The impact of temperature upon the phenology of Pieris rapae (Cabbage White Butterfly) as an indication of climate change.

Cygnus (2012) 1:21-30 DOI 21140496, 21127332, 21160938, 20759308 RESEARCH ARTICLE The impact of temperature upon the phenology of Pieris rapae (Cabbage White Butterfly) as an indication of climate change. Jessica Cockerill Aiden Depiazzi Stephanie Gill James Rogerson Received: 22 May 2012 / Accepted: 28 May 2012 Abstract A preoccupation with climate change in contemporary society has led to many investigations into its authenticity. Scientists suspect that it is causing phenological changes among a variety of species on our planet. To investigate this, Earthwatch developed a citizen science website, ClimateWatch, in which Australian citizens can observe and record data on climatological indicator species in the hope of collaborating the data to find out if and how the species are affected by climate change. To investigate this we used ClimateWatch data to examine whether the P. rapae (Cabbage white butterfly) are affected by climate change, and predicted that mature butterflies would appear earlier in the year, and reach greater numbers, corresponding to increasingly warmer climates. Data revealed that the mean number of P. rapae recorded per sighting has increased in earlier months of the year between 2009 to 2011 in Western and Eastern areas of Australia. It was also noted, through examination of data attained from the Australian Bureau of Meteorology, that in these earlier months the average maximum temperature had increased. Although our data supports the predictions, by relying upon citizen scientists for data, there is a high potential for experimental error as citizens are not qualified scientists, and may therefore be unaware of the strict scientific method required for reliable observations. We can conclude from these results that P. rapae s phenology is affected by mean maximum temperature fluxes, but though we may project quantitative information about climate, the long-term qualitative implications upon species phenology in general would require further and more detailed experimentation across decades, species and climates. Keywords Pieris rapae, Cabbage white, phenology, climate change, Australia 21

1 Introduction It is normal for climates to change, but since the proliferation of human civilisation and agriculture, this change seems to be occurring at a rate too fast for species to adapt. Many species are responding to altered climates through changes in phenological behaviour (Parmesan 2006): that is, the timing of recurrent biological events, the causes of their timing with regard to biotic and abiotic foreces, and the interrelation among phases of the same or different species (Badeck et al. 2004). However, they are limited to protected areas due to an increasing range of human habitation and agriculture, which means they cannot relocate to better-suited climates as easily. As climate change accelerates, species may not be able to adjust or migrate to keep up, and this interruption of essential phenological occurrences has the potential to lead over a million species into extinction (ClimateWatch: an initiative of Earthwatch Institute, 2012). Earthwatch is an international, non-profit institution that was developed to achieve the ultimate goal of sustainable living, where ecosystems thrive and the diversity of life flourishes (Earthwatch Institute, Australia, 2012). ClimateWatch was developed by Earthwatch to study the behaviours of Australia s indicator species, defined by Landres et al. (1988) and McGeoch et al. (1998) as organisms whose presence is used to mirror environmental conditions or biological phenomena too difficult, inconvenient, or expensive to measure directly (Rolstad et al. 2002). In this case species are observed to see if and how climate change affects them. ClimateWatch allows every Australian citizen to be involved in this research project by helping collect and record data on different phenological changes within species, such as flowering times, breeding cycles and migration movements. It is thought that these phenological changes are being affected predominantly by temperature changes caused by anthropogenic global warming, and hence the following investigation focuses upon temperature, rather than other climatic factors such as rainfall, as the seasonal variable (ClimateWatch: an initiative of Earthwatch Institute, 2012). One of ClimateWatch s many indicator species is the Pieris rapae (Cabbage white butterfly). Its larvae are 20mm in length, and coloured green with faint yellow stripes across their back. When resting, the larvae will align themselves on a leaf so as to line up with the veins, hence camouflaging themselves from Fig. 1 Male (above) and female (below) of the cabbage white butterfly, Pieris rapae (Lokkers & Jones 1999) 22

