First Investigations of the Consumption of Seal Carcasses by Terrestrial And

The Glasgow Naturalist (online 2016) Volume 26, Part 3

First investigation of the consumption of seal carcasses by terrestrial and marine scavengers

M.-M. Quaggiotto¹, L.R. Burke, D.J. McCafferty¹, D.M. Bailey¹

¹Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK

ABSTRACT carrion is often an unpredictable resource, making Marine mammal carrion contains a large amount of scavenging a high risk/high reward strategy. This nutrients and energy of potential value to terrestrial risk is reduced where animals can search large and marine scavengers, but its impact on coastal areas at low cost, which can be accomplished by habitats has not been studied. This study aimed to specialised birds (Ruxton & Houston, 2004) and provide a detailed documentation of the fate of two possibly by abyssal fish (Ruxton & Bailey, 2005). grey seal (Halichoerus grypus) pup carcasses, one However, scavengers are often facultative rather placed on the shore of Little Cumbrae and one at a than obligate: many large mammalian carnivores, depth of 6 m off Great Cumbrae, Firth of Clyde, and a for instance, switch from hunting to scavenging record of the changes in the carcasses and the depending on prey availability (Pereira et al., 2014). succession of scavengers using these resources. The In some food webs scavenging links have been carcasses were monitored using time lapse and/or underestimated 16-fold, so that the energy motion-activated cameras. On the shore, great transferred through scavenging is likely to be black-backed gulls, juvenile gulls and ravens fed on greater than that transferred by predation (Wilson the carcass and there was a distinct shift in the & Wolkovich, 2011). relative proportions of the bird groups feeding over the period observed. Herring gulls spent In UK coastal systems the families Laridae (gulls) significantly less of their time at the carcass feeding and Corvidae (crows and ravens) are opportunistic than other birds, while lesser black-backed gulls scavengers. In contrast to the Tubinares (petrels), were not observed scavenging despite being which are seabirds highly dependent on carrion and common on the island. Over the six week period of using their excellent sense of smell to find it (Nevitt, observation, more than 90% of the carcass was 2000), gulls and corvids employ sight. This food- consumed. However, the deployment of the carcass finding behaviour includes visual surveillance of the did not influence the spatial and temporal coast, recognition of the food item and attraction to distribution of the scavenging birds. The the sight of other animals feeding (Frings et al., underwater carcass was monitored for two periods 1955). Although frequently observed, the role of of two weeks and one week respectively. In the first marine mammal carrion on the scavenging activity period Echinodermata (dominated by Asterias of coastal birds is not clear, as previous research on rubens) had the highest maximum number of this subject has been opportunistic and qualitative individuals at the carcass, followed by (e.g. Bruyn & Cooper, 2005; Reid & Forcada, 2005; Actinopterygii (fish) and Malacostraca (crabs). Van den Hoff & Newbery, 2006). Numbers of fish and starfish dropped in the second period, while crustaceans were present in similar Knowledge of marine scavengers, focused mainly on numbers as previously. The daily mass loss of the deep-sea whale-falls, has shown that whale carcasses was 0.56 and 0.07 kg day-1 in the carcasses can support a widespread and terrestrial and marine ecosystems respectively. characteristic faunal community during different Both the terrestrial and marine experiments successional stages (Smith & Baco, 2003). By displayed evidence of bacterial activity. In the contrast, the impact of carrion in shallow waters is absence of any previous detailed study, the present less well known. As food falls occur together with work provides important insights into the roles of other natural and anthropogenic perturbations, it is seal carcasses in coastal systems, especially in an difficult to evaluate their impact on coastal era when carrion from fisheries discards will scavengers, being mostly facultative and not become increasingly unavailable. exclusively dependent on carrion (Ramsay et al., 1997). In shallow water the main scavengers are INTRODUCTION thought to be benthic invertebrates (principally Scavenging is a widespread life-history strategy crustaceans and molluscs). These species likely employed by many carnivorous animals (Selva & detect carrion from the dispersion of chemical cues Fortuna, 2007). Although potentially valuable, indicating the location, quantity and quality of the food source (Britton & Morton, 1994). Faunal properties can, then, lead to a diverse hierarchal colonisation and decompositional changes from structured assemblage of scavenging organisms marine mammal carcasses in coastal systems also (Beasley et al., 2012). appear to be understudied and only a few investigations have taken these phenomena into The aim of this study was to document the account (e.g. Dahlgren & Wiklund, 2006; Glover et consumption of a grey seal (H. grypus) pup carcass al., 2010). by the scavengers in a terrestrial and a marine environment. The terrestrial experiment was a The main factors modelling the structure of the simulation of a dead pup stranded on a beach, scavenging community include competitive and whereas the underwater experiment represents a facilitative interactions, behavioural adaptations, negatively buoyant carcass washed offshore. The carcass size and environment (Selva et al., 2005; hypotheses tested were: 1. the presence of the Sebastián-González et al., 2013; Moleón et al., 2015; carcass alters the distribution of the local Sebastián-González et al., 2016). Intra- and inter- scavenging birds; 2. a defined temporal succession specific interactions may lead to successional of scavengers can be identified during consumption patterns in the scavenging community during the of the carcass in both ecosystems. process of carrion consumption. Many forensic studies focused on post-mortem intervals and the MATERIALS & METHODS associated fauna, but they examined mostly the Ethics statement and permissions succession of terrestrial arthropods (Amendt et al., The grey seal pup carcasses were originally found 2004). Exceptionally, Anderson & Hobischak (2004) dead due to natural mortality on the Isle of May observed the sequence of marine invertebrates (Firth of Forth, Scotland, UK) during the 2011 associated with submerged pig carcasses. pupping season. The Sea Mammal Research Unit Terrestrial vertebrates were rarely considered (University of St Andrews) collected them when still when exploring temporal occurrence of species in fresh condition (between 1-3 days after death) linked to carrion (e.g. Cortés-Avizanda et al., 2012; for the purpose of this project. Carcasses were Young et al., 2014). frozen at -20oC and stored at the University of Glasgow until the study commenced. The Isle of May The total UK populations of both harbour seals is a Scottish Natural Heritage (SNH) National Nature Phoca vitulina (Linnaeus, 1758) and grey seals Reserve (NNR), a Special Protection Area (SPA) and Halichoerus grypus (Fabricius, 1791) were a Site of Special Scientific Interest (SSSI). The island estimated to be around 150,000 individuals in 2012 is owned by SNH, and the collection of carcasses (SCOS 2013). Owing to their body size, high energy was approved under research licences issued by demand and sometimes high local abundance, seals SNH. can strongly influence marine ecosystems, as they The terrestrial experiment required the approval of are capable of transporting energy and nutrients the manager of Little Cumbrae Island for operations over long distances and between habitats. Large on the littoral zone of the island. No Marine Licence aggregations of seals occur on mainland and island was necessary for the underwater experiment, as coasts and it is therefore likely that mortality causes the proposal was treated as scientific experiment. major transfer of energy and nutrients between The permission for the use of the seabed (to the trophic levels and habitats. Annual mortality rate of south of Clashfarland Point, Great Cumbrae Island) UK adult grey seal population is estimated to be was granted by the Crown Estate and Marine around 5% (Thomas & Harwood, 2005), whereas Scotland Licensing Operations. Use of the shore for pup mortality can reach more than 30% in the first the placement of the recording equipment for the month of life in certain areas of the colony underwater camera was granted by the Bute Estate. (Summers et al., 1975). As a result, large adult seal Other authorities and institutes directly or carcasses containing very large amounts of indirectly involved in the experiment were nutrients and energy are relatively rare (one was informed, included the Local Authority’s observed on Great Cumbrae while the terrestrial Environmental Health Department, the University experiment was underway; Quaggiotto, personal Marine Biological Station Millport (UMBSM, now observation), while the smaller pup carcasses are Field Studies Centre Millport), the local police, the probably common following the seal breeding Scottish Agriculture College (SAC now SRUC), the season. So, both terrestrial and the marine food Scottish Environmental Protection Agency (SEPA), webs are affected by seal carrion, but the recycling the Scottish Natural Heritage (SNH), the Sea processes in which it is involved can be Mammal Research Unit (SMRU) and the Scottish fundamentally different (Beasley et al., 2012). Society for the Prevention of Cruelty to Animals Beasley et al. (2012) identified the physical (SSPCA). properties of air and water as main drivers of the fate of carrion in the two ecosystems. Other features Terrestrial experiment of influence include the three-dimensional space of The terrestrial experiment was conducted on the the aquatic system which allows one more island of Little Cumbrae, SW Scotland dimension for movements of carcasses. These (55°43'50.46"N, 4°56'18.59"W) (Fig. 1) between the end of July and September 2012. The resident bird after the deployment of the carcass as indication of populations of Little Cumbrae were estimated to changes in behaviour and spatial use after the comprise 120 great black-backed gulls (Larus carcass became available in the study area. This marinus, Linnaeus, 1758), 1200 lesser black-backed methodology is used also to assess the impact of gulls (Larus fuscus, Linnaeus, 1758) and 2000 wind turbines on birds present in the area of herring gulls (Larus argentatus, Pontoppidan, 1763) installation (e.g. Barrios & Rodríguez, 2004; (JNCC, 2010). There are no data available on ravens Everaert & Stienen, 2006). Continuous sampling (Corvus corax, Linnaeus, 1758) nesting on the (Martin & Bateson, 1993) of flying birds was used to island, but it is likely that some individuals, if not obtain the number of passages during a period of 2 resident, travel from the nearby Great Cumbrae h at each site (2 h per survey). Counts were (Zonfrillo, personal comment). The study area undertaken at different times of the day, at low and (carcass present) and control area (no carcass) high tide at both sites (Table 1). As suggested by were chosen at a distance of approximately 570 m Gregory et al. (2004), the vantage points for counts from each other along the eastern coast of the island were raised and/or concealed positions and were to avoid anthropogenic disturbance and were chosen at a sufficient distance (30 m) from the areas selected based on their similar topographic features to minimise disturbance. Areas of observations had and ease of observation. an approximate size of 150 x 40 m covering both land and sea and only birds flying over this area were counted. The bird counts included herring gulls, lesser black-backed gulls, great black-backed gulls and ravens. Immature individuals belonging to the family Laridae, but of different species, were not distinguished and were grouped together. Avian scavengers were identified by researchers who were previously trained in bird identification and according to Grant (1982) and Holden et al. (2009). Prior to deployment, the seal carcass was intact, with the exception of a missing left eye. Its body length (nose to tail) was 110 cm and mass was 25.0 kg. The carcass was allowed to defrost and was deployed in the upper-littoral (at 3.49 m height and 38.8 m distance to the lower limit of the infralittoral zone) of the study area on 26 July 2012. The appearance of the carcass was documented with photographs in order to define the decompositional stages. Mass loss was recorded by weighing the carcass on a plastic sheet using a digital scale (min = 10g, max = 40kg, accuracy = ± 10g) at approximately weekly intervals. The carcass was monitored by infrared motion-triggered and time- lapse cameras (n = 3; Bushnell Trophy Cam models 119436 and 119435) for the duration of the experiment. Cameras were located at a maximum distance of 3 m from the carcass. Two cameras were set on motion-triggered time lapse mode (two 8 MB resolution photographs every five minutes and Fig. 1. Map of locations of the experimental areas. The terrestrial experiment was run in Little Cumbrae (red every two minutes if movement-triggered) (Hamel circle) and the underwater experiment in Great Cumbrae et al., 2013); the third camera was set on motion- (black circle), West of Scotland, UK. Maps provided by triggered 10s video mode (640 X 480 pixels EDINA Marine Digimap Service, resolution when movement-triggered). The entire http://edina.ac.uk/digimap. © Crown Copyright/SeaZone photo/video collection was used in the analysis Solutions. All Rights Reserved. 052006.001 31st July 2011 including times (maximum 30 min) when the Not to be Used for Navigation. researchers were present in the study area. For the periods 8/13, 16/19-08 and 2/5-09 only videos Seabird surveys were undertaken at the study and were available due to malfunction of the other control sites both before and after the deployment cameras. Birds occurring in the field of view of the of a single grey seal pup carcass (study-before: N = cameras were identified from images and the times 4; study-after: N = 13; control-before: N = 4; spent actively scavenging on the carcass (feeding) control-after: N = 11) at intervals of 2-6 days for the and present but not scavenging (attending the area, total duration of the experiment (from 18/07 to but not feeding) were recorded. Time spent both 5/09/2012) (Table 1). Counts were performed to actively and inactively by gulls on the carcass was evaluate the traffic of birds in the areas before and estimated from the number of minutes included

