Artificial light at night and temperature as combined stressors on the development, life-history, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus

doi:10.21203/rs.3.rs-4846057/v1

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Artificial light at night and temperature as combined stressors on the development, life-history, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus

https://doi.org/10.21203/rs.3.rs-4846057/v1

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Unprecedented rates of urbanisation cause detrimental impacts on the natural environment. Two of the most prominent and ubiquitous urban stressors are artificial light at night (ALAN) and the urban heat island (UHI) effect. Individually, these two stressors have a wide array of effects on physiological, behavioural, and life-history traits of organisms. However, stressors rarely work in isolation, and the potential interactions of ALAN and elevated temperatures on organismal life-history traits, particularly with respect to sexual signalling and reproduction, are not well understood. Here, in a fully factorial design, we manipulated intensities of ALAN exposure (simulating urban light pollution) and/or developmental rearing temperatures (simulating UHI effects) to explore the consequences for juvenile development, survival, sexual signalling, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus. Our data revealed significant effects of temperature on key life-history traits. Crickets reared under elevated temperatures had higher mortality; reduced adult longevity, altered sexual signalling and male attractiveness. In isolation, ALAN had very limited impacts, reducing male juvenile development time. Similarly, both stressors acting in concert also had little impact; ALAN reduced female developmental duration when reared at control temperatures, but not elevated temperatures. These data suggest very limited effects of combined stressors in this species, while elevated temperatures, consistent with urban heat island effects, had equivocal effects on life-history traits, reducing survival, but potentially increasing male fitness. Our data highlight the complexity of urban stressors on wildlife behaviour and fitness. Understanding these processes is essential as both ALAN and temperature are predicted to intensify.

ALAN

climate change

urbanisation

multistressor

urban heat island

Animals living in urban environments face a wide range of stressors including habitat loss and degradation, a concomitant increase in the proportion of impervious surfaces, increased pathogen load and a suite of anthropogenic pollutants, such as noise, chemicals, and light at night (Gaston 2012; Parris 2016). Urban environments are also typically hotter during the day and even more so during the night (Speights et al. 2017; Tougeron and Sanders 2023) than their rural counterparts due to anthropogenic heat sources (e.g., vehicles, factories), removal of urban vegetation (Chapman et al. 2018), and heat retention of urban infrastructure (Yow 2007). This has inevitable consequences for species living in urban environments affecting individual fitness (Tuomainen and Candolin 2011; Isaksson 2015; Villalobos Jiménez 2017; Heinen-Kay et al. 2021; Wemer et al. 2021) and disrupting population and community dynamics (Johnson and Munshi-South 2017).

Aside from habitat loss, temperature is arguably the leading global environmental stressor. Rising temperatures influence individual behaviour and physiology, and lead to broadscale changes to biodiversity within an urban landscape (Oleson et al. 2015). Recent models predict that the future expected rises in temperature will increase extinction risk probability by nearly 8% (Urban 2015) and night-time warming, often referred to as the Urban Heat Island (UHI) effect (Yow 2007), is specifically highlighted as a driver of ecological outcome (Speights et al. 2017; Tougeron and Sanders 2023). While environmental temperature fluctuations influence a range of biological processes, they are particularly critical for ectothermic species, such as insects, that are less able, or unable, to physiologically regulate body temperature (Speights et al. 2017; Lahondere 2023). In invertebrates, higher temperatures are linked to increased metabolic rate (Zuo et al. 2012; Verberk et al. 2021), faster growth and development (Beck 1983; Johnson et al. 2020), earlier sexual maturation (Walker II et al. 2019), aging (Burraco et al. 2020), and shifts in immunity and the gut microbiome (Mason and Shikano 2023). Rising temperatures can also affect activities such as mating and sexual signalling due to the dependence of these behaviours on metabolic rate and energy expenditure (García‐Roa et al. 2020; Singh et al. 2020; Heinen-Kay et al. 2021). Shifts in signalling and signal reception can arise indirectly due to temperatures related impacts on growth and development which may affect an individual’s overall quality and capacity to signal (Tuomainen and Candolin 2011). Alternately, they may arise because signal production and rate are influenced by metabolic rate, which is in itself temperature dependent, as is the case for acoustic signalling in insects (Martin et al. 2000; Hedrick et al. 2002; Gillooly and Ophir 2010; Mhatre et al. 2016; Singh et al. 2020).

