The Indirect Impact of COVID-19 on the Life of Animals
Mansi Rana1, Ros Rouse2, Tim J. Craig1, Heather Macdonald1, John T. Hancock1*
1 - Department of Applied Sciences, University of the West of England, Bristol, UK
2 - Research, Business and Innovation (RBI), University of the West of England, Bristol, UK
The COVID-19 pandemic is an ongoing major health crisis that is the result of the SARS-CoV-2 virus. The virus was first identified in Wuhan, China during December 2019; many patients were initially reported with pneumonia and later the cause was found to be a coronavirus, and soon it was spreading across the world. As of March 2022, the virus had reached 220 countries and had caused 6 million deaths worldwide. There are many impacts that COVID-19 has had directly and indirectly on humans. There are direct effects on animals too, with many testing positive for the virus. However, many indirect effects of COVID-19 on animals have been overlooked. Such indirect effects include euthanasia, abandonment, entanglement in PPE, and reduced funding for animal welfare projects. With the knowledge and experience gained from the COVID-19 pandemic it is hoped that lessons can be learnt so animal welfare is better managed for any future viral outbreaks.
1 - Introduction
The COVID-19 pandemic was originally thought to have originated from the Hubei Province of Wuhan, China and is believed to come from Huanan Seafood Market, a ‘wet market’ where animals are sold live or slaughtered at stalls in the open . However, this origin has been contested , with some people postulating that the virus originated from a bat species many kilometres from Wuhan, and that it entered the human population from a biosecurity breach from a Wuhan laboratory. What has been established is that the most similar viral sequence to that of the SARS-CoV-2 virus is indeed a virus that originated in a bat, but how it started to infect humans, and whether an intermediate species was involved is yet to be determined, and indeed, this may never be established.
What is also known is that humans are not the only animals susceptible to the virus. Many other animal species have been found to be SARS-CoV-2 positive including non-human primates, dogs, cats, mustelids (such as mink), deer, and hamsters. Some animals become mildly ill, whilst others have died, for example, big cats have died in zoos . For a full list of which animals have tested positive for the virus in the USA see .
Although the death of animals because of a SARS-Cov-2 infection is not good, especially if they are part of a zoo collection , the virus has had a range of other consequences for animals; the indirect impacts. Many countries, including the UK, went into extended lockdowns where peoples’ movement, and that of companion animals, was restricted. Indeed, in some country’s lockdowns are still happening. Xi’an in China went through a lockdown in July 2022, for example . As discussed below, such lockdowns have positive and negative consequences for animal welfare. Other effects on animals are caused by the increase in the use of Personal Protection Equipment (PPE). Here, some of the indirect effects of the COVID-19 pandemic are reviewed.
2 - Animal Euthanasia/Culling
Animals, in particular bats, were thought to be the cause of the COVID-19 pandemic, as it is thought to be a zoonotic disease. It may have also infected humans through an intermediate species. Such suggestions throw the blame for the COVID-19 pandemic onto animals and therefore they have, in some cases, become vulnerable, with some killing of animals because they are thought to be associated with the spread of the virus. Even with the lack of evidence, there appeared to be a “shoot first, ask later” attitude.
With the continued debate about the origin of the virus, many still believe that bats were the cause and that pangolins were an intermediary species. As a consequence of this, there has been an increase of concern over the conservation of these animals, especially bats, with some being killed . Therefore, even if there is no direct evidence of these animals being involved , such animals may be threatened. However, others are questioning the involvement of these species , with these authors stating: “… bats and pangolins must be conserved and not blamed…”.
One of the animal groups that has posed most concern for the spread of the SARS-CoV-2 virus is the mustelids, which includes mink. It is not only that the animals were virus positive, but that they could re-infect humans in the vicinity . One of the concerns here is that the virus may mutate in the animal population before jumping back to humans, and so the current vaccination programmes will be put in jeopardy. Once this was realised there was a mass euthanasia programme in several countries. This included Denmark, Spain and the USA. In Denmark alone there was the culling of 17 million minks at more than 200 mink farms in November of 2020 . Despite this mass killing there was little evidence of variants in the virus arising in these mink populations that would be more harmful to humans . The euthanasia programmes appeared to be put in place as a precautionary measure as much as anything. On the other hand, as the animals were being farmed for fur, they would have been killed later anyway, and outbreaks in mink farms threw into relief the crowded nature of such breeding facilities.
