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Intra-bull semen quality variationTo understand variation in bull semen quality, we assessed 1271 ejaculates from 79 different bulls (11 different breeds) housed at Rockhampton stud farm, in the state of Queensland, Australia, over a period of 5 years (2014–2018). The raw data, together with the semen analysis and when the samples for each individual bull were collected is available in Supplementary 1. The climate in this area (23.3786° S, 150.5089° E) is considered sub-tropical, ranging from 16 °C in winter to over 30 °C in summer. A comprehensive semen analysis was undertaken, including sperm morphology and motility. To determine the variation in semen quality, we plotted the percentage of sperm normal forms for each bull that had 5 or more ejaculates taken annually. Morphology was used as a measure of sperm quality, as Söderquist et al.17 demonstrated that sperm motility is heavily influenced by the collection/collectors and, therefore potentially unreliable and irreproducible. This resulted in the analysis of 1178 ejaculates from 50 bulls, with an average of 23 ejaculates per bull. The percentage of sperm normal forms as a box and whiskers plot for each bull is given (Fig. 1). As shown, many bulls demonstrated extremely high variation between ejaculates, with several males ranging from  70% (considered an outright “pass” in terms of cryopreservation potential) of normal sperm morphology. On the contrary, some bulls appeared to produce consistent semen samples across the year.Figure 1Changes in sperm normal forms. Semen samples were taken from bulls via electroejaculation and the percentage sperm normal forms were counted. The data show a box and whiskers plot consisting of 50 bulls, each of which had at least 5 different ejaculates across a minimum one month. Each box and whiskers plot represents an individual Bull showing the median, upper and lower quartile range. Outliers are represented by individual dots.Full size imageTo determine the amplitude and the proportion of bulls demonstrating variation in the number of normal sperm forms, we measured the difference between the maximum and the minimum values recorded for each animal. From this analysis we found that: 9 (18%) bulls showed less than 20% variation in normal forms; 15 (30%) bulls had between 20–40% variation; 13 (26%) bulls were between 40–60% and for 13 (26%) bulls this number was over 60%. These data have major implications when interpreting semen analysis, since a bull could be classified as either fertile or infertile depending on which ejaculate was considered. This data also sheds light into why correlations between the vBBSE parameters such as morphology and the bull fertility are so variable.Seasonal effect on semen qualitySeveral sources of environmental influence have been suggested to affect bull sperm quality. These include feed availability (i.e., higher conception rates in rainy seasons)27, excessive protein intake28, day length29, thermal heat stress and age30,31. To better understand the dynamics of semen quality variation within our samples, we plotted sample “pass” and “fail” cryopreservation criteria against the month of collection. A raw bull semen sample is classified as “pass” when motility is above 60% and normal forms greater than 70%. When samples were between 30 and 60% motility and 50–70% normal forms, they were classified as a “compensatory” (or qualified) pass (q-pass). The compensatory pass relied on there being the ability to have at least 10 million motile normal forms of spermatozoa in each straw to allow for conception. An outright failure was given to any sample with less than 30% progressive motility or 50% normal forms. This allowed each ejaculate to be placed into a binary “pass” or “fail”.The data for the percentage of total males that “failed” within each month (1271 ejaculates) is shown (Fig. 2A). Clearly, there is a seasonal pattern, with over 90% pass rate in winter (June–August) that fell to 50% or lower in summer (Dec-Feb). Considering that all bulls were greater than 4 years old, housed on the same stud farm and received the same dietary supplement we found no relationship in terms of “pass” or “fail” rates to these parameters. Thus, the data clearly suggested that Temperature/Temperature-Humidity or day length were responsible for the increased failure rates seen during Summer. Therefore, to understand if there was any causal relationship, we correlated either the