macroscopic taphonomic alterations to human … taphonomic alterations to human bone recovered from...

Journal of Forensic Identification65 (6), 2015 \ 953

1 Office of the Chief Medical Examiner and Boston University School of Medicine, Boston, MA

2 Plymouth University Marine Institute, Drake Circus, Plymouth, U.K.

Received March 9, 2015; accepted June 12, 2015

Article

Macroscopic Taphonomic Alterations to Human Bone Recovered from Marine Environments

James T. Pokines 1 Nicholas Higgs 2

Abstract: The present research examines a sample (n=25) of human bone cases that were recovered from the shoreline or ocean waters near Massachusetts, United States, and submitted for analysis to the Office of the Chief Medical Examiner, Boston. All macroscopic taphonomic changes resulting from the physical and biological effects of extended marine immersion were compiled and compared to taphonomic altera-tions from other environments. Multiple taphonomic characteristics were prevalent after extended marine immersion, including battering and rounding (96.0% of cases) and bleaching (88.0%), with adher-ence by marine species of mollusks (8.0%), barnacles (36.0%), and Bryozoans (4.0%), or, in some cases, surface alterations to bone by these adhering taxa. Other common changes included adipocere for-mation (20.0%); reddish (24.0%) or dark (12.0%) mineral staining; and adhering sand (52.0%), silt (8.0%), or algae and seaweed (36.0%). Bone condition (disregarding bleaching or staining) included still greasy because of leaching fat (32.0%), retaining an organic sheen (44.0%), or a chalky appearance (24.0%). Multiple traits may be used to distinguish a marine environment as the origin of unknown osseous remains from other common forensic sources, including terrestrial surface decomposition and weathering or buried remains.

IntroductionThe forensic analysis of human remains recovered from

marine environments is a relatively common occurrence in medical examiner settings in coastal regions because of the high

Journal of Forensic Identification954 / 65 (6), 2015

frequency at which bodies or portions of bodies are introduced into this environment and are later discovered and reported to law enforcement. The manners in which human remains get introduced into marine contexts include deaths at sea from homicide, suicide, and accidents [1–6]. Disasters at sea, including shipwrecks and airplane crashes, may introduce large numbers of bodies, or parts thereof, at one time [4, 7–11]. Although rare, instances of shark or other marine animal predation upon humans may introduce partial remains after feeding [12–22]. Human remains from burials at sea also may be discovered later [23], and the original method of disposal may not be immediately clear. Oceans can also be used for remains disposal after an individual has been killed on land [5], and these bodies may be deposited whole or dismembered. Similarly, river systems may transport remains for great distances, including into the ocean [24–30], especially in cases where suicides or accidental falls from bridges have occurred near coastal margins [4, 5]. These marine remains are often found f loating or accidentally snagged in f ishing nets or scallop dredges, whole or in parts, and are forwarded to a medical examiner for analysis and identification [31].

Coastal margins are also a common source of human (and nonhuman) remains because of their spatial attributes [6, 32, 33]. The shoreline presents a significant barrier to further marine transport of bodies, or portions thereof, as these remains are moved by ocean currents or wave action. Tidal f luctuations also allow remains to be deposited above the water line, thus increasing their chances for discovery. Shore areas attract large numbers of people into an area normally devoid of significant plant cover, making remains deposited here much easier to spot than in many other terrestrial environments (forests, grasslands, etc.). Adhering soft tissue may attract large numbers of avian and terrestrial scavengers, thus making decomposing remains easier to locate. Coastal waters, including estuaries and harbors, are often high-traffic areas, and human remains f loating in such shallow environments have an increased chance of being spotted relative to those f loating in open ocean waters. Shorelines thus create an intersection of often intense human activity with a natural barrier to fur ther remains transport, thereby concentrating human remains from marine environments in one small strip of land.


