[Palaeontology, 2017, pp. 1–22]

COMPARATIVE EXPERIMENTAL TAPHONOMY OF EIGHT MARINE ARTHROPODS INDICATES DISTINCT DIFFERENCES IN PRESERVATION POTENTIAL by ADIEL€ A. KLOMPMAKER1,2 , ROGER W. PORTELL1 and MICHAEL G. FRICK3 1Florida Museum of Natural History, University of Florida, 1659 Museum Road, PO Box 117800, Gainesville, Florida 32611, USA; [email protected] 2Department of Integrative Biology & Museum of Paleontology, University of California, Berkeley, 1005 Valley Life Sciences Building #3140, Berkeley, CA 94720, USA 3Archie Carr Center for Sea Turtle Research & Department of Biology, University of Florida, PO Box 118525, Gainesville, FL 32611, USA

Typescript received 9 January 2017; accepted in revised form 30 May 2017

Abstract: Global biodiversity patterns in deep time can We found limited variation in the decay rate between con- only be understood fully when the relative preservation specifics, and we did not observe size-related trends in potential of each clade is known. The relative preservation decay rate. Conversely, substantial differences in the decay potential of marine arthropod clades, a diverse and ecologi- rate between species were seen after c. 50 days, with cally important component of modern and past ecosystems, shrimps and stomatopods decaying fastest, suggesting a rel- is poorly known. We tackled this issue by carrying out a atively low preservation potential, whereas the lobster, cal- 205-day long comprehensive, comparative, taphonomic ico crabs, horseshoe crabs and barnacles showed relatively experiment in a laboratory by scoring up to ten tapho- slow decay rates, suggesting a higher preservation potential. nomic characters for multiple specimens of seven crus- These results are supported by two modern and fossil tacean and one chelicerate species (two true crabs, one record-based preservation potential metrics that are signifi- shrimp, one lobster, one hermit crab, one stomatopod, one cantly correlated to decay rate ranks. Furthermore, we spec- barnacle and one horseshoe crab). Although the results are ulate that stemward slippage may not be ubiquitous in preliminary because we used a single experimental setup marine arthropods. Our results imply that diversity studies and algal growth partially hampered observations, some of true crabs, lobsters, horseshoe crabs and barnacles are parts of hermit crabs, stomatopods, swimming crabs and more likely to yield patterns that are closer to their true barnacles decayed slowly relative to other parts, implying biodiversity patterns than those for stomatopods, shrimps differential preservation potentials within species, largely and hermit crabs. consistent with the fossil record of these groups. An inferred parasitic isopod, manifested by a bopyriform swel- Key words: Arthropoda, biodiversity, Crustacea, decay, ling within a hermit crab carapace, decayed relatively fast. preservation, taphonomy.

U NDERSTANDING the fossil record and its biodiversity the initial stages of fossilization can be investigated. This hinges on knowing how fossils preserve, the chances of has led to a surge in research involving taphonomic fossilization and the preservation potential between experiments, especially since the 1980s (e.g. Briggs 1995; clades. An assessment of the relative preservation poten- Sansom 2014; Briggs & McMahon 2016). Experimental tial between taxa can be performed in several ways: (1) taphonomy has been widely used for a variety of clades, comparing the fossil content of Konservat-Lagerst€atten to to decipher the decay rate of whole organisms or parts fossils from coeval, nearby deposits; (2) comparing the thereof (e.g. Raff et al. 2006; Sansom et al. 2010; Mur- fossil record to modern biota; and (3) comparative exper- dock et al. 2014; Nanglu et al. 2015), the physical and imental taphonomy. chemical conditions that enhance the preservation poten- Whereas interpreting the taphonomy of the fossil tial and early mineralization of soft tissues (e.g. Briggs & record a posteriori can be very insightful, a priori experi- Wilby 1996; Briggs 2003; Raff et al. 2006; Darroch et al. ments are extremely useful to better explain why organ- 2012), to reconstruct colour (McNamara et al. 2013a, b; isms do or do not fossilize (Plotnick 1986) and the Vinther 2015) and its implications for phylogeny includ- conditions required for preservation, even though only ing tests of stemward slippage, a process whereby

