Research Article

Technology Mitigation of Pigs Parasites Contamination Using Laleken and Free-Range Systems Applied by Highland Farmers

Trisiwi Wahyu Widayati1*, Aris Triyono Syahputra2, Andoyo Supriyantono1, Onesimus Yoku1, Deny Anjelus Iyai1, Priyo Sambodo1, Iriani Sumpe1

1Department of Animal Science Papua University, Jl. Gunung Salju, Amban, Manokwari Papua Barat, 98314, Indonesia; 2Program of Post-graduate Papua University, Jl. Gunung Salju, Amban, Manokwari Papua Barat, 98314, Indonesia.

Received | November 10, 2022; Accepted | January 15, 2023; Published | February 24, 2023

*Correspondence | Trisiwi Wahyu Widayati, Department of Animal Science Papua University, Jl. Gunung Salju, Amban, Manokwari Papua Barat, 98314, Indonesia; Email: [email protected]

Citation | Widayati TW, Syahputra AT, Supriyantono A, Yoku O, Iyai DA, Sambodo P, Sumpe I (2023). Technology mitigation of pigs parasites contamination using laleken and free-range systems applied by highland farmers. Adv. Anim. Vet. Sci. 11(3): 508-516.

DOI | http://dx.doi.org/10.17582/journal.aavs/2023/11.3.508.516

ISSN (Online) | 2307-8316

 

 

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

Pigs place the first animal agriculture raised in the world (Eliakunda et al., 2015; de Greef et al., 2011; Kanis 2003; Baxter and Edwards 2017). Pigs will produce many piglets and have three parturition times by average 8-12 piglets born (Ouma et al., 2013; Muhanguzi et al., 2012; Mbaso and Kamwana 2013; Tekle et al., 2013; Iyai et al., 2018; Montsho and Moreki 2012; Holt et al., 2019). Pigs (Sus scrofa sp) are livestock that are easily found in Papua and have many meanings in the social and cultural livings of the Papuan people. Apart from being a symbol of wealth, pigs can also be used to solve customary problems in Papua such as paying a fine for a case, paying a dowry, a funeral ceremony and celebrating a bountiful garden harvest (Pattiselanno and Iyai, 2005).

Most of the patterns of rearing pigs in Papua are carried out semi-intensively or traditionally, namely by means of public display (Pattiselanno and Iyai, 2018). This pattern of maintenance opens up opportunities for various environmental problems such as contamination of water, soil and agricultural products by pig waste, which in turn can endanger human health (Terry and Khatri 2009; Jonge et al. 2008; Camerlink and Turner 2017; Wischner et al. 2009; Petit and van der Werf 2003).  

Pig livestock waste such as feces and urine can be categorized as environmental pollutants. This is because the parasites contained in the feces and urine of livestock have the ability to pollute the environment, especially water and soil, which in turn is dangerous for humans who live around them (Sudiarto, 2008). Damriyasa et al. (2013) suggested that soil samples from the Arfak Mountains and Baliem Valley were positive for soil-transmitted helminths (STH) eggs such as Ascaris spp and Trichuris spp (Wabacha et al. 2004). One of the factors that support the presence of STH in the soil from these two locations is thought to be due to the traditional pig rearing pattern that allows pigs to roam. This maintenance pattern reduces the quality of environmental sanitation which will have an impact on the health of farmers and the wider community who live around them (Pedersen 2017; Muhanguzi et al., 2012; Mugonya et al., 2021; Ouma et al., 2013; Chau et al., 2017; Petit and van der Werf 2003; Iyai 2010; Kijlstra and Eijck 2006; Holt et al., 2019).  

Laleken is a tribe term and language defined as pig farming production practiced by Dani tribe in Central Highland of Papua, i.e. Wamena (Cargill et al., 2015; Soplanit et al. 2021; Siagiaan 2010; Cargill et al., 2009; Cargill and Mahalaya 2014; Wahyuni et al., 2020; Mahalaya 2010). Laleken is a plot of land that is fenced off as a place for pigs to spend the day playing and eating high protein grass (Cargill et al., 2014). In laleken, certain plants or plants are usually planted, such as  Peurasia cephaloides, Centrosema sp, Colopagonium sp and Ipomoea batatas or other plants that can be eaten by pigs. The pattern of rearing pigs with the laleken system allows the pigs to be in a controlled environment all day long, so it is believed that the possibility of pigs as a source of environmental pollution (Wea et al., 2017, Terry and Khatri 2009; de Barcellos et al., 2013; Petit and van der Werf 2003) does not occur. Until now, no research has been conducted that compares the level of environmental pollution caused by pigs reared with the Laleken system with the traditional system. This study aims to compare the pig rearing model between the laleken system and the free-range system on the possibility of preventing contamination of water, vegetables and soil around the yard caused by parasites originating from pig feces and urine.

