Impact of invasive species on the density and body size of an insular endemic lizard (Trachylepis atlantica)

BackgroundInvasive species have been responsible for the extinction of several species around the world. The Noronha skink is an endemic lizard from the Fernando de Noronha archipelago, Brazil, that has been suffering from habitat changes and the introduction of invasive species. ResultsTwo methods were used to estimate the density of the Noronha skink. The density on the main island was 0.167 ± 0.090 individuals/m²; that on the secondary islands was 0.357 ± 0.170 individuals/m²; and that on the entire archipelago was 0.184 ± 0.109 individuals/m². Moreover, the morphometric parameters of the Noronha skink were compared between the main island and secondary islands. The values of all parameters were higher on the secondary islands. ConclusionThe occurrence of invasive species on the main island seems to be a determining factor in the density and body size of the Noronha skink.

The Noronha skink ( Figure 1) is one of the oldest residents of the Fernando de Noronha archipelago, since radiation from its African ancestors occurred during the Miocene (10-27 million years ago) [11]. This is the lizard species located farthest east from South America [12] and is the only species of the genus Trachylepis in the New World.
This lizard is charismatic and fearless towards humans due to its evolution and speciation in a predator-free environment and shows important ecological functions associated with the equilibrium of the archipelago ecosystem. One of these functions is the pollination of plants such as mulungu (Erythrina velutina) when the skink visits its flowers searching for nectar [13].
Although a reduction in the abundance of T. atlantica can be easily visualized on the archipelago, it is now also being reported by local inhabitants. Considering that the skink is endemic to Fernando de Noronha in an area smaller than 30 km 2 , in 2017, this species was designated as threatened by the State of Pernambuco, which administers the archipelago [10].
The present work aimed to determine the density and morphometry of this species in different landscapes of the archipelago and to associate these findings with the human presence, anthropic activities and threats caused by invasive species. As of the time of writing, this study was the first to examine the density and perform morphometric comparisons of T. atlantica between the islands of the archipelago.

Density and abundance
The capture and recapture method was performed in six parcels in different landscapes of the main island of the archipelago of Fernando de Noronha. The results are shown in Table   1.

Morphometric evaluation
Among the 135 individuals captured between 2014 and 2016, 114 (84.4%) were from the main island, and 21 (15.5%) were from the secondary islands (10 from Rata Island, 7 from Meio Island, 2 from Sao Jose Island, and 2 from Chapeu Island). All morphometric parameters showed greater values on the secondary islands. Males from the secondary islands were larger and heavier than males from the main island (Table 2). Moreover, males were heavier and larger than females on both the main island and the secondary islands (Table 3).  [14], and T. seychellensis (0.021 individuals/m 2 ), endemic to the Seychelles Islands [15].
The increased density of T. atlantica in comparison with those of other Trachylepis species may be explained by the fact that Tinhosa Grande Island has a small size and no vegetation, offering few resources for T. adamastor. In contrast, the Seychelles Islands have a larger area than Fernando de Noronha but harbour numerous natural and invasive predators of T. seychellensis, such as snakes and birds of prey [16]. Both the Tinhosa

Grande and Seychelles Islands exhibit unfavourable environments preventing their
Trachylepis species from reaching the densities observed for T. atlantica .
The phenomenon known as density compensation [17] indicates the expected abundance of T. atlantica and why it is currently lower than expected. According to Buckley and Jetz [18], insular species tend to reach population densities above those of their continental conspecifics. An example of this phenomenon is provided by the tegu lizard (Salvator merianae), which presents densities of 6.9*10 -4 individuals/m 2 in the main island of State) [20], i.e., at least 10 times higher in insular environment.
The low native species richness of the Fernando de Noronha archipelago and the absence of natural predators prior to human occupation in the sixteenth century are probably the key factors in the high density of T. atlantica on the archipelago [21]. The lack of species sharing the same ecological niche as T. atlantica means that there is low interspecific competition, which, allied with the absence of natural predators, resulted in low predation rates during the early establishment of this species on the archipelago [21].
However, the actual population density of T. atlantica is not sufficient to maintain the species in the long term. If all the archipelago presented the same density found on the secondary islands, which are free of cats and exhibit low densities of tegu lizards [19], the abundance of the Noronha skink would be 6,504,540 individuals. Thus, it can be inferred that the actual population of T. atlantica is at least 50.7% below the expected abundance.  [22]. Cats were probably introduced to the archipelago with the first landing of the European colonizers, during the sixteenth century [23]. These animals are superpredators in insular environments and are responsible for the extinction of birds, mammals and reptiles on several islands worldwide [24,25]. On the Fernando de Noronha archipelago, the number of cats is estimated to be approximately 1,300 individuals on the main island, which is considered one of the highest densities on islands worldwide [23].
Due to the evolution and speciation of the Noronha skink in the absence of natural predators, behavioural defences are also absent in this species, making it vulnerable in interspecific encounters. Cats, rats and cattle egrets are the main threats and prey upon T. atlantica individuals daily. Dias et al. [23] described the predation frequency of T. atlantica by cats reported by the resident inhabitants who maintain cats in their households with the aim of controlling the Noronha skink population.
The predation pressure generated by invasive species, especially cats, may directly influence the population densities of the T. atlantica recorded in the present study. This hypothesis is corroborated by Case and Bolger [26], who noted that cats are considered successful predators of small reptiles in several types of environments. Smith et al. [27] concluded that the predation of reptiles by invasive species on Christmas Island was the main factor of the decline of its native reptiles.
Through stable isotope analyses and analyses of prey fragments in faecal samples of cats and rats and the stomach contents of tegu lizards, Gaiotto [28] determined the potential trophic relations of producers and consumers on Fernando de Noronha. The results showed that T. atlantica corresponded to 18.8% of the cats' diet and 30.3% of the rats' diet [28].
No proven presence of cats, a proven low presence or absence of tegu lizards [19], and a high density of rodents [29] are reported for the secondary islands of the Fernando de Noronha archipelago. The absence of a single invasive species with a high predation potential, such as cats, may have allowed the higher density of T. atlantica on the secondary islands (0.357 individuals/m²), which was 119% higher than the density observed on the main island (0.167 individuals/m²). Not only is the density higher, but the body size and mass of T. atlantica individuals are also significantly higher on the secondary islands than on the main island, despite the expected body size and mass of males being greater than those of females.
The greater body size and mass of T. atlantica on the secondary islands may also be related to longevity. Classic studies have shown that reptiles grow constantly during their lives and, according to Goss [30], amphibians and reptiles retain their cartilage epiphyses throughout their lives, allowing constant growth. These findings were corroborated by Andrews [31], who noted that even if growth is insignificant after reaching asymptotic size, reptiles grow throughout their lives.
According to Olsson and Shine [32], the constant growth of reptiles is best observed in some lizards with short longevity. This information corroborates the results of the present work. The secondary islands of the Fernando de Noronha archipelago have been subject to fewer anthropic interferences and harbour fewer invasive species, which may increase the longevity of T. atlantica compared to the individuals on the main island.
The effects of the insular conditions on body size are referred to as the "island rule" and may be associated with intrinsic (p.e., climate) or extrinsic (p.e., predation) factors [33,34,35]. According to Russell et al. [36], when islands exhibit the same biogeographic climatic conditions, extrinsic factors may not explain body size differences. However, the high predation rate of cats on the Noronha skink and competition with other invasive species have probably created selective pressure that determines the observed density and body size differences, resulting in population decline on the main island.
With the arrival of new invasive species in recent decades, such as the tegu lizard (Salvator merianae), which was introduced before 1950 [19], and the cattle egret (Bubulcus ibis), which arrived naturally in the 1990s [37], the increases in the mortality rates and population decline of T. atlantica are concerning. According to Gaiotto [28], 19.6% of the tegu's diet is composed of T. atlantica. Silva-Jr et al. [38] also reported predation of cattle egrets upon T. atlantica.

Conclusions
The morphometric comparisons showed that the longevity of T. atlantica on the main island is reduced compared to that of individuals on the secondary islands. The difference in the invasive species communities of the main and secondary islands is the most likely factor determining the density and morphometric parameter differences of T. atlantica.
The results are robust to indicate the threats that this endemic species, T. atlantica, is subjected to, and these findings may contribute to mitigation actions and the inclusion of this species in the red list of IUCN.

Study area
The archipelago of Fernando de Noronha (3°51'13.71"S, 32°25'25.63"W) is composed of 21 islands and islets with a total area of 18.2 km² [22,23]. It is one of the four Brazilian oceanic insular sets, including the Archipelago of Sao Pedro and Sao Paulo, the Rocas Atol,

Trindade and Martin Vaz Islands and the Archipelago of Fernando de Noronha.
The archipelago has a wet and dry tropical climate, with the rainy season occurring from March to July and the dry season from August to February [39]. Currently, the predominant vegetation of the archipelago is deciduous seasonal forest, similar to that in the Brazilian northeast [40]. On the south face of the archipelago, which is exposed to equatorial trade winds, the vegetation is arboreal with some patches where grass prevails [41].
Fernando de Noronha was discovered in 1503 by Vespucci and was occupied by several different countries, such as the Netherlands, France, Portugal and the United States; in 1942, it became Brazilian federal territory, and in 1988, it started to be administered by the Brazilian State of Pernambuco [40,42]. Currently, only the main island is occupied, and the entire terrestrial area is occupied by two federal protected areas: a Marine National Park, which is an IUCN category II protected area covering 70% of the terrestrial territory, and a Protected Area designated as IUCN category V that is destined for human use, covering 30% of the terrestrial area. The estimated human population was 2.9 thousand inhabitants in 2017, with approximately 7.5 thousand concurrent tourists visiting the archipelago at a given time in 2016 [43].

Visual capture and recapture
The visual capture and recapture method was used in six parcels conveniently defined according to the accessibility of sampling sites on the main island of the archipelago of Fernando de Noronha. The parcels had a mean area of 31.3 m² and were located in four of the seven landscape types of the main island. Each parcel was observed once daily for six subsequent days during the same campaign and were not resampled in a different campaign.
The animals observed inside the parcels were captured using a stick with a loop made of fishing line at the tip. Fishing line was chosen since can be slipped more easily than sewing thread. After capture, the animals were identified with non-permanent marks.
Numeric marks were made on the back of the individuals with a water-based ink pen and remained on the animals for approximately two weeks. Captured animals were carefully inspected for ecdysis, avoiding those animals on which the marks would not remain long enough to complete the capture and recapture session. Marks were made only on the first day of the campaign, and marked and unmarked animals were counted. After the marking procedures, the animals were released inside the parcel.
The analysis was performed with Mark software [44] using the Poisson log-normal model [45], considering the population as closed (no births, deaths, emigration or immigration during the observations) and without using covariates. Of the seven previously categorized phytophysiognomy strata, four (quarry, shrub, urbanized and tree) were compared, and the observations were made within six days after the catches and marking (Supplementary Material).

Point abundance
The point abundance was determined as a complementary method to the visual capture and recapture approach. The data were obtained on the main island and secondary islands (Rata, Meio, Morro da Viúva, and Chapéu).
The point transects were randomly distributed in the accessible areas of the archipelago.
A single observer remained still for seven minutes, observing a 2 m radius area covering 12.6 m 2 at each point. The observations were performed in the seven landscape types, which were sampled during the day when the temperature was approximately 29.8 ± 2.2°C, during the period of increased activity for the species defined by Rocha et al. [12].
These inclusion criteria are essential for the observation of ectothermic animals, which are more active in warm periods of the day.
The irregular spatial distribution of the abundance points was used to calculate the continuous variation of density using point interpolation analysis. The inverse distance weighting (IDW) method of the Interpolation plugin of QGIS software was used. The resulting raster had a grid size of 3.5 x 3.5 m, resulting in an area similar to the sampled area (12.6 m 2 ). In each grid cell, the T. atlantica density was calculated by dividing the number of counted individuals by this area. The tridimensional area of the archipelago was used in the calculations of density and abundance. The digital elevation model and the calculations of the tridimensional area are described elsewhere [23].

Morphometric evaluation
To perform morphometric evaluation of T. atlantica, individuals were captured at aleatory points on the main and secondary (Rata, Meio, Sao Jose, and Chapeu) islands at distinct points from those used under the density and distribution assessment methods. Samples were obtained from the different landscape types of the archipelago.

Consent for publication
Not applicable.

Availability of data and materials
The data that support the findings of this study are available from the corresponding author upon reasonable request.

Supplementary Files
This is a list of supplementary files associated with the primary manuscript. Click to download. supplementary_material.pdf