Insect Conservation and Diversity (2016) doi: 10.1111/icad.12199
Computer-aided photographic identification of Rosalia alpina (Coleoptera: Cerambycidae) applied to a mark-recapture study
SARAH ROSSI DE GASPERIS,1 GIUSEPPE M. CARPANETO,1 GIULIO NIGRO,2 GLORIA ANTONINI,3 STEFANO CHIARI,1,4 ALESSANDRO CINI,4,5,* EMILIANO MANCINI,1 FRANCO MASON,6 FABIO MOSCONI,3,4 LARA REDOLFI DE ZAN,4,5 PIO FEDERICO ROVERSI,4 GIUSEPPINO SABBATINI PEVERIERI,4 EMANUELA SOLANO3,4 and ALESSANDRO 4,5 CAMPANARO 1Dipartimento di Scienze, Universita Roma Tre, Roma, Italy, 2Facolta di Scienze Matematiche, Fisiche e Naturali, Universita di Pisa, Pisa, Italy, 3Dipartimento di Biologia e Biotecnologie Charles Darwin, Universita La Sapienza, Roma, Italy, 4Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Centro di ricerca per l’agrobiologia e la pedologia (CREA-ABP), Cascine del Riccio, Firenze, Italy, 5Corpo Forestale dello Stato, Centro Nazionale per lo Studio e la Conservazione della Biodiversita Forestale “Bosco Fontana” di Verona, Marmirolo, Mantova, Italy, 6Corpo Forestale dello Stato, Centro Nazionale Biodiversita Forestale, Laboratorio Nazionale Tassonomia Invertebrati “Lanabit”, Verona, Italy and * Current address: Dipartimento di Biologia, Universita di Firenze, Via Madonna del Piano 6, 50019, Sesto Fiorentino, Firenze, Italy
Abstract. 1. Assessing the conservation status of protected species needs quantita- tive population data, generally obtained using Capture-Mark-Recapture methods (CMR). The exploitation of natural marking (e.g. individual morphological traits) offers an interesting alternative, based on image analyses, which may result in a less manipulation of protected species compared to the typical artificial marking method. 2. In our 2-year CMR study, we tested for the first time in the natural setting the feasibility and the application of the computer-aided photographic identifi- cation method of Rosalia alpina using the individual elytral spots as the natural marking. The I3SC software was used for the photographic analysis. 3. Data were collected from populations of two National Parks of central Italy during July–August in 2014 and 2015. We developed a standard procedure in order to optimise the image acquisition in the field and to acquire clear and comparable images, facilitating the I3SC screening process. 4. The results demonstrated that the computer-aided photographic identifica- tion of natural markings can be implemented in a CMR population study of R. alpina. Our image processing approach showed that using only the elytral central spot contours made the tracing contour process less time-consuming obtaining reliable results. Furthermore, I3SC output scores were used to identify a threshold value for the identification of new individuals or recaptures, facili- tating the final identification proposed by operators. 5. Finally, we assessed the possibility of performing the methodology using a Citizen Science approach. Key words. Elytral spots, I3SC software, natural marking, protected species, saproxylic insects.
Correspondence: Sarah Rossi de Gasperis, Dipartimento di Scienze, Universita Roma Tre, Roma, Italy. E-mail: sarahrodega@ gmail.com
Ó 2016 The Royal Entomological Society 1 2 Sarah Rossi de Gasperis et al.
Introduction could prove time-consuming. In such a case, the matching of photographs aided by a specific software was a success- Proper implementation of conservation measures for pro- ful solution (Kelly, 2001; Speed et al., 2007; Hiby et al., tected species requires reliable quantitative population 2009; Sacchi et al., 2010; Caci et al., 2013). In particular, studies on survival ability, demography and population computer-aided photographic identification using the dynamics, in order to assess their conservation status Interactive Individual Identification System version “Con- (Shrader-Frechette & McCoy, 1993; Schwarz & Seber, tour” 3.0 software (I3SC) (see Van Tienhoven et al., 2007) 2001; Butchart et al., 2004). was successfully applied to R. alpina images by Caci et al. Rosalia alpina (Linnaeus, 1758) is a saproxylic longhorn (2013). The authors analysed a sample of 75% of museum beetle typically inhabiting beech forests. Although the spe- specimens and 25% of living individuals and suggested cies occurs in a vast territory across the Central and the employment of I3SC for a less invasive approach in a Southern Europe reaching the Anatolian peninsula, cur- monitoring programme. To date, however, we lack data rently its distribution area is highly fragmented (Sama, on the reliability of computer-aided photographic identifi- 2002; Binner & Bussler, 2006; Cizek et al., 2009; Jurc cation, using natural markings under field settings and et al., 2008; Bosso et al., 2013; Lachat et al., 2013). At applied to large datasets of many (e.g. hundreds) individu- local scale, forest management can seriously affect the als for populations of the same locality, where genetic population viability of the species; the removal of huge resemblance and shared environment might limit pheno- dead trees and a longer distance between suitable trees, in typic variation. fact, can reduce the habitat availability and the dispersal The present study was performed within the framework of the species affecting the population success (Russo of the Project LIFE11 NAT/IT/000252 MIPP “Monitor- et al., 2011, 2015). Thus, the beetle is ranked as a priority ing of Insects with Public Participation” (Mason et al., species in the Annexes II and IV of the European Habi- 2015), which aims at testing different standard monitor- tats Directive 92/43EEC (HD) and population status ing protocols for saproxylic beetles listed in HD. The assessment is required. R. alpina is also a flagship species, project also benefits