average monthly temperature (Fig. 2B) or daylight (Fig. 2C) with monthly failure rates. The data showed a correlation with monthly temperature (r2 = 0.55; and temperature-humidity index – see further modelling below) but not with daylight hours (r2 = 0.05). Combined, these data suggest that temperature was the most likely reason for increased failure rates during the warm/hot months.Figure 2Seasonal variation in the semen quality of 1271 bull semen ejaculates. Semen samples were taken from bulls via electroejaculation and a full semen analysis was undertaken. Each sample was then classified as a pass or fail as described in Materials and Methods. (A) The percentage failure rate for each month is shown for all bulls. The number above each column indicate how many semen ejaculates were processed that month. (B). Scatter plot showing the average monthly temperature of Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.55. (C) Scatter plot showing the average daily sunlight in Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.04.Full size imageChanges in normal sperm forms categorised by breedThe present study investigated 11 different breeds of cattle, and we reasoned that maybe one, or more breed(s) contributed to failure rates more than others. Therefore, we plotted the percentage of normal forms for every ejaculate against the breed (Fig. 3). All breeds showed similar variation except for the Belmont Red, Boran and Wagyu. However, a relatively small number of bulls from the Belmont Red and Boran breeds were assessed in this study, therefore, it is unclear if they are indeed more resistant to heat. In the case of the Wagyu, it is worth mentioning that only one animal exhibited poor sperm morphology in several ejaculates (Fig. 3 circled) during winter. A close inspection of the records showed that during this time the animal had a fever episode, with body temperature reaching 39.4 °C, and that the sperm morphology returned to normal in approximately 70 days.Figure 3Variation in Semen quality as judged by Bull breed. Semen sample was collected and analysed for sperm morphology. The animals were then separated according to breed and the percentage normal forms for each ejaculate are shown.Full size imageSome bulls are heat-sensitive, whilst others are heat-tolerantAnalysis of the present data clearly illustrated that some bulls showed marked variation in terms of their semen quality throughout the year (Fig. 1). Meanwhile, others demonstrated much less variation, and were reasonably consistent. To further clarify these differences, we closely analysed the percentage of sperm morphology from two bulls, both of whom had several ejaculates were taken throughout the year, including during and after summer (Fig. 4). There was a clear pattern, and evidence of two types of bulls. Prior to the summer season, bull 1 (Fig. 4, red), designated here as “heat-sensitive”, exhibited  > 70% normal forms of spermatozoa. This value decreases dramatically, reaching its lowest point (10%) mid-January, before undergoing a recovery by April ( > 70%). In contrast, bull 2 (Fig. 4, green) showed a consistent semen profile throughout the year. The data suggest this bull was more “heat-tolerant”.Figure 4Identification of Heat-Sensitive and Heat-Tolerant bulls. The percentage normal sperm morphology from two bulls, both Droughtmasters, which had several ejaculates taken over the course of the year were plotted against the month in which the semen sample was taken. The first bull (red) is an example of a heat-sensitive bull. The second bull (Green) an example of heat-tolerant response.Full size imageTo further explore the concept of “heat-tolerant” and “heat-sensitive” bulls, we subjected 20 Wagyu bulls to a single event of controlled heat stress (40 °C, 12 h). This experiment was performed during Winter, at Singleton (New South Wales, Australia, 32.5695° S, 151.1788° E), where the average temperature was 17 °C and never exceeded 18 °C. Prior to the heat stress event, baseline semen samples were taken from each animal. After heat stress, semen samples were taken every week for 11 weeks. During the experiment, two bulls were removed from the program due to infection and sickness whilst a 3rd bull was removed as it refused to co-operate with electroejaculation procedure. From the remaining bulls, we were able to reproduce the heat-sensitive and heat-tolerant bull phenomenon. The raw data from this work is given in Supplementary 1, and an example of the data