Discussion

In the first two VENUS studies, the carcass biomass was removed through animal activity rather than classic decomposition. In contrast, in the shallower experiments, biomass loss was partially due to animal activity, but was primarily due to natural decomposition. In the shallower experiments, the carcasses floated when

Fig. 12.38 Day 92, 2008. Rapid oxygen renewal in Saanich Inlet resulted in large numbers of fish repopulating the area (VENUS Project, University of Victoria)

Fig. 12.39 Day 106, 2008. Large numbers of Pandalus platyceros on carcass. Note large grazed areas on shoulder and legs (VENUS Project, University of Victoria)

first placed, then sank and later refloated (Anderson and Hobischak 2004, 2002). Whether a body will refloat depends on many factors including but not limited to; timing and type of last meal, water temperature, depth, body mass index and health of the individual and is, therefore, very variable (Teather 1994). Bodies that come to rest below 61 m (200 ft) are not expected to refloat, as cold temperatures and high pressure reduce the volume of gases and also make the gases very soluble in water and tissues (Teather 1994). Therefore, flotation and reflotation were not expected in the deeper studies. In the first two VENUS studies, bacterial decomposition was not seen and no visible signs of adipocere formation or tissue degradation were observed other than that created by animals, although a bacterial mat did start to form on the bones of the second carcass just before recovery. In the third VENUS study, a bacterial mat was seen to form over the entire carcass. In the shallower experiments, tidal action and currents impacted the remains and would have resulted in their removal had they not been tethered. At 94 and 99 m, there was little impact of tides or currents so movement of the carcasses was entirely due to animal action.

Dissolved oxygen levels in the water can have a major impact on the fauna attracted to a carcass. Levels of dissolved oxygen were not directly measured in the shallow experiments in Howe Sound, however, these shallow waters are, in general much more highly oxygenated that that of the Saanich Inlet, where the deeper carcasses were deployed. It is probable that the dissolved oxygen levels at the shallower research sites were at or above 5 mL/L (Tunnicliffe 2006). The Saanich Inlet has restricted water circulation due to a submerged sill at its mouth. The anoxic basin is only flushed when water above the sill is dense enough to run into it, so for much of the year, the basin is anoxic (Jamieson and Pikitch 1988; Tunnicliffe 1981; Anderson and Devol 1973).

The levels of dissolved oxygen in all the deeper coastal studies were low. Levels below 2.0 mL/L are considered hypoxic, with levels below 1.0 mL/L being stressful for most animals (Diaz and Rosenburg 1995). In 2006, the dissolved oxygen levels were hypoxic after the first few days but did not drop below 1 mL/L until part way through the study. In 2007, oxygen remained below 1 mL/L for most of the study. Nevertheless, this did not discourage the fauna, although when oxygen was very low, M. quadrispina were the main and sometimes the only invertebrates present (Peters 2007). As the Saanich Inlet is regularly hypoxic at this depth, it is probable that many of the local species are adapted to these conditions (Tunnicliffe 1981). In the Saanich Inlet, Tunnicliffe has reported that even when dissolved oxygen is below 1.0 mL/L the zone between 85 and 100 m did not exhibit low diversity or small populations (Tunnicliffe 1981). Also, although crustaceans are in general not tolerant of hypoxic conditions, M. quadrispina are an exception, being present in conditions below 0.2 mL/L (Peters 2007; Burd and Brinkhurst 1985; Farrow et al. 1983). The lack of species diversity may reflect the hypoxic conditions. It does not reflect depth as great faunal diversity can be seen at much greater depths on whale falls (Kemp et al. 2006; Baco and Smith 2003; Smith and Baco 2003; Smith et al. 1989). It was clearly seen that M. quadrispina was less affected by the hypoxic conditions, but even C. magister was commonly seen on the remains despite very low oxygen levels. Many decapod crustacea, including Cancer magister, are capable of surviving for periods of time in acute hypoxic conditions by employing various physiological mechanisms to cope with low oxygen (Bernatis et al. 2007). These include increasing the ventilation of the branchial chambers, exhibiting brachycardia, and altering blood flow, directing blood to tissues requiring more oxygen (Bernatis et al. 2007). They have also been shown to exhibit differing behavioural responses to hypoxic conditions such as entering hypoxic conditions to obtain food but moving the food to a more oxygen rich environment to feed