© The Palaeontological Association doi: 10.1111/pala.12314 1 2 PALAEONTOLOGY taphonomic loss of phylogenetically informative charac- molluscs (e.g. Kidwell & Flessa 1995; Stempien 2005) and ters results in erroneously primitive phylogenetic place- possibly also to tetrapods and fishes (Wills 2001). First- ment of fossils (Sansom et al. 2010; Sansom & Wills order biodiversity patterns through time of various arthro- 2013; Murdock et al. 2014; Nanglu et al. 2015), among pod clades have become increasingly well known recently others. Comparative experimental taphonomy, defined (Sepkoski 2000; Klompmaker et al. 2013; Schweitzer & here as decay experiments in which multiple species are Feldmann 2014, 2015), but fully taking into account dif- used and compared to each other, has been performed ferential preservation between clades to better quantify within some clades using a few taxa usually (Allison 1986; diversity through time remains challenging. Comparative Sansom et al. 2010; Powell et al. 2011; Sigwart et al. experimental taphonomy will help to improve our under- 2014; Nanglu et al. 2015). Conversely, comparative exper- standing of Phanerozoic arthropod biodiversity. iments involving a range of species that differ substan- Although comparisons between taxa are highly problem- tially in morphology are rare (e.g. Parsons-Hubbard et al. atic, previous work on individual arthropod species not 2008). involving tumbling experiments found that swimming The same applies to experimental taphonomy of marine shrimp disarticulated and fragmented within weeks to macroarthropods; rarely more than one species is used months in experimental setups (Plotnick 1986; Allison (Table 1). Comparing results of existing studies is difficult 1988; Briggs & Kear 1994). A lobster in the same experi- because of different experimental conditions and setups. ment by Allison (1988) decayed slower: many fragments This lack of knowledge severely hampers our understand- were left after 25 weeks. Stomatopod carcasses were still ing of the differential preservational biases across arthro- complete after 25 weeks into an experiment, but limbs had pod clades and, as a result, their true biodiversity through fallen off (Hof & Briggs 1997). Long-term experiments with time, which is already confounded by their lower preserva- true crabs (Callinectes sapidus) deployed in ocean settings tion potential compared to the more heavily calcified within mesh bags showed that claws are the parts that pre- serve best after 2–13 years (Mutel et al. 2008; Parsons- Hubbard et al. 2008; Krause et al. 2011), and the same spe- TABLE 1. Previous taphonomic experiments involving marine cies used in an archaeological study on land also resulted in macroarthropods with the primary goal of assessing the decay of claws being most resistant to decay (Rick et al. 2015). Bur- whole organisms and/or chemical gradients near or within ial experiments using the crab Panopeus sp. showed disar- decaying organisms. ticulation within two weeks, but fragmentation was still Common Taxon name(s) Reference(s) limited after ten months (Plotnick et al. 1988). name(s) The aim of this research was to evaluate the relative preservation potential of eight marine macroarthropod Shrimp Pandalus danae Plotnick (1986) Stimpson, 1857 clades by carrying out comprehensive comparative tapho- Shrimp Crangon crangon Sagemann nomic experiments using multiple specimens of seven (Linnaeus, 1758) et al. (1999) crustacean and one chelicerate species. Taphonomic Shrimps Crangon crangon and Briggs & Kear experiments have also been carried out on a mm-sized Palaemon sp. (1993, 1994) brine shrimp which primarily lives in lakes (e.g. Gostling Lobster and Nephrops norvegicus Allison (1986, 1988) et al. 2009; Butler et al. 2015). Unlike our experiment, shrimp (Linnaeus, 1758) other investigations of marine arthropods were performed and Palaemon primarily to infer chemical changes or alteration of the adspersus Rathke, 1837 cuticle (Poulicek et al. 1986; Schimmelmann et al. 1986; True crabs Soja (1999) Baas et al. 1995; Stankiewicz et al. 1998; Gupta et al. and shrimps 2006, 2009; Gupta 2014). We determined decay rate True crab Callinectes sapidus Mutel et al. (2008); Rathbun, 1986 Parsons-Hubbard within and between macroarthropod species, and com- et al. (2008); pared our results to the preservation of fossils from each Krause et al. (2011); clade and two preservation potential metrics based on the Rick et al. (2015) number of fossil and modern taxa. True crab Panopeus sp. Plotnick et al. (1988) Stomatopod Neogonodactylus Hof & Briggs (1997) oerstedii MATERIAL AND METHOD (Hansen, 1895) Horseshoe Limulus polyphemus Babcock & Chang Trial experiment crab (Linnaeus, 1758) (1997); Babcock et al. (2000); Because this is the first time that decay rates have been Tashman (2014) compared for different extant clades of arthropods in the KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 3 same experimental setup, a trial experiment was run first removed around the barnacles where possible. All speci- to determine the morphological characters best suited for mens originated from the Gulf of Mexico in the Florida comparing decay rates between arthropods and to test a panhandle region, except for P. versicolor from the Wes- compartmented saltwater aquarium (see below). One tern Pacific or Indian Ocean. The live specimens were specimen each was used of the calico crab Hepatus purchased from a local marine lab and an aquarium shop epheliticus (Linnaeus, 1763), the swimming crab Portunus for the lobster. Transparent lids with holes for aeration gibbesii (Stimpson, 1859), the pink shrimp Penaeus duo- were put on the compartments containing specimens to rarum Burkenroad, 1939, the striped hermit crab Cliba- minimize the settling of dust and other particles into the narius vittatus (Bosc, 1802) as well as other arthropods aquarium. Four specimens were put in the lower and lar- including the mantis shrimp Squilla empusa Say, 1818, ger compartments, whereas two specimens were put into and the Atlantic horseshoe crab Limulus polyphemus the smaller upper compartments. Specimens were placed (Linnaeus, 1758). about equidistantly and next to electrical tape with a width of 19 mm for scale. A pump in a separate basin allowed for continuous through-flow of artificial seawater Full experiment at c. 36&, especially in the uppermost part of the water column where the compartments were interconnected, For the full experiment, five differently-sized live speci- whereas circular flow occurred in the rest of the water mens of each species mentioned above were dispatched column. Through-flow ensured mixing of waters resulting by freezing (as in Plotnick (1986), Plotnick et al. (1988), in similar conditions for all specimens throughout the Gupta et al. (2006) and Krause et al. (2011)) in fresh- experiment. Artificial seawater was made by mixing dry water for c. 20 h and subsequently put on the bottom of or granular salt with dechlorinated freshwater. The aquar- saltwater aquarium compartments in a lab at the Univer- ium lacked large-bodied scavengers and natural perturba- sity of Florida (Fig. 1). Additionally, tens of specimens of tions such as storms so that the decay process was the barnacle Amphibalanus eburneus (Gould, 1841) and dominated by microorganismal activities because micro- one specimen of the blue spiny lobster Panulirus versicolor bial decay is a major determinant of preservation poten- (Latreille, 1804) were added using the same procedure. tial (Briggs & McMahon 2016, and references therein). Additional conspecific lobsters were not available at the No sediment was added to the bottom of the tank to start of the experiment. All species belong to marine ensure that all appendages could be readily observed. The arthropod clades (Crustacea and Chelicerata) that have an specimens were not handled during the experiment and existing fossil record and these taxa are here considered algal growth was not removed once it formed. The speci- to be morphologically representative of the clades they mens were observed and photographed (requiring tempo- belong to. The specimens were not scrubbed or rinsed rary removal of the transparent lids) about three times prior to placement into the aquarium to minimize dam- per week for the first three months. After these months, age to the specimens, but algae and invertebrates were during which all relatively fast changes had occurred, the same procedure occurred about once a week until the end of the experiment after 205 days, when algal growth was judged to have become too pervasive to continue the experiment. Salinity was measured each time and distilled freshwater and saline water was added as needed to keep salinity levels near that of normal seawater. Temperature and other characteristics of the water, using an API salt- water master test kit (marine), were measured 4–5 times during the experiment. Experimental conditions in the water column were as follows (Klompmaker et al. 2017, table S1): salinity: 36.2 1.7& (1 SD), n = 57; tempera- ture = c. 21.3°C(n= 4); light conditions: 12 hours dark and 12 hours light per day; pH = 8.2 (n = 5); ammonia þ = ≤ (NH3/NH4 ): 0 ppm (n 5); nitrite (NO2 ): 10 ppm = ≤ = (n 5); nitrate (NO3 ): 5 ppm (n 5). Since the com- partments were in contact with the ambient air in the lab during the entire experiment, oxygen levels of the saltwa- FIG. 1. Full experimental setup of the compartmented aquar- ter should not have varied and be in equilibrium with ium. The basin with the pump for through-flow is located on oxygen levels in the atmosphere (~9 mg/L; this does not the other side of the aquarium (not visible). Colour online. necessarily apply to fluids within and around the 4 PALAEONTOLOGY carcasses as demonstrated by Sagemann et al. 1999). The In the rare case of missing scores bracketed by scores with presence of oxygen does not appear to be a major control a difference of two (e.g. 0 and 2), those scores and the on the decay rate of arthropods (Plotnick 1986; Briggs & mean are used divided evenly among the missing scores Kear 1994). (for example, for 0, –, –, –, 2, the three missing scores are Based on observations from the trial experiment and filled out as follows: 0, 0, 1, 2, 2), and when evenly divid- previous taphonomic work on crustaceans (Plotnick 1986; ing was not possible, the lowest score(s) were used to fill Hof & Briggs 1997; Mutel et al. 2008; Krause et al. 2011) out the remaining missing scores (for example, 0, –, –, –, ten taphonomic characters were assigned scores as listed –, 2 becomes 0, 0, 0, 1, 2, 2). Specimens lifted by strings in Table 2. The wall plates of barnacles were herein con- of algae (Fig. 2A) were typically not easily observable and sidered analogous to the carapaces of other arthropods remained floating. Scores attributed to these specimens, because they protect the soft tissues inside. Measurements when recorded, were not included. were taken from each arthropod specimen prior to the start of the experiment using digital callipers (Klomp- maker et al. 2017, table S2): carapace length, width and Analytical methods height; abdominal length and width; telson length and width; hermit crab gastropod shell height and width; After normalization of the data (i.e. each taphonomic minimum and maximum diameters of barnacles at the character is equally weighted), two data sets were used: base. All experiments were carried out in accordance with those with all taphonomic characters included (method local ethical guidelines. 1) and a subset based on the articulation and fragmenta- tion of calcified/chitinous parts of each taxon only (#1, 4, 6, 7, 9 and 10 from Table 1, method 2) because these Data treatment parts have the highest chance of fossilization. Tapho- nomic scores were compared per species per character The data (Klompmaker et al. 2017, table S3), consisting after normalization. of 58 days during which observations were made over a The data were analysed within species to assess time span of 205 days, were treated in multiple ways after whether differences in size affect decay rates. Addition- digitization. For missing scores bracketed by scores on ally, possible differences between species were evaluated both ends (typically due to temporary algal coverage) the and we assessed whether variation within species differs conservative lower score was chosen for all missing scores. from variation between species. Between species compar- isons were done in two ways: first, scores from all con- TABLE 2. Taphonomic characters scored for the full experi- specifics were averaged and, second, the lowest and ment using marine macroarthropods. highest score for each species was used to determine a range of taphonomic variability within a species. The Taphonomic character Score low number of specimens per species (five as the maxi- 1. Soft tissue presence All present (0); some (1); none (2) mum, except for barnacles that were not scored individ- 2. Cuticle colouration Original (0); faded (1); ually) in combination with the fact that only 73 days discoloured/white (2) could be observed for all specimens due to algal growth 3. Separation abdomen No (0); yes (1) does not allow for meaningful statistical analyses and carapace between species. Analyses were carried out in RStudio v 4. Carapace completeness Intact (0); abundant fragments (1); 0.99.902 (https://www.rstudio.com). few fragments (2); To test whether the fossil record of the eight clades no fragments (3) may be explained by the relative decay rate of the 5. Carapace translucency No (0); yes (1) 6. Claw completeness Whole, articulated (0); arthropod clades as found in our study, we calculated disarticulated, nearly whole (1); two preservation potential indices: (1) number of extant badly fragmented (2); absent (3) species/number of species in the Cenozoic fossil record 7. Other appendage Whole, articulated (0); (to reduce the possible influence of long-term changes completeness disarticulated, nearly whole (1); in diversity in certain clades, the possible influence of badly fragmented (2); absent (3) mass extinctions and different times of origination); and 8. Appendage translucency No (0); yes (1) (2) following Valentine et al. (2006), the percentage of 9. Abdomen completeness Whole, articulated (0); genera with a missing fossil record. We then compared disarticulated, nearly whole (1); those metrics to the provisional rank based on our badly fragmented (2); absent (3) experiment using Spearman’s rank correlation coefficient 10. Telson completeness Intact (0); fragmented (1); and associated p-values using PAST 2.17 (https://folk. absent (2) uio.no/ohammer/past/). KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 5

