Interference competition following a recent invasion of plague skinks ( Lampropholis delicata ) into a nationally critical native skink population
Sarah J. Wells
A,* , Dylan van Winkel
Band Ben P. Barr
CABSTRACT
For full list of author affiliations and declarations see end of paper
*Correspondence to:
Sarah J. Wells
School of Environmental and Animal Sciences, Unitec Te Pu¯kenga, Auckland, New Zealand
Email:[email protected]
Handling Editor:
Harriet Mills
Context. Invasive species can threaten native species through exploitative and interference competition if they occupy similar ecological niches. The invasive plague skink (Lampropholis delicata) has been accidently introduced to New Zealand, Lord Howe Island, and the Hawaiian Islands. Resource usage overlaps between plague skinks and several New Zealand skinks, suggesting the potential for exploitative and interference competition. However, no competitive mechanism or population impact has been identified. In 2014–15, plague skinks colonised Bream Head Scenic Reserve, Northland, New Zealand, where they overlap in occupancy and habitat with the‘Nationally Critical’ kakerakau skink (Oligosoma kakerakau).Aims. We investigated intra- and interspecific interference competition between kakerakau and plague skinks in the wild.Methods. We recorded naturally occurring encounters and quantified aggression at a short-lived resource (sun-basking sites). Key results. Behavioural interactions were observed in 72% of all encounters with similar proportions of encounters resulting in agonistic interactions between intraspecific kakerakau skink encounters and interspecific kakerakau-plague encounters. Although kakerakau skinks and plague skinks reacted equally aggressively in an interspecific interaction, kakerakau skinks behaved significantly more aggressively in an interaction with a plague skink than with a conspecific. Juvenile kakerakau skinks were more likely than adults to exhibit submissive behaviours such asfleeing during interspecific interactions.Conclusions. This is thefirst evidence of interference competition occurring between plague skinks and a native skink. Our study suggests that kakerakau skinks, particularly juveniles, may experience competitive exclusion at important resources.Implications. Ourfindings indicate that plague skinks may pose a threat to native skink populations when habitat use overlaps.
Keywords: agonistic behaviour, biological invasions, competitive exclusion, ectotherms, interference competition, interspecific aggression, invasive species,Lampropholis delicata,Oligosoma kakerakau, sun-basking, territorial behaviour.
Introduction
Received:17 January 2023 Accepted:12 May 2023 Published:6 June 2023
Cite this:
Wells SJet al. (2023) Pacific Conservation Biology doi:10.1071/PC23003
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Biological invasions are one of the foremost threats to biodiversity (Di Castri 1990;
Williamson 1996; Sanders et al. 2003; Crowl et al. 2008; Miehls et al. 2009). The invasion of exotic species into habitats occupied by native species can cause significant impacts on the fitness of native species. This conflict is particularly apparent when the invasive and native species overlap in their occupancy and niches, and can ultimately lead to either niche partitioning or extirpation via competitive exclusion (Volterra 1931;
Lotka 1932; Gause 1934; Hardin 1960; Pianka 1974; Chesson 2000).
The competitive mechanisms in which competition between species can manifest are typically grouped into two broad categories: (1) exploitative; and (2) interference competition. Exploitative competition occurs when two species indirectly compete for the same resource but do not interact directly. Interference competition occurs when one species directly, for example, using aggression or displays of aggression, limits another species access to resources such as food, mates, or space (Miller 1967; Case and Gilpin 1974).
Schoener (1983) further divided interference competition into territorial competition, when an individual aggressively defends, or by its behaviour signals its intention to defend, a unit of space against other individuals; and encounter competition, in which some harm comes to one or more individuals. Such harm can include time or energy losses, theft of food, injury, or death by predation, fighting, or mere accident. Exploitative and interference competition are not mutually exclusive, and both can lead to competitive exclusion or niche partitioning (Amarasekare 2002).
Exploitative and interference competition are often asymmetric (e.g. Hersteinsson and Macdonald 1992; Žagar et al. 2015), with the native species usually being the most affected (e.g. Human and Gordon 1996; van Kessel et al.
2011; Culbertson and Herrmann 2019; but see Yang et al.
2012; Cisterne et al. 2019). Competitive asymmetry is often a consequence of the evolution of behavioural and life history adaptations in invasive species in habitats with higher levels of competition. For example, invasive species tend to be highly fecund (Söderbäck 1995), have enhanced growth rates (Byers 2000; Funk and Vitousek 2007; Graebner et al. 2012), reach sexual maturity at younger ages (Söderbäck 1995), be more generalist or efficient feeders (Feng et al.
2007; Damas-Moreira et al. 2020), and possess dominant behavioural traits (reviewed in Chapple et al. 2012) such as aggression (Morse 1974; Robinson and Terborgh 1995;
Usio et al. 2001; Rychlik and Zwolak 2006; Kimura and Chiba 2010), greater phenotypic plasticity (Davidson et al.
2011) or predator avoidance mechanisms (e.g. Polo-Cavia et al. 2008). Quantifying levels of competition and their effects on fitness of the participants is therefore essential for understanding the impacts of invasive species on native populations.