MATERIALS AND METHODS

This research was conducted in three villages in Minyambouw District, Arfak Mountains Regency, namely Upload Village, Sigim Village and Sinaitosi Village. The research is divided into two stages. In the first stage, sample collection was carried out before treatment and in the second stage, sample collection was carried out by comparing the legal system with the traditional (traditional) system. A total of 30 local pigs weighing 10-15 kg were placed intentionally based on village origin. All pigs used were positive for worm parasites based on the McMaster method of faecal examination with eggs per gram (EPG) of at least 2000 (Sambodo et al., 2020). Each system contains 5 pigs for each village. The variables observed in this study were the diversity and prevalence of environmental polluting parasites originating from the feces and urine of pigs in water, vegetable and soil samples before treatment and between laleken and traditional rearing systems. Identification of helminth parasite eggs based on (Midha et al., 2018).

Stool samples come from fresh feces that have just been secreted. The collection of water, vegetable and soil samples in this study was carried out according to Tymezyna et al. (1999) with three repetitions. Water sample collection was carried out in water puddles around the farmer’s house in both patterns of pig rearing. Water samples were taken as much as 250 ml for each point of water puddles. Vegetable samples were taken as much as 250 g, collection of vegetable samples was done by cutting the part of the stem that borders the ground. The collection of vegetable samples was carried out at three points, each ± 0 m, ± 1 m, and ± 2 m from the guardrail. Soil sample collection was carried out at three points, namely in the area around the house with a distance of ±1 m, ±10 m, ±25 m respectively from the house. Soil samples were taken as much as 50 g at a depth of 2-5 cm using a sterilized spatula. The sample collection in the second stage was carried out on day 0 and day 30 after the laleken system was applied. The method of examining the types of worm eggs in feces is carried out using the native method (Purwaningsih et al., 2017) and on water, vegetables and soil using the sedimentation method (Hadidjaja 1990).

Data Analysis

Quantitative data are presented in mean ± standard deviation. The results of the comparison of the two systems were analyzed using a t-test comparison (t-test) using (Field et al., 2012) the SPSS program at a significance level of 5% (Ott and Longnecker 2001).

RESULTS AND DISCUSSION

Study Area and Design Laleken

Minyambouw District is one of the districts included in the administrative area of Arfak Mountains District (Figure 1). Geographical Location of Arfak Mountains Regency, as follows: Northern part: 0º55’ South Latitude; Southern Part: 1º40’ South Latitude; West: 133º10’ East Longitude; East: 134º05’ East Longitude. 

 

In terms of physiography, the district with the highest percentage of area included in the extremly steep (very steep with a slope of >40%) is Minyambouw (73.83%). Soil structure in Arfak Mountains Regency consists of alluvial species (18.7%), Mediterranean (2.44%), red-yellow podzolic (10.41%), gray-brown podzolic (7.57%), complex soil (complex of soil) (49.21%), latosol (4.5%), and organosol (7.17%). The average annual precipitation is 260.82 mm, the average rainy days per month is 20.92 days. The minimum air temperature is 27.08 oC, while the maximum temperature is 27.80 oC with an average air temperature of 27.49 oC, the average humidity is 84.07%. (Wambrauw et al., 2015; Kabupaten Arfak 2016).

Laleken is a traditional term for a plot of land that is fenced off (Cargill et al., 2009; Siagiaan 2010; Soplanit et al., 2021; Cargill et al. 2015), where certain plants or plants can be planted, such as Peurasia cephaloides, Centrosema sp, Colopagonium sp and Ipomoea batatas or other plants that can be eaten by pigs. Laleken can be divided into smaller parts so that they can be used to rotate pigs from one license to another (Figure 2). Rotation is carried out when the pigs have eaten half (50%) of the plants or plants in one laleken. After the pigs are transferred to another laleken, then the abandoned laleken is immediately replanted, so that when the pigs return to the (abandoned) laleken it has grown back and the pigs can eat it again. The replanting process continues every time the rotation is carried out (Cargill and Mahalaya 2014).

 

STH Parasite Type and EPG Value

The mean EPG value in pigs used in this study was 2185.56. The types of STH parasites and the average EPG observed in pig feces samples in this study can be seen in Table 1. All research pigs were superinfected, where the host that had been infected with one type of parasite was infected by another type of parasite (Nowak and May, 1994). The types of parasites obtained are in accordance with the results of research by Nugroho et al. (2016) which states that there are at least 20 types of internal parasites in pigs in Papua, including Ascaris Suum, Trichuris ransomy and Strongyloides.

Based on the standard of parasitic infection according to Thienpont et al. (2003) then the infection of all parasites in the study pigs was classified as a moderate infection level (number of eggs 500-5000/g feces). The severity of the infection can be evaluated by a score, although it is highly dependent on the worm species, as egg production varies from day to day.worm Ascaris , can produce a large number of eggs, sometimes up to thousands of worm eggs and Ostertagia found in the host, but the results of stool examination do not show severe infection due to the small number of eggs.

The number of parasitic eggs in pig feces is strongly influenced by the number of parasites contained in the pig’s body and the characteristics of each parasite include reproduction time and mode of transmission. STH parasite Strongyloides is the type of parasite with the highest number of eggs that infects pigs with the fastest reproductive time. The larvae of 3 Strongyloides become adult female worms which are present in the intestines in about 4 days, with reproduction starting soon after, detected by the presence of eggs and/or larvae in the feces (Viney and Lok 2015).