A BC

DEF

FIG. 2. Various crustaceans in different stages of decay highlighting either important decay processes or differential preservation. A, the middle-sized specimen of the swimming crab Portunus gibbesii lifted by black algae 101 days into the full experiment; the ventral side of the crab with the abdomen of up to 10.4 mm wide can still be seen. B, the second largest swimming crab P. gibbesii with a white coating 7 days into the full experiment; note that the appendages, containing a limited amount of soft tissue, do not exhibit much coating; direction of bottom current is up. C, the smallest hermit crab specimen of Clibanarius vittatus, after losing its original colour, shows a better preserved anterior carapace compared to the posterior part, and has its telson and uropods preserved, whereas the abdomen had fully decayed after 75 days into the full experiment. D, raptorial dactyli preserve better than the remainder of the stomatopod body of Squilla empusa (diagonally toward upper left corner) 68 days into the full experiment; the two white points stick- ing out of the body remains, left of the centre of the image, most likely represent partly covered mandibles. E, the smallest swimming crab specimen of P. gibbesii showing translucent non-cheliped appendages and translucent eyes that have fallen out of their sockets 92 days into the full experiment. F, the chela and dactyli of other appendages decay slower than the rest of the hermit crab C. vittatus (photo from the trial experiment); length of left chela c. 10–15 mm. Scale bars (B–E) represent 10 mm. Colour online.