New Zealand has one of the most diverse lizard assem- blages per unit area in the world (Chapple and Hitchmough 2016) with 124 accepted species. All species are endemic, and more than 85% are at risk or threatened with extinction (Hitchmough et al. 2021). The plague or rainbow skink (Lampropholis delicata) (also known as the delicate skink in its native range) is native to Australia but has established populations in New Zealand, the Hawaiian Islands, and Lord Howe Island via human-mediated dispersal (Chapple et al. 2016). The plague skink was inadvertently introduced to Auckland, New Zealand in the 1960s from eastern Australia and since then, the population has spread across most of the upper North Island, and more recently to locations in the South Island (Chapple et al. 2016; van Winkel et al. 2018). It is now listed as an ‘Unwanted Organism’ under the Biosecurity Act (1993). However, the ecological impact of the plague skink on native lizard fauna remains largely unknown and is yet to be quantified (Chapple et al. 2016; Harris et al.
2021). Chapple et al. (2016) posited that predation pressure from introduced plague skinks were negatively impacting the invertebrate fauna on Lord Howe Island. However, they were unable to separate the predation pressure of plague skinks
from the concurrent effects of rat predation. Competitive exclusion from plague skinks has also been hypothesised to be responsible for the decline of the moth skink (Lipinia noctua) and possibly the azure-tailed skink (Emoia cyanura) in the Hawaiian Islands (Baker 1979). Plague skink invasions could also indirectly contribute to native species declines. For example, it is hypothesised that they may act as possible vectors for disease connecting regionally endemic species that would otherwise remain isolated from each other (Wairepo 2015). It has also been suggested that in high densities they could artificially inflate predator numbers, resulting in increased predation pressure on native species(Chapple et al. 2016).
Despite their invasive potential, little research has been conducted to quantify the effect that plague skinks have on native skink populations, and no study has demonstrated any direct competitive interactions between plague skinks and native species in the wild. Peace (2004) found that in a captive setting, plague and copper skinks (Oligosoma aeneum) utilise common microhabitats, forage in the same way, and prey upon invertebrates of the same type and size. Similarly, Harris et al. (2021) found plague skinks had broad range niche and food size preference overlaps with three native skinks, moko skink (Oligosoma moco), ornate skink (Oligosoma ornatum), and copper skink (O. aeneum). These studies suggest that there is potential for competition. However, captive studies have not detected any aggressive interactions between plague skinks and either copper skinks (Peace 2004) or moko skinks (Muchna 2009), suggesting that if competition exists, it may be exploitative rather than interference. While captive studies such as these are invaluable due to their repeatability and ability to manipulate and control the experi- mental environment, forced interactions in captive conditions can cause changes to an animal’s natural behaviour and temperament (Archard and Braithwaite 2010). Therefore, studies of unforced behavioural responses to naturally occurring variation in resources are equally important and are more likely to be a true representation of the competitive mechanisms occurring in nature (Archard and Braithwaite 2010).
Bream Head Scenic Reserve is an 800-ha coastal broadleaf forest located near Whang¯arei, Northland, New Zealand. It is home to five native species of skinks, including the recently described ‘Nationally Critical’ kakerakau skink (Oligosoma kakerakau Barr et al. 2021) (previously known as the Whirinaki skink, Oligosoma ‘Whirinaki’; Hitchmough et al.
2021) and four other species (O. moco, O. ornatum, O. aeneum, and the shore skink, Oligosoma smithi). Plague skinks appear to have arrived in Bream Head Scenic Reserve in approximately 2014–15 and in 2016, they were first observed within the range of the kakerakau skink (Barr et al. 2021). Because the plague skink and kakerakau skink are both diurnal and conspicuous in this location, this site provided a unique opportunity to observe how plague skinks interact with native skinks in the wild following a recent invasion.
In this study, we used video recordings at known kakerakau skink sun-basking locations to examine naturally occurring B
interactions between kakerakau and plague skinks in the wild.
Both plague and kakerakau skinks are heliotherms, for which sun basking is a critical behaviour that enables thermoregu- lation (Cowles and Bogert 1944; Cowles 1962). Thermoregulation increases body temperature and consequently optimises activity and physiological processes such as metabolic rate, digestion, reproduction, and vitamin D synthesis (Huey and Slatkin 1976; Avery et al. 1982; Downes and Bauwens 2004; Seebacher and Franklin 2005). Thus, sun-basking locations are likely to be an important limited resource to be defended via agonistic interactions in these species (e.g.
Žagar et al. 2015). Our aim was to determine if interference competition is occurring between plague skinks and kakerakau skinks at this resource, and if so, to quantify and describe these interactions. Pacala and Roughgarden (1982) showed that the strength of interspecific competition in lizard communities is inversely related to the degree of resource partitioning (prey size, horizontal and vertical space, and activity time); i.e. where there is less resource partitioning, there is greater competitive effect. Since plague and kakerakau skinks are both diurnally active they are predicted to have greater overlaps in niche space and behaviour than more crepuscular and cryptic native skinks such as the copper skink. Indeed, there are strong overlaps between kakerakau and plague skinks in most of these resource partitioning parameters; with the exception of vertical space as kakerakau skinks readily climb and occupy arboreal habitats (Barr et al.
