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Behavioural traits to identify subclinical diseases of grazing ruminants : A thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy at Lincoln University
Animal welfare and wellbeing can be improved through the early detection and diagnosis of disease. Subclinical infections in particular can be difficult to determine, however, animals may demonstrate subtle changes in behaviour. These changes related to eating, ruminating, inactive behaviour and active behaviour can potentially be identified and measured through sensor technologies. This thesis composes of a series of studies designed to explore changes in behavioural patterns of grazing ruminants experimentally challenged with subclinical infections using commercially available accelerometers.
The objective of the first trial (Chapter 3) was to investigate the changes in grazing, ruminating and activities of grazing dairy calves infected with the internal gastrointestinal nematodes Ostertagia ostertagi and Cooperia oncophora and determine the behavioural patterns after receiving an anthelmintic treatment, using neck mounted sensor collars. At Day -12 relative to an experimental infection, animals were dewormed and fitted with Allflex EveryCow collars which can identify mutually exclusive behaviours such as eating, ruminating, resting, walking, medium activity, high activity and behaviour related to heavy breathing. On Day 0, they were allocated into one of two treatments, viz, Infected, in which animals were orally dosed weekly for three weeks with a 1:1 mixture of 20,000 O. ostertagi and C. oncophora L3 larvae, or Control in which animals remained uninfected, and grazed a new pasture that had not previously been grazed. Animals were rotationally grazed as a mob with weekly shifts and each break back-fenced to reduce the risk of self-infection. On Day 49, to assess the behavioural response following anthelmintic treatment, half of calves in each treatment were orally administered with the Matrix Oral triple combination anthelmintic and continued to be monitored, using a 2 × 2 factorial experimental design, viz, Control without Drench (COD), Control with Drench (CD), Infected without Drench (IOD), Infected with Drench (ID). Results showed nematode challenge increased daily eating time (+14.8 minutes per day, mins/d, P = 0.007) and reduced daily ruminating time (-9.8 mins/d, P = 0.001) and daily mid-activity duration (-5.3 mins/d, P = 0.023) in grazing calves.
After 49-day challenge of gastrointestinal nematode (GIN) infection, the mean faecal egg counts (FEC) of Infected and Control groups were 700 ± 181 and 33 ± 18 eggs/gram, respectively. Furthermore, there was a lack of a consistently high level of parasitism in the calves. To help determine if there was any potential for subtle changes in behaviour to be detected, three animals at the extremes of each of the initial intended treated groups, viz, animals in IOD and 3 animals in ID with the highest FEC and three calves in COD and four calves in CD with highest body weight gain were selected. Parasitism increased FEC and decreased daily live weight gain (643.7 g/day vs 790.6 g/day for parasitized animals and control animals respectively, P = 0.029) from Day 20 to Day 49. There were non-significant negative correlations between log10 (FEC+1) and behavioural measurements for daily eating duration (r = -0.085, P = 0.501), daily walking duration (r = -0.16, P = 0.191), daily mid-activity duration (r = -0.18, P = 0.155), daily high activity duration (r = -0.060, P = 0.636), and daily heavy breathing duration (r = -0.17, P = 0.174) with non-significant positive correlations for daily ruminating duration (r = 0.018, P = 0.889) and daily rest duration (r = 0.16, P = 0.197). In the parasitized animals with the high-level output of FEC, nematode infection significantly increased their mean daily eating duration (+34.6 mins/d, P = 0.020), compared with their uninfected counterparts, and had no effect on mean daily ruminating duration (-18.2 mins/d, P = 0.737), mean daily walking duration (-14.4 mins/d, P = 0.598), mean daily mid-activity duration (-10.3 mins/d, P = 0.498), mean daily high activity duration (-7.2 mins/d, P = 0.744). Moreover, nematode infection increased eating time during cooler periods of the day (+1.7 mins/h from 0400 to 0800 hours, +1.5 mins/h from 2000 to 2300 hours) and decreased in the early morning (-0.7 mins/h from 0000 to 0300 hours) and in the afternoon (-1.5 mins/h from 1300 to 1700 hours) (P < 0.001), and reduced the duration of mid-activity during most times of the day (-0.5 mins/h from 0000 to 0700 hours, -0.2 mins/h from 1100 to 1300 hours, -0.2 mins/h from 1500 to 2300 hours, and +0.2 mins/h from 0800 to 1000 hours, P = 0.007). In parasitized animals post anthelmintic drenching, heavy breathing duration was decreased (-0.1 mins/h) from 0200 to 0500 hours and then increased (P = 0.010) during most time of the day (from 0600 to 0900 hours, from 1100 to 1600 hours and from 2200 to 0100 hours) with fluctuations from 1700 to 2100 hours. In control animals post anthelmintic drenching, walking duration was reduced (P = 0.010) during early morning from 0100 to 0700 hours (-0.4 mins/h) and at dusk from 1700 to 1800 hours (-0.6 mins/h), and increased from 0800 to 1600 hours (+0.3 mins/h) and in the late evening from 1900 to 0000 hours (-0.2 mins/h), while heavy breathing duration was increased (P = 0.018) during most times of the day (+0.1 mins/h from 0500 to 0900 hours, +0.2 mins/h from 1100 to 0000 hours).
