Pigs (Sus scrofa) are well known for using their highly developed sense of smell, for instance while hunting for truffles in the ground. Pigs’ motivation to sniff and root is even mentioned in various children’s books:

This quote is from the popular children’s novel Charlotte’s Web, and it emphasizes how many people, not only within the scientific community but also in the public, acknowledge the sense of smell in pigs and its importance in pigs’ lives. Pigs are omnivorous animals and their natural sources of food are found sporadically within large home range areas, and sometimes underground. Pigs will use their snouts to sniff and root in the substrate to locate edible parts and, to some degree, to satisfy a motivation to explore (termed inquisitive exploration) (Wood-Gush and Vestergaard, 1989; Day et al., 1995). Pigs, in addition, use their sense of smell to detect and differentiate between conspecifics (Meese and Baldwin, 1975; Mendl et al., 2002), and body odors are an important component in mating behavior and when interacting with (unknown or known) individuals (Stolba and Woodgush, 1989).

Pigs have been co-existing with humans for about 10,000 years (Giuffra et al., 2000; Amaral et al., 2011; Meiri et al., 2013) and though many parallels are drawn between humans and pigs, for instance when considering pigs as human models in biomedical research, it should be emphasized that the olfactory systems of pigs and humans differ (Pond and Houpt, 1978). For instance, the olfactory bulb of pigs constitutes 7% of their brain size (Brunjes et al., 2016) and pigs have 1,113 functional olfactory receptor genes (Nguyen et al., 2012; Paudel et al., 2015) as compared with 0.01% of the brain (Kavoi and Jameela, 2011) and 347 olfactory receptor genes in humans. Therefore, we must assume that the sense of smell differs between the two species and thus precautions should be taken with regard to the olfactory environment in which we house farmed pigs. This is particularly important when considering the large population of pigs living under human care within the worldwide farming industry. In 2020, there were 146 million farmed pigs in the EU alone (Eurostat, 2022).

Not surprisingly, with regard to olfaction, porcine research has mainly focused on studying aspects deemed relevant for enhancing commercial pig production, and thereby benefiting farm economy. One aspect is the importance of smell for the palatability of feed (i.e., combination of taste, smell, and texture of the feed, which is sensed before swallowing) (Jacela et al., 2010). This research is aimed at increasing feed intake in pigs (e.g., Jacela et al., 2010) and hence adds important information for optimizing production. Another aspect is the use and importance of odors for reproduction. Odors (boar smell/androsterone) may be utilized to stimulate estrus in sows, thereby facilitating reproduction (e.g., Booth and Signoret, 1992; Sørensen, 1996; Rekwot et al., 2001). A line of studies has examined how pheromones are detected and processed in pigs (e.g., McGlone, 1985; Dorries et al., 1997; Guiraudie et al., 2003; Salazar et al., 2003; Salazar et al., 2004). In the social context, studies show that pigs are able to use odors/pheromones (compounds not specified) when discriminating between conspecifics (Meese and Baldwin, 1975; Mendl et al., 2002), and boar odour or androsterone may be utilized to stimulate oestrus in sows (e.g., Rekwot et al., 2001; McGlone et al., 2019a; McGlone et al., 2019b). A line of studies has also investigated the use pf pig appeasing pheromone to reduce aggression in pigs (for review see: Peden et al., 2018). This is of interest due to the frequent mixing of pigs within the pig industry (e.g., piglets are weaned and later moved from the weaner to the finisher unit, and sows are mixed after weaning).