In a similar scenario, hamsters were found to be SARS-CoV-2 positive and were thought to have infected the pet shop workers in Hong Kong. Subsequently 2000 hamsters were euthanised along with other small mammals; this was spread across 34 different pet stores . It was stated that authorities in Hong Kong “has maintained a "zero Covid" strategy” and that the animal killing was a “preventative measure" . Similarly, there has been news of three cats being euthanized in China, again as a precautionary measure. It appears that the owner gave no consent to the government to treat the cats in this manner .
Clearly, the COVID-19 pandemic has led to the deliberate killing of numerous animals (for example, millions of mink), not because they were all infected, but because they were deemed to be a hazard for public health.
3 - Lockdown on Animal Life and Welfare
As pointed out above, one of the methods employed to attempt to stop the spread of COVID-19 is to establish a lockdown and insist on social distancing in different countries and so reducing viral spread. Interestingly, in many ways this had a positive impact on animal welfare. With fewer humans on the streets and countryside there was less interaction with animal populations. Animals could roam in places where before the lockdowns they would have felt vulnerable. This manifested itself in several, what at first seemed, strange reports. For example, there were sightings of puma along the streets of Santiago, Chile , herds of deer spotted in Nara, Japan  or even groups of ducks crossing the roads of Paris, France . All these observations conveying an easier and carefree way of living for these animals, away from human interference. There was also a significant shift in behaviour of other birds. There were more sightings of some species and many had longer stays within bird sanctuaries. The species of bird affected included open bill stork, spot-billed pelican, grey heron, spoonbill and many more . Usually, noise pollution is seen to have a negative effect as birds require more energy to sing at a higher pitch, however due to reduced human activities noise pollution was reduced allowing birds to sing at a normal pitch . This in turn caused a positive effect as their energy would be preserved for other parts of their life such as maintaining a healthier immune response or increased breeding . On the other hand, the effects of seeing more animals in unusual spots and urban areas could be due to food scarcity. Many different animals depend on humans as source for food, including gulls, pigeons, street cats, dogs and monkeys. Therefore, lockdown measures have generated an impact on their diet and well-being . As lockdown causes less human interaction and no tourism, this means that leftover or spilled foods are less likely to be found for the animals, resulting in more starvation . As Reid says: “this could cause starvations, lower breeding success and perhaps cause populations to decline”.
In conservation areas there have been positive effects too. Sea turtles have seen an increase in breeding in Thailand, India and Florida , probably because of the reduction of human interactions. However, it is not all good news. Conservation International stated: “There is a misperception that nature is ‘getting a break’ from humans during the Covid-19 pandemic. Instead, many rural areas in the tropics are facing increased pressure from land grabbing, deforestation, illegal mining and wildlife poaching.” . With a reduction on park rangers and less money, there is evidence in parts of Latin America, Asia and Africa that there have been spikes of poaching activities and wildlife conflicts . In the Mayurjharna Elephant Reserve, Eastern India, an elephant corridor project had to be left incomplete due to lockdown measures and this in turn resulted in elephants terrorizing villages and homes. To stop this continuing 5 elephants were killed . Facing a lack of ecotourism in Brazil 600 jaguars were found slaughtered, displaced or burned by fires in the Pantanal. Sloth sanctuaries have also come user pressure. Lockdowns have dramatically reduced donations and in turn many of these animals are left vulnerable .
Therefore, although it can be seen that there are several positive effects of the pandemic on animal populations there are many detrimental effects too. The lack of human interactions during lockdown is in some ways mirrored by the effects of a nuclear disaster. It has been recognised that the exclusion zone around the Chernobyl power station has become a haven for certain wildlife, although this is a complex situation and many species have also declined . Nature, therefore, sometimes seems to prosper when human activity is removed. On the other hand, with many people forced to stay home during lockdowns, many veterinarians were limited to only serious appointments. As a result, many animals were not able to have their routine check-ups, having a detrimental effect on many animals .
Overall, lockdown was not good for many animal groups. With human movement limited, and subsequent spending, finances have been tight for many organisations and animals have suffered.
4 - Lockdown on Companion Pets
Companion pets have faced a lot of impacts regarding the COVID-19 lockdown which has mainly been indirect. Initially, during lockdown many people were working from home which initiated many mental health problems as their day-to-day lives came to a halt . Studies show that companion pets may help, combating loneliness and stress as they allow companionship and emotional support to their owner, and as an effect of this many adoption rates and pet ownership were seen to have increased . Many pets were rescued from shelters and put into homes where they are cared for and looked after . This all sounds good for improved animal welfare.