from the collaboration of citizens having a charismatic attractive power for people due to that can give their support for a more detailed descrip- its distinctive elytral pattern (Duelli & Wermelinger, tion of the geographical range of the target species 2005). (Zapponi et al., 2016) by sending images and geographic Population studies are generally carried out by capture- position of the individuals. The possibility of using these mark-recapture method (CMR), an approach that poten- images for monitoring purposes has never been assessed tially stresses or injures the specimens of both, vertebrates for R. alpina. and invertebrates (Day et al., 1980; Kock et al., 1987; The present study is a methodological assay, with the Nietfeld et al., 1994; Lemckert, 1996; Davies & Ovaska, following main goals: (i) to set up a standard methodol- 2001; Hagler & Jackson, 2001; Arnemo et al., 2006; Mat- ogy in a CMR protocol that allows the application of son et al., 2006; Spotswood et al., 2012). The use of the computer-aided photo-identification of R. alpina; (ii) to typical CMR marking tools, that is pen, stickers or small explore time-saving approaches for image processing by drill, does not produce serious injuries to the large pro- considering only a selected part of the elytral pattern; (iii) tected saproxylic beetles as Cerambyx cerdo (Linnaeus, to find threshold values of the output scores given by the 1758), Elater ferrugineus (Linnaeus, 1758), Lucanus cervus software in order to assist the operator during the screen- (Linnaeus, 1758), Morimus funereus (Mulsant, 1863) and ing process and the final identification; (iv) to test the Osmoderma eremita (Scopoli, 1763) (Ranius, 2001; Cam- developed methodology with images provided by non- panaro et al., 2011; Chiari et al., 2013, 2014; Zauli et al., experts (citizen science approach) and evaluate whether 2014). The more slender R. alpina has a smaller body size citizen data can be implemented in a standard monitoring and softer elytras and for these reasons, the possibility to programme. injure sampled specimens during the handling could be definitely much higher. The use of photo-identification for individuals of R. alpina has been recently suggested as a Material and methods valid alternative to the classic marking techniques (see Campanaro et al., 2011; Pagola Carte, 2011; Trizzino Study area et al., 2013) and the coloured elytral pattern was used as an individual natural marking for photographic identifica- The study was conducted in five study sites within two tion (Pagola Carte, 2011; Caci et al., 2013; Castro & National Parks of Central Italy: (i) Parco Nazionale Fernandez, 2016). Other similar examples of photo-identi- Foreste Casentinesi, Monte Falterona and Campigna fication occur in mammals, reptiles and amphibians (Wil- (PNFC), in the Northern Apennines (two study sites); (ii) son et al., 1999; Bradfield, 2004; Gamble et al., 2008; Parco Nazionale Abruzzo, Lazio and Molise (PNALM) Schofield et al., 2008; Hoque et al., 2011; Lahiri et al., in the Central Apennines (three study sites) (Fig. 1). The 2011; Knox et al., 2012; Rydell & Russo, 2015). The pho- exact geographic position of the five study sites are not tographic approach showed some limitations, since it reported to limit the possibility of illegal collection of requires the processing of even hundreds of images that R. alpina specimens.
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity Photo-identification of Rosalia alpina 3
Fig. 1. The two National Parks of central Italy selected for the survey of Rosalia alpina.
Fieldwork and data collection insect net and released after the marking procedure, which involved two types of marking: Within monitoring programmes of a highly protected species, the following protocol proposed, based on collect- 1 Artificial marking, by writing a progressive number of ing data on adult beetles in the wild, is limited to experi- capture on the elytra with a non-toxic black perma- enced entomologists that must be authorised to nent colour (Stabilo S OHPen universal) (cf. Drag manipulate specimens by the relevant authorities in all et al., 2011) (Fig. 2a). The number was reported on countries, where R alpina is legally protected. both elytra to reduce at minimum the possibility of Trees potentially suitable for hosting R. alpina (large loss of data (e.g. in cases of ink abrasion or by recog- decaying trees exposed to sun with bark partially or nising dead individuals with single elytron remain). totally absent) (Duelli & Wermelinger, 2005; Russo et al., 2 Natural marking, using the elytral spots as the individ- 2011, 2015) were selected through a preliminary field ual code, which was collected by photographing the inspection, for a total of 136 trees mainly belonging to the dorsal surface of the adults for the photo-identification species F. sylvatica. The trees were visually inspected of individuals (Fig. 2b). During image acquisition, searching for R. alpina adults between the middle of July Caci et al. (2013) suggested that the angle under which and the end of August, that is during the adult flight per- images must be taken should not exceed 30°. Prelimi- iod. Seven surveys were performed in 2014 and fourteen nary trials of photo-acquisition of specimens directly in 2015. on the substrate in the wild, led in some cases to the Data were collected by following the capture-mark- acquisition of not usable pictures due to sharpness and recapture method (CMR) (Amstrup et al., 2005), that is wrong framing angle. Therefore, we standardised pic- adults were gently captured directly by hand or with an ture acquisition in the wild by placing each individual
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity 4 Sarah Rossi de Gasperis et al.
