ECHINOIDS AS SUB STRATES FOR ENCRUSTATION –
RE VIEW AND QUAN TI TA TIVE ANAL Y SIS
Tomasz BORSZCZ
In sti tute of Oceanology, Pol ish Acad emy of Sci ences, Powstañców Warszawy 55, 81-712 Sopot, Po land, e-mail: tomekb@iopan.gda.pl
Borszcz. T., 2012. Echinoids as sub strates for encrustation – re view and quan ti ta tive anal y sis. Annales Societatis Geologorum Poloniae, 82: 139–149.
Ab stract: The ex ist ing lit er a ture, in clud ing re cords of both fos sil and ex tant echinoid encrustation, is quan ti -ta tively ana lysed and re viewed. This shows that echinoid encrus-tation (num ber of en crusted echinoid - tapho-coenoses) has in creased nearly con tin u ously and dra mat i cally to the pres ent day, as con firmed by lin ear re gres sion val ues of more than 85 per cent. It also dem on strates that cur rent lev els of echinoid foul ing sta bi lised by the Mio cene, while there has been a more or less con tin u ous re cord of echinoid encrustation since the Late Cre ta ceous. Sev eral in creases have been iden ti fied since echinoid encrustation first noted oc cur rence from the Late Car bon if er ous. This trend is ex plained as the prob a ble re sult of cor re spond ing in creases in pro duc tiv ity (rich ness, bio mass, energetics, ecospace uti li sa tion) and re sources in the ma rine en vi ron ment, in clud ing epibionts and their hosts. This con clu sion matches other in di ca tors, in clud ing the num ber and thick ness of shell beds, bioerosion and pre da tion in ten sity or biodiversity. The tra jec tory might have been al tered to some de gree by bi ases (e.g. se lec tive re cord ing, sam pling ef fort, out crop area, rock vol ume) in the same way as palaeobiodiversity es ti mates. Two re cog nised long-term gaps in echinoid encrustation (Up per Or do vi cian–Lower Car bon if er ous and Perm ian–Lower Cre ta ceous) are ex plained in part as bias and as bi o log i cal and taphonomic sig nals. These gaps are caused mostly by the rapid disarticulation of Palaeozoic-type echinoids, the meth od ol ogy ap plied here, and a lack of in ter est in the encrustation of Ju ras sic echinoids. Con versely, three short-term gaps in the Ce no zoic are in ter preted ex clu sively as bias. If cor rect, the pres ent study dem on strates quan ti ta tively the step-wise in crease of pro duc tiv ity through time. It also sug gests po ten tial fo cus on fur ther study, in clud ing the col lec tion of new data from the field and pre-ex ist ing col lec tions, as best for other encrustation prox ies (e.g., per cent of cov er age by epibionts, ra tio of en crusted to nonencrusted shells, taxa rich ness or nu mer i cal abun dance of sclerobionts) in cases of large-scale anal y ses.
Key words: Echinoids, encrustation, Re cent, fos sil re cord, pat terns, meta-anal y sis, re view. Manu script re ceived 3 June 2012, ac cepted 3 Oc to ber 2012
IN TRO DUC TION
Echinoids first ap peared in the fos sil re cord in the lat est Or do vi cian (e.g., Kier, 1965; Smith, 1984; Smith and Savill, 2001; Sprin kle and Guensburg, 2004), as rep re sen ta tives of the Great Or do vi cian Biodiversification Event (re view in Webby et al., 2004). How ever, as they have been eco log i -cally sig nif i cant only since the Me so zoic, they are gen er ally clas si fied as “mod ern fauna” (e.g., Sepkoski, 1981). On the other hand, in mod ern set tings they are a di verse and abun dant group, and suc cess fully serve as one of the fun da men -tal com po nents of many ben thic com mu ni ties around the world, com pris ing, with other echinoderms, up to 90 per cent of the bio mass in equa to rial to po lar en vi ron ments (e.g., Smith, 1984). Echinoid his tory spans var i ous, sub -stan tial events (e.g., Kier, 1982; Smith, 1984), in clud ing the evo lu tion of the first ir reg u lar forms dur ing the Ju ras sic, re -lated infaunalisation, and the ap pear ance of sand dol lars, with nu mer ous mor pho log i cal in no va tions dur ing the Ce no
-zoic. In ad di tion, it is worth not ing that Foote and Sepkoski (1999) showed that the echinoid fos sil re cord is fairly com -plete and better than that of any other echinoderm class. Through out their his tory, they have pro vided di verse sub strates for colo nis ation by var i ous sclerobionts (sensu Tay -lor and Wil son, 2002, 2003). This makes them a use ful tool for both long-term and large-scale stud ies.