While knowledge of pigs’ sense of smell with regard to feed palatability and detection of pheromones is relatively well documented, research on the more general olfactory abilities of pigs is sparse. As a result, some on-farm practices and management procedures might not be adapted to accommodate this sensory modality of pigs, nor may it satisfy pigs’ motivation for using their sense of smell. This is first and foremost a welfare issue, as pigs may suffer from living in an environment with low levels of olfactory stimulation, which may lead to boredom or anhedonia (Figueroa et al., 2015), and exposure to high concentrations of potentially aversive gasses such as ammonia [NH₃ (Koerkamp et al., 1998; Seedorf and Hartung, 1999; Jones et al., 2001)] and hydrogen sulfide [H₂S (Beauchamp et al., 1984; Ni et al., 2021)]. Conversely, there may be several ways in which more knowledge of the olfactory abilities of pigs could be used for optimizing on-farm management. If pigs are given an outlet from boredom by stimulating their motivation to investigate through sniffing, odors could provide a means to reduce abnormal behaviors such as oral stereotypies (Lawrence and Terlouw, 1993) and tail/ear biting (e.g., Zonderland, 2010; Valros and Heinonen, 2015; Godyn et al., 2019) and possibly lower aggression (Godyn et al., 2019). If current concentrations of gasses such as ammonia and hydrogen sulfide are aversive and/or harmful to pigs, regulations should account for this, and means should be initiated to prevent exposing pigs to such concentrations. Improving the olfactory environment in commercial pig houses could benefit on-farm management as well as the welfare of the animals, ultimately resulting in a more sustainable pig production. If science is successful in mapping the odors that pigs can detect and differentiate and find aversive or attractive, the favorable chemicals might be used as enrichment, as conditioned stimuli, or to increase feed intake during critical periods in a pig’s life.

This review explores the available literature on pig olfaction, with the aim of elucidating the current knowns and unknowns within the topic. The review covers topics such as chemicals in the pig environment, olfactory organs of the pig, olfactory detection and acuity, behavioral reactions to odors, aversive odors, reaction to novel odors, attractive odors, and odors as a management tool in commercial pig production. Due to the limited available research, literature on feed palatability and taste preferences will be included when relevant but these are not the main focus of the review, and hence the authors refer to the original papers on feed palatability for readers who might wish for further details (e.g., Jacela et al., 2010). The review further seeks to elucidate potential risks in terms of animal welfare in the commercial pig industry that the lack of knowledge poses, for instance poor olfactory stimulation or potentially harmful effects of chemicals arising from a poor air quality. Lastly, we suggest potential ways to utilize odors in practical pig management and identify promising areas still in need of further research. Based on these unexplored areas, we propose the most central new research questions, which should be the focus in order to improve pig welfare and sustainability of the commercial production.

In their daily life, domestic pigs will encounter various types of substances, which may or may not be odorous. In commercial pig barns ammonia and hydrogen sulfide are present at varying concentrations (Hoff et al., 2006; Ni et al., 2021), and the buildings and inventory of a pig barn may also emit odors. As pigs are housed in groups, and typically with several groups within one barn section, each pig will be exposed to—and have to relate to—the smell of several conspecifics. The pig has evolved nine glands for the production of social odors [digital, preputial, vulvar, anal, mental, salivary, buccal, pre-orbital, and Harderian glands (Pond and Houpt, 1978; Watson, 2004)], illustrating the complexity of pigs’ social olfactory communication. Domestic pigs are also exposed to the smell of humans, as well as of straw, feed, and water (it is currently unknown if water is odorless or may contain odorants). Furthermore, when moved to a new barn section, pigs are exposed to the smell of disinfectants and cleaning agents, and in the farrowing barn there is often a smell of blood when piglets are newly tail docked and male piglets castrated. As pigs can encounter a broad variety of chemicals in their environment, definitions of the terms used to classify various chemicals and odorants in this review and within the scientific community are listed in Tables 1 , 2 . The tables include classifications of the chemicals and types of odors, as well as the definition and examples of such chemicals from the pigs’ environment.

In the next section, the review expands on the currently available knowledge on pig olfactory abilities and discusses the potential of using odors in commercial pig production and management. The review focuses on odors of non-social origin, meaning any odors arising from the pigs’ surroundings (for example, those listed as natural aromas in Table 2 ) and not from other pigs. In contrast to other odorants in the environment of the pig, non-social odors of complex structure are likely sparsely represented in commercial pig houses, whereas pigs are exposed to a variety of these under natural conditions. Based on the ubiquitous presence of such odors in the pig’s natural habitat, we hypothesize that these substances are of relevance to pigs—also when the animals are housed under commercial conditions. In addition, these types of substances are easily accessible and may be added to the pig environment without interfering with farm practices (e.g., by clotting the slurry system). Making use of such complex odors in management routines of commercial pig production is interesting with respect to improving or optimizing, for instance enrichment procedures to increase pig welfare. Knowledge about pheromones and complex odors from a social origin will be included when deemed necessary for the understanding of the proposed research questions or implications on farm, but it is not the main focus of this review (we refer to McGlone et al. (2022) for a detailed review of odors of social origin).