 

Table 1: Types of STH parasites and mean EPG infecting research pigs

Species of helminths	Village Unggah		Village Sigim		Village Sinaitosi
	L	T	L	T	L	T
Ascaris spp	840±30,82	850±55,05	800±10,05	870±12,25	820±18,08	830±22,00
Trichuris spp	1250±18,32	1200±30,30	1160±25,22	1240±30,03	1180±19,23	1200±14,04
Strongyloides spp	4500±14,81	4540±15,02	4420±10,10	4350±17,40	4720±44,04	4570±18,08

Explanation: L: laleken; T: traditional

 

Table 2: Prevalence (%) of parasitic egg contamination in water, vegetables and soil

Species of Parasites	Water	Vegetables				Soil
		Plot 1	Plot 2	Plot 3	Average	Plot 1	Plot 2	Plot 3	Average
Ascaris spp	79,63	100,00	66,67	44,44	70,37	100,00	94,44	100,00	98,15
Trichuris spp	77,77	83,33	77,77	50,00	70,37	94,44	94,44	88,89	92,59
Strongyloides spp	87,04	83,33	55,56	50,00	62,96	94,44	94,44	94,44	94,44

 

Table 3: Average EPG on the 30th day in water puddles with and without laleken

Samples	Parameters
	Ascaris spp		Trichuris spp		Strongyloides spp
	L	T	L	T	L	T
Water puddle	29,63±22,23b	337,04±20,20a	35,19±15,79b	353,70±15,67a	0,00±0,00b	305,55±15,79a
Vegetable
Plot 1	16.67±17,17b	100.00±18,23a	22.22±23,34b	122.22±20,22a	0,00±0,00b	100.00±0,00a
Plot 2	0,00±0,00b	44.44±50,48a	0,00±0,00b	38.89±14,14a	0,00±0,00b	33.33±0,50a
Plot 3	0,00±0,00b	11.11±17,08a	0,00±0,00b	22.22±12,12a	0,00±0,00b	38.89±12,13a
Average	5,56	51,85	7,41	61,11	0,00	57,41
Soil
Plot 1	16.67±13,27b	583.33±55,00a	50.00±45,47b	600.00±5,50a	50.00±20,22b	538.89±25,25a
Plot 2	27.78±20,21b	350.00±20,25a	44.44±16,75b	327.78±17,15a	16.67±17,17b	222.22±22,21a
Plot 3	11.11±17,18b	355.56±5,00a	22.22±67,98b	555.56±28,79a	16.67±15,67b	283.33±34,33a
Average	18,52	429,63	38,89	494,45	27,78	348,15

The different superscripts between columns T and L in the same parasite are significantly different

Ascaris suum takes approximately 6-7 days after infection to release the first eggs (Ballweber, 2001). After a series of moltings, Trichuris suis can be found in the intestinal lumen. The prepatent period is 6 to 7 weeks (Laber et al., 2002).

The high number of eggs of the Strongyloides spp parasite is thought to be influenced by other modes of transmission, namely transmamari or through milk. Infective 3 larvae that are transmitted via the transmammary route may stop their development and migration in the mammary gland, and then reactivate when the mother suckles (Viney and Lok, 2015). This allows the pigs to have been infected since they were still suckling the mother, which is also suspected to be positive for Strongyliodes spp.

Believed to be a type of parasite STH found in this study will determine the type of parasitic contamination in the environment. While the number of eggs counted, in addition to affecting the level of infection in pigs, is also believed to affect the level of pollution in the environment, where the greater the number of parasitic eggs contained in the feces of pigs, it will increase the burden of pollution caused in the environment. Eggs A. suum in the feces was positively correlated with the concentration of eggs in the soil used for pigs to move. The highest egg concentrations in soil were found in areas frequently used by pigs (Lindgren et al., 2020).

Prevalence of STH Pollution in the Environment

The results of the examination of water, vegetable and soil samples can be seen in Table 2. All types of worm parasites that infect pigs also contaminate water, vegetables and soil. These results are in accordance with the research of Tymcyna et al. (2015) and Kochanowski et al. (2017) which states that the soil and water in pig farms and surrounding areas are infected with eggs and larvae of worms of the genus Strongylidae and Trichostrongylidae, eggs of nematodes of the genus Trichuris, eggs of Ascaris suum and oocysts of the genus Eimeria.

The Effect of the Laleken System on Prevention of Environmental Pollution

The average EPG on day 30 of water, vegetable and soil samples from the pig pen without and with the laleken system can be seen in Table 3. In all samples, the average EPG experienced a significant decrease after the laleken system. applied. In waterholes, parasites of Ascaris spp were reduced by 91.21%, Trichuris spp. by 90.05% and Strongyloides spp. by 100%. In vegetables, parasites of Ascaris spp were reduced by 89.28%, Trichuris spp. by 87.88% and Strongyloides spp. by 100%. In soil, parasites of Ascaris spp were reduced by 95.69%, Trichuris spp. by 92.14% and Strongyloides spp. by 92.02%.

This is believed to be due to the limited activity of pigs, where before the laleken system was implemented, pigs were free to roam anywhere so that they became a source of contamination in water, vegetables and soil. Parasitic positive pigs will be a source of spread in the herd and in the environment. Animals with high positive numbers indicate widespread transmission within the herd and if infected pigs are transferred to pastures or other pens, the pigs are more likely to carry the infection with them (Katakam et al., 2016).