AREA PERIOD DATE TIME TIDE 18/07 17:30 low 20/07 06:20 low control before 24/07 15:55 high 26/07 17:10 high 19/07 12:35 high 19/07 18:20 low study before 25/07 09:40 low 25/07 16:30 high 26/07 17:10 high 29/07 08:10 high 02/08 17:50 low 03/08 13:15 high 04/08 07:10 low control after 14/08 15:47 low 15/08 09:45 high 20/08 19:05 low 21/08 08:15 low 29/08 16:00 low 30/08 08:20 high 27/07 10:30 low 29/07 14:00 low 30/07 09:35 high 02/08 12:25 high 03/08 17:50 low 04/08 14:05 high study after 05/08 07:30 low 14/08 15:35 low 15/08 09:35 high 20/08 14:50 high 21/08 08:30 low 29/08 16:15 low 30/08 09:00 high

Table 1. Seabirds surveys carried out in the control and study areas before and after the carcass deployment. between consecutive images till the gull attached to the frame and connected by 80 m cable disappeared. When the body of the carcass was to a SD-DVR, a memory card-digital video recorder found opened, the rectangular area containing the onshore. The cable was protected from abrasion by internal organs was measured. Daily maximum being placed inside a length of garden hose. The unit number of individuals (mean MaxN day-1) feeding at was powered By two 12V-55Ah batteries one time at the carcass was calculated for each (Camdenboss Electronics & Enclosures VRLA group of birds. Specimens of invertebrate LeadAcid AGM). Batteries were charged and SD scavengers were collected in the study area (on micro-card changed approximately every four days 02/08), preserved in 70% ethanol and identified in to keep the system working continuously. The the laboratory using Smith (1989). At the end of the carcass was intact, was 100 cm in length and had a study, the remains of the carcass were disposed of mass of 19.7 kg. It was attached (still frozen to at sea. Data on daylight hours and air temperatures facilitate the deployment) to the base of the frame were obtained from timeanddate.com and and then deployed at 6 m depth by the vessel metoffice.gov.uk, respectively. Actinia (UMBSM). The frame’s position on the seabed was adjusted by two SCUBA divers, who Underwater experiment then ran the camera cable back up the shore, A second grey seal pup carcass was deployed on the attaching it to the seabed at intervals using lengths seabed south of Clashfarland Point in Great of chain. The frame was located in the circalittoral Cumbrae Island, SW Scotland (55°45'44.40"N, zone, close to the border with the infralittoral zone. 4°53'41.82"W) (Fig. 1), on 1st August and recovered The seabed was characterized by gravel and sand on 17th October 2013. The carcass was secured to substrate with extensive beds of kelp (Laminaria the wire mesh base of a purpose-built steel frame spp.) within 3-5 m of the frame at the start of the (120 x 60 x 93 cm, LxWxH). The monitoring system experiment. The carcass was monitored consisted of an underwater 24/7 CCTV wired continuously for two periods (2-15/08/13 and 17- camera (1/4 inch Sharp Color CCD, 24 white LEDs) 25/09/13). The interval between periods was caused by technical problems due to fouling by the null and final model. P values of significant barnacles and ultimately leaks into the underwater terms came from an analysis-of-variance (ANOVA camera, which had to be replaced. At the end of the function in R). Ravens were excluded from this experiment the carcass was removed from the analysis because of insufficient data. frame by divers and placed within a waterproof dry- bag before being brought back to the shore. Excess A GLM followed by a Tukey post-hoc multiple water was drained from the dry-bag and then the contrasts test was run to investigate differences carcass was frozen to -20°C while still in the bag and among the absolute feeding times (min day-1; weighed. After carcass removal the camera frame response variable) among the groups of birds equipment was recovered using the vessel winch (explanatory categorical variables). Again, dealing and A-frame. Seawater temperatures were provided with counts, data were modelled with both Poisson by the Field Studies Centre Millport and data on and negative binomial distributions and the model daylight hours were obtained from with the lowest AIC was chosen. timeanddate.com. Videos were analysed using iDRV Player (version V3.5 2011/1/5) and times when The analyses were performed in R 3.0.3 (R bad visibility occurred due to turbulence, bad light Development Core Team, 2012), using the packages conditions or algae interference (Laminaria spp.) ‘MASS’ for the model (glm.nb()) (Venables & Ripley were excluded (Appendix 1). Where possible, 2002), ‘epicalc’ for the likelihood ratio tests organisms were identified to the species level, but (Chongsuvivatwong, 2012) and ‘multcomp’ for the for the purpose of analysis the following taxonomic Tukey contrast test (Torsten et al., 2008). classes of marine organisms were considered: Gastropoda, Bivalvia, Asteroidea (starfish), A purely temporal scanning statistic was used to Malacostraca (crabs) and Actinopterygii (fish). detect the predicted temporal succession of Individuals occurring on the carcass were counted scavengers occurring during consumption of the at 10 min time intervals. The daily maximum carcass: clusters of feeding activity (min day-1) of number of individuals (MaxN day-1) was calculated the same group of birds at particular times at the for the five groups. The proportions of visits by carcass during the experiment were therefore crustaceans were calculated for day and night in the identified. The temporal scan statistic uses a two periods. Agonistic events were recorded when window, defined as an interval time of variable size, observed. which scans the temporal data to be analysed. The number of observed and expected observations Statistical analysis inside the window is noted and the window with Statistical analysis was carried out following the maximum likelihood is the most likely cluster. procedures and methods explained in Dytham This analysis was performed in the program (2003), Zuur et al. (2009) and Zuur et al. (2010). SaTScan (Kulldorff et al., 2005): the purely temporal analysis was implemented by selecting a discrete Terrestrial experiment Poisson probability model and a temporal cluster Generalised linear models (GLMs) were carried out size between 2 days and 50% of the study period. A to evaluate whether the deployment of the seal total of 9999 Monte Carlo simulations were made to carcass at the study area altered the distribution of calculate p-values for detected clusters. the scavenging birds. The response variable was the number of passages of each group of birds counted Once checked for non-normal distribution running a in two hour survey (N passages 2 h-1), while the Shapiro–Wilk test, the nonparametric pairwise explanatory variables were the Area (categorical: Wilcox Mann-Whitney test with Holm’s adjustment study and control), the Period (categorical: before method, giving a strong control of the family-wise and after the carcass deployment), the Tide error rate, was used to compare the proportions of (categorical: high and low) and the Time of the day time spent actively feeding among groups of birds. (categorical: morning and afternoon). The primary Lesser black-backed gulls were excluded in the aim was to test for a significant interaction effect previously described three analyses because they between Area and Period as a significant interaction we not observed feeding on the carcass. would imply that bird abundance changed differently in the study and control sites after the Underwater experiment carcass was deployed. After exploring data Poisson GLMs were used to evaluate differences in according to Zuur et al. (2010), the model was run the composition of the scavenger assemblage including all the explanatory variables and the only between the two periods of monitoring and interaction of interest and the minimum adequate between day and night. The relationship between model was identified by step-wise removal of non- maximum number of individuals (MaxN day-1; significant terms choosing the model with the response variable), and Period of monitoring lowest AIC (Akaike Information Criterion). Dealing (categorical: period 1 and period 2), and Time of the with counts, data were modelled with both Poisson day (categorical: day and night) was investigated and negative binomial distributions. The likelihood for each taxonomic class (excluding gastropods and ratio test score was calculated in order to compare bivalves because of insufficient data). The model was run including all the explanatory variables and to be in the putrefaction stage (day 30). The carcass their interaction and the minimum adequate model was disposed of at day 42, when only bones and was identified by step-wise removal of non- mummified hide were present. significant terms choosing the model with the lowest AIC. The likelihood ratio test score was The presence of the carcass led to an increase of calculated in order to compare the null and final great black-backed gulls, juvenile gulls, ravens and model. P values of significant terms came from an lesser black-backed gulls flying over the study area analysis-of-variance (ANOVA function in R). after the start of the experiment (Fig. 2). In the control area the great black-backed and juvenile The proportions of visits made by malacostracans at gulls together with ravens also increased their visits day and night for the two periods were compared after the carcass became available, but there was a by using the nonparametric pairwise Wilcox Mann- decrease in the presence of lesser black-backed and Whitney test with Holm’s adjustment method, after herring gulls. checking the non-normality nature of the data by No best fitting model carried out for each group of using a Shapiro–Wilk test. birds showed a statistically significant interaction between Area and Period (Appendix 2). In Analyses were performed in R 3.0.3 using the same particular, the distribution of great black-backed packages as mentioned previously. gulls was explained by the variables Tide (P = 0.0296), Area (P < 0.0001) and Period (P = 0.0003), RESULTS whereas the number of herring gulls varied Terrestrial experiment according to the Tide (P = 0.0001). The fitted The maximum and minimum air temperatures models for the other groups of birds did not have recorded in July were 18.1°C and 11.2°C, 19.7° and significant terms (Appendix 2). 11.8° in August and 15.3°C and 8.9°C in September. The daylight hours ranged from 16.83 to 16.10 h in Great black-backed gulls, herring gulls, juvenile July, from 16.02 to 13.88 h in August and from 13.80 gulls and ravens, but not lesser black-backed gulls, to 13.50 h in September. all scavenged the seal carcass (Fig. 3). Juveniles spent more time at the carcass in comparison to the Within 24 h of carcass placement, abrasions and other group of birds for a total of 237.63 h, both wounds were evident. The first areas to be fed upon feeding (51.1%) and non-feeding (min day-1; Table were the umbilicus and the eye region. From the 2). The second most frequent visitors were great camera footage, at day 2, a great black-backed gull black-backed gulls which spent a total of 41.02 h on was seen pulling out the intestines from the carcass the carcass and actively scavenged for 81.4% of this which were then found spread over an area of 18 time. Ravens made infrequent visits, spending 11.43 m2. From day 3, initial wounds were further opened h around the carcass and were feeding for 66.5% of and fly larvae and adults (Calliphora vicina the time. Herring gulls were rarely seen scavenging (Robineau-Desvoidy, 1830), Lucilia sericata on the dead seal (20.8% of a total of 2.88 h), (Meigen, 1826), Lucilia sp.) together with the spending most of the time attending the scene burying beetle (Nicrophorus humator (Gleditsch, without participating. Lesser black-backed gulls did 1767)) were present in the mouth, nostrils and not scavenge the carcass and their presence underneath the body. Occasionally crabs were occurred for a total of only 15 minutes. They were observed visiting the carcass during the night. excluded from the subsequent analyses. The highest As the holes in the head and abdomen grew, mean maximum number of individuals observed at wounds also began to appear on the flippers (day the carcass at one time was observed in the 8). At day 20 the spine and internal viscera were juveniles. The latter were also the most frequent exposed and the head was disarticulated. The front visitors of the experimental area, followed by great flippers were consumed quickly. The rear flippers black-backed gulls, ravens and finally herring gulls were only superficially damaged and appeared (Table 2). The absolute feeding times were desiccated by the end of the experiment. compared between groups of birds and the great The carcass showed successive stages of decay over black-backed gulls scavenged more than the ravens the course of the study. In the initial stage (Tukey contrasts test, P = 0.0116), but less than the arthropods quickly colonised the carcass (day 3). juvenile gulls (P = 0.0383). All the other The next stage was characterized by bloating (day comparisons between groups of birds were highly 9) followed by liquefaction (day 11), in which the significant (P < 0.001). carcass appeared much flatter and the tissues within the openings started to decay. A strong putrid smell was noted, apparently caused by liquids leaking from the carcass. The collapse stage was observed when a large quantity of the tissue was consumed and the head broke down (day 21). Approximately nine days later, the carcass appeared