Unfortunately due to an outbreak on Mycoplasma bovis on the research farm the first study was required to be terminated after only a short-time post-drenching. Due to biosecurity requirements continuing investigations in cattle was not an option and it was decided to instead use sheep as the species of choice for the remainder of the studies. A paucity of commercially available sensors for sheep meant that alternatives must be found and validated. Of these, the Cowmanager sensor tags were chosen due to their relative size and weight and possible suitability for a sheep ear. However, these tags had not previously been evaluated in sheep. The second trial (Chapter 4) was aimed to determine if the Cowmanager tags could provide an accurate and meaningful representation of the behaviour of sheep. In order to do this, a lipopolysaccharide (LPS) challenge model was used which provides a predictable and consistent short-term change in animal behaviour such as lethargy, and inappetence without long-term negative consequences. At recruitment (Day -10), twenty female Coopworth lambs of 8-10 months (mean live weight = 38.63 ± 2.04 kg) were weighed and fitted with CowManager SensOor ear tags which can identify mutually exclusive activities of five categories: eating, ruminating, inactive behaviour, active behaviour and highly active behaviour, and allocated within live weight strata to one of two treatments, respectively receiving 0 or 0.5 μg/kg body weight of endotoxin LPS with an experimental design of 2 × 2 Latin square. On Day 0, the lambs in the LPS group were intravenously injected with LPS contained in sterile saline, while the control lambs were intravenously injected with sterile saline solution. Seven lambs (four lambs in the LPS group and three control lambs) were randomly selected and individually marked for visual identification for verification of the behavioural changes. To validate the data between visual observation and sensor recordings, the behaviours of the seven lambs were visually observed and recorded every minute for 60 consecutive minutes for two hours between 0900 hours and 1600 hours within three days around the period of LPS infusion. A week after the first intravenous infusion of LPS, the two groups were swapped and intravenously administered with 0.5 or 0 μg/kg body weight of LPS, and the experimental procedure was repeated for the second period. The behaviours of the same seven lambs previously marked for visual identification was recorded via visual observation based on the same procedure to compare with sensor recordings. LPS infusion elevated rectal temperatures after 4 hours from 39.31℃ to 39.95℃, indicating successful establishment of an acute fever response for comparison between groups (P < 0.001). Results showed there was good agreement between visual observations and sensors for active and not active behaviour, but poor agreement with eating and ruminating time. For each of the five recorded behaviours, time spent eating, ruminating, not active, active and highly active, the accelerometers were able to detect an effect of LPS challenge. Compared with the control, LPS infusion decreased eating time (-6.7 mins/h, P < 0.001), active behaviour (-8.4 mins/h, P < 0.001) and highly active (-2.9 mins/h, P < 0.001) and rumination time (-1.4 mins/h, P = 0.075) and increased inactive behaviour (+16.0 mins/h, P < 0.001) in challenged lambs. This provided validation of the Cowmanager tags for use in sheep.
