Reproductive adaptation of local Algerian ewes to seasonal constraints: follicular dynamics and oocyte morphology during anestrus

Reproductive adaptation of local Algerian ewes to seasonal constraints: follicular dynamics and oocyte morphology during anestrus | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Reproductive adaptation of local Algerian ewes to seasonal constraints: follicular dynamics and oocyte morphology during anestrus Mohammed Sehnine, Hamida Djilali, Louiza Skandri, Ibrahim Belabdi, and 2 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8475129/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 4 You are reading this latest preprint version Abstract Seasonal anestrus in ewes is typically associated with reduced ovarian activity due to photoperiod-driven reduction of gonadotropin secretion. However, locally adapted sheep breeds raised under subtropical conditions may exhibit adaptive reproductive mechanisms that mitigate this seasonal constraint. This study is the first in Algeria to evaluate follicular dynamics, oocyte yield, and oocyte morphology in local ewes during the anestrous period. A total of 124 ovaries were collected from abattoir-derived ewes between March and June. Visible follicles were classified as small (≤ 2 mm) or large (≥ 3 mm), and recovered oocytes were morphologically graded (Q1–Q4). Overall, 1,284 follicles and 430 oocytes were obtained. Ovarian examination revealed a predominance of small antral follicles (median 32 [16–89] vs. 11 [5–25]; p < 0.01), with no significant difference in total follicle numbers between right and left ovaries (median 23 [11–53] vs. 20 [13–47]; p ≥ 0.05). In contrast, a significant right-sided asymmetry was observed in oocyte recovery (median 12 [10–18] vs. 10 [6.5–13]; p = 0.04), particularly for high-grade oocytes (Q1 + Q2) (median 7 [4–8] vs. 3 [1.5–6.5]; p = 0.02). Moreover, higher high-grade oocyte-to-follicle ratios were observed at the ovarian level in ovaries characterized by a greater proportion of large follicles, particularly in the right ovary (1.52 ± 0.29 vs. 0.42 ± 0.07; p < 0.001). These findings demonstrate that local Algerian ewes maintain active follicular development and produce high morphological grade oocytes during seasonal anestrus, reflecting adaptive reproductive flexibility under subtropical environmental conditions. This resilience supports the potential year-round application of assisted reproductive technologies in locally adapted sheep production systems. subtropical environment ewes anestrus reproductive resilience antral follicles oocyte morphology Figures Figure 1 Figure 2 Figure 3 Introduction Sheep exhibit marked reproductive seasonality, primarily regulated by photoperiodic cues that modulate ovarian function through neuroendocrine pathways (Kopycinska et al., 2022 ; Wyse et al., 2018 ). Day length is transduced into melatonin rhythms by the pineal gland, which in turn regulates pulsatile secretion of gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH), driving follicular growth and ovulation (Chemineau et al., 2010 ; Clarke et al., 2009 ; Nestor et al., 2018 ). Typically, most breeds are sexually active during short-day periods (autumn to winter), and enter seasonal anestrus during long-day periods (spring to summer), characterized by reduced LH pulse frequency, incomplete follicular development, and absence of ovulation (Dardente et al., 2016 ; Goodman et al., 2010 ; Seekallu et al., 2010b ). Structural changes in the ovarian stroma may also create a biomechanical environment unfavorable for ovulation during anestrus (Grosbois et al., 2025 ). Comparative studies indicate a latitudinal gradient in reproductive seasonality and notable between-breed variability. Breeds from equatorial, tropical, or subtropical regions often display reduced photoperiodic influence and maintain ovarian cyclicity and estrous activity for most of the year (Pampori et al., 2018 ; Rosa & Bryant, 2003 ; Serranito et al., 2021 ). In Algeria, local breeds such as Ouled Djellal, Rembi, Hamra, and D’Man— which together represent the majority of the national sheep population—exhibit low reproductive seasonality, prolonged estrous activity, residual ovarian function during anestrus, and the capacity for multiple lambing seasons (Adaouri et al., 2023 ; Boubekeur et al., 2019 ; Meddah et al., 2024 ; Taherti et al., 2024), reflecting long-term adaptation to arid and semi-arid environments (Gani & Niar, 2019 ; Zidane et al., 2021 ). These traits contribute to reproductive resilience, which is essential for sustaining local livestock production under challenging subtropical conditions. Despite this relative resistance to seasonality, detailed studies of ovarian function during anestrus remain scarce in Algerian ewes. Most reports focus on estrous behavior, lambing intervals, or general reproductive performance, whereas follicular development and oocyte competence remain poorly characterized. These traits are assessable only via morphological evaluation, although they are essential for understanding low-seasonality adaptations and guiding reproductive management (Simoes et al., 2021 ). The present study aimed to characterize follicular dynamics and oocyte morphology in local Algerian ewes during anestrus, with particular attention to ovarian asymmetry and the relationship between follicle size and oocyte morphological grade, providing insights into adaptive reproductive strategies in locally adapted breeds. Materials and methods Study area The study was conducted at the Laboratory of Natural Bio-Resources (LBRN), Hassiba Ben Bouali University of Chlef, situated in northern Algeria (36°09′ N, 1°20′ E), a semi-arid subtropical region. Summers are hot and dry, winters cool and partly cloudy, with annual temperatures ranging 6–37°C. The wet season lasts September to June, and day length varies from 9 hours 45 minutes (winter solstice) to 14 hours 30 minutes (summer solstice), defining short-day (autumn–winter) and long-day (spring–summer) photoperiods. These seasonal and thermal conditions present environmental challenges that influence reproductive performance, making local ewes suitable models for studying reproductive adaptability. Animals and sampling A total of 124 ovaries from 62 local ewes, mostly Ouled Djellal, were collected post-mortem from a state-approved abattoir during 15 weekly sessions from early March to late June, corresponding to the long-day photoperiod and main seasonal anestrous period. Animals–with unknown age and body weight–were reared under extensive semi-arid farming systems. Ovarian collection and follicular assessment Immediately post-slaughter, the uteri were removed and the ovaries were excised, trimmed, and disinfected with 70% ethanol. Each ovary was placed in a labeled container (identified as right or left) containing saline (0.9% NaCl) supplemented with 50 µg/mL gentamicin. Containers were maintained at 35–37°C during transport and delivered to the laboratory within approximately 2 hours, with temperature preserved using a water bath inside a cooler (Izquierdo et al., 2019 ). Upon arrival, ovaries were rinsed with warm saline, and visible surface follicles were counted under a stereomicroscope. Antral follicles were classified as small (≤ 2 mm) or large (≥ 3 mm) (Paramio & Izquierdo, 2016 ). Total follicle counts and follicle-to-ovary ratios were calculated for right and left ovaries separately. Oocyte recovery and grading Cumulus–oocyte complexes (COCs) were manually punctured separately from visible follicles using a 20G needle attached to a 5 mL syringe containing 0.5–1 mL phosphate-buffered saline (PBS, 30–35°C) (Mondal et al., 2019 ). COCs were isolated and morphologically graded based on cumulus cell investment and cytoplasmic homogeneity (Fig. 1): Q1 (Excellent): ≥ 3 cumulus cell layers, homogeneous cytoplasm; Q2 (Good): 2–3 layers, slightly granulated cytoplasm; Q3 (Fair): few cumulus cells, irregular cytoplasm; Q4 (Poor): denuded or abnormal oocytes (Almeida et al., 2011 ). Only high-grade oocytes (combined Q1 + Q2) were considered suitable for in vitro maturation procedures. Oocyte-to-follicle ratios were calculated at the ovarian level to evaluate overall follicular efficiency. These ratios represent global estimations, as individual matching between retrieved oocytes and follicle size classes was not possible. Statistical analysis Data were analyzed using GraphPad Prism version 9.5.1 (GraphPad Software, San Diego, USA). Right and left ovaries were treated as independent samples. Descriptive data are presented as mean ± SEM for normally distributed variables and median [IQR] for non-normal variables. Comparisons between right and left ovaries were performed using the Mann–Whitney U test (one-tailed when a directional hypothesis applied), while within-ovary paired comparisons used the Wilcoxon signed-rank test. Statistical significance was set at p < 0.05. Results Descriptive data of the collected ovaries During the long-day photoperiod (from early March to late June), 124 ovaries were collected from abattoir-derived local Algerian ewes over 15 sessions, averaging 8.27 ± 1.86 ovaries per session. Transport to the laboratory was completed within 120 ± 12 minutes while maintaining physiological temperature. Right and left ovaries were equally represented, allowing balanced comparison of ovarian activity during seasonal anestrus (Table 1). Table 1 Descriptive data of ovary collection, transport conditions, and follicular–oocyte yield in Algerian local ewes. Parameter Overall Right ovary Left ovary Right vs Left (p-value) Sampling sessions (n) 15 – – – Transport time (min) 120 ± 12.42 – – – Total ovaries collected (Sum) 124 62 62 – Ovaries per session 8.27 ± 1.86 4.13 ± 0.94 4.13 ± 0.93 ns Total follicles punctured (Sum) 1284 693 591 ns Follicles per ovary 9.65 ± 1.12 9.91 ± 1.29 9.43 ± 1.07 ns Total oocytes collected (Sum) 430 264 166 p = 0.04 Oocytes per ovary 4.40 ± 0.52 5.32 ± 0.63 3.50 ± 0.56 p = 0.02 Note. Values are expressed as mean ± SEM. “Sum” refers to the absolute number. Comparisons between right and left ovaries were performed using the Mann–Whitney U test. ns = not significant; p < 0.05 was considered statistically significant. Follicle counts and size distributions A total of 1284 antral follicles were manually punctured from all ovaries, corresponding to a median of 44 [23–100] and a mean of 9.65 ± 1.12 follicles