Alexander Irwe

Degree project for Bachelor of Science inBiology

BIO602 Biology: Degree project 15 hecSpring 2015

Department of Biological and Environmental SciencesUniversity of Gothenburg

Examiner: Christer ErséusDepartment of Biological and Environmental Sciences

University of Gothenburg

Supervisor: Urban OlssonDepartment of Biological and Environmental Sciences

University of Gothenburg

Importance of Flightfor habitat occupancy

A pilot study on American Ground Beetles

Frontpage photo by: Jeffrey S. Pippen Macon Co. NC12 May 2006

Table of content Abstract…………………………………………………………………1 Introduction……………………………………………………………..2 Material and Methods…………………………………………………3 Results………………………………………………………………….5 Discussion………………………………………………………………5 Table 1 and 2…………………………………………………………..6 Acknowledgements……………………………………………………8 References……………………………………………………………..9

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Abstract

Abstrakt

Insects are one of the oldest groups of terrestrial animals still living today and were the first to evolve wings. Since then insects have evolved into many different shapes and sizes and occupy a wide range of niches. One group of insects, the Carabidae or ground beetles are interesting as they contain both species with good flight capacity and species with reduced wings that have lost the capacity to fly. The genus Cicindela is a group of ground beetles that have a larger than average flight capacity of most beetles. Carabus on the other hand is a genus were most of the species have reduced wings and lack the ability to fly. There is both cost and benefit in having flight capabilities and one benefit would be quicker and better movement. The assumption that flying species would better disperse themselves could be tested by comparing fundamental niche usage between two groups that differ in flight capabilities. To test this occurrence data of species from the Carabus and Cicindela genera were retrieved to calculate their realized niche, and Ecological niche modelling (ENM) was done to project their fundamental niche. The difference in realized and fundamental niche area was calculated for both genera and statistical tests were performed. The results indicate that Cicindela occupies a larger proportion of their fundamental niche than Carabus but the results from the statistical tests were not conclusive. A significant difference between the two genera was only seen when looking at the proportional difference but not when looking at the difference in real values. More species and further refinement of the ENM could help to increase confidence of the test.

Insekter är en av de äldsta landlevande djur som fortfarande lever idag och var de första som utvecklade vingar. Insekter har sedan dess utvecklats till många olika former och storlekar och ockuperar en mängd olika nischer. En grupp av insekter, Carabidae eller jordlöpare är en intressant grupp då de innehåller både arter med god flygförmåga och arter med reducerade vingar som har förlorat sin förmåga att flyga. Släktet Cicindela är en grupp jordlöpare som har en flygförmåga över det vanliga för de flesta skalbaggar. Carabus är istället ett släkte där de flesta arter har reducerade vingar och saknar flygförmåga. Det finns både för och nackdelar av att kunna flyga och en fördel är att kunna förflytta sig snabbare och lättare. Antagandet att flygande arter skulle ha lättare att sprida sig kan testas genom att jämföra fundamental nischanvändning mellan två grupper med olika flygförmåga. För att testa detta hämtades data på förekomst av arter från släkterna Carabus och Cicindela för att sedan räkna ut deras realiserade nisch. ”Ecological niche modelling” (ENM) användes för att projicera arternas fundamentala nisch. Skillnaden mellan realiserad och fundamental nisch area räknades ut och statistiska tester utfördes. Resultaten visar på att Cicindela ockuperade en större andel av sin fundamentala nisch än Carabus men resultaten från de statistiska testen var inte fullt övertygande. En signifikant skillnad mellan de två släkterna sågs endast för den proportionella skillnaden men inte för den faktiska skillnaden. Fler arter och mer finputsning av ENM kunde hjälpa till att öka säkerheten av undersökningen.