Alkaloids produced by ryegrass endoyphytes are known to cause changes in animal behaviour, inducing heat stress and ryegrass staggers in severe cases. In Chapter 5, the potential for CowManager SensOor ear tags to categorize changes in eating, ruminating and other behavioural activities of grazing lambs exposed to endophyte-infected perennial ryegrass was evaluated. Thirty Coopworth lambs with a mean live weight (± SE) of 33.6 ± 0.46 kg were allocated randomly within live weight strata to either endophyte-free cultivars of ryegrass (Control) or wild type endophyte-infected cultivars of ryegrass pasture (Endophyte). Live weight change, behaviour and incidence of ryegrass staggers were monitored over a 2-month grazing period. Moderately severe staggers (score 4/5) occurred in 40% of lambs in the endophyte treatment with a mean staggers score of 2.33 ± 0.41 (P < 0.001) for the endophyte group at the end of trial. During the period of ryegrass staggers, compared with those grazing the control pasture, lambs in the endophyte group had had no significant difference in eating time (-36.0 mins/d, P = 0.516), time spent being active (+29.9 mins/day, P = 0.556) and being inactive duration (-43.7 mins/day, P = 0.114), but increased time spent ruminating (+40.2 mins/d, P = 0.051). When comparing lambs in the same group with stagger score 4 and those with staggers score 1 or 0 during staggers period, these behavioural differences were even more pronounced though non-significance was presented (-82.2 mins/d for eating, P = 0.073; -62.9 mins/d for being inactive, P = 0.221; +124.0 mins/d for being active, P < 0.001; +48.9 mins/d for ruminating, P = 0.015), indicating that it was not a reflection of the different swards or the physical characteristics. Changes in the pattern of behaviours during staggers period were also evident as reflected in a diurnal alteration of each activity over time of the day. The challenge of toxic alkaloids produced in endophyte-infected ryegrass led to more time eating during cooler period of the day (P < 0.001) and more time being active for compensation during day-time (P < 0.001) as well as more ruminating time during night-time (P < 0.001) and less time being inactive (P < 0.001) and highly active (P < 0.001), especially in the lambs with severe ryegrass staggers.
The final trial then compared the effect of a chronic subclinical infection with gastrointestinal nematode parasites on sheep behaviours (Chapter 6). At start of this trial on Day 0, thirty-six Coopworth ram lambs at 8-10 months of age were weighed, fitted with CowManager SensOor ear tags, and randomly allocated within live weight to one of four experimental groups, non-parasite exposure groups (NP), NP1 (n = 9, 34.89 ± 3.93 kg,) and NP2 (n = 9, 34.56 ± 2.82 kg), oral administration of parasites (OP), OP1 (n = 9, 34.89 ± 3.00 kg) and OP2 (n = 9, 34.44 ± 2.94 kg) with a three-times weekly trickle infection for four weeks with the equivalent of 130 Teladorsagia (Ostertagia) circumcincta L3 larvae per kg live weight (LW) and 80 Trichostrongylus colubriformis L3 larvae per kg LW per day. After 4 weeks of infection, the NP1 group and OP1 group were orally administered once with an anthelmintic. Two weeks later, the NP2 group and OP2 group were orally treated once with the same anthelmintic. GIN infection resulted in a reduction in mean daily eating time (-91.7 mins/d, P = 0.001) and an increase in mean time spent being inactive (+88.4 mins/d, P = 0.001) and active (+7.4 mins/d, P = 0.017) with no differences in mean daily ruminating time (-15.5 mins/d, P = 0.395) and mean daily highly active duration (+12.7 mins/d, P = 0.400). Compared with the control, the animals challenged with nematode infection increased eating time during cooler period of the day (+1.5 mins/h from 2000 to 0200 hours) with less time spent eating during sunrise (-4.7 mins/h) and sunset (-1.7 mins/h) (P < 0.001). Further, compared with the control, the animals infected with nematode reduced daytime ruminating (-0.5 mins/h from 0600 to 1600 hours) and increased ruminating time at dusk (+0.5 mins/h from 1700 to 1900 hours) and in the evening (+0.8 mins/h from 2100 to 0000 hours) (P < 0.001). In addition, compared with the control, nematode infection increased inactive time of parasitized animals in the early morning/after sunset with a reduction during