is shown (Fig. 5). For 14 bulls, we found no difference in terms of their baseline samples, which were between 70–90% normal forms. This is consistent with the Wagyu bull characteristics and their heat-tolerance (Fig. 5, yellow, green, blue lines). Within these “heat-tolerant” bulls, there was a variation of 16–22% sperm normal forms. For the other three bulls, two of them showed a decline in sperm quality, which began 2–3 weeks after the heat event, dropping from a baseline of 85% and 90% normal forms to 55% and 59%, respectively (30–31% variation in normal forms; Fig. 5, grey and orange line). The third bull showed a greater degree of heat-sensitivity. Starting at 77% morphologically normal sperm, the spermiogram of this bull illustrated a rapid decrease in normal forms in a short time (2 weeks), reaching around 40% after 4–5 weeks. Sperm morphology remained at this level (37% variation in normal form) for four weeks, before recovery. These data show that under experimental condition, the phenomenon of heat-sensitive and heat-tolerant animals can be reproduced. Further, it appears that there are degrees of heat-sensitivity.Figure 5Heating of Wagyu bulls to identify heat-sensitive and heat-tolerant effect. Twenty Wagyu bulls all 3 years of age and over were heated to 40 °C for 12 h in an insulated barn. Before heating, bassline samples were taken (week 1). After heating, electroejaculation was used to collect semen every week for 11 weeks. For every sample, sperm morphology was counted by a qualified theriogenologist. The data show the percentage normal morphology for 5 bulls. The light blue line indicates a heat-sensitive bulls, whose morphology was affected by heat, then returned back to baseline. The orange and grey line represent two related bulls (same father) who also produced less than 70% normal forms. The yellow, green and dark blue lines represent three heat-tolerant bulls, whose semen profile did not drop below the 70% normal spermatozoa threshold.Full size imageEnvironmental heat stress leads to poor sperm quality 17 days laterSimilar to previous reports, we noted that sperm quality does not begin to deteriorate until 2–3 weeks after the heat stress event of the bulls32. Based on the timing of spermatogenesis, this is consistent with reports that meiotic cells are more susceptible to heat stress following a heating event, with poor quality spermatozoa appearing in the ejaculate around 2–3 weeks later. To better understand the relationship between a “heat-event” and the production of poor-quality spermatozoa, we modelled both maximum temperature and maximum temperature humidity index (THI) and their relationship to the proportion of morphologically normal spermatozoa. The THI is an index representing the effect of humidity on the heat stress of an animal. THI was obtained using the following formula:$$mathrm{THI}=0.8* frac{{T}_{max}}{100}+frac{left(humidity*left({t}_{max}-14.4right)right)}{1}+46.4$$where Tmax = maximum temperature, (oF), and H = relative humidity.We plotted the correlation between semen quality and Tmax on the day, and every day prior (up to 40 days) to semen collection (Fig. 6). This modelling demonstrated that poor semen quality was due to maximum daytime temperature 17 days prior (Fig. 6a, arrow). Notably, 1 day of heat-stress appears to be sufficient to cause poor sperm quality, since if we take the average of 2 (Fig. 6b) or 3-day maximal temperatures prior to collection (Fig. 6c) the correlation patterns were similar. Supplementary 3 shows further modelling for Tmax and THI using between 1 and 5-day average temperatures prior to semen collection.Figure 6Bull semen quality (as percentage sperm normal forms) is related to the temperature that occurred 17–19 days ago. Correlation between sperm quality and maximum Temperature (Tmax). The Y axis is the Pearson correlation coefficient and X axis represents the number of days before the day the sperm sample was taken. (a) Uses one day of Tmax data whilst (b) averages two and (c) averages three consecutive days of Tmax data. The arrow shows the best correlation between Tmax and poor sperm quality, which occurs around 17–19 days before the semen sample is collected.Full size imageUnderstanding the temperatures at which heat-sensitive bulls failTo determine the Tmax at which bulls in the paddock begin to produce poor quality spermatozoa, we modelled data using both parameters measured at 17 days prior to the heat event, and plotted samples from 12 heat-sensitive bulls (6 Brahmans, 4 Drought Masters and 2 Santa Gertrudis). The relationship between sperm morphology and Tmax 17 days prior to heat even was plotted, with a spline smoothing cure to show the mean quality as a function of Tmax (Fig. 7a). As the temperature increase, so the quality of sperm morphology decreases as expected. To gain further clarity, we next fitted a nominal logistic regression analysis to model the proportion of spermatozoa that would either pass, Q-pass or fail sperm cryopreservation criteria as a function of Tmax 17 days prior. Tmax effect was highly significant for both outcome categories, with both p  More