RESULTS (lobster, crabs) so that not all soft tissue had fully decayed at the end of the experiment. Soft tissue of other Per-character per-taxon observations taxa (shrimp, stomatopods, barnacles, hermit crabs) had decayed entirely after c. 100 days. The first phase of decay Klompmaker et al. (2017, table S3, figs S1–S10) provide in every arthropod studied was the development of a the full details of the per-character per-taxon decay white coating (bacterial or fungal) around the parts that scores, and the following summarizes the trends observed contain soft tissue, leading to a swollen appearance of in Figure 3. specimens, although bottom currents also have some influence on the extent of the coating (Fig. 2B). This pro- Soft tissue presence. Soft tissue decayed relatively uni- cess occurred within days of putting the specimens into formly commencing shortly after the start of the experi- the aquarium and could take tens of days depending on ment (Fig. 3A). Within-species variation was limited to the amount of decaying soft tissue inside the exoskeleton. non-existent (Klompmaker et al. 2017, fig. S1). It A higher amount of decaying soft tissue resulted in a appeared to occur slower within well-calcified taxa thicker coating, and odour was limited during the entire 6 PALAEONTOLOGY

A B C

1.00 Arthropod clade 1.00 1.00 Barnacles Calico crabs Hermit crabs 0.75 Horseshoe crabs 0.75 0.75 Lobster Shrimps Stomatopods Swimming crabs 0.50 0.50 0.50

Taphonomic score Taphonomic 0.25 0.25 0.25

0.00 0.00 0.00

0 50 100 150 200 0 50 100 150 200 0 50 100 150 200

D E F

1.00 1.00 1.00

0.75 0.75 0.75

0.50 0.50 0.50

Taphonomic score Taphonomic 0.25 0.25 0.25

0.00 0.00 0.00

0 50 100 150 200 0 50 100 150 200 0 50 100 150 200

G H I

1.00 1.00 1.00

0.75 0.75 0.75

0.50 0.50 0.50

Taphonomic score Taphonomic 0.25 0.25 0.25

0.00 0.00 0.00

0 50 100 150 200 0 50 100 150 200 0 50 100 150 200 Days since start experiment Days since start experiment J

1.00

0.75

0.50

Taphonomic score Taphonomic 0.25

0.00

0 50 100 150 200 Days since start experiment FIG. 3. Per-species comparisons for each of the ten taphonomic characters (normalized) throughout the full experiment. A, soft tis- sue presence. B, cuticle colouration. C, separation of abdomen and carapace. D, carapace completeness. E, carapace translucency. F, claw completeness. G, other appendage completeness. H, appendage translucency. I, abdomen completeness. J, telson completeness. KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 7 decay process. Some opercular plates (scuta and terga) of (Klompmaker et al. 2017, fig. S5). Intraspecific variation barnacles fell out of the wall plates surrounding them due is limited to non-existent for each taxon (Klompmaker to the swelling of internal tissue in the early phase of et al. 2017, fig. S5). The anterior part of the carapace of decay or due to their upside-down orientation after soft hermit crabs became translucent at a slower pace than the tissue holding them in place had decayed (Fig. 3, c. less calcified posterior part (Fig. 2C). 100 days). The relatively soft eyes decayed relatively fast for each taxon: after c. 75 days most eyes had fully Claw completeness. Claw fragmentation could not be decayed, becoming translucent or shrinking substantially recorded for horseshoe crabs, shrimps, barnacles and the (Figs 2C, E, 4–5). The smallest hermit crab specimen lobster because these taxa did not exhibit a major claw. For exhibited a bopyriform swelling in the right branchial other taxa, the claws of stomatopods decayed fastest (start- chamber (Fig. 6), almost certainly caused by a soft-bodied ing at c. 60 days), followed by those of hermit crabs and parasitic isopod such a member of the Entoniscidae or, swimming crabs (starting at c. 75 days), while those of cal- more likely, Bopyridae (e.g. McDermott et al. 2010; Wil- ico crabs started to disintegrate only after c. 110 days liams & Boyko 2012; Boyko & Williams 2016). An outline (Fig. 3F). Intraspecific variation is limited to non-existent of this isopod was seen at 25 days into the full experi- for each taxon (Klompmaker et al. 2017, fig. S6). The rap- ment when the cuticle of the hermit crab appears to have torial dactyli and, most likely, the mandibles decayed much been partially decayed, and a red spot marked the former slower than the rest of the stomatopods (at least these position of this isopod at 75 days when the isopod had dactyli were observed after 205 days) (Fig. 2D). further decayed (Fig. 4). Other appendage completeness. The non-claw appendages, Cuticle colouration. Cuticle discoloured in most species or all appendages for some taxa, decayed fastest for bar- except for pink shrimp and barnacles, and was particu- nacles because they are non-calcified, followed by those of larly apparent for both crabs and the hermit crabs stomatopods and shrimps after c. 60 days (Fig. 3G). (Fig. 3B; Klompmaker et al. 2017, fig. S2). Discolouration Appendages of other taxa disintegrated from 60 to started within 100 days for nearly all specimens, with lar- 100 days onward. There is some variation within species, ger specimens losing their colour more slowly in some especially for horseshoe crabs, calico crabs, swimming taxa. Within-species variation was limited to non-existent, crabs and hermit crabs, unrelated to the size of the with most variation occurring within both crab species arthropod (Klompmaker et al. 2017, fig. S7). and hermit crabs (Klompmaker et al. 2017, fig. S2). Appendage translucency. It was not possible to judge the Separation of abdomen and carapace. Separation of the translucency of appendages for barnacles (very small) and abdomen from the carapace was observed for shrimps, horseshoe crabs (covered by the carapace), but it increased stomatopods and hermit crabs, while this was not for only the lobster and swimming crabs after c. 60 days observed for other taxa (Fig. 3C). When it does occur, (Fig. 3H). There was no variation within species for any separation is visible usually within 50–100 days. taxa except for the swimming crabs in which limited vari- Intraspecific variation is limited to non-existent with ation was seen during days 60–85 (Klompmaker et al. most variation occurring within hermit crabs (Klomp- 2017, fig. S8). The non-cheliped appendages of the swim- maker et al. 2017, fig. S3). ming crabs became translucent first and may decay faster than other parts of this taxon (Fig. 2E). The chela and Carapace completeness. Disintegration of the carapace dactyli of other appendages of hermit crabs became trans- (Fig. 3D) commenced after c. 50 days for shrimps, stom- lucent at a slower rate than other parts of the exoskeleton atopods and hermit crabs, while it took 100–150 days for (Fig. 2F). it to occur in swimming crabs. Other species showed no sign of carapace disintegration over the duration of the Abdomen completeness. The abdomina of hermit crabs, experiment (Fig. 3D). Intraspecific variation is limited to stomatopods and shrimps decayed fast after c. 50 days, non-existent with most variation occurring within hermit whereas no noticeable fragmentation was observed for crabs (Klompmaker et al. 2017, fig. S4). horseshoe crabs or the lobster (Fig. 3I). It was not feasible to quantify the decay of the abdomen for either of the Carapace translucency. It took c. 50 days for increases in crab species or the barnacles (not visible in all cases). the translucency of carapaces of shrimps, hermit crabs Variation within species is limited to non-existent, except and horseshoe crabs to occur, while other taxa did not for hermit crabs, where the abdomen of the smallest her- show any change throughout the experiment (Fig. 3E) mit crab decayed faster than that of conspecifics (Klomp- with the exception of a single swimming crab maker et al. 2017, fig. S9). 8 PALAEONTOLOGY

FIG. 4. Differential decay rates during the full experiment over the course of 100 days for the smallest specimens of eight clades of marine arthropods. Algal growth changed the colour of the bottom of the aquarium, and black algae surrounded and lifted some spec- imens (Fig. 2A). All scale bars (first column) represent 10 mm. Colour online.