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Introduction Insects were one of the first animals to invade land some 400 million years ago which created many new opportunities for insects to adapt to new niches (Grimaldi et al, 2005). Since then insects have adapted to a number of different environments and evolved many types of features. The ability to fly was first evolved by insects sometime in the Carboniferous time period and has since then evolved in many different species and groups of animals (Knecht et al, 2011). Flight allowed for rapid movement to catch pray, avoid being caught or to reach new otherwise inaccessible habitats. Flying is costly since it requires a lot of energy to remain airborne, so for it to evolve the benefit has to outweigh the cost of maintaining the ability to fly (Roff, 1986). When studying newly formed habitats such as islands made from volcanic activity, species with flying capabilities and plants with air-travelling seeds and pollen are usually the first ones to settle in the newly formed habitat. Interestingly enough, islands and other isolated habitats have a proportionally larger number of species without flight capabilities than inland habitats. This suggests that selection pressure for flight may decrease in isolated islands (Gillespie, 2007). The term brachypterous is used to describe the loss of or reduced wings in animals and can be seen throughout the Insecta lineage. Some species have both winged and brachypterous morphs in a population and are thought to be an adaptation depending on the stability of the environment or a trade-off from other features (Roff, 1986). One obvious drawback from wing reduction is the loss in mobility and perhaps the potential ability to disperse. One interesting group of insects are the ground beetles Carabidae which today have more than 40,000 species described (Erwin, 1985). They are found

in almost all types of environments and can be found all around the globe. Most of them are carnivores (Lövei et al, 1996) but some species seem to be omnivores or even frugivores (Hill et al, 1992). A lot of species have lost their ability to fly or have reduced wings (Lövei et al, 1996) but many species of the genus Cicindela or common tiger beetle which is part of the Carabidae family can still fly (Carter, 1989). Another large group of ground beetles is the genus Carabus in which most species lack functional wings (Lindroth, 1986). Most ground beetle species seem to have similar habitat and food preference (Lövei et al, 1996), so the major difference between the Carabus and Cicindela genera are the flight capabilities. One can then assume that species from the Cicindela group would be much more proficient in finding new areas with suitable habitats. Since most of the Cicindela species still have functional wings it would be assumable that they have an easier way to disperse themselves. One possible way of testing this would be to calculate the area of the realized niche for the species in each group and then calculate the area of the fundamental niche for each species. Realized niche in this case refers to a species current niche where it actually resides and fundamental niche refers to a species potential niche were it could live (Sadava et al, 2011). A species realized niche is usually smaller than its fundamental niche as it might be restricted from a number of factors such as competition from other species or migration hinders. If Cicindela species are better at dispersing they would use their potential habitats to a higher extent than species from the Carabus genus. In this study I gathered information on the current distribution and compared it to the potential distribution estimated by Ecological niche modeling. The test is to see if flight capability has a positive

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effect on the ability to disperse. The null hypothesis is that no difference in relative utilization of available habitat exists between two groups of different flight capabilities. A difference would violate the assumptions of the null hypothesis and indicate that flight is important for the ability to colonize all areas of suitable habitat.

Material and Methods Occurrence data retrieval and Ecological niche modelling For this study 10 species of each ground beetle genus Carabus and Cicindela were used, giving a total of 20 species. More species would have been selected but there was a limited number of Carabus species with occurrence data available. North America was selected as an area of interest since it has a lot of well documented records of species and is a relatively large area with no large expanses of water interfering with species migration. The selected species were chosen by looking at which of them had the most available data from the Global Biodiversity Information Facility (GBIF) (http://www.gbif.org/). The occurrence data for each individual species was retrieved using the Data Refinement Workflow v17 available at the Biovel portal (https://portal.biovel.eu/). This workflow is connected to GBIF for automatic species occurrence retrieval. After the occurrence data was retrieved a refinement of the data was done using Open Refine (http://openrefine.org/) which is a part of the Data Refinement Workflow. This refinement included removing any data points lacking valid coordinates, any data points that were older than 1970, and excluding any data points not found in the United States of America or Canada. To calculate the area for the species potential habitats I used Ecological niche modelling (ENM). This process uses occurrence data