The decrease in the amount of EPG in all types of samples is believed to be caused by several factors, including temperature fluctuations (Cargill and Mahalaya 2014; Cargill et al., 2009; Siagiaan 2010; Soplanit et al., 2021). In outdoor conditions, the average embryonization and survival of A. suum and T. suis were influenced by season (temperature), soil type and vegetation (Pittman et al., 2015; Boyko and Brygadyrenko, 2020; Katakam et al., 2016; Baies et al., 2022; Kim et al., 2012; Whitehead et al., 2022; Midha et al., 2018). The rate of dehydration in A. suum and T. suis will increase as an exponential function of the increase in ambient temperature. High temperature combined with severe dehydration of faecal samples may be a major factor in mortality for A. suum eggs and T. suis during the summer (Larsen and Roepstorff, 1999). Added by Kim et al. (2012) that embryonation of A. suum is very limited at 5℃. On the other hand, at a temperature of 35℃ egg embryonation experienced a more pronounced acceleration than 25℃. The laleken system has an effect on lowering water, vegetable and soil pollution around the yard caused by Ascaris spp, Trichuris spp and Strongyloides spp from pig feces and urine (Mahalaya 2010; Cargill and Mahalaya, 2014; Cargill et al., 2009; Soplanit et al., 2021).

DISCUSSIONS

Water pollution can occur due to the entry of feces, urine and pig waste, either directly or indirectly through soil gaps into water sources. Lindgren et al. (2020) found eggs of A. suum and, to a lesser extent, T. suis in the area around the pigsty, which had previously been used for swine activity and/or for disposing of pig waste. Referring to the results of research supported by previous research, it is believed that the type of parasite found in water puddles comes from parasites found in pig feces (Kochanowski et al., 2017). This proves that pigs that are positively infected with parasites have the ability to contaminate water puddles around the area where pigs are active. The prevalence of water pollution is thought to be influenced by the number of eggs counted in pig feces. Although not significantly different, the Strongyloides spp species, which was the highest in faecal EPG, had the highest prevalence of pollution in water puddles as well.

Besides being influenced by the number of parasitic eggs in faecal EPG, the prevalence of water pollution contamination is thought to be influenced by the survival ability of an egg in water (Lindgren et al., 2020; Widayati et al., 2020; Kim et al., 2012; Baies et al., 2022; Kochanowski et al., 2017; Pittman et al., 2015). This can be seen in the Ascaris spp species where the number of parasitic eggs in the polluted faeces EPG is lower than the number of eggs of the polluting parasite Trichuris spp, but has a higher prevalence. Ascarid worm eggs (nematodes) are known to be very resistant and very resistant to unfavorable environmental conditions. Eggs A. suum from pigs are commonly used as an indicator of pathogen inactivation in pig waste (Katakam et al., 2016). In addition to temperature, pH and ammonia levels affect the viability of A. suum eggs.

The highest prevalence of pollution in vegetables is at point 1 and the farther away the vegetables are from the fence, the lower the prevalence of pollution (Table 2) or in other words, the higher the concentration of pollutants in an area, the higher the level of pollution. These results are in accordance with the opinion of Roepstorff et al. (2001) and Katakam et al. (2012) that the average transmission of A. suum decreased in areas farther away from the pigsty. The results showed that the eggs of the parasite were able to move up to a distance of two meters from the boundary of the laleken fence or the limit of active pigs. The movement and distribution of these eggs is thought to be influenced by the movement of water flow due to rain. The development and survival of the infective stage of A. suum depends on the microclimate and the rate of transmission which may be related to biotic and abiotic factors. Eggs A. suum released in the fall may have a much higher survival rate because they are transported rapidly into the soil by rain and earthworms (Roepstorff et al., 2001).

In addition to rainwater, egg distribution is also thought to be strongly influenced by soil texture and topography. Based on visual observations in the field, the location of the vegetable gardens around the cages on average has a sandy clay texture and a slightly sloping relief shape. The slope is included in the slope of 8-15%. Soil texture greatly affects the infiltration capacity (Lindgren et al., 2020; Alberto et al., 2010; Fragoso et al., 2016; Salem et al., 2015; Adjei-Nsiah 2006). Soil with a fine texture has a low infiltration capacity so that if it rains, surface runoff will quickly occur (Dunkell et al., 2011; Pratama and Yuwono, 2016; Alberto et al., 2010). The difference in slope will affect the rate of infiltration that occurs, a flat slope will be easier for water to infiltrate while a gentle slope will be difficult for infiltrated water and tends to become runoff (Strauch et al., 2016; Ariani and Haryati, 2020).

The high prevalence of soil pollution at the three sample collection points is thought to be influenced by the routine or movement of pigs in these areas. This shows that the movement and distribution of parasites is strongly influenced by the movement of pigs as hosts. The movement of pigs which is only limited to the area around the farmer’s house causes the spread of feces to accumulate only in that area. This is what causes the high prevalence of parasitic contamination at these three points. The movement of pigs throughout the pen (area) may result in the spread of eggs through the legs (Katakam et al., 2016, 2012).