In addition to UHIs, artificial light at night is a pervasive environmental pollutant that is inextricably linked to urbanisation (Hopkins et al. 2018). Its presence masks daily and seasonal light patterns, disrupting long-evolved circadian (biological) rhythms and associated behaviours and physiologies (Bradshaw and Holzapfel 2007; Gaston et al. 2017; Desouhant et al. 2019; Sanders et al. 2021). Underpinning the observed adverse effects of ALAN is its influence on the photosensitive melatonin pathway. Melatonin is an ancient chemical that is both ubiquitous and conserved across life. It is typically synthesised during darkness (Jones et al. 2015; Zhao et al. 2019) and is inherently involved in modulating circadian rhythm as well as acting as a powerful antioxidant. However, all forms of light (daylight, or ALAN) interfere with its synthesis (Jones et al. 2015; Zhao et al. 2019). Accordingly, ALAN-related shifts in hormones (Robert et al. 2015; Bruning et al. 2018a; Bruning et al. 2018b), immune function (Fonken et al. 2012; Durrant et al. 2015; Durrant et al. 2020; Kenny and Howey 2020; Walker et al. 2022), development and reproduction have been documented (Willmott et al. 2018; Schligler et al. 2021). As with temperature, there is increasing evidence that ALAN can also influence the synthesis of sexual signals either indirectly due to ALAN-related reductions in the quality of the signaller (van Geffen et al. 2015a; van Geffen et al. 2015b) or directly, because its presence masks natural light cycles and signalling behaviours. Accordingly, ALAN is linked to shifts in the daily timing of signalling (Miller 2006; Kempenaers et al. 2010; Nordt and Klenke 2013; Da Silva et al. 2015; Dias et al. 2019); masking of signals produced (Elgert et al. 2021; Owens and Lewis 2022); and, a reduced likelihood that the signaller will attempt to signal, because the enhanced brightness of the nocturnal environment increases predation risk (Owens and Lewis 2018; Dickerson et al. 2022).

There is compelling evidence linking the presence of ALAN and rising temperatures as individual stressors to negative ecological impact, yet urban species are rarely exposed to a single stressor. The effect of multiple stressors is likely species-specific and environmentally context-dependent making predictions of their combined impact challenging (Crain et al. 2008; Francis 2015; Kaunisto et al. 2016; Hale et al. 2017). Multi-stressor impacts can be broadly classified as: (i) additive - the impact of the stressor interaction results in a combined effect equal to the sum of individual effects); (ii) antagonistic - the combined effect is less than the sum of individual effects or (iii) synergistic - the interaction effect is greater than the additive effects of individual stressors (Hale et al. 2017; Seebacher 2022). However, despite the global presence of elevated temperatures and ALAN, studies investigating their effects as combined stressors are relatively rare (see Tougeron and Sanders 2023) with a few studies exploring predator-prey dynamics (Miller et al. 2017) and reproductive output (Stahlschmidt et al. 2022). How these two stressors interact to promote changes to life-history traits, sexual signalling and therefore fitness in ectotherms is untested.

Here, we explore the relative impact of increased temperatures and ALAN on traits related to growth, reproduction and survival in the Pacific field cricket, Teleogryllus oceanicus. The Pacific field cricket is an ectothermic, largely nocturnal species, which is distributed across urban and rural areas of the western and northern coasts of Australia (Otte and Alexander 1983). Male T. oceanicus produce three conspicuous song types: a long-range attraction call, a short-range agonistic call and a courtship call (Alexander 1961; Ulagaraj and Walker 1973). Male calling behaviours are positively linked to male immune function (Simmons et al. 2005; Drayton et al. 2012) and female T. oceanicus prefer calls of particular rates and frequency (Simmons et al. 2001; Rebar et al. 2009; Rebar and Zuk 2009). The independent effect of temperature on life-history traits, including signalling, has been studied in T. oceanicus (Martin et al. 2000; Walker and Cade 2003; Cullum and Gonsalves 2004; García‐Roa et al. 2020) and the closely related, congeneric species, T. commodus (Masaki et al. 1979; Loher and Wiedenmann 1981; Li 2006). In contrast, the effect of ALAN on comparable traits has been explored in only T. commodus (Botha et al. 2017; Durrant et al. 2018; Thompson et al. 2019; Durrant et al. 2020). To date, no study has explored simultaneously the effect of variation in temperature and light at night during rearing on juvenile development and growth or adult survival and reproduction. To address this, we reared juvenile T. oceanicus from first instar nymphs through to mature adult crickets under one of four experimental treatments that varied in temperature and/or ALAN. We assessed the combined effect of these stressors on a range of life-history traits, including development, survival, sexual signalling, and mating success. We predicted that, as ectotherms, increased temperatures will speed the growth of individuals, alter sexual signalling and mating behaviour, and reduce survival (Beck 1983; Dell et al. 2011; Leith et al. 2021). We further predicted a negative effect of ALAN, including longer development times, reduced survival and shifts in mating behaviour as observed in the sister species T. commodus (Botha et al. 2017; Durrant et al. 2018; Thompson et al. 2019; Durrant et al. 2020). However, the relative importance of ALAN and temperature on life history traits and behaviours are harder to predict as the impacts of combined stressors are often complex and unpredictable (Halfwerk and Slabbekoorn 2015; Orr et al. 2020; Pirotta et al. 2022), and are likely to affect traits differently in a species-specific, environmental context-dependent manner.