Multiple researchers have examined the question of decom-position, scavenging, and transport of whole bodies in marine environments [34–37] and how these processes differ in their taphonomic effects and timing from related processes in terres-trial environments. Marine environments present an entirely different range of physical conditions and scavenging fauna than do terrestrial environments, and these marine environments are in turn highly variable based upon local conditions, including water depth and temperature, current, oxygenation, salinity, season, local faunal community, and duration of exposure [31]. The present research examines the taphonomic alterations to human bone recovered from marine environments in comparison with taphonomic alterations common to other forensic contexts (e.g., terrestrial surface decomposition, terrestrial burials, and cultural modification). The taphonomic characteristics include those caused directly to the bones themselves (such as round-ing, battering, bleaching, and mineral staining), general bone condition, adhering sediments and biological organisms, and the traces that the latter leave on bone even after they have been removed. Examination of all taphonomic changes, includ-ing how they form and how they differ in patterning from those caused by other environments, is crucial toward understanding the depositional environment of the remains and determining this environment in cases where the context is unknown. It is also necessary to differentiate all kinds of natural taphonomic changes from those potentially caused by humans, including perimortem trauma. A full analysis of all taphonomic changes therefore should be included in any complete forensic analysis of human remains.

SampleThe present sample (n=25) comes from cases turned in to the

Office of the Chief Medical Examiner, Boston, Massachusetts, from the period 1993 to 2015. All cases were recovered from the shoreline of, or ocean near, this state, including some remains accidentally captured in fishing nets. All remains were consis-tent in development with an adult or at least an older juvenile (i.e., adult size and with fully fused epiphyses where present). Skeletal representation (Table 1) favored isolated postcranial elements, with tibiae (n=4), femora (n=6), and a single innomi-nate comprising 44.0% of the sample. A par tial postcranial skeleton was represented primarily by the pelvis, leg, and foot elements, and an additional partial skeleton had a similar


postcranial inventory plus a cranium. One of these two cases was found after it washed ashore, and the other was caught in a fishing net far offshore in water of an unknown depth. Isolated partial cranial vaults (n=7) comprised 28.0% of the sample, with one additional partial cranial vault associated with cervi-cal vertebrae 1 through 3. Two mostly complete crania and two mandibles (one mostly complete, the other partial) comprised a further 16.0% of the sample.

Portions Present n %Tibia 4 16.0Femur 6 24.0Innominate 1 4.0Partial postcranial 1 4.0Cranium, partial postcranial 1 4.0

Partial vault 7 28.0Partial vault, C1-3 1 4.0Cranium 2 8.0Mandible 2 8.0

Table 1Skeletal representation (n=25 cases).

Taphonomic CharacteristicsGeneral bone preservat ion was var iable (Table 2) and

likely dependent upon the duration of marine immersion and other factors, which may include degree of scavenging, water temperature, distance of transport, exposure to high-energy environments, type of substrate, and amount of time buried in sediment. In three cases (12.0%), decomposing soft tissue was still present. These cases included the two partial skeletons discussed previously, both of which retained some articulation of largely def leshed elements. Both partial skeletons included well-preserved, intact feet (Figure 1) contained within footwear that restricted access to macroscavengers. The single case of a partial cranial vault with vertebrae C1 through 3 articulated also retained some soft tissue. Including these aforementioned three cases with soft tissue present, a total of eight cases (32.0%) had visible fat content leaching from the bones (Figure 2). The presence of fat leaching did not, however, preclude significant bleaching and erosion of other portions of the same bone. A further 11 cases (44.0%) lacked leaching fat but retained visible sheen from their remaining organic content, primarily bone collagen (Figure 3). A further six cases (24%) had been degraded


further and presented no residual organic sheen; instead, all exposed bone surfaces were dull and chalky (Figure 4). At least in part, this chalkiness may have been caused by the crystal-lization of absorbed marine mineral salts on the bone surfaces, but this chalky texture was similar to bones from terrestrial environments that have undergone signif icant loss of organic content or surface erosion, such as bones that have undergone long-term burial. Bleaching was observed, however, even in bones that were still wet and could not have been yet affected by this potential source of apparent color lightening (surface crystallization of pale minerals).

Characteristic n %Soft tissue also present 3 12.0Bone condition Chalky 6 24.0 Organic sheen 11 44.0 Fat Leaching 8 32.0Adipocere 5 20.0Battering/rounding 24 96.0Windowing 5 20.0Bleaching 22 88.0Mineral staining Reddish 6 24.0 Dark 3 12.0Adhering Sediments Adhering sand 13 52.0 Adhering silt 2 8.0Adhering Taxa Mollusks 2 8.0 Mollusk scars 4 16.0 Barnacles 9 36.0 Barnacle scars 1 4.0 Other crustacean 1 4.0 Algae (all types) 9 36.0 Bryozoa 1 4.0

Table 2Taphonomic characteristics of marine remains (n=25 cases).