CONCLUSIONS

The laleken system is able to reduce water, vegetable and soil pollution around the farming land of the farmers caused by Ascaris spp, Trichuris spp and Strongyloides spp resulted from pig feces and urine. The decrease in the amount of EPG in all types of samples caused by several factors, including temperature fluctuations. In outdoor conditions, the average embryonization and survival of A. suum and T. suis were influenced by season (temperature), soil type and vegetation.

Acknowledgement

We thanked all farmers as informants, and staffs for collecting and sharing data including information. Statisticians from Papua University was grateful for consulting the statistical analysis. We also thanked all blind reviewers for improving this manuscript to be readable and understandable.

Ethical Statement

Consent has been obtained from all the participants for this research and the Animal Ethics Committee of Animal Science Faculty, The University of Papua coordinated by Budi Santoso (No. of Reference letter: SP-004/UN42.3/PP/2022).

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding statement

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sector.

novelty statement

The health and hygiene status from parasite of raising pigs can be done using the free range system model by adopting local wisdom.

Authors’ contribution

TWW, ATS, AS, OY, DAI, PS, IS done concept, run, analyze field data, and write the final manuscript.

REFERENCES

Adjei-Nsiah S. (2006). “Cropping Systems , Land Tenure and Social Diversity in Wenchi , Ghana : Implications for Soil Fertility Management.” Wageningen University, The Betherlands.

Alberto C, Eduardo G, Cledimar R, Gustavo T, Renan C, Beber V, Gustavo B (2010). Agriculture , Ecosystems and Environment Nutrient Transfer by Runoff under No Tillage in a Soil Treated with Successive Applications of Pig Slurry. Agricult. Ecosyst. Environ. 139 (4): 689–99. https://doi.org/10.1016/j.agee.2010.10.016.

Ariani R, Umi H (2020). Sistem Alley Cropping: Analisis SWOT Dan Strategi Implementasinya Di Lahan Kering DAS Hulu. J. Sumberdaya Lahan. Indonesian Agency For Agricultural Research and Development (IAARD). https://doi.org/10.21082/jsdl.v12n1.2018.13-31

Baies, MH, Z Boros, CM Gherman, M Spinu, A Mathe, S Pataky, M Lefkaditis, V Cozma. (2022). “Prevalence of Swine Gastrointestinal Parasites in Two Free-Range Forms from Nord-Wes Region of Romania. Pathogens. 11 (954): 1–13.

Ballweber LR. (2001). The Practical Veterinarian Veterinary Parasitology. USA: Butterwoerth- Heinemann.

Barcellos, Marcia Dutra de, Klaus G. Grunert, Yanfeng Zhou, Wim Verbeke, F. J.A. Perez-Cueto, and Athanasios Krystallis. (2013). “Consumer Attitudes to Different Pig Production Systems: A Study from Mainland China.” Agricult. Human Values. 30 (3): 443–55. https://doi.org/10.1007/s10460-012-9416-4.

Baxter, Emma M., Sandra A. Edwards. (2017). “Piglet Mortality and Morbidity. Adv. Pig Welfare, 73–100. https://doi.org/10.1016/b978-0-08-101012-9.00003-4.

Boyko, OO, VV Brygadyrenko. (2020). “Regulatory Mechanisms In.” Regulatory Methani. Biosyst. 8521 (2017): 334–48. https://doi.org/10.15421/022052.

Camerlink, Irene, Simon P. Turner. (2017). “Farmers’ Perception of Aggression between Growing Pigs.” Appl. Anim. Behav. Sci. 192: 42–47. https://doi.org/10.1016/j.applanim.2016.11.009.

Cargill, C, S Mahalaya, A Soplanit, AT Syahputra, L Kossay, N Muid, G Lyons, et al. (2015). “Teknik Budidaya Tanaman Dan Produksi Ternak.” Australia.

Cargill, CF, S Mahalaya. (2014). “Farm-Based Multidisciplinary Research to Improve Pig Production Efficiency in the Papua Province of Indonesia.”

Cargill, CF, S Mahalaya, TA Syahputra. (2009). “Final Report.”

Chau, Le Thi Minh, Philippe Lebailly, and Tran Quang Trung. (2017). “Enhancing Farmers’ Market Power and Income in the Pig Value Chain; a Case Study in Bac Giang Province, Vietnam. Livestock Research for Rural Development. Volume 29, Article #221. Retrieved from Http://Www.Lrrd.Org/Lrrd29/12/Ltmc29221.Html. Accessed 8 Dece.” Livest. Res. Rural Develop. 29 (12): 2017. http://hdl.handle.net/2268/217153.

Dunkell, Dashiell O, Gregory L Bruland, Carl I Evensen, and Mark J Walker. (2011). “Effects of Feral Pig ( Sus Scrofa ) Exclusion on Enterococci in Runoff from the Forested Headwaters of a Hawaiian Watershed,” 313–26. https://doi.org/10.1007/s11270-011-0792-y.

Eliakunda K, Faustin L, James M, Helena M, Stig T (2015). “Smallholder Pigs Production Systems in Tanzania.” J. Agricult. Sci. Technol. A 5 (1). https://doi.org/10.17265/2161-6256/2015.01a.007.

Field, A, J Miles, and Field Zoe. (2012). Discovering Statistics Using R. 1st ed. London: Sage Publication Ltd.