In spite of a long and rich his tory of re search and apart from phylo gen etic anal y ses, in cor po rat ing a geo log i cal time scale (see Kroh and Smith, 2010), only about a dozen stud -ies so far have fo cused on the quan ti ta tive treat ment of echinoids as a macroecological and macroevolutionary model group, ana lysed ‘through time’ (Kier, 1974, 1977a; McKinney, 1986; Greenstein, 1992; Smith, 1992, 2001, 2007a; Smith and Jeffery, 1998; Eble, 2000; Smith et al., 2001; Villier and Eble, 2004; Villier and Navarro, 2004; Smith and Stockley, 2005; Bar ras, 2008). This is es pe cially
low, by com par i son with in ves ti ga tions, fo cus ing on bi -valves and many gen eral stud ies, in cor po rat ing echinoids as one of many tar get groups (e.g., Sepkoski, 1981; Jablonski and Bottjer, 1991; Jablonski, 1993; Benton, 1995; Foote and Sepkoski, 1999; Bambach et al., 2002; Alroy et al., 2008). How ever, an a lyt i cal ap proaches, in te grat ing case stud ies from the lit er a ture or many new, lo cal field in ves ti -ga tions in one anal y sis (meta-anal y sis), like “through-time anal y ses”, have shaped many is sues in geobiological re -search. Ex am ples of these is sues in clude geo chem is try and biomineralogy (e.g., Kiessling et al., 2008; Zhuravlev and Wood, 2008), palaeobiodiversity (e.g., Sepkoski, 1993; Benton, 1995; Powell and Kowalewski, 2002; Alroy et al., 2008), taphonomy (e.g., Allison and Briggs, 1993a) and evo lu tion ary palaeo ec ol ogy (e.g., Kidwell and Brenchley, 1994; Trammer and Kaim, 1997; Trammer, 2005; Hunt ley and Kowalewski, 2007; Pow ers and Bottjer, 2007).
Encrustation, also known as bioencrustation, biofouling or epibiosis, is a wide spread pro cess of per ma nent at tach -ment by ses sile or gan isms to sub strates of bi o log i cal and non-bi o log i cal or i gin, pri mar ily in ma rine en vi ron ments, and rang ing through geo log i cal time to the pres ent day (for re views see e.g., Wahl, 1989; Tay lor and Wil son, 2003; Kukliñski, 2009). Un til now, only a few stud ies re searched large-scale trends of encrustation through geo log i cal time, in spite of a few de cades of in ten sive field work, of fer ing a suf fi cient da ta base for meta-anal y sis. For in stance, Palmer (1982; up dated by Wil son and Palmer, 1992) ana lysed the di ver sity of epibionts on hardgrounds from the Cam brian to the Cre ta ceous. Hansen (1988) in ves ti gated the abun dance and di ver sity of ses sile sus pen sion-feed ing bi valves through time, while McKinney (1995), fol lowed by Barnes and Dick (2000; see also Barnes, 2006), tracked the com pet i tive in ter -ac tions of bryo zoans through the last 100 Ma. Re cently, Tay lor (2008) tal lied a num ber of stud ies of hardgrounds as prox ies for test ing their dis tri bu tion against past ocean chem is try. There are only a few re cords of the long-term his tory of echinoids as sub strates for colo nis ation, which is also true for other pat terns of encrustation (see also Lescinsky, 2001; Tay lor and Wil son, 2003). Santos and May -oral (2008, p. 317) pointed out that, ‘dur ing a long span in the his tory of life, tests of dead echinoids have ap peared to serve as po ten tial and sta ble sub strata for bioeroders and epibiont col o ni za tion’. Nebelsick et al. (1997, p. 272) men tioned that ‘en crusted fos sil echinoids are known in the fos -sil re cord, es pe cially from the Mio cene and Cre ta ceous’, while Tay lor and Wil son (2003, p. 30) merely stated that, ‘skeletobionts are com mon on some post-Pa leo zoic echi-noids’. All of these ‘con clu sions’ were drawn with out any rig or ous data col lec tion and quan ti fi ca tion, but may stand as test able hy poth e ses, chal lenged in the pres ent pa per.