Figure 1Pair of feet recovered mostly intact from footwear, associated with

largely skeletonized remains that were not protected (upon recovery).

Figure 2Fat leaching (arrow) from the distal epiphysis of a femur. Note also

the bleaching to the remainder of the bone.


Figure 3Organic sheen on a partial cranial vault. Note also the beginning

overall bleaching and battering of the vault surface.

Figure 4Cranium displaying chalky surface texture after marine immersion. Note also the bleaching and extensive battering to the facial area.


Five cases (20.0%), independent of any leaching grease, displayed traces of adipocere, a pale, crumbly, soaplike substance composed of hydrated body fats that forms in moist, anaerobic conditions and is promoted by the presence of the bacterium Clostridium [38, 39]. This process is also termed saponification, and it is slowed but not halted in colder environments [40]. Adipocere adhered to the bone in two cases, and in another three cases, it was visible embedded in exposed cancellous bone (Figure 5). In this partially enclosed space, the adipocere is largely protected from surface erosion through abrasion and therefore may persist for long periods in this environment [39]. This gradual loss of fat and other organic content paralleled other degradation to the bone. The cold North Atlantic Ocean near Massachusetts therefore may be conducive to slow adipocere formation [40] and its long-term persistence in marine cases, if low temperatures are a factor in its persistence after formation.

Figure 5Adipocere in cancellous bone that has been exposed by abrasion and

rounding of the cortical bone of a proximal femur.


Physical Changes to Bone

Sediment and Substrate AbrasionCoastal marine environments may have highly energetic water

movement and therefore can tumble any mobile objects through an abrasive (sandy or gravelly) substrate. This overall process batters and abrades bone, giving it a characteristic rounding of exposed margins [41–43]. This process also may create holes or expand existing anatomical structures (i.e., foramina) in a process termed windowing. As battering and rounding progress, areas of cancellous bone are exposed frequently. The ocean bottom and margin also often have sharp, immobile rocks against which items may be impacted. This type of surface scoring can be oriented randomly, although parallel scores can be formed as the bone is dragged across a rock with multiple projecting points. The bones also may spend some intervals buried in underwater sediments until exposed and again subjected to tumbling within the sea environment; partially buried bones may be scoured in place as sediments are moved past them [28]. Because many bones are recovered from coastal margins, and beaches specif ically, the skeletal elements are likely to have spent some time agitating within this environment along the ocean water’s edge.

In the present sample, 24 cases (96.0%) displayed some degree of battering of the bone (Figure 6), including rounding of exposed margins; these alterations sometimes included multiple random striations across the bone surfaces or occasional fractures (Figure 7). Among the cases with battering or rounding, f ive (20.0% of the total sample) fur ther displayed some form of windowing (Figure 8).


Figure 6Heavily battered and rounded mandible. Note also the heavy

bleaching.

Figure 7Heavily battered and rounded partial cranial vault. Note also the

bleaching, postmortem fracturing, and windowing of the parietals.


Figure 8Heavily battered and rounded mandible. Note also the heavy

bleaching and windowing of the mental foramina.


Bleaching and StainingBones immersed in marine environments typically become

heavily bleached over time, at least in part because of a loss of organic (including collagen and lipid) content [6]. Little is known about the timing of this change, but heavy bleaching often accompanies heavy rounding and other signs of long-term marine immersion. Bleaching was present in 22 cases (88.0%) (Figures 2–4, 6–8), although this color change was often overlain or otherwise obscured by sediments, mineral staining, or biological adherence, which are discussed later in this article. In some cases, later surface abrasion exposed underlying bleaching.

Surface stains most likely ascribable to mineral deposition (based upon their color, overall appearance, and comparison with known organic staining sources) were present in multi-ple cases. In six cases (24.0%), the stains were categorized as reddish in color. This reddish coloration is likely due to some combination of iron oxides (Figure 9). In three cases (12%), the stains were categorized as dark in color. This dark coloration likely indicates the presence of iron sulphides, formed under anaerobic conditions (Figure 10) [44].

Figure 9Reddish staining most consistent with iron oxide on a tibia shaft.

Figure 10Dark staining most consistent with iron sulphides on a femur.


Adhering SedimentBones recovered f rom marine set t ings f requently have

embedded sand in their crevices, including within cancellous bone exposed by rounding and abrasion, foramina, and drying cracks [43], and they may have concreted surfaces or loosely adherent sand. The present sample had 13 cases (52.0%) with sandy sediments visible macroscopically. Finer, silty sediments (Figure 11a) were found adhering in two cases (8.0%), with the differences in sediment likely associated with the coastal depositional environment in which the bone last spent significant time prior to discovery.