2021). Therefore, we predict that there will be signifi- cant interference competition between plague skinks and kakerakau skinks. Because this study evaluates interference
interactions between a native and an exotic species after a recent invasion, it provides invaluable empirical insight into competition effects that may lead to competitive exclusion after a biological invasion.
Materials and methods
Site description
Bream Head Scenic Reserve is an 800-ha coastal forest located at the south-eastern extent of Whang¯arei Heads, in Northland, New Zealand (Fig. 1). The key topographical feature of Bream Head Scenic Reserve is the central ridge, running in an east- west direction. The northern and southern facing slopes have unique macrohabitats converging at the ridge line. The northern slope is dominated by k¯anuka (Kunzea robusta/
Kunzea linearis) and m¯ anuka (Leptospermum scoparium) forest, although some forest areas at the ridge line and in the gullies are at a more advanced seral stage and include kiekie (Freycinetia banksia), tawa (Beilschmiedia tawa), and mixed broadleaf species. The southern slope is dominated by intact coastal broadleaf forest. The reserve also includes shrubland and small areas of rockland and duneland (Goldwater and Beadel 2010).
Skink encounters
Encounters between plague skinks and kakerakau skinks were observed two ways during austral summer 2018/2019 and 2020/2021. First, point and shoot cameras (Canon IXUS
Fig. 1. Location map of Bream Head Scenic Reserve, Whang¯arei Heads, Northland, New Zealand (red square) including location of Whang¯arei township (blue square).
C
185; 8× optical zoom) with video capability were mounted on trees, tripods, or stakes at 33 discrete light wells (basking locations) during daylight hours where there was a clear view of the forest floor. Both skink species utilise light wells for thermoregulation, so they offer an immobile and reliable resource to document competitive interactions. The cameras were positioned to capture a frame width of approxi- mately 1 m at ground level and set to record up to 30 min of footage. Second, opportunistic video footage was recorded where a plague or kakerakau skink was observed in the leaflitter beside walking tracks. Attempts were made to film any encounters between individuals at distance using the video and zoom functions on handheld cameras. Footage was discarded where signs of human disturbance to skinks was identified. Disturbance was considered to be any human behaviour that elicited an obvious reaction by the skinks (e.g.
skink turning its attention to human, making eye contact, repositioning, fleeing or taking cover).
We explored three types of encounters: (1) intraspecific kakerakau–kakerakau (K–K); (2) intraspecific plague–plague (PL–PL); and (3) interspecific kakerakau–plague (K–PL).
However, due to the small sample size of PL–PL encounters (n = 2), these were not analysed further. An encounter was defined as two lizards being within 20 cm of one another.
Distance between individuals was estimated from the 1 × 0.75 m dimensions of the video frame established during installation of the cameras. To explore encounters, we used a system similar to those used to quantify aggression in other lizard taxa (Ortiz and Jenssen 1982; Hess and Losos 1991; Husak and Fox 2003; Lailvaux et al. 2004; Lailvaux and Irschick 2007; Cisterne et al. 2019). Initially, we developed an ethogram of behaviours exhibited by the skinks (i.e.
behaviours observed during encounters) and these were then scored with a weighted scale ranging from −2 (submissive) to 8 (most aggressive) (Table 1). Encounters resulting in no behavioural response (i.e. the behaviours ‘Ignoring’ and
‘Basking on one another’; the latter of which was considered a form of tolerance) were given a score of zero. Encounters that involved behaviours other than those with zero scores were considered an interaction. To score an interaction, the point values for all behaviours performed by each individual during an interaction were summed; this total formed an individual’s ‘aggression score’ for an interaction.
Since both intra- and interspecific aggressive interactions can be influenced by body size, we categorised the size of all individuals as either adult or juvenile, with juveniles being those less than half the size of full-grown individuals of each representative species (Peace 2004; Wiles 2014).
Because the trials were conducted in the field, we could not control for potentially confounding effects of familiarity.
Statistical analyses
Intraspecific plague skink (PL–PL) encounters were excluded from statistical analyses due to low sample size (n = 2).
Table 1. Descriptions of the behaviours selected for the ethogram and the corresponding aggression scores (point values).
Behaviour Description Score
Flee Rapid movement away in response to another individual
−2
Move away/
reposition
Slow or controlled movement in any direction in response to another individual
−1
Basking on one One individual with more than one-third of 0 another body on top of another individual
Ignoring No response to other individual(s) or their 0 movement(s)
Contact Brief contact between individuals 1
Tongueflick Tongue rapidly moving in and out of mouth 2 Direct look/glare Deliberate head movement towards 3
opponent
Tail waving Undulating movement in the end of the tail 4 Approach Steady and deliberate movement towards an 5
individual
Competing Two individuals actively pursuing the same 6 prey item
Attack–chase Rapid movement towards an individual to 7 within at least a body length of an opponent Attack–bite/strike Rapid movement towards an individual and 8
delivering a bite
Negative scores indicate submissive responses by the focal individual.