Here, all ex ist ing lit er a ture sources on echinoid encrustation are re viewed. This should be treated as com ple men -tary to the gen eral com pre hen sive re view by Tay lor and Wil son (2003), where in fact the encrustation of echinoids was treated only su per fi cially. Since then sig nif i cant prog -ress has been made. Fur ther more, re viewed data are used to cre ate a quan ti ta tive anal y sis of echinoid encrustation through time. In this lit er a ture-based study, the num ber of com mu ni ties (taphocoenoses) per time in ter val, where echi-
noids served as sub strate for col o ni za tion, are uti lised for de ci pher ing the tra jec tory of echinoid encrustation through time. This ap proach of ten ta tively fo cus ing on one clade is used as a tool to wards search ing for large-scale trends in encrustation. The au thor con cen trates on quan ti ta tive test -ing of the widely re cog nised, but un tested hy poth e sis (yet of ten used as ‘hard ev i dence’, see e.g., Finnegan et al., 2011) that “encrustation in ten sity” has in creased through time to the pres ent (e.g., Vermeij, 2004), and fo cuses on re -cog nis ing the mag ni tude and tim ing of pre dicted changes.
RE VIEW OF ECHINOID ENCRUSTATION
Only re cently has Schnei der (2003) pro vided the first in sight into echinoid encrustation in the Palaeozoic. She pre sented data from the Up per Car bon if er ous Winchell For -ma tion in Texas (USA), based on hun dreds of echinoids of the or der Cidaroida (see also Schnei der et al., 2005), pre -served as ar tic u lated ma te rial. Schnei der (2003) showed that only spines were en crusted by nu mer ous com men sals, in clud ing brachi o pods and bryo zoans, pref er en tially lo cated on the prox i mal por tion of spines. In ad di tion, she dem on -strated that encrusters showed no host-size pref er ence, and she noted that the costs for echinoids of such an as so ci a tion far out weighed the ben e fits. In the light of a re cent re port by Zapalski (2011), such an in ter pre ta tion is im pos si ble to in -fer from the fos sil ma te rial and thus should be rather treated as un proved. Nev er the less, Schnei der (2003) pro vided the sole ex am ple from the fos sil re cord to date of the in vivo encrustation of echinoids. In that case, encrustation in vivo is sup ported by (i) the set tle ment of episkeletobionts ex clu -sively on echinoid spines, (ii) the rapid burial of echinoids dur ing life or shortly af ter death, pre clud ing post-mor tem encrustation, and (iii) the non-ran dom dis tri bu tion of encrusters. A search for re cords of echinoid encrustation from Perm ian to Early Cre ta ceous yielded no re sults, an ob -ser va tion that is dis cussed be low.
There are a few pa pers on encrustation pro cesses of Late Cre ta ceous age, mostly from Eu rope (Ta ble 1). Sub strates for colo nis ation are var i ous echinoid clades, pref er -en tially spatangoids and holasteroids (e.g., Kidwell and Baumiller, 1990; Kudrewicz, 1992; Rose and Cross, 1993; Olszewska-Nejbert, 2007), the dom i nant groups at that time. To date, the best ex am ples from the Up per Cre ta ceous were pro vided by Zamora et al. (2008) and Borszcz et al. (2012). Zamora et al. (2008) showed that 94 per cent of echinoids in their ma te rial were colo nised by epibionts, one of the most in ten sive encrustations of echinoids ever re -corded. Kudrewicz (1992), among oth ers, on the ba sis of Santonian echinoids from Po land, pro posed a taphonomic sce nario for echinoids and sug gested the role of encrustation in their postmor tem paths. Borszcz et al. (2012) in tro -duced new ex am ples for echinoneid and holectypoid clades from the Turonian of Po land, which fill some tax o nomic and strati graphic gaps in the re cord of encrustation. Among other is sues, they found a lesser encrustation in ten sity than that, shown by Zamora et al. (2008), which Borszcz et al. (2012) re garded as a “loos en ing effect” in as sem blages, char ac ter ised by mod er ate abun dance and low di ver sity.