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Effects of light intensity and temperatureThe germination of P. paradoxa (91 to 95%) and wheat (93 to 97%) was not affected by light intensity (data not shown). Our results conform to previous studies which revealed that light intensity had little role in influencing P. paradoxa germination24.The germination of wheat and P. paradoxa was influenced by temperature regimes (Fig. 1). At temperature regimes of 15/5 °C and 20/10 °C, germination of wheat and P. paradoxa did not vary. Seed germination in wheat remained similar at temperatures ranging between 15/5 °C to 30/20 °C. However, in P. paradoxa, germination was reduced at higher temperature regimes (35/25 C) compared with lower temperature regimes (15/5 °C to 25/15 °C). At the highest temperature regime (35/25 °C), the germination of wheat was 79%, while, at this temperature regime, the germination of P. paradoxa was only 1%. This suggests that wheat can germinate at high-temperature ranges, while, germination of P. paradoxa may be reduced at high temperatures (35/25 °C). These results implied that at the time of planting wheat in Australia if the air temperature is low, the chances of emergence of P. paradoxa are very high. This suggests that efforts should be made towards early control of P. paradoxa in wheat if the air temperature in the winter season falls early. These results also suggest that early planting of wheat could reduce the emergence of P. paradoxa as the prevailing temperature conditions are relatively high in early planting (e.g., end of April). In the Indo-Gangetic Plains, better control of P. minor was observed in the early planting of wheat (high-temperature conditions) due to less emergence of P. minor25.Figure 1Effect of alternating day/night temperatures (15/5 to 35/25 °C) on germination of Phalaris paradoxa and wheat seeds (incubated for 21 d) under light/dark (12-h photoperiod). LSD: Least significant difference at the 5% level of significance.Full size imagePrevious studies have also revealed that germination of P. paradoxa was highest at 10 °C and then failed to germinate at 30 °C 24,26, however, these studies were conducted at constant temperatures and the germination response of P. paradoxa was not studied in comparison with wheat in those studies.Effect of radiant heatThe germination of P. paradoxa seeds that were stored at room temperature (25 °C) was 97%, which reduced to 88% after exposure to the 100 °C pretreatment for 5 min and became nil at 150 °C (Fig. 2). About 88% of P. paradoxa at 100 °C suggests that it can tolerate heat stress for short periods.Figure 2Effect of high-temperature pretreatment for 5 min (℃) on germination of Phalaris paradoxa seeds. LSD: Least significant difference at the 5% level of significance.Full size imageGermination was nil at 150 °C and above, suggesting that burning could help in managing P. paradoxa, particularly in a no-till field where seeds are on the soil surface or at shallow depths. Exposure of seeds to fire could inhibit germination by desiccating the seed coat or by damaging the embryo27,28,29.Burning of residue in the fields could kill weed seeds and other pests in the topsoil layer30. Windrow burning proved to be an effective tool for killing weed seeds in paddocks31. However, the crop residue burning may cause environmental destruction by killing microbes and polluting the air. Also, it reduces the amount of soil organic matter due to the high heat, causing soil degradation. Therefore, these aspects should also be considered while formulating weed management strategies through crop residue burning. Burning may also release the dormancy of other weed seeds present in the subsoil and thus may increase infestation; therefore, this technique should be used cautiously32,33.Effect of osmotic stressGermination of P. paradoxa