(Bernatis et al. 2007). However, in these studies, the same crabs, identified by barnacle pattern on their carapace, stayed to feed for days on the carcass, ripping and eating tissue in situ. Bernatis and colleagues' study show that well fed crabs moved to higher oxygen levels and remained at that site for 48 h (Bernatis et al. 2007), however, crabs in these studies were clearly very well fed but remained at the carcass until little remained or oxygen dropped too low.

In the first two VENUS studies, the carcass was deployed when oxygen was at an acceptable level for the three dominant arthropod species. However, the third carcass was deployed when oxygen levels were very low. In such conditions, Cancer magister and Pandalus platyceros were unable to access the carcass and although low numbers of Munida quadrispina were able to reach the carcass, they were unable to break the skin. This left the carcass intact for months until the oxygen levels increased. Clearly, the larger arthropods are required to break the pig skin. As pig skin is so similar to that of humans, it is likely that the same would occur with a human body. In this particular habitat, oxygen was a major driving force for decomposition and animal feeding. In the low oxygen environment, decomposition produced hydrogen sulphide (Herlinveaux 1962).

Temperature can obviously impact both decomposition and faunal colonization (Simpson and Knight 1985; Spitz 1980; Fisher and Petty 1977; Jaffe 1976; Picton 1971; Mant 1960). Temperature was not continuously measured in the earlier experiments as it was during the VENUS studies, but was measured during dives. In the shallow experiments, temperatures ranged from 6-10°C, whereas they held very constant at 9.4-9.8°C during the VENUS studies, except for a 1°C drop in the latter part of the third study. As these temperatures are considered reasonably warm and were very similar, it is unlikely that temperature was a major variable.

The most obvious faunal differences between the experiments at 7.6 and 15.2 m and those done at 94 and 99 m are that, at the greater depths, there was much less species diversity but many more actual animals feeding on the remains. At 94 m, the tissue was lost almost entirely to animal feeding rather than decomposition, with carcasses reduced to bones in a matter of weeks. This is much more in line with the personal experience of public safety divers (MacFarlane 2001; Teather 2000). In the deeper studies, the carcass was dominated by just three species of large crustacean: C. magister, M. quadrispina and P. platyceros, with M. quadrispina the most common, being present in 85.7% of the photographs taken in the 2006 study (Peters 2007). Even during the very low oxygen study, the majority of the fauna were still M. quadrispina, C. magister and P. platyceros.

In the Saanich Inlet, Munida quadrispina are endemic but occurred in much greater numbers in the presence of a carcass (Peters 2007). Cancer magister and P. platyceros were not commonly seen on the sea floor prior to the carcass deposition so were directly attracted, although they are endemic to the area. Pandalus platyceros is the largest species of shrimp in British Columbia and is usually associated with rocky terrain, although the VENUS studies were all conducted on a substrate consisting of a rock base, thickly covered in a light silt.

Pandalus platyceros is commonly found in the Saanich Inlet, with greatest densities at a depth of 70-85 m (Jamieson and Pikitch 1988). These animals were all actively attracted to the carcass immediately after deposition. It is believed that most animals detect a carcass using chemoreception, although more recent work on Pandalus sp. has shown that hydroacoustic stimuli may also be important, either detecting the carcass fall itself, or the feeding activity of other crustacea (Klages et al. 2002). In this case, it may also be the sound of ROPOS as it deposited the carcass. A much greater diversity of fauna were seen on the shallower carcasses, and these fauna were not limited to crustacea but rather included many invertebrate phyla and families. However, the actual number of organisms was low. Invertebrates were clearly attracted to the remains, and invertebrates could be seen moving actively towards the carcasses in both sets of experiments. Although it was not possible to tell whether there was a turnover in the specimens of M. quadrispina and P. platyceros, some of the specimens of C. magister were quite distinctive due to the barnacles adhering to their carapaces. Therefore, it was possible to tell that much of the time, the same crabs were returning to the carcass, or perhaps not leaving the vicinity at all.