points together with environmental data to model the species fundamental niche over a geographical area (Kearney, 2006). Before the initial ENM was done a trial and error phase was conducted to see which environmental layers were to be used in the final model. This was done using a custom made workflow based on jackknife resampling that test which of the chosen layers affected the model the most (Leidenberger et al). The layers that had the biggest effect were considered most important for the accuracy of the model. Correlation tests using ENMtools (http://enmtools.blogspot.se/) were also conducted to make sure none of the layers correlated with each other. If any layers correlated the one that had the lowest effect from the jackknife tests was removed. The environmental layers selected by the jackknife and correlation tests were: annual mean temperature, precipitation of driest month, temperature annual range, bulk density, salinity, gravel content, ph and altitude in meters. Studies on ground beetles suggested that humidity would be a limiting factor for habitat preference (Lövei et al 1996) which coincides with the precipitation of driest month layer in the model. Sand fraction was also added as a layer because a study on habitat preference for eight Cicindela species showed a preference for sandier ground types (Schultz, 1989). The occurrence data from all the species were also used in the Bioclim workflow (also available at the Biovel portal) to only select data points that were environmentally unique to be used in the ENM. The same selected layers were both used for the Bioclim workflow and the ENM. The models were created using the default Ecological niche modelling workflow at the Biovel portal. The ENM algorithm was set to Maximum Entropy and the default algorithm parameters were used. The selected layers were projected in 10arc-minutes and cross validation on 10 replicates, with threshold set to

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lowest presence point, was done in order to test the accuracy of the models. The projections made from the models were not projected on the entire North American continent as some areas were left out using a mask created for the projections. This was done by mapping all findings of beetles in North America by looking at a map from GBIF showing all beetle findings (Fig. 1). Projections from all the species was saved as tif-files for further analyses. Area calculation using QGIS To calculate the specie’s realized and fundamental niche area, the free open source program QGIS was used (http://www.qgis.org/en/site/). The occurrence data points and the projection tif-files were imported into QGIS and projected using the World

Equidistant Cylindrical coordinate reference system that uses meters as length unit. Each projection has a set of values indicating the habitat suitability for a particular species were the highest value equals 100% suitability and the lowest 0% suitability (Fig. 2). A new raster tif-file was generated using the raster calculator of QGIS. The new raster file only included values higher than 40-50% suitability depending on the strength of the projection model. This new raster file was then transformed into a vector file for easier area calculation using the area function included in attribute tables in vector files. To calculate the realized niche area of a species, a buffer zone was made around each occurrence point forming another vector file. The buffer zones were approximately 150 km in diameter and the summed area for all buffer zones were also calculated using the area function in the attribute tables. All of the above steps were done for each of the 20 species. Statistics using SPSS To test the significant difference between the two groups a statistical test was performed using the software IBM SPSS Statistics 22. Before the actual test a minor analysis was performed to see if the data was normally distributed as this is a requirement for certain

Figure 2. The projection tif-file for Carabus chamissonis showing the suitability and occurrence points.

Figure 1. Map showing occurrence data points from all species of beetles in North America.

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statistical tests. The difference in area between the realized and fundamental niche of the two groups was tested by a simple independent T-test with a confidence interval of 95%. This was done for the actual values but also on the ratio between realized and fundamental area divided by the fundamental one. This is done since the realized niche area differs between some of the species and having it in percentage gives a better representation of the difference. The percentage values were also arcsin transformed to make them closer to a normal distribution but also because values near 100 or 0% could hamper with the statistical test. (Chestnut, 1995).

Results The number of data points differed between the two genera as the Cicindela group had a larger average of 93 data points and Carabus only had an average of 31 data points per species (Table 1). The average internal area under the curve (AUC) from the ENM for all the models was 0.955. The AUC is a sort of measure of model strength and a value above 0.8 for this study is considered acceptable (Hanley et al, 1982). Average omission error for all species was 8.03 which are at an acceptable level for this study. Figure 3 shows a

map of the realized and fundamental niche area for one of the species after all the steps in QGIS were made. Cicindela has a higher average realized niche area of 1006587 km2 and Carabus an average value of 372296 km2. Difference in fundamental niche area is not as high between the two genera as both are close to 2000000 km2. The difference between the realized and fundamental niche is slightly higher in Carabus with an average value of 1589605.4 km2 as opposed to Cicindela with an average of 1207211.3 km2 (Table 1). The statistical test does not show a significant difference between the groups for the actual values. The transformed values do show a significant difference between the groups (Table 2).