A loosening ef fect is a com monly oc cur ring (but rarely in -ves ti gated) phe nom e non and con cerns in stances, where more sub strates are avail able than nec es sary, thus a part of avail able sur faces for encrusters re mains un oc cu pied. Their in ves ti ga tion is the larg est study, fo cus ing on the encrusta-tion of such sub strates to date, and the pla nar pro jec encrusta-tions of epibionts that they pro pose may have a much wider ap pli ca tion. On the ba sis of the di vi sion of an echinoid’s test sur faces on vir tual sec tors, such a pro jec tion al lows the vi su al -iza tion of the dis tri bu tion of encrusters or other is sues (e.g., bioerosion, drill holes, re pair scars) on the tests of echinoids (or other or gan isms).
As with epibionts from other times, Late Cre ta ceous echinoids have been il lus trated on nu mer ous oc ca sions, but epibionts have not been spe cif i cally noted or, more im por -tantly, stud ied in de tail (see e.g., Ma³ecki, 1982; McKinney, 1995; Gale, 2002a, b; Tay lor and Wil son, 2002).
Ce no zoic re cords are mainly from Eu rope (but see e.g., ElHedeny, 2007) and in clude nu mer ous, en crusted ex am -ples of spatangoids, clypeasteroids and cassiduloids (Ta-ble 1). The most spec tac u lar ex am ple is that by Santos and Mayoral (2008), who found nearly 1,500 spec i mens of bala- nomorph cirripedes, at tached to a sin gle test of Clypeaster from the Mio cene of Spain. Balanomorph bar na cles were wide spread and com mon encrusters in the Neo gene (see also e.g., Seilacher, 1979; Philippe, 1983). Santos and May oral (2008) also car ried out nu mer ous anal y ses, which dem -on strated the n-on-uni form dis tri bu ti-on of epibi-onts, am-ong other pat terns. Their study in di cated that the set tle ment of the cirripeds was ini tially con trolled by the avail abil ity of free space, while the to pog ra phy of the echinoid test played a mi nor role. In fact, the lat ter is sue, i.e., the im pact of the to pog ra phy of echinoid tests on encrustation pat tern, should be ad dressed more rig or ously in fu ture works.
Ta ble 1
Lit er a ture com pi la tions of Re cent and fos sil echinoid encrustation ex am ples
PERIOD (STAGE) LOCALITY CLADE REFERENCES
Recent Scotia Arc various Linse et al. (2008)
Recent Gulf of Mexico Cidaroida Davis et al. (2005)
Recent Antarctic Cidaroida Cerrano et al. (2009)
Recent Antarctic Cidaroida Gutt and Schickan (1998)
Recent Antarctic various David et al. (2009)
Recent Panama Clypeasteroida Seilacher (1979)
Recent USA, California Clypeasteroida Lescinsky (2001), Giltay (1934), Houk and Duffy (1972)
Recent Red Sea Clypeasteroida Nebelsick (1999a, b)
Recent Adriatic Sea Spatangoida Nebelsick et al. (1997)
Recent France ?Camarodonta Jagt et al. (2007)
Recent Mediterranean Sea Spatangoida Ernst et al. (1973)
Miocene/ Lower France Clypeasteroida Philippe (1983)
Miocene - - Mitroviæ-Petroviæ and Uroševiæ-Daèiæ (1963)
Miocene - Clypeasteroida Mitroviæ-Petroviæ (1972)
Miocene ( Badenian) Croatia various Mikša (2009)
Miocene/ (Eggenburgian) Austria Clypeasteroida Nebelsick (1999a)
Miocene (Eggenburgian) Austria Cassiduloida Nebelsick (1996), Nebelsick et al.(1997) Miocene Egypt Cassiduloida + Clypeasteroida El-Hedeny (2007)
Miocene (Tortonian) Spain Clypeasteroida Santos and Mayoral (2008) Palaeocene (Danian) Italy Spatangoida Giusberti et al. (2005)
Late Cretaceous - - Schmid (1949), Müller, 1969)