A fourth crustacea, the sea louse, Orchomenella obtusa was seen on the deeper carcasses in small numbers in 2006 and very large numbers in 2007. Species in this genus have been known to eat large pieces of seal meat bait in less than 24 h and were reported to be collected by the "bucketful" in experiments in the McMurdo Sound area of the Ross Sea in Antarctica (Dearborn 1967 cited in Sorg et al. 1997, p 572). Fish caught in the traps were frequently eaten alive by the time the traps were checked. The temperature of the water in the McMurdo Sound averaged -1.8°C so these amphipods can clearly survive such cold temperatures (Sorg et al. 1997). They have been reported as being common in the Saanich Inlet at depths of 80-210 m and were found in large swarms on dead and dying prawns in a mass anoxic fatality (Jamieson and Pikitch 1988). Orchomenella obtusa is in the Family Lysianassidae which are commonly referred to as "sea lice". Teather reported that crustacea, in particular sea lice, have been known to remove almost all the tissue from a body in less than 12 h in some situations, and to commonly partially skeletonize a body in less than a week (Teather 1994). The actual conditions in which this rapid skeletonization occurred were not mentioned, but the majority of Teather's case histories come from British Columbia waters. In the present studies, large numbers of small amphipods were only seen in the 2007 VENUS pig, with smaller numbers seen briefly on the 2006 carcass. These were also not in the numbers described by Teather, who reported that the body could be almost completely obscured by the small shrimp, and that they could become a hazard to the public safety diver when they recover the body, by causing panic (Teather 1994). As well, Teather reported their arrival on humans within 24 h of submergence (Teather 1994) and lysianassid amphipods were found on deployed cetacean carcasses within an hour of deployment (Jones et al. 1998). In the present studies, small unidentified amphipods were seen on the shallow carcasses within 24 h, although not in great numbers and O. obtusa was not seen until Day 11 and Day 14 respectively on the deeper carcasses.

In the shallow carcasses, the remains were not skeletonized for many weeks whereas the first two deeper carcasses were skeletonized in less than a month. This is more in line with other studies that suggest that skeletonization usually occurs within a month (Sorg et al. 1997; Teather 1994), although soft tissue can persist for a year or more in certain situations (Sorg et al. 1997). Sorg and colleagues report that cartilage loss was observed in one human case at 10 months but was found in some cases up to 18 months after submergence (Sorg et al. 1997). In these studies, cartilage was removed by Day 42 when oxygen levels were acceptable. A case report from 1987 in waters very close to the VENUS experiments showed that a human body could be at least partially skeletonized with disarticulation of the mandible within 3 weeks of death in these waters (Skinner et al. 1988). This report referred to the historic cases of Rex v. Sowash and Rex v. Charles King in which two men in 1924 (during American prohibition) were murdered near Vancouver Island, for the liquor they were carrying. Their bodies were weighted down and dropped in the ocean at a depth of approximately 30 m (Skinner et al. 1988). The bodies were not recovered despite extensive searches. As no case at that time had been won in Canada without the corpus delecti, prosecuting counsel decided to conduct an experiment to prove that the remains would have been lost within weeks of death, so could not have been expected to be recovered. A quarter of beef was weighted and sunk in the same waters and retrieved after 1 month. The beef had been reduced to bones in that time by crabs and amphipods. This was used in the case to show that the failure of the police to find the bodies was "comparatively immaterial" (p141) and the defendants were convicted (Skinner et al. 1988).