Experimental crickets were derived from a wild-caught population located in Carnarvon, Western Australia (Simmons and Lovegrove 2020). The population had been maintained as a large, outbred laboratory population for more than 100 generations (approximately 1000 individuals per generation). A large sub-population (approximately 1000 eggs) was transferred to the University of Melbourne in 2021 where it was maintained for three generations at 25˚C on a 12hr light (2600 lx): 12 hr dark night (0.10 lx) cycle.

Lighting and Temperature Treatments

Experimental individuals were reared from first instar nymphs until the end of the experiment under ecologically relevant day-night temperatures (Control, Elevated-UHI) and light treatments (Dark, ALAN). Each treatment was exposed to a 12:12 hr light:dark cycle, which included 2600 lux during daylight hours. At night, ALAN-exposed containers were exposed to 10 lux, which approximates urban street lighting; while control males were exposed to 0.01 lux, which mimics natural moonlight levels. For the temperature manipulation, control temperature treatments approximated the average ambient day (26˚C) and night (20˚C) temperatures for T. oceanicus in the wild in their natural distribution (Chapman et al. 2018). The Elevated UHI treatment was based on projections for Cairns, Australia, a city included in the natural habitat range of T. oceanicus (Chapman et al. 2018)(Table 1) and was set at 26˚C during the day, and 24˚C at night, which approximates a UHI effect of higher daytime temperatures and warmer night temperatures. Lighting was created using standard cool-white LED light strips (6000k; Jaycar, Australia); variation in temperature was created using thermostat-controlled reptile heat mats (Reptile One® Heat Mat, AC220-240v/50Hz20W, © Kong’s (Australia) Pty Limited 2022). Rearing containers were rotated weekly between shelves (both horizontally and vertically) within the laboratory to reduce any impact of micro-climate variation. Behavioural trials were conducted under common conditions: 24-25˚C, approximately 2 hours after the onset of the scotophase, which is the typical mating activity period for this species (Durrant et al. 2018), and under red led light for mating assays (approximating darkness) and in darkness for male sexual signalling assays.

Table 1 Experimental temperature and light conditions that crickets were exposed to during the day and night during development

	Temperature (˚C)		Lighting (lx)
	Day	Night	Day	Night
Control: Dark	24	20	2600	0.01
Control: ALAN	24	20	2600	10
Elevated-UHI: Dark	26	24	2600	0.01
Elevated-UHI: ALAN	26	24	2600	10

Fitness traits

(i) Development, growth, and survival

To investigate the effects of developmental exposure to the combined stressors of ALAN and temperature on T. oceanicus life-history, juvenile development, and reproductive behaviour, we removed multiple egg pads from our stock population (containing eggs from approximately 80 females). Upon emergence, we transferred 12 groups x 100 one-day-old, first instars to experimental rearing containers (32 cm x 27.5 cm x 20 cm), containing shelter, ad libitum food and water-soaked cotton wool. Experimental containers were placed under one of our four treatments that manipulated temperature and/or ALAN exposure (see Table I; N = 3 replicate boxes containing 100 first instar nymphs per experimental treatment).

To determine early juvenile survival (proportion of individuals surviving), we censused experimental boxes weekly for the first seven weeks. After the seven-week census, a total of 224 surviving crickets (typically pre-penultimate stage nymphs; between 10-17 males and females per juvenile box) were transferred to individual containers (9 cm x 9 cm x 5.2 cm), provided with a single egg carton shelter, ad libitum food and water, and then monitored daily until death. For the resulting, individually housed, crickets we recorded survival to adult (0, 1), the day of the final juvenile to adult moult (juvenile development time), sex (male, female) and pronotum width (mm) (McNamara et al. 2014).