Fig. 2. Total number of bird passages per 2 hour count. Great black-backed gulls (GBBG) , ravens (RAVEN) , herring gulls (HG), lesser black-backed gulls (LBBG) and juvenile gulls (JUV) in the control (C) and study (S) areas before (B) and after (A) the deployment of the carcass in the study site. On each box, the central mark is the median, the edges of the box are the lower hinge (25th percentile) and the upper hinge (75th percentile), the whiskers extend to the maximum and minimum data points, outliers are plotted individually.

Fig. 3. Avian scavengers occurring in the terrestrial experiment. A white arrow indicates the seal’s head. A) Great black-backed gull pulling out the internal organs of the carcass (day 3); B) Herring gull visiting the study area (day 3); C) Two juvenile gulls (day 21); D) Raven feeding on the carcass at a late stage of consumption and decomposition (day 29).

Adult gulls Juvenile gulls Ravens GBBG HG LBBG Feeding time day-1 (min) 47.95 0.85 0 173.52 10.85 (SE) (11.58) (0.43) (0) (23.4) (3.25) Non-feeding time day-1 (min) 10.93 3.27 0.37 165.98 5.48 (SE) (2.45) (1.25) (0.25) (33.47) (0.25) Visits (n day-1) 3.17 0.50 0.12 11.29 1.69 (SE) (0.54) (0.16) (0.08) (1.58) (0.42) Mean MaxN day-1 0.86 0.33 0.07 1.83 0.67 (SE) (0.009) (0.07) (0.04) (0.18) (0.12)

Table 2. Daily means of feeding time, non-feeding time, number of visits and maximum number of individuals (MaxN) for groups of birds. Means and standard errors (SE) are presented in minutes. GBBG = great black-backed gulls, HG = herring gulls, LBBG = lesser black -backed gulls, juvenile gulls and ravens.

Temporal pattern in the feeding activity of different backed gulls (interval time 13-27/08; P = 0.0001). groups of birds was observed during the Ravens were active mostly in the final stage of experiment (Fig. 4) and temporal clusters were consumption (interval time 23-31/08; P = 0.0001). detected at different times for different groups: the Herring gulls visited the carcass forming the great black-backed gulls opened the carcass the day shortest time cluster (interval time 9-16/08; P = following its deployment (27/07) and contributed 0.0001) between great black-backed gulls and to the dismantling of the carcass for a temporal juveniles. The mass of the carcass decreased from cluster of 11 days (interval time 27/07 – 06/08; P = 25.00 to 1.83 kg, resulting in an estimated daily 0.0001). Juveniles were the most common for a long mass loss of 0.56 kg. period after the decrease in visits by great black-

Fig. 4. Daily feeding activity (percentage) of groups of birds (columns) and carcass mass loss ( ). Great black-backed gulls (GBBG, red), juvenile gulls (JUV, white), ravens (blue) and herring gulls (HG, yellow).

Great black-backed gulls (pairwise Wilcox Mann- recovered (day 78), the carcass was barely Whitney test, P = 0.0017), juvenile gulls (P = recognisable: it was still positively buoyant, even if 0.0005) and ravens (P = 0.0028) showed flattened, and presented exposed bones of the neck significantly higher proportion of feeding time than and pelvis regions. The whole body was covered by herring gulls. a thick grey layer of bacteria. The mass of the carcass at the end of the experiment was 14.45 kg, Underwater experiment resulting in a total reduction of 5.25 kg and an The daily seawater temperature ranged from 14.8°C estimated daily mass loss of 0.07 kg. to 17.0°C during the first survey period in August, 12.0°C to 13.0°C during the second period in September. The mean daily seawater temperature for the month of August was 15.3°C (SD =0.81) and for September was 13.2°C (SD = 0.87). The daylight hours ranged from 16.03 to 13.9 h in August and from 13.82 to 11.62 h in September.