Like the majority of mammals, the pig’s olfactory, gustatory, and trigeminal systems are involved in chemical sensing (i.e., the sense of taste, smell, and somatosensation). While chemosensitivity involves both taste and smell, most mammalian animals rely on olfaction as the primary chemosensory modality, which makes the olfactory systems prominent and well developed (Wackermannová et al., 2016). Although the pig has functional trigeminal sensory neurons (Salazar et al., 2000) that likely play a role in pig olfaction, the below sections will focus on the two most studied olfactory systems of the pig: the main olfactory system and the accessory olfactory system.

Only a few studies have sought to demonstrate the olfactory acuity in pigs. Jones et al. (2001) found that juvenile Duroc × Landrace crossbreds had an olfactory detection threshold for butanol at 2.09 parts per trillion, and Sondergaard et al (2010) found a detection threshold for Göttingen minipigs of 0.05 parts per million (ppm) for ethanol and 0.01 ppm for ethyl acetate. As for other animal species, results of the study indicated inter-individual variability in the sensitivity (Sondergaard et al., 2010). For comparison, the detection threshold for methyl and ethyl acetate in humans are around 103 and 102 ppm, respectively (Cometto-Muniz and Cain, 1991). In a study by Laska and Seibt (2002), squirrel monkeys and pigtail macaques could detect ethanol at 368.55 ppm (110.56 for the best individual). In another study, Croney et al. (2003) tested whether pigs (so-called micro pigs) could utilize visual (colors orange and green) or olfactory (odors coconut and almond) cues to locate a food source in novel surroundings. Pigs provided with either a visual or an olfactory cue performed equally well in the test and the authors thus suggested that olfactory cues are as salient as visual cues for pigs in learning and foraging situations. Collectively these studies imply a high olfactory acuity in pigs.

Pigs are omnivorous animals and their natural sources of food are found sporadically within large home range areas. Hence, under natural conditions, pigs spend a substantial amount of their active time searching for food (Stolba and Woodgush, 1989). When pigs explore their environment, they rely on their sensory apparatus, which includes sight, hearing, taste, touch, and smell. To allow their olfactory organ to detect odorants of potential interest, pigs will direct their snout toward the odor, and sniff the air near the source to allow their olfactory organ to detect volatile odorants (see details about the pig olfactory organ and odor detection and acuity above). Sniffing behavior is a well-known part of pig exploratory behavior (Studnitz et al., 2007), and since pigs are already able to utilize olfaction at birth (Morrow-Tesch and McGlone, 1990a), sniffing/smelling is an innate part of pigs’ behavioral repertoire. Pigs display sniffing in several situations, for instance when exploring odors and new environments, and sniffing is also an important part of feed-seeking behavior (see: Studnitz et al., 2007). The pig will use its snout to sniff and root in the substrate to locate edible parts, and, to some degree, to satisfy a motivation to explore (termed inquisitive exploration) (Wood-Gush and Vestergaard, 1989; Day et al., 1995). Sniffing and rooting are thus often connected. Explorative behavior may, moreover, include licking and/or biting the substrate. While solely inhaling the air near an odor may not allow for the detection of less-volatile substrates, rooting, licking, and biting behavior may allow the less-volatile substrates to be detected by the VNO ( Figure 1 ). In addition to sniffing, rooting, licking, and biting behavior, pigs may also express rubbing and rolling behavior when exposed to certain odors (Rørvang et al., 2023b.). These behaviors were recently described as a response to odors in pigs for the first time, and, although the mechanisms underlying the behaviors are not fully understood, the behaviors emphasize that pigs’ behavioral repertoire when exposed to odors includes more than just sniffing and rooting. However, it remains to be shown if rubbing and rolling behaviors imply that physical access to odors is important to pigs, and if, when given access, these behaviors will increase or decrease. Nonetheless, some odors seem to evoke specific types of behavioral reactions in pigs (as, e.g., rubbing and rolling), emphasizing the need for further studies of how pigs perceive the chemicals in their surroundings.

