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Table 1
Live weights (LW), gonadal weights (GW), and gonadosomatic index (GSI) of duck layers
from Groups I and II (6-12 months)
LW (g) GW (g) GSI (%)
Sample I II I II I II
1 1460 1350 1.6 3.5 0.11 0.26
2 1250 1320 3.5 4.7 0.28 0.356
3 1320 1420 1.7 3.3 0.129 0.232
4 1240 1320 2.7 3.4 0.218 0.258
5 1150 1380 11.5* 1.8* 1 0.13
6 1340 1420 6.9* 12.9 0.515 0.908
7 1600 1240 2.1 3.2 0.131 0.258
8 1000 1100 1.8 3.5 0.18 0.318
9 - 1280 - 2.7 - 0.211
10 1380 1430 10.2 4.2 0.739 0.294
Mean 1304 1326 4.667 4.32 0.367 0.323
* - presence of preovulatory follicles in the gonads.
Table 2
Live weights (LW), Gonadal weights (GW), and Gonadosomatic index (GSI) of duck layers
from Groups III and IV (13-24 months)
LW (g) GW (g) GSI (%)
Sample III IV III IV III IV
1 1780 1340 5.1* 2.6 0.287 0.194
2 1440 1400 3.4 2.8 0.236 0.2
3 1470 1420 6.4 1.6 0.435 0.113
4 1540 1470 3.7* 1.6 0.24 0.109
5 1240 1370 5.3 5.9* 0.427 0.431
6 1340 1170 3.4 1.4 0.253 0.12
7 1320 1260 2.8 1.2 0.212 0.0952
8 1310 1500 1.6 5.2* 0.122 0.347
9 1620 1480 - 4.2 - 0.284
10 1660 1460 7.8* 4.9 0.47 0.336
Mean 1472 1387 4.388889 3.14 0.298 0.22292
* - presence of preovulatory follicles in the gonads.
A comparison on the LWs and GWs in each group showed two opposite trends. Group I
data give a negative correlation between LW and GW (Figure 2). Group II data however
showed that increasing LW is related with rapidly increased GW. Group III ducks showed
the linearity between the LW and GW relationship while Group IV duck samples showed
almost similar pattern as Group II with more confined increasing GW within a very small
range of LWs. Generally, all duck samples showed that increasing LW was related with
increased GW as shown in both semi-ranged farms except for Group I consisting of 6-12
month old ducks from Pagadian City.
Although the graph above shows a good relationship between the LW and GW, the
actual condition of the gonads tells otherwise. Of the nine ducks in Group I, only two
individuals (samples 5 and 6) had preovulatory follicles (follicles >9 mm), all the rest
have follicles at an early stage (Table 3). The inconsistent gonadal weight to live weight
relationship in Group I is another thing that needs revisiting. This observed trend in the
mature ovary of ducks in a flock would be quite alarming.
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Figure 2. Correlation coefficient and regression equation between gonadal weight (GW)
and live weight (LW) of ducks in all groups.
Table 3
Area of preovulatory follicles (mm2) from duck layers and the number of preovulatory
follicles each produced (>9mm)
F1 F2 F3 F4 F5 F6 Mean
Group I-5 189.572* 130.138*
133.826 137.717*
- - 147.813
Group I-6 103.842 - - - - - 103.842
Group II-5
1,243.214
335.138*
347.039*
178.586*
238.573
169.658*
418.701
* - atretic large follicle.
The advanced preovulatory follicles (F1 and F2) of sample 5 were atretic with only the F3
appearing as viable (Figure 3). Already on its second clutch, sample 6 of Group I only
had one preovulatory follicle in which succeeding prehierarchal follicles are discolored and
have an irregular shape.
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Figure 3. Image compilation of ducks with follicular hierarchy. (A) Group I sample 5 with
four preovulatory follicles wherein three are atretic. (B) Group I sample 6 with one
preovulatory follicle and a discolored prehierarchal follicle. (C) Group II sample 5 with six
preovulatory follicles, note the irregular yolk deposition from in F2-F4 and F6. (D) An
ovary with prehierarchal follicles with the largest having an abnormal blood deposition on
its surface (original).
Ducks from Group II only had one sample, sample 5, with follicular hierarchy wherein
only two are viable preovulatory follicles, F1 and F5. All succeeding follicles were all
atretic, with irregular coloration and shapes due to abnormal yolk deposition. Sizes of the
preovulatory follicles in Group I were rather small with mean area of 147.813 mm2 and
103.842 mm2 compared to the sizes of follicles in Group II which had a mean area of
418.701 mm2.
