European red squirrel population dynamics driven by squirrelpox at a gray squirrel invasion interface

Infectious disease introduced by non‐native species is increasingly cited as a facilitator of native population declines, but direct evidence may be lacking due to inadequate population and disease prevalence data surrounding an outbreak. Previous indirect evidence and theoretical models support squirrelpox virus (SQPV) as being potentially involved in the decline of red squirrels (Sciurus vulgaris) following the introduction of the non‐native gray squirrel (Sciurus carolinensis) to the United Kingdom. The red squirrel is a major UK conservation concern and understanding its continuing decline is important for any attempt to mitigate the decline. The red squirrel–gray squirrel system is also exemplary of the interplay between infectious disease (apparent competition) and direct competition in driving the replacement of a native by an invasive species. Time series data from Merseyside are presented on squirrel abundance and squirrelpox disease (SQPx) incidence, to determine the effect of the pathogen and the non‐native species on the native red squirrel populations. Analysis indicates that SQPx in red squirrels has a significant negative impact on squirrel densities and their population growth rate (PGR). There is little evidence for a direct gray squirrel impact; only gray squirrel presence (but not density) proved to influence red squirrel density, but not red squirrel PGR. The dynamics of red SQPx cases are largely determined by previous red SQPx cases, although previous infection of local gray squirrels also feature, and thus, SQPV‐infected gray squirrels are identified as potentially initiating outbreaks of SQPx in red squirrels. Retrospective serology indicates that approximately 8% of red squirrels exposed to SQPV may survive infection during an epidemic. This study further highlights the UK red squirrel – gray squirrel system as a classic example of a native species population decline strongly facilitated by infectious disease introduced by a non‐native species. It is therefore paramount that disease prevention and control measures are integral in attempts to conserve red squirrels in the United Kingdom.     

On the Age of Leprosy

Leprosy is a chronic infection of the skin and nerves caused by Mycobacterium leprae and the newly discovered Mycobacterium lepromatosis. Human leprosy has been documented for millennia in ancient cultures. Recent genomic studies of worldwide M. leprae strains have further traced it along global human dispersals during the past ∼100,000 years. Because leprosy bacilli are strictly intracellular, we wonder how long humans have been affected by this disease-causing parasite. Based on recently published data on M. leprae genomes, M. lepromatosis discovery, leprosy bacilli evolution, and human evolution, it is most likely that the leprosy bacilli started parasitic evolution in humans or early hominids millions of years ago. This makes leprosy the oldest human-specific infection. The unique adaptive evolution has likely molded the indolent growth and evasion from human immune defense that may explain leprosy pathogenesis. Accordingly, leprosy can be viewed as a natural consequence of a long parasitism. The burden of leprosy may have affected minor selection on human genetic polymorphisms.     

Detection of squirrel poxvirus by nested and real-time PCR from red (<Emphasis Type="Italic">Sciurus vulgaris</Emphasis>) and grey (<Emphasis Type="Italic">Sciurus carolinensis</Emphasis>) squirrels

Background  

Squirrel poxvirus (SQPV) is highly pathogenic to red squirrels (Sciurus vulgaris), and is a significant contributing factor to the local extinction of the species in most parts of England and Wales, where infection is endemic in Eastern grey squirrel (Sciurus carolinensis) populations. Although a nested PCR assay has been used successfully to study the epidemiology of SQPV, samples have a long processing time and the assay is not quantifiable.     

Poxviral Disease in Red Squirrels Sciurus vulgaris in the UK: Spatial and Temporal Trends of an Emerging Threat