Within five days from the start of the experiment the eye of the carcass was scavenged (Fig. 5A). A large wound appeared on the front left flipper at day 10 (Fig. 5B) and another one of smaller size on the top of the shoulder at the day 13. After three days (day 15) the nose was bitten, the mouth opened showing the teeth and the abrasion around the eye enlarged. Several whitish patches also developed on the fur which broadened in the following days to cover all visible areas of the body surface. Furthermore, the seal’s head appeared to have risen a few centimetres from the base of the Fig. 5. Underwater experiment at different stages of structure suggesting that the carcass was positively consumption and decomposition of the carcass. A) The buoyant (Fig. 5C). At the beginning of the second carcass shows a scavenged eye; starfish are feeding on it period of monitoring the carcass was still in this (day 5); B) A large wound appears on the front left floating state showing a more advanced stage of flipper; a labrid, a crab and few starfish are present (day decomposition (at day 48 of submersion). The body 10); C) The carcass shows positive buoyancy and several whitish patches; kelp is partially covering the dead seal appeared white and covered by new greyish (day 15); D) The carcass is on late stage of decomposition patches; the head was damaged exposing the facial and epidermis with fur detaches, bones are exposed on bones, and the jaws were still attached (Fig. 5D). At the area of the face (day 48). day 54 (end of the camera recording) several sections of epidermis with fur had detached denuding small areas of exposed dermis. When

Generally the carcass was visited by members of the their bodies on the surface of the carcass. During phyla Mollusca, Arthropoda, Echinodermata and the the night few individuals of Pholis gunnellus subphylum Vertebrata. In total 4 phyla, 5 classes, 9 (Linnaeus, 1758) were seen around the carcass and orders, 14 families and 16 species were identified sometimes attached to it pushing their heads on it. (Table 3). Agonistic interactions were observed only during the first period and involved intra- and inter-class In the first period Asterias rubens (Linnaeus, 1758) events between two crabs (N = 4), a crab and belonging to the class Asteroidea (starfish) was the starfish (N = 4), two starfishes (N = 2) and a crab most common scavenger (mean MaxN = 11.03, SE = and fish (N = 1). Cancer pagurus successfully forced 0.72) followed by the classes Actinopterygii (fish; several starfish to abandon the carcass by moving mean MaxN = 9.14, se = 1.16) and Malacostraca them with its claws. Only once was a starfish seen to (crabs; mean MaxN=1.53, SE = 0.14). The netted dog force a crab to move away. In the second period the whelk Tritia reticulata (Linnaeus, 1758) was rarely maximum number of asteroids reduced drastically observed and never more than one individual per (mean MaxN = 1.13, SE = 0.22) together with fish time. The Atlantic scallop Pecten maximus (mean MaxN = 2.8, SE = 0.81), while the relative (Linnaeus, 1758) was also observed in the video. abundance of crustaceans showed no obvious However, its visits were probably accidental (Fig. change (mean MaxN = 1.26, SE = 0.15) (Fig. 6B). 6A). Starfish exhibited feeding preference on the head and on the areas of the joints. Some Best fitting model for the class Asteroidea showed individuals were seen disappearing under the that the MaxN of starfish decreased significantly carcass and during the second period of monitoring during the second period of monitoring (P < 0.0001) a specimen was partly hidden in the eye cavity. of the underwater carcass (Appendix 3). The MaxN Crabs scavenged in the same areas of starfish when of Actinopterygii (fish) was explained by both accessible. Individual fish or schools were recorded, Period and Time of the day, being lower during the but particular behaviours were also noted: an adult second period (P < 0.0001) and during night (P < of the family Labridae was seen interacting with the 0.0001); whereas in Malacostraca (crabs) no carcass by spitting its food on it, while the saithe significant changes were seen (Appendix 3). Pollachius virens (Linnaeus, 1758) and the pollack P. pollachius (Linnaeus, 1758) were observed scraping

Phylum Class Order Family Species Mollusca Gastropoda Neogastropoda Nassariidae Tritia reticulata Bivalvia Pectinoidea Pectinidae Pecten maximus Arthropoda Malacostraca Decapoda Paguridae Pagurus bernhardus Cancridae Cancer pagurus Portunidae Carcinus maenas Polybiidae Necora puber Liocarcinus depurator Echinodermata Asteroidea Forcipulatida Asteriidae Asterias rubens Marthasterias glacialis Chordata Actinopterygii Gadiformes Gadidae Pollachius virens Pollachius pollachius Perciformes Labridae Symphodus melops Labrus mixtus Blenniidae Gobidae Pholidae Pholis gunnellus Pleuronectiformes Pleuronectidae Limanda sp. Syngnathiformes Syngnathidae Syngnathus acus

Tot 4 5 9 14 16

Table 3. Systematic classification of marine organisms occurring on the carcass.

DISCUSSION The present study represents the first detailed observational study on scavengers feeding on pinniped carrion in both the terrestrial and marine systems: so far no study has compared carrion consumption in the two ecosystems (Beasley et al., 2012). Existing literature concerning scavenging on seals consists mainly of singular opportunistic observations, as in the case of the red fox (Vulpes vulpes) and the southern giant petrel (Macronectes giganteus), seen feeding on dead seals (or seal placenta) around a seal colony (Culloch et al., 2012) and in submerged conditions (Van den Hoff & Newbery, 2006) respectively. Bruyn & Cooper (2005), instead, focused on inter- and intra-specific behaviour of southern and northern giant (Macronectes halli) petrels feeding on a southern elephant seal carcass, but for a limited time (150 minutes). Stable isotope analyses showed that seal carrion was part of the diet of giant petrels (Forero et al., 2005) and also of Arctic foxes (Vulpes lagopus) (Roth, 2002). Scat analyses combined with behavioural observations showed that seal carrion is also consumed by brown hyenas (Hyaena brunnea) on the Namibian coast (Kuhn et al., 2008). -1 Fig. 6. Maximum number of individuals (MaxN day ) for However, there have been no studies investigating the observed classes in the two periods of monitoring (A: the patterns and processes involving these Period 1; B: Period 2). On each bar, the top of the bar is the mean of the MaxN day-1, error bars are ± SE. scavengers as part of a wider scavenging community and their interactions within it. Crustaceans visited the carcass more often during the first stage of the experiment with 14.64 (SE = Terrestrial experiment 2.45) and 8.33 (SE = 1.41) mean visits per day This experiment described how scavenging seabirds during the first and second periods, respectively. dismantle a marine mammal carcass: eyes were the The proportion of visits by crabs in the first period first body organs consumed and feeding at the of monitoring was significantly higher during the umbilicus was the most accessible way for night than during the day (pairwise Wilcox Mann- scavengers to open the carcass. Secondary openings Whitney test, P = 0.0001), while in the second appeared to arise as a result of longer pecking period there was no significant difference (P = 0.61) activity on the carcass. Pavés et al. (2008) have (Fig. 7). described how vultures first feed on the eyes of dead sea lion pups and adults, and then the navel, genitals and anus. However, as scavenging and decomposition occur simultaneously, it was not possible to separately measure each of the two processes. It is likely that the carcass was influenced by temperature and moisture levels, which strongly affect the decomposition rate (Barton et al., 2013). The carcass was also consumed by invertebrate scavengers, where the colonization by fly larvae contributed to the liquefaction of the tissues (Putman, 1983).