Cretaceous/ (Maastrichtian) Germany Camarodonta Jagt et al. (2007) Cretaceous (Maastrichtian) Belgium Holasteroida Jagt et al. (2007) Cretaceous (Santonian) Poland Spatangoida Kudrewicz (1992) Cretaceous (Santonian) Spain Spatangoida Zamora et al. (2008)
Cretaceous (Turonian-Campanian) England various Kidwell and Baumiller (1990), Rose and Cross (1993)* Cretaceous (Turonian-Coniacian) Kazakhstan various Olszewska-Nejbert (2007)
Cretaceous (Turonian) Poland Echinoneida + Holectypoida Borszcz et al. (2012) Carboniferous (Missourian) USA, Texas Archaeocidaridae Schneider (2003) * ex cluded from finer-scale anal y sis
All of these ex am ples come from post-mor tem encrus-tation. This may be iden ti fied by as pects of encrustation that can not be rec on ciled with live echinoids: (i) Dur ing life, echinoid tests are cov ered by epi der mis, pro duc ing anti-foul ing sub stances such as biocides (e.g., McKenzie and Grigolava, 1996). (ii) A dense spine can opy in some taxa pre vents encrustation. (iii) The encrustation of oral sides is pre cluded dur ing life, be cause this part of tests is close to the sea floor in epifaunal ex am ples, or is bur ied in sed i ment in semi-infaunal rep re sen ta tives (infaunal spe cies bur ied whole). (iv) In ner test sur faces (e.g., Jagt et al., 2007) of live or gan isms are in ac ces si ble to colo nis ers. The pres ence or ab sence of stereom mal for ma tions in places of encrustation or epibionts embedment within test walls/spines pro vide di rect in di ca tions of when the echinoderm skel e ton was set tled upon, i.e. dur ing life (syn vivo) or af ter death (postmor
tem). An in hib it ing (antifouling) role for pedicellariae is de
-bat able (see Camp bell, 1983; Schnei der, 2003; Coppard et
al., 2012). More over, Camp bell and Rain bow (1977) ar
gued that set tle ment of the cyprid lar vae of bar na cles is im -pos si ble, when spines and pedicellariae were ac tive, on the ba sis of ex per i ments with set tle ment slates, coated with var -i ous parts of the ech-ino-id test, -in clud -ing -interambulacral plates. They also noted that there was no re pul sion, due to the chem i cal prop er ties of the ep i the lium or the pedicel-lariae.
In Re cent set tings, ex am ples of echinoid encrustation are known mostly in the Ant arc tic (Gutt and Schickan, 1998; Linse et al., 2008; Cerrano et al., 2009; Da vid et al., 2009), and Red and Med i ter ra nean Seas, while noth ing is known from e.g., the Arc tic. Among these pa pers, Da vid et
al. (2009) ques tioned the adap tive sig nif i cance of the cor ti
cal stereom layer. Linse et al. (2008) showed a great di ver -sity of epibionts on echinoids, with up to 51 spe cies, found on only 70 cidaroid spec i mens. Echinoid encrustations have been well re cog nised in Re cent set tings of the Med i ter ra nean (Ernst et al., 1973), and com bined with stud ies of fos -sil set tings (Nebelsick et al., 1997; Nebelsick, 1999a, b, 2008). These stud ies re cog nised encrustation, act ing both
syn vivo and post mor tem. In their model study, Nebelsick et al. (1997) in te grated ex tant and fos sil ma te rial to de velop a
taphonomicencrustation model, and showed a dis par ity be tween the two scales of ob ser va tion, sug gest ing that in ves ti -ga tions of fos sil ma te rial clearly need mod ern analogs for com par i son pur poses. Other ex am ples of echinoid encrustation are listed in Ta ble 1.
