Our study combining field data and aerial imagery analysis clearly showed that the spotted souslik avoids close coexistence with another burrowing species, i.e. the European mole, in the period of low population abundance. This is the first study on this subject described in the available literature, as attention has been paid mainly to other parameters of the habitat so far14,18,20. The present results can (1) make a new contribution to the knowledge of the ecology of burrowing mammals and their interspecies relationships, (2) contribute to better designs of conservation and assessment of the quality of habitats of endangered burrowing mammals, and (3) indicate new possibilities of using remote sensing and deep learning methods in ecology and conservation. Below we will try to address each of these issues.
The interaction between underground animals is not a new idea in ecology (e.g.22); however, this issue has not been analyzed for the mole and the souslik so far. This was probably related to the fact that the potential negative or positive relationships between these species are not intuitively obvious. The spatial distribution of underground tunnels of these animals is completely different: the mole builds an extensive network of horizontal tunnels close to the ground surface, while the souslik usually builds one deep nest burrow with a vertical entrance and possibly a small number of shallow safety burrows near the nest burrow. Moreover, the food preferences of the souslik and the mole differ, i.e. the former is mainly a herbivore, while the latter is an obligatory predator. There are also clear differences in the annual cycle: the mole is active all year round, and the souslik hibernates in an underground nest for about half a year from October to March. Thus, it seems that the emergence of competitive relationships between these two species is unlikely. Our study shows, however, that these species avoid each other in space, which raises the question of the mechanism of this relationship. Based on the knowledge of the biology of both species, some hypothetical mechanisms can be proposed.
Although they are colonial animals, sousliks inhabit burrows alone (except for mother and offspring) and they have a strong behavioural trait of a negative reaction to the presence of other animals in their burrows and their close vicinity14,23. The negative reaction to other sousliks is a reflection of the intraspecific competition in the population and the territoriality of individuals. It is regulated by odour signals and the social structure of the population30,31. Koshev32 described aggressive reactions of free-ranging European sousliks to other vertebrate species that appeared near burrows: towards the reptile Lacerta trilineata, the bird Corvus frugilegus, and the mammal Mustela nivalis. Theoretically, the mole can get into the souslik’s burrow unintentionally when digging new tunnels. For souslik, the presence of moles in their nest burrow means a violation of its strictly defended territory and is probably a highly stressful episode. It can therefore be assumed that sousliks should choose places outside areas of frequent occurrence of other burrowing mammals to set up a nest burrow.
It remains an open question whether avoidance of areas where the mole is often present may be important for the souslik during winter hibernation. Theoretically, the presence of moles in souslik burrows during hibernation may disturb this process and cause waking up and energy-consuming increases in metabolism, which may reduce winter survival. It is also unknown whether the mole can be a predator for the souslik during winter hibernation. Remains of rodent species were found in the digestive tracts of moles33; therefore, at least theoretically, the mole may use such a food source. On the other hand, remains of vertebrates, including the remains of moles, were sometimes found in the stomachs of sousliks18. The relationship between the souslik and the mole may therefore be more complex and require further research focused on this issue. It is possible that the moles can avoid the souslik colonies as well. This scenario seems also realistic, since the moles home ranges are likely much more dynamic than that of sousliks, that likely benefit from dwelling within an existing colony of the conspecifics.
The spotted souslik protection requires the designation of special areas of conservation16. A number of various conservation activities are also routinely undertaken for this species, including regular monitoring of the population size, habitat monitoring, mowing, reduction of predation risk, and application of more invasive methods such as reintroduction. Similar activities are also performed for a closely related species, i.e. the European souslik Spermophilus citellus, in Europe. Importantly, in the current guidelines of souslik conservation, the issue of the competition with other species and its impact on spatial distribution is not considered. In turn, there is evidence in the literature that interspecies interactions may be important for the souslik population21. In periods of low abundance, when the survival of the population is at risk, the sousliks may have different habitat preferences than in periods of the abundant population20. It seems, therefore, that nowadays, when the souslik most often forms small populations, more attention should be paid to a wider range of factors and threats that may determine longer term population trends or the health condition, survival, and abundance of their colonies.
Our study indicates that, in the period of low population abundance, the presence of other burrowing species may be an important factor determining the distribution of sousliks. This observation shows that in addition to the assessment of the area and condition of the habitat the presence of other potentially competitive species should also be taken into account in the analysis of population survival. In such a case, the actual area of habitats suitable for sousliks in a given location may turn out to be much lower than assumed. In our study area, the habitat suitable for the souslik was reduced from 105 ha to approx. 65 ha, i.e. by nearly 38%, but it probably is even smaller (compare Fig. 8). This observation has consequences for improvement of the reintroduction methods of sousliks (or other burrowing mammals), which are constantly of scientific interest20,34,35. Our results indicate that the reintroduction of sousliks should be carried out in places where there is the lowest probability of competition for resources including even shelter or space with other burrowing species and where adequate space for the settlement of the population is ensured.
So far, investigations of the distribution of small burrowing mammals have been based on laborious field studies involving site inspections by trained observers (e.g.36,37,38). Our results show that, in certain conditions, high-resolution imagery can be successfully used to support studies of the distribution of such animals. As reported by other authors (e.g.7,10,12), however, such animals must produce clear signs of their presence in the environment. Evidence of the presence of the European mole, i.e. mounds of soil, in short vegetation habitats has shown that remote sensing can detect moles and their area of occupancy successfully. The advantage of these markers of the presence of moles is that the mounds are redundant and quite durable and can be visible in the environment for up to several months.
By combining field research and remote sensing, it is also possible to study more sophisticated ecological issues, e.g. interspecies interactions. In this work, the remote estimation of the distribution of moles facilitated estimation of the actual habitat available to the souslik and excluded areas with the lowest probability of its occurrence. As a result, the population may be monitored more economically. Since the conservation guidelines recommend monitoring souslik populations by means of laborious inspections of transects, the indication of areas with no burrows may significantly reduce the amount of fieldwork without negative consequences for the accuracy of results. Some areas of the souslik occurrence are large, e.g. Świdnik (105 ha) or Pastwiska nad Huczwą (150 ha), and every 10 ha to be monitored means one day’s work for one observer (according to the calculations presented in the results). Our study showed that when the area of the occurrence of moles is excluded from the monitoring (Fig. 8), the error in estimating the size of the souslik population will be relatively small (0.9–8.7%). At the same time, the time devoted to the research can be limited by 14% or 38%, respectively. This suggests that our method can contribute to improved monitoring and management of these protected species, especially that souslik monitoring requires considerable research effort and has to be carried out twice a year.
However, mole mounds may be underestimated by remote sensing, which can be seen in Fig. 7. Small mole mounds that are easily identified during field research may not be noticed by remote sensing. Such underestimation does not constitute a critical threat to the determination of the mole area according to the scheme shown in Fig. 8, since its marks are highly redundant. However, since there is currently little research on this subject, we recommend combining field research and remote sensing in assessments similar to ours. Finally, it is worth noting that, for a better understanding of the issue of the interactions between souslik and other burrowing species, it is advisable to use another remote sensing technique—telemetry. Telemetry studies are successfully conducted in Bulgarian souslik populations34 and their combination with studies of habitat selectivity dependent on other burrowing species may provide new and valuable insight into this issue.
Source: Ecology - nature.com