The squirrel poxvirus (SQPV) is the probable mediator of apparent competition between the introduced invading gray squirrel (Sciurus carolinensis) and the red squirrel (Sciurus vulgaris) in the UK, and modeling studies have shown that this viral disease has had a significant impact on the decline of the red squirrel in the UK. However, given our limited understanding of the epidemiology of the disease, and more generally the effects of invasive species on parasite ecology, there is a need to investigate the transmission dynamics and the relative pathogenicity of the virus between species. We aimed to increase our knowledge of these processes through an empirical study in which we: (i) used pathological signs and transmission electron microscopy (TEM) to diagnose SQPV disease in red squirrels found dead during scanning surveillance between 1993 and 2005; (ii) detected antibody to SQPV using an enzyme-linked immunosorbent assay (ELISA) in the same animals; and (iii) mapped cases of the disease, and the gray squirrel distribution, using a geographical information system. We analyzed the distribution of cases of SQPV disease according to woodland type, a measure of squirrel density. SQPV disease occurred only in areas of England also inhabited by seropositive gray squirrels, and as the geographical range of gray squirrels expanded, SQPV disease occurred in these new gray squirrel habitats, supporting a role for the gray squirrel as a reservoir host of the virus. There was a delay between the establishment of invading gray squirrels and cases of the disease in red squirrels which implies gray squirrels must reach a threshold number or density before the virus is transmitted to red squirrels. The spatial and temporal trend in SQPV disease outbreaks suggested that SQPV disease will have a significant effect on Scottish populations of red squirrels within 25 years. The even spread of cases of disease across months suggested a direct rather than vector-borne transmission route is more likely. Eight juvenile and sub-adult free-living red squirrels apparently survived exposure to SQPV by mounting an immune response, the first evidence of immunity to SQPV in free-living red squirrels, which possibly suggests a changing host-parasite relationship and that the use of a vaccine may be an effective management tool to protect remnant red squirrel populations.     

Morphological diversity of the red squirrel, <Emphasis Type="Italic">Sciurus vulgaris</Emphasis>, in Ireland

The red squirrel in Britain and Ireland has been described as a separate subspecies, Sciurus vulgaris leucourus, based on bleaching of the tail and ear tufts. However, recent investigations in northern England found this light colour confined to one area, probably due to the rapid spread of introduced continental European red squirrels. This study reports the first detailed survey of tail colour and cranial measurements in the Irish red squirrel population to (1) investigate the distribution of the light colour morph in Ireland and (2) determine whether the Irish red squirrel population is morphologically divergent from populations elsewhere in the species range. The light tail colour was found in 57% of individuals and in all regions, although it was most common in the northwest. The mixture of different colour morphs indicates the Irish population is a mixture of different subspecies, including S. vulgaris leucourus, while the cranial measurements suggest the Irish squirrel may be morphologically divergent from populations elsewhere. Combined, these results support previous suggestions that conservation measures seek to maintain the diversity within the Irish red squirrel population.     

Using GPS telemetry to validate least‐cost modeling of gray squirrel (Sciurus carolinensis) movement within a fragmented landscape

In Britain, the population of native red squirrels Sciurus vulgaris has suffered population declines and local extinctions. Interspecific resource competition and disease spread by the invasive gray squirrel Sciurus carolinensis are the main factors behind the decline. Gray squirrels have adapted to the British landscape so efficiently that they are widely distributed. Knowledge on how gray squirrels are using the landscape matrix and being able to predict their movements will aid management. This study is the first to use global positioning system (GPS) collars on wild gray squirrels to accurately record movements and land cover use within the landscape matrix. This data were used to validate Geographical Information System (GIS) least‐cost model predictions of movements and provided much needed information on gray squirrel movement pathways and network use. Buffered least‐cost paths and least‐cost corridors provide predictions of the most probable movements through the landscape and are seen to perform better than the more expansive least‐cost networks which include all possible movements. Applying the knowledge and methodologies gained to current gray squirrel expansion areas, such as Scotland and in Italy, will aid in the prediction of potential movement areas and therefore management of the invasive gray squirrel. The methodologies presented in this study could potentially be used in any landscape and on numerous species.     

Grauhörnchen vs. Eichhörnchen

Competition for resources in Europe's forests – grey versus red squirrels As a result of the introduction of the north American grey squirrel in Britain, Ireland and Italy in the 19th and 20th century, the sole native tree squirrel species in Europe – the red squirrel – faced a completely novel competitor. In order to understand the interactions between the two species and to develop a conservation strategy, the two species' biology and ecology was the focus of intense research over the last 25 years. We provide an overview of research findings and the complex competitive interactions for resources and the curcial role of disease in the replacement of native red by introduced grey squirrels. Key factors in the competitive replacement process are habitat composition and patterns of seed food availability, which directly influence individual body condition and reproductive success. In addition, in the British Isles a squirrelpox virus for which grey squirrels act as a reservoir and vector has a drastic impact on the competitive interactions between the two species.     