Results did not show a significant change in seabird passage in the study area compared with the control site after the deployment of the carcass. This can be related to the infrequency of this resource for the Fig. 7. Proportions of visits by malacostracans during day scavenging birds of Little Cumbrae, but also by the and night in the two periods of monitoring. On each box, little interest showed by some species such as the the central mark is the median, the edges of the box are lesser black-backed gull and the herring gull. An the lower hinge (25th percentile) and the upper hinge increase in the number of passages of the great (75th percentile), the whiskers extend to the maximum black-backed gull after the deployment of the dead and minimum data points, outliers are plotted individually. seal was, instead, observed, but in both areas. In contrast to the unpredictability characterising the carcass used for this experiment, the effect of a final days the consumption rate decreased possibly resource predictable in time and space on seabird due to the low availability of edible material left. foraging behaviour has been suggested instead in The deterrent effect of decomposing matter and other studies. Cama et al. (2012) identified the high toxin production on the behaviour of terrestrial density of vessels providing fishing discards as the scavengers (DeVault et al., 2004; Selva et al., 2005; best explanatory variable for the distribution of Parmenter & Macmahon, 2009) was not observed, gulls in the Western Mediterranean. Monsarrat et al. as the carcass was not abandoned prior to complete (2013), instead, observed that vultures also consumption. restricted their searching home range around artificially-maintained feeding stations when Underwater experiment weather conditions were not optimal or food was The present experiment represents one of the few scarce, preferring stations with lower amounts of existing studies on the successional pattern of food where intra-specific competition was reduced. scavenging on carrion in the subtidal marine A defined temporal succession of scavenging birds environment. Forensic science has paid attention to feeding on the carcass was observed, in which this subject before: Hobischak & Anderson (2002), segregation of different groups of birds was for instance, examined the species and sequence of possibly related to competition due to overlap in invertebrates associated with carrion, but in fresh resource utilization. The great black-backed gull water, whereas Anderson & Hobischak (2004) was the first to approach the carcass and was able described those scavengers that occur on to break through the thick skin of the carcass. As experimental pig carcasses submerged in marine described by Camphuysen et al. (1995), it is a waters. “powerful scavenger”, which out-competes the herring gull for food when the two species share the Results showed that abundance of scavengers same breeding site (Rome & Ellis, 2004). In fact, attracted to the carcass changed during time. This despite being the most abundant species, the suggests that temporal variation in the extent of herring and lesser black-backed gulls seldom visited exploitation of carrion by different scavengers the carcass and rarely exploited it, even though they exists. In the first period the scavenging community are both known to scavenge in other contexts was dominated by asteroids which occurred in (Camphuysen et al., 1995; Catchpole et al., 2006). great numbers (up to 17 individuals) to colonize the During summer, Little Cumbrae is a breeding site carcass. A. rubens is one of the most abundant for the three gull species with nesting occurring scavenging species found in fishery discards in the around mid- April and the first chicks hatching in west of Scotland (Nickell & Moore, 1991; Bergmann May (Cramp et al., 1974). The numerous juveniles et al., 2002). Moreover, the experimental area was visiting the carcass may have been part of the new in the ideal habitat for this sublittoral species which generation of gulls born in the island. They were not prefers sandy, muddy substrata. The occurrence of observed early in the study during the dominance of adult and juvenile actinopterygian fish could be the great black-backed gull on the carcass. linked to shallow coastal waters which may offer Moreover, they spent an equal proportion of their protection from predation, in particular to new time being inactive at the carcass, possibly because recruitment of juvenile gadoids during summer of the lack of experience and the unfamiliarity with (Pihl, 1982). Decapods exhibited nocturnal habits this food source. Seal carrion is a fairly uncommon mostly in the first period, while they showed less resource outside of seal colonies (Culloch et al., preference for the dark during the second period, 2012) and juvenile gulls were unlikely to have probably due to the reduction of daylight hours previously encountered this food type. During the towards the autumn and in the number of starfish. project period a natural seal carcass washed up on Generally crabs are nocturnal predators with peaks Great Cumbrae (Quaggiotto, personal observation), of activity during high tide, like C. pagurus (Skajaa et so such events can occur in this area. Despite being al., 1998) and Carcinus maenas (Naylor, 1958; active carrion feeders (Heinrich, 1988), ravens Ropes, 1968), but they can also be diurnal (Novak, scavenged more consistently from day 30 onwards. 2004). In accordance with other studies focusing on It is likely that the ravens were unable to feed at the scavenging aggregations on fishery discards in the same time as the great black-backed gulls or Irish, Clyde and Adriatic Seas, Liocarcinus depurator juveniles, as found by Hewson (1995). In this study was the most abundant among all the other the mass loss of the carcass was approximately brachyuran scavengers (Ramsay et al., 1997; linear. Although the single sample prevents any Ramsay et al., 1998; Wieczorek et al., 1999). The meaningful statistical comparison, the mass loss of a infrequent visits of dog whelks T. reticulata could be carcass has previously been shown to follow a related to the fact that it is considered an occasional sigmoidal decrease with time (Putman, 1983; Carter species in this habitat. et al., 2007), being initially untouched, but then being dismantled quickly. In the current At the second stage of the experiment the carcass experiment, instead, the carcass was detected showed an increase of what appeared to be almost immediately (on day 2 after the deployment) microbial mat covering its surface and even if the and consumed at a constant rate during time. On the number of crabs stayed stable, a drastic drop in the number of asteroids together with the number of approximate the seabed phases in the cycle of fish occurred. Also Burkepile et al. (2006) found floating and sinking that occurs with natural that crabs still scavenge on aged fish carrion. carcasses in the marine environment. Bacteria use chemicals to compete against other One other investigation included underwater microbes, but these chemicals can also act as observations and, similarly to the present study, the deterrent from carrion for animal scavengers marine mammal carcasses were constrained to the (Burkepile et al., 2006). Scavenging marine seabed by using ropes during the period of organisms detect prey by olfactory foraging cues monitoring (Glover et al., 2010). Thus, the flotation and different taxa have specific chemo-sensitivity and natural drift of the carcasses were impeded. according to the olfactory organ (e.g. Morton & Glover et al. (2010) observed the first floating state Yuen, 2000; Tran et al., 2014). Therefore, the of an experimental Phocoena phocoena (Linnaeus, bacterial action is likely to be an important biotic 1758) for two days after implantation at 30m depth, factor influencing the post-mortem fate of a carcass but argued that negatively buoyant carcasses are in aquatic contexts. Burkepile et al. (2006) likely to occur at this depth. Pup carcasses are also demonstrated that scavengers were 2.6 times more likely to be found in shallow waters: during pupping attracted by fresh carrion than microbe-laden season, for instance, a certain number of dead pups carcass. However, different species of crabs reacted may enter the marine system without reaching differently, suggesting that species-specific upper levels because they are trapped among rocks palatability exists. The present study focused on the or have sunk to the seabed. It is possible, in fact, scavenging mega-faunal succession on carrion, but that most of the carcasses provided during the grey it was evident that bacterial decomposers also seal pupping season are negatively buoyant, as the benefited from it, taking part in the recycling of major cause of death is starvation (Baily, 2014) carrion. Dickson et al. (2011) described five which depletes the pups’ blubber. different phases of bacterial colonisation on partial carrion proving that the rate at which successive Comparison between terrestrial and marine stages appeared was temperature dependent with experiments warmer waters allowing a faster decomposition. Comparing the scavenging processes observed in Therefore, seasonal changes in sea water the two experiments, it is clear that the daily mass temperature could underlie differences in the loss of carrion was lower in the marine ecosystem duration of successive decay stages dominated by than in the terrestrial one, at a ratio of 1:8. This either marine animals or bacteria. could be in part due to the larger size of terrestrial scavengers and their endothermic nature in The floating carcass stage generally occurs when comparison to their marine counterparts which bacteria start to produce gas inside the body permitted a faster consumption rate of the carcass. (Reisdorf et al., 2012). In the current study the Generally, at greater depths (1200-1800 m), bathyal appearance of microbes on the body’s surfaces scavenger assemblages remove tissue from whale coincided with the carcass becoming positively carcasses at rates of 40–60 kg day-1 (Smith & Baco, buoyant; a state which lasted until the end of the 2003). However, the scavengers involved are not experiment. Carrion has two floating stages: the only invertebrates, as observed in the current study, primary flotation is due to gas forming in the but also large vertebrates such as sleeper sharks, digestive tract, while the secondary flotation hagfish and grenadiers, which aggregate in large depends on bacterial activity within the corpse numbers to remove the soft tissue of the whale (Teather, 1994). Owing to the unknown post- carcass. This process can last from months to years mortem age of the experimental carcass and its and involves mostly obligate scavengers. Together frozen conditions before the deployment, it is very with the scavenger community, it was suggested likely that secondary flotation would occur if the that the size of the carcass is a factor determining carcass had not been tethered. Putrefaction gases the rate of its consumption. In fact, at the same are likely to cause the surfacing of the carcass in depth, smaller cetacean carcasses were eaten at a shallow waters at temperature above 4°C (Moreno lower rate (1.2 - 9.6 kg day-1) than the whale falls et al., 1992; Sorg et al., 1997; Petrik et al., 2004), (Jones et al., 1998; Smith & Baco, 2003). Also on whereas negative buoyancy is expected when land larger carcasses (>100 kg) were found to be carcass integrity is compromised (Anderson & consumed 33 times faster than smaller ones (<10 Hobischak, 2004). However, floating marine kg) (Moleón et al., 2015). However, specialised mammal carcasses may be exposed to scavenging scavengers may accelerate the process. birds when reaching the water surface and even to mammals when stranded on the beach. For Changes in the scavenging community were example, Hewson (1995) observed great black- detected over the duration of both experiments. On backed gulls defending floating carrion and pulling land, a hierarchical succession of dominant it to shallow water for consumption. This process scavengers through competitive displacement of may cause the carcass to sink quickly back to the subordinates occurred during the exploitation of seabed making it available again to the marine the carcass. Underwater, instead, a change in the community. The two periods of recording may then numbers of scavengers between the two periods of monitoring might be caused by the deterrent effect Considering the high usage of fishery discards by on starfish rather than crabs of the microbial mat scavengers, it is uncertain what repercussions the that formed on the dead pup. reformed Common Fisheries Policies will have to the foraging behaviour of scavengers. The discard Future studies and implications ban came into force on 1st January 2014 and will The terrestrial experiment provides a long-term gradually require EU fishing vessels to land the and continuous dataset from the initial to the final whole of each catch (http://www.scotland.gov.uk). stage of seal carcass consumption on land. Several According to a recent publication by Heath et al. studies have continuously monitored carcasses in (2014) the discard ban may cause a bottom-up terrestrial ecosystems until the carcass was trophic cascade which will lead to a reduction in consumed completely (Blázquez et al., 2009; biomass of scavengers such as benthic invertebrates Sebastián-González et al., 2013; Huang et al., 2014; and birds. At this point other sources of carrion, Moleón et al., 2015; Sebastián-González et al., such as pinniped carcasses, could represent an 2016), but only few in a coastal system (e.g. important alternative resource for scavengers and Schlacher et al., 2013). There is only one study of understanding their impact in the ecology of these this type using marine mammal carrion in the species will become necessary. terrestrial ecosystem of which we are aware (Pavés et al., 2008). The underwater experiment is one of ACKNOWLEDGEMENTS the few existing studies on the succession of marine The authors gratefully acknowledge the dive team scavengers exploiting carrion in shallow waters (e.g. and field assistants N. Burns, J. Clarke, S. Elliott, C. Anderson & Hobischak, 2004; Glover & Higgs, Hopkins and D. McNeill for their help in the 2010). However, the long-term nature of the underwater experiment; the support of the experiment and the technical constraints limited the University Marine Biological Station Millport collection of a continuous dataset. Similar (UMBSM) and in particular its boat crew of RV complications have also been encountered in other ‘Actinia’ formed by C. McLachlan, D. Patrick, and K. studies (e.g. Anderson & Hobischak, 2004). Cameron. We would also like to thank N. Mirzai, A. Torry and T. Wallace of MVLS Bioelectronics Unit Further investigations are needed to assess the (University of Glasgow) for creating the underwater value of this food resource as energy and biomass system and fixing it when necessary, J. Magill of the inputs released to the ecosystem and its impact on MVLS Mechanical Workshop (University of the scavenging community. Coastal regions are, in Glasgow) for building the underwater frame; the fact, often affected by marine-derived inputs (Polis Sea Mammal Research Unit (SMRU – University of St & Hurd, 1996a; Polis & Hurd, 1996b; Polis et al., Andrews) for providing the carcasses and giving 1997; Rose & Polis, 1998) whose effects on the useful advice. S. White kindly loaned the infrared receiving ecosystem include alteration of trophic cameras. This work was supported by College of species dynamics (Polis et al., 1997, Briggs et al., Medical, Veterinary and Life Sciences Scholarship - 2012) and their distribution (Schlacher et al., 2013). University of Glasgow. In particular, bird and marine mammal carrion is frequently deposited ashore because of large scale REFERENCES or seasonal perturbations, especially in areas where Amendt, J., Krettek, R. & Zehner, R. (2004). Forensic these animals live (Bodkin & Jameson, 1991). entomology. Die Naturwissenschaften, 91(2), 51– Despite the limited number of experimental 65. doi: 10.1007/s00114-003-0493-5 carcasses used, this novel study brings new insights Anderson, G.S. & Hobischak, N.R. (2004). to our understanding of the ecological process Decomposition of carrion in the marine involving the exploitation of pinniped carrion by environment in British Columbia, Canada. coastal scavengers. International journal of legal medicine, 118(4), 206–209. doi: 10.1007/s00414-004-0447-2 Marine mammal carrion could become an Barrios, L. & Rodríguez, A. (2004). Behavioural and increasingly important part of the diets of European environmental correlates of soaring-bird scavengers, partly because of the continual increase mortality at on-shore wind turbines. Journal of in grey seal pup production since the 1960s (SCOS, Applied Ecology, 41(1), 72–81. doi: 2013), but also because of regulations banning the 10.1111/j.1365-2664.2004.00876.x discarding by pelagic and then demersal fishing Barton, P.S., Cunningham, S.A., Lindenmayer, D.B. & operations (EU Regulation 1830/2013). Catchpole Manning, A.D. (2013). The role of carrion in et al. (2006) estimated the partitioning of discards maintaining biodiversity and ecological between marine and aerial scavengers based on the processes in terrestrial ecosystems. Oecologia, English Nephrops norvegicus fisheries. The resulting 171, 761–772. doi: 10.1007/s00442-012-2460-3 bioenergetic model showed that 57% of discards Baily, J.L. (2014). The pathology and occurrence of was taken by seabirds with the remainder becoming pathogens in Scottish grey seals (Halichoerus available to marine fauna. The total amount of grypus). PhD thesis, University of St Andrews. biomass and energy released were 4780 t and 19.7 Beasley, J.C., Olson, Z.H. & DeVault, T.L., (2012). x 109 kJ respectively (Catchpole et al., 2006). Carrion cycling in food webs: comparisons