the late afternoon (-0.6 mins/h from 1400 to 1800 hours) and late evening (-1.1 mins/h from 2200 to 0100 hours) (P < 0.001), increased active duration in the early morning (+1.2 mins/h from 0400 to 0700 hours) with reductions in the late morning (-0.2 mins/h from 1000 to 1200 hours) and from late afternoon to evening (-0.3 mins/h from 1500 to 2200 hours) (P < 0.001), and increased highly active duration during most times of the day (+0.6 mins/h from 0300 to 1800 hours) with a decrease in the evening (-1.1 mins/h from 1900 to 0200 hours) (P < 0.001). Compared with the control animals, for the infected animals, anthelmintic drenching increased eating time during most of the daytime +1.6 mins/h with a decrease during cooler times of the day (-2.4 mins/h from 2000 to 0300 hours) (P < 0.001), increased night-time ruminating (+1.3 min/h from 2000 to 0200 hours) with an increase in the early morning (-1.1 mins/h from 0300 to 0800 hours) and in the afternoon (-1.0 mins/h from 1300 to 1800 hours) (P < 0.001), increased inactive duration in the morning (+0.9 mins/h from 0200 to 1000 hours) and in the afternoon (+1.3 mins/h from 1200 to 1700 hours) with a decrease in the early evening (P < 0.001), reduced active duration from 0300 to 0500 hours (-0.6 mins/h) and from 0700 to 1400 hours (-1.1 mins/h) with an increase from 1500 to 1800 hours (+0.9 mins/h) and from 2000 to 0200 hours (+0.9 mins/h) (P < 0.001), decreased highly active duration during most of the daytime (-1.1 mins/h from 1000 to 1800 hours) with an increase in the evening (+2.2 mins/h from 1900 to 0100 hours) (P < 0.001).
In summary, the results from these trials demonstrate that altered behavioural patterns of grazing animals due to health challenges of diseases or toxins can be detected through commercially available sensor technologies. Acute health challenge in lambs can increase inactive duration and compensate to reduce eating duration, rumination duration, active duration and highly active duration in a short period, whereas chronic endophyte staggers challenge in lambs results in increased daily active duration and daily ruminating duration with a decrease in daily eating duration, daily inactive duration and daily highly active duration. Chronic subclinical parasitic challenge in dairy calves can induce an increase in daily eating duration and daily rest duration, and decrease daily durations of ruminating, walking, mid-activity, high-activity and heavy breathing. However, chronic subclinical nematode challenge in lambs can result in a decrease in daily durations of eating, ruminating and an increase in the daily durations of being inactive, active and highly active. The magnitude and duration of total daily behavioural changes varied under these health challenges. Moreover, both chronic subclinical GIN challenge and chronic challenge of toxic alkaloids in endophyte-infected ryegrass can increase eating time during cool periods of the day, decrease time spent being active during nighttime with an increase in the daytime in grazing lambs at pasture. However, chronic subclinical GIN challenge can increase inactive duration at sunrise and sunset and decrease daytime ruminating and increase ruminating duration in the evening, while chronic challenge of toxic alkaloids can increase ruminating duration with a reduction in inactive duration during most of the day. Consequently, behavioural changes detected by commercially available sensor technologies evaluated in these studies could be applied as a useful and potential tool to identify changes in behavioural patterns of each category under infection challenges of diseases or toxins, indicating animal health status and determining the need of treatments for individuals or a whole mob
The commercial application of insect protein in existing human food products: A product audit based on online resources
Background: The growing global population and expanding pet food market have contributed to the increasing demand for protein. Escalating costs and environmental con-cerns regarding traditional animal protein production have prompted a search for sus-tainable alternatives, and insect protein has received considerable attention due to its high nutritional content and eco-friendly credentials. This study aims to examine how available insect-based protein sources compare with other protein sources.