per ovary. The right ovary contained slightly more follicles (693; median 23 [11–53]; 54% of total follicles) than the left (591; median 20 [13–47]; 46% of total follicles), although the difference was not statistically significant ( p ≥ 0.05) (Table 2). In addition, no significant difference in the mean follicle-to-ovary ratio was observed between the right (9.91 ± 1.29) and left (9.43 ± 1.07) ovaries (Table 1), indicating a uniform antral follicle pool. Table 2 Follicle counts and size distribution in right and left ovaries. Parameter Overall Right ovary Left ovary Right vs Left Sum (p-value) Total follicles 1284 44 [23–100] 23 [11–53] 20 [13–47] ns Small follicles ≤ 2 mm 913 32 [16–89] 16 [6–46] 16 [10–43] ns Large follicles ≥ 3 mm 371 11 [5–25] 5 [2–12] 4 [2–12] ns Small-to-large ratio – – 3.1 [1.5–6.6] 3.33 [1.5–6] ns Note. Data are presented as median [IQR]. “Sum” refers to the absolute number of follicles collected from all ovaries combined. Comparisons between right and left ovaries were performed using the Mann–Whitney U test. ns = non-significant; p < 0.05 was considered statistically significant. Analysis of follicle size revealed that small follicles (≤ 2 mm) dominated the ovarian structure (913; median 32 [16–89]; 71.1% of total follicles) compared with large follicles (≥ 3 mm) (371; median 11 [5–25]; 28.9% of total follicles; p < 0.001; Wilcoxon signed-rank test), confirming the predominance of basal follicular recruitment (Fig. 2). This pattern was consistent across both ovaries ( p < 0.01). However, no significant right–left differences were observed between follicle size categories, supporting the presence of a stable follicular pool (Table 2). Oocyte yield and morphological grading A total of 430 cumulus-oocyte complexes (COCs) were recovered (median 22 [16.5–36]), corresponding to a mean of 4.40 ± 0.52 oocytes per ovary and an oocyte recovery rate of 33.5% from all follicles. The right ovary yielded significantly more COCs (264; median 12 [10–18]; 61.4% of total oocytes) than the left ovary (166; median 10 [6.5–13]; 38.60% of total oocytes; p = 0.04) (Table 3). This right-sided predominance was also observed in the mean oocyte-to-ovary ratio (right: 5.32 ± 0.63 vs. left: 3.50 ± 0.56; p = 0.02), indicating a clear functional asymmetry despite similar total follicle counts between the ovaries (Table 1). Table 3 Comparison of total oocyte number and their morphology grades (Q1–Q4) between right and left ovaries. Parameter Overall Right ovary Left ovary Right vs Left Sum (p-value) Total oocytes 430 22 [16.5–36] 12 [10–18] 10 [6.5–13] p = 0.04 Q1 (Excellent) 126 7 [3.5–10.5] 4 [2.5–6.5] 2 [0.5–5] p = 0.03 Q2 (Good) 69 3 [1–6.5] 2 [1–3.5] 1 [0–2] p = 0.02 Q3 (Fair) 102 5 [3–8] 3 [2–5.5] 3 [1–4.5] ns Q4 (Poor) 133 8 [4.5–12] 4 [3–6] 3 [1–5] ns High-grade (Q1 + Q2) 195 10 [6–15] 7 [4–8] 3 [1.5–6.5] p = 0.02 Low-grade (Q3 + Q4) 235 13 [9–21] 7 [4.5–12] 6 [4–7.5] ns Note. Data are presented as median [IQR]. “Sum” refers to the absolute number of oocytes collected from all ovaries combined. Comparisons between right and left ovaries were performed using the Mann–Whitney U test. ns = non-significant; p < 0.05 was considered statistically significant. Assessment of COC quality indicated that morphologically high-grade oocytes (Q1 and Q2) were significantly higher in the right ovary ( p < 0.05; Mann–Whitney U test) (Table 3). A total of 195 high-grade oocytes (combined Q1 + Q2) were collected (median 10 [6–15]), accounting for 45.35% of total oocytes. This category of oocytes was more abundant on the right side than on the left (median 7 [4–8] vs. 3 [1.5–6.5]; p = 0.02), accounting for 30.46% vs. 14.88% of total oocytes recovered, respectively. Considered individually, the number of excellent-grade oocytes (Q1) (median 4 [2.5–6.5] right vs. 2 [0.5–5] left) and good-grade oocytes (Q2) (median 2 [1–3.5] right vs. 1 [0–2] left) were also significantly greater on the right ( p < 0.05). In contrast, morphologically low-grade oocytes (Q3 and Q4), whether considered individually or combined (Q3 + Q4), showed no significant differences between the two sides. Oocyte quality according to follicle size Functional asymmetry became evident when oocyte recovery was normalized to follicle number. Because oocytes could not be individually assigned to their follicle of origin, these ratios reflect ovarian-level (session-level) associations between follicle size distribution and oocyte morphology. Accordingly, the ratios do not represent individual follicle–oocyte correspondence (Table 4). Table 4 Within-ovary comparisons of follicular and oocyte ratios in Algerian local ewes during seasonal anestrus. Parameter Overall Right ovary Left ovary Right vs Left (p-value) Total follicles-to-ovary 9.65 ± 1.12 9.91 ± 1.29 9.43 ± 1.07 ns Small (≤ 2 mm) 7.33 ± 0.98 7.64 ± 1.11 7.05 ± 0.96 ns Large (≥ 3 mm) 2.32 ± 0.47 2.27 ± 0.58 2.38 ± 0.44 ns Total oocytes-to-ovary 4.40 ± 0.52 5.32 ± 0.63 3.50 ± 0.56 p = 0.02 High-grade (Q1 + Q2) 1.93 ± 0.31 2.60 ± 0.41 1.27 ± 0.36 p < 0.01 Low-grade (Q3 + Q4) 2.47 ± 0.37 2.72 ± 0.39 2.23 ± 0.44 ns Total oocytes-to-follicles 0.52 ± 0.07 0.63 ± 0.08 0.43 ± 0.08 p = 0.04 Small (≤ 2 mm) 0.73 ± 0.10 0.88 ± 0.14 0.62 ± 0.13 p = 0.04 Large (≥ 3 mm) 3.46 ± 1.17 3.09 ± 0.57 2.22 ± 0.45 p = 0.03 High-grade oocytes-to-follicles 0.22 ± 0.03 0.31 ± 0.05 0.14 ± 0.04 p < 0.01 Small (≤ 2 mm) 0.32 ± 0.05 0.42 ± 0.07 0.23 ± 0.07 p = 0.01 Large (≥ 3 mm) 1.27 ± 0.36 1.52 ± 0.29 0.58 ± 0.12 p < 0.01 Note. Data are expressed as mean ± SEM. Differences between right and left ovaries were analyzed using the Mann–Whitney U test. ns = non-significant; p < 0.05 was considered statistically significant. The mean total oocyte recovery appears to be higher in large follicles (≥ 3 mm) than in small follicles (≤ 2 mm) (3.46 ± 0.17 vs. 0.73 ± 0.10; p < 0.001; Wilcoxon signed-rank test). Moreover, the right ovary displayed a higher oocyte-to-follicle ratio in both small (right: 0.88 ± 0.14 vs. left: 0.62 ± 0.13; p = 0.04) and large follicles (right: 3.09 ± 0.57 vs. left: 2.22 ± 0.45; p = 0.03). This ratio was higher in large follicles compared with small follicles, notably on the right side (3.09 ± 0.57 vs. 0.88 ± 0.14; p = 0.001; Wilcoxon signed-rank test) (Table 4). Similarly, the mean total high-grade (Q1 + Q2) oocyte-to-follicle ratios were higher in large follicles (≥ 3 mm) than in small follicles (≤ 2 mm) (1.27 ± 0.36 vs. 0.32 ± 0.05; p < 0.0001; Wilcoxon signed-rank test). When ratios of high-grade oocytes were expressed according to follicle size in both ovaries, the right ovary yielded higher proportions of high-grade oocytes in both large follicles (right: 1.52 ± 0.29 vs. left: 0.58 ± 0.12; p < 0.01) and small follicles (right: 0.42 ± 0.07 vs. left: 0.23 ± 0.07; p = 0.01; Mann–Whitney U test). Moreover, high-grade oocytes appear to be more frequently recovered from the right ovary, particularly from large follicles, compared with small follicles (1.52 ± 0.29 vs. 0.42 ± 0.07; p < 0.001; Wilcoxon signed-rank test) (Fig. 3). Discussion This study provides the first comprehensive characterization of follicular dynamics and oocyte morphology in local Algerian ewes during seasonal anestrus, revealing adaptive reproductive traits not previously documented in North African breeds. Despite the expected photoperiod-driven reduction in ovarian activity, ovaries consistently contained recoverable antral follicles and high-grade oocytes (Q1 and Q2), supporting the notion that these breeds maintain functional ovarian reserves and reduced reproductive seasonality under subtropical long-day conditions. Follicular population and ovarian activity In this study, we demonstrate that small antral follicles (≤ 2 mm) were predominant within the ovarian structure, accounting for 71.11% of total follicles. Both small (≤ 2 mm) and large (≥ 3 mm) follicle categories were proportionally represented in right and left ovaries, indicating a stable and uniform antral follicular pool. Similar follicular distributions, assessed by laparoscopy numbering, have been reported during the breeding season in Ouled Djellal ewes, representing approximately 70% of the national flock (Gharbi et al., 2012 ), suggesting that follicular recruitment remains relatively stable throughout the year. These observations align with studies showing that follicular waves continue to emerge during anestrus, although progression to preovulatory stages is limited in highly seasonal breeds (Bartlewski et al., 2011 ; Bartlewski et al., 1998 ; Evans et al., 2001 ) Under our geographical conditions, the local breeds studied, notably Ouled Djellal ewes, showed reduced photoperiodic sensitivity (Titaouine et al., 2023 ; Zidane et al., 2021 ) and exhibit a mild seasonal modulation of gonadotropins and steroids under both semi-arid (Zidane & Ababou, 2017 ) and arid or Saharan conditions (Gani & Niar, 2019 ). The persistence of follicular activity, able to induce estrus and ovulation in these ewes, likely reflects the interaction of genetic adaptation and environmental conditions, including subtropical photoperiods and seasonal nutritional variability (Dekhili, 2014 ; Joy et al., 2020 ; Taherti et al., 2016 ). Nutritional signals also interact with the photoperiodic cycle through central pathways regulating melatonin and GnRH neurosecretion (Abecia et al., 2018 ; Menassol et al., 2012 ). Moreover, an adequate nutritional status may enhance LH secretion by reducing estradiol negative feedback (Scaramuzzi et al., 2014 ), allowing Mediterranean breeds to ovulate even during anestrus (Forcada & Abecia, 2006 ). Accordingly, Ouled Djellal ewes in good body condition resume estrus earlier, exhibit shorter anestrous periods (Benyounes, 2013 ; Hadef, 2014 ), and show better adaptation to fluctuations in forage availability (Deghnouche et al., 2017 ). Despite the fact that we did not find a significant difference in the ratio of follicles per ovary between right and left ovaries, a numerical tendency toward greater follicular activity in the right ovary (54% of total follicles) was observed in our study, a phenomenon previously described in sheep (Ali & Derar, 2021 ), goats (Lyngset, 1968 ), and cattle (Karamishabankareh et al., 2015 ; Trigal et al., 2014 ). Collectively, these factors likely contribute to maintaining a functional ovarian reserve throughout the year, as supported by the oocyte recovery patterns observed in this