However, both these encounters resulted in aggression scores of zero as the two skinks ignored each other. A chi-squared test was used to determine the difference in likelihood of intraspecific kakerakau skink (K–K) and interspecific (K–PL) encounters escalating into behavioural interactions (i.e. those encounters resulting in aggression scores other than zero).
Because the aggression scores and probability of retreat of each competitor within an encounter are likely to be non- independent and negatively correlated, for all analyses that compare individuals within an encounter type, we first randomly designated one competitor from each encounter, the ‘focal individual’, and then only included scores from the focal individual within each analysis.
All statistical analyses were conducted in R ver. 4.2.0 (R Core Team 2022). Non-parametric Mann–Whitney U tests were used to compare aggression scores of: (1) kakerakau skinks and plague skinks overall across both intra- and interspecific encounters; (2) kakerakau and plague skinks within an inter- specific (K–PL) encounter; and (3) kakerakau skinks between intraspecific (K–K) and interspecific (K–PL) encounters.
To test whether the aggression scores of adult and juvenile kakerakau skinks differed, and whether this depended on encounter type, we conducted a two-way ANOVA with an interaction between age (adult vs juvenile) and encounter type. An equivalent adult-juvenile test for plague skinks was not conducted because we observed no encounters that involved a juvenile plague skink.
D
To examine whether kakerakau skinks could be experiencing competitive exclusion due to competition with plague skinks, we examined whether kakerakau skinks were more likely to ‘retreat’ (i.e. showed submissive aggression scores of ‘move away/reposition’ or ‘flee’) in interspecific interactions. For those encounters that resulted in an interac- tion, we used chi-squared tests (or Fisher’s exact tests in instances where the expected values were less than 5) to examine the retreat rates of: (1) kakerakau skinks versus plague skinks; (2) adult kakerakau skinks versus juvenile kakerakau skinks between interspecific interactions; and (3) adult kakerakau skinks versus juvenile kakerakau skinks within intraspecific interactions.
Results
There were 31 recorded interspecific (K–PL) encounters and 77 intraspecific (K–K) encounters. These interactions covered the full spectrum of behaviours from aggressive ‘Attack – bite/
strike’ to submissive ‘Fleeing’ (Fig. 2). There was a tendency for interspecific encounters to be more likely to escalate into an aggressive interaction than intraspecific encounters(62.3%
of intraspecific encounters versus 77.4% of interspecific encounters). However, this difference was not significant (P = 0.13).
There was no significant difference between the aggression scores of kakerakau skinks and plague skinks in a K–PL
encounter (P = 0.89). This indicates that plague skinks and kakerakau skinks react equally aggressively when they encounter each other (Fig. 3). However, kakerakau skinks had significantly lower aggression scores in intraspecific encoun- ters in comparison to interspecific encounters (Fig. 4) (W = 418, P = 0.030). Similarly, when also including aggression scores from plague skinks in this analysis, this result became more significant with overall aggression scores in intraspecific encounters being significantly lower than in the interspecific encounters (W = 823, P = 0.007).
This demonstrates the overall higher levels of aggression in interspecific encounters due to both the lower aggression scores of kakerakau skinks within a K–K encounter, and the mutually high aggression scores of plague skinks and kakerakau skinks in a K–PL encounter.
Juvenile kakerakau skinks tended to have lower aggression scores than adults (F1,90 = 3.40, P = 0.068), even while accounting for the previously discussed difference in aggres- sion scores between inter- and intraspecific encounters (F1,90 = 13.31, P < 0.001). There was no difference in aggression scores of adults and juveniles between the different types of encounters (P = 0.48). Therefore, adult kakerakau skinks were more aggressive, and juveniles less aggressive, irrespective of whether it was an interspecific or intraspecific encounter.
Within those interspecific encounters that resulted in a behavioural interaction, there was no significant difference
Fig. 2. Frequency histogram of total aggression scores per competitor of 77 intraspecific kakerakau skink–kakerakau skink (K–K) and 31 interspecific kakerakau skink–plague skink (K–PL) encounters. Total aggression scores represent the summed values of all the scores for each individual’s behaviours within an encounter; i.e. two scores per encounter. Note, zero scores here also include aggression scores from an interaction where an individual’s total aggression score tallied to zero, as well as zeros resulting from‘no interaction’encounters.
E
Fig. 3. Tukey boxplots showing the aggression scores of kakerakau skinks (K) and plague skink (PL) in interspecific kakerakau skink–plague skink encounters (K–PL). Negative scores indicate a submissive response (‘move-away’or‘flee’), while zero scores indicate no agonistic interaction occurred.
Fig. 4. Tukey boxplots showing the aggression scores of kakerakau skinks in a kakerakau skink–kakerakau skink encounter (K–K) and in a kakerakau skink–plague skink encounter (K–PL). Negative scores indicate a submissive response (‘move-away’ or ‘flee’), while zero scores indicate no agonistic interaction occurred.
in the rates of retreat between kakerakau skinks and plague skinks (P = 0.22). However, juvenile kakerakau skinks had significantly higher retreat rates in these encounters than adult kakerakau skinks (χ2 = 17.629, P < 0.001; Fig. 5).