(a) (b)
Fig. 2. A male of Rosalia alpina with the artificial marking (a) and its image of the elytral pattern obtained by photographing the individ- ual within the high density polyethylene sample bottle (b). Pictures made by Lara Redolfi De Zan.
of R. alpina on the bottom of a 1000 ml High Density to save the fingerprint and to proceed with the analysis. Polyethylene (HDPE) wide mouth square sample bot- The screening process is carried out by matching the con- tle. Pictures were taken by putting the camera lens tour of the unknown individual image under examination (CanonÒ PowerShot D20, Canon Inc., Tokyo, Japan) with the contours of all the images included in the refer- directly on the mouth of the bottle, so that the fram- ence library (i.e. all photo records included in the data- ing angle was maintained as perpendicular as possible base). The match output gives a ranked photo list where to the specimen. Individuals inside the bottle usually each rank shows a score value of similarity between the remained quiet, so that image acquisition was rela- two contours matched. The perfect match between two tively easy and fast; pictures were taken on each adult fingerprints will correspond to a zero score in the first when it was completely still and placed approximately rank position. At the final step of the procedure, to mini- in the centre of the bottle. Four pictures were collected mize errors attributable to the system (identification based for each individual to enable us to choose the best only on score values), the decision of final identification is during image analysis. left to the operator (den Hartog & Reijns, 2011). In 2014, at first capture, adults were sexed and marked Photographic analysis. Dataset of 2014, containing using the two marking methods described above. During artificial marking data and photo-records data, was used to the surveys when a previously marked beetle was inter- validate the photographic identification method performed cepted (i.e. recaptured), the number of the individual was by I3SC, that is evaluating whether the software made annotated and its elytral pattern was photographed for a errors in the identification of recaptured individuals. Only second time. The same procedure was performed for one of the four pictures of each individual was used to build marked remains of dead individuals. up the database for analysis. At least two images in the In 2015, taking into account the results obtained in 2014 dataset are available for recaptured individuals: the image (see results), only the photographic procedure was used; each of mark event and the image of the recapture event (or adult was sexed and photographed at every capture. Remains more if the individual was recaptured more than once). of dead individuals, collected at the base of inspected trees, The validation procedure was performed in the three were also photographed with the same method. following steps: Finally, we selected from the Life MIPP data base all the images taken by citizens in the five study sites during 1 We traced the elytral spot contours for each image the sampling period of 2014 and 2015, in order to explore and all the images were included in the reference the possibility of using them in our analyses. library; 2 The screening process was performed by matching one by one each image against the reference library, there- fore at least two matches were obtained for recaptured Data analysis individuals; 3 We compared I3SC results with the artificial marking The I3SC software. Photographic analysis was con- of the specimens and we considered a correct identifi- ducted using the Interactive Individual Identification cation of the recaptured individual when the correct System version ‘Contour’ 3.0 (I3SC) (Van Tienhoven image is ranked in one of the three top positions (Caci et al., 2007), available on http://www.reijns.com/i3s/in- et al., 2013) in the two matches. Otherwise, we dex.html; the same software previously used by Caci et al. recorded a case of discrepancy (i.e. one error occurs (2013). This software uses a semiautomatic tracing algo- for one of the two matches) and erroneous identifica- rithm, which can detect and trace the optimal contour tion (i.e. errors occur in both matches). (i.e. fingerprint) by joining the points, manually selected by the operator, on the elytral black spots of R. alpina. In order to find out a less time-consuming contour trac- The operator must trace the spot contour of both elytra ing method, the validation procedure was separately
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity Photo-identification of Rosalia alpina 5 performed using contours of different spots area of the in order to see if images were good enough to be pro- elytra: the total elytral spot contours (TSC) and a contour cessed by I3SC software, thus giving new information for each pair of elytral spots: anterior spot contours about the studied populations. (ASC), central spot contours (CSC), and posterior spot All statistical analyses were performed using Past 3 contours (PSC) (Fig. 3). (Hammer et al., 2001); the alpha set for all the analyses One-way ANOVA test was performed to compare the dis- was 0.05. crimination power, that is Delta score, of the best two tracing methods. The Delta score is defined as the differ- ence between the score of the correct recapture identifica- Results tion ranked in the first place (or at most 2nd and 3rd) and the subsequent ranked score identified as a different The 2014 dataset included photo records of 148 images individual. gathered from the study areas corresponding to: 133 The time spent in the contour-tracing operation, per- marked individuals (n = 13 from PNFC and n = 120 from formed by a trained operator, was recorded by an ana- PNALM) and 15 recaptured individuals (all from logic chronometer for the two best contours, for a PNALM), of which 12 living individuals and three dead random sample of images (n = 20) in order to compare individuals (remains). the two best methods (Kruskal–Wallis test). Table 1 shows the results of the validation procedure The best contour method was used for the photo- obtained by comparing the artificial marking with the graphic analysis of the 2015 dataset. We included in the identification results of I3SC analysis of recaptured indi- reference library only the images of individuals pho- vidual images. Among the four types of contours used for tographed during the first survey (i.e. all new individuals) this analysis, TSC and CSC identified correctly all the 12 in 2015 among the study sites. Then we proceeded with images of recaptured living individuals, and both types of the screening process by matching the images collected contours ranked the correct image at the first place of the during the subsequent surveys with the reference library output list. In both methods, the same erroneous identifi- and then progressively including them in the library as cations occurred for the three images of marked remains new individuals or recaptured individuals. of dead individuals. The one-way ANOVA test was used to compare, in each The mean and standard deviation of Delta score year and between years, the first-ranked score obtained for recaptured identification turned out to be: for the identification of new individuals and recaptures, 2315.8 Æ 1948.4 for CSC and 3791.13 Æ 2551.8 for TSC. and to compare Delta score of recaptures identifications Both methods discriminated in the same way (F = 3.16, between years. We drew up a graph of match frequencies d.f. = 1, P = 0.09). and Delta scores in order to identify a possible threshold The total time spent for tracing the spot contours of 20 value of scores facilitating the operator in the final identi- images was 24.13 min for TSC and 15.27 min for CSC. fication of new individuals and recaptures. The mean and standard deviation of the time used for the Finally, we analysed the data collected from citizens contour-tracing procedure on a single image was using the best contour method and by matching them 48.7 Æ 6.3 s for TSC and 24.5 Æ 2.9 s for CSC. Compar- with the reference library, respectively, for 2014 and 2015 ing the two methods, CSC turned out to be the less time-
Fig. 3. Comparison of the four spot contours traced with I3SC software on the same image of Rosalia alpina. From left to right: total spot contours, anterior spot contours, central spot contours and posterior spot contours. Pictures made by Sarah Rossi de Gasperis.
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity 6 Sarah Rossi de Gasperis et al.
Table 1. Results of the recaptured individuals, obtained from marking. In 2015, five images were collected from the validation procedure of I3SC using the four different elytral PNALM and five images from PNFC. The quality of spot contours. seven pictures was not good enough to process the images with I3SC software. Spot Correct The software identified correctly one image of 2014 contours identification Erroneous Discrepancy from PNALM, ranked at third place with a high score of type rate identification rate rate 14537; it did not show the marking number because the TSC 12/15 3/15 0/15 image was taken before our marking procedure. Five CSC 12/15 3/15 0/15 images of 2015 from PNFC were processed and no match ASC 4/15 3/15 8/15 was found with the reference library of 2015, therefore PSC 1/15 12/15 2/15 they were considered all new individuals (mean of first score 11448 Æ 2014). All the results were visually con- TSC, Total spot contours; ASC, anterior spot contours; CSC, firmed. central spot contours; PSC, posterior spot contours. consuming contour tracing method (H = 29.27, Discussion P < 0.001). The 2015 dataset included 222 images, of which 35 were Our study demonstrated that the computer-aided photo- photo records from PNFC (34 individual and 1 remains graphic identification method using images of natural of a dead individual) and 187 were photo records from marking can be reliably applied in a CMR study of PNALM (180 individuals and 7 remains of dead individu- R. alpina. The temporary capture of individuals was nec- als). The reference library only included 33 individuals, essary in the present study for some practical constrains: those photographed in the first survey among the study (i) it is not possible to take good pictures of specimens sites (n = 15 from PNFC and n = 18 from PNALM). that are located in high position on trees; (ii) on natural The I3SC identification procedure by using the CSC, substrates, the specimens rarely assume the right position that is the less time-consuming contour tracing method, that allows to get pictures suitable for the software used gave the following results for new individuals (NI) and in our analysis; (iii) waiting for specimens to show correct recaptures (R): 31 NI and 3 R in PNFC, 135 NI and 45 positioning for the picture would cause a waste of time R in PNALM. Of the 48 R, 91.7% (n = 44) was ranked interfering with the sampling. R. alpina is a very active at first score, 6.2% (n = 3) was ranked at second score, species: the individuals can move fast and rarely stand still and 2.1% (n = 1) was ranked at third score. Only one on the trunk; these features did not allow a complete non- error for a single NI, which was recognised as a recapture, invasive approach. Thus, in our sampling protocol, we was found for an image collected in PNFC. All images of considered the use of a wide mouth bottle to facilitate the the remains of dead individuals (n = 8) under examination image acquisition of the elytral pattern, minimising the were identified as NI. handling of specimens. In addition, a fundamental aspect On the total identifications, the first-ranked scores of of the developed protocol is that the photographic fram- NI showed higher values than that of R in 2015, while no ing constraints given by the use of the square bottle allow difference resulted in 2014 (Table 2). Between years, NI obtaining standardised and