study. Oocyte yield and morphological grading Oocyte recovery provides a direct measure of ovarian functional capacity (Souza-Fabjan et al., 2023 ). In this study, the mean recovery rate was 33.5%, with 4.40 ± 0.52 oocytes per ovary, and 45.35% classified as high-grade (Q1 + Q2). A previous study reported the same oocyte recovery rate (33.6%) in Rasa Aragonesa ewes in the Mediterranean region (Spain) during anestrus (from March to April); however, oocytes were collected in vivo using the ovum pick-up technique (OPU) following FSH pretreatment (Alberio et al., 2002 ). Comparisons with other subtropical breeds, such as Iranian Zandi ewes, highlight slight variations in recovery rates (3.4 ± 1.1 oocytes per ovary) and more high-grade oocytes (78.8%), likely due to technical differences or timing within the anestrous period (Davachi et al., 2014 ). In fact, our study was conducted during the main anestrus period (from early March to late June), whereas the study on Zandi ewes focused on the transitional anestrous period (from June to August). The influence of seasonality on oocyte competence and reproductive success in highly seasonal breeds is well established (Rosa & Bryant, 2003 ). During the breeding season, these breeds typically exhibit higher oocyte quality and improved recovery rates (Serra et al., 2021 ). In contrast, strongly seasonal breeds show a marked decline in oocyte competence during anestrus due to reduced gonadotropic support (Vazquez et al., 2010b ), resulting in decreased in vitro embryo production (Mara et al., 2013 ; Souza-Fabjan et al., 2021 ). Exogenous hormonal treatments, including FSH, eCG, hCG, melatonin, and progestins, have been widely used to enhance follicular development in seasonal breeds during the non-breeding season (Braganca et al., 2018 ; Cox et al., 2024 ; Dias et al., 2020 ; Forcada et al., 2007 ; Menchaca et al., 2018 ; Vazquez et al., 2010a ). The ability of local ewes to produce high-grade oocytes without exogenous hormonal interventions underscores their reproductive resilience and their adaptability to environmental challenges. However, the mechanisms underlying the interaction between the relatively longer photoperiod and sometimes drastic, feed availability in arid and semi-arid environments, as well as their effects on oocyte competence, remain to be elucidated. A clear functional right-sided asymmetry was observed, with the right ovary producing more oocytes (61.40% of total) and a higher proportion of high-grade oocytes (67.18% of Q1 + Q2 oocytes). This pattern has been reported in ewes (Majeed et al., 2019 ). It has been interpreted as the right ovary often exhibiting higher ovulatory activity (Ginther, 2019 ), congenital differences in follicular reserves (Dangudubiyyam & Ginther, 2019 ), and more frequent emergence of early follicular waves (Ginther & Dangudubiyyam, 2018 ). Our results extend these observations by demonstrating that this asymmetry also applies to oocytes recovered during anestrus, and their competence should be further confirmed by assessing oocyte maturation rates. Relationship between follicle size and oocyte morphology Follicle size is a key determinant of oocyte developmental competence (Paramio & Izquierdo, 2014 ). In our study, we found that sessions with a higher proportion of large follicles (≥ 3 mm) were associated with higher numbers of high-grade oocytes (Q1 + Q2) compared with sessions dominated by small follicles (≤ 2 mm). A previous study has shown that a high oocyte recovery rate is obtained from large follicles (Majeed et al., 2019 ). This pattern is consistent with reports indicating that oocytes from larger follicles exhibit more advanced cytoplasmic and nuclear maturation (Xiao et al., 2019 ), a process supported by the increased metabolic and paracrine activity of granulosa and cumulus cells via follicular fluid (Dos Santos-Neto et al., 2020 ; Passos et al., 2022 ). In contrast, cumulus oocyte complexes (COCs) derived from small antral follicles possess lower competence due to immature regulatory signaling (Varnosfaderani et al., 2020 ). It should be noted that individual oocytes were not traced to specific follicles; therefore, the contribution of each follicle size category to high-grade oocyte recovery cannot be precisely determined. Overall, the findings highlight the reproductive resilience of local Algerian ewes under subtropical conditions. Persistent antral follicles, morphologically high-grade oocytes, and right-sided ovarian asymmetry indicate strong adaptive reproductive capacity, supporting the potential for year-round application of assisted reproductive technologies (ARTs), including in vitro embryo production. Such traits offer valuable opportunities for genetic improvement and sustainable livestock production under changing climatic conditions. Like other studies using slaughterhouse-derived material, certain limitations should be acknowledged. The reproductive stage of the animals could not be determined, and variation in age, body condition, or health status may influence both the morphology and the number of oocytes recovered (Lorenzo-Torres et al., 2023 ; Souza-Fabjan et al., 2023 ), as well as potential variability due to the retrieval technique (Davachi et al., 2014 ; Majeed et al., 2019 ). In addition, the use of ovaries collected post-mortem limits the ability to directly link recovered oocytes to their follicular origin and to monitor follicular wave dynamics. Finally, oocyte quality was assessed solely based on morphological criteria. Although these criteria are widely used and predictive of developmental potential, they do not fully reflect nuclear and cytoplasmic maturation or subsequent embryo development. Functional validation through in vitro maturation, fertilization, and embryo culture would provide a more accurate assessment of oocyte developmental competence. Conclusion The findings of this study demonstrate that local Algerian ewes maintain active folliculogenesis and a functional ovarian reserve during seasonal anestrus, with evidence of right-sided ovarian asymmetry favoring oocyte production. Despite the expected photoperiod-induced reduction in reproductive activity, both the number and morphological quality of recovered oocytes remained relatively high, particularly in sessions with a greater proportion of large follicles. These results highlight the reproductive resilience and adaptive flexibility of low-seasonality breeds raised under subtropical conditions, reinforcing their suitability for year-round assisted reproductive technologies. Such traits represent a valuable biological asset for sustainable livestock production and genetic improvement strategies in the context of climatic variability. Future studies combining in vivo follicular monitoring, endocrine profiling, and molecular markers of oocyte competence are therefore required to better elucidate the mechanisms underlying this reproductive resilience and to further optimize reproductive management practices in locally adapted sheep breeds. Declarations Acknowledgements The authors sincerely thank the staff of the Laboratory of Natural Bio-Resources (LBRN) for their technical support during sample processing and analysis. We also extend our gratitude to the veterinarian and personnel at TAIBA Abattoir for their assistance with ovary collection and for providing access to the biological material. Their contributions were essential to the successful completion of this study. Author contributions M.S. conceived and planned the study, analyzed the data, and wrote the first draft of the manuscript. H.D. and L.S. contributed equally to the conception, data collection, and analysis. I.B. and M.B. primarily contributed to critical review of the manuscript. I.B and T.M. read and approved the final version of the manuscript. All authors have read and approved the final. Funding No funding was received for this study. Compliance with ethical standards This study was conducted in accordance with ethical standards for the use of animal biological materials. All ovaries were collected post-mortem from routinely slaughtered ewes at a state-approved abattoir under veterinary supervision. No animals were sacrificed specifically for this study. Data availability statement The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request. Consent for publication The authors all agree and consent to the publication of the manuscript in its current version. Conflict of interest The authors declare that the study was conducted without any conflict of interest. Data availability statement The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request. References Abecia, J. A., Forcada, F., Vazquez, M. I., Muino-Blanco, T., Cebrian-Perez, J. A., Perez-Pe, R., & Casao, A. (2018). Role of melatonin on embryo viability in sheep [Review]. Reprod Fertil Dev , 31 (1), 82-92. https://doi.org/10.1071/RD18308 Adaouri, M., M. Lebied, H. Mefti Korteby, C. Merkoune, S. Guenzet, & Sebbag, L. (2023). Évaluation des performances de reproduction et de productivité chez la race Rembi dans la région de Médéa (Algérie). Recherche Agronomique , 21 (1), 63-75 [in French], Available at: https://asjp.cerist.dz/en/article/217555. Alberio, R., Olivera, J., b, A. R., J. 