Methods: To explore the commercial application of insect protein in existing human foods, this study aims to profile and compare ultra-processed food products containing insect protein (insect protein-enhanced foods) with equivalent traditional products. A global product audit was conducted in August 2023 drawing from English-language online retail portals to determine the product formats using insect protein and statistically compare their nutritional content with products enhanced more traditional proteins.
Results: Results show that insect protein has been utilised in the development of four categories of ultra-processed food products: flour/powder, pasta/noodle, starch-based snacks (chips, crackers, and cookies), and energy bars. Both flour/powder and pasta/noo-dle enriched by insect protein demonstrate comparable protein content to traditional pro-tein enhancers, highlighting insects' potential as robust protein fortifiers. Due to the high fat content of insect protein, food items with less demanding flavour requirements may offer more suitable platforms for integrating insect protein as an ingredient.
Conclusions: Despite its potential, high fat content limits the use of insect protein in food products. Innovation is needed to overcome this barrier and expand its application. Our research contributes to bridging existing knowledge gaps and providing a foundation for future research through a comprehensive audit of insect protein-enhanced food prod-ucts, paving the way for future exploration in various domains
Training a new generation of agrifood specialists - Learning from the development of a specialist agribusiness and food marketing degree programme
Presentation at IFAMA 2024
Seaweed as the denizens of the new commons in the anthropocene
The article presents a case for coastal cities to re-envision the current dualistic boundary between city and sea, human and nonhuman, in light of the sea-level rise and storm surges. The aim is to go beyond the traditional defence-driven, mechanical handling of water to engage more meaningfully with the marine world as the water enters our cities. We present seaweed as the representative of the marine world, as a connector between the urban and the marine realm due to its capacity to support life, mitigate climate change, strengthen coastal resilience and impact the local culture and education due to its various ecosystem services. These findings are derived from learnings from three state of-the-art case studies in Denmark. First, is a design competition incorporating a marine nature-based solution to rethink storm surge protection in Vejle; second is a marine restoration project of a former coastal lagoon in Gyldensteen Strand in Fyn and an artificial underwater reef by the art collective in Copenhagen. The research is based on trans-disciplinary discussions on the value and the role of inviting seaweed as a welcomed key resident of a new coastal commons that fundamentally transform how we live with our watery neighbour, the sea
Coastal sea ice thickness in Antarctica from airborne measurements
Cryospheric, oceanic and atmospheric processes along the Antarctic coast find their expression in the sea-ice mass balance along the continental shelf. The sea ice thickness in this area and its dynamics is particularly hard to assess because of both its spatial and temporal heterogeneity and the logistical constraints for in-situ observations. In this contribution we provide an overview and results of our airborne observations of ice thickness and snow in the western Ross Sea, including our newest observations along the far East-Antarctic coastline.
By conducting six airborne geophysical sea ice campaigns between 2009 and 2023, we obtained unique insights in ice-ocean-atmosphere processes in this important region of sea-ice formation. It includes; characteristic sea-ice processes as a result of the regular occurrence of coastal polynyas, such as the Ross Sea, McMurdo Sound, and Terra Nova Bay polynyas; processes as a result of the outflow of ice shelf water, which finds its expression in the formation of a sub-ice platelet layer under persistent fast ice.
Our main instruments are (i) an airborne electromagnetic induction (AEM) device and (ii) an airborne snow radar. In one season we were able to trial co-incident measurements with both instruments. The most representative flights have been achieved using a Basler BT-67 and Twin Otter fixed wing aircraft, whereas helicopter flights were restricted to land-fast sea ice.