Adenovirus: an emerging factor in red squirrel Sciurus vulgaris conservation

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Conservation of genetic uniqueness in remaining populations of red squirrels (Sciurus vulgaris L.) in the South of England

The Eurasian red squirrel (Sciurus vulgaris) is an emblematic species for conservation, and its decline in the British Isles exemplifies the impact that alien introductions can have on native ecosystems. Indeed, red squirrels in this region have declined dramatically over the last 60 years due to the spread of squirrelpox virus following the introduction of the gray squirrel (Sciurus carolinensis). Currently, red squirrel populations in Britain are fragmented and need to be closely monitored in order to assess their viability and the effectiveness of conservation efforts. The situation is even more dramatic in the South of England, where S. vulgaris survives only on islands (Brownsea Island, Furzey Island, and the Isle of Wight). Using the D‐loop, we investigated the genetic diversity and putative ancestry of the squirrels from Southern England and compared them to a European dataset composed of 1,016 samples from 54 populations. We found that our three populations were more closely related to other squirrels from the British Isles than squirrels from Europe, showed low genetic diversity, and also harbored several private haplotypes. Our study demonstrates how genetically unique the Southern English populations are in comparison with squirrels from the continental European range. We report the presence of four private haplotypes, suggesting that these populations may potentially harbor distinct genetic lineages. Our results emphasize the importance of preserving these isolated red squirrel populations for the conservation of the species.     

What future for British red squirrels?

The geographic range of red squirrels contracted sharply in Britain during the 1940s arid 1950s, as increasingly large areas were colonized by the congeneric North American grey squirrel. Red squirrels remain common only on offshore islands, and in the large conifer forests of northern England and Scotland. The initial replacement of red squirrels was in arras dominated by oak woodland, probably because acorn crops are exploited less efficiently by red squirrels than by grey squirrels. Dirt studies have shown that acorns are digested less efficiently by the red squirrel, which occurs in conifers through most of its Eurasian range, than by the introduced grey squirrel, which is primarily a native of deciduous woodland. The red squirrel will probably be replaced in deciduous and mixed woodland throughout mainland Britain, and may eventually persist only in large areas of conifers which arc far from oak trees. The conservation of red squirrels on islands is therefore particularly important for their survival, perhaps making it worthwhile to create new island populations where they do not at present exist.     

A systematic review into the suitability of urban refugia for the Eurasian red squirrel Sciurus vulgaris

1. Urban growth and intensification are projected to increase as the global human population increases. Historically, urban areas have been disregarded as suitable wildlife habitat, but it is now known that these areas can be biodiverse and that wildlife species can adapt to the environmental conditions. One such urban-dwelling species is the Eurasian red squirrel Sciurus vulgaris, which has suffered population declines in several countries throughout its range in recent decades.
2. The current published literature was systematically reviewed to determine whether or not urban habitats are suitable refugia for red squirrels, through identifying and discussing key topics regarding the urban ecology of red squirrels.
3. Urban environments can support higher population densities of red squirrels than rural areas, probably due to the widespread and reliable provision of anthropogenic supplemental food alongside natural food sources. The availability and quality of urban greenspaces are important determinants of the suitability of urban habitats for red squirrels, as they provide natural food sources and nesting sites. Despite the barriers present in urban landscapes (e.g. roads), red squirrels can still disperse and maintain gene flow at the population level.
4. Road traffic accidents appear to be a significant cause of mortality in some urban red squirrel populations, and seasonal peaks of mortality occur during the autumn months. Diseases (e.g. squirrelpox virus) can also be a significant cause of mortality, although effects differ between populations and depend on whether grey squirrels Sciurus carolinensis are present. Many of the predation events that affect red squirrels appear to be due to free-ranging domestic and feral cats Felis catus, although there is currently little evidence to suggest that predation is a limiting factor for urban red squirrel populations.
5. We conclude that urban areas can be suitable refugia for red squirrels, provided that high-quality greenspaces are maintained. Mitigation measures may also be necessary to reduce population mortality and to prevent disease outbreaks.