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Rev. élev. méd. vét. pays trop , 74 , 193-198 [in French]. https://doi.org/10.19182/remvt.36801 Cite Share Download PDF Status: Under Review Version 1 posted Reviewers agreed at journal 12 Jan, 2026 Reviewers invited by journal 12 Jan, 2026 Editor assigned by journal 30 Dec, 2025 First submitted to journal 29 Dec, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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1","display":"","copyAsset":false,"role":"figure","size":307427,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend\u003c/p\u003e","description":"","filename":"floatimage1.png","url":"https://assets-eu.researchsquare.com/files/rs-8475129/v1/0aca0828b800ee2263628f72.png"},{"id":100263924,"identity":"a5309d1f-49c8-4eb3-8971-54f025b6b776","added_by":"auto","created_at":"2026-01-14 17:49:01","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":177143,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend\u003c/p\u003e","description":"","filename":"floatimage2.png","url":"https://assets-eu.researchsquare.com/files/rs-8475129/v1/abae6be87a8ca2e0dcc49e5a.png"},{"id":100263921,"identity":"dac3b7d8-e1a0-4226-831f-6058974fb054","added_by":"auto","created_at":"2026-01-14 17:49:01","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":251599,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend\u003c/p\u003e","description":"","filename":"floatimage3.png","url":"https://assets-eu.researchsquare.com/files/rs-8475129/v1/0eac14fdc2276a84dea975a3.png"},{"id":100383625,"identity":"f0ae0899-8c98-461a-a188-e208d546a448","added_by":"auto","created_at":"2026-01-16 10:47:44","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1889135,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8475129/v1/30a63815-9de8-4bff-bb28-3c5a688bcdd7.pdf"}],"financialInterests":"","formattedTitle":"Reproductive adaptation of local Algerian ewes to seasonal constraints: follicular dynamics and oocyte morphology during anestrus","fulltext":[{"header":"Introduction","content":"\u003cp\u003eSheep exhibit marked reproductive seasonality, primarily regulated by photoperiodic cues that modulate ovarian function through neuroendocrine pathways (Kopycinska et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; Wyse et al., \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Day length is transduced into melatonin rhythms by the pineal gland, which in turn regulates pulsatile secretion of gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH), driving follicular growth and ovulation (Chemineau et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Clarke et al., \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Nestor et al., \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Typically, most breeds are sexually active during short-day periods (autumn to winter), and enter seasonal anestrus during long-day periods (spring to summer), characterized by reduced LH pulse frequency, incomplete follicular development, and absence of ovulation (Dardente et al., \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Goodman et al., \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Seekallu et al., \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2010b\u003c/span\u003e). Structural changes in the ovarian stroma may also create a biomechanical environment unfavorable for ovulation during anestrus (Grosbois et al., \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2025\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eComparative studies indicate a latitudinal gradient in reproductive seasonality and notable between-breed variability. Breeds from equatorial, tropical, or subtropical regions often display reduced photoperiodic influence and maintain ovarian cyclicity and estrous activity for most of the year (Pampori et al., \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Rosa \u0026amp; Bryant, \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Serranito et al., \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn Algeria, local breeds such as Ouled Djellal, Rembi, Hamra, and D\u0026rsquo;Man\u0026mdash; which together represent the majority of the national sheep population\u0026mdash;exhibit low reproductive seasonality, prolonged estrous activity, residual ovarian function during anestrus, and the capacity for multiple lambing seasons (Adaouri et al., \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Boubekeur et al., \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Meddah et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2024\u003c/span\u003e; Taherti et al., 2024), reflecting long-term adaptation to arid and semi-arid environments (Gani \u0026amp; Niar, \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Zidane et al., \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). These traits contribute to reproductive resilience, which is essential for sustaining local livestock production under challenging subtropical conditions.\u003c/p\u003e \u003cp\u003eDespite this relative resistance to seasonality, detailed studies of ovarian function during anestrus remain scarce in Algerian ewes. Most reports focus on estrous behavior, lambing intervals, or general reproductive performance, whereas follicular development and oocyte competence remain poorly characterized. These traits are assessable only via morphological evaluation, although they are essential for understanding low-seasonality adaptations and guiding reproductive management (Simoes et al., \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The present study aimed to characterize follicular dynamics and oocyte morphology in local Algerian ewes during anestrus, with particular attention to ovarian asymmetry and the relationship between follicle size and oocyte morphological grade, providing insights into adaptive reproductive strategies in locally adapted breeds.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy area\u003c/h2\u003e \u003cp\u003eThe study was conducted at the Laboratory of Natural Bio-Resources (LBRN), Hassiba Ben Bouali University of Chlef, situated in northern Algeria (36\u0026deg;09\u0026prime; N, 1\u0026deg;20\u0026prime; E), a semi-arid subtropical region. Summers are hot and dry, winters cool and partly cloudy, with annual temperatures ranging 6\u0026ndash;37\u0026deg;C. The wet season lasts September to June, and day length varies from 9 hours 45 minutes (winter solstice) to 14 hours 30 minutes (summer solstice), defining short-day (autumn\u0026ndash;winter) and long-day (spring\u0026ndash;summer) photoperiods. These seasonal and thermal conditions present environmental challenges that influence reproductive performance, making local ewes suitable models for studying reproductive adaptability.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eAnimals and sampling\u003c/h3\u003e\n\u003cp\u003eA total of 124 ovaries from 62 local ewes, mostly Ouled Djellal, were collected post-mortem from a state-approved abattoir during 15 weekly sessions from early March to late June, corresponding to the long-day photoperiod and main seasonal anestrous period. Animals\u0026ndash;with unknown age and body weight\u0026ndash;were reared under extensive semi-arid farming systems.\u003c/p\u003e\n\u003ch3\u003eOvarian collection and follicular assessment\u003c/h3\u003e\n\u003cp\u003eImmediately post-slaughter, the uteri were removed and the ovaries were excised, trimmed, and disinfected with 70% ethanol. Each ovary was placed in a labeled container (identified as right or left) containing saline (0.9% NaCl) supplemented with 50 \u0026micro;g/mL gentamicin. Containers were maintained at 35\u0026ndash;37\u0026deg;C during transport and delivered to the laboratory within approximately 2 hours, with temperature preserved using a water bath inside a cooler (Izquierdo et al., \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Upon arrival, ovaries were rinsed with warm saline, and visible surface follicles were counted under a stereomicroscope. Antral follicles were classified as small (\u0026le;\u0026thinsp;2 mm) or large (\u0026ge;\u0026thinsp;3 mm) (Paramio \u0026amp; Izquierdo, \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Total follicle counts and follicle-to-ovary ratios were calculated for right and left ovaries separately.\u003c/p\u003e\n\u003ch3\u003eOocyte recovery and grading\u003c/h3\u003e\n\u003cp\u003eCumulus\u0026ndash;oocyte complexes (COCs) were manually punctured separately from visible follicles using a 20G needle attached to a 5 mL syringe containing 0.5\u0026ndash;1 mL phosphate-buffered saline (PBS, 30\u0026ndash;35\u0026deg;C) (Mondal et al., \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). COCs were isolated and morphologically graded based on cumulus cell investment and cytoplasmic homogeneity (Fig.\u0026nbsp;1): Q1 (Excellent): \u0026ge; 3 cumulus cell layers, homogeneous cytoplasm; Q2 (Good): 2\u0026ndash;3 layers, slightly granulated cytoplasm; Q3 (Fair): few cumulus cells, irregular cytoplasm; Q4 (Poor): denuded or abnormal oocytes (Almeida et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Only high-grade oocytes (combined Q1\u0026thinsp;+\u0026thinsp;Q2) were considered suitable for in vitro maturation procedures. Oocyte-to-follicle ratios were calculated at the ovarian level to evaluate overall follicular efficiency. These ratios represent global estimations, as individual matching between retrieved oocytes and follicle size classes was not possible.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eData were analyzed using GraphPad Prism version 9.5.1 (GraphPad Software, San Diego, USA). Right and left ovaries were treated as independent samples. Descriptive data are presented as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SEM for normally distributed variables and median [IQR] for non-normal variables. Comparisons between right and left ovaries were performed using the Mann\u0026ndash;Whitney U test (one-tailed when a directional hypothesis applied), while within-ovary paired comparisons used the Wilcoxon signed-rank test. Statistical significance was set at \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eDescriptive data of the collected ovaries\u003c/h2\u003e \u003cp\u003eDuring the long-day photoperiod (from early March to late June), 124 ovaries were collected from abattoir-derived local Algerian ewes over 15 sessions, averaging 8.27\u0026thinsp;\u0026plusmn;\u0026thinsp;1.86 ovaries per session. Transport to the laboratory was completed within 120\u0026thinsp;\u0026plusmn;\u0026thinsp;12 minutes while maintaining physiological temperature. Right and left ovaries were equally represented, allowing balanced comparison of ovarian activity during seasonal anestrus (Table\u0026nbsp;1).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Taba\" border=\"1\"\u003e \u003ccolgroup cols=\"9\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"8\" nameend=\"c8\" namest=\"c1\"\u003e \u003cp\u003eTable\u0026nbsp;1 Descriptive data of ovary collection, transport conditions, and follicular\u0026ndash;oocyte yield in Algerian local ewes.