(ii) Male sexual signalling

At approximately 10 days (average age = 10.16 ± 0.13 days; N = 72 males) post-adult eclosion, we explored variation in male courtship calls (a measure of male sexual signalling). To separate developmental and immediate exposure to ALAN and temperature stress, assays were conducted around laboratory sunset (lights-off; night) under standard laboratory conditions (temperature = 24˚C). To ensure we were able to observe behaviours we also used a red light that simulated darkness for the cricket (Hedrick 2013). At the start of a trial, we transferred an individual male to one side of an individual anechoic chamber (17.5 x 11.8 x 7.6 cm). The chamber was divided into two equal size compartments using fine mesh and surrounded (except the top) by thick anechoic foam (Clark Rubber, Australia). An already mated stock female (isolated for 12 h prior to trial to ensure sexual receptivity) was immediately introduced to the other side of the container. The fine mesh prevented mating but allowed antennal contact (which induced male courtship calling). We recorded the pair for 30 mins using a Zoom H6 Audio Recorder (Zoom, Australia) with an attached microphone that was suspended over the anechoic chamber. If a male failed to call within 30 mins, the first female was replaced with a second non-virgin stock female. If the male again failed to produce a courtship call, he was deemed unmated and excluded from further analyses (N = 21/72 males).

To assess the relative impact of ALAN and temperature on male investment in courtship calling and call microstructure we used Audacity (Audacity Team, 2021, v. 3.0.2.). Prior to analysis recording were filtered using a low-pass filter (< 3kHz) to minimise background noise. We then counted the total number of discrete calling bouts that had at least four consecutive calls within the 30 min recording period as a measure of male investment in calling activity. We also selected at random four consecutive courtship calls and assessed their microstructure (nine parameters that described the number and rate of chirp and trill production following Simmons et al (2013)(Fig. S1; Table S1) as a measure of a male’s call quality.

(iii) Male mating behaviour

To explore the effect of variation in temperature and ALAN on adult mating behaviour, we tested the reproductive potential of two-week-old adult males (average age = 11.62 ± 0.10 days; N = 100 males) in no-choice mating trials. Prior to the trial, the male was weighed, transferred to a standard mating arena (9 cm x 9 cm x 5.2 cm) along with a similar age stock, virgin female (10-14 days post adult eclosion). Mating pairs were observed for 30 minutes, or until a successful mating (spermatophore transfer to the female was observed). If the pair did not mate within 30 minutes, the female was replaced with a second stock virgin female and the pair was permitted another 30 minutes to mate. If no mating occurred, the experimental male was considered unmated. The latency to first male call, female mounting attempts and spermatophore transfer were recorded.

Statistical Analysis

All statistical analysis was conducted using R version 5.5.4 (R Core Team 2019). Prior to analysis, response variables were assessed for normality, and transformed, where appropriate (and the exponent was noted for each model). For all models, the temperature and light treatment (and their interaction) were entered as fixed effects, and body size and male age (where appropriate) were entered as covariates. To account for the temperature treatment’s effect on female body size (see results), relative female pronotum size was used as an index of female body size ([individual pronotum - mean temperature treatment pronotum width]/standard deviation of temperature treatment pronotum width).

The proportion of nymphs surviving to seven weeks, and the likelihood of a male producing a courtship call were explored using generalised linear models, with binomial error distributions. Longevity was analysed using a cox-hazard proportional model using the ‘survival’ package in R (Therneau 2012). Variation in juvenile development, adult pronotum width, mating trial data and courtship call bout number were explored using general linear models. For mating trial data, whether a second female was required was included as a covariate. Late juvenile mortality (7 wk – adult) was extremely low (<4%) and thus we did not formally analyse this trait.

To explore variation in the courtship song, we used Principal Components Analysis (PCA) to reduce the dimensionality of these highly-correlated call traits, while minimising information loss (Jolliffe and Cadima 2016). The PCA returned four principal components (PCs) with eigenvalues > 1. These PCs were then used as response variables in a subsequent regression analysis.

(i) Growth and Survival

Early juvenile survival (first instar to week 7) was significantly lower for individuals reared under the Elevated-UHI treatment, regardless of their light treatment, or its interaction with temperature (Table 2; Fig. 1a). Of the surviving adult crickets, females reared under the Control temperature took significantly longer (20 days, 27%) to develop compared to the Elevated-UHI treatment (Mean ± SE days for Control temperature = 73.59 ± 0.61, Elevated-UHI = 53.62 ± 0.58; Table 2). Moreover, within the Control temperature treatment, Dark crickets took significantly longer (5 days) to develop than crickets exposed to light at night (significant interaction between light and temperature; Table 2; Fig. 1b). In contrast, males took 26% longer (21 days) to develop under the Control temperature and were marginally (3 days) faster to develop in the ALAN compared to the Dark lighting treatment but there was no interaction between light and temperature (Table 2; Fig. 1b).