Although a weaker result, juveniles also tended to retreat more than adults within intraspecific interactions (Fisher’s exact test, P = 0.013) indicating that juveniles tend to retreat more than adults in either encounter type.
Fig. 5. Barplot showing the different proportions of 12 adult and 12 juvenile kakerakau skinks that retreated in interspecific (K–PL) interactions.
Discussion
Plague skinks have been accidently introduced from Australia to several islands in the Pacific, including New Zealand, Lord Howe Island, and the Hawaiian Islands. They are now a permanent fixture in the New Zealand landscape, and their shared resource use with native skinks. Peace (2004) and Harris et al. (2021) suggests that where they are syntopic, there is the potential for competition that negatively impacts native skink populations. Here, we described and quantified interspecific interactions of plague skinks with a native New Zealand skink in the wild. We examined the use of sun-basking sites as the limited resource in this study, which are important microhabitats for thermoregulation in heliothermic lizards. Our study demonstrates that sun- basking sites are an important shared resource that are defended via agonistic interactions in these species. At this resource, kakerakau skinks regularly encounter and interact with plague skinks. Both plague and kakerakau skinks exhibit aggressive, neutral, and submissive behaviours towards one another that cover the full spectrum of known agonistic behavioural responses, including ‘biting’, ‘striking’, and
‘chasing’; ‘ignoring’; and ‘moving away’ and ‘fleeing’, respec- tively. These behaviours fall neatly within Schoener’s
‘territorial’ and ‘encounter’ competition categories, which themselves are types of interference competition. Our study is therefore the first to show evidence of interference competition between plague skinks and a native skink species.
The frequency at which encounters escalated into an agonistic interaction were similar between intra- and inter- specific encounters. Furthermore, during interspecific interactions, there was no difference in the aggression scores between F
species (i.e. kakerakau skinks and plague skinks behaved equally aggressively). These findings indicate that both kakerakau skinks and plague skinks show equal inclination to an agonistic response irrespective of who they encounter.
Within both their native and introduced ranges, plague skinks tend to be found in high densities (Quay 1973; Baker 1979; Forsman and Shine 1995; Harris et al. 2021) and can dominate lizard guilds in terms of abundance (Taylor and Fox 2001; Harris et al. 2021). Thus, it is likely that the invasion of plague skinks has, at its simplest, led to an increased frequency of agonistic interactions for kakerakau skinks. However, our results demonstrate that the competitive effect of plague skinks is not merely additive because there was a key difference in how kakerakau skinks interacted with plague skinks compared to conspecifics. Kakerakau skinks behaved more aggressively in interspecific interactions than in intraspecific interactions. This suggests a degree of social tolerance of conspecifics and is incongruent with the classical Lotka-Volterra competition equation, which implies that species only coexist when intraspecific competition is stronger than interspecific competition (Lotka 1920; Volterra 1926). However, this model does not always fit real and complex systems, and previous studies have also shown that heterospecific lizard interactions are either equally or more aggressive than conspecific interactions (Ortiz and Jenssen 1982; Jenssen et al. 1984; Langkilde and Shine 2004).
This study did not determine the fitness costs of these interactions. However, because the presence of plague skinks within the range of kakerakau skinks results in interactions that are more aggressive and therefore, more energetically costly than if plague skinks were absent, they are likely to be negatively impacting the overall fitness of the kakerakau population. For example, poorer outcomes were seen in American Yarrow’s spiny lizards (Sceloporus jarrovii) whose aggression was artificially increased by supplementary testos- terone. These lizards had increased mortality, were more conspicuous to predators, and lost more weight than the less aggressive control individuals (Marler and Moore 1988).
At the other end of the aggression spectrum, there are potential fitness costs to a submissive interaction response.
Studies have shown that in cases of shared habitat use, competitively inferior species are forced to use sub-optimal habitats (Jaeger 1972; Tokarz and Beck 1987; Leal et al.
1998; Downes and Bauwens 2004; Langkilde and Shine 2004; Polo-Cavia et al. 2010; Champneys et al. 2021) resulting in the subordinate species experiencing competitive exclusion. Access to sun-basking sites is also determined through the outcome of agonistic interactions in Podarcis lizards, where a submissive response resulted in less time spent basking (Downes and Bauwens 2004). In lacertid lizards, interference competition at sun-basking sites disrupted lizard thermoregulation and reduced body temperatures of the species that was more frequently chased or forced to reposition (Žagar et al. 2015). Native turtles are more likely to be displaced from basking sites and consequently spent
less time basking than their invasive competitors (Cadi and Joly 2003; Polo-Cavia et al. 2010). These native turtles experienced weight loss and higher mortality than the invasive species (Cadi and Joly 2004). In Anolis lizards, competitive exclusion resulted in lower growth rates and a change in perch heights in the subordinate species (Pacala and Roughgarden 1982).
In kakerakau–plague interactions, juvenile kakerakau skinks were less aggressive and more likely to retreat than adults in both intraspecific and interspecific interactions.
Therefore, the costs associated with interference competition are likely to be primarily borne by juvenile kakerakau skinks.