     

Potential impact of grey squirrels Sciurus carolinensis on woodland bird populations in England

Several woodland bird species have declined markedly in abundance in England over the past 40 years, whilst the grey squirrel Sciurus carolinensis, a non-native nest predator, has increased. Given the timing, there has been concern that grey squirrels have driven these declines, although there is little data to support this view. Using novel analytical methods and extensive national bird and grey squirrel monitoring data, we examine whether there is evidence that woodland bird populations in England have been depressed by grey squirrels and whether there is a relationship between nest failure and squirrel numbers. Our results indicate that grey squirrels are very unlikely to have driven observed declines of woodland birds in recent years, although the number of associations, positive as well as negative, between grey squirrels and woodland birds is greater than expected by chance. For this reason, we cannot exclude the possibility that the populations of a small number of bird species, principally increasing species, have been depressed to some degree at sites where a greater number of grey squirrels were present. Of these species, perhaps the most convincing evidence is for Common Blackbird Turdus merula and Eurasian Collared Dove Streptopelia decaocto where nest record data also identified a positive relationship between nest failure at the egg stage and squirrel abundance.     

Landscape scale impacts of culling upon a European grey squirrel population: can trapping reduce population size and decrease the threat of squirrelpox virus infection for the native red squirrel?

The control of grey squirrels (Sciurus carolinensis) is widely undertaken as a conservation measure to protect red squirrel (Sciurus vulgaris) populations in the UK. However, inconsistencies and omissions in data collection, as well as fluctuating financial resourcing of control efforts, have meant that it has to date proved difficult to quantify the impact of any regional control initiative upon populations. Here we have scrutinized a 13 years period (1998–2010) within an ongoing grey squirrel control project that reflects the resource challenges typically faced by red squirrel conservation programmes. We present evidence that despite variation in grey squirrel control intensity, the abundance of grey squirrels ultimately decreased significantly. Trapping success was significantly higher in spring and summer months and a greater abundance of grey squirrels was found in deciduous woodland and hazel dominated scrub relative to other habitats; two findings that reinforce existing guidance within national control best practice. Grey squirrels carry an infection that causes epidemic pathogenic disease if spread to the native red squirrel. We observed that the proportion of seropositive grey squirrels decreased constantly from 2003 to 2010 when only 4 % of sampled animals were seropositive. This discovery indicates that culling can in parallel remove both the competitive and disease threat posed to red by grey squirrels. The historical paucity of scientific data on the effectiveness of grey squirrel control as a tactic in UK red squirrel conservation means that the findings of this study will significantly advance conservation best practice and inform the development of future national strategy.     

Epizootiology and pathologic findings associated with a newly described adenovirus in the red squirrel, Sciurus vulgaris

An infectious disease caused by Squirrelpox virus has contributed to the decline of red squirrels, Sciurus vulgaris, in the British Isles. Because of the heightened disease surveillance activity in red squirrels, adenovirus infection with associated mortality has been detected. Adenoviral disease is described in other rodent species usually associated with stressors. Here we 1) describe the pathologic findings in red squirrels found dead with adenoviral infection and gastrointestinal disease, and 2) investigate the epizootiology of the disease through pathologic investigation, scanning surveillance, and virologic studies. Ten red squirrels involved in conservation studies were diagnosed with adenoviral infection by electron microscopy or PCR. All squirrels exhibited diarrhea and small intestinal inflammation or hemorrhage was evident in seven cases. Lesions indicative of splenic lymphocytolysis were observed in one squirrel and leukocytic hepatitis in another. No adenovirus was detected in grey squirrels, Sciurus carolinensis, inhabiting the same forest area, but previous serologic studies showed that grey squirrels cannot be discounted as a reservoir of the virus. Scanning surveillance showed that 12% of 493 red squirrels had diarrheal disease and two of 13 free-living red squirrels with diarrheal disease had adenovirus infection. Adenoviral disease in declining free-living wild red squirrel populations in the British Isles occurs at a detectable frequency and its impact on the conservation of this species deserves further attention.     