The vertebrate that removed a large piece of the carcass on Day 2 in the first study and half the carcass on Day 18 in the second study is unknown, but suspected to be Hexanchus griseus. This is a deep water shark normally feeding primarily on cartilaginous and bony fish (Ebert 1986) although it has also been known to eat marine mammals and invertebrates (Wheeler 1975; Hart 1973, cited by Ebert 1986). This shark rests in deep waters during the day and swims to shallower waters at night to feed (Dumser and Turkay 2008). In a human case, H. griseus was seen near the remains, but did not bite it (Dumser and Turkay 2008). In this case, the shark may have been attracted by the large numbers of invertebrates or may have merely been 'tasting'. In both cases, it did not come back to finish the carcass but rather seemed to take a single swipe at it, then leave it alone. Sharks and rays are considered to be first-order scavengers of human bodies in coastal waters (Rathbun and Rathbun 1997; Sorg et al. 1997).

Prior to the large piece of tissue removal from the first VENUS carcass, C. magister, M. quadrispina and P. platyceros were attracted to the carcass and were found picking at the orifices, skin and silt on the remains, with no one area being more attractive than another. Once the large piece of tissue was removed, the focus of all the scavengers was at the bite site and this continued throughout the duration of the study, with very little attention paid to the head or front half of the animal. In the second VENUS carcass study, despite a head wound, the abdominal area was the most attractive, being opened up by Cancer magister very rapidly. This became the focus of subsequent feeding, with again, little activity at the head.

Although few faunal studies have been done on human bodies, or on human models such as pigs in the marine environment, whale carcass communities, or whale falls have been studied sporadically for over 150 years (Smith and Baco 2003). In the past, the accidental discovery of a whale carcass provided a rich opportunity to study the ecology of a very large ephemeral pulse of organic material (Smith and Baco 2003). More recently, carcasses of a variety of cetaceans have been deliberately deployed for study ( e.g. Kemp et al. 2006; Witte 1999; Jones et al. 1998).

Such extremely large carcasses (up to 160 t adult body weight (Smith and Baco 2003)) are very different from that of a human and most whale studies have been conducted at depths much greater than the experiments presented here e.g. 4,0004,800 m (Jones et al. 1998). However, whale falls do provide information that is valuable in understanding the ecology and community structure that builds in relation to a sudden input of nutrients in the ocean. Smith and Baco state that bathyal (pelagic zone 1,000-4,000 m below surface) carcasses provide a massive amount of nutrients to the deep sea floor, with the organic carbon in a 40 t whale being equal to that which normally sinks from the "euphotic zone to a hectare of abyssal sea floor over 100-200 years" (Smith and Baco 2003, p312). Smith and Baco have divided the decomposition and succession process on whale falls into four stages (2003). The first is the "mobile scavenger stage" (p 318) during which great numbers of large scavengers remove the soft tissue. These scavengers include sharks, hagfish and invertebrates. This stage can last for several months up to 18 months and in itself contains a temporal succession (Smith and Baco 2003). The increased macrofauna in the vicinity of experimentally placed whale falls had an inverse relationship with the abundance of nematodes in the sediment for at least 30 m from the carcass, although after 18 months, nematode abundance increased, probably due to increased nutrient levels in the sediment (Debenham et al. 2004). The second stage is that of the "enrichment opportunist stage" (Smith and Baco 2003, p 319) which can last for months and up to years, where large aggregations of heterotrophic macrofauna colonize the now enriched sediments and the bones. The third stage is the "sulphophilic stage" (p 322) which lasts decades. Here, a chemoautotrophic assemblage colonize, as the bones anaerobically produce sulphide during sulphate reduction (Smith and Baco 2003). Those organisms that are able to tolerate sulphur proliferate, including chemoauto-trophic and heterotrophic bacteria, some isopods and Galatheid crabs, mytilids, dor-villeid polychaetes, cocculinid limpets, provannid gastropods and columbellid snails, as well as others (Smith and Baco 2003). This is very similar to the fauna found at hot vents (Smith et al. 1989). The final stage is the "reef stage" (p 325) which occurs after the organic material has been removed and only mineral material remains. At this time, the remains would be colonized by suspension feeders (Smith and Baco 2003). In the present experiments, due to the much smaller carcasses and the short time of observation, only the mobile scavenger stage was observed, although other stages may well have occurred as sediment below and around the carcass was not sampled and examined. The low oxygen environment of the thuird VENUS carcass study may have been similar to the sulphophilic stage. In further experiments, it would be interesting to examine the bones and sediment for a longer time period.