predators(climatewatch: an initiative of Earthwatch Institute, 2012). Mature butterflies have a wingspan of 44mm, a black tip on the front of their forewing and a black patch on the front of their hind wing. The female butterflies have two black spots on their front wing whereas the male butterflies have only one (Museum Victoria: Cabbage White Butterfly Pieris rapae 2012). Pieris rapae is an introduced species in Australia, first sighted in Melbourne 1929, and is thought to have arrived accidentally from New Zealand. The butterfly quickly spread throughout Australia, and was particularly prolific in the south, including Tasmania, before finally making its way to Western Australia in 1942 (Braby 2000; Peters 1970). P. rapae is considered an agricultural pest because of its diet of cruciferous crops when in larval form. The larvae mainly eat plants from the Brassicaceae family, including key agricultural vegetables such as broccoli, cabbage, Brussel sprouts and many more. Because of this they were able to move across Australia and live in urban areas, forests and woodlands, and are regularly found in vegetable and domestic gardens (Australian Museum: Cabbage White Butterfly, 2009). Pieris rapae s life cycle is temperature dependent, and easily observed by citizens in both metropolitan and rural areas, so although not an Australian native, they are an ideal indicator species for ClimateWatch. The butterfly will lay its eggs on the underside of a fresh leaf on a healthy plant. When the egg hatches the larvae begin to eat the leaf, before progressing onto other leaves on the plant. Emergence of the mature butterfly begins mainly at the end of winter and early spring, but there may be several generations throughout the year if weather is favourable. As such, the life cycle may vary throughout the year: in late summer in Sydney, a full cycle may only take around three to four weeks, with the pupae dormant for only nine days, whereas in cooler months, the pupae may be dormant for several months before emergence (Braby 2000; Jones 1981). It is therefore expected that if the Australian climate is indeed changing, the timing of emergence as an adult butterfly will be affected. As such, the purpose of this investigation is to observe if climate change is causing P. rapae to appear earlier in relation to increasingly warmer climates. This is tested by analysing data collected by citizens, which they are encouraged to upload to the ClimateWatch website. Citizens are asked to provide details on the number of P. rapae in one sighting, the location of a sighting, and the date of sighting. Through this we may devise the average number of butterflies observed during spring and summer months from late 2009 to early 2012 in two different locations (coastal western Australia and coastal eastern Australia) as average temperatures increase. We predict that the mean number of P. rapae per sighting has increased in earlier months of the year from November 2009 to January 2012 as a result of climate change. 23

2 Materials and Methods The data source for this article is a collection of observations of P. rapae recorded by citizens through the ClimateWatch program. ClimateWatch instructs its citizen scientists to mark each observation in terms of: the species being observed, including the number present; the specific behaviour of the species; the location, time, and date of the sighting; and any other comments about the observation. ClimateWatch provides its citizen scientists with a list of indicator species, which by definition are common and easily recognisable species whose presence and behaviour can be observed around the country by a large number of people, and whose phenology changes according to climatic conditions. Hence ClimateWatch simplifies its process by limiting the number of indicator species, and also the number of possible observable behaviours. In the case of the cabbage white butterfly, citizen scientists were limited to observing the butterflies: being present (P), courting or mating (C), egg laying (EL), or in a chrysalis phase (Ch). Observers who sighted the species recorded its presence according to the criteria listed above, and registered the observation via the ClimateWatch website. The collection of data for P. rapae was then made available to us for analysis to prove or disprove the terms of our hypothesis. The file containing all of the observations sourced by ClimateWatch for P. rapae, from November 2009 to January 2012, contained 740 individual observations from a diverse range of locations. We found that the vast majority of data were gathered from two geographical clusters, in and around Perth (Zone A), and in and around metropolitan areas in Victoria and New South Wales (Zone B). Due to the comparatively small number of observations recorded from areas such as northern Western Australia or South Australia, discarded all observations outside of latitude ranges A -33.65 to -30.60 and B -38.51 to -36.86, and longitude ranges A 115.34 to 118.38 and B 142.03 to 146.25. This reduced the data space to 513 observations for Zone A and 131 observations for Zone B. We believed this to be a good way to separate the data, as it effectively separated observations into (A) a Mediterranean climatic Zone, and (B) a moderate temperate maritime climatic Zone. Hence, in addition to analysing the number of butterflies per sighting across time, we were also able to do so across different climate types. We further sorted the observations according to date. We grouped observations into months, from November 2009 to January 2012. We then took the mean number of butterflies per sighting for each month (values shown in Table 3.1) and plotted these values for Zones A (see Fig. 2) and B (see Fig. 3). To assist in our analysis, we gathered further data from the Bureau of Meteorology (Meteorology 2012) to represent the change in mean temperatures for the same time period as our data on P. rapae (November 2009 to January 2012). The climate data for Zone A is shown in Fig 2, and for Zone B, Fig. 3. 24