We present our strategy to combine these measurements with satellite information, and how it contributes to a better understanding of the coastal Antarctic cryosphere as a whol
Shared Water Policy in New Caledonia: Feedback on a mechanism for policy co-construction and co-planning
In March 2019, the government of New Caledonia approved the framework for the country’s first water management policy. Called the “Shared Water Policy” (PEP1), it is the result of a broad consultation involving approximately one in six hundred New Caledonians. This
chapter presents a retrospective of the consultation mechanism put in place for the development of this policy. It focuses in particular on the process and the planning support tools used, partly inspired by the CoOPLAN mechanism
Asymmetric sharing of generalist pathogens between exotic and native plants correlates with exotic impact in communities
1. As exotic plants invade into a new range, they can escape from specialist enemies. However, they may support generalist enemies, including both native and introduced fungal pathogens, which creates the potential for spillover and apparent competition from exotic to native plants in communities.
2. To assess the potential for spillover of putatively pathogenic, root-associated fungi (hereafter, ‘pathogens’) in communities invaded by exotic plants, we conducted a two-phase plant–soil feedback experiment: a monoculture experiment with native and exotic plants grown alone and a multi-species, community-level experiment that ranged in the extent of exotic dominance. We used next-generation sequencing to characterise sharing of pathogens between native and exotic plants in communities.
3. Exotic plants outperformed natives in communities, despite harbouring higher relative abundance of generalist pathogens. The higher generalism of pathogens supported by exotic plants made them more prone to be shared with natives. The proportion of pathogens shared between exotic and native plants in communities correlated with reduced competitive ability of native compared with exotic plants.
4. Synthesis: These data suggest that exotic plants host more generalist pathogens that are shared with native plants, which may confer an indirect benefit to exotic over native plants through apparent competition
The uniformity of ground spreading common New Zealand blended fertilisers
Farmers increasingly ask spreading contractors to apply fertiliser blends. Most fertiliser in NZ is spread using twin-disc fertiliser spreaders mounted on trucks or tractors. These spreaders aim to achieve a uniform spread by overlapping passes in the field. Fertiliser spread testing in NZ uses the Spreadmark® scheme as a fertiliser placement quality assurance programme.
This study assessed the Field Coefficient of Variation (Field CV) achieved when spreading commonly blended compound fertilisers in NZ, including measuring the Field CV of the individual components of the fertiliser blend. Fertiliser blends were tested using commercially available, Spreadmark® accredited, twin-disc spreaders on flat fields in the Waikato and South Canterbury with a standard pan test method.
Across the four blended fertilisers tested in the Waikato, there were significant differences in the Field CV achieved when spreading the fertiliser component alone, versus its spread as a component of the fertiliser blend, in 80% of comparisons. For the two blends tested in South Canterbury, there were significant differences in the Field CV achieved when spreading the fertiliser component alone, versus its spread as a component of the fertiliser blend, in only 40% of the six comparisons. The average deviance between spreading a fertiliser component alone, versus its spread as a component of a fertiliser blend between the two spreaders in Waikato, and the two spreaders in South Canterbury, was 11.8%. The average deviance between spreading a fertiliser component alone, versus its spread as a component of a fertiliser blend between the Waikato, and South Canterbury, was 16.8%.
The differences between the spreading variability of components lead to differences in the maximal Bout (working) Width of spreading such fertiliser mixes. The tested non-nitrogen fertilisers can only be spread at a 22 m working width to stay within maximal variability (25%), whereas the tested N-fertiliser can be spread at a 27 m working width to stay within maximal variability (15%)
Implementation of gender quota requirements by local associations in New Zealand cricket
Purpose/rationale: To examine the implementation of a gender quota requirement for boards, introduced by Sport NZ in 2018, on local cricket governance in New Zealand.
Design/methodology/approach: An open-ended qualitative survey to local board members, face-to-face interviews with management and key stakeholders, and examination of organisational documentation.
Findings: The study confirmed that the male-dominated boards did not know how to source female members but showed that the gender quota requirement was effective since boards all described making changes to reach the quota requirement. Professionalisation of the boards was also improved.
Practical implications: Quotas do work in creating change but ideally should also be implemented with more assistance about how to make change and provide platforms for associations to share knowledge about their processes.
Research contribution: Strongly entrenched male sports cultures can be disrupted and improved through top-down externally driven policies.
Originality/value: The implementation of gender quota requirements results in increased professionalisation of boards