Telson completeness. Disintegration of the telson was fast- change noticeably and neither did that of the hermit est for shrimps, followed by that of stomatopods and the crabs, although the telson of hermit crabs is relatively lobster (Fig. 3J). The telson of the horseshoe crab did not small. Telson decay could not be scored for either the KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 9 A A

B

B

C

FIG. 6. The smallest specimen of the hermit crab Clibanarius vittatus, with a bopyriform swelling (ichnotaxon Kanthyloma crusta) in its right branchial chamber, almost certainly caused by a parasitic isopod. A, dorsal view. B, right lateral view. Both scale D bars represent 10 mm. Colour online.

crabs or the barnacles. Variation within species is limited to non-existent (Klompmaker et al. 2017, fig. S10). Not only the telson but also the uropods of the hermit crabs decayed more slowly than the abdomen, the posterior

FIG. 5. Rapid fragmentation within six days of a specimen of the stomatopod Squilla empusa (A–D) after soft tissue had decayed during the trial experiment. Carapace length = 22.6 mm; abdomen length = 51.1 mm; telson length = 15.0 mm. See also Klompmaker et al. (2017) for time- lapse movie of this process. Colour online. 10 PALAEONTOLOGY carapace region and the non-cheliped appendages These results suggest that decay rate is an important fac- (Fig. 2C). tor of the apparent diversity of fossil arthropods.

Comparative taphonomic analyses DISCUSSION

Comparison within taxa. Under the experimental condi- Sources of variation tions, distinct increases in the taphonomic scores occurred from c. 50 days for most specimens and both Algal growth occurred frequently during the full experi- methods (Figs 7–8). Differences in decay rates between ment. Black and green covers on the bottom of the conspecific specimens appeared to be limited as the tra- compartmented aquarium and specimens temporarily jectories of most taxa are tightly spaced, except for the hampered observations, and later dark green–black masses swimming and hermit crabs where the smallest specimen and strings developed in the water column and ultimately of both taxa decayed relatively fast. No obvious size- lifted multiple specimens. This lifting is the prime reason related structuring of decay trajectories was observed, that observations could not be continued for those speci- although the geometric size differences of carapaces are mens. As none of the specimens were scrubbed prior to limited for some taxa (the largest was 33–132% larger placement into the aquarium, algae could have grown than the smallest, see Klompmaker et al. 2017, table S2). from insignificant amounts on any of the specimens. This lack of size-related structuring suggests that compar- However, the most likely source of algal growth were the isons between taxa may be meaningful. barnacles, having the most noticeable amounts of algae on both them and their attachment substrate (plastic Comparisons between taxa. Differences between species hose), even though an attempt was made to remove algae. appeared after c. 50 days (Fig. 9) when using all ten This hypothesis is supported by the fact that the trial scored taphonomic characters (Fig. 9A) as well as for the experiment, for which algal growth was more limited dur- six characters with the highest chance of fossilization ing the first 100 days, did not include barnacles with (Fig. 9B). Subsequently, pink shrimps decayed fastest fol- algae growing on them. Although we were primarily lowed by stomatopods for both methods. There is sepa- interested in decay rate between taxa instead of absolute ration between the lowest scores of the five shrimp decay rates, algal growth may have influenced the decay specimens and the highest scores for stomatopods for rate by encasing the specimens when the specimens were the first method, suggesting that decay differences are still on the bottom so that disarticulation was inhibited. meaningful, whereas there is some overlap using the sec- Future work will attempt to minimize algal growth so ond method. Barnacles show different trajectories for the that the decay process can be observed more continuously two methods because the non-calcified appendages and for a longer duration. decayed fast, but only calcified parts were included for It is possible that the absolute decay rate was influ- the second method. The swimming crabs, horseshoe enced by the method of dispatching the specimens. Freez- crabs, hermit crabs and the lobster show overlap for the ing in freshwater may have loosened the cuticle, although available trajectories. Using method 1, the calico crabs we did not note any major damage afterwards, and may appear to have experienced the slowest decay rates and have harmed microbes that are critical in the decay pro- show no overlap with others, even for their highest cess so that results may not entirely mimic of what would taphonomic scores. Horseshoe crabs show overlapping happen on the seafloor. The relative decay rate, the main scores with calico crabs for method 2, even though the factor of interest herein, may not have been altered sub- horseshoe crabs could be observed for <100 days only. stantially because circumstances were similar for each In summary, shrimps and stomatopods decayed fastest, specimen. Additionally, the sequence of morphological whereas calico crabs experienced the slowest decay rate changes is unlikely to be affected by different boundary for method 1. The fastest decaying taxa were the same conditions (e.g. Briggs 1995). for method 2, but barnacles decayed more slowly than calico crabs. The results are supported by the modern and fossil Implication for the preservation of eyes record of these arthropods based on two preservation potential metrics (Table 3). Both the decay rate rank vs The study of the evolution of vision hinges largely on percentage of genera missing from fossil record and decay preserved eyes (e.g. Aberhan et al. 2012) although socket rate rank vs extant species/species in Cenozoic fossil size has been used as a proxy for eye size (e.g. Klomp- record are significantly correlated (Spearman rs = 0.955, maker et al. 2016). Ample research on the vision of other p = 0.003; Spearman rs = 0.937, p = 0.005; respectively). arthropods such as trilobites has been performed (e.g. KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 11

A B

1.00 Carapace size (mm) 1.00 Carapace size (mm) 16.3 20.7 0.75 17.5 0.75 21.3 17.8 22.1 0.50 22.3 0.50 23.1 27.8 27.5 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

C D

1.00 Carapace size (mm) 1.00 Carapace size (mm) 11.5 07.2 0.75 12.6 0.75 07.9 14.3 10.6 0.50 20.9 0.50 11.5 26.7 14.7 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

E F

1.00 Carapace size (mm) 1.00 Carapace size (mm) 09.4 09.4 0.75 10.0 0.75 12.4 11.1 13.2 0.50 11.5 0.50 13.9 13.1 14.2 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