The abovementioned illustrates that, when conducting pig olfactory research, it is important to consider which behaviors are relevant to include with regard to the study aim. For example, if investigating the suitability of a given odor as enrichment for pigs, measuring only sniffing behavior would likely not paint the full picture of pigs’ interest in, or preference for, the odor. We therefore recommend that researchers consider the full odor exploration behavioral repertoire by (1) allowing pigs physical access to the odors studied to allow for the display of licking, biting, rooting, rubbing, and rolling, as well as other relevant behaviors not currently mapped, and (2) including the aforementioned behaviors in the ethograms when studying pig odor exploration. If, on the other hand, the study aims at clear-cut olfactory research as, for instance, pigs’ ability to detect a given odor, then pigs should not be allowed physical contact to the odor, to avoid confounding smell and taste of the substrate being tested. It is important to consider the health status of the olfactory organs of the pigs, as recent studies on the pig VNO have shown that inflammation of the VNO leads to increased aggression (see above, and Asproni et al., 2022; Mechin et al., 2022) and thus this will affect the results if pigs are tested/housed in a social environment. Lastly, it may also be important to consider the previous housing conditions of the animals studied, as Jones et al. (2001) found indications that prolonged exposure to 40 ppm NH3 was damaging to the olfactory apparatus of pigs.

In the below sections the review considers potentially aversive and attractive odors and discusses the implications these may have on the welfare and production of pigs in a commercial environment. Unfortunately, so far, no studies have sought to clarify why pigs appear to perceive some odors as aversive and others as attractive. Therefore, it is not known if attractive/aversive odors share some specific structural/chemical properties or whether the reactions are elicited by, for example, the concentration or potency of the odors.

In their pioneering study, Morrow-Tesch and McGlone (1990a) demonstrated that piglets learn to recognize the odor of their mother within the first 12h after birth. Before that time, a maternal–neonatal pheromone is controlling nursing behavior (Morrow-Tesch and McGlone, 1990a) ( Figure 3 ). The authors further suggest that the olfactory abilities of piglets should be considered when aiming to modify pig behavior to improve survival. Attractive or controlling odors are thus a central aspect of the life of pigs. In this section we focus on complex odors of non-social origin, as studies of pig pheromones and the effects of these are covered elsewhere (e.g., McGlone et al., 2022).

Only a few studies have assessed pigs’ interest in odors of non-social origin. These studies have mainly used complex odors and only a few controlled for taste (i.e., pigs are restricted from licking/eating the odors) and thereby purely tested for the effect of smell. Blackie and de Sousa (2019) investigated if weaner pigs (housed in a semi-barren environment) showed a preference for an odorized rope with garlic to a non-odorized rope. The pigs showed a preference for the odorized rope and although the authors noted habituation over time (2-week testing period), interest was reinstated by re-spraying the odor onto the rope. It is unclear if the pigs preferred the odorized rope due to the taste or smell, or a combination of the two, as pigs had physical access to biting and licking the ropes.

In conformity with this, Nowicki et al. (2015) found that pigs spent more time near natural odors (in the Nowicki article termed “aromas”)—moist soil, grass, and dried mushrooms—than synthetic odors—vanilla, orange, and strawberry, with strawberry being the most popular synthetic aroma. In a second part of their experiments, Nowicki et al. (2015) further showed that pigs used odorized objects (aromas of natural origin) for longer than identical odorless objects, although the detected difference was insignificant. Moreover, the authors found that, although the interest in the objects decreased over time, interest in the odorized objects remained at a higher level for the duration of the experiment (14 days). Changing the odor after 14 days resulted in a significant rise in interest in the odorized object in comparison to odorless objects. These results suggest that a given enrichment object or material may have increased value to pigs if odors are added to it, and, further, that odors in general may constitute a useful tool to increase the attractiveness and durability of enriching objects and materials.

In a recent study, we and our co-authors investigated pigs’ interest in a range of complex odors of non-social origin (Rørvang et al., 2023a). The study was an attempt at mapping pigs’ ability to detect and distinguish between such odors and to evaluate pigs’ interest in each odor. The pigs were free to explore and sniff the odor but did not have access to physically bite/lick/touch the odor source (i.e., not able to taste the odor). The study showed that pigs were able to detect and differentiate between all odors and that sniffing, licking, biting, and rooting were common parts of pig odor exploration behavior (as pigs directed these behaviors toward the odor, rather than an odorless control) even without having physical access to reach the odor. None of the odors, however, elicited more sniffing (as a measure of interest) than others, although non-significant differences were found. Moreover, since pigs were tested in pairs, social behavior was observed when pigs were exploring the odors. Pushing of the other pig while sniffing the odor, bite aggressions, and displacements of the other pig from the odor were observed, and these were almost exclusively expressed while exploring the odors as opposed to the odorless controls. The occurrence of these social behaviors was not dependent on the specific odor (Rørvang et al., 2023a). Collectively, the results of the above-described studies imply that odors are perceived as a resource to pigs, and that access to odors may constitute enrichment either directly via sniffing or when applied to other existing enrichment materials. However, odors should be selected with care as some may result in aggression/resource guarding. Further studies on the use of odors as enrichment materials are needed.