If this behaviour persists over multiple generations, it could result in poorer adult recruitment and an adult-skewed population. In addition to costs associated with displacement from the resource itself, there may be further indirect costs associated with subordinate behavioural responses. For example, fleeing kakerakau skinks may be more detectable to visual predators such as sacred kingfishers (Todiramphus sanctus). Fleeing and/or hiding could also result in less time spent foraging or interacting with potential mates.
This study has significant implications for understanding the impact of an invasive skink on native skink communities.
New Zealand lizards are particularly susceptible to displace- ment by introduced species because of their reproductive life histories. Most New Zealand lizards are viviparous, giving birth to relatively small numbers of offspring per year. In contrast, plague skinks exhibit several characteristics of successful invaders. For example, they are oviparous and can multi-clutch, leading to a greater reproductive output than native skinks. In addition, being smaller they may be more efficient at evading predation because they can take advantage of smaller refuges (Peace 2004). They are also more likely to have a greater resistance to habitat disturbance;
occurring frequently in association with humans (Quay 1973;
Baker 1979; Peace 2004; Chapple et al. 2016). The consequence of these traits is that where they are found, they tend to occur in high densities. Our study has shown that in addition to their successful life histories and overlaps in resource use and food preferences, plague skinks also are capable of equally aggressive behavioural responses towards native lizards that could favour the expansion of this invasive species and the potential exclusion of natives.
Due to the unmanipulated nature of the study, the compet- itive effects demonstrated here are likely to be representative of true competition occurring in nature. However, observational studies are also subject to substantial constraints. First, due to the complex background vegetation, it was difficult to determine when each competitor arrived at the sun-basking sites. This limited our ability to record other common variables used to quantify agonistic interactions such as latency to attack (e.g. Lailvaux et al. 2012; Herringe et al. 2022). This is important particularly when studying interactions at basking resources, because latency could affect the amount of time a lizard is able to spend basking, and therefore influence the G
fitness costs of an encounter. Second, because we were unable to consistently discriminate individuals, it is possible that interactions from repeated individuals could be a potential confound in our study. However, because of this study was conducted over different days over a period spanning 3 years, and because multiple kakerakau skinks and plague skinks were observed using the same basking sites, any repeated individuals are likely to represent a significantly small number of the total observations. Furthermore, due to the short-lived nature of these light wells, they are unlikely resources to be defended for extended periods of time. In addition, we were unable to control for the effect of body size and limited our comparisons to the categories of adult versus juvenile. However, because this study focused on:
(1) interspecific variation where there is a natural asymmetry in size; and (2) variation in adults versus juveniles, small variations in body size are unlikely to have greatly influenced the results.
Despite these constraints, our study still demonstrates that interference competition is a natural occurrence between plague skinks and kakerakau skinks, and therefore represents a significant step forward in our understanding of competitive interactions between invasive and native species in New Zealand. Our findings contrast with those of two previous studies conducted under captive conditions which found no evidence of interference competition between the plague skink and two native skinks, the copper skink (O. aeneum) (Peace 2004) and the moko skink (O. moco) (Muchna 2009).
The reason for the disparity between these studies and ours is unclear, particularly as the moko skink is another diurnally active skink inhabiting a similar niche space to the kakerakau skink. The difference could be due to the smaller sample sizes of the previous studies, or differences in territorial behaviours of the kakerakau skink and the copper skink or moko skink.
However, we posit that the difference is more likely an outcome of the different experimental settings of these studies. Captive studies can coerce animals into performing unnatural or modified behaviours (Archard and Braithwaite 2010). In contrast, despite being subject to other constraints, unmanipulated studies conducted in the wild are more likely to capture natural interactions between individuals. Nevertheless, we urge researchers to confirm the application of this study’s findings to native skink species more generally by conducting captive and wild studies in other native skink species that repeat and refine this experiment under more controlled settings.
In conclusion, this study provides insight into competition between native and invasive species that can occur following a recent invasion. The two main mechanisms through which interspecific competition can manifest are interference and exploitative competition. Our study demonstrates significant levels of interference competition occurring between a native skink species and the invasive plague skink. On the other hand, exploitative competition is difficult to quantify and this study has not achieved this. Empirical and theoretical evidence suggests that invasive species are superior at both
exploitative and interference competition (Amarasekare 2002). Indeed, the numerical dominance of plague skinks in skink guilds in both its native and introduced range, and the fact they are predators on similar invertebrates (Peace 2004), strongly infers that this type of competition will be occurring in addition to the interference competition identified here. However, the arboreal habit exhibited by kakerakau skinks could provide a selective mechanism to partition ecological niches of the two species and accordingly reduce interspecific competition. Further research could be conducted to quantify the fitness costs to kakerakau skinks in relation to both interference and exploitative competitive effects from plague skinks. While our study quantified competition arising at sun-basking sites, there is evidence that skinks display increased levels of aggression when they are competing for food (Baines et al. 2020). Quantification of competition occurring for this important resource is also critical, as any negative effects on foraging ability are likely to incur significant costs. Finally, lizard social systems in New Zealand can be complex (Barry et al. 2014), and because our study followed a relatively recent plague skink invasion, longer-term studies investigating abundance– impact relationships and driving mechanisms behind the potential long-term co-existence of these invasive and native skinks is encouraged.