Discussion When looking at the actual results from Table 1 there is indication of a difference between the two genera. Carabus has a lower average realized niche area and there is a bigger difference between realized and fundamental niche area for Carabus than for Cicindela. This could indicate that the assumption made earlier is correct. Species with lower flight capabilities are worse at using their potential habitat range than species with good fight capabilities.

Figure 3. A map of the realized and fundamental niche area of Carabus chamissonis after all QGIS steps.

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Species Data points

Realized niche area (km2)

Fundamental niche area (km2) Difference

Proportional difference (arcsin)

Cicindela formosa 62 664195 1880915 1216720 53.54

Cicindela hirticollis 62 876397 1914265 1037868 47.42

Cicindela limbalis 43 549719 2717214 2167495 63.27

Cicindela longilabris 41 589651 2241531 1651880 59.14

Cicindela oregona 78 956365 1415283 458918 34.71

Cicindela purpurea 53 844475 1464253 619778 40.59

Cicindela repanda 170 1093278 1916588 823310 40.95

Cicindela scutellaris 63 1017693 3333723 2316030 56.46

Cicindela sexguttata 260 1696390 1913007 216617 19.66

Cicindela tranquebarica 99 1777707 3341204 1563497 43.16

Carabus chamissonis 45 452777 2985853 2533076 67.08

Carabus granulatus 11 126462 2032449 1905987 75.56

Carabus maender 28 355631 2304385 1948754 66.87

Carabus nemoralis 41 554612 1572411 1017799 53.57

Carabus rossii 7 204464 1334504 1130040 66.96

Carabus sylvosus 5 151497 3585108 3433611 78.14

Carabus taedatus 137 1362728 1951764 589036 33.32

Carabus truncaticollis 12 180154 1464045 1283891 69.46

Carabus vietinghoffi 19 116203 534035 417832 62.19

Carabus vinctus 7 218432 1854460 1636028 69.93

Mean Cicindela 93 1006587 2213798,3 1207211,3 45.89

Mean Carabus 31 372296 1961901.4 1589605.4 64.31

Values Sig. (2-tailed) value Significant Real 0,310 No

Arcsin proportional 0,005 Yes

Table1. Showing data points, realized and fundamental niche area, difference and arcsin transformed proportional difference for all the species of the two genera.

Table 2. Results from the statistical t-test showing significance for the proportional values but not from the real.

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The evidence for this is not clear though. The results from the statistical t-test could both be interpreted as significant or not. One can both argue for using the actual or transformed values from the statistical test. Some of the species, especially from the Carabus genus had very few data points, thus giving a large difference between realized and fundamental niche area. The numbers would differ greatly between species resulting in outliers interfering with the test. This is somewhat fixed by using a percentage ratio instead reducing the intensity of outliers. The aim of this study was to see if there was any difference in fundamental niche usage between the two genera so the actual value difference is not as important in this case. The real interest is in the proportional difference of fundamental niche usage. The real value difference could be of some interest but should not represent this study’s main result. Even so, by having more species of each genus could perhaps make the statistical test stronger showing significance from the actual values as well. As stated earlier Carabus was the limiting genus only having around 10 species with available data points at GBIF. Carabus also had a lower average number of data points per species. This could lead to a difference in model accuracy between the two genera as seen in this case, where Carabus had a larger average external omission error than Cicindela when performing the cross validation.