It has been suggested that sessile marine life such as barnacles and bryozoans could be excellent indicators of elapsed time since submergence (Sorg et al. 1997). Such animals do tend to grow at predictable rates and could be useful in estimating the time that has elapsed since the remains were skeletonized. They have been used in some human cases (Dennison et al. 2004; Sorg et al. 1997; Skinner et al. 1988), although caution must be exercised as growth rates vary with quantity and quality of food as well as water temperature and other physical parameters (Sorg et al. 1997; Bertness et al. 1991). In the first VENUS study, the carcass was removed from camera range within 3 weeks of submergence and no bones were recovered but in the second, the bones were recovered 5 months after submergence and no sessile organisms were found to be attached to them. This was, perhaps, too short a time to assess encrustation by sessile organisms. However, in the shallower studies, the carcasses were observed for some months post submergence, and very few such organisms were recovered from the bones. On Day 47 in the shallow spring experiments, a barnacle appeared to have settled in the left eye but was gone, possibly scavenged, by the next sampling time. Barnacles did settle on a tag used to restrain a carcass at Day 225 in the fall experiment, and mussels were seen in the area but not on the remains, with mussel beds developing nearby (Anderson and Hobischak 2002). Some mollusks were found attached to the bones at final collection (Table 12.4) but these were only observed many months after death. Therefore, the value of sessile organisms may be limited to the later postmortem interval.

When a body is recovered from the water, the remains often exhibit abrasions and other damage. It is important to understand whether this trauma was caused pre or peri-mortem versus post-mortem, as this may have a bearing on the manner of death (Stubblefield 1999). If such trauma can be explained by animal activity, then valuable investigative time is not wasted, and the presence of the post-mortem trauma may help to explain where the remains have been in the water, i.e. depth or habitat. In these studies, marks on the soft tissue by a number of animals were observed and could be mistaken for ante-mortem wounds if not studied carefully. Circular grazed areas were seen here and similar shallow oval or circular holes approximately 10-20 or more mm in diameter were seen in the skin of drowning victims, believed to be caused by crabs in the Japan Sea (Koseki and Yamanouchi 1963) Such trauma has also been seen on hard tissue causing crater-like defects (Sorg et al. 1997; Mottonen and Nuutila 1977).

Bodies are frequently recovered a considerable distance from where they went into the water and taphonomic information may be valuable in determining where the body went into the water and what conditions it has been exposed to in the time of submergence. Sorg et al. relate a case in which human remains were found 4 weeks after death in the clam flats where the Damariscotta River enters the Gulf of Maine (Sorg et al. 1997). The question was whether the remains had entered the water up river or from the ocean. Marine shell fragments and a single spine from the green sea urchin, Strongylocentrotus droebachiensis, indicated that the remains originated from the estuary or the ocean but were unlikely to have come from the river (Sorg et al. 1997). In another case, human remains were recovered after 32 years submergence but the condition of the body suggested that the upper and lower halves of the body had been in different environments. The lower body showed little signs of erosion damage, but the upper body exhibited extensive erosion. As well, the upper body showed signs of having been in a well oxygenated environment, with octopus eggs in the clothing, while the lower body exhibited evidence of an anoxic environment. The authors' conclusions were that the remains had been partially buried in the sand (Sorg et al. 1997). These cases illustrate the possibility of determining the conditions under which the body has been by interpreting faunal activity and decompositional changes.

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