However, companion pets have also experienced the harshness of lockdown. As lockdowns bit, many individuals witnessed an economic crisis as companies and businesses were left bankrupt . Many families were left with no choice but to rehome (or abandon) their pets as they would not afford to look after them. Others were concerned about the transmission of COVID-19 from other animals or humans to pets (with the risk of transmission within the household), and in some cases, there appeared to be an inability of owners to recognize the responsibility of owning a companion pet . On the other hand, Morgan et al.  state: “Our data indicate that not only is the concern of increased dog abandonment not justified, at least so far, the opposite has occurred.”. Although some areas, as discussed above, are reporting the a different situation, Morgan et al. found in their study that the number of adoptable dogs decreased, as did the length of stay of the animals at the shelters.
Even as life started to return to normal, pets are also faced with a consequence as many owners will find it difficult to handle owning a pet once they are able to go back to the office or workplace. There are concerns that this will result in additional abandonment rates . Many pets are also predicted to experience separation anxiety as a result of their owners going back to their normal lives where their time is not spent at home with their pets; this meant that many of these animals may face distress or discomfort .
It appears that lockdown may have had a benefit for some companion pets, but as life returns to ‘normal’ there may be abandonment issues and overall, the welfare for many animals has suffered because of the COVID-19 pandemic.
5 - COVID-19 on Aquatic Animals
Evidence of the direct effects of COVID-19 on aquatic animals is hard to find. Although there seems to be no direct evidence that aquatic mammals have been found positive for the SARS-CoV-2 virus there are predictions that they may be susceptible. Such evidence is based on the sequence homology of the ACE2 protein, as discussed in an earlier “Members article” on the AWRN website, and highlighted by others . Mammals such as whales, dolphins and seals are predicted to be of “high” susceptibility. Is it likely that this will manifest in a problem? Sewage water could be one of the main sources from which aquatic animals could catch coronavirus, but there have been no cases of live virus found . There have been fragments of the virus genetic material found in wastewater, however, this is an indication of spikes in human cases in an area and does not correlate with infections reported in aquatic animals .
Recently, China has started to test for the virus on fish and crabs in Xiamen, with COVID-19 PCR tests being used. However, this has already be reported in Hainan. Clearly there is a concern than fish and other seafoods may be able to transmit the virus to the local human population 
As discussed below, as well as direct effects of the virus, the pandemic created a significant quantity of litter and this did have effects on aquatic life. However, because of the vastness of the oceans and the difficulty in tracing and monitoring aquatic animals there may be a larger problem than reported. The marine mammals are certainly a group which needs to be carefully looked at in the future.
6 - COVID-19 Litter and its Impact on Animal Life
As a result of the COVD-19 pandemic many precautionary measures had to be put in place in order to prevent the transmission of SARS-CoV-2 in the human population. One of these was the use of personal protection equipment (PPE), including the use of face masks and gloves. A proportion of such items are deposited as litter. It is not unusual to see masks lying on pavements and on footpaths. Unfortunately, this can have a profound effect on animals.
After mandatory face mask wearing in the UK, PPE were found to be present on 30% of beaches . At the uninhabited Soko Islands of Hong Kong 70 face masks across just over 100-metre stretch from the beach were reported, and then more later . In a social media trend known as “#glovechallenge” more than 11,000 photos of COVID-19 litter were posted . Such litter may cause problems to animals through entanglement, entrapment and ingestion. The immediate effect may be death from suffocation or drowning. Animals may have feeding difficulties from strangulations, and entanglement can cause wounding and infection, which can later result in amputation . For example, in the canals of Leiden, Netherlands, a freshwater fish was reported dead after being entrapped in a latex glove. In Chilliwack, BC, Canada, a robin was found entangled in a face mask . Furthermore, PPE can be ingested by animals, as seen in Brazil where a Magellanic penguin ingested a face mask . Traces of the mask were present in their stomach. Several long-tailed macaques were also seen consuming face masks in Genting Sempah, Malaysia . It is not all negative, however. In The Netherlands and Poland birds were seen to use gloves and medical masks as nesting materials .
PPE and medical waste from the general population is certainly a major problem. Much of the PPE is plastic-based and does not readily degrade, meaning that is likely to persist in ecosystems for a considerable time. Animals will suffer, and lessons need to be learnt for any future epidemics/pandemics.
7 - Animal Coronaviruses
COVID-19 is caused by SARS-CoV-2 and this virus readily infects humans. It can also infect a range of animals, including cats, dogs and mustelids. However, there are many other animal coronaviruses, and this can cloud the diagnosis of the animals. For example, there are canine and feline coronaviruses.