among terrestrial and marine ecosystems. Oikos, Epidemiological calculator. R package version 121(7), 1021–1026. doi: 10.1111/j.1600- 2.15.1.0. 0706.2012.20353.x https://cran.r-project.org/src/contrib/Archive/epicalc/?C=N;O=A Bergmann, M. , Wieczorek S.K., Moore, P.G. & Cortés-Avizanda, A., Jovani, R., Carrete, M. & Atkinson, R.Y.A. (2002). Utilisation of Donázar, J.A. (2012). Resource unpredictability invertebrates discarded from the Nephrops promotes species diversity and coexistence in an fishery by variously selective benthic scavengers avian scavenger guild: A field experiment. in the west of Scotland. Marine Ecology Progress Ecology, 93(12), 2570–2579. Series, 233, 185–198. doi: 10.3354/meps233185 Cramp, S., Bourne, W.R.P. & Saunders, D. (1974). Blázquez, M., Sánchez-Zapata, J.A., Botella, F., The Seabirds of Britain and Ireland, Great Carrete, M. & Eguía, S. (2009). Spatio-temporal Britain, Collins. segregation of facultative avian scavengers at Culloch, R., Pomeroy, P., Lidstone-Scott, R., Bourne, ungulate carcasses. Acta Oecologica, 35, 645– L. & Twiss, S.D. (2012). Short Note: Observations 650. doi: 10.1016/j.actao.2009.06.002 from Video Footage of Red Fox (Vulpes vulpes) Bodkin, J.L. & Jameson, R.J. (1991). Patterns of Activity Within a Grey Seal (Halichoerus grypus) seabird and marine mammal carcass deposition Breeding Colony on the UK Mainland. Aquatic along the central California coast, 1980–1986. Mammals, 38(1), 81–85. doi: Canadian Journal of Zoology, 69, 1149–1155. doi: 10.1578/AM.38.1.2012.81 10.1139/z91-163 Dahlgren, T.G., Wiklund, H., Källström, B., Lundälv, Briggs, A.A., Young, H.S., McCauley, D.J., Hathaway, T.,Smith, C.R.& Glover, A.G. (2006). A shallow- S.A., Dirzo, R. & Fisher, R.N. (2012). Effects of water whale-fall experiment in the north spatial subsidies and habitat structure on the Atlantic. Cahiers de Biologie Marine, 47, 385–389. foraging ecology and size of geckos. PloS One, DeVault, T.L., Brisbin, I.L. & Rhodes, O.E. (2004). 7(8), e41364. doi: Factors influencing the acquisition of rodent 10.1371/journal.pone.0041364 carrion by vertebrate scavengers and Britton, J.C. & Morton, B. (1994). Marine carrion and decomposers. Canadian Journal of Zoology, scavengers. Oceanography Marine Biology 82(3), 502–509. doi: 10.1139/z04-022 Annual Review, 32, 369–434. Dickson, G.C., Poulter, R.T.M., Maas, E.W., Probert, Bruyn, P.J.N. & Cooper, J. (2005). Who’s the boss? P.K., Kieser, J. (2011). Marine bacterial Giant petrel arrival times and interspecific succession as a potential indicator of interactions at a seal carcass at sub-Antarctic postmortem submersion interval. Forensic Marion Island. Polar Biology, 28(7), 571–573. science international, 209(1-3), 1–10. doi: doi: 10.1007/s00300-005-0724-7 10.1016/j.forsciint.2010.10.016 Burkepile, D.E., Parker, J.D., Woodson, C.B., Mills, Dytham C. (2003). Choosing and Using Statistics: A H.J., Kubanek, J., Sobecky, P.A. & Hay, M.E. Biologist’s Guide. Second Edition. Blackwell (2006). Chemically mediated competition Publishing, Malden. between microbes and animals: Microbes as Everaert, J. & Stienen, E.W.M. (2006). Impact of consumers in food webs. Ecology, 87(11), 2821– wind turbines on birds in Zeebrugge (Belgium). 2831. doi: 10.1890/0012- Biodiversity and Conservation, 16(12), 3345– 9658(2006)87[2821:CMCBMA]2.0.CO;2 3359. doi: 10.1007/s10531-006-9082-1 Cama, A., Abellana, R., Christel, I., Ferrer, X. & Forero, M.G., González-Solís, J., Hobson, K.A., Vieites, D.R. (2012). Living on predictability: Donázar, J.A., Bertellotti, M., Blanco, G. & modelling the density distribution of efficient Bortolotti, G.R. (2005). Stable isotopes reveal foraging seabirds. Ecography, 35(10), 912–921. trophic segregation by sex and age in the doi: 10.1111/j.1600-0587.2011.06756.x southern giant petrel in two different food webs. Camphuysen, K.C.J., Calvo, B., Durinck, J., Ensor, K., Marine Ecology Progress Series, 296, 107–113. Follestad, A., Furness, R.W., Garthe, S., Leaper, G., doi: 10.3354/meps296107 Skov, H., Tasker, M.L. & Winter, C.J.N. (1995). Frings, H., Frings, M., Cox, B. & Peissner, L. (1955). Consumption of Discards by Seabirds in the Auditory and visual mechanisms in food-finding North Sea. Final Report EC DG XIV research behavior of the Herring Gull. The Wilson Bulletin, contract BIOECO/93/10, NIOZ rapport. 67(3), 155–170. Carter, D.O., Yellowlees, D. & Tibbett, M. (2007). Glover, A.G. Higgs, N.D., Bagley, P.M., Carlsson, R., Cadaver decomposition in terrestrial Davies, A.G., Kemp, K.M., Last, K.S., Norling, K., ecosystems. Die Naturwissenschaften, 94(1), 12– Rosenberg, R., Wallin, K., Kallstrom, B. & 24. doi: 10.1007/s00114-006-0159-1 Dahlgren, T.G. (2010). A live video observatory Catchpole, T.L., Frid, C.L.J. & Gray, T.S. (2006). reveals temporal processes at a shelf-depth Importance of discards from the English whale-fall. Cahiers de Biologie Marine, 51, 1–7. Nephrops norvegicus fishery in the North Sea to Grant, P.J. (1982). Gulls: a Guide to Identification., marine scavengers. Marine Ecology Progress Poyser, Calton. Series, 313, pp.215–226. doi: Gregory, R.D., Gibbons, D.W. & Donald, P.F., (2004). 10.3354/meps313215 Bird census and survey techniques. , 6(2002), Chongsuvivatwong, V. (2012). epicalc: 17–56. doi:

10.1093/acprof:oso/9780198520863.001.0001 African scavenging assemblage. Oikos, 124(10), Hamel, S., Killengreen, S.T., Henden, J.A., Eide, N.E., 1391–1403. doi: 10.1111/oik.02222 Roed-Eriksen, L., Ims, R.A. & Yoccoz, N.G. (2013). Monsarrat, S., Benhamou, S., Sarrazin, F., Bessa- Towards good practice guidance in using Gomes, C., Bouten, W. & Duriez, O. (2013). How camera-traps in ecology: Influence of sampling predictability of feeding patches affects home design on validity of ecological inferences. range and foraging habitat selection in avian Methods in Ecology and Evolution, 4(2), 105–113. social scavengers? PloS One, 8(1), e53077. doi: doi: 10.1111/j.2041-210x.2012.00262.x 10.1371/journal.pone.0053077 Heath, M.R., Cook, R.M., Cameron, A.I., Morris, D.J. & Moreno, P., Benke, H. & Lutter, S. (1992). Behaviour Speirs, D.C. (2014). Cascading ecological effects of Harbour (Phocoena phocoena) carcasses in the of eliminating fishery discards. Nature German Bight: surfacing rate, decomposition communications, 5. doi: 10.1038/ncomms4893 and drift routes. In: BohlkenH, BenkeH(eds) Heinrich, B. (1988). Winter foraging at carcasses by Untersuchungen über Bestand, three sympatric corvids, with emphasis on Gesundheitszustand und Wanderungen der recruitment by the raven, Corvus corax. Kleinwalpopulationen (Cetacea) in deu, Kiel. Behavioral Ecology and Sociobiology, 23(3), 141– Morton, B. & Yuen, W.Y. (2000). The feeding 156. doi: 10.1007/BF00300349 behaviour and competition for carrion between Hewson, R. (1995). Use of salmonid carcasses by two sympatric scavengers on a sandy shore in vertebrate scavengers. Journal of Zoology, Hong Kong: the gastropod, Nassarius festivus 235(1), 53–65. doi: 10.1111/j.1469- (Powys) and the hermit crab, Diogenes 7998.1995.tb05127.x edwardsii (De Haan). Journal of experimental Hobischak, N.R. & Anderson, G.S. (2002). Time of marine biology and ecology, 246(1), 1–29. submergence using aquatic invertebrate doi:10.1016/S0022-0981(99)00170-7 succession and decompositional changes. Journal Naylor, E. (1958). Tidal and diurnal rhythms of of Forensic Sciences, 47(1), 142–151. locomotory activit in Carcinus maenas (L.). Van den Hoff, J. & Newbery, K. (2006). Southern Journal of Experimental Biology, 35, 602–610. giant petrels Macronectes giganteus diving on Nevitt, G.A. (2000). Olfactory foraging by Antarctic submerged carrion. Marine Ornithology, 64, 61– procellariiform seabirds: life at high Reynolds 64. numbers. The Biological bulletin, 198(2), 245– Holden, P., Housden, S. & Burn, H. (2009). RSPB 53. handbook of Scottish birds., London: Christopher Nickell, T.D. & Moore, P.G. (1991). The behavioural Helm. ecology of epibenthic scavenging invertebrates Huang, Z.-P. Qi, X.-G., Garber, P., Jin, T., Guo, S.-T., Li, in the Clyde Sea area: field sampling using baited S. & Li, B.-G. (2014). The use of camera traps to traps. Cahiers de Biologie Marine, 32, 353-370. identify the set of scavengers preying on the Novak, M. (2004). Diurnal activity in a group of Gulf carcass of a golden snub-nosed monkey of Maine decapods. Crustaceana, 77(5), 603–620. (Rhinopithecus roxellana). PloS One, 9(2), doi: 10.1163/1568540041717975 e87318. doi: 10.1371/journal.pone.0087318 Parmenter, R.R. & Macmahon, J.A. (2009). Carrion JNCC (2010). Seabird Monitoring Programme decomposition and nutrient cycling in a semiarid Database. http://jncc.defra.gov.uk/page-1550. shrub-steppe ecosystem. Ecological Monographs, Jones, E.G., Collins, M.A., Bagley, P.M., Addison, S. & 79(4), 637–661. doi: 10.1890/08-0972.1 Priede, I.G. (1998). The fate of cetacean Pavés, H.J, Schlatter, R.P. & Espinoza, C.I. (2008). carcasses in the deep sea: observations on Scavenging and predation by Black Vultures consumption rates and succession of scavenging Coragyps atratus at a South American sea lion species in the abyssal north-east Atlantic Ocean. breeding colony. Vulture News, 58, pp.4–15. Proceedings of the Royal Society B: Biological Pereira, L.M., Owen-Smith, N. & Moleón, M. (2014). Sciences, 265, 1119–1127. doi: Facultative predation and scavenging by 10.1098/rspb.1998.0407. mammalian carnivores: seasonal, regional and Kuhn, B., Wiesel, I. & Skinner, J. (2008). Diet of intra-guild comparisons. Mammal Review, 44(1), brown hyaenas (Parahyaena brunnea) on the 44–55. doi: 10.1111/mam.12005 Namibian coast. Transactions of the Royal Society Petrik, M.S., Hobischak, N.R. & Anderson, G.S. of South Africa, 63(2), 1–8. (2004). Examination of factors surrounding Kulldorff, M., Heffernan, R., Hartman, J., Assunção, R. freshwater decomposition in death & Mostashari, F.A. (2005). A space-time investigations: a review of body recoveries and permutation scan statistic for the early detection coroner cases in British Columbia. Canadian of disease outbreaks. PLoS Medicine 2, 216–224. Society of Forensic Science Journal, 37, 9–17. Martin, P. & Bateson, P. (1993). Measuring behavior: Pihl, L. (1982). Food intake of young cod and An introductory guide Second., Cambridge, flounder in a shallow bay on the Swedish west England: Cambridge University Press. coast. Netherlands Journal of Sea Research, 15, Moleón, M., Sánchez-Zapata, J.A., Sebastián- 419–432. doi:10.1016/0077-7579(82)90068-0 González, E. & Owen-Smith, N. (2015). Carcass Polis, G.A., Anderson, W.B. & Holt, R.D. (1997). size shapes the structure and functioning of an Toward an integration of landscape and food

ecology: The Dynamics of Spatially Subsidized vertebrate scavengers must be large soaring Food Webs. Annual Review of Ecology and fliers. Journal of theoretical biology, 228(3), 431– Systematics, 28(1), 289–316. doi: 436. doi: 10.1016/j.jtbi.2004.02.005 10.1146/annurev.ecolsys.28.1.289 Schlacher, T.A., Strydom, S. & Connolly, R.M., 2013. Polis, G.A. & Hurd, S.D. (1996a). Allochthonous input Multiple scavengers respond rapidly to pulsed across habitats, subsidized consumers, and carrion resources at the land–ocean interface. apparent trophic cascades: examples from the Acta Oecologica, 48, 7–12. doi: ocean-land interface. In G.A. Polis & K. 10.1016/j.actao.2013.01.007 Winemiller, eds. Food Webs. Springer US, 275– SCOS (2013). Scientific Advice on Matters Related to 285. the Management of Seal Populations : 2013., Polis, G.A. & Hurd, S.D. (1996b). Linking Marine and p.155. Terrestrial Food Webs: Allochthonous Input Sebastián-González, E., Sánchez-Zapata, J.A., from the Ocean Supports High Secondary Donázar, J.A., Selva, N., Cortés-Avizanda, A., Productivity on Small Islands and Coastal Land Hiraldo, F., Blázquez, M., Botella, F. & Moleón, M. Communities. The American Naturalist, 147(3), (2013). Interactive effects of obligate scavengers 396–423. and scavenger community richness on Putman, R.J. (1983). Carrion and Dung: The lagomorph carcass consumption patterns R. Decomposition of Animal Wastes, Southampton, Fletcher, ed. Ibis, 155(4), 881–885. doi: The Camelot Press. 10.1890/15-0212.1 Ramsay, K., Kaiser, M.J., Moore, P.G. & Hughes, R.N. Sebastián-González, E., Moleón, M., Gibert, J.P., (1997). Consumption of fisheries discards by Botella, F., Mateo-Tomás, P., Olea, P.P., benthic scavengers: utilization of energy Guimarães Jr., P.R. & Sánchez-Zapata, J.A. (2016). subsidies in different marine habitats. Journal of Nested species-rich networks of scavenging Animal Ecology, 66, 884–896. doi: 10.2307/6004 vertebrates support high levels of interspecific Ramsay, K., Kaiser, M.J. & Hughes, R.N. (1998). competition. Ecology, 97(1), 95–105. doi: Responses of benthic scavengers to fishing 10.1111/ibi.12079 disturbance by towed gears in different habitats. Selva, N. Jędrzejewska, B., Jędrzejewski, W. & Journal of Experimental Marine Biology and Wajrak, A. (2005). Factors affecting carcass use Ecology, 224(1), 73–89. doi: 10.1016/S0022- by a guild of scavengers in European temperate 0981(97)00170-6 woodland. Canadian Journal of Zoology, 83, Reid, K. & Forcada, J. (2005). Causes of offspring 1590–1601. doi: 10.1139/z05-158 mortality in the Antarctic fur seal, Arctocephalus Selva, N. & Fortuna, M. (2007). The nested structure gazella: the interaction of density dependence of a scavenger community. Proceedings of the and ecosystem variability. Canadian Journal of Royal Society B: Biological Sciences, 274(1613), Zoology, 83, 604–609. doi: 10.1139/Z05-045 1101–1108. doi: 10.1098/rspb.2006.0232 Reisdorf, A.G., Bux, R., Wyler, D., Benecke, M., Klug, Skajaa, K., Fernö, A., Løkkeborg, S. & Eli, K.H. (1998). C., Maisch, M.W., Fornaro, P. & Wetzel, A. (2012). Basic movement pattern and chemo-oriented Float, explode or sink: postmortem fate of lung- search towards baited pots in edible crab breathing marine vertebrates. Palaeobiodiversity (Cancer pagurus L.). Developments in and Palaeoenvironments, 92(1), 67–81. doi: Hydrobiology, 130, 143–153. 10.1007/s12549-011-0067-z Smith, C.R. & Baco, A.R. (2003). Ecology of whale Rome, M.S. & Ellis, J.C. (2004). Foraging ecology and falls at the deep-sea floor. Oceanography and interactions between herring gulls and great marine biology, 41, 311–354. black-backed gulls in New England. Waterbirds, Smith, K. G.V. (1989). Handbooks for the 27(2), 00–210. Identification of British Insects: Diptera: An Ropes, J.W. (1968). The feeding habits of the green Introduction to the Immature Stages of British crab, Carcinus maenas (L.). Fishery Bulletin, Flies., Royal Entomological Society, London. 67(2), 183–203. Sorg, M.H., Dearborn, J.H., Monahan, E.I., Ryan, H.F., Rose, M.D. & Polis, G.A. (1998). The distribution and Sweeney, K.G. & David, E. (1997). Forensic abundance of coyotes: the effects of taphonomy in marine contexts. In: Haglund W.D., allochthonous food subsidies from the sea. Sorg M.H. (eds) Forensic taphonomy – The Ecology, 79(3), 998–1007. postmortem fate of human remains. CRC Press, Roth, J.D. (2002). Temporal variability in arctic fox Boca Raton, 567–604. diet as reflected in stable-carbon isotopes; the Summers, C.C., Burton, R.W. & Anderson, S.S. importance of sea ice. Oecologia, 133(1), 0–7. (1975). Grey seal (Halichoerus grypus) pup doi: 10.1007/s00442-002-1004-7 production at North Rona: a study of birth and Ruxton, G.D. & Bailey, D.M. (2005). Searching speeds survival statistics collected in 1972. Journal of and the energetic feasibility of an obligate Zoology, 439–451. whale-scavenging fish. Deep Sea Research Part I: Teather, R.G., 1994. Encyclopedia of Underwater Oceanographic Research Papers, 52(8), 1536– Investigations., Best Publishing Company, 1541. doi: 10.1016/j.dsr.2005.02.008 Flagstaff, Arizona, AZ. Ruxton, G.D. & Houston, D.C. (2004). Obligate Thomas, L. & Harwood, J. (2005). Estimating the