comparable images, giving the and R first-ranked scores of 2014 resulted higher than optimal conditions for the analysis performed with the 2015, while no difference resulted for Delta score for R I3SC software. This is a highly important aspect when identification. monitoring programmes are performed on a large-scale In 2015, the highest number of matches which identified and when the personnel involved is made of people with a NI were recorded within the range 7000–10 000 of first different experience level. The I3SC performance resulted ranked scores, highlighting 8000 as a good threshold to in 100% of living recaptured individuals being correctly identify a new specimen from that value onward (Fig. 4). identified if we consider the three top positions in the out- Match frequencies of R resulted in a partial overlap with put list, and 91.7% if we consider only the first-ranked that of NI, therefore it is difficult to identify a clear position. Caci et al. (2013) obtained similar results using a threshold for the identification of recaptured individuals dataset mostly made up of images of museum specimens: using only the first score value. Of the 48 recaptures, 32 94.8% when we considered the three top positions, and showed a Delta score >1000; this Delta score value was 92.1% if we considered only the top position. The identifi- used as good threshold to be confidence in R identifica- cation procedure proved to be limited when the I3SC tion in 2015. The remaining 16 recaptures of 2015 with examined images of dead individual’ remains, probably delta score <1000, which indicate uncertainty, were because these assumed a different shape due to the degra- recorded mostly for R with first-ranked scores ranging dation process. between 5500 and 7500 (Fig. 4). The approach tested in this study, by comparing the Citizen Science dataset consisted in 13 images of differ- contours of different elytral spots, suggests that using ent living individuals. In 2014, three images were collected either the central spot contours or the total spot contours from PNALM and two of them showed the artificial we obtain fingerprints, which provide the same level of
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity Photo-identification of Rosalia alpina 7
Table 2. Comparisons of mean and SD of first-ranked score for individuals identified as new (NI) and individuals identified as recaptured (R), and Delta score between first- and second-ranked scores of recaptured identifications, for dataset of 2014 and 2015.
NI R Delta score Year Mean Æ SD Mean Æ SD Mean Æ SD
2014 11 734.1 Æ 4058.9 10 583.5 Æ 2131.33 2315.8 Æ 1948.4 2015 8687.8 Æ 2327.4 6048.8 Æ 1495.9 1832.4 Æ 1240.3 One-way ANOVA test results NI 2014 versus R 2014 F = 1.60 d.f. = 1 P = 0.21 NI 2015 versus R 2015 F = 38.37 d.f. = 1 P < 0.001* NI 2014 versus NI 2015 F = 42.1 d.f. = 1 P < 0.001* R. 2014 versus R 2015 F = 101 d.f. = 1 P < 0.001* Delta score 2014 versus Delta score 2015 F = 1.29 d.f. = 1 P = 0.26
Fig. 4. The number of matches for new individuals (NI) and recaptures (R) in relation to their first ranked score value given in I3SC for the dataset of 2015 are reported. Uncertainty in R identification is represented by Delta score <1000. The scores of NI over 19 000 (range: 20 000–29 000, only 1 match) were excluded from the graph for better visualizing the frequencies. correct identification among individuals. Indeed, the vari- (i.e. Delta score). Even if the operator always makes the ation that allows a correct discrimination is mainly con- final decision, the screening process is facilitated by I3SC centrated in the central elytral spot contours. Sub-setting software; otherwise, it would be time-consuming and hard an area of the natural marking is a technique used in to perform manually (Kelly, 2001; Speed et al., 2007; other studies, in particular when the analysis is performed Sacchi et al., 2010). Although the photo-identification by following the ROI approach, that is by selecting the method used in our study does not avoid the need to cap- region of interest of the image (Hoque et al., 2011; Lahiri ture specimens, the procedure that we carried out was et al., 2011). Both spot contours, central and total, have probably quicker than other marking methods, facilitating returned the same identification results. Moreover, only the sampling procedures even for unexpert surveyors. the central spot contours made the tracing contour pro- The Citizen Science’s support for our CMR study was cess less time-consuming, reducing the image elaboration limited because the number of images collected from the to half the time. In a few cases, the central spot contours study areas was low and half of them have not an ade- of two different specimens proved very similar, in such quate quality to be processed. The lower quality of pic- cases the operator has to focus his attention on the ante- tures was usually due to blurred images, inadequate light rior or posterior spots in the final recognition. When indi- or framing angle, as normally occurs without an opti- viduals exhibited one elytron damaged or covered by the mised photographic protocol, especially when beetles are hind flight wing (only two specimens in our dataset), it not manipulated as expected for a Citizen Science was possible to perform the match using the spot contour approach. This result proved the need to provide better of only one elytron (Caci et al., 2013). During the identifi- indications to citizens on how to take pictures of speci- cation process, it was also possible to find a threshold of mens. Recently, Zapponi et al. (2016) demonstrated how certainty to identify new individuals or recaptures by the citizens’ contribute can be a fast, reliable and informa- looking at the first score value (or at least the second or tive tool to map the distribution range of protected third score) in combination with the discriminant value saproxylic beetles in Italy. The cited authors showed that