References
Amarasekare P (2002) Interference competition and species coexistence.
Proceedings of the Royal Society of London. Series B: Biological Sciences 269(1509), 2541–2550. doi:10.1098/rspb.2002.2181
Archard GA, Braithwaite VA (2010) The importance of wild populations in studies of animal temperament. Journal of Zoology 281(3), 149–160.
doi:10.1111/j.1469-7998.2010.00714.x
Avery RA, Bedford JD, Newcombe CP (1982) The role of thermoreg- ulation in lizard biology: predatory efficiency in a temperate diurnal basker. Behavioral Ecology and Sociobiology 11(4), 261–267.
doi:10.1007/BF00299303
Baines H, Gini B, Chang Y-M, Michaels CJ (2020) Dominance and aggression in captive gidgee skinks (Egernia stokesii). Herpetological Journal 30(2), 83–92. doi:10.33256/hj30.2.8392
Baker JK (1979) The rainbow skink, Lampropholis delicata, in Hawaii.
Pacific Science 33(2), 207–212.
Barr BP, Chapple DG, Hitchmough RA, Patterson GB, NgatiWai Trust Board (2021) A new species of Oligosoma (Squamata: Scincidae) from the northern North Island, New Zealand. Zootaxa 5047(4), 401–415. doi:10.11646/zootaxa.5047.4.1
Barry M, Shanas U, Brunton DH (2014) Year-round mixed-age shelter aggregations in Duvaucel’s geckos (Hoplodactylus duvaucelii).
Herpetologica 70(4), 395–406. doi:10.1655/HERPETOLOGICA-D- 13-00056
Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81(5), 1225–1239. doi:10.1890/
0012-9658(2000)081[1225:CBTESI]2.0.CO;2
Cadi A, Joly P (2003) Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81(8), 1392–1398. doi:10.1139/z03-108 Cadi A, Joly P (2004) Impact of the introduction of the red-eared slider
(Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13(13), 2511–2518. doi:10.1023/B:BIOC.0000048451.07820.9c
H
Case TJ, Gilpin ME (1974) Interference competition and niche theory.
Proceedings of the National Academy of Sciences 71(8), 3073–3077.
doi:10.1073/pnas.71.8.3073
Champneys T, Genner MJ, Ioannou CC (2021) Invasive Nile tilapia dominates a threatened indigenous tilapia in competition over shelter. Hydrobiologia 848, 3747–3762. doi:10.1007/s10750-020- 04341-8
Chapple D, Hitchmough R (2016) Biogeography of New Zealand lizards.
In ‘New Zealand Lizards’. (Ed. DG Chapple) pp. 109–132. (Springer International)
Chapple DG, Simmonds SM, Wong BB (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends in Ecology and Evolution 27(1), 57–64.
doi:10.1016/j.tree.2011.09.010
Chapple DG, Reardon JT, Peace JE (2016) Origin, spread and biology of the invasive plague skink (Lampropholis delicata) in New Zealand. In
‘New Zealand lizards’. (Ed. DG Chapple) pp. 341–359. (Springer International)
Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–366. doi:10.1146/annurev.
ecolsys.31.1.343
Cisterne A, Schwarzkopf L, Pike DA (2019) Australian house geckos are more aggressive than a globally successful invasive Asian house gecko.
Behavioral Ecology 30(1), 107–113. doi:10.1093/beheco/ary156 Cowles RB (1962) Semantics in biothermal studies. Science 135(3504),
670. doi:10.1126/science.135.3504.670
Cowles RB, Bogert CM (1944) A preliminary study of the thermal requirements of desert reptiles. Bulletin of the American Museum of Natural History 83(5), 261–296.
Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment 6(5), 238–246.
doi:10.1890/070151
Culbertson KA, Herrmann NC (2019) Asymmetric interference competition and niche partitioning between native and invasive Anolis lizards. Oecologia 190(4), 811–820. doi:10.1007/s00442- 019-04466-1
Damas-Moreira I, Riley JL, Carretero MA, Harris DJ, Whiting MJ (2020) Getting ahead: exploitative competition by an invasive lizard.
Behavioral Ecology and Sociobiology 74(10), 117. doi:10.1007/
s00265-020-02893-2
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14(4), 419–431. doi:10.1111/
j.1461-0248.2011.01596.x
Di Castri FD (1990) On invading species and invaded ecosystems: the interplay of historical chance and biological necessity. In ‘Biological invasions in Europe and the Mediterranean Basin. (Eds F di Castri, AJ Hansen, M Debussche) pp. 3–16. (Springer: Dordrecht)
Downes S, Bauwens D (2004) Associations between first encounters and ensuing social relations within dyads of two species of lacertid lizards.
Behavioral Ecology 15(6), 938–945. doi:10.1093/beheco/arh090 Feng Y-L, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates
more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153(3), 501–510. doi:10.1007/s00442-007-0759-2 Forsman A, Shine R (1995) Parallel geographic variation in body shape and reproductive life history within the Australian scincid lizard Lampropholis delicata. Functional Ecology 9(6), 818–828. doi:10.2307/
2389979
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446(7139), 1079–1081. doi:10.1038/
nature05719
Gause GF (1934) ‘The struggle for existence.’ (Williams and Wilkins:
Baltimore)
Goldwater N, Beadel S (2010) Natural areas of Manaia Ecological District (Northland Conservancy). Department of Conservation unpublished report, Northland Conservancy, Whangarei.