In this section, we want to highlight the five areas identified for future study into pig olfaction, identified as the most urgent for the sustainability of pig production and for improving the welfare of commercially housed pigs:

(1) Ammonia and hydrogen sulfide are a major concern in animal welfare as these gases are present at temporarily high concentrations in all types of pig house units and barn sections. Future studies should aim to clarify what levels of ammonia and hydrogen sulfide are acceptable when considering the welfare of the pigs, and the potential effects on the pigs’ olfactory abilities. Currently, the regulations and/or recommendations stating a maximum acceptable level of emissions are merely based on a concern for the humans working in the barn rather than a concern for animal welfare. Additionally, the standards are set from a human health perspective and do not consider how the animals (or human workers) may perceive the constant exposure to aversive odors. Future studies should thus focus on defining at which level or concentration these gases become unpleasant, aversive, and damaging to pigs (and humans).

(2) It may be argued that the smell of feed is attractive to pigs, but, considering restrictively fed pregnant sows, it may be that the constant smell of non-accessible feed (especially in the increasingly used automatic feeding systems (e.g., electronic sow feeders (ESFs)) is a stressor to the animals. Whether this is the case, however, is currently not known, and thus warrants further investigation to safeguard the welfare of sows.

(3) A large number of pigs are usually housed in the same barn section, and this arrangement means that each pig has to process and relate to odors of social origin arising from many different individuals. Whether this arrangement causes stress remains unexplored and deserves further studies, but it is also worth analyzing if pigs perceive the many different origins, or if pigs may habituate or only relate to the social odors in their very near vicinity.

(4) During management practices such as tail docking and castration, the smell of blood can become intense in the farrowing unit, at least to the human nose (personal perception, and personal communication with numerous Scandinavian pig farmers and staff). To the best of our knowledge there are currently no studies on how this exposure affects the animals—with respect to the smell of blood from both unfamiliar animals and siblings and offspring—and hence it is unknown if measures should be taken to limit or cover up the smell. As a first step, it is necessary to investigate if pigs detect the smell of conspecific blood, and secondly whether this odor is perceived negatively.

(5) A variety of odors is present in pig houses, but usually the odor composition is rather constant throughout the life of the pig. Hence, the olfactory environment lacks complexity in terms of odor variation. Considering the macrosmatic pig, it would be worth looking into if a lack of olfactory stimulation can contribute to boredom, and if odor stimulation could reduce symptoms of boredom. Additionally, it would be relevant to unravel if olfactory stimulation of pigs affects pigs’ sense of smell, thereby improving pigs’ olfactory abilities; the equivalent has been documented in humans (Oleszkiewicz et al., 2021). Since odors do not interfere with the inventory or housing system and could readily be applied by, for instance, spraying odors onto existing enrichment material, it may be relatively easy to implement “odor provision” and thereby stimulate these macrosmatic animals. These are all central future research questions in order to refine and optimize commercial pig production management and systems.

Olfaction is a central part of the life of pigs. However, pigs’ highly developed sense of olfaction combined with the conditions of commercial pig production gives rise to concerns for animal welfare. Various emissions from pig barns and chemicals used inside the barns may be perceived as aversive by the animals, which could be detrimental to their welfare. Contrarily, other odors, rarely present in pig facilities, appear attractive and could hold enriching properties for pigs. Considering the central role of olfaction, improvements to the olfactory environment for commercial pig-producing facilities could be a major step forward in improving the welfare of our farmed pigs and the sustainability of the production system.

Author contributions according to CRediT in the order authors appear on the paper: S-LS: conceptualization, investigation, writing—original draft, writing—review and editing, and funding acquisition. MR: conceptualization, methodology, investigation, resources, writing—original draft, writing—review and editing, visualisation, project administration and funding acquisition.