Table 2 The effect of temperature and light treatment, and body size (where relevant) on juvenile development duration (days from egg to adult), adult body size (mm) and adult longevity (days). Bolded values are significant, with P < 0.05. (^) denotes the exponent used for the response variable. For models where Sex was significant, males and females were analysed separately. For models where the Temperature x Light treatment interaction was not significant, reduced models are reported (full models are in Supplementary Materials)

Early juvenile survival

Egg to adult development (d)

Pronotum width (mm)

Longevity (d)

Female (^2.92)

Male (^0.04)

Female (^4)

Male (^4)

n = 12

n = 109

n = 115

n = 102

n = 113

n = 213

F_1,9

F_1,105

F_1,112

F_1,99

F_1,110

c²

Temperature

29.94

<0.001

429.20

<0.001

462.02

<0.001

8.81

0.004

0.03

0.86

6.17

0.01

Light treatment

0.44

0.52

18.78

<0.001

4.18

0.04

0.01

0.92

1.43

0.23

0.41

0.52

Temperature x Light

12.57

0.001

Body size

2.27

0.13

Sex

0.00

0.97

Adult body size

Elevated-UHI treatment females had a reduced pronotum width (approx. 3%) compared to Control temperature females, but pronotum width was unrelated light treatment, or its interaction with temperature (Table 2, Fig. 1c). Male pronotum width at adult eclosion was comparable regardless of juvenile rearing treatment (Table 2).

Adult longevity

For both males and females, adult longevity decreased when reared under the Elevated-UHI treatment but was not affected by the light treatment (or its interaction with temperature), or body size (Table 2; Fig. 2).

Figure 2 Survival probability for different temperature treatments for both sexes. ‘Control’ developmental temperatures were 24˚C (day): 20˚C (night), and ‘Elevated – Urban Heat Island’ temperatures were 26˚C (day): 24˚C (night)

(ii) Mating behaviour

We found no evidence that light treatment, its interaction with temperature, or male body size influenced any mating behaviours measured (Table 3). Rearing temperature was implicated in the latency period prior to female mounting: males reared under the Elevated-UHI treatment took less time to elicit a mounting (mean temperature ± standard error: control = 4.34 ± 0.56; elevated = 3.98 ± 0.82; Table 3) but temperature did not influence the remaining behaviours. Finally, males initiated the first call, were mounted earlier and transferred sperm earlier for the first compared to the second female (mean latency ± standard error to first call: first female = 2.24 ± 0.33 mins; second female = 6.10 ± 1.76 mins; female mounting: first female = 3.33 ± 0.36 mins; second female = 10.20 ± 2.94 mins; sperm transfer: first female = 9.59 ± 0.67 mins; second female = 17.80 ± 5.39 mins; Table 3).

Table 3 The effect of developmental temperature, light treatment, male body size, and whether the male required a second female on the likelihood of mating, and the latency to calling, mounting and spermatophore transfer. Bolded values indicate significance, with P < 0.05. For models where the Temperature x Light treatment interaction was not significant, reduced models are reported (full models are in Supplementary Materials)

	Latency to call (^0.36)		Latency to mount (^0.4)		Latency to transfer (^0.04)		Likelihood of mating
	n = 92		n = 81		n = 76		n = 95
	F_1,87	P	F_1,76	P	F_1,71	P	X²	P
Temperature	1.97	0.16	6.23	0.01	0.37	0.54	1.36	0.24
Light treatment	1.17	0.28	0.03	0.86	1.67	0.20	0.16	0.69
Body size	0.00	0.99	0.49	0.49	3.68	0.06	0.23	0.63
Second female	8.02	<0.01	12.34	<0.001	4.91	0.03	76.15	<0.001

(iii) Male sexual signalling

On average, males called in about two thirds of all trials (proportion of males calling = 0.65). The likelihood of producing a courtship call was positively related to male size (estimate (standard error); ß = 1.65 (0.87)) but was not affected by developmental temperature or light treatment, or their interaction (Table 4).

Considering individuals that called, males averaged 2.82 ± 0.19 calling bouts within each trial. The number of male calling bouts was unrelated to developmental temperature or light treatment (or their interaction), or body size (Table 4).

Table 4 The effect of developmental temperature, light treatment, body size and male age on the likelihood of calling and the number of calling bouts in courtship calls produced by males. Bolded values indicate significance, with P < 0.05. For models where the Temperature x Light treatment interaction was not significant, reduced models are reported (full models are in Supplementary Materials)

	Likelihood of calling		Call bout number (^0.28)
	n = 64		n = 48
	X²	P	F_1,44	P
Temperature	0.27	0.60	0.30	0.58
Light treatment	0.00	0.96	0.38	0.54
Body size	4.31	0.04	1.66	0.20

Courtship call structure

The PCA produced four principal components with eigenvalues greater than 1 (Supplementary tables; Table S2) and explained a combined total of 87.31% of variation in courtship call structure. PC1 and 2 explaining the highest amount of variation between parameters.

PC3, which were weighted positively by chirp number and duration, and negatively by trill number and duration, was greater for males reared at high temperatures (Table 5; Fig. 3). PC3, however, was not affected by light treatment, or male weight (Table 5).

In contrast, PC1 (which is positively loaded for chirp and trill pulse duration and negatively for chirp intervals), PC2 (which is positively loaded for chirp and trill duration and chirp and trill pulse number and negatively for chirp pulse duration) and PC4 (which is positively loaded for chirp interval and trill pulse duration and negatively for trill pulse interval) were not explained by any parameter measured (Table 5).

Table 5 The effect of developmental temperature, light treatment, body size and male age on the four principal components of male courtship calls. Bolded values indicate significance, with P < 0.05. For models where the Temperature x Light treatment interaction was not significant, reduced models are reported (full models are in Supplementary Materials)

	PC1		PC2		PC3		PC4
	F_1,44	P	F_1,44	P	F_1,44	P	F_1,44	P
Temperature	1.34	0.25	3.19	0.08	11.81	0.001	0.04	0.83
Light treatment	0.09	0.76	0.96	0.33	0.00	0.99	0.04	0.84
Body size	0.03	0.87	0.05	0.83	0.10	0.75	0.69	0.41

Figure 3. Mean ± SE principal component values for male courtship song in the different temperature treatments. ‘Control’ developmental temperatures (blue bars) were 24˚C (day): 20˚C (night), and ‘Elevated – Urban Heat Island’ temperatures (red bars) were 26˚C (day): 24˚C (night)

Our data demonstrate that, for T. oceanicus, elevated temperature has a significantly greater influence on development, survival and mating outcomes than the presence of artificial light at night. Consistent with more than 80% of ectotherms, elevated developmental temperatures were associated with shorter juvenile development times for both males and females (Atkinson 1994) and reduced survival of both juveniles and adults (Beck 1983; Speakman 2005; Dell et al. 2011; Schulte 2015; Verberk et al. 2021). However, there was also evidence of temperature-related differences between males and females. Adult females reared under the higher temperature were smaller, while there was no difference in male size. In contrast, males reared under elevated temperatures produced longer chirp durations and were faster to mate (under standardised conditions) which may positively influence their reproductive success. Evidence of ALAN-related impacts or an interaction between temperature and ALAN was less clear: juvenile development time was shorter for both males and females reared under ALAN and, for females, this difference was more significant when reared at lower temperatures. Nonetheless, our data highlight the potential for urban heat islands to alter the timing and development of key life-history traits and sexual selection, which is likely to have consequences for individual fitness, and may potentiate speciation between urban and rural populations.

In isolation, temperature increases analogous to the urban heat island effect result in predictable general patterns of significantly faster juvenile development and reduced survival of juveniles and adults likely driven by shifts in metabolic processes (Beck 1983; Speakman 2005; Dell et al. 2011; Schulte 2015; Riemer et al. 2018; Verberk et al. 2021). In our study, however, these temperature-driven shifts in development, only manifested in a different body size for females. Body size is both genetically and phenotypically negatively correlated with temperature in multivoltine species, such as T. oceanicus (Atkinson 1994; Horne et al. 2015), which may offset some of the costs associated with increased metabolic processes (Riemer et al. 2018). The fact that male body size was not affected suggests potential sex-specific differences in life-history optima. Males and females differ in a wide range of traits and typically differ in their response to the thermal environment (Pottier et al. 2021). Our results are also consistent with broader patterns demonstrating greater plasticity for female invertebrates in body size and development (Stillwell et al. 2010; Cabon et al. 2024).

For T. oceanicus females, elevated developmental temperatures are likely to lead to reduced fecundity, given the positive relationship between female body size and reproductive output in this species (Simmons 2003), which may then be exacerbated by their reduced adult longevity at these higher temperatures. Males, however, do not appear to pay the same fitness costs; while male survival was reduced, they produced more attractive courtship calls (this study, Drayton et al. 2012), and were quicker to attract a mate, potentially increasing their fitness. Although ambient temperature has a positive effect on the pulse rate of T. oceanicus (Zuk et al. 2001), the duration of the chirp pulses, in particular, are under sexual selection (Rebar et al. 2009). As our study examined female preferences under common garden conditions, the increased chirp rate of males reared at higher temperatures may reflect male quality, rather than an immediate response to temperature. A similar result is observed for male south-eastern field crickets, Gryllus rubens, reared at high temperatures had calls that differed significantly in structure, speed and frequency compared with those reared at a lower temperature (Beckers 2020). A consequence of such temperature variation is that urban environments facilitate faster development and may produce more generations annually which may explain how some species, such as crickets establish so rapidly in urban areas (McNeil and Grozinger 2020).

Ultimately, our experimental approach allows us to only speculate regarding the underlying mechanisms driving the observed temperature-dependent changes in development, survival and male sexual signalling. Variation in survival may be explained by temperature-related increases in metabolic rate and associated increases in oxidative stress (Habeeb 2018; Ritchie and Friesen 2022). This increased mortality may have downstream effects on fitness that we observed in our study. The higher early mortality associated with elevated temperatures in our experiment is indicative of strong selection under this stressor. Although this may explain the increased attractiveness of this cohort, if only high-quality males survived, it does not satisfactorily account for the reduction in female body size, which is under fecundity selection. One way this may have arisen is if males, but not females, were able to offset increased metabolic rates and more rapid growth by adjusting the timing or frequency of feeding or by more efficient conversion of resources to growth (Biro and Stamps 2010). This would be further exacerbated if females traded-off somatic growth for investment in reproductive tissue. Enhanced reproductive investment in response to thermal stress has recently been demonstrated in the nematode, Caenorhabditis elegans (Gulyas and Powell 2022), while variable field crickets, Gryllus lineaticeps, exposed to a simulated heatwave preferentially invested in ovaries, compared with somatic tissue (Stahlschmidt et al. 2022). Ultimately, the underlying mechanisms of these sex-specific life-history responses to elevated temperatures requires further investigation.

In contrast to the marked impacts of higher temperatures during development on life history traits there was less evidence that crickets reared under ALAN varied compared to their Dark counterparts. Predictions and empirical evidence for developmental responses to ALAN are equivocal and are likely to depend on species-specific life-history (McLay et al. 2017; Durrant et al. 2018; Willmott et al. 2018). ALAN is a stressful unnatural light source that effectively increases the photoperiod, which is the primary seasonal cues by which insects adjust their life cycle (Nylin and Gotthard 1998). Accordingly, ALAN may theoretically decrease development times and body size for species where prolonged photoperiods indicate the approaching end of the optimal reproductive period (Masaki 1978; Carrière et al. 1996; Peter et al. 1996). Our findings of a nominal increase in developmental duration contrasts with the marked effect of ALAN on juvenile development and body size in the congeneric species, T. commodus (Durrant et al. 2018). Unlike T. oceanicus, T. commodus is facultatively univoltine, and is thus predicted to lengthen their developmental time to grow larger over the season and increase fecundity (Horne et al., 2015). Such comparisons highlight the importance of considering life-history when predicting outcomes to ALAN, and other stressors, even amongst closely-related species. Our finding that ALAN did not have an effect on signalling behaviour or mating is consistent with previous studies in this genus (Botha et al. 2017). This contrasts with previous ALAN studies documenting chemical (Kempenaers et al. 2010; Dominoni et al. 2013; Da Silva et al. 2015; Dickerson et al. 2022), visual (Owens and Lewis 2022) and acoustic (Baker and Richardson 2006; Dickerson et al. 2022) disruptions to signalling, and mating (Touzot et al. 2020). It is pertinent, however, to note that all acoustic recordings and matings were observed under dark conditions, resulting in a mismatch between developmental and immediate ALAN conditions in some treatments. Immediate ALAN conditions may alter calling behaviour as it is entrained to the photoperiod; male T. oceanicus commence calling prior to sunset (Loher and Rence 1978; Evans 1988), but chorusing typically starts after astronomical twilight (Meixner and Shaw 1979). Indeed, immediate, rather than developmental, exposure to ALAN has been shown to alter mating success in other orthopterans (Stahlschmidt et al. 2022).

Finally, our study provides limited evidence for a significant interaction between ALAN and temperature. Recent attempts to characterise the general patterns of multi-stressor interactions have been equivocal and (Schäfer and Piggott 2018; Mack et al. 2022): some studies suggest synergisms as the most prevalent outcome (Gunderson et al. 2016), while other studies report single-stressor dominance, in which negative impacts are primarily explained by the strongest stressor (Folt et al. 1999; Morris et al. 2022), which may be more likely when there is asymmetry in the strength of the stressor (Piggott et al. 2015; Côté et al. 2016), or when there are co-tolerances (Vinebrooke et al. 2004). For example, ALAN and elevated temperatures may have negative effects on a particular cohort of the population, but if elevated temperatures killed these vulnerable individuals during early development, then ALAN may no longer appear to have an effect when these stressors act in concert. Consistent with this, adult variable field crickets, Gryllus lineaticeps, exposed to an acute (not developmental) period of high-intensity ALAN (97 lx), in combination with a simulated heatwave, also failed to find consistent combined effects of ALAN and temperature on morphology or mating success (Stahlschmidt et al. 2022). Other studies have also highlighted that multi-stressor interactions may not be consistent across stressor gradients. For example, in the springtail, Orchesella cincta, thermal stress was reduced when it was applied under longer photoperiods ecologically consistent with higher temperatures (Summer)(Liefting et al. 2017). We intentionally chose biologically relevant stressor intensities and durations for both ALAN and temperatures in this experiment, suggesting that the absence of multi-stressors effects may indeed reflect observed conditions for wildlife.

In conclusion, understanding how anthropogenic stressors, such as ALAN and temperature, act in combination is critical to predicting future environments, especially given the inexorable increase in the pervasiveness and intensity of both these stressors. While this study provides clear evidence of temperature-modifying changes to both the development, mating behaviour and sexual signalling in a nocturnal ectotherm, we found overwhelmingly little support for an effect of ALAN in isolation, or in combination with temperature on any of the other traits measured. Instead, our data indicates the neutral or positive impact of rising temperatures on individual behaviour and potentially fitness of this species. In general, there is consistent evidence for intra-specific differences between urban and rural populations (Evans 2010). The disruption to mating signals that we observed under UHI conditions here could trigger local mate preferences and eventually incipient speciation between urban and rural populations (Johnson and Munshi-South 2017; Hopkins et al. 2018).

SIGNIFICANCE STATEMENT

Both light pollution and elevated temperatures can have significant impacts on wildlife health, development and reproduction. However, we know very little about how these stressors interact, which is typical in urban environments. We exposed Pacific field crickets, over their lifetime, to both stressors at the same time, or each in isolation. We demonstrate that combined stressor impacts are complex. Elevated temperature was the dominant stressor, reducing juvenile development and adult survival, while increasing male attractiveness to females. Despite predictions, light pollution had relatively little impact, when in isolation or in concert with elevated temperatures. Our data demonstrate the importance of investigating multi-stressor or combined stressor processes when quantifying the impacts of urban stressors on wildlife, as they are not predictable.

Competing Interests
The authors have no relevant financial or non-financial interests to disclose. This research was funded by the Australian Research Council (DP210101915 to TMJ).

Author contributions:

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Nicholas Fitzgerald, Zion Kim and Nicola-Anne J. Rutkowski. The first draft of the manuscript was written by Kathryn B McNamara and Therésa M Jones and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

ACKNOWLEDGEMENTS

We thank Marty Lockett for assistance with acoustic recordings.

DATA AVAILABILITY

Data used in analysis has been available as electronic supplementary materials.

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Artificial light at night and temperature as combined stressors on the development, life-history, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus

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Abstract

Figures

Introduction

Methods

Lighting and Temperature Treatments

Fitness traits

(i) Development, growth, and survival

(ii) Male sexual signalling

(iii) Male mating behaviour

Statistical Analysis

Results

(i) Growth and Survival

(ii) Mating behaviour

(iii) Male sexual signalling

Courtship call structure

Discussion

Declarations

Competing Interests
The authors have no relevant financial or non-financial interests to disclose. This research was funded by the Australian Research Council (DP210101915 to TMJ).

Author contributions:

ACKNOWLEDGEMENTS

DATA AVAILABILITY

References

Supplementary Files

Status:

Version 1

Artificial light at night and temperature as combined stressors on the development, life-history, and mating behaviour of the Pacific field cricket, Teleogryllus oceanicus

Status:

Version 1

Abstract

Figures

Introduction

Methods

Lighting and Temperature Treatments

Fitness traits

(i) Development, growth, and survival

(ii) Male sexual signalling

(iii) Male mating behaviour

Statistical Analysis

Results

(i) Growth and Survival

(ii) Mating behaviour

(iii) Male sexual signalling

Courtship call structure

Discussion

Declarations

Competing Interests The authors have no relevant financial or non-financial interests to disclose. This research was funded by the Australian Research Council (DP210101915 to TMJ).

Author contributions:

ACKNOWLEDGEMENTS

DATA AVAILABILITY

References

Supplementary Files

Status:

Version 1

Competing Interests
The authors have no relevant financial or non-financial interests to disclose. This research was funded by the Australian Research Council (DP210101915 to TMJ).