3 Results We found that the mean number of P. rapae per sighting has increased in earlier months of the year from 2009 to 2011. Zone A (West Australian coast) and Zone B (East Australian coast) are separated due to general overall climatic differences of their latitudes and longitudes. The mean number of butterflies per sighting (N) of P. rapae in these two Zones are displayed in Table 3.1. The cropped data for P. rapae sightings are illustrated in Fig 3. 1 for Zone A and Fig 3.2 for Zone B alongside the mean monthly maximum temperatures in degrees Celcius (T) from November 2009 to February 2012. By comparing trends in P. rapae sightings to the change in mean maximum temperatures gathered from the Bureau of Meteorology (Meteorology 2012) over the same time period, we were able to see that spikes in P. rapae sightings and spikes in mean maximum temperature seem to correspond. Note that the mean number of butterflies per sighting spikes within the same time period as the mean maximum temperature in both Zones, and that spikes in both Zones are also higher in summer 2011 than in summer 2010. This increase in the average number of butterflies per sighting corresponds in both regions to increasing mean maximum temperature, as the highest average number of 25

butterflies per sighting was 15 for Zone A, and approximately 18 for Zone B, in early December 2011 and in late November 2011 respectively. Climatically, this is a period of evident increase in monthly mean maximum temperature in both regions. It is also evident that spikes in P. rapae sightings occur earlier in the year in summer 2011 than in summer 2010 for both Zones. For some months, no sightings occurred in either region. These were in June and July, in early and mid-winter, during a period of decreasing monthly mean maximum temperature. This decrease in the average number of butterflies per sighting corresponds in both regions corresponds with decreasing mean maximum temperature. Fig 2 Mean number of butterflies per sighting (M) and mean monthly maximum temperature in degrees Celsius (T) for Zone A, the western region Fig 3 Mean number of butterflies per sighting (N) and mean monthly maximum temperature in degrees Celcius (T) for Zone B, the eastern region. 26

While Zone A showed a distinct spike in mean number of P. rapae per sighting for each summer, Zone B displayed a pattern of two spikes within each summer. From November 2009-June 2010, the mean number of butterfly per sighting began at approximately six, before reducing to two in January, and then returning to four mid May 2010. The consistent absence of sightings then ran from June until late August. Between August 2010 and April 2011 the two spikes occurred in late August, with a mean of six butterflies per sighting, and over January 2011, with a mean of ten butterflies per sighting. Between these two spikes mean numbers of butterflies per sighting reduced to four, in late December 2010. This same pattern emerged again over August 2011-February 2012, except that the first spike in mid November 2011 reached a mean of 18 butterflies per sighting, and the second, mid January 2012, only six butterflies per sighting, with a reduction to a mean of two butterflies per sighting in late December 2011. The two spikes in summer of 2011-12 differed from the preceding year in that the maximum spike in mean butterflies per sighting was reached in the first spike, with the second showing twelve less butterflies per sighting, whereas in summer 2010-11, the maximum was reached in the second spike: four more butterflies per sighting than in the first spike. It was also observed in Fig. 2 that for Zone A, in 2010 P. rapae were sighted from mid August to late December (a period of approximately four months) while in 2011 they were sighted in mid July to mid January (a period of approximately six months. So, in Zone A, not only were butterflies sighted earlier in the year, but they were also sighted for a longer period of time. This was noticeably not the case for Zone B in Fig. 3, in which butterfly sightings increased rapidly mid August 2010 before decreasing rapidly between April and May 2011 (a period of seven months), while at the end of 2011 they appeared early August until mid February 2012 (a period of only approximately six months). So, in Zone B, the period of time for which butterflies appeared was in fact shorter in the successive year than the initial year upon which our data is focused. 4 Discussion We hypothesised that the mean number of P. rapae per sighting has increased from 2009-2011 as a result of climate change. After the analysis of ClimateWatch data it was found that the number of P. rapae sighted had increased in the warmer months of the year, with no data recorded for the winter months (June-August).We also found that the butterfly was sighted earlier in the year in 2011 compared to 2010, where the first sighting was in September, as opposed to August in 2011. Additional meteorological data was collected on climate over this time period to compare with the ClimateWatch data to see if there was any relationship between climate and the number of butterflies present. The data collected does, in part, support our hypothesis, in that the mean number of P. rapae per sighting has increased in earlier months of the year from 2009 to 2011. A possible correlation may be drawn when analysing patterns in sightings of P. rapae alongside data on 27