G H

1.00 Diameter (mm) 1.00 Carapace size (mm) 5.0−16.1 17.8 0.75 0.75

0.50 0.50

0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200 Days since start experiment Days since start experiment FIG. 7. Per-specimen per-species scores using all taphonomic characters. Carapace size represents the geometric mean of the length, width and height. The lines discontinue once a specimen is picked up by algal strings. A, horseshoe crabs (Limulus polyphemus). B, cal- ico crabs (Hepatus epheliticus). C, swimming crabs (Portunus gibbesii). D, hermit crabs (Clibanarius vittatus). E, pink shrimps (Penaeus duorarum). F, stomatopods (Squilla empusa). G, barnacles (Amphibalanus eburneus). H, lobster (Panulirus versicolor). 12 PALAEONTOLOGY A B

1.00 Carapace size (mm) 1.00 Carapace size (mm) 16.3 20.7 0.75 17.5 0.75 21.3 17.8 22.1 0.50 22.3 0.50 23.1 27.8 27.5 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

C D

1.00 Carapace size (mm) 1.00 Carapace size (mm) 11.5 07.2 0.75 12.6 0.75 07.9 14.3 10.6 0.50 20.9 0.50 11.5 26.7 14.7 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

E F

1.00 Carapace size (mm) 1.00 Carapace size (mm) 09.4 09.4 0.75 10.0 0.75 12.4 11.1 13.2 0.50 11.5 0.50 13.9 13.1 14.2 0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200

G H

1.00 Diameter (mm) 1.00 Carapace size (mm) 5.0−16.1 17.8 0.75 0.75

0.50 0.50

0.25 0.25 Taphonomic score Taphonomic 0.00 0.00 0 50 100 150 200 0 50 100 150 200 Days since start experiment Days since start experiment FIG. 8. Per-specimen per-species scores using six taphonomic characters (articulation and fragmentation of calcified/chitinous parts assessed only). Carapace size represents the geometric mean of the length, width and height. The lines discontinue once a specimen is picked up by algal strings. A, horseshoe crabs (Limulus polyphemus). B, calico crabs (Hepatus epheliticus). C, swimming crabs (Portunus gibbesii). D, hermit crabs (Clibanarius vittatus). E, pink shrimps (Penaeus duorarum). F, stomatopods (Squilla empusa). G, barnacles (Amphibalanus eburneus). H, lobster (Panulirus versicolor). KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 13

A B 1.00 Arthropod clade 1.00 Barnacles Calico crabs Hermit crabs 0.75 Horseshoe crabs 0.75 Lobster Shrimps Stomatopods Swimming crabs 0.50 0.50

Taphonomic score Taphonomic 0.25 0.25

0.00 0.00

0 50 100 150 200 0 50 100 150 200

C D 0.8

0.6

0.6

0.4 0.4

0.2 Taphonomic score Taphonomic 0.2

0.0 0.0

0 50 100 150 200 0 50 100 150 200 Days since start experiment Days since start experiment FIG. 9. Comparisons of taphonomic scores between arthropod species. Mean taphonomic scores per species using ten (A) and six (B) characters. Shaded bands represent the minimum and maximum scores for five specimens per species using ten (C) and six (D) characters (barnacles and lobster are excluded). The lines and bands discontinue when one of the specimens per species is lifted by algal strings.

Clarkson 1979; Schoenemann & Clarkson 2013, 2017; show that some hardened parts decay faster than others. Tanaka et al. 2015) due to the calcified lenses of their Since most pink shrimps had largely or entirely decayed compound eyes. Although the primarily less-calcified eyes without leaving identifiable hard parts during the trial of other marine arthropods groups including crustaceans and full experiments prior to being lifted by algae, either can preserve in Konservat-Lagerst€atten, the stratigraphic none or a great portion of the shrimp body could be record of such eyes is patchier (e.g. Tanaka et al. 2009; expected to be preserved as a fossil. This hypothesis is lar- Paterson et al. 2011; Schoenemann et al. 2012; Anderson gely consistent with the fossil record of shrimp that are et al. 2014; Audo et al. 2016; Poschmann et al. 2016; capable of swimming (Dendrobranchiata and Caridae) Vannier et al. 2016). Our experiment suggests that the which yields specimens that are often complete or nearly relatively fast decay of eyes relative to other parts of the so (e.g. Carriol & Riou 1991; Schweigert & Garassino arthropod body explains the patchy record of poorly 2004; Feldmann & Schweitzer 2010; Audo & Charbonnier calcified eyes. Specimens that do show such eyes were 2013; Garassino et al. 2013; Huang et al. 2013; Pinheiro preserved under favourable taphonomic conditions. et al. 2014; Schweitzer et al. 2014; Winkler 2016). Such specimens are predominantly preserved under favourable preservational conditions in thinly-bedded limestones of Implications for the preservation of individual taxa Konservat-Lagerst€atten. Conversely, differential preservation potential of parts Little differential decay within species was observed for of specimens of barnacles, swimming crabs, hermit crabs pink shrimps, horseshoe crabs, calico crabs and the lob- and mantis shrimps were observed. As would be expected ster, but longer experiments for the latter three taxa may based on the outcome of the full experiment, barnacle 14 PALAEONTOLOGY

TABLE 3. Data on the modern and fossil record of the marine macroarthropod clades studied followed by metrics of preservation potential including one based on our experiment with the lowest number representing the lowest observed decay rate.

Common Clade name(s) Extant Extant Species found Species in Extant species Extant genera Extant % Genera Provisional rank name(s) species genera as fossils Cenozoic with fossil record with fossil record species/species missing from our experiment fossil record in Cenozoic fossil record (using Fig. 9B) fossil record

Hermit crabs Paguroidea 1057 120 128 60 16 13 17.6 89.2 5 True crabs Brachyura 6559 1298 2057 1564 276 253 4.2 80.5 3 Swimming Caridea and 3808 436 155 32 0 10 119.0 97.7 7 shrimps Dendrobranchiata Lobsters Polychelida, 833 74 515 37 8 9 22.5 87.8 3 Glypheidea, Astacidea and Achelata Horseshoe crabs Xiphosura 4 3 46 1 0 2 4.0 33.3 2 Stomatopods or Stomatopoda 449 111 33 18 0 7 24.9 93.7 6 mantis shrimps Barnacles Cirripedia 809 152 497 364 64 62 2.2 40.8 1 (Thoracica)