Canine coronavirus (CCoV)  is known to infect dogs and puppies which can cause multiple different symptoms, including fever, lethargy, diarrhoea and vomiting. There are two genotypes reported: CCoV-I and CCoV-II. The latter affects puppies more harshly . It appears that dogs can also harbour the canine respiratory coronavirus (CRCoV) which later can develop into the canine infectious respiratory disease complex (CIRDC).
Cats, meanwhile, are susceptible to the feline coronavirus (FCoV) . Felines are known to be more susceptible to the SARS-CoV-2 virus than canines and reveal other types of symptoms , including signs of complications within the upper respiratory tract and diarrhea; there was also a mutant variant present within a small population of cats which caused infectious peritonitis .
Therefore, the suspected symptoms of SARS-CoV-2 may be due to the infection of the animal with a different, more species-specific, coronavirus and it cannot be assumed that the animal is SARS-CoV-2 positive. This makes a quick diagnosis difficult and can make owners suspect that the animal is suffering ‘COVID-19’ when it is not. Regular testing of animals is not routine, although there are now animal-specific COVID-19 vaccines available [41,42].
8 - Animal Models and Testing during COVID-19
As the COVID-19 pandemic continues, with new SARS-CoV-2 variants likely to appear in the future, the need for new vaccines or drugs becomes more important. Consequently, the race for an animal model began, as it can be used to understand how the transmission of COVID-19 occurs and for the development and testing of a new treatment . The World Health Organization (WHO) therefore has assembled a panel to contribute to the development of animal models in order to find a therapeutic option against COVID-19; as a result of this there have been numerous animals that have been used for testing . One of the models produced are mice infected with the SARS-CoV-2. These animals appear to have presented with very mild disease; as time passed on the mice later developed encephalitis, severe pneumonia, thrombosis and anosmia . Similarly, Syrian hamsters after infection of the virus manifested with mild to moderate symptoms of the disease, alongside the symptoms of weight loss, respiratory distress and lethargy, although the hamsters were seen to have recovered after 2 weeks of infection . During the search for an animal model, ferrets were also included in the study where healthy ferrets were infected with SARS-CoV-2. These animals soon showed signs of lethargy, nasal discharge, sneezing and loose stools .
Therefore, one of the indirect effects of the pandemic is the use of laboratory animals. These animals suffered the symptoms of the virus and would have been subsequently euthanised. Many petitions to ban animal testing have been put forward which would help save the suffering of these animals. However, the current COVID-19 pandemic has brought to the fore the fact that the public currently rely on animal research when it comes to therapeutic options . As the pandemic wanes, the use of laboratory animals will no doubt continue, especially as there is a search for ways to stop or mitigate the next epidemic/pandemic.
On the other hand, animal vaccines have been developed  and will no doubt continue to be rolled out around the world, so this will be a benefit for future animal welfare.
9 - Conclusions and the future
Although the COVID-19 pandemic has had devastating consequences for the human population around the world, many animals have suffered too. Several species are susceptible and have tested positive for the SARS-CoV-2 virus, and some have subsequently died .
As well as the direct infection of animals with the virus, there are numerous indirect effects of the COVID-19 pandemic on animals. Lockdown may have increased the roaming of some animals, and it can be argued that some have benefited. There are many negative effects too, including animal culling because of the scares over their detriment to human health, the abandonment of animals no longer needed, and the necessary constraints upon the service which could be offered by veterinary surgeons. Animal conservation areas and sanctuaries have found their funding slashed and many animals have suffered as a consequence.
In the understandable race to protect human health, PPE has been produced in vast quantities and a significant amount has been left as litter, with animals becoming entangled and suffering from trying to swallow it. Plastics in the PPE will no doubt persist in the environment for years too.
COVID-19, or at the virus causing it, may well have originated in an animal population, i.e. bats, but it has also had a profound effect on many animals around the world. To prevent a future pandemic, more needs to be understood about the mutation of coronaviruses, how they are transmitted in animal populations, and how they can infect human populations. But also, what is also required is a clearer understanding of how the animal populations across the world will suffer as an epidemic/pandemic unfolds. There are huge populations of animals for which is virtually nothing is known, despite the prediction of them being SARS-CoV-2 susceptible, such as the marine mammals. Clearly more research about animals is required .
The world will see future epidemics/pandemics, and it is hoped that the COVID-19 pandemic will open the eyes of many to the suffering of animals and how we can help prevent this in years to come.
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