average maximum temperatures, from the Bureau of Meteorology. The ClimateWatch data has distinct periods with no observations during colder months; Jones and Ives (1979) provide a possible explanation in that adult butterflies emerge towards the end of winter and early spring. However, the gaps are also a limitation in our data set, as we don t know for certain whether the butterfly was not present during these periods, or whether the absence of observations is simply due to ClimateWatch citizens not making observations during these colder months. It is possible that there is a correlation between the overall increase in mean maximum temperatures in 2011-2012 as opposed to 2010 (in both zones), and number of butterflies per sighting, as shown in figure 3.1 and 3.2. A more rapid cycling of butterfly life spans in warmer months would be able to occur for a longer time, resulting in greater proliferation of P. rapae and thus more numbers per sightings. Unfortunately our dataset is relatively smallscale, and therefore does not necessarily show a pattern of long-term climatic temperature increase for either zone, nor does it specifically show distinct long-term changes in the numbers of butterflies sighted. As such we cannot draw a causal relationship between mean number of butterflies per sighting and climate change, as per our hypothesis. For example, in Zone B, it was observed that the time period in which butterflies were sighted in 2011-12 was in fact less than in 2010. If observed in conjunction with meteorological trends for Zone B, it is possible to infer that this corresponds with a lower maximum average temperature in 2011-12 than in 2010. Temperatures became hotter in 2011 sooner than in 2010, so butterflies were sighted sooner (as with Zone A), however reached only a maximum of approximately 22 degrees in summer 2012 (within the limitations of the dataset), in comparison to the maximum of 28 degrees reached in summer 2011. In the data there are obvious areas where insufficient data has been collected. If this is due to a lack of butterflies, or just lack of citizens collecting data at this time, we are unsure, but there is a notable difference in the times of year butterflies have been spotted. In zone A, there is clearly a lack of observations before September 2010 and in early 2011. Again, we cannot state for certain that this is due to no butterflies being present. But if we look and the number of butterflies recorded per sighting there is a clear increase in population size of the P. rapae from 2010 to 2011. In zone B there is a sufficient sample of sightings that show patterns of the P. rapae s presence in different seasons. There is an increase in the numbers of butterflies sighted from 2009 to 2011, which is maintained for the earlier months of 2012 (there is no available data after February 2012). We can also see a significant difference when the first butterflies have been spotted after the winter months. This has occurred earlier in 2011 than 2010, which could be explained by the higher mean maximum temperature in August 2011 and August 2010. This data from zone B also shows that the butterfly s presence as been reduced earlier in the later years. This could be due to average temperatures falling earlier in 2011 than in 2010, but the only factor we have focused upon here is temperature and number of P. rapae, though there are many more other environmental factors that could be at play here. Between 1950 and 2003, temperatures in Australia rose significantly, with the warmest year occurring in 1998. Since 1990 the continental average temperature for Australia has increased 28

by approximately 0.8 C, and from this trend it is possible to forecast increasingly hot temperatures (Hughes 2003). The butterflies lifecycle occurs faster under hotter temperatures due to their phenology, so that there is a population spike and therefore more frequent sightings in warmer temperatures. Temperatures necessary for P. rapae to reach maturity would occur earlier in the year if the climate is hotter overall, so the appearance of mature P. rapae could be expected to occur earlier in the year. Similarly, fewer sightings in winter months may be explained by a longer pupae dormancy in cooler weather (Braby 2000; Jones 1981). If, as projected by Hughes (2003) annual mean temperatures over most of Australia are 0.4-2.0 C higher by 2030, and 1.0-6.0 C higher by 2070, with warming occurring most prominently in spring, it may be predicted that more butterfly sightings will occur increasingly earlier in the year in the future, and that numbers will be more prolific. Employing citizen science as a means of experimental method attributes a degree of error to any data collected, as seen in the often inconsistent or invalid contributions to the ClimateWatch dataset analysed in this report. Internal validity is compromised by (1) a lack of detail in some of the observations made; (2) by periods of time where no observations are made, which leaves it ambiguous as to whether it is due merely to an absence of P. rapae or an absence of citizen scientist observations; (3) the time of day and specific place the data was collected is not consistent over the data set: it is very difficult to have citizens record data for the same species at the same location and at the same time of day everyday for a long period of time; (4) the potential for fabricated or incorrect observations. These inconsistencies in the data could be avoided by increasing the quantity of willing citizen scientists that record P. rapae sightings throughout all times of the year over at least thirty years. With a large number of results, faulty results will not have as much impact upon the overall trends in the data, and final results are less likely to be distorted by occasional observations that are flawed in these ways. If enough data is gathered to be considered a reliable indication of trends in phenology of P. rapae, and acknowledge seasonal variables that may impact the numbers of P. rapae per sighting or the number of sightings - such as pesticides, variation in populations, and insufficient participants collecting observations- then it may become possible attribute the phenological changes in P. rapae to climate change. Because our data is only for a three-year period it is not lengthy enough to draw conclusions from. It may, however, provide a basis for future research into the phenology of other species as impacted by climate change, as well as the contribution of changes in other factors, such as rainfall or non-climatic conditions, to the shifting phenology of P. rapae and other indicator species. Acknowledgements We are grateful to Emile van Lieshout for his advice; to Colin Flower, Robin Hare, Daniel Malecki and Daniel Della Vedova for reviewing the draft paper; and finally, to ClimateWatch, Earthwatch, and the Australian Bureau of Meteorology for the provision of data. 29

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