Figure 11aSilt adhering to the surface of a proximal left femur. Note also the exposure of the cancellous bone of the head, underlying bleaching, two large acorn barnacles, and seaweed strands. These changes are in high contrast to the right femur from the same individual (Figure 11b) also recovered from the

ocean, but with three fewer years of marine immersion time; see text.

Figure 11bRight femur removed from the ocean approximately three years prior to the left femur illustrated in Figures 11a and 19. Note that bleaching has begun,

but fat continues to leach from the bone.


Adhering OrganismsMultiple marine taxa adhere to a variety of hard or semihard

substrates as a part of their life cycle. Some of these taxa are sessile (i.e., attached and non-moving at a given developmen-tal stage, although their larval stage likely was highly mobile to allow distant colonization of new surfaces). Some mobile taxa colonize surfaces to feed upon other taxa, as in the case of limpets (a common gastropod) feeding upon surface algae. The buildup of these colonizing organisms on artificial surfaces (including docks, buoys, cables, and ships) is known as biofoul-ing and is a pervasive problem affecting marine commerce [45, 46]. These marine taxa in most cases adhere to bone as they would any available surface. The adhering organisms or traces of their previous adherence may remain upon a bone after its recovery, although drying of the bone often causes some loss of these organisms. Any tumbling of a bone against other objects tends to remove some of these adhering taxa as well, so they are often found in only the more recessed portions of a bone.

MollusksThe phylum Mollusca (mollusks) includes species that have

paired shells joined by a hinge (class Bivalvia), such as mussels, clams, and oysters. It also includes single-shelled species such as limpets, winkles, and periwinkles (class Gastropoda) that are not sessile and move about on hard surfaces when feeding; they often colonize the intertidal zone in high densities. Gastropods can adhere tightly to a hard surface through the secretion of an adhesive mucus [47]. Their habitual resting spots also may leave an identifiable circular patch on the substrate (referred to as a homing scar). When removed from the ocean, most gastropods will eventually dehydrate and die, but they may remain attached to a bone or other object even after drying.

In the present sample, only two cases (8.0%) retained adher-ing mollusks (Figure 12), but a total of four cases (16.0%) retained surface homing scars (Figures 13, 14) where mollusks had formerly adhered (one of these four cases with scarring also had adhering mollusks).


Figure 13Mollusk homing scars on the endocranial surface of a partial cranial vault;

close-up of mollusk scars on the exocranial surface.

Figure 12Small gastropods and algal strands adhering to an innominate,

with some sediments.


BarnaclesBarnacles (infraclass Cirripedia) are marine or brackish water

species and members of the arthropod subphylum Crustacea, which includes crabs, shrimp, and lobster (order Decapoda). The most commonly encountered of these are acorn barnacles (order Sessilia); their larvae drift in the ocean and attach themselves permanently by their dorsal surface to a substrate and then grow into their adult form. They attach themselves using a natural protein polymer [46]. Their bodies have a rounded shape and are protected by calcified plates, which often continue to adhere after the barnacle dies. They are found most abundantly in shallow water and within the intertidal zone, thus emerging temporarily as the tide f luctuates. Incremental growth bands of their calcare-ous plates or overall basal diameter increase potentially could be used to determine the minimum time of submergence of an object [48–51], including forensic cases [31, 52].

Barnacle encrustation was common in the sample, with nine cases (36.0%) having acorn barnacles still adhered to the bone (Figures 11a, 14). One of these nine cases (4.0% overall) also had visible traces where some barnacles formerly adhered (i.e., barnacle scars; Figure 15). In the present sample, barnacles frequently were small, so care sometimes may be needed in their detection. They also were most common in recessed areas, such as in the intercondylar notch of the distal femur (Figure 16), where subsequent battering of the bone could not remove them easily.

Figure 14Large, oval mollusk homing scars on a femur shaft that have been partially

eroded away by subsequent battering and abrasion. The homing scars appear as moatlike depressions around central, relatively unaffected areas. Note also

the small acorn barnacles.


Figure 16Acorn barnacles in the recessed area (intercondylar notch) of a distal femur.

Figure 15Acorn barnacles and acorn barnacle scars on bone.