QUAN TI TA TIVE ANAL Y SIS
Data, meth ods and ra tio nale
The anal y sis of encrustation in ten sity is based on sam-pling of the ex ist ing lit er a ture. In ad di tion to a li brary search, in clud ing ref er ences in ex ist ing echinoid encrustation pa pers, the fol low ing elec tronic da ta bases were used: Scopus, Sci
-ence Di rect, Ingenta, Geo ref and Google-Scholar. Echinoid
encrustation re ports are rather ran domly dis trib uted in the lit er a ture, but some rel e vant jour nals, such as Palaios,
Geo-bios, Jour nal of Pa le on tol ogy and Fa cies, were checked in
de tail. Apart from a few ex cep tions, mostly peer-re viewed pa pers were used. Lit er a ture data were ‘ver i fied’ by read ing com piled pa pers and such ap proach was suc cess fully ap -plied in other case stud ies (e.g., Schu bert et al., 1997; Kiessling, 2001; Powell and Kowalewski, 2002; Harper, 2003; Fraiser and Bottjer, 2007). In the as sem bled dataset, case stud ies, based only on sin gle spec i mens, were also in -cluded (e.g., Santos and May oral, 2008). Re ports, in which en crusted echinoids are oc ca sion ally il lus trated, but not stud ied or marked ex plic itly, were ex cluded from the anal y -sis. Encrustation in ten sity in the pres ent study, con trary to that re corded by Rodland et al. (2004) for brachi o pods (encrustation fre quency) and Borszcz et al. (2012),where the num ber of en crusted to non-en crusted echinoids were counted, is ana lysed on the ba sis of the num ber (abun dance) of echinoid com mu ni ties (as sem blages) with encrustation per time in ter val through time, re gard less of how many tests were en crusted within par tic u lar cases. A com pi la tion of pa pers, used in the pres ent study, in clud ing geo graphic, strati -graphic and tax o nomic de tails, is pre sented in Ta ble 1.
Encrustation cases (ex clud ing bioerosion) were re -corded by strati graphic and geo graphic unit, the lat ter over a ra dius of 50 km. Data were ana lysed at low and high res o lu tions. In the for mer, in ter vals, such as Perm ian to Early Cre -ta ceous, were used as sin gle time bins. In the lat ter, da-ta were binned to ep ochs or in ter vals, such as “Santonian– Maastrichtian”. As a re sult, six and eight time bins were ap -plied to the lower and higher res o lu tions, re spec tively. The vari a tions in du ra tion of time bins do not gen er ate bias (see be low). For anal y ses, 29 and 26 data points were col lected for the lower and higher res o lu tions, re spec tively. Re gres -sion anal y sis (R2)was used to ex plore the re la tion ships be -tween the num ber of bio/taphocoenoses of echinoids with encrustation (dis tinct echinoid encrustation cases) vs geolo-gical time scale. Sta tis ti cal anal y ses were done, us ing Statistica 8 soft ware and p < 0.05 was as sumed to be sig nif i -cant.
Re sults
The tra jec tory of echinoid encrustation through time (Fig. 1A), based on 29 data points (Ta ble 1), shows a trend of sig nif i cant in crease (R2 = 0.85, p = 0.009). It is also ap -par ent that re cent lev els of encrustation sta bi lised around the Mio cene. Since the Late Cre ta ceous, a more or less con -tin u ous re cord of echinoid encrustation is ob served (see Fig. 1). In re cent times, how ever, rather low lev els of echinoid encrustation have been re corded, but the post-Mio cene time bins are of shorter du ra tion (cf. c. 18 myr in the Mio cene or
c. 15 and 20 myr in sub se quent Late Cre ta ceous bins).
Two longterm gaps were iden ti fied, from the Late Or -do vi cian to the Early Car bon if er ous and from the Perm ian to the Early Cre ta ceous. Ad di tion ally, on a finer time scale, three short gaps were de tected in the Ce no zoic, viz. in the Eocene, Oligocene and PlioPleis to cