Annual response patterns in activity and demographic parameters of reptile species occupying a predictable Mediterranean climate

Over the 30 years of Regime III, 29 species were captured on 16,613 individual occasions (Table 1). During the first 7 years of Regimes I and II combined, 26 species were captured on 2477 individual occasions (from Table 2). The three species not captured during the earlier regimes were the snake, Echiopsis curta, the legless lizard, Pletholax gracilis and the gecko, Heteronotia binoei; the former two were first captured in February 1994 and November 1998, respectively, while the gecko was first captured in February 2016. Captures of H. binoei in every subsequent year indicates the species has been a recent coloniser that is now established in Bold Park.

The six most abundant species comprised 80.6% of captures in Regime III and 24 species, generally captured over numerous years, comprised 99.7% of total captures (Table 1). The capture rates of those 24 species were averaged over annual demi-monthly periods for the 30 annual sampling periods in Regime III (Fig. 2), illustrating the annual activity profile for the total reptile assemblage.

Fig. 2.

Demi-monthly capture rates, expressed as captures/100 trap days (mean + s.e.), averaged for all species in the Bold Park assemblage during the 30 trapping seasons of Regime III.

Highest activity within the reptile assemblage occurs during the spring and summer months between late October and late December (Fig. 2). However, large standard errors associated with mean demi-monthly capture rate indicates significant variation exists between the 24 species regularly trapped. That variance is best explained by variable emergence times of species’ hatchlings (Fig. 3), generally occurring from late January to late March, and different seasonal activity patterns within adults.

Fig. 3.

Activity patterns for adults and hatchlings (<1 year) in 16 species, expressed as captures/100 trap days (left axis), over an annual demi-monthly timescale (females, solid line; males, dashed line). Hatchling activity over their first year (grey columns), also expressed as captures/100 trap days (right axis), over the same annual demi-monthly timescale. Menetia greyii is functionally parthenogenetic.

The five additional species that contribute to the total assemblage, were the recent colonist, H. binoei, the rare habitat specialist, P. gracilis, and three species that have become locally extinct over the course of the study. The snake, E. curta, the ground gecko, Lucasium alboguttatum and the fossorial snake Brachyurophis fasciolatus have not been captured for the past 29, 27 and 23 years, respectively. Additionally, P. gracilis and the heath dragon, Ctenophorus chapmani, have only been captured once during the past 20 years, making them likely contenders to become the next local extinctions. Two species, the snake, Pseudonaja affinis, and monitor, Varanus gouldii, have large adult individuals, not amenable to pitfall capture, and were poorly represented as only their hatchlings and juveniles were captured.

The six commonest species strongly influence activity pattern in the total assemblage.

Emergence of hatchlings occurred between the end of January to early March in Ctenotus fallens, Strophurus spinigerus, Lerista elegans and Simoselaps bertholdi (Fig. 3). Hatchlings first appear in December for Lerista lineopunctulata and live young may be born before winter in Hemiergis quadrilineatus but are mostly captured during the following late October and November (see Table 2). Few hatchlings of S. spinigerus were caught in autumn but many more during the spring and summer months of their first year. The late summer early autumn emergence of hatchlings appears to be a consistent pattern for most of the 16 species with adequate data that account for 97% of all captures (Fig. 3).

Adults also show variable activity patterns but, almost universally, there is a marked decline over the hotter months from mid-January and through the hatching season of February and March. Adult female C. fallens were active slightly later in the spring than adult males; however, both had similar spring-dominated abundances then showed a marked decline in activity from early January onwards through summer and into autumn. Both adult sexes in S. spinigerus had similar activity patterns although adult females greatly outnumber adult males in all demi-months and decreased activity later than males. The decline in H. quadrilineatus adult activity from early January was marked in both adult sexes, despite fewer males recorded than females. The decline in female activity occurred when they are carrying late-stage clutches. Adults in the two fossorial Lerista species shared similar peak activity patterns in spring and early summer with males active slightly earlier than females and females remaining active longer (Fig. 3). Males of S. bertholdi were more active from November to early December than females, the latter peaking during January–February after depositing eggs; a pattern previously documented by How and Shine (1999) for this population. Patterns of adult activity amongst these commonest species were broadly mirrored in adults of the remaining species in Fig. 3 that had peak activity between November and early January but slightly contrasting patterns over those demi-months.

Size-age categories were appraised from the time of peak demi-month emergence of hatchlings for all species and their subsequent size (SVL, mm) changes in following demi-monthly periods. Examination of those plots illustrated inferred age of cohorts at the end of each sampling (yearly) period and the size attained by species by the end of their first (hatchling), second and, occasionally, third years. Infrequently captured species, resulting from either their rarity (L. alboguttatum, P. gracilis) or trap size limitations (V. gouldii, P. affinis), had insufficient data for age category assessment. Viviparous species (H. quadrilineatus, Tiliqua rugosa, Cyclodomorphus celatus) had young at the end of autumn and juveniles that generally appeared in the trap record in early spring (Table 2).

C. fallens and Pogona minor, two regularly trapped species with uniquely marked individuals, had growth patterns determined from recaptured, known-aged individuals. Both sexes in C. fallens showed similar patterns of growth over demi-months through their first, second and third years and, despite size dimorphism between adults (see Supplementary material Table S1), there was no clear indication from known-age individuals when that dimorphism commenced (Fig. 4). Growth patterns in both C. fallens and P. minor hatchlings and yearlings indicated continuing increases in size and mass between late autumn and early spring over both their first and second years, despite a complete absence of capture-activity throughout that period.

Fig. 4.

Growth patterns for Ctenotus fallens (above) and Pogona minor (below) for demi-months over successive years determined from mark–recaptured individuals first caught during their hatchling and first years. SVL (mm) (lines; left axis) and mass (g) (columns; right axis) for females (filled + s.d.) and males (open −s.d.). Hatchlings (year 0) are followed by age in years (digits).

Only 26 individual hatchling S. spinigerus individuals were captured over their first autumn and just 149 within their hatchling year. Of those, only nine were recaptured in later months, insufficient to allow known-age growth rates to be determined. P. minor, Cryptoblepharus buchananii, Ctenotus australis and C. chapmani individuals did not show clear evidence of sex dimorphism in growth over their early years, while both T. rugosa and C. celatus individuals were too infrequently recaptured to determine growth pattern from size-age categories.

The size at maturity (adults) was evaluated from the combination of the minimum size of individuals illustrating reproductive activity and size determined growth category over demi-monthly periods. The smallest reproductively active individuals are documented (Table 2). However, occasionally those individuals were ‘outliers’ in a species maturity-size distribution and probably unlikely to represent routine onset of maturity for that species.

Age at reproductive maturity varied greatly between species and occasionally between sexes. The agamids, P. minor and C. chapmani, matured by the end of their first year as did some male C. fallens. However, it appears that in most species both sexes do not become reproductively active until the end of their second or usually, in their third years. In snake species (S. bertholdi, Brachyurophis semifasciatus, Narophis bimaculatus) reproductive activity commenced a year or two later than the lizard species, based on their size-age category (Table 2).

Reproductive pattern was conservatively determined from the proportion of adult individuals in each demi-month (Fig. 5) having either yolky follicles or eggs (females) or seminal plugs (males).

Fig. 5.

Numbers in 18 species of adult females (filled columns) and adult males (open columns) captured during each demi-month (left axis) and the percentage of females gravid (solid lines) and males reproductively active (dotted line) during those periods (right axis). Male H. quadrilineatus and S. spinigerus were not categorised for reproductive status.

Reproduction occurred, almost universally, from late spring to early summer months in the 18 most abundant species (Fig. 5). Information for other species suggested a similar pattern despite limited sample sizes and/or temporal coverage. The viviparous species, H. quadrilineatus, T. rugosa and C. celatus, produced young at the end of autumn but determination of reproductively active or gravid females in those species was difficult given the robust opaqueness of the ventral scales.

The upper range in clutch size recorded (Table 2) indicated the likely maximum individual fecundity in Bold Park species populations. One or two eggs are only ever produced by all gecko and legless lizard species, consequently that represents the maximum clutch size in those taxonomic groups; no evidence for double clutching during a year was recorded in marked S. spinigerus individuals. The maximum clutch recorded in skinks, agamids and all snakes varied considerably but could reflect the observational inconsistencies mentioned in the Material and Methods section. For the nine species, where 10 or more clutches were counted (Table 2), larger females carried larger clutches, notably in H. quadrilineatus, L. lineopunctulata, Anilios australis, C. fallens and N. bimaculatus. In C. fallens clutches of six were recorded in the largest females, but many large gravid individuals had only two to four eggs, probably reflecting egg deposition prior to examination.

Captures of hatchlings, based on their demi-monthly SVL classes, inferred that high mortality occurs during the first year in all species (Fig. 3), specifically during autumn and winter following hatching. Few individuals survive to the yearling category. For marked individuals of C. fallens and P. minor, the low survival of hatchlings was illustrated by lower captures and few marked individuals reaching spring with continuing low captures through the following year. In S. spinigerus, very few hatchlings were captured before winter and their capture rates diminished rapidly over the following spring and summer. In other species, survival of hatchlings also appeared low with decreasing capture rates over autumn and few surviving to spring.

Indicative longevity (Table 3), determined from the longest period between recaptures of uniquely identified individuals (measured in sampling years), illustrated large variation between species. Most re-trapped individuals occurred within their hatchling year, but numerous survived for several years afterwards to infer a longevity greater than a decade for two viviparous (T. rugosa, C. celatus) and two oviparous (C. fallens, C. buchananii) skink species as well as the oviparous gecko, S. spinigerus (Table 2). Another oviparous skink, C. australis, was documented to live at least 6 years, an estimate probably curtailed by the rapid decline of the species population over the study period. Both oviparous agamid species, P. minor and C. chapmani, were relatively short-lived with only one female P. minor known to survive 4 years (Table 3). These estimates of longevity are conservative as they do not consider size-age category at first capture.

Most recaptures of uniquely marked individuals occurred within traps at the same sampling site and year as their previous capture (Table 3), particularly among hatchlings. Those trap-indicated movements within the same site restrict the maximum distance moved between recaptures to less than 43 m.

Some individuals of all marked species traversed between different sampling sites throughout Bold Park. In ‘straight line’ distances these movements varied from 150 m to 1.7 km (Table 4), indicating individuals may move extensively through the study area. The skinks C. fallens and T. rugosa had recorded movements between all sites, while the gecko, S. spinigerus, had recorded movements almost exclusively between sites BP1, BP5 and BP3, sites dominated by proteaceous heath understoreys. The arboreal skink, C. buchananii, had recorded movements only between the Banksia and Tuart woodland sites of BP3 and BP4, respectively.

Most movements between sites were recorded over one to several sampling years. However, one adult C. fallens moved 150 m between sites BP3 and BP2 over a period of 15 days, while two hatchlings moved 1665 m between sites BP1 and BP3 and 1565 m between sites BP5 and BP4 over periods of 7 and 5 days, respectively. A gravid female S. spinigerus moved between sites BP1, BP3 and BP5 over a 28-day period, distances of 1665 m and 1450 m, while another adult female moved 750 m between site BP1 and BP5 over 5 days.

The mass (g) and size (SVL, mm) of adult females and males in different reproductive categories for the dominant 18 species are in Table S1. Sample sizes were limited in the other less frequently captured species.

Gravid females in all species were significantly heavier (P < 0.01) than other adult females determined as not reproductively active. Similarly significant differences in female length occurred, except for C. buchananii, B. semifasciatus and N. bimaculatus. Reproductively active males were of similar mass to other males, except for being significantly lighter (P < 0.05) in A. australis and significantly heavier in L. elegans and Lialis burtonis (both P < 0.05), and L. lineopunctulata (P < 0.01). Lengths of adult males were significantly longer in L. lineopunctulata (P < 0.01) and N. bimaculatus (P < 0.05) but significantly shorter (P < 0.01) in A. australis for adults determined as not reproductively active. Female T. rugosa were not reliably categorised for reproductive condition and no seminal plugs were recorded from any adult male S. spinigerus and only four in H. quadrilineatus. Two Menetia greyii males were captured, a skink known to have parthenogenic populations.

Sexual dimorphism in length was significantly greater (P < 0.01) in non-gravid females than non-reproductive males in all species, except M. greyii, P. minor and T. rugosa. Dimorphism in mass was also significant greater (P < 0.01) for adult females, except in C. fallens, M. greyii (only two males captured), P. minor, C. buchananii, and T. rugosa, and significantly less (P < 0.01) in H. quadrilineatus. Only four male H. quadrilineatus extruded seminal plugs, which likely accounts for non-reproductive males being significantly heavier than their female counterparts.

The extensive SVL range in adults in several species suggests extended individual longevity, since many reptiles show continuous growth with age. In most species individuals were not uniquely marked, and therefore not permitting accurate documentation of longevity. However, two exceptionally large female A. australis (SVL 360 mm) were captured in Tuart woodland at BP4, and a large female B. fasciatus (SVL, 390 mm) in Banksia woodland at BP3; those measurements were greater than 2 s.d. above the means for adults of their sex.

Adult individuals are key to defining behavioural and demographic parameters of populations, including variation in activity, fecundity, size and mass that determine species performance through time and over space. During the 30-year period of standard methodology for Bold Park, adult male activity in most species preceded that of adult females during the spring-summer reproductive period. A further generalisation was a marked decline in adult activity from January to April that preceded an almost complete cessation of activity over the late autumn and winter; indicating a late summer aestivation period as well as supporting known brumation in reptiles from late autumn through winter. Activity of hatchlings and juveniles within the study populations, however, showed different species-specific seasonal patterns.

Evaluating the ecological traits of the five fossorial elapid snakes occurring in Bold Park, How and Shine (1999) also reported overall low abundance and reduced activity through mid-summer, as well as winter, and noted male S. bertholdi were more active in spring, during the mating season, while females were more active in autumn, after oviposition. That broad pattern was also reflected by B. semifasciatus and the blind snake, A. australis, in this study, but in N. bimaculatus seasonal activity was similar in both adult sexes. Two other fossorial snakes (B. fasciolatus, Neelaps calonotos) had limited adult data to interpret general patterns, although increased activity was noted in N. calonotos during both late autumn and early spring.

Comprehending seasonal variation in activity patterns of age cohorts in species provides insights into their longer-term demographic performance, probability of detection and potential for local extinction.

Three issues are inherent in detectability – variable demographic factors and activity responses of populations though time as well as suitability of capture methods employed. Those issues are particularly relevant within the isolated reptile populations in Bold Park.

Several species had unreliable detectability using pitfall trapping due to their large adult sizes (P. affinis, V. gouldii) or their potential climbing abilities (Christinus marmoratus, C. buchananii). Additionally, marked changes in annual activity were also noted in capture rates of S. spinigerus and H. quadrilineatus throughout the study (How et al. 2022) while variable seasonal activity patterns of species hatchlings and adults also impacts detectability, particularly if sampling duration is constrained to certain times of the year.

The great majority of species in Bold Park showed altered capture rates between Regime III and Regime I + II combined, necessitating caution in interpreting activity and relative abundance patterns even when using only slightly different pitfall trapping methodologies. The methodological study by Bamford and Calver (2015), contrasting pitfall trapping with active foraging through habitat destruction on the SCP, showed few species were equally detectable using those differing techniques. Environmental impact assessments are mandated by regulatory authorities for development projects and require use of various methodologies to focus on biotic richness, particularly threatened species (Western Australian Government 2018; Thompson and Thompson 2020). Inherent in those assessments is an understanding of seasonal variation within individual species activity that would impact both the design and temporal sequence of biodiversity surveys. This is relevant to Guidance Statements, Technical guidance and Standard Operating Procedures proposed by regulatory authorities (Thompson and Thompson 2024).

While acknowledging methodological differences between pitfall trapping studies, comparison of species activity could still provide evidence of regional differences in relative abundance of otherwise cryptic species. Pitfall trapping of four fossorial snake species, in common between this study and in WA deserts (Goodyear and Pianka 2008), indicated that higher activity (captures/100 pit trap days) occurred in Bold Park for S. bertholdi (0.46 vs 0.21) and N. bimaculatus (0.13 vs 0.05), similar activity in B. semifasciatus (0.17 vs 0.17) but lower activity in B. fasciolatus (0.01 vs 0.07), a species now locally extinct in isolated Bold Park.

Size is crucial to defining reptile size-age demographic categories and essential to determining parameters in naturally occurring populations over extended timeframes – despite recent studies showing that indeterminate growth is not universal among ectothermic reptiles (Frýdlová et al. 2020). Growth patterns were determined for both C. fallens and P. minor from marked, known-aged hatchlings and juveniles that were followed through subsequent demi-months or monthly intervals for up to 3 years. There was no indication of variable growth rates in P. minor hatchlings or juveniles as has been documented for the saxiphilous agamid, Ctenophorus ornatus, that occurs on granite outcrops adjacent to Perth (Baverstock 1975). Growth in both C. fallens and P. minor hatchlings and yearlings increased in size and mass between captures in late autumn and early spring, providing a conundrum because that is a period of supposed brumation and during which there was a complete absence of capture-activity.

However, in most species size-age categories were inferred from changes in SVL over demi-months after peak hatchling emergence and then through juvenile categories for their first 2 years, and occasionally 3 years. Growth was maximal during those early-age cohorts and pulses in size classes were traced to provide inferred age categories and probable age at reproductive maturity.

Reproduction occurred between late spring and early summer in both lizards and snakes while hatching, or birth, of young occurred from late summer to early autumn. Spring reproduction and hatchling emergence in the late autumn for snakes accords with earlier findings, determined through dissected specimens (Shine 1984, Strahan et al. 1998; Goodyear and Pianka 2008), while the reproductive parameters in lizards was in broad agreement with other populations in the Mediterranean climate of the WA wheatbelt region (Chapman and Dell 1985) and the SCP (Davidge 1980). Informatively, Bradshaw (1981) indicated that in some lizard species there was variation in reproductive onset, with breeding commencing earlier in more northerly latitudes. Reproductive parameters in two arboreal gecko species, Gehyra variegata and Hesperoedura reticulata, in the WA wheatbelt region (Kitchener et al. 1988) had fixed clutch sizes of one and two eggs, respectively, in spring but the former reached sexual maturity in its third, while the latter only reproduced after their fifth year.

Age at maturity, based on size-age categories and assuming continuous growth, varied between most lizards and snakes, although it was generally acquired between 2 and 4 years of age. Marked P. minor individuals achieved sexual maturity toward the end of their first year, as did some male C. fallens, but in the latter both male and female maturity usually occurred a year later. The granite rock-inhabiting dragon, C. ornatus, in localities nearby to Perth (Baverstock 1975, 1978), was relatively short-lived and had a high fecundity with populations being either slow or fast growing and age at sexual maturity occurring in less than 1 year for the fast growers and between 1.5 years and 2 years for slow growers.

Survival of hatchlings appeared low in all species in Bold Park with few individuals reaching spring of their hatchling year and even fewer the yearling age category, as inferred from capture rates within size-age classes over those periods. For two species with marked individuals, low survival of hatchlings was informed by few surviving to spring and through to the following year. High mortality among hatchling and juveniles has been documented for both gecko species studied by Kitchener et al. (1988) in the wheatbelt region of WA, although other studies of natural populations seldom address low survival in early-age cohorts. Adult survival in Bold Park was more difficult to assess due to infrequent recaptures of marked individuals and their potential for movement throughout the larger study area.

Longevity was determined only for species with uniquely marked individuals. Several of those species had individuals that survived for over a decade and longevity reached at least 22 years in S. spinigerus. Extensive longevity was recorded for the arboreal geckos G. variegata and H. reticulata, (How and Kitchener 1983; Kitchener et al. 1988) and a continuation of that study showed individual Gehyra survived at least 13 years and Hesperoedura at least 18 years (J. Dell, unpubl. data); both individuals being adult when first captured. Agamids have relatively short longevity with individuals surviving for only a few years (Bradshaw 1971; Baverstock 1975), such as both Bold Park agamids, P. minor and C. chapmani.

Movement of individuals occurred regularly within trapping sites and most recaptures occurred there. However, movements by marked individuals of several species of nearly 2 km occurred between trapping sites, suggesting they utilise the entire contiguous study area of 338 ha. In contrast, two arboreal geckos studied in the wheatbelt region of WA showed exceptionally strong site fidelity; in the case of H. reticulata some individuals were confined to a single tree for the entirety of their capture record over 18 years (J. Dell, pers. comm.).

Reproductively active females were larger and heavier than their non-reproductive counterparts, lending support to the observation that larger females are probably more fecund. Adult males were rarely different between their reproductive categories. The comparison of non-reproductively active categories between the sexes supports sexual dimorphism in size and mass with females being larger and heavier than males for most species. However, the reverse situation occurred in H. quadrilineatus, a probable consequence of very few males extruding plugs that potentially reflects sperm storage in that live-bearing taxon, as previously demonstrated in its congener Hemiergis peronii (Smyth and Smith 1968).

Populations of the same reptile species on individual islands of the Houtman Abrolhos archipelago, isolated for the past 6K years and also experiencing a Mediterranean climate, showed significant differences in adult size (How et al. 2020). They postulated that differing relative abundances and adult size in populations probably reflected divergent resource states on islands of differing size and biological heterogeneity. Resource states were also indicated as the principal driver of different population abundances in G. variegata populations across vegetated isolates of the WA wheatbelt (Sarre 1998).