Are social groups at higher risk of disease?

By Zikora Izuora, Sarah Lange, Savannah Mendoza, Amy Norheim, Thomas Thurlow, and Rachel West (Edited by Anna Mosser)

It is generally assumed that animals living in social groups, and therefor living in close proximity to one another, are at higher risk of infectious disease. Verifying this claim, however, is not an easy task, as the availability of direct comparisons between non-social and social groups are limited, adaptions to risk reduce disease prevalence in social groups, and measuring disease presence is often difficult to do.  Still, some direct evidence does show a link between social interactions and disease transmission, while other evidence indirectly reflects the risk, namely years of evolutionary adaptation to the increased risk of diseases in social groups. Interestingly, in some circumstances the risk of disease is actually lower in social groups. Below we review the question of whether social animals are at higher risk for disease in six different types of social animals…

Birds

In one study, trying to determine how bird feeders accounted for the prevalence of a disease in wild birds, Mycoplasma conjunctivitis was enhanced in areas of increased bird feeder density (Moyers et al., 2018). Groups of birds feeding on the same source increases the likelihood of the disease being spread, much like in a social group. Another article referred to colonial breeding which is a form of social reproduction seen in birds. They compared solitary to colonial species and found an increase of parasite infestation. They noticed that the prevalence of blood parasites was higher in colonial than in solitary species (Tella, 2002).

Winter crow roost
(https://www.flickr.com/photos/moonjazz/6786116363)

Further due to the range of places visited by birds, they can spread the virus over large distances. This is shown in the migrating patterns of birds. During the winter, crows enter communal roosts with thousands of other birds. This close contact has facilitated the spread of the West Nile virus during cold winter when mosquitoes are not blood feeding. This has allowed this virus, which is usually not as active during winter, to spread to other birds (Montecino-Latorre & Barker, 2018). This shows that gathering in groups of high density leads to the increased transmission of disease.

However, there are examples where social groups do not have an increase in infection rates. In a study of American robins, they found that the per-capita number of mosquitoes, a vector for West Nile virus, was lower at communal roost sites, reducing the individual risk of transmission (Janousek et al., 2014). For host-seeking vectors, and presumably parasites, social groupings provide the benefit of a dilution effect.

Burrowing animals

Living in close quarters with infected individuals could lead to disaster for a group of burrowing animals who live in underground tunnels with limited circulation, yet there are still many examples of social burrowing animals. Burrowing animals are at an advantage when it comes to avoiding parasites due to their underground homes. The subterranean location leads to decreased diversity of parasites, but restricted movement caused by the tunnels may lead to an increased burden of individual burrowing animals (Archer et al., 2017). This decrease in parasite diversity underground could allow for burrowing animals having an increased ability to be social when faced with the risks of an enclosed burrow.

Naked mole rats in burrow
(https://commons.wikimedia.org/wiki/File:Naked_Mole_Rats-cropped.jpg)

When considering the impact of infectious diseases and parasites on burrowing animals, the naked mole rat must not be ignored. As described by Schilze-Makuch in his 2019 study on the potential for increased intelligence of naked mole rats, they are one of the two eusocial mammal species. A naked mole rat colony has one breeding female with 3-4 consorts and up to 300 nonbreeding subordinates. With the close quarters they keep, it seems that one parasite would wipe out the whole colony. Naked mole rats seem to have adapted to this threat, and have evolved to be very sanitary creatures. As individuals and as a population they are cleaner than humans (Schulze-Makuch, 2019). Subordinate naked mole rats consistently groom offspring and keep separate chambers for the toilet, sleeping, and food storage (Buffenstein et al., 2012; Watarai et al., 2018). 

European badgers are social animals that burrow in groups of around six in a group territory. It has been found that male badgers are more likely to contract diseases because of a testosterone-induced immune-deficiency, and that badgers with a larger radius of exploration are more likely to contract disease than those with a smaller radius of exploration. In a study of bTB in European badgers, higher movement between social groups resulted in a higher number of cases (Weber et al., 2013). The interactions between different social groups is a cause for spikes in cases, meaning burrowing animals with looser social groups are likely at a higher risk of infection than those with more restricted entry.

Gophers are independent burrowing animals. Despite their distance from each other, the same species of parasites were found in four different species of gophers in Texas and the presence of the two different parasites tested for was not statistically different from species to species. The non-social behavior of these gophers did not keep them from getting infected (Lebrasseur, 2017). 

Although there are no studies comparing the susceptibility of social and non social burrowing animals, there is evidence that animals that live in groups have adapted to avoid being overwhelmed by parasites, but interactions between different social groups can lead to an increase of infections. The independence of solitary animals does not protect them from being infected. Burrowing animals as a group get some defense from parasites by living underground, and this may increase the number of species able to live socially.

Social carnivores

Overall, in the majority of carnivore populations has have been a decrease in populations, and infectious diseases have contributed to the decline and account for 45% and 3% in social and solitary carnivores, respectively (Sanderson et al., 2014). These statistics suggests that carnivores are at a greater risk of contracting diseases. When analyzing disease prevalence in social carnivores, it is important to understand Allee effect and its significance. Within social groups, the Allee effect is an increased risk of extinction for the group if the total or density of individuals decreases until it falls below a certain threshold as a result of ecological or genetic factors. These factors typically include habitat loss, persecution, and the negative perception humans have of carnivores. Due to this, the Allee Effect is able to impact a carnivore’s social group when it is below the threshold because of the increase in the chance of inbreeding and less genetic diversity from a smaller group size (Sanderson et al., 2014).

Additional theoretical analysis has shown relationships between social groups and multi-host pathogens. The effects of a multi-host epidemic in regard to size, velocity, and spatial pattern are unique to the

Lions fiercely defend
their territories
(https://pixabay.com/photos/lions-friends-africa-predator-cat-4038314)

targeted social group’s structure. Disease is spread most quickly to multiple species through When the social structure permitts more neighbor-to-neighbor transmission (Craft et al., 2008). A factor determining whether the structure will allow for such interactions is how territorial the social group is and if they have more distrust towards their “neighbors” than “strangers” (Müller & Manser, 2007).

Another means for increased disease risk in social groups relates to the effects of chronic stress. In social groups individuals have to fight for food, mates, and space, and where these situations are more prevalent, individuals can experience persistent stress, which can lower the individual’s immune system’s efficiency (Kappeler et al., 2015). For example, lower ranking individuals are sometimes at great risk of disease or suffer the effects more severely.

 

Primates

The evidence for primates living in social groups being more susceptible to infectious disease and parasites is mixed. Living in large social groups is assumed to increase the risk of disease in populations of primates because there are more opportunities for transmitting communicable diseases (Griffin & Nunn, 2012). However, there is evidence that sub-grouping, smaller sleeping groups, isolated populations, and transitory social interactions diminish the risk of disease in primates. 

Increased social network modularity, sub-grouping in larger groups, has a negative impact on the risk of parasitism associated with living in larger social groups which could be a reason for the inconsistent empirical evidence on the association between group size and parasite risk (Griffin & Nunn, 2012). This is considered the ‘social bottleneck’ hypothesis where social subdivisions that form in larger groups act as barriers to the spread of infection, thereby weakening the association between group size and infectious disease (Nunn et al., 2015). A higher prevalence of infectious disease is associated with larger group sizes, but subgrouping reduces prevalence, acting as a ‘brake’ on disease spread between groups.

Many primates groom each each
other, removing ectoparasites
(https://www.needpix.com/photo/1203109/coat-baboons-ape-primates-animals-zoo-zoo-animal-sit-male-baboons)

In studying malaria infection rates of different Amazonian primate species, susceptibility to infection by Plasmodium brasilianum and frequency of bites by infected mosquitoes varied significantly across species (Daviews et al., 1991). A significant determinant of being bitten by an infected mosquito was the size of the sleeping group of each primate species. As primate group size increases, the average number of mosquito bites per host increases, thus leading to higher infection rates. (This contrasts with the dilution effect seen in some birds.)