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity 8 Sarah Rossi de Gasperis et al. the new records provided by citizens in the last 2 years authors thank all the MIPP staff and the Institutions have considerably modified the knowledge of the distribu- involved: Corpo Forestale dello Stato, Consiglio per la tion range of the species recorded in the national inven- Ricerca in Agricoltura e l’Analisi dell’Economia Agraria – tory of the last 10 years. In the present work, the Citizen Centro di Ricerca per l’Agrobiologia e la Pedologia, Science approach alone was not able to substitute the Universita degli studi di Roma La Sapienza, Universita classical CMR protocol that needs a considerable amount degli studi di Roma Tre, Ministero dell’Ambiente e della of data and must be carried out by experts under specific Tutela del Territorio e del Mare, Regione Lombardia. programmes. Moreover, the authorisation for handling Moreover, the authors are grateful to the local offices of the protected species is required by the relevant authori- the Corpo Forestale dello Stato that administrate the ties. Further efforts are needed to understand with greater study sites, that is the UTB Castel di Sangro (Tiziana confidence if it is worth, or not, to invest efforts on Altea, Federica Desprini, Lucia Eusepi, Mario Romano) Citizen Science to improve datasets for population size and the UTB Pratovecchio (Giovanni Quilghini, Silvia assessments. Bertinelli, Sandro Marsella, Matteo Padula, Barbara As practical indications for the implementation of a Rossi, Antonio Zoccola), and also the staff of the Citizen Science support on monitoring programmes of Abruzzo National Park (Cinzia Sulli, Paola Tollis). Rosalia alpina, we suggest to provide at least two pictures We are also grateful to all the field assistants who vol- always without handling the beetle. The first picture untarily help during the surveys: Sara Amendolia, Marco should frame the complete individual (including antennae) Boscaro, Giulia Caruso, Anna Cuccurullo, Patrizia Gian- in order to obtain the identification of species and sex; the gregorio, Andrea Mancinelli, Marco Molfini, Alessandro second one, should be focused on the elytral pattern, Morelli, Margherita Norbiato, Giulia Albani Rocchetti, maintaining the framing angle as much as possible per- Randi Rollins, Rosaria Santoro, Ventura Talamo, Melissa pendicular to the elytra and taking special care on Yslas, Ilaria Zappitelli and Cooperativa In Quiete. light exposure. Finally, we thank Martin Bennett for editing the English The methodology described in this study might be suit- text. able for other species that exhibit a spotted elytral pattern as that of many longhorn beetles; among them, there is also the protected species M. funereus that seems to show References an individual elytral pattern (Polak, 2012). In order to facilitate the identification procedure with I3SC software, Amstrup, S.C., McDonald, T.L. & Manly, B.F.J. (2005) Hand- images must be obtained following some guidelines for book of Capture-Recapture Analysis. Princeton University Press, both expert entomologists and people involved in Citizen Princeton, New Jersey. Science projects, always taking into account the role of Arnemo, J.M., Ahlqvist, P., Andersen, R., Berntsen, F., Ericsson, G., Odden, J., Brunberg, S., Segerstro¨m, P. & Swenson, J.E. relevant authorities concerning any approach with the (2006) Risk of capture related mortality in large free-ranging protected species. mammals: experiences from Scandinavia. Wildlife Biology, 12, Standardised monitoring techniques are urgently needed 109–113. for conservation of saproxylic fauna in EU Habitat Direc- Binner, V. & Bussler, H. (2006) Erfassung und Bewertung Von tive and the presented procedure for R. alpina represents Alpenbock-Vorkommen. Naturschuz und Landscaftsplanung, 38, an unprecedented and valuable implementation of the 378–382. photographic approach to acquire data on the species Bosso, L., Rebelo, H., Garonna, A.P. & Russo, D. (2013) Model- conservation status over its distribution range. Moreover, ling geographic distribution and detecting conservation gaps in the use of the proposed standardised photographic Italy for the threatened beetle Rosalia alpina. Journal for Nat- 21 – approach allows the studying of morphological variability ure Conservation, ,72 80. Bradfield, K.S. (2004) Photographic Identification of Individual among populations and can be used in further studies Archey’s Frog Leiopelma archeyi, From Natural Markings. thereby focusing on testing if the phenotypic characteris- Department of Conservation, Wellington, New Zealand. tics reflect the genetic variability of the species. This will Butchart, S.H.M., Stattersfield, A.J., Bennun, L.A., Shutes, allow drawing up more efficient conservation strategies S.M., Akcakaya, H.R., Baillie, J.E.M., Stuart, S.N., Hilton- and evaluating the long-term efficacy of such efforts for Taylor, C. & Mace, G.M. (2004) Measuring global trends in maintaining viable populations of R. alpina in Europe. the status of biodiversity: red list indices for birds. PLoS Biology, 2, e383. Caci, G., Biscaccianti, A.B., Cistrone, L., Bosso, L., Garonna, A.P. Acknowledgements & Russo, D. (2013) Spotting the right spot: computer-aided indi- vidual identification of the threatened cerambycid beetle Rosalia alpina. Journal of Insect Conservation, 17, 787–795. Authors are grateful to Danilo Russo and the two anony- Campanaro, A., Bardiani, M., Spada, L., Carnevali, L., Mon- mous reviewers for their valuable comments on the talto, F., Antonini, G., Mason, F. & Audisio, P. (2011) Linee manuscript. guida per il monitoraggio e la conservazione dell’entomofauna The present work was developed within the EU project saproxylica/Guidelines for monitoring and conservation of LIFE11 NAT/IT/000252, with the contribution of the saproxylic insects. Quaderni Conservazione Habitat, 6. Cierre LIFE financial instrument of the European Union. The Grafica, Verona, Italy.