\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eParameter\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eOverall\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eRight ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eLeft ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003eRight vs Left\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003e(p-value)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSampling sessions (n)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTransport time (min)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e120\u0026thinsp;\u0026plusmn;\u0026thinsp;12.42\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal ovaries collected (Sum)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e124\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e62\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e62\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOvaries per session\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.27\u0026thinsp;\u0026plusmn;\u0026thinsp;1.86\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e4.13\u0026thinsp;\u0026plusmn;\u0026thinsp;0.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e4.13\u0026thinsp;\u0026plusmn;\u0026thinsp;0.93\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal follicles punctured (Sum)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1284\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e693\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e591\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFollicles per ovary\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9.65\u0026thinsp;\u0026plusmn;\u0026thinsp;1.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e9.91\u0026thinsp;\u0026plusmn;\u0026thinsp;1.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e9.43\u0026thinsp;\u0026plusmn;\u0026thinsp;1.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal oocytes collected (Sum)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e430\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e264\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e166\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOocytes per ovary\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4.40\u0026thinsp;\u0026plusmn;\u0026thinsp;0.52\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.63\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.56\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"8\" nameend=\"c8\" namest=\"c1\"\u003e \u003cp\u003eNote. Values are expressed as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SEM. \u0026ldquo;Sum\u0026rdquo; refers to the absolute number. Comparisons between right and left ovaries were performed using the Mann\u0026ndash;Whitney U test. ns\u0026thinsp;=\u0026thinsp;not significant; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eFollicle counts and size distributions\u003c/h3\u003e\n\u003cp\u003eA total of 1284 antral follicles were manually punctured from all ovaries, corresponding to a median of 44 [23\u0026ndash;100] and a mean of 9.65\u0026thinsp;\u0026plusmn;\u0026thinsp;1.12 follicles per ovary. The right ovary contained slightly more follicles (693; median 23 [11\u0026ndash;53]; 54% of total follicles) than the left (591; median 20 [13\u0026ndash;47]; 46% of total follicles), although the difference was not statistically significant (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026ge;\u0026thinsp;0.05) (Table\u0026nbsp;2). In addition, no significant difference in the mean follicle-to-ovary ratio was observed between the right (9.91\u0026thinsp;\u0026plusmn;\u0026thinsp;1.29) and left (9.43\u0026thinsp;\u0026plusmn;\u0026thinsp;1.07) ovaries (Table\u0026nbsp;1), indicating a uniform antral follicle pool.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabb\" border=\"1\"\u003e \u003ccolgroup cols=\"11\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"11\" nameend=\"c11\" namest=\"c1\"\u003e \u003cp\u003eTable\u0026nbsp;2 Follicle counts and size distribution in right and left ovaries.\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eParameter\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eOverall\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eRight ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eLeft ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003eRight vs Left\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eSum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003e(p-value)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal follicles\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1284\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e44 [23\u0026ndash;100]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e23 [11\u0026ndash;53]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e20 [13\u0026ndash;47]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSmall follicles\u0026thinsp;\u0026le;\u0026thinsp;2 mm\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e913\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e32 [16\u0026ndash;89]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e16 [6\u0026ndash;46]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e16 [10\u0026ndash;43]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLarge follicles\u0026thinsp;\u0026ge;\u0026thinsp;3 mm\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e371\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e11 [5\u0026ndash;25]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e5 [2\u0026ndash;12]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e4 [2\u0026ndash;12]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSmall-to-large ratio\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u0026ndash;\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3.1 [1.5\u0026ndash;6.6]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e3.33 [1.5\u0026ndash;6]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"10\" nameend=\"c10\" namest=\"c1\"\u003e \u003cp\u003eNote. Data are presented as median [IQR]. \u0026ldquo;Sum\u0026rdquo; refers to the absolute number of follicles collected from all ovaries combined. Comparisons between right and left ovaries were performed using the Mann\u0026ndash;Whitney U test. ns\u0026thinsp;=\u0026thinsp;non-significant; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAnalysis of follicle size revealed that small follicles (\u0026le;\u0026thinsp;2 mm) dominated the ovarian structure (913; median 32 [16\u0026ndash;89]; 71.1% of total follicles) compared with large follicles (\u0026ge;\u0026thinsp;3 mm) (371; median 11 [5\u0026ndash;25]; 28.9% of total follicles; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; Wilcoxon signed-rank test), confirming the predominance of basal follicular recruitment (Fig.\u0026nbsp;2). This pattern was consistent across both ovaries (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01). However, no significant right\u0026ndash;left differences were observed between follicle size categories, supporting the presence of a stable follicular pool (Table\u0026nbsp;2).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eOocyte yield and morphological grading\u003c/h2\u003e \u003cp\u003eA total of 430 cumulus-oocyte complexes (COCs) were recovered (median 22 [16.5\u0026ndash;36]), corresponding to a mean of 4.40\u0026thinsp;\u0026plusmn;\u0026thinsp;0.52 oocytes per ovary and an oocyte recovery rate of 33.5% from all follicles. The right ovary yielded significantly more COCs (264; median 12 [10\u0026ndash;18]; 61.4% of total oocytes) than the left ovary (166; median 10 [6.5\u0026ndash;13]; 38.60% of total oocytes; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04) (Table\u0026nbsp;3). This right-sided predominance was also observed in the mean oocyte-to-ovary ratio (right: 5.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.63 vs. left: 3.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.56; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02), indicating a clear functional asymmetry despite similar total follicle counts between the ovaries (Table\u0026nbsp;1).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabc\" border=\"1\"\u003e \u003ccolgroup cols=\"11\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"10\" nameend=\"c10\" namest=\"c1\"\u003e \u003cp\u003eTable\u0026nbsp;3 Comparison of total oocyte number and their morphology grades (Q1\u0026ndash;Q4) between right and left ovaries.\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eParameter\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eOverall\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eRight ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eLeft ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003eRight vs Left\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cem\u003eSum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003e(p-value)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal oocytes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e430\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e22 [16.5\u0026ndash;36]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e12 [10\u0026ndash;18]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e10 [6.5\u0026ndash;13]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQ1 (Excellent)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e126\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e7 [3.5\u0026ndash;10.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e4 [2.5\u0026ndash;6.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e2 [0.5\u0026ndash;5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.03\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQ2 (Good)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e69\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e3 [1\u0026ndash;6.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e2 [1\u0026ndash;3.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e1 [0\u0026ndash;2]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQ3 (Fair)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e102\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e5 [3\u0026ndash;8]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3 [2\u0026ndash;5.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e3 [1\u0026ndash;4.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQ4 (Poor)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e133\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e8 [4.5\u0026ndash;12]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e4 [3\u0026ndash;6]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e3 [1\u0026ndash;5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHigh-grade (Q1\u0026thinsp;+\u0026thinsp;Q2)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e195\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e10 [6\u0026ndash;15]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e7 [4\u0026ndash;8]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e3 [1.5\u0026ndash;6.