Fragoso, Carlos, Eurídice L, Marisol García-robles, Jorge Montero-muñoz, Patricia R (2016). “Dominance of Native Earthworms in Secondary Tropical Forests Derived from Slash-and-Burn Mayan Agricultural Practices ( Yucatán , Mexico ).” Appl. Soil Ecol. 104: 116–24. https://doi.org/10.1016/j.apsoil.2015.12.005.

Greef, K. H. de, H. M. Vermeer, H. W.J. Houwers, A. P. Bos. (2011). “Proof of Principle of the Comfort Class Concept in Pigs.. Experimenting in the Midst of a Stakeholder Process on Pig Welfare.” Livest. Sci. 139 (1–2): 172–85. https://doi.org/10.1016/j.livsci.2011.03.005.

Hadidjaja P. (1990). Penuntun Laboratorium Parasitologi Kedokteran. Jakarta: Fakultas Kedokteran, Universitas Indonesia.

Holt, H R, P Inthavong, K Blaszak, C Keokamphe, A Phongmany, S D Blacksell, P A Durr, et al. (2019). “Production Diseases in Smallholder Pig Systems in Rural Lao PDR.” Prevent. Vet. Med. 162 (August 2018): 110–16. https://doi.org/10.1016/j.prevetmed.2018.11.012.

Iyai, D A, B W I Rahayu, I Sumpe, D Saragih. (2018). “Analysis of Pig Profiles on Small-Scale Pig Farmers in Manokwari-West Papua Analysis Of Pig Profiles On Small-Scale Pig Farmers In Manokwari-West Papua,” no. July. https://doi.org/10.14710/jitaa.36.3.190-197.

Iyai, Deny Anjelus. (2010). “Sosial-Ekonomi, Penilaian Pendefinisian Faktor-Faktor Peternakan, Sistem Barat, Papua.” J. Ilmu Peternakan. 5 (1): 35–45.

Jonge, Francien H De, Monique Ooms, Willem W Kuurman, Joseph H R Maes, Berry M Spruijt. (2008). “Are Pigs Sensitive to Variability in Food Rewards ?” 114: 93–104. https://doi.org/10.1016/j.applanim.2008.01.004.

Journal, Admin. (2019). “Kajian Erosi, Aliran Permukaan Dan Kehilangan Hara Pada Tanaman Kelapa Sawit Dengan Umur Yang Berbeda Study of Erosion, Runoff and Nutrient Losses from Oil Palm Plantation with Different Ages.” AgriPeat. Universitas Palangka Raya. https://doi.org/10.36873/agp.v20i02.143.

Kabupaten Arfak, Dinas Peternakan dan Perikanan Darat Pegunungan. (2016). “Penyusunan Masterplan Peternakan Kabupaten Pegunungan Arfak.” Anggi.

Kanis, Egbert, A. B F Groen, and Karel H. De Greef. 2003. “Societal Concerns about Pork and Pork Production and Their Relationships to the Production System.” J. Agricult. Environ. Ethics. 16 (2): 137–62. https://doi.org/10.1023/A:1022985913847.

Katakam, KK, A Roepstorff, O Popovic, NC Kyvsgaard, and SM Thamsborrg. (2012). “Viability of Ascaris Suum Eggs in Stored Raw and Separated Liquid Slurry.” Parasitology., no. November. https://doi.org/10.1017/S0031182012001722.

Katakam, KK, SM Thamsborg, A Dalsgaard, NC Kyvsgaard, H Mejer. (2016). “Environmental Contamination and Transmission of Ascaris Suum in Danish Organic Pig Farms.” Parasit. Vect. 9 (80): 1–12. https://doi.org/10.1186/s13071-016-1349-0.

Kendran AAS, IM Damriyasa, NS Dharmawan, IBK Ardana, LD Anggreni (2012). “Profil Kimia Klinik Darah Sapi Bali (Blood Clinical Chemistry Profiles Of The Bali Cattle).” J. Vet. 13 (4): 410–15. https://ojs.unud.ac.id/index.php/jvet/article/view/6033.

Kijlstra, A, I A J M Eijck. (2006). “Animal Health in Organic Livestock Production Systems : A Review.” NJAS - Wageningen Journal of Life Sciences 54 (1): 77–94. https://doi.org/10.1016/S1573-5214(06)80005-9.

Kim, Mk, KH Pyo, YS Hwang, KH Park, IG Hwang, JY Chai, and EH Shin. (2012). “Effect of Temperature on Embryonation of Ascaris Suum Eggs in an Environmental Chamber.” Korean J. Parasitol. 50 (3): 239–42.

Kochanowski, M, J Karamon, J Dąbrowska, A Dors, E Czyżewska, T Cencek. (2017). “Occurance of Intestinal Parasites in Pigs in Poland-the Influence of Factors Related to the Production System.” J. Vet. Res. 61: 459–66. https://doi.org/10.1515/jvetres-2017-0053.

Larsen MN, A Roepstorff (1999). “Seasonal Variation in Development and Survival of Ascaris Suum and Trichuris Suis Eggs on Pastures.” Parasitology. Aus 199 (2): 209–20. https://doi.org/10.1017/s0031182099004503.