Small, isolated host populations, specifically threatened species, that do not emigrate, harbor fewer of the three major parasite groups found in primates (helminths, protozoa, and viruses) (Altizer et al., 2007). Primates that spend more time interacting within-group prior to emigration, particularly larger-bodied primates, increase their individual risk of infection as well as that of their social group and the entire population (Ryan et al., 2013)(Ryan et al., 2013). A long-lived, large-bodied primate in a complex social system is more likely to sustain an infectious disease because the slow population turnover rate of certain primate species minimizes the population resilience.

Although the evidence for an increased susceptibility to infectious disease in primates living in social groups is mixed, social network modularity, small sleeping group size, smaller populations, and more transient social interactions are associated with decreased rates of infectious diseases in primates.


Fish

Social groups of fish—more commonly known as shoals—are among the most well-known examples of large aggregations of species available. Shoaling plays a major role in more than half of all discovered fish species including krill and herring which each can form two the largest animal aggregations on earth with nearly a trillion separate organisms grouped together (Ward & Webster, 2016). Intuitively, these groupings seem especially vulnerable to parasitism and disease given their sheer size and continual recurrence. However, research suggests the opposite positing that many shoals have a negligible presence of parasites and that individuals have a much higher propensity for parasitism than large shoals.

One of the reasons for this seeming contradiction is derived from the earliest entry point into the shoal. Using juvenile sticklebacks as examples, Dugatkin, Fitzgerald & Lovoie (1994) showed that given the option between parasitic and non-parasitic conspecifics, juvenile fish overwhelmingly avoid parasitic individuals. Since fish deal initially with ectoparasites, or parasites that live outside the hosts, there is a visible parasite often around the head or gills that is an evident physical marker of parasitism for other fish. In addition, Dugatkin et al. noticed erratic behavior by infected fish including odd swimming patterns and frequent trips to the water’s surface which the researchers thought to be in an attempt to free themselves from the parasite. These unique physical and physiological differences related to parasitism allows juvenile fish to largely avoid parasitic fish.

Mikheev (2009) moves beyond juvenile fish and highlights

Fish shoal
(https://www.piqsels.com/en/public-domain-photo-oduuy)

three main reasons why shoaling is effective in mitigating the effects of parasitism in grown fish already accepted into the shoal. He notes that most endoparasites use the gills as an entry point which makes the propensity for infection relative to the amount of water circulating through the gills. Since gill

respiration is directly correlated to stress levels, the proven lower stress associated with a shoal makes it conducive to lower levels of parasitism. However, this correlation between stress and contracting a parasite also reveals the adverse effect on shoals that predators can have. The strong presence of predators dramatically increases the stress levels on fish and also constricts the shoal, both of which increases the potential for parasitism. Once a fish gets a parasite, its chances of getting another soar because the parasites are drawn to the already weakened and slower fish who has begun to succumb to the effects of an initial parasite. This in some ways protects other fish within the shoal who are less likely to become infected. The third reason is due to the “oddity effect” which Mikheev (2009) and Dugatkin et. Al (1994) both cite as the reason why heterogenous fish are often eliminated from a shoal by predators first. In a shoal, fish that look or swim differently are noticed first by predators and are often the first prey that are killed. Shoals that contain a small minority of parasitic individuals will experience a quick dismantlement of infected members because the parasites physically impair the fish making them especially vulnerable to potential predation.

There is some controversy over the role of shoal size and density related to the potential for a parasite to spread within a shoal (Bagge et al., 2004; Sasal, 2003). Some researchers intuit that high-density groupings of fish have a significant impact on the spread of parasitism simply due to the amount of contact points available for a parasite to take advantage of. Sasal (2003) for example, using the coral reef fish (Haemulon flavolineatum), argues that fish density has a “positive effect” on the establishment of parasites while fish group size has no direct relation to parasitism, although he does note the tendency of parasites to prefer smaller shoals to larger ones. Bagge et al. (2004), however, dispute Sasal’s claims with their own findings involving the crucian carp (Carassius carassius). They found density to have no effect on the carp within a controlled environment and instead attributed total population size as the only factor to unify the variance in parasite abundance, or “monogenean individuals” as the research describes it. Suffice to say, there seems to be no unifying argument for shoal density or size having a strong impact across fish social groups and there is still room for more research to unify any theories favoring one or both factors. The fact that the research does not overwhelmingly support either factor again shows the strength of shoaling against parasitism despite the logical inference that groupings should cause higher infection rates. 