was highest (95%) in the control treatment and germination reduced to 75% at an osmotic potential of −0.8 MPa, and became nil at −1.6 MPa (Fig. 3). However, in wheat, germination did not reduce with an increase in water potential and it was 94% in the control treatment.Figure 3Effect of osmotic potential on germination of Phalaris paradoxa and wheat seeds at alternating day/night temperatures of 20/10 °C under 12 h photoperiod. Seeds were incubated for 21 d. LSD: Least significant difference at the 5% level of significance.Full size imageAt a very high concentration of PEG, the metabolic activity of P. paradoxa might be reduced due to water stress. Seed germination is affected when seeds are not able to get critical moisture threshold levels for imbibitions34,35. These results indicate that high water stress may inhibit the seed germination of P. paradoxa. However, under no water stress or mild water stress conditions, P. paradoxa may infest the wheat crop.Contrary to these results, previous studies reported that germination of P. paradoxa was reduced by 90% at an osmotic potential of −0.25 MPa25. Good germination of wheat at high osmotic potential indicates that the wheat variety used in this study may have water stress tolerance traits for germination. It was observed that wheat could germinate well (75%) at a high-water stress level (−1.6 MPa)36. This suggests that it is possible to menace P. paradoxa by growing stress-tolerant varieties of wheat and manipulating irrigation. In a previous study, less infestation of P. paradoxa was observed in drip-irrigated wheat crops due to optimal soil moisture conditions for the crop37.Effect of salt stressGermination of P. paradoxa was highest (93%) in the control treatment, and at a NaCl of 150 mM, germination was reduced to 76% (Fig. 4). Similarly, in wheat, germination was highest (94%) in the control treatment and at a salt concentration of 150 and 200 mM, germination was reduced to 84 and 79%, respectively. These results suggest that at a high salt concentration, P. paradoxa may infest the wheat crop owing to its ability to germinate under high salt concentrations.Figure 4Effect of sodium chloride concentration on germination of Phalaris paradoxa and wheat seeds at alternating day/night temperatures of 20/10 °C under 12 h photoperiod. Seeds were incubated for 21 d. LSD: Least significant difference at the 5% level of significance.Full size imageContrary to this, in Iran, it was observed that germination of P. paradoxa was reduced by 70% at a NaCl of 160 mM24. Most of the Australian soils are saline; therefore, it is quite possible that P. paradoxa in Australia might have developed traits for salt tolerance38. The variable response of populations of P. paradoxa to salt concentrations in Iran and Australia might be due to genetic differences between the P. paradoxa populations38. These observations suggest that P. paradoxa could invade the agroecosystem under the saline conditions of Australia.Effect of seed burial depth on emergenceGermination of P. paradoxa was very low (10%) on the soil surface, and seedling emergence was highest (74%) at a soil burial depth of 0.5 cm (Fig. 5). Seedling emergence was similar when seeds were buried in the soil at a depth ranging from 0.5 to 4 cm. Seedling emergence was 32% at a burial depth of 8 cm.Figure 5Effect of seed burial depth on seedling emergence of Phalaris paradoxa. LSD: Least significant difference at the 5% level of significance.Full size imageThe results from this experiment suggest that a no-till production system may inhibit the germination of P. paradoxa. This study also suggests that deep tillage ( > 4 cm) could reduce the emergence of P. paradoxa to some extent; therefore, inversion tillage could be a weed management strategy if the seedbank is in the shallow layer of the soil. It has been reported that the emergence of small-seeded weeds is reduced from deeper burial depths, as the soil-gas exchange is limited 21. However, it is important to know the seed longevity of this weed in different soil and environmental conditions when considering tillage operations39.Likewise, previous studies also reported that seed germination of P. paradoxa was lowest on the soil surface and no seedlings emerged from a soil depth of 10-cm2,40. Contrary to this in Iran, germination of P. paradoxa was found to be  > 65% on the soil surface 24.Evaluation of PRE-herbicidesResults revealed that cinmethylin, pyroxasulfone, and trifluralin provided 100% control