Lindgren, K, S Gunnarsson, J Höglund, C Lindahl, A Roepstorff. (2020). “Nematode Parasite Eggs in Pasture Soils and Pigs on Organic Farms in Sweden.” Org. Agr. 10: 289–300. https://doi.org/https://doi.org/10.1007/s13165-019-00273-3.

Mahalaya, S. (2010). “Impact Evaluation of Agricultural Research in Papua , Indonesia Using the Sustainable Livelihood Framework.”

Mbaso, Marvin, Bonet K. (2013). “Comparative Analysis of Profitability among Feeder-Pig, Pig-Finishing, and Farrow-to-Finish Production Systems under the Smallholder Improvement Management System in Ntcheu District of Central Malawi.” Livest. Res. Rural Develop. 25 (10): 2013.

Midha, A, K Janek, A Niewienda, P Henklein, S Guenther, DO Serra, J Schlosser, R Hengge, and S Hartmann. (2018). “The Intestinal Roundworm Ascaris Suum Releases Antimicrobial Factors Which Interfere With Bacterial Growth and Biofilm Formation.” Front. Cellul. Infect. Microbiol. 8 (271): 1–13. https://doi.org/10.3389/fcimb.2018.00271.

Montsho, T, J C Moreki. (2012). “Challenges in Commercial Pig Production in Botswana.” J. Agricult/ Technol. 8 (4): 1161–70. http://www.ijat-aatsea.com.

Mugonya, J, SW Kalule, EK Ndyomugyenyi. (2021). “Effect of Market Information Quality , Sharing and Utilisation on the Innovation Behaviour of Smallholder Pig Producers.” Cogen Food Agricult. 7 (1): 1–18. https://doi.org/10.1080/23311932.2021.1948726.

Muhanguzi, D, V Lutwama, F N Mwiine. (2012). “Factors That Influence Pig Production in Central Uganda - Case Study of Nangabo Sub-County, Wakiso District.” Vet. World. 5 (6): 346–51. https://doi.org/10.5455/vetworld.2012.346-351.

Ott, R. Lyman, Michael L (2001). An Introduction to Statistical Methods and Data Analisys. 5th ed. USA: Duxbury.

Ouma, E.A., M.M. Dione, Peter Lule, Kristina Roesel, L. Mayega, D. Kiryabwire, G. Nadiope, and Danilo Pezo. 2013. “Characterization of Smallholder Pig Production Systems in Uganda. Livest. Res. Rural Develop. 26 (3): 2014. http://hdl.handle.net/10568/29094.

Pattiselanno F, Iyai, Deny A (2005). Peternakan Babi Di Manokwari: Mempertahankan Tradisi & Meningkatkan Taraf Hidup. Majalah Pertanian Berkelanjutan SALAM, 24–25.

Pedersen, Lene Juul. (2017). “Overview of Commercial Pig Production Systems and Their Main Welfare Challenges.” Adv Pig Welfare, no. 1: 3–25. https://doi.org/10.1016/B978-0-08-101012-9.00001-0.

Petit, Jean, and Hayo M.G. van der Werf. (2003). Perception of the Environmental Impacts of Current and Alternative Modes of Pig Production by Stakeholder Groups. J. Environ. Manag. 68 (4): 377–86. https://doi.org/10.1016/S0301-4797(03)00105-1.

Pittman, JS, GH Myers, KJ Stalder, LA Karriker. (2015). Effect of Fenbendazole on Shedding and Embryonation of Ascaris Suum Eggs from Naturally Infected Sows. J.Swine Health Prod. 23 (October): 252–63.

Pratama, Willy, Slamet BY. (2016). “Analisis Perubahan Penggunaan Lahan Terhadap Karakteristik Hidrologi Di Das Bulok.” Jurnal Sylva Lestari. Lembaga Penelitian dan Pengabdian kepada Masyarakat Universitas Lampung. https://doi.org/10.23960/jsl3411-20.

Purwaningsih, P, TA Kusumastuti, B Sumiarto. (2017). Analisis Kelayakan Finansial Pengobatan Pedet Parasitiasis Pada Usaha Pembibitan Sapi Potong Rakyat Di Kabupaten Magelang Provinsi Jawa Tengah. Buletin Peternakan (Bulletin of Animal Science) 41 (2): 197–202. https://doi.org/10.21059/buletinpeternak.v41i2.15730.

Roepstorff, A, KD Murrell, J Boes, S Petkevi (2001). Ecological Influences on Transmission Rates of Ascaris Suum to Pigs on Pastures. Vet. Parasitol. 101: 143–53.

Salem, Haytham M, Constantino Valero, Miguel Ángel, María Gil, Luis L Silva. (2015). “Geoderma Short-Term Effects of Four Tillage Practices on Soil Physical Properties , Soil Water Potential, and Maize Yield.” Geoderma. 237–238: 60–70. https://doi.org/10.1016/j.geoderma.2014.08.014.

Sambodo, P, J Prastowo, K Kurniasih, WW Mubarokah, and S Indarjulianto. (2020). “In Vivo Efficacy of Biophytum Petersianum on Haemonchus Contortus in Goats. Adv. Anim. Vet. Sci. 8 (3): 238–44.