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity Photo-identification of Rosalia alpina 9
Castro, A. & Fernandez, J. (2016) Tree selection by the endan- pattern differentiation. New Zealand Journal of Ecology, 37, gered beetle Rosalia alpina in a lapsed pollard beech forest. 60–66. Journal of Insect Conservation, 20, 201–214. Kock, M.D., Jessup, D.A., Clark, R.K., Franti, C.E. & Weaver, Chiari, S., Zauli, A., Audisio, P., Campanaro, A., Donzelli, P.F., R.A. (1987) Capture methods in five subspecies of free-ranging Romiti, F., Svensson, G.P., Tini, M. & Carpaneto, G.M. bighorn sheep: an evaluation of drop-net, drive-net, chemical (2014) Monitoring presence, abundance and survival probabil- immobilization and the net-gun. Journal of Wildlife Diseases, ity of the stag beetle, Lucanus cervus, using visual and odour- 23, 634–640. based capture methods: implications for conservation. Journal Lachat, T., Ecker, K., Duelli, P. & Wermelinger, B. (2013) Popu- of Insect Conservation, 18,99–109. lation trends of Rosalia alpina (L.) in Switzerland: a lasting Chiari, S., Zauli, A., Mazziotta, A., Luiselli, L., Audisio, P. & turnaround? Journal of Insect Conservation, 17, 653–662. Carpaneto, G.M. (2013) Surveying an endangered saproxylic Lahiri, M., Tantipathananandh, C., Warungu, R., Rubenstein, beetle, Osmoderma eremita, in Mediterranean woodlands: a D.I. & Berger-Wolf, T.Y. (2011) Biometric animal databases comparison between different capture methods. Journal of from field photographs: identification of individual Zebra in Insect Conservation, 17, 171–181. the wild. Proceedings of the 1st ACM International Conference Cizek, L., Schlaghamersky, J., Bo rucky, J., Hauck, D. & Hele sic, J. on Multimedia Retrieval, New York City, New York. ISBN: (2009) Range expansion of an endangered beetle: Alpine Long- 978-1-4503-0336-1, doi:10.1145/1991996.1992002. horn Rosalia alpina (Coleoptera: Cerambycidae) spreads to the Lemckert, F. (1996) Effects of toe-clipping on the survival and lowlands of Central Europe. Entomologica Fennica, 20, 200–206. behaviour of the Australian frog Crinia signifera. Amphibia- Davies, T.M. & Ovaska, K. (2001) Individual recognition of Reptilia, 17, 287–290. amphibians: effects of toe clipping and fluorescent tagging on Mason, F., Roversi, P.F., Audisio, P., Bologna, M.A., Carpa- the salamander Plethodon vehiculum. Journal of Herpetology, neto, G.M., Antonini, G., Mancini, E., Sabbatini Peverieri, G., 35, 217–225. Mosconi, F., Solano, E., Maurizi, E., Maura, M., Chiari, S., Day, G., Schemnitz, S. & Taber, R. (1980) Capturing and Mark- Sabatelli, S., Bardiani, M., Toni, I., Redolfi De Zan, L., Rossi ing Wild Animals. Wildlife Management Techniques Manual, de Gasperis, S., Tini, M., Cini, A., Zauli, A., Nigro, G., Bot- 4th edn. (ed. by S.D. Schemnitz), pp. 61–88. The Wildlife Soci- tacci, A., Hardersen, S. & Campanaro, A. (2015) Monitoring ety, Bethesda, Maryland. of insects with public participation (MIPP; EU LIFE project Drag, L., Hauck, D., Pokluda, P., Zimmermann, K. & Cizek, L. 11 NAT/IT/000252): overview on a citizen science initiative (2011) Demography and dispersal ability of a threatened and a monitoring programme (Insecta: Coleoptera; Lepi- saproxylic beetle: a mark-recapture study of the rosalia longi- doptera; Orthoptera). Fragmenta entomologica, 47,51–52. corn (Rosalia alpina). PLoS ONE, 6, e21345. Matson, K.D., Tieleman, B.I. & Klasing, K.C. (2006) Capture Duelli, P. & Wermelinger, B. (2005) Der Alpenbock (Rosalia stress and the bactericidal competence of blood and plasma in alpina). Ein seltener Bockkafer als Flaggschiff Art. Merkblatt five species of tropical birds. Physiological and Biochemical fur€ die Praxis, 39,1–8. Zoology, 79, 556–564. Gamble, L., Ravela, S. & McGarigal, K. (2008) Multi-scale fea- Nietfeld, M.T., Barrett, M.W. & Silvy, N. (1994) Wildlife Mark- tures for identifying individuals in large biological databases: ing Techniques. Research and Management Techniques for an application of pattern recognition technology to the marbled Wildlife and Habitats (ed. by T.A. Bookhout), pp. 140–168. salamander Ambystoma opacum. Journal of Applied Ecology, The Wildlife Society, Bethesda, Maryland. 45, 170–180. Pagola Carte, S. (2011) Seguimiento de la poblacion de Rosalia Hagler, J.R. & Jackson, C.G. (2001) Methods for marking alpina en el hayedo de trasmochos de Oieleku (LIC de Aiako insects: current techniques and future prospects. Annual Review Harria) (Accion E.7 del Proyecto Life + Maneyo y Conser- of Entomology, 46, 511–543. vacion de los habitats de Osmoderma eremita, Rosalia alpina y Hammer, O., Harper, D. & Ryan, P. (2001) PAST: paleontologi- otros saproxılicos de inter es comunitario en Gipuzkoa), pp. 57. cal statistics software package for education and data analysis. Dissertation, Donostia-SanSebastian, Spain. Paleontologia Electronica, 4,1–9. Polak, S. (2012) Phenology and mating behaviour of Morimus den Hartog, J. & Reijns, R. (2011) I3S contour manual: interac- funereus (Coleoptera, Cerambycidae). Saproxylic beetles in Eur- tive individual identification system.