A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy

Introduced mammals can cause extinction of native species due to replacement competition, disease, predation or hybridization. We studied the colonization of Piedmont (NW-Italy) by American grey squirrel (Sciurus carolinensis) and its effect on the native red squirrel (Sciurus vulgaris). Presence/absence data (2 × 2 km²), of both species were (re)constructed using questionnaires, literature, existing databases, unpublished information, and direct monitoring with hair-tubes. In 1970 red squirrels were still widespread and greys were restricted to forests near the introduction site. By 1990, grey squirrels had increased their range to 220 km², which coincided with the disappearance of native squirrels from 33 squares inside this range. The invasive species continued its spread occupying an area of 2,016 km² in 2010; within this area red squirrels went extinct in 88 squares. Overall, from 1970 to 2010 red squirrel went extinct in 62 % of 2 × 2 km² (ca. 1,689 km²), and were replaced by grey squirrels. The spread of the alien species was slow in the first 20 years, but doubled in the successive two decades. Nevertheless spread was slower than in Ireland and England. Grey squirrel adapt to climate and habitats in both North and South Europe, causing extinction of the native red squirrel. A EU LIFE co-funded project with the aim to control the grey squirrel in North Italy and recent trade-restrictions and trade-ban are a first step in reducing the risk of grey squirrels invading other countries, but their effectiveness will have to be evaluated.     

Evolutionary history of Mycobacterium leprae in the Pacific Islands

As one of the oldest known human diseases, leprosy or Hansen''s disease remains a public health concern around the world with over 200 000 new cases in 2018. Most human leprosy cases are caused by Mycobacterium leprae, but a small number of cases are now known to be caused by Mycobacterium lepromatosis, a sister taxon of M. leprae. The global pattern of genomic variation in M. leprae is not well defined. Particularly, in the Pacific Islands, the origins of leprosy are disputed. Historically, it has been argued that leprosy arrived on the islands during nineteenth century colonialism, but some oral traditions and palaeopathological evidence suggest an older introduction. To address this, as well as investigate patterns of pathogen exchange across the Pacific Islands, we extracted DNA from 39 formalin-fixed paraffin-embedded biopsy blocks dating to 1992–2016. Using whole-genome enrichment and next-generation sequencing, we produced nine M. leprae genomes dating to 1998–2015 and ranging from 4-63× depth of coverage. Phylogenetic analyses indicate that these strains belong to basal lineages within the M. leprae phylogeny, specifically falling in branches 0 and 5. The phylogeographical patterning and evolutionary dating analysis of these strains support a pre-modern introduction of M. leprae into the Pacific Islands.This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.     

Patterns of exploitation of annually varying Pinus sylvestris cone crops by seed‐eaters of differing dispersal ability

Food consumption by animals depends on functional and numerical responses, and particularly the latter for food specialists. Some birds and mammals are conifer seed specialists and are likely to exploit the varying seed production in different ways according to differences in dispersal capabilities. This in turn may determine which species is more likely to affect the evolution of cone morphology. This study examined the inter‐annual pattern of foraging on Scots pine Pinus sylvestris cones by crossbills Loxia spp. (highly dispersive) and red squirrels Sciurus vulgaris (weakly dispersive) over 16 yr in three stands of ancient native pines at Abernethy Forest in Highland Scotland. There were synchronous annual variations in cone production across the stands, and an indication of a three‐year cycle. The number of cones taken by crossbills was correlated with cone production, indicating a numerical response by the birds, up to a certain limit of cone production. By contrast, the number of cones taken by red squirrels was not correlated with cone production. Rather, the percentage of cones taken by squirrels was high when cone production was low, and low when production was high. There was also a long‐term decline in the number of cones taken by squirrels, suggesting a decline in squirrel numbers. Although a high percentage of cones was removed from some cohorts on some trees, either by crossbills (maximum of 94.8%) or red squirrels (100%), the mean percentage of cones taken by crossbills from trees was small, ranging from 3.7 to 17.1% across all cone cohorts. For red squirrels, mean values ranged from 0.1 to 46.1% across all cohorts. However, given that crossbills can track changes in cone production by rapid numerical responses (i.e. through migration), and take a larger percentage of cones from cohorts of high production (10.7%), compared with red squirrels (3.6%), crossbills may be more important in driving the evolution of cone morphology because future trees are more likely to come from cohorts of high cone production.     