Other CrustaceanA single case (4.0%) was associated with a crustacean other

than those already described: a single small crab (Decapoda) of unknown species was still contained within the cranial vault. Many crustaceans are scavengers, so it is likely that this set of remains had been def leshed to some degree by feeding by these taxa [31]. Because decapods do not adhere to bone as barnacles do, they will likely be retrieved in association with bone only if there is still significant soft tissue remaining or, as in the present case, they are trapped within the cranial vault.

Algae and Seaweed“Algae” are not a taxonomically coherent group, and species

under this broad category may belong to at least four different kingdoms [6]. These species range in size from microscopic protists (which commonly form the green organic staining on moist surfaces) to seaweeds and kelp [53]. “Kelp” specifically refers to the very large foliose forms of brown algae, and these have a stemlike structure that at taches to a hard substrate using a natural adhesive that can leave a scar if subsequently removed [54]. Algae are found in mar ine and f reshwater environments, so their presence alone on bone is not an indicator of marine immersion (or indeed, any immersion at all in the case of the smaller species), and they readily colonize most hard substrates primarily within the euphotic (sunlight) zone where they can produce food through photosynthesis.

In the present sample, nine cases (36.0%) displayed some form of algae adherence, ranging from diffuse green surface staining of single-celled protist types (Figure 17) to larger, multicellular forms including seaweed (Figure 11a) and f ilamentous brown algae (Figures 12, 18).


Figure 18Filamentous brown algae strands adhering to bone.

Figure 17Diffuse green algae adhering to bone.


BryozoaPhylum Bryozoa consists of colonial f ilter-feeders that are

found in freshwater and marine environments; these taxa, despite superf icial resemblance, are distinct from coral (in phylum Cnidaria). Colonies are made up of minute (~0.5 mm) individual zooids, housed in a protective covering that may be organic or mineralized (e.g., calcium carbonate) and that may persist on a colonized surface after the Bryozoa have died. The growth rate of these taxa may have some utility regarding determination of the minimum immersion time of bone [31, 55]. A single case (4.0%) of the present sample displayed Bryozoa colonization of a bone surface that had partially abraded away (Figure 19).

Figure 19Bryozoa colony adhering to bone; close-up of same. Note also the abrasion,

which has removed part of the colony.


Timing of ChangesOne set of cases allowed for computation of the time that

it took for some of these taphonomic changes to accrue. From nuclear DNA analysis, it was determined that two isolated femora that were recovered by f ishing nets from the ocean off the north coast of Cape Cod, Massachusetts, had in fact originated from the same individual. One femur was recovered in November 2011, and the other was recovered in October 2014, so it was possible to examine the changes brought about by an additional approximately three years of submersion time in the same environment. Of course, no particulars can be determined regarding whether the two elements spent any of their submersion time buried in sediments or otherwise partially protected from some sources of marine taphonomic alteration. The fresher (right) femur, however, had undergone very little taphonomic alteration (Figure 11b), had adipocere adhering and in crevices, and retained a strong decomposition odor; its time since entry into the water was estimated as under one year. In that time, minor battering and rounding had begun, but the bone retained a very fresh overall appearance including leaching fat. Some mollusk homing scars and algae had formed.

The (left) femur with the additional three years of submer-sion time had undergone advanced marine taphonomic alteration (Figure 11a). Battering and rounding had greatly advanced past that displayed by the right femur, exposing much cancellous bone, and underlying bleaching also was advanced from the right femur. The left femur no longer retained an organic sheen to its surface and had a chalky appearance overall. It also had acquired reddish and dark mineral staining in patches and had silty sediments, seaweed, two large barnacles, and Bryozoa adhering (Figure 19). The left femur also contained some adipo-cere within its exposed cancellous spaces. Thus, these advanced taphonomic changes can take place over the space of three years for isolated elements in this environment.

Discussion

Continuum of Taphonomic AlterationsMany sets of human remains int roduced into mar ine

environments proceed through some common taphonomic pathways [31], and the present sample represents some individual points along this spectrum of changes. Few remains retained soft tissue, which is a ref lection of the deliberate way in which the


sample was compiled: cases of intact or mostly intact remains were not included in the analysis, although these are a significant component of forensic case work in the study region. Soft tissue decomposition generally proceeds more slowly in submerged marine environments than on land [34–37]; this is in part due to generally lower temperatures and the exclusion of large blow f ly (Calliphoridae) larval masses. Intact, decomposing human bodies also may drift great distances if they remain buoyant [56] and shed individual elements as the extremities decompose [37]. Marine scavengers, however, can greatly increase the speed of soft tissue loss [31, 57–59]. This soft tissue loss results in bone exposure and its more direct and extensive taphonomic alteration.