If parasites have already managed to infect many members of a shoal, the shoal often splinters into smaller groups containing fewer individuals (Seppälä et al., 2008). The infected fish often become strongly impaired by the effects of the parasite and naturally move to the peripheral of the shoal or even splinter from the shoal entirely to form a less cohesive unit filled with fish also impaired by parasites or deformities. These infected fish are unable to react and move in the same way that the spry, healthy fishes can and usually aggregate into smaller shoals filled primarily with parasitic conspecifics or even just become individuals without a shoal altogether. This helps keep the integrity of the healthy shoals intact in that members which are not homogenous to the shoal will naturally be selected against due to their inability to blend and keep up with the healthy fish or will be first attacked by predators due to the oddity effect. This natural vetting keeps the integrity of shoals healthy and strong by quickly eliminating factors like parasitism that cause weakness and vulnerability. The continual, dynamic nature of a shoal makes such vetting possible and is a rather unique factor separating fish from non-aquatic species. Thus, fish are naturally able to maintain shoals with high aggregates of individuals without the rapid spread of parasitism and disease with individuals or small groups containing most of the infected.

  

Social Insects

Studies of insects have shown the prevalence of disease to be high in social groups of a species, because of frequent interactions with others as well as population density within the group (Cremer et al., 2007). Behaviors exhibited by insects in social groups provide evidence that rates of disease are higher than in solitary groups.

High levels of direct interaction between social groups is one of the biggest factors in the spread of pathogens. Certain species of bumblebee and wasp, those that rob honey bee groups that are positive with DWV (Deformed Wing Virus), also test positive for DWV (Manley et al., 2015). Another form of transmission is indirect, usually through shared flower sources for pollination. In a controlled greenhouse study, with the only source of interaction between infected bumblebees with IAPV (Israeli

Honey bees groom each other
(https://commons.wikimedia.org/wiki/File:Honey_Bee_Grooming.png)

Acute Paralysis Virus) and uninfected honey bees, IAPV is transmitted to the honey bees (Manley et al., 2015). These methods of transmission of pathogens between and within social groups increase in risk as population density increases and more individuals are exposed to them. 

Disease is also an important issue addressed in beekeeping practices, often with integrated pest management procedures. Keeping multiple colonies of honey bees in close proximity to each other encourages the spread of those pathogens throughout the beekeeping farm (Zawislak, 2019). A strategy used in integrated pest management is to remove a generation of larvae that is infected in order to break the cycle. This practice is also seen in natural honey bee social groups, called hygienic behavior. Adult honey bees recognize broods that are anomalous or infected, and discard them from the colony (Mondet et al., 2016). The development of hygienic behavior in natural honey bee colonies is a sign that the species had to adapt to increased risk of disease.

Solitary insects such as the Japanese beetle also exhibit behaviors dedicated to reducing disease spread. Individuals will choose to avoid soil that has been infected with parasites such as entomopathogenic fungi (Meunier, 2015). These behaviors demonstrate the risk of disease transmission from contaminated surfaces, which indicates that more densely populated groups would have a higher risk of disease spread. Furthermore, group-living insects use more methods of limiting parasitic infections than solitary insects, and immunity to disease is not always higher in social insects than solitary insects, as demonstrated by Lepidoptera caterpillars and Australian plague locusts (Meunier, 2015). 

Studies on disease in social and solitary insects rarely compare the two types of groups, but there is ample evidence to conclude that disease is more prevalent in social groups of insects due to their recurrent interactions and adapted avoidance behaviors.

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