Graebner RC, Callaway RM, Montesinos D (2012) Invasive species grows faster, competes better, and shows greater evolution toward increased seed size and growth than exotic non-invasive congeners. Plant Ecology 213(4), 545–553. doi:10.1007/s11258-012-0020-x
Hardin G (1960) The competitive exclusion principle: an idea that took a century to be born has implications in ecology, economics, and
genetics. Science 131(3409), 1292–1297. doi:10.1126/science.131.
3409.1292
Harris J, Smith CR, van Winkel D, Brunton DH, Goulet CT, Chapple DG (2021) Does the invasive plague skink (Lampropholis delicata) compete with native skink species in New Zealand? Austral Ecology 46(3), 463–474. doi:10.1111/aec.12984
Herringe CA, Middleton EJ, Boyd KC, Latty T, White TE (2022) Benefits and costs of social foraging in velvet worms. Ethology 128(3), 197–206.
doi:10.1111/eth.13256
Hersteinsson P, Macdonald DW (1992) Interspecific competition and the geographical distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64(3), 505–515. doi:10.2307/3545168 Hess NE, Losos JB (1991) Interspecific aggression between Anolis
cristatellus and A. gundlachi: comparison of sympatric and allopatric populations. Journal of Herpetology 25(2), 256–259. doi:10.2307/
1564669
Hitchmough R, Barr B, Knox C, Lettink M, Monks JM, Patterson GB, Reardon JT, Van Winkel D, Rolfe J, Pascale M (2021) Conservation status of New Zealand reptiles, 2021. New Zealand Threat Classification Series. (Department of Conversation)
Huey RB, Slatkin M (1976) Cost and benefits of lizard thermoregulation.
The Quarterly Review of Biology 51(3), 363–384. doi:10.1086/409470 Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105(3), 405–412. doi:10.1007/BF00328744 Husak JF, Fox SF (2003) Adult male collared lizards, Crotaphytus collaris,
increase aggression towards displaced neighbours. Animal Behaviour 65, 391–396. doi:10.1006/anbe.2003.2058
Jaeger RG (1972) Food as a limited resource in competition between two species of terrestrial salamanders. Ecology 53(3), 535–546.
doi:10.2307/1934249
Jenssen TA, Marcellini DL, Pague CA, Jenssen LA (1984) Competitive interference between the Puerto Rican lizards, Anolis cooki and A. cristatellus. Copeia 1984, 853–862. doi:10.2307/1445328 Kimura K, Chiba S (2010) Interspecific interference competition alters
habitat use patterns in two species of land snails. Evolutionary Ecology 24, 815–825. doi:10.1007/s10682-009-9339-8
Lailvaux SP, Irschick DJ (2007) The evolution of performance-based male fighting ability in Caribbean Anolis lizards. American Naturalist 170, 573–586. doi:10.1086/521234
Lailvaux SP, Herrel A, Vanhooydonck B, Meyers JJ, Irschick DJ (2004) Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis).
Proceedings of the Royal Society of London. Series B: Biological Sciences 271, 2501–2508. doi:10.1098/rspb.2004.2891
Lailvaux SP, Huyghe K, Van Damme R (2012) Why can’t we all just get along? Interspecific aggression in resident and non-resident Podarcis melisellensis lizards. Journal of Zoology 288(3), 207–213.
Langkilde T, Shine R (2004) Competing for crevices: interspecific conflict influences retreat-site selection in montane lizards. Oecologia 140(4), 684–691. doi:10.1007/s00442-004-1640-1
Leal M, Rodríguez-Robies JA, Losos JB (1998) An experimental study of interspecific interactions between two Puerto Rican Anolis lizards.
Oecologia 117, 273–278. doi:10.1007/s004420050658
Lotka AJ (1920) Analytical note on certain rhythmic relations in organic systems. Proceedings of the National Academy of Sciences 6, 410–415.
doi:10.1073/pnas.6.7.410
Lotka AJ (1932) The growth of mixed populations: two species competing for a common food supply. Journal of the Washington Academy of Sciences 72, 461–469.
Marler CA, Moore MC (1988) Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology and Sociobiology 23(1), 21–26. doi:10.1007/BF00303053 Miehls ALJ, Mason DM, Frank KA, Krause AE, Peacor SD, Taylor WW
(2009) Invasive species impacts on ecosystem structure and function:
a comparison of Oneida Lake, New York, USA, before and after zebra mussel invasion. Ecological Modelling 220(22), 3194–3209.
doi:10.1016/j.ecolmodel.2009.07.020
Miller RS (1967) Pattern and process in competition. Advances in Ecological Research 4, 1–74. doi:10.1016/S0065-2504(08)60319-0 Morse DH (1974) Niche breadth as a function of social dominance. The
American Naturalist 108, 818–830. doi:10.1086/282957
I