The gradual loss of bone grease content and the formation of adipocere proceed throughout this initial decomposition phase, with the loss of any adhering adipocere through agitation and abrasion as a body breaks apart and its bones are dispersed. Throughout this t ime, the gradual breakdown and loss of grease and other organic content of the bone causes the loss of its organic sheen, eventually reducing the surface to a chalky texture. Simultaneously, the surface becomes bleached through processes that include loss of organic content, and agitation along the sea f loor among damaging rocks and abrasive sand gradually batters the bone, leaving broken margins that become rounded along with other exposed portions and in some cases fracturing and windowing.

Mineral staining also may occur during this process. Some bones show that rounding occurred, followed by mineral staining, and others show that mineral staining occurred, then was worn away by additional rounding. Sand and silt may adhere to the surfaces, although it is likely that repeated agitation constantly changes the degree to which these sediments adhere until the bone is f inally removed from the water. The multiple taxa noted here also may colonize the bone throughout this process. For example, barnacles were found on bones that were highly bleached, chalky, battered, and rounded; they were also found on bones that were unbleached, greasy, and unabraded. The physical processes therefore may remove earlier traces of colonization, with new waves of organisms attempting to establish themselves on a bone surface as the physical processes of abrasion remove some of them. Colonization may begin as soon as bone is exposed from its soft tissue covering. Long-term colonization by some species of Gastropoda may leave round scars on the bone surface that can persist long after that individual organism has become


detached from the surface. Many of these taphonomic processes may occur on the bone at once, with processes ongoing even when the remains are discovered. Given that marine coastal environments are often high-energy, the f inal state for most bones that do not become buried in sediments (or are encased in a ship or other wreckage) is likely to be fragmentation because of battering and incorporation into the sediment matrix, with gradual dissolution to follow.

Another taphonomic path that human bones in marine environ-ments may follow is colonization by organisms that consume the bone itself for dietary reasons or to form tunnels for housing their bodies [60]. These processes, too, lead to the gradual destruction of the bone. These organisms include bone-boring worms of the genus Osedax, which are often found colonizing large marine vertebrate carcasses on the deep ocean f loor [44, 61–63]. The present sample did not display any macroscopic signs of boring by marine organisms. Microscopic organisms also may bore into bone in marine environments [64, 65], although these changes were not examined for in the present study. Some marine inver-tebrates also scour surfaces while feeding and may leave traces of this activity on the bone surface, such as mollusks feeding with their scraping radula [31, 66, 67] and sea urchins grazing with their teeth [6]. Surface scoring on rocks by fish (including parrotfish, family Scaridae) feeding on adhering algae has been observed (personal observation), so it is possible that this type of feeding activity also could alter any bone encountered with surface algae. Other, rarer processes resulting in bone destruc-tion include gradual digestion and decalcification by scavenging shark species [21]. The present sample therefore represents one par ticular, but forensically common, taphonomic subset of human bones that may be recovered from marine environments.

Confusion with Other Sources of Taphonomic AlterationsA combination of the multiple taphonomic alterations listed

here is a strong indicator of extended marine immersion for human bone, although continuing research into freshwater environments may detect more commonalities between these two environments [28]. Some individual characteristics, however, can be mistaken for or be caused by taphonomic alterations from other, nonaqueous environments. Isolated remains were common in the present sample, which is a partial function of the exclusion of more intact, f leshed bodies. Because full disar ticulation is a common end result of decomposit ion in a mar ine environment [29], it is not surprising that individual elements


are often turned in for forensic analysis. Bone condition followed a path of gradual degreasing, loss of other organic content and surface sheen, and finally a chalky condition. A similar pattern, however, is found in bones degrading in other environments, including cemetery burial [68]. Similarly, adipocere may form in many types of moist environments, including terrestrial surface exposure and cemetery remains [38, 39].