Science, Applied Vegetation. (2017). “Impact of Free-Range Pigs on Mountain Pastures in the Swiss Jura Author ( s ): Pascal Vittoz and Pierre Hainard Published by : Wiley Stable URL : Http://Www.Jstor.Org/Stable/1479072 Impact of Free-Range Pigs on Mountain Pastures in the Swiss Jura” 5 (2): 247–54.

Siagiaan PH. (2010). “Pig Production in Indonesia.”

Soplanit A, S Tirajoh, MWT Batseba, GP Dominanto, and MK Rumbarar. (2021). The Integration Model of Sweet Potato-Pigs in the Papua Highlands The Integration Model of Sweet Potato-Pigs in the Papua Highlands.” In Earth Environ. Sci., 10. https://doi.org/10.1088/1755-1315/807/4/042018.

Staaveren, Nienke Van, Bernadette Doyle, Alison Hanlon. n.d. “Multi-Stakeholder Focus Groups on Potential for Meat Inspection Data to Inform Management of Pig Health and Welfare on Farm.” https://doi.org/10.3390/agriculture9020040.

Strauch, Ayron M, Gregory L Bruland, Richard A Mackenzie, Christian P Giardina. (2016). “Geoderma Soil and Hydrological Responses to Wild Pig ( Sus Scofa ) Exclusion from Native and Strawberry Guava ( Psidium Cattleianum ) -Invaded Trop. Montane Wet Forests.” Geoderma 279: 53–60. https://doi.org/10.1016/j.geoderma.2016.05.021.

Sudiarto B. (2008). “Pengelolaan Limbah Peternakan Terpadu Dan Agribisnis Yang Berwawasan Lingkungan.” In Seminar Nasional Teknologi Peternakan Dan Veteriner. Universitas Padjajaran Bandung. Bandung: Universitas Padjajaran Bandung.

Tekle, T, A Tesfay, and T Kifleyohannes. (2013). “Smallholder Pig Production and Its Constraints in Mekelle and Southern Zone of Tigray Region, North Ethiopia. Livestock Research for Rural Development. Volume 25, Article #184. Retrieved September 5, 2016, from Http://Www.Lrrd.Org/Lrrd25/10/Tekl25184.Htm.” Livest. Res. Rural Develop. 25 (10): 5455. https://doi.org/10.1186/1746-6148-9-97.Ashebir.

Terry, James P., Kamal K. (2009). “People, Pigs and Pollution - Experiences with Applying Participatory Learning and Action (PLA) Methodology to Identify Problems of Pig-Waste Management at the Village Level in Fiji. J. Cleaner Prod. 17 (16): 1393–1400. https://doi.org/10.1016/j.jclepro.2009.06.001.

Thienpont D, P Rochette, OVJ Vanparijs. (2003). Diagnosing Helminthiasis By Coprological Examination. Turnhoutseweg 30 B-2340 Beerse, Belgium.

Tymcyna, L, A Chemielowiec-Korzeniowska, L Saba. (2015). “Effect of a Pig Farm on the Physical and Chemical Properties of a River and Ground Water.” Polish J. Environ. Stud. 9 (2): 97–102.

Viney, ME, JB Lok. (2015). The Biology of Strongyloides Spp. WormBook.

Wabacha, J K, J M Maribei, C M Mulei, M N Kyule, K H Zessin, W Oluoch-Kosura. (2004). Health and Production Measures for Smallholder Pig Production in Kikuyu Division, Central Kenya. Prevent. Vet. Med. 63 (3–4): 197–210. https://doi.org/10.1016/j.prevetmed.2004.02.006.

Wahyuni, BRI, TW Widayati, N Logo. (2020). “Produktivitas Ternak Babi Di Wamena Kabupaten Jayawijaya.” In Teknologi Dan Agribisnis Peternakan VIII-Webinar, 414–20.

Wambrauw L, A Ungirwalu, S Syaranamual, LY Sonbait, Y Wambrauw (2015). “Studi Masterplan Pembangunan Pertanian Di Pegunungan Arfak.” Manokwari.

Wea, Redempta, Andy YN, Bernadete BK. (2017). “Peternakan Babi Berbasis Zero Waste.” J. Pengabdian Kepada Masyarakat. State University of Medan. https://doi.org/10.24114/jpkm.v23i3.7450.

Whitehead, B, SM Thomsborg, MJ Denwood, and P Nesjum. (2022). “Assessing the Impact of Ascariasis and Trichuriasis on Weight Gain Using a Porcine Model.” Plos Neglected Rop. Dis. 16 (8): 1–13. https://doi.org/10.1371/journal.pntd.0010709.

Widayati, I, BW I Rahayu, N Degei. (2020). “Identifikasi Cacing Gastrointestinal Pada Babi Di Kabupaten Jayawijaya Dan Paniai, Provinsi Papua.” J. Ilmu Peternakan Dan Ve. Trop. 10 (1): 23. https://doi.org/10.46549/jipvet.v10i1.75.

Wischner, Diane, Nicole K, Joachim K (2009). Nest-Building Behaviour in Sows and Consequences for Pig Husbandry. Livest. Sci. 124 (1–3): 1–8. https://doi.org/10.1016/j.livsci.2009.01.015.