Survey for zoonotic rickettsial pathogens in northern flying squirrels, Glaucomys sabrinus, in California

Epidemic typhus, caused by Rickettsia prowazekii, is maintained in a southern flying squirrel (Glaucomys volans) sylvatic cycle in the southeastern United States. The northern flying squirrel (Glaucomys sabrinus) has not been previously associated with R. prowazekii transmission. A second rickettsial pathogen, Anaplasma phagocytophilum, infects dusky-footed woodrats (Neotoma fuscipes) and tree squirrels in northern California. Because northern flying squirrels or their ectoparasites have not been tested for these rickettsial pathogens, serology and polymerase chain reaction (PCR) were used to test 24 northern flying squirrels for R. prowazekii and A. phagocytophilum infection or antibodies. Although there was no evidence of exposure to R. prowazekii, we provide molecular evidence of A. phagocytophilum infection in one flying squirrel; two flying squirrels also were seropositive for this pathogen. Fleas and ticks removed from the squirrels included Ceratophyllus ciliatus mononis, Opisodasys vesperalis, Ixodes hearlei, Ixodes pacificus, and Dermacentor paramapertus.     

Limited diversity associated with duplicated class II MHC-<Emphasis Type="Italic">DRB</Emphasis> genes in the red squirrel population in the United Kingdom compared with continental Europe

The red squirrel (Sciurus vulgaris) population in the United Kingdom has declined over the last century and is now on the UK endangered species list. This is the result of competition from the eastern grey squirrel (S. carolinensis) which was introduced in the 19th century. However, recent evidence suggests that the rate of population decline is enhanced by squirrelpox disease, caused by a viral infection carried asymptomatically by grey squirrels but to which red squirrels are highly susceptible. Population genetic diversity provides some resilience to rapidly evolving or exotic pathogens. There is currently no data on genetic diversity of extant UK squirrel populations with respect to genes involved in disease resistance. Diversity is highest at loci involved in the immune response including genes clustered within the major histocompatibility complex (MHC). Using the class II DRB locus as a marker for diversity across the MHC region we genotyped 110 red squirrels from locations in the UK and continental Europe. Twenty-four Scvu-DRB alleles at two functional loci; Scvu-DRB1 and Scvu-DRB2, were identified. High levels of diversity were identified at both loci in the continental populations. In contrast, no diversity was observed at the Scvu-DRB2 locus in the mainland UK population while a high level of homozygosity was observed at the Scvu-DRB1 locus. The red squirrel population in the UK appears to lack the extensive MHC diversity associated with continental populations, a feature which may have contributed to their rapid decline.     

The anatomy of a range expansion: changes in cranial morphology and rates of energy extraction for North American red squirrels from different latitudes

Species with expanding ranges provide unique opportunities to examine environmentally induced adaptations in ecological traits and anatomical characteristics. Since the late 1800s, the North American red squirrel (Tamiasciurus hudsonicus) has expanded its range into the central hardwoods of the United States in conjunction with increasing agricultural fragmentation. We examined whether red squirrels from the central hardwoods (west‐central Indiana, USA) displayed differences in foraging behaviors and morphology relative to red squirrels from conifer‐dominated environments (upper peninsula of Michigan, USA), a biome in which red squirrels evolved. Specifically, we measured rates of energy extraction, variation in cranial morphology, and diet preference between red squirrels from both regions. In addition, we compared foraging behaviors of red squirrels from the central hardwoods to those of a competitor that coevolved with nut‐producing trees, the gray squirrel (Sciurus carolinensis). Red squirrels from Indiana and Michigan differed significantly in the efficiency with which they used food items, with individuals from each region extracting calories at a more rapid rate for items that were common in their region. The enhanced efficiency of southern red squirrels feeding on black walnuts (Juglans nigra) was correlated with geographic differences in cranial morphology; skulls of southern squirrels were larger, with longer jaws and higher metrics associated with greater mandibular force than northern squirrels. Contrary to our expectations, red squirrels from Indiana and Michigan did not differ qualitatively in preferences for food items, suggesting that diet choice may be governed by perishability of food items rather than by rates of energy extraction. Gray squirrels were more efficient than Indiana red squirrels in using all food items, and differed only slightly from red squirrels with regard to preference for food items. Measures of efficiency of resource use, after accounting for species‐specific metabolic requirements, suggest that red squirrels are unlikely to compensate ecologically for declining gray squirrel populations in fragmented portions of the central hardwoods, with potentially adverse effects for forest regeneration and succession. Our results demonstrate that invading species can display significant flexibility in adapting to new environments, but they may not be flexible enough to exploit resources in a manner comparable to native species.