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity 10 Sarah Rossi de Gasperis et al.
Galeotti, P. & Fasola, M. (2010) Photographic identification in Conservazione Habitat, 7. CFS-CNBFVR, Centro Nazionale reptiles: a matter of scales. Amphibia-Reptilia, 31, 489–502. Biodiversita Forestale, Cierre Grafica, Sommacampagna, Ver- Sama, G. (2002) Atlas of the Cerambycidae of Europe and ona, Italy. Mediterranean Area: Northern, Western, Central and Eastern Van Tienhoven, A.M., den Hartog, J.E., Reijns, R.A. & Pedde- Europe. British Isles and Continental Europe from France (excl. mors, V.M. (2007) A computer-aided program for pattern- Corsica) to Scandinavia and Urals. Vit Kabourek, Kabourek, matching natural marks on the spotted ragged tooth shark Zl ın, Czech Republic. Carcharias Taurus (Rafinesque, 1810). Journal of Applied Ecol- Schofield, G., Katselidis, K.A., Dimopoulos, P. & Pantis, J.D. ogy, 44, 273–280. (2008) Investigating the viability of photoidentification as an Wilson, B., Hammond, P.S. & Thompson, P.M. (1999) Estimat- objective tool to study endangered sea turtle populations. ing size and assessing trends in a coastal bottlenose dolphin Journal of Experimental Marine Biology, 360, 103–108. population. Ecological Application, 9, 288–300. Schwarz, C.J. & Seber, G.A.F. (2001) Estimating animal abun- Zapponi, L., Cini, A., Bardiani, M., Hardersen, S., Maura, M., dance: review III. Statistical Science, 14,1–134. Maurizi, E., Redolfi De Zan, L., Audisio, P., Bologna, M.A., Shrader-Frechette, K.S. & McCoy, E.D. (1993) Method in Ecol- Carpaneto, G.M., Roversi, P.F., Sabbatini Peverieri, G., ogy: strategies for Conservation. Cambridge University Press, Mason, F. & Campanaro, A. (2016) Citizen science data as an Cambridge, UK. efficient tool for mapping protected saproxylic beetles. Biologi- Speed, C.W., Meekan, M.G. & Bradshaw, C.J.A. (2007) Spot the cal Conservation in press. Available online at http://www.scien match—wildlife photoidentification using information theory. cedirect.com/science/article/pii/S0006320716301744. Frontiers in Zoology, 4, 2. doi:10.1186/1742-9994-4-2. Zauli, A., Chiari, S., Hedenstrom,€ E., Svensson, G.P. & Carpa- Spotswood, E.N., Roesch Goodman, K., Carlisle, J., Cormier, neto, G.M. (2014) Using odour traps for population monitor- R.L., Humple, D.L., Rousseau, J., Guers, S.L. & Barton, G.G. ing and dispersal analysis of the threatened saproxylic beetles (2012) How safe is mist netting? evaluating the risk of injury and Osmoderma eremita and Elater ferrugineus in central Italy. mortality to birds. Methods in Ecology and Evolution, 3,29–38. Journal of Insect Conservation, 18, 801–813. Trizzino, M., Audisio, P., Bisi, F., Bottacci, A., Campanaro, A., Carpaneto, G.M., Chiari, S., Hardersen, S., Mason, F., Nardi, Accepted 12 September 2016 G., Preatoni, D.G., Vigna Taglianti, A., Zauli, A., Zilli, A. & Cerretti, P. (2013) Gli artropodi italiani in Direttiva Habitat: Editor: Simon R. Leather biologia, ecologia, riconoscimento e monitoraggio. Quaderni Associate editor: Jorg€ Muller€
Ó 2016 The Royal Entomological Society, Insect Conservation and Diversity