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLow-grade (Q3\u0026thinsp;+\u0026thinsp;Q4)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e235\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13 [9\u0026ndash;21]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e7 [4.5\u0026ndash;12]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e6 [4\u0026ndash;7.5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"10\" nameend=\"c10\" namest=\"c1\"\u003e \u003cp\u003eNote. Data are presented as median [IQR]. \u0026ldquo;Sum\u0026rdquo; refers to the absolute number of oocytes collected from all ovaries combined. Comparisons between right and left ovaries were performed using the Mann\u0026ndash;Whitney U test. ns\u0026thinsp;=\u0026thinsp;non-significant; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAssessment of COC quality indicated that morphologically high-grade oocytes (Q1 and Q2) were significantly higher in the right ovary (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05; Mann\u0026ndash;Whitney U test) (Table\u0026nbsp;3). A total of 195 high-grade oocytes (combined Q1\u0026thinsp;+\u0026thinsp;Q2) were collected (median 10 [6\u0026ndash;15]), accounting for 45.35% of total oocytes. This category of oocytes was more abundant on the right side than on the left (median 7 [4\u0026ndash;8] vs. 3 [1.5\u0026ndash;6.5]; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02), accounting for 30.46% vs. 14.88% of total oocytes recovered, respectively. Considered individually, the number of excellent-grade oocytes (Q1) (median 4 [2.5\u0026ndash;6.5] right vs. 2 [0.5\u0026ndash;5] left) and good-grade oocytes (Q2) (median 2 [1\u0026ndash;3.5] right vs. 1 [0\u0026ndash;2] left) were also significantly greater on the right (\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05). In contrast, morphologically low-grade oocytes (Q3 and Q4), whether considered individually or combined (Q3\u0026thinsp;+\u0026thinsp;Q4), showed no significant differences between the two sides.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eOocyte quality according to follicle size\u003c/h2\u003e \u003cp\u003eFunctional asymmetry became evident when oocyte recovery was normalized to follicle number. Because oocytes could not be individually assigned to their follicle of origin, these ratios reflect ovarian-level (session-level) associations between follicle size distribution and oocyte morphology. Accordingly, the ratios do not represent individual follicle\u0026ndash;oocyte correspondence (Table\u0026nbsp;4).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabd\" border=\"1\"\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"5\" nameend=\"c5\" namest=\"c1\"\u003e \u003cp\u003eTable\u0026nbsp;4 Within-ovary comparisons of follicular and oocyte ratios in Algerian local ewes during seasonal anestrus.\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eParameter\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eOverall\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eRight ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eLeft ovary\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003eRight vs Left\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003e(p-value)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal follicles-to-ovary\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9.65\u0026thinsp;\u0026plusmn;\u0026thinsp;1.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9.91\u0026thinsp;\u0026plusmn;\u0026thinsp;1.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e9.43\u0026thinsp;\u0026plusmn;\u0026thinsp;1.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSmall (\u0026le;\u0026thinsp;2 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e7.33\u0026thinsp;\u0026plusmn;\u0026thinsp;0.98\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e7.64\u0026thinsp;\u0026plusmn;\u0026thinsp;1.11\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e7.05\u0026thinsp;\u0026plusmn;\u0026thinsp;0.96\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLarge (\u0026ge;\u0026thinsp;3 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.47\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.58\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.38\u0026thinsp;\u0026plusmn;\u0026thinsp;0.44\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ens\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal oocytes-to-ovary\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4.40\u0026thinsp;\u0026plusmn;\u0026thinsp;0.52\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.63\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e3.50\u0026thinsp;\u0026plusmn;\u0026thinsp;0.56\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHigh-grade (Q1\u0026thinsp;+\u0026thinsp;Q2)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.93\u0026thinsp;\u0026plusmn;\u0026thinsp;0.31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.60\u0026thinsp;\u0026plusmn;\u0026thinsp;0.41\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.36\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u0026thinsp;\u0026lt;\u003c/em\u003e\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLow-grade (Q3\u0026thinsp;+\u0026thinsp;Q4)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2.47\u0026thinsp;\u0026plusmn;\u0026thinsp;0.37\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.72\u0026thinsp;\u0026plusmn;\u0026thinsp;0.39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.23\u0026thinsp;\u0026plusmn;\u0026thinsp;0.44\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003ens\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal oocytes-to-follicles\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.63\u0026thinsp;\u0026plusmn;\u0026thinsp;0.08\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.43\u0026thinsp;\u0026plusmn;\u0026thinsp;0.08\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSmall (\u0026le;\u0026thinsp;2 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.73\u0026thinsp;\u0026plusmn;\u0026thinsp;0.10\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.88\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.62\u0026thinsp;\u0026plusmn;\u0026thinsp;0.13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLarge (\u0026ge;\u0026thinsp;3 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3.46\u0026thinsp;\u0026plusmn;\u0026thinsp;1.17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.22\u0026thinsp;\u0026plusmn;\u0026thinsp;0.45\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.03\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHigh-grade oocytes-to-follicles\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.22\u0026thinsp;\u0026plusmn;\u0026thinsp;0.03\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.31\u0026thinsp;\u0026plusmn;\u0026thinsp;0.05\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.14\u0026thinsp;\u0026plusmn;\u0026thinsp;0.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSmall (\u0026le;\u0026thinsp;2 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.05\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.42\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.23\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLarge (\u0026ge;\u0026thinsp;3 mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.36\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.58\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"5\" nameend=\"c5\" namest=\"c1\"\u003e \u003cp\u003eNote. Data are expressed as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SEM. Differences between right and left ovaries were analyzed using the Mann\u0026ndash;Whitney U test. ns\u0026thinsp;=\u0026thinsp;non-significant; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe mean total oocyte recovery appears to be higher in large follicles (\u0026ge;\u0026thinsp;3 mm) than in small follicles (\u0026le;\u0026thinsp;2 mm) (3.46\u0026thinsp;\u0026plusmn;\u0026thinsp;0.17 vs. 0.73\u0026thinsp;\u0026plusmn;\u0026thinsp;0.10; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; Wilcoxon signed-rank test). Moreover, the right ovary displayed a higher oocyte-to-follicle ratio in both small (right: 0.88\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14 vs. left: 0.62\u0026thinsp;\u0026plusmn;\u0026thinsp;0.13; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04) and large follicles (right: 3.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57 vs. left: 2.22\u0026thinsp;\u0026plusmn;\u0026thinsp;0.45; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.03). This ratio was higher in large follicles compared with small follicles, notably on the right side (3.09\u0026thinsp;\u0026plusmn;\u0026thinsp;0.57 vs. 0.88\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001; Wilcoxon signed-rank test) (Table\u0026nbsp;4).\u003c/p\u003e \u003cp\u003eSimilarly, the mean total high-grade (Q1\u0026thinsp;+\u0026thinsp;Q2) oocyte-to-follicle ratios were higher in large follicles (\u0026ge;\u0026thinsp;3 mm) than in small follicles (\u0026le;\u0026thinsp;2 mm) (1.27\u0026thinsp;\u0026plusmn;\u0026thinsp;0.36 vs. 0.32\u0026thinsp;\u0026plusmn;\u0026thinsp;0.05; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.0001; Wilcoxon signed-rank test). When ratios of high-grade oocytes were expressed according to follicle size in both ovaries, the right ovary yielded higher proportions of high-grade oocytes in both large follicles (right: 1.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 vs. left: 0.58\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01) and small follicles (right: 0.42\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07 vs. left: 0.23\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.01; Mann\u0026ndash;Whitney U test). Moreover, high-grade oocytes appear to be more frequently recovered from the right ovary, particularly from large follicles, compared with small follicles (1.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 vs. 0.42\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001; Wilcoxon signed-rank test) (Fig.\u0026nbsp;3).