Figure 4 shows the follicular hierarchy of Group III and Group IV duck samples
with distinct preovulatory follicles. Among the 20 sampled individuals, only a few
preovulatory follicles were noted while most have inhibited, unresponsive, and atretic
conditions. The noticeable delay in the egg laying of the ducks can be attributed to the
presence of atretic follicles.
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Figure 4. Image compilation of duck gonads (13-24 months old) with follicular hierarchy.
(A.) Group III sample 1 with single preovulatory follicle wherein most surrounding
follicles are undeveloped and unresponsive. (B.) Group III sample 4 with two
preovulatory follicles and irregular yolk deposition. (C.) Group IV sample 5 with five pre-
hierarchal follicles wherein 3 are atretic. (D.) Group IV sample 8 gonad with two
preovulatory follicles wherein one is unresponsive (original).
Table 4 presents the sizes of the follicles in Group III and IV duck samples as well as the
number of preovulatory follicles each one produced. Group III has small sizes of follicles
with a mean area of 95.656 mm2, 124.939 mm2 and 146.5647 mm2 compared to Group
IV with a mean area of 210.8916 mm2 and 120.039 mm2.
Table 4
Area (mm2) and number of preovulatory follicles of duck layers (13-20 months)
Sample F1 F2 F3 F4 F5 Mean
Group III - 1 95.656 - - - - 95.656
Group III - 4 95.663 58.552 - - - 124.939
Group III – 10 88.996 46.781 32.363 - - 146.5647
Group IV - 5 83.347 56.829 43.335 22.931 22.248 210.8916
Group IV - 8 100.929 38.22 - - - 120.039
Data showed that from Groups III and IV, only five (three and two, respectively) were
seemingly reproductively capable with the other seven having delayed maturity since no
mature follicles were present despite their age. Follicles in these samples were all in PGC,
primary, or prehierarchal stage and most have abnormal atresia. The apparent delay in
the reproductive maturity of the ducks and the presence of abnormal atresia can be
partially attributed to management system of the farm and its feed administration.
A study of Arora & Samples (2011) reported a linear relationship between body
weight and the number of large yellow follicles in heavier birds compared to lighter birds
at the onset of sexual maturity. Data collected exhibit the role of body weight as a means
of assessing reproductive and physiological traits since body weight is the most important
A
B
C
D
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factor in determining the onset of egg production (Ocak et al 2004). This is partially
supported with the data gathered since duck samples with distinct follicles were also the
ones exhibiting an increased weight. Previous studies have shown that larger follicles
yield oocytes with increased rates of development, fertilization, and embryo development
than those yielded by smaller follicles (Thomas et al 2000). Large follicles may indicate
the beginning of preovulatory luteinization which has a potential role in ovulation (Rice et
al 1996). However, most of the ducks with good LW and GW had low follicle quality, even
late growing follicles have intervening atresia.
The primordial follicles of all ducks, except for one, were already exhibiting yolk
deposition. More advanced follicles in the ovary have no yolks while those in earlier
stages were already exhibiting yolk deposition. In addition, all viable preovulatory follicles
found had irregular blood vessel formation on its vitelline membrane and all samples with
preovulatory follicles are coupled with severely atretic follicles. Data indicate that a large
number of individuals have delayed maturity since there were no mature follicles
observed in the gonads despite their age along with the fact that they are supposed to be
in the peak of laying eggs. Regression of follicle size often makes it difficult to distinguish
between POFs and atretic follicles at later stages of envelopment (Lindstrom 2005).
Atresia can occur when large yolk-filled follicles or pre-ovulatory follicles are reabsorbed
prior to ovulation. Involution atresia occurs when the oocyte and yolk are enveloped into
the ovary and the follicle becomes discolored and irregularly shaped. During bursting
atresia, ovarian follicles rupture and their yolk contents are released into the body cavity
(Johnson 2000).
It was gathered through key informant interviews that the farmers transport the
ducks almost every three months to places where there are rice harvests for ducks to
feed and help in the consumption of snails which are considered pests on rice.
Transportation to long distances causes stress in ducks which is a probable cause for the
atresia. This can be verified by the accounts of the farmers that egg production
significantly decreases after long distance transport of the ducks.