The ranks for lobsters and crabs are the same because the trajectory for the lobster is in between that the two crabs (Fig. 9B). Data sources: Foster & Buckeridge (1987); Hauschke & Wilde (2004); Schram & Muller€ (2004); De Grave et al. (2009); Klompmaker et al. (2013); Lamsdell (2016); Paleobiology Database. KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 15 wall plates and opercular plates are often found in the et al. 2010, 2015) but also in isolation (Ando et al. 2013, fossil record (e.g. Darwin 1855; Buckeridge 1983; Zullo 2015, 2016). The fact that isolated raptorial dactyli and 1992; Carriol & Schneider 2013; Collins et al. 2014; Gale mandibles are not often figured relative to (nearly) com- & Sørensen 2015; Klompmaker et al. 2015a;Kocı et al. plete stomatopods in the fossil record (Hof & Briggs 2015) whereas soft tissue preservation (including the 1997, table 4) despite their higher preservation potential, appendages) is extremely rare (Briggs et al. 2005). The suggests that these dactyli are under-represented in the same applies to swimming crabs because often only the literature, probably because they are not recognized and/ chelipeds, carapace and/or ventral side of fossil members or related to the fact that isolated raptorial dactyli may of swimming crabs (Portunidae) are preserved (e.g. Vega have limited taxonomic value (see also below). et al. 1999; Schweitzer & Feldmann 2000; Beschin et al. Bopyriform swellings (Fig. 6), termed Kanthyloma 2001; Nyborg et al. 2003; Varela & Schweitzer 2011). crusta Klompmaker et al., 2014, are well-known from the However, chelipeds and carapaces are more diagnostic fossil record (e.g. Wienberg Rasmussen et al. 2008; and therefore end up more often in the taxonomic litera- Klompmaker et al. 2014; Klompmaker & Boxshall 2015) ture than other appendages do. but body fossils of the inferred isopod culprits are Although hermit crab inhabitation of now fossilized unknown from within decapod fossils. Our results gastropods can be recognized (Walker 1992), the hermit directly show that these isopods decay fast, also compared crab body fossil record is dominated by chela (e.g. to their host, and are unlikely to preserve unless early Aguirre-Urreta & Olivero 1992; Fraaije 2003; Cronier^ & mineralization has halted decay. Courville 2004; Beschin et al. 2007; Schweigert et al. 2013; Hyzny et al. 2016) but also increasingly by isolated sixth abdominal tergites (mostly ascribed to (para)py- Implications for biodiversity patterns lochelids) and anterior parts of carapaces (e.g. Van Bakel et al. 2008; Fraaije et al. 2012a, b, 2013, 2014; Fraaije Although our results are preliminary because of one 2014) whereas only two nearly complete fossil hermit experimental setup and algal growth hampering observa- crab specimens are known to date (Garassino et al. 2009; tions, the differences in relative decay rates between the Schweigert et al. 2013). The hermit crab in this study, eight clades may shed light on the abundance and diver- Clibanarius vittatus, is a member of the Diogenidae and sity of fossil arthropods. The different decay rates may at does not have a strongly calcified sixth abdominal tergite least in part be explained by the degree of calcification (rather, weakly calcified remnants of the abdominal seg- and the overall cuticle thickness (cf. Amato et al. 2008; ment(s) are present), but our observations indicate that Mutel et al. 2008). The moderate to low decay rates of chela, dactyli of other appendages, the anterior part of horseshoe crabs, as also observed by others in mostly the carapace and the telson have a relatively high preser- tumbling experiments (Babcock & Chang 1997; Babcock vation potential for this taxon. This hypothesis largely et al. 2000; Tashman 2014), are consistent with the sug- agrees with the fossil record of paguroids (see references gestion that the chitinous exoskeleton of horseshoe crabs above) but isolated fossil non-cheliped dactyli and telsons is resistant to decay (Baas et al. 1995) compared to other would be difficult to ascribe to hermit crabs because of a arthropods studied herein. Moreover, chitin is known lack of diagnostic characters for assigning them to hermit from the fossil record (Stankiewicz et al. 1997; Ehrlich crabs. Moreover, hermit crab telsons are difficult to find et al. 2013). Thus, the observed relatively low genus and due to their small size. species richness of xiphosurids through the Phanerozoic In agreement with Hof & Briggs (1997, p. 435), our (Rudkin & Young 2009; Lamsdell 2016, fig. 2) is not as results indicate that raptorial dactyli of stomatopods have severely influenced by preservational factors as hypothe- a relatively high preservation potential. These dactyli have sized (Rudkin & Young 2009), but may have some bio- indeed been fairly well-documented in the fossil record of logical implication in that their fossil record, although stomatopods, either as part of the stomatopod body incomplete, was never as rich as for the other crustacean under favourable preservational circumstances (e.g. De clades studied herein. Angeli & Messina 1996; Hof & Schram 1998; Jenner et al. Similarly, our experiment suggests that barnacles have 1998; De Angeli & Beschin 2006; Ahyong et al. 2007; a relatively high preservation potential, although their Cunningham et al. 2008; Haug et al. 2010) or as isolated genus and species richness throughout the Phanerozoic is elements (e.g. Hof & Briggs 1997; De Angeli & Beschin not extremely high with 93 genera and 497 species 2006; Ando et al. 2013, 2015, 2016, Haug et al. 2013, reported (Foster & Buckeridge 1987; Sepkoski 2000). This 2016). We also noted the presence of likely mandibles pattern of low diversity can at least in part be explained well after the stomatopod body had disintegrated because sediments deposited in the intertidal range, where (Fig. 2D) and they have been found as fossils in (near) many barnacles live today, are prone to erosion. There is complete specimens occasionally (Jenner et al. 1998; Haug also a paucity of barnacle systematists. 16 PALAEONTOLOGY