of P. paradoxa. Atrazine, bixlozone, imazethapyr, isoxaflutole, prosulfocarb + s-metolachlor, and s-metolachlor were not found to be effective against P. paradoxa (Table 1). Pendimethalin and triallate controlled P. paradoxa by 80 and 42%, respectively, compared with the nontreated control.Table 1 Effect of PRE herbicides on the survival of Phalaris paradoxa and wheat seedlings (28 d after spray).Full size tableIn wheat, all tested herbicides performed similarly for plant survival except dimethenamid-P and prosulfocarb + s-metolachlor, which caused wheat mortality by 41 and 16%, respectively, compared with the nontreated control. These results suggest that pyroxasulfone, pendimethalin, and trifluralin can be successfully used for the management of P. paradoxa in wheat. Alternative use of these herbicides in wheat crops could provide sustainable weed control of P. paradoxa. In previous studies conducted in Australia, herbicides namely cinmethylin, pyroxasulfone, and trifluralin were found safe for wheat and provided excellent grass weed control41.Efficacy of PRE-herbicides in relation to crop residue coverCinmethylin, pendimethalin, and pyroxasulfone were proven to be very effective against P. paradoxa under no residue cover conditions (Table 2). However, at the residue cover of 6 t ha-1 (high output systems), the efficacy of these herbicides decreased and these three herbicides failed to provide effective control of P. paradoxa. At the residue cover of 2 t ha-1 (low output systems), the efficacy of pyroxasulfone in controlling P. paradoxa was not affected; however, cinmethylin and pendimethalin at the residue load of 2 t ha-1 did not control P. paradoxa. These results suggest that in a residue-retained, no-till system, pyroxasulfone could provide better control of P. paradoxa compared with cinmethylin and pendimethalin.Table 2 The interaction of PRE herbicides and wheat residue amount on the survival of Phalaris paradoxa seedlings at 28 d after spray.Full size tableThe crop residue binds some herbicides, which results in a reduced dose to target weeds and provides poor weed control42. A crop residue cover of 1 t ha-1 may prevent 50% of the herbicide from reaching the target weed seeds in the soil and thus provide poor weed control43.Efficacy of POST herbicides in relation to plant sizeWhen plants were sprayed at the 4-leaf stage, the herbicides clodinafop and propaquizafop were not effective against P. paradoxa compared with the other tested herbicides (Table 3). The efficacy of clethodim, glyphosate, haloxyfop, and paraquat in controlling P. paradoxa was not decreased even when plants were sprayed at the 10-leaf stage. In previous studies, poor control of P. paradoxa was observed with ACCase-inhibiting herbicides44,45. These results also suggest that under noncropped or fallow situations, early and late cohorts of P. paradoxa can be controlled successfully by delaying applications of clethodim, paraquat, haloxyfop, and glyphosate.Table 3 The interaction effect of plant size (large plants-10 leaves and small plants-4 leaves) and herbicide treatments on the survival of Phalaris paradoxa seedlings at 28 d after spray.Full size tableGermination of P. paradoxa at 25/15 °C (day/night) was lower compared with 20/10 °C. This suggests that early sowing of wheat (relatively high-temperature conditions) could reduce the emergence of P. paradoxa in fields. Phalaris paradoxa did not germinate after exposure to radiant heat of 150 °C (for 5 min), which suggests that burning may be a useful tool for managing P. paradoxa, particularly when seeds are on the soil surface or at the shallow surface. A high level of tolerance of P. paradoxa to water and salt stress was observed. These observations suggest that this weed can dominate under saline and water stress conditions in Australia. Low germination of P. paradoxa was observed on the soil surface, suggesting that a no-till system could provide better control of P. paradoxa. PRE herbicides cinmethylin, pyroxasulfone, pendimethalin, and trifluralin were effective for control of P. paradoxa in wheat; however, under a conservation tillage system, pyroxasulfone provided better control of P. paradoxa compared with other herbicides. Haloxyfop and clethodim were the most effective herbicides among the ACCase-inhibiting herbicides. Under noncropped or fallow land situations, larger plants of P. paradoxa can be successfully controlled with the application of clethodim, glyphosate, and paraquat. More