The noticeable delay in the reproductive maturity of the ducks can be attributed to
the presence of these atretic follicles. A study conducted by Urata et al (2006) suggested
that atretic follicles present lower estrogen values which reduce their antioxidant
mechanisms.
The ducks sampled in this study were ranged in rice fields in order to control snail
populations. These rice fields, however, are regularly sprayed with pesticides to increase
rice production. Studies have shown that reproduction may be at risk from chemical
discharge into the environment particularly those which exist throughout the food chain
where ducks were involved. Feeds laced with pesticide and cadmium cause abnormalities
which include atretic follicles, deformed follicles, and fibrosis in the ovary of female A.
platyrhynchos domestica (Anggraeni 2010). Likewise, exposure of 7-11 month old
mallard ducks to organophosphate pesticide reduces body weight, egg production, and
egg quality (Gile & Meyers 1986). This can explain the presence of abnormally occurring
atresia in the ducks from both sampling sites since the ranging ducks drink the water and
feed on rice fields which are sprayed with pesticides. In a separate study of Renema et al
(1999), it was found that hens fed ad libitum had a sharp increase in follicular atresia,
the reason for this is still unknown (Robinson & Renema 2003). From this we can say
that the abnormal atresia in the ducks sampled is contributed upon by the feeding style
and the quality of feeds being obtained by the ducks. Although the ducks are used to
control snail population in rice fields, they appear to be unknowing victims of the adverse
effects of pesticides.
In a study on Coturnix japonica layers (Arora & Samples 2011), body weight was
found to have a distinct bearing on the weight of reproductive and physiological traits.
One disadvantage of the feeding method the farmers use is that each duck does not have
a regular intake of food as food availability in rice fields is limited since ducks can only
graze on fields that have been freshly harvested and the food the ducks eat are not being
regulated. Feed restriction results in loss of body weight which ultimately causes
alterations in body composition and reduction of ovarian follicles (Arora & Samples
2011).
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This paper found that the semi free-range duck management system that some
Mindanao farmers employ can have adverse effects on the reproductive physiology of
ducks as evidenced by the apparent delayed reproductive maturity of the supposed duck
layers and the presence of abnormal atresia in their ovaries. The system in itself does not
cause the physiological problems of the ducks, instead, it is the quality of food and water
the ducks are getting from the rice fields.
Conclusions. All the ducks sampled although reaching the required live weights to be
considered to belong to laying age, showed problematic follicular development which
includes irregular yolk deposition, abnormal atresia, and delayed gonadal maturity. It
appears that these problems can be attributed to the diet of ducks sourced from
pesticide-laced rice fields. This study acknowledges the significant implication of farming
system to the reproductive performance of sexually mature ducks.
Acknowledgment. We thank the Department of Science and Technology – ASTHRDP for
the financial grant and Glenda Enriquoso and Janet Aquino for allowing their farms to be
sampled.
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Received: 11 February 2016. Accepted: 16 March 2016. Published online: 23 March 2016.
Authors:
Leocris Saavedra Batucan Jr., Mindanao State University – Iligan Institute of Technology, College of Science and
Mathematics, Department of Biological Sciences, Philippines, Iligan City, Tibanga, Andres Bonifacio Avenue,
9200, e-mail: leocrisjr@yahoo.com
Bryan George De Pedro Belleza, Mindanao State University – Iligan Institute of Technology, College of Science
and Mathematics, Department of Biological Sciences, Philippines, Iligan City, Tibanga, Andres Bonifacio Avenue,
9200, e-mail: bryangeorge.belleza@gmail.com
Henry Ibita Rivero, Mindanao State University – Iligan Institute of Technology, College of Science and
Mathematics, Department of Biological Sciences, Philippines, Iligan City, Tibanga, Andres Bonifacio Avenue,
9200, e-mail: henryrivero@gmail.com
Olga Macas Nuñeza, Mindanao State University – Iligan Institute of Technology, College of Science and
Mathematics, Department of Biological Sciences, Philippines, Iligan City, Tibanga, Andres Bonifacio Avenue,
9200, e-mail: olgamnuneza@yahoo.com
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution and reproduction in any medium, provided the original author and source
are credited.
How to cite this article:
Batucan L. S. Jr., Belleza B. G. D., Rivero H. I., Nuñeza O. M., 2016 Follicular hierarchy evaluation of pateros
ducks (Anas platyrhynchos domestica) from semi free-range farms of Zamboanga del Sur and Misamis
Occidental, Mindanao, Philippines. ABAH Bioflux 8(1):1-9.