As for the horseshoe crabs and barnacles, the two taxa. Indeed, the fossil record of stomatopods consists of brachyuran crabs and the lobster species also show rela- 33 species while only 155 fossil species of Caridea and tively low decay rates, indicating that they may preserve Dendrobranchiata were known in 2009 (Table 3). Preser- reasonably well. Unlike xiphosurids and the Cirripedia vational circumstances must be ideal for entire stom- however, at least the true crabs have a relatively rich fos- atopods to preserve, which is consistent with the fact that sil record with >2000 species of true crabs (infraorder they are often reported from Konservat-Lagerst€atten (Hof Brachyura), whereas c. 550 lobster species (infraorders & Briggs 1997; Hof 1998). Our experiment shows that Polychelida, Glypheidea, Astacidea and Achelata) are raptorial dactyli have a relatively high preservation poten- known (De Grave et al. 2009; Schweitzer & Feldmann tial, yet their fossil record is sparse (Hof & Briggs 1997; 2014). The diversity and body size of true crabs and lob- Hof 1998). Assigning isolated raptorial dactyli to lower sters first increased significantly as part of the Mesozoic taxonomic ranks appears to be difficult, especially for taxa decapod revolution (Klompmaker et al. 2013, 2015b), that may not have modern representatives (see also Haug followed by a decrease in raw genus richness for lobsters et al. (2013, 2016)), but further investigation appears (Schweitzer & Feldmann 2014) and an increase in raw warranted. brachyuran species richness (Schweitzer & Feldmann The fossil record of the shrimps (Caridea and Dendro- 2015). branchiata) is very fragmentary with major occurrences in The preservation potential of hermit crabs, as deter- Mesozoic Konservat-Lagerst€atten (e.g. Carriol & Riou mined by our experiment, relative to other clades requires 1991; Schweigert & Garassino 2004; Klompmaker et al. more research because many of the specimens were cov- 2013; Santana et al. 2013). However, they also occur as ered by too much algae during the greater portion of the fairly complete specimens in Cenozoic deposits occasion- 205 day survey, except for the smallest specimen. Never- ally (e.g. Garassino & Teruzzi 1996; Garassino & Jakobsen theless, their decay rate appears to have been slower than 2005; Garassino et al. 2014). Since they usually have no that of shrimps and stomatopods, supported by observa- parts with a high preservation potential, this pattern is tions during the trial experiment. This hypothesis is con- not expected to change with targeted searches in other firmed by their comparatively decent fossil record starting deposits. Diversity analyses focusing on shrimps or in the Jurassic (e.g. Schweigert et al. 2013; Fraaije 2014) including shrimps as a major component will not yield although taxa are often based on isolated chela, carapaces biologically meaningful patterns. The fact that shrimps and sixth abdominal tergites (i.e. parataxonomies), and decay faster than stomatopods was also pointed out by linking carapaces to tergites (as attempted first by Fraaije Hof & Briggs (1997), who compared results from a previ- et al. 2013) and ultimately chela will be necessary to ous study with the same experimental setup as theirs. assess the true diversity of paguroids. This relatively This similarity suggests that relative decay rates based on decent fossil record is supported by the preservation one or a few taxa may be generalized for this entire potential metrics based on the modern and fossil record group. The difference in decay rate between stomatopods (Table 3). and shrimps appears to be related the larger proportion The relatively fast decay rates of stomatopods and of decay-resistant chitin in stomatopods (Hof & Briggs shrimps suggest a low preservation potential for these 1997).

TABLE 4. Characters commonly used for species-level assignment in fossil arthropods and the best-preserved characters per group based on our experiment.

Common name(s) Clade name(s) Characters commonly used for Well-preserved at end experiment or species-level assignment in fossils last element preserved

Hermit crabs Paguroidea Carapaces and/or claws or sixth Claw, anterior part carapace abdominal tergites True crabs Brachyura Carapaces and/or claws Carapaces and claws Swimming shrimps Caridea and Dendrobranchiata Rostrum, carapace, abdomen All and/or appendages Lobsters Polychelida, Glypheidea, Carapace, abdomen and/or claws Carapace and abdomen Astacidea and Achelata Horseshoe crabs Xiphosura Prosoma and opisthosoma Prosoma, opisthosoma and telson Stomatopods or Stomatopoda Telson, abdomen and/or carapace Raptorial dactyli and mandibles mantis shrimps Barnacles Cirripedia (Thoracica) Wall and opercular plates Wall and opercular plates KLOMPMAKER ET AL.: ARTHROPOD EXPERIMENTAL TAPHONOMY 17

Stemward slippage in arthropods? 4. Major differences were apparent in the decay rates between species, with shrimps and stomatopods Stemward slippage can occur when phylogenetically decaying fastest, whereas the lobster, calico crabs, important characters decay faster than less informative horseshoe crabs and barnacles showed relatively slow characters, as shown for chordates and vertebrates (San- decay rates. Barnacles had the slowest decay rate som et al. 2010, 2011) but not for hemichordates and vel- when only calcified/chitinous parts were evaluated. vet worms (Murdock et al. 2014; Nanglu et al. 2015; Beli 5. The results of our experiment are supported by two et al. 2017). Of the ten taphonomic characters scored preservation potential metrics using the modern and (Table 2), four may be used to evaluate stemward slip- fossil record of the studied arthropods clades. page: carapace completeness, claw completeness, abdomen 6. We speculate that stemward slippage may not be completeness and telson completeness. These are all char- ubiquitous in marine arthropods. acters that are used frequently in erecting fossil species of 7. Our results provide an improved framework for the arthropod clades herein (Table 4). Pronounced differ- understanding arthropod biodiversity through time. ential decay occurred in the hermit crab and stomatopod Diversity studies of brachyuran crabs, lobsters, horse- species. The characters that decay relatively slowly for shoe crabs and barnacles are more likely to yield pat- hermit crabs are frequently used to determine fossil taxa terns that are closer to their true biodiversity than to the species-level (Table 4). Conversely, the decay-resis- those for stomatopods, shrimps and hermit crabs. tant elements of stomatopods, isolated raptorial dactyli and mandibles, cannot be used for species-level ascription Acknowledgements. We thank Stephan Barron (Department of generally, but genus- and family-level assignments may be Biology, University of Florida), Gustav Paulay (FLMNH, Univer- possible (Ahyong et al. 2013; Ando et al. 2013, 2015, sity of Florida) and Sean Roberts (FLMNH, University of Flor- 2016; Haug et al. 2016). Thus, stemward slippage may ida) for equipment-related logistics. Two scientific reviewers and editor Andrew Smith made very helpful comments that substan- occur for stomatopods. Other arthropods herein showed tially improved the quality of this article. AAK is very grateful to a lower degree of differential decay and the parts that The Palaeontological Association for providing funding for this appear to preserve best are often used for species-level ongoing research (PA-RG201401). This is University of Florida ascriptions (Table 4). Although more detailed analyses are Contribution to Paleobiology 823 and Paleobiology Database needed to determine whether stemward slippage is an publication 287. issue for arthropods, we speculate that stemward slippage may not be ubiquitous in marine arthropods because decay-resistant characters are usually phylogenetically DATA ARCHIVING STATEMENT informative for low taxonomic ranks. Data for this study (3 supplementary tables, 10 figures and 1 movie) are available in the Dryad Digital Repository: https://doi.org/10.5061/ CONCLUSIONS dryad.4fj7r

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