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eThis study provides the first comprehensive characterization of follicular dynamics and oocyte morphology in local Algerian ewes during seasonal anestrus, revealing adaptive reproductive traits not previously documented in North African breeds. Despite the expected photoperiod-driven reduction in ovarian activity, ovaries consistently contained recoverable antral follicles and high-grade oocytes (Q1 and Q2), supporting the notion that these breeds maintain functional ovarian reserves and reduced reproductive seasonality under subtropical long-day conditions.\u003c/p\u003e \u003cdiv id=\"Sec14\" class=\"Section2\"\u003e \u003ch2\u003eFollicular population and ovarian activity\u003c/h2\u003e \u003cp\u003eIn this study, we demonstrate that small antral follicles (\u0026le;\u0026thinsp;2 mm) were predominant within the ovarian structure, accounting for 71.11% of total follicles. Both small (\u0026le;\u0026thinsp;2 mm) and large (\u0026ge;\u0026thinsp;3 mm) follicle categories were proportionally represented in right and left ovaries, indicating a stable and uniform antral follicular pool. Similar follicular distributions, assessed by laparoscopy numbering, have been reported during the breeding season in Ouled Djellal ewes, representing approximately 70% of the national flock (Gharbi et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), suggesting that follicular recruitment remains relatively stable throughout the year. These observations align with studies showing that follicular waves continue to emerge during anestrus, although progression to preovulatory stages is limited in highly seasonal breeds (Bartlewski et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Bartlewski et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Evans et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2001\u003c/span\u003e)\u003c/p\u003e \u003cp\u003eUnder our geographical conditions, the local breeds studied, notably Ouled Djellal ewes, showed reduced photoperiodic sensitivity (Titaouine et al., \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Zidane et al., \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) and exhibit a mild seasonal modulation of gonadotropins and steroids under both semi-arid (Zidane \u0026amp; Ababou, \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2017\u003c/span\u003e) and arid or Saharan conditions (Gani \u0026amp; Niar, \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). The persistence of follicular activity, able to induce estrus and ovulation in these ewes, likely reflects the interaction of genetic adaptation and environmental conditions, including subtropical photoperiods and seasonal nutritional variability (Dekhili, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Joy et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Taherti et al., \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eNutritional signals also interact with the photoperiodic cycle through central pathways regulating melatonin and GnRH neurosecretion (Abecia et al., \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Menassol et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Moreover, an adequate nutritional status may enhance LH secretion by reducing estradiol negative feedback (Scaramuzzi et al., \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), allowing Mediterranean breeds to ovulate even during anestrus (Forcada \u0026amp; Abecia, \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). Accordingly, Ouled Djellal ewes in good body condition resume estrus earlier, exhibit shorter anestrous periods (Benyounes, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Hadef, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), and show better adaptation to fluctuations in forage availability (Deghnouche et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eDespite the fact that we did not find a significant difference in the ratio of follicles per ovary between right and left ovaries, a numerical tendency toward greater follicular activity in the right ovary (54% of total follicles) was observed in our study, a phenomenon previously described in sheep (Ali \u0026amp; Derar, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), goats (Lyngset, \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1968\u003c/span\u003e), and cattle (Karamishabankareh et al., \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Trigal et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eCollectively, these factors likely contribute to maintaining a functional ovarian reserve throughout the year, as supported by the oocyte recovery patterns observed in this study.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eOocyte yield and morphological grading\u003c/h2\u003e \u003cp\u003eOocyte recovery provides a direct measure of ovarian functional capacity (Souza-Fabjan et al., \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). In this study, the mean recovery rate was 33.5%, with 4.40\u0026thinsp;\u0026plusmn;\u0026thinsp;0.52 oocytes per ovary, and 45.35% classified as high-grade (Q1\u0026thinsp;+\u0026thinsp;Q2). A previous study reported the same oocyte recovery rate (33.6%) in Rasa Aragonesa ewes in the Mediterranean region (Spain) during anestrus (from March to April); however, oocytes were collected in vivo using the ovum pick-up technique (OPU) following FSH pretreatment (Alberio et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Comparisons with other subtropical breeds, such as Iranian Zandi ewes, highlight slight variations in recovery rates (3.4\u0026thinsp;\u0026plusmn;\u0026thinsp;1.1 oocytes per ovary) and more high-grade oocytes (78.8%), likely due to technical differences or timing within the anestrous period (Davachi et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). In fact, our study was conducted during the main anestrus period (from early March to late June), whereas the study on Zandi ewes focused on the transitional anestrous period (from June to August).\u003c/p\u003e \u003cp\u003eThe influence of seasonality on oocyte competence and reproductive success in highly seasonal breeds is well established (Rosa \u0026amp; Bryant, \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2003\u003c/span\u003e). During the breeding season, these breeds typically exhibit higher oocyte quality and improved recovery rates (Serra et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In contrast, strongly seasonal breeds show a marked decline in oocyte competence during anestrus due to reduced gonadotropic support (Vazquez et al., \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2010b\u003c/span\u003e), resulting in decreased in vitro embryo production (Mara et al., \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Souza-Fabjan et al., \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Exogenous hormonal treatments, including FSH, eCG, hCG, melatonin, and progestins, have been widely used to enhance follicular development in seasonal breeds during the non-breeding season (Braganca et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Cox et al., \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2024\u003c/span\u003e; Dias et al., \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Forcada et al., \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Menchaca et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Vazquez et al., \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2010a\u003c/span\u003e). The ability of local ewes to produce high-grade oocytes without exogenous hormonal interventions underscores their reproductive resilience and their adaptability to environmental challenges. However, the mechanisms underlying the interaction between the relatively longer photoperiod and sometimes drastic, feed availability in arid and semi-arid environments, as well as their effects on oocyte competence, remain to be elucidated.\u003c/p\u003e \u003cp\u003eA clear functional right-sided asymmetry was observed, with the right ovary producing more oocytes (61.40% of total) and a higher proportion of high-grade oocytes (67.18% of Q1\u0026thinsp;+\u0026thinsp;Q2 oocytes). This pattern has been reported in ewes (Majeed et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). It has been interpreted as the right ovary often exhibiting higher ovulatory activity (Ginther, \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), congenital differences in follicular reserves (Dangudubiyyam \u0026amp; Ginther, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and more frequent emergence of early follicular waves (Ginther \u0026amp; Dangudubiyyam, \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Our results extend these observations by demonstrating that this asymmetry also applies to oocytes recovered during anestrus, and their competence should be further confirmed by assessing oocyte maturation rates.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eRelationship between follicle size and oocyte morphology\u003c/h2\u003e \u003cp\u003eFollicle size is a key determinant of oocyte developmental competence (Paramio \u0026amp; Izquierdo, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). In our study, we found that sessions with a higher proportion of large follicles (\u0026ge;\u0026thinsp;3 mm) were associated with higher numbers of high-grade oocytes (Q1\u0026thinsp;+\u0026thinsp;Q2) compared with sessions dominated by small follicles (\u0026le;\u0026thinsp;2 mm). A previous study has shown that a high oocyte recovery rate is obtained from large follicles (Majeed et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). This pattern is consistent with reports indicating that oocytes from larger follicles exhibit more advanced cytoplasmic and nuclear maturation (Xiao et al., \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), a process supported by the increased metabolic and paracrine activity of granulosa and cumulus cells via follicular fluid (Dos Santos-Neto et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Passos et al., \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). In contrast, cumulus oocyte complexes (COCs) derived from small antral follicles possess lower competence due to immature regulatory signaling (Varnosfaderani et al., \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). It should be noted that individual oocytes were not traced to specific follicles; therefore, the contribution of each follicle size category to high-grade oocyte recovery cannot be precisely determined.