The limited number of species was not the only thing that could interfere with the results. The Ecological niche modelling available at the Biovel portal has a limited number of environmental layers to choose from when creating the model but there might be other aspects that determine a species habitat range. None-biological factors such as human agriculture or infrastructure could limit a species range but are not considered in

the models. Competition and predation from other species are also not taken into account in the modelling. Studies have shown that habitat preference for species of Carabidae are among other things influenced by number of competitors in the area (Lövei et al, 1996). To increase the accuracy of the models one could map out where the competitors have their habitat range and use that as a factor in the models. Wind current and strength could also perhaps in some way effect flying individuals disperse patterns. The reason for not projecting the models on the entire North American continent and only project on areas known to have been sampled from was to try and increase the accuracy of the models. If the unsampled areas would have been included the results could have been biased since one cannot know if the unsampled areas do contain the species of interest or not thus projecting suitable area where it might actually reside. The calculations of the fundamental and realized niche areas were also quite rough and could possibly be done with more accuracy. Time and resources was a limiting factor for this study so the calculations of the areas were not as precise as hoped for. The buffer zones around the occurrence points are a rough estimate of the beetle’s habitat as the area they live in around that point could very well be more than 150 km wide. Also points located close to the shoreline or near the edge of large water masses could possibly include large areas of water where the ground beetles do not reside. For further development of this study all of these sources of error have to be thought about and one would have to try to eliminate them. Studies on migration and species dispersal could be key factors to help in the understanding of evolution and speciation. One way of many for new species to arise is through migration of curtain members of a population that

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later isolate themselves from the rest (Sadava et al, 2011). One way of migration is of course to fly to reach new suitable areas. To study the impact of flight on migration and other aspects could lead to better understanding of speciation. The research on why and when species evolve wings is another interesting field of study that with the help of migration studies could increase our understanding of winged animals. Flight capability seems to have a positive effect on speciation as insects are the largest group of animals today with almost one million described species and an estimate number of 2.5 to 10 million species to exist (Grimaldi et al, 2005). Another great example of species richness in flying animals are of course the birds with around ten thousand species alive today (Clements, 2007). Bats are another group of animals capable of flight and they as well show a great species richness with around a thousand species being the second biggest mammal group after the rodents (Tudge, 2000). The connection between flight capabilities and species richness is an interesting subject and increasing our understanding of migration of flying species will definitely help in the research of such connections. An interesting continuation of this study would be to test more species for the two groups or to use different genera. Carabus mostly have reduced wings (Lindroth, 1986) and most of the Cicindela species have good flight capabilities (Carter, 1989), so it would be interesting to see the results from a genus that is something in between Carabus and Cicindela that has intermediate flight capabilities. One step further would be to look at different types of insects and see if they also differ in niche usage depending on flight capabilities. Different types of moths, butterflies, bees and wasps certainly differ in their speed and efficiency when

flying. This could also be applied on other flying animals such as birds and bats. Conclusion There is indication of difference in fundamental niche usage between the two genera Carabus and Cicindela. The genus Carabus containing species with reduced wings seems to have a harder time reaching new suitable habitats. Cicindela is using its fundamental niche to a fuller extent than Carabus. The statistical test shows a significant difference depending on which values are tested. The actual value difference between realized and fundamental niche area shows no significance but when looking at the proportional difference there is a significant difference. To increase the power of the statistical test, more species could help in making the difference significant even for the actual value difference. Further development of the Ecological niche models could also make the experiment more accurate. This indication of flight importance for habitat occupancy will hopefully inspire more people to investigate in this subject and together we might increase our understanding of winged individuals.

Acknowledgements Matthias Obst Researcher and project leader Department of Biological and Environmental Sciences, Systematics and Biodiversity Göteborg University Helping with ENM. Sarah Bourlat Researcher Department of Biological and Environmental Sciences Systematics and Biodiversity Göteborg University Helping with ENM. Peter Tiselius Professor in marine zooplankton ecology Department of Biological and Environmental Sciences,

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Systematics and Biodiversity Göteborg University Helping with statistics. Donald Blomqvist Researcher Department of Biological and Environmental Sciences Systematics and Biodiversity Göteborg University Helping with statistics. Urban Olsson Associate professor Department of Biological and Environmental Sciences Systematics and Biodiversity Göteborg University Supervisor during the project.

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Schultz, T. D. 1989. Habitat Preferences and Seasonal Abundances of Eight Sympatric Species of Tiger Beetle, Genus Cicindela (Coleoptera: Cicindelidae), in Bastrop State Park, Texas. The Southwestern Naturalist Vol. 34: 468-477. Tudge, Colin. 2000. The variety of Life Vol. 2 Oxford University Press.