size of the UK grey seal population between 1984 and 2004: model selection, survey effort and sensitivity to priors. SCOS Briefing Paper 05/3. Torsten, H., Bretz, F. & Peter, W. (2008). Simultaneous Inference in General Parametric Models. Biometrical Journal, 50(3), 346–363. doi: 10.1002/bimj.200810425 Tran, M.V., O’Grady, M., Colborn, J., Van Ness, K. & Hill, R.W. (2014). Aggression and food resource competition between sympatric hermit crab species. PloS One, 9(3), e91823. doi: 10.1371/journal.pone.0091823 Van den Hoff, J. & Newbery, K. (2006). Southern giant petrels Macronectes giganteus diving on submerged carrion. Marine Ornithology 64:61– 64. Venables, W.N. & Ripley, B.D. (2002). Modern Applied Statistics with S. Fourth Edi., Springer, New York. Wieczorek, S.K., Campagnuolo, S., Moore, P.G., Froglia, C., Atkinson, R.J.A., Gramitto, E.M. & Bailey, N. (1999). The composition and fate of discards from Nephrops trawling in Scottish and Italian waters. Final report to the EC (96/092)., Millport. Wilson, E.E. & Wolkovich, E.M. (2011). Scavenging: How carnivores and carrion structure communities. Trends in Ecology and Evolution, 26(3), 129–135. Young, A., Stillman, R., Smith, M.J. & Korstjens, A.H. (2014). An experimental study of vertebrate scavenging behavior in a northwest European woodland context. Journal of Forensic Sciences, 59(5), 1333–1342. doi: 10.1111/1556- 4029.1246 Zuur A.F., Ieno E.N., Walker N.J., Saveliev A.A. & Smith G.M. (2009). Mixed effects models and extensions in ecology with R. Springer New York. Zuur, A.F., Ieno, E.N. & Elphick, C.S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1(1), 3–14. doi: 10.1111/j.2041- 210X.2009.00001.

Appendix 1. Times of bad visibility during the underwater experiment.

Period 1 Period 2 Date Time Date Time 02/08 05:00 / 08:50 17/09 23:40 02/08 22:30 18/09 02:20 03/08 04:40 / 07:10 18/09 03:30 03/08 22:50 18/09 20:50 / 21:30 04/08 01:10 19/09 00:30 04/08 03:30 19/09 05:20 04/08 23:30 19/09 21:50 / 22:00 05/08 01:20 / 01:40 19/09 22:30 / 23:20 05/08 02:20 20/09 00:00 / 00:20 05/08 13:20 20/09 04:00 / 04:20 05/08 22:40 / 23:40 20/09 - 21/09 14:40 / 14:00 06/08 00:00 21/09 21:30 06/08 00:50 / 01:20 23/09 03:20 06/08 02:40 24/09 02:40 / 03:00 06/08 03:30 24/09 05:30 06/08 04:00 / 04:20 25/09 00:50 06/08 23:10 25/09 04:10 /04:20 06/08 23:40 25/09 05:40 07/08 02:00 07/08 04:.30 07/08 23:00 08/08 01:20 08/08 02:00 / 02:20 09/08 04:30 10/08 02:00 10/08 02:40 / 02:50 10/08 05:00 / 05:10 11/08 00:00 / 00:20 11/08 02:40 11/08 23:00 12/08 14:00 / 15:00 13/08 01:00 13/08 01:50 / 02:10 14/08 12:00 14/08 20:00 / 23:00 15/08 03:10 / 03:30

Appendix 2. Terrestrial experiment: summary of results obtained by individual negative binomial GLMs for each group of birds. Count of bird passages (GBBG = great black-backed gull, HG = herring gull, LBBG = lesser black-backed gull, JUV = juveniles gulls) undertaken at the study and control sites both before (Period 1) and after (Period 2) the deployment of a single grey seal pup carcass. Formula = Log (Total Number of Bird Passages) ~ Tide + Time of the day + Area : Period.

GBBG (likelihood ratio test: Χ2 (df = 3) = 25.98, P < 0.001) Estimate Std. Error Z value Pr (>|z|) Intercept -2.3401 0.8343 -2.805 0.0050 Tide - Low 0.5789 0.2818 2.055 0.0399 Area - Study 1.2523 0.2951 4.244 < 0.0001 Period - 2 1.4395 0.4120 3.494 0.0005 HG (likelihood ratio test: Χ2 (df = 4) = 15.54, P = 0.0037) Estimate Std. Error Z value Pr (>|z|) Intercept 3.8625 0.6382 6.052 < 0.0001 Tide - Low 0.8318 0.2191 3.797 0.0001 Area - Study -1.1621 0.8955 -1.298 0.1944 Period – 2 -0.7410 0.3554 -2.085 0.0371 Area – Study : Period - 2 0.7798 0.4988 1.563 0.1180

LBBG (likelihood ratio test: Χ2 (df = 3) = 4.32, P = 0.2290) Estimate Std. Error Z value Pr (>|z|) Intercept 4.9236 0.7949 6.194 < 0.0001 Area - Study -2.0490 1.1334 -1.808 0.0706 Period – 2 -0.8293 0.4459 -1.860 0.0629 Area – Study : Period - 2 1.1116 0.6317 1.760 0.0785 JUV (likelihood ratio test: Χ2 (df = 1) = 2.51, P = 0.1130) Estimate Std. Error Z value Pr (>|z|) Intercept 3.8410 0.2253 17.0510 < 0.0001 Area - Study -0.4921 0.3055 -1.6110 0.1070

Appendix 3. Underwater experiment: summary of results obtained by individual Poisson GLMs for each taxonomic class. Maximum number of individuals (MaxN) observed for the classes Asteroidea (starfish), Actinopterygii (fish) and Malacostraca (crabs) in the Periods of monitoring (1 and 2) at day and night time. Formula = Log (MaxN) ~ Period + Time of the Day + Period : Time of the day.

Asteroidea (likelihood ratio test: Χ2 (df = 1) = 167.4, P < 0.0001) Estimate Std. Error Z value Pr (>|z|) Intercept 2.4011 0.0570 42.208 < 0.0001 Period - 2 -2.2760 0.2491 -9.136 < 0.0001 Actinopterygii (likelihood ratio test: Χ2 (df = 2) = 101.88 , P = < 0.0001) Estimate Std. Error Z value Pr (>|z|) Intercept 2.5087 0.0744 33.722 < 0.0001 Period – 2 -1.1602 0.1665 -6.967 < 0.0001 Time of the day - Night -0.7174 0.1230 -5.831 < 0.0001

Malacostraca (likelihood ratio test: null) Estimate Std. Error Z value Pr (>|z|) Intercept 0.3659 0.1270 2.881 0.0040