\u003c/p\u003e \u003cp\u003eOverall, the findings highlight the reproductive resilience of local Algerian ewes under subtropical conditions. Persistent antral follicles, morphologically high-grade oocytes, and right-sided ovarian asymmetry indicate strong adaptive reproductive capacity, supporting the potential for year-round application of assisted reproductive technologies (ARTs), including in vitro embryo production. Such traits offer valuable opportunities for genetic improvement and sustainable livestock production under changing climatic conditions. Like other studies using slaughterhouse-derived material, certain limitations should be acknowledged. The reproductive stage of the animals could not be determined, and variation in age, body condition, or health status may influence both the morphology and the number of oocytes recovered (Lorenzo-Torres et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Souza-Fabjan et al., \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), as well as potential variability due to the retrieval technique (Davachi et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Majeed et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). In addition, the use of ovaries collected post-mortem limits the ability to directly link recovered oocytes to their follicular origin and to monitor follicular wave dynamics. Finally, oocyte quality was assessed solely based on morphological criteria. Although these criteria are widely used and predictive of developmental potential, they do not fully reflect nuclear and cytoplasmic maturation or subsequent embryo development. Functional validation through in vitro maturation, fertilization, and embryo culture would provide a more accurate assessment of oocyte developmental competence.\u003c/p\u003e \u003c/div\u003e"},{"header":"Conclusion","content":"\u003cp\u003eThe findings of this study demonstrate that local Algerian ewes maintain active folliculogenesis and a functional ovarian reserve during seasonal anestrus, with evidence of right-sided ovarian asymmetry favoring oocyte production. Despite the expected photoperiod-induced reduction in reproductive activity, both the number and morphological quality of recovered oocytes remained relatively high, particularly in sessions with a greater proportion of large follicles. These results highlight the reproductive resilience and adaptive flexibility of low-seasonality breeds raised under subtropical conditions, reinforcing their suitability for year-round assisted reproductive technologies. Such traits represent a valuable biological asset for sustainable livestock production and genetic improvement strategies in the context of climatic variability. Future studies combining in vivo follicular monitoring, endocrine profiling, and molecular markers of oocyte competence are therefore required to better elucidate the mechanisms underlying this reproductive resilience and to further optimize reproductive management practices in locally adapted sheep breeds.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u0026nbsp;\u003c/strong\u003eThe authors sincerely thank the staff of the Laboratory of Natural Bio-Resources (LBRN) for their technical support during sample processing and analysis. We also extend our gratitude to the veterinarian and personnel at TAIBA Abattoir for their assistance with ovary collection and for providing access to the biological material. Their contributions were essential to the successful completion of this study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor contributions\u0026nbsp;\u003c/strong\u003eM.S. conceived and planned the study, analyzed the data, and wrote the first draft of the manuscript. H.D. and L.S. contributed equally to the conception, data collection, and analysis. I.B. and M.B. primarily contributed to critical review of the manuscript. I.B and T.M. read and approved the final version of the manuscript. All authors have read and approved the final.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u0026nbsp;\u003c/strong\u003eNo funding was received for this study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompliance with ethical standards\u003c/strong\u003e This study was conducted in accordance with ethical standards for the use of animal biological materials. All ovaries were collected post-mortem from routinely slaughtered ewes at a state-approved abattoir under veterinary supervision. No animals were sacrificed specifically for this study.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability statement\u0026nbsp;\u003c/strong\u003eThe datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e The authors all agree and consent to the publication of the manuscript in its current version.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e The authors declare that the study was conducted without any conflict of interest.\u003c/p\u003e\u003ch2\u003eData availability statement\u003c/h2\u003e \u003cp\u003eThe datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAbecia, J. A., Forcada, F., Vazquez, M. 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Seasonal hormonal variations of Ouled Djellal ewes in the region of Chlef, Algeria. \u003cem\u003eLRRD\u003c/em\u003e,\u003cem\u003e 29\u003c/em\u003e, 12 [in French], Available at: https://www.lrrd.org/lrrd29/12/azdi29239.html.\u003c/li\u003e\n\u003cli\u003eZidane, A., M. Taherti, M., L. Gadouche, L., S. Metlef, S., \u0026amp; A. Ababou. (2021). Variations saisonni\u0026egrave;res des performances de reproduction des brebis Ouled Djellal dans la r\u0026eacute;gion de Chlef, Alg\u0026eacute;rie. \u003cem\u003eRev. élev. méd. vét. pays trop\u003c/em\u003e,\u003cem\u003e 74\u003c/em\u003e, 193-198 [in French]. https://doi.org/10.19182/remvt.36801\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":true,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"tropical-animal-health-and-production","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"trop","sideBox":"Learn more about [Tropical Animal Health and Production](https://www.springer.com/journal/11250)","snPcode":"11250","submissionUrl":"https://submission.nature.com/new-submission/11250/3","title":"Tropical Animal Health and Production","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"subtropical environment, ewes, anestrus, reproductive resilience, antral follicles, oocyte morphology","lastPublishedDoi":"10.21203/rs.3.rs-8475129/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8475129/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eSeasonal anestrus in ewes is typically associated with reduced ovarian activity due to photoperiod-driven reduction of gonadotropin secretion. However, locally adapted sheep breeds raised under subtropical conditions may exhibit adaptive reproductive mechanisms that mitigate this seasonal constraint. This study is the first in Algeria to evaluate follicular dynamics, oocyte yield, and oocyte morphology in local ewes during the anestrous period. A total of 124 ovaries were collected from abattoir-derived ewes between March and June. Visible follicles were classified as small (\u0026le;\u0026thinsp;2 mm) or large (\u0026ge;\u0026thinsp;3 mm), and recovered oocytes were morphologically graded (Q1\u0026ndash;Q4). Overall, 1,284 follicles and 430 oocytes were obtained. Ovarian examination revealed a predominance of small antral follicles (median 32 [16\u0026ndash;89] vs. 11 [5\u0026ndash;25]; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01), with no significant difference in total follicle numbers between right and left ovaries (median 23 [11\u0026ndash;53] vs. 20 [13\u0026ndash;47]; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026ge;\u0026thinsp;0.05). In contrast, a significant right-sided asymmetry was observed in oocyte recovery (median 12 [10\u0026ndash;18] vs. 10 [6.5\u0026ndash;13]; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.04), particularly for high-grade oocytes (Q1\u0026thinsp;+\u0026thinsp;Q2) (median 7 [4\u0026ndash;8] vs. 3 [1.5\u0026ndash;6.5]; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.02). Moreover, higher high-grade oocyte-to-follicle ratios were observed at the ovarian level in ovaries characterized by a greater proportion of large follicles, particularly in the right ovary (1.52\u0026thinsp;\u0026plusmn;\u0026thinsp;0.29 vs. 0.42\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07; \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001). These findings demonstrate that local Algerian ewes maintain active follicular development and produce high morphological grade oocytes during seasonal anestrus, reflecting adaptive reproductive flexibility under subtropical environmental conditions. This resilience supports the potential year-round application of assisted reproductive technologies in locally adapted sheep production systems.\u003c/p\u003e","manuscriptTitle":"Reproductive adaptation of local Algerian ewes to seasonal constraints: follicular dynamics and oocyte morphology during anestrus","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-01-14 17:48:57","doi":"10.21203/rs.3.rs-8475129/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"reviewerAgreed","content":"","date":"2026-01-13T00:10:37+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-01-12T15:44:58+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-12-31T04:15:38+00:00","index":"","fulltext":""},{"type":"submitted","content":"Tropical Animal Health and Production","date":"2025-12-30T03:43:54+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"tropical-animal-health-and-production","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"trop","sideBox":"Learn more about [Tropical Animal Health and Production](https://www.springer.com/journal/11250)","snPcode":"11250","submissionUrl":"https://submission.nature.com/new-submission/11250/3","title":"Tropical Animal Health and Production","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"9515b2ef-d197-4046-88ff-5fbf8488c75b","owner":[],"postedDate":"January 14th, 2026","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-04-09T13:44:29+00:00","versionOfRecord":[],"versionCreatedAt":"2026-01-14 17:48:57","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-8475129","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8475129","identity":"rs-8475129","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}