Bleaching frequently resulted from marine immersion. Marine bone bleaching can be distinguished from bleaching that is due to subaerial weathering in exposed terrestrial environments [69] in multiple ways. Marine bleaching typically affects all areas of a bone simultaneously, because the saltwater normally can reach every surface at once; exceptions to this pattern include bones periodically exposed to the air in tidal f lats. Sunlight in terrestrial environments is limited in its effects to one surface of a bone at a time. Subaerial weathering therefore often advances to a higher stage on the uppermost side of a bone, whereas the portion of the bone in contact with the ground lags behind [69]; the side in contact with the ground often develops other indica-tors of terrestrial exposure, including soil staining, acidic soil erosion, and plant root infiltration [70]. Extensive cracking of the bone surface is also a major component of subaerial weather-ing but is not observed on marine remains, unless cracks form because of subsequent drying.

Bleaching of mar ine bones is of ten accompanied by rounding of margins, whether part of the original bone struc-tures [6, 42, 43] or margins exposed by breakage, as the bone slowly gets worn away by abrasion. Rounding of bone may also occur in f luvial environments [28], although in some cases, f luvial rounding of bone is minimal despite long transpor t distances in rivers [28, 71].

Windowing may be formed in some areas because of abrasion. Other taphonomic processes can cause windowing, includ-ing gastric corrosion during digestion [72] or acidic corrosion during burial [70]. Gastric corrosion normally can affect only small bones that can be swallowed, whereas bones from burials are often accompanied by overall surface acidic corrosion, soil staining, and possibly plant root inf iltration or etching [70]. Similarly, mineral and other dark staining may appear on buried bones (especially those in contact with oxidizing metal), includ-ing all-over color changes or more isolated and variable patches of staining. The type of sediments adhering to a bone also may


suggest a marine environment, especially where sand (especially sand with a high component of crushed shell) is present.

The adhering taxa described in the present research are strong indicators of aquatic immersion. Although mollusks, Bryozoa, and decapod crustaceans are found in both fresh- and saltwa-ter, marine and freshwater species are readily distinguishable and so may be used to distinguish saltwater immersion from freshwater. Algae forms also may indicate aquatic environments, except that single-celled algae can grow on most moist terres-trial surfaces. Identification of the larger species of seaweed and kelp may be possible by specialists in order to separate fresh-water from saltwater origin. Barnacles are exclusively marine taxa and moreover favor shallow coastal waters, such as tidal zones. Their presence on a bone indicates marine immersion, and additional research into the time interval of colonization and growth of common species may be useful for determination of the minimum amount of times that def leshed bones have been exposed in saltwater.

Notably, despite apparently long inter vals of mar ine immersion prior to forensic analysis, human remains may retain replicable DNA for analysis and identification; the authors have noted this to occur even among heavily battered and bleached bones.

ConclusionMarine environments can alter human bone in ways that are

distinct from other common forensic settings, including surface terrestrial, buried terrestrial, and cultural contexts. Multiple environmental processes affect the bone during immersion, including mechanical abrasion, bleaching, sediment adherence, and biological alteration through the colonization of multiple taxa. These taphonomic characteristics can be used to determine the environment of origin of these remains in cases where the recovery context was unknown, when it is suspected that the remains have been moved, or if the case information is later lost.

Further research into these processes also may yield useful data regarding the time over which bones have been exposed to marine immersion. This research could include the minimum time of colonization of various organisms and their growth rates once established on a bone surface [31, 48–52], although these estimates would have to take into account the effects of any temporary protection from colonization of bone surfaces by


clothing, other artifacts, and the soft tissue as it decomposes. Because these patterns are likely to vary signif icantly based upon the type of marine environment, the species that populate that environment, degree of covering by soft tissue or burial, and season, the results may be highly specif ic to a local set of conditions. More general time of immersion patterns may be developed through fur ther research of broad patterns of bone breakdown, including loss of organic content, bleaching, battering, rounding, and the development of mineral staining. Given the often high-energy environment of coastal waters, these physical changes may develop on disarticulated bones and progressively damage them, as was indicated generally in the present sample.

AcknowledgmentThe authors thank Dr. Henry Nields and the Office of the

Chief Medical Examiner, Boston, Massachusetts, for their kind access to data, and Dr. Joan Baker and Dr. Ericka L’Abbé for their review of previous versions of this manuscript. The authors also thank the two anonymous peer reviewers for their helpful comments.

For further information, please contact:James T. Pokines, Ph.D., D.A.B.F.AOffice of the Chief Medical Examiner720 Albany StreetBoston, MA 02118 andBoston University School of Medicine72 E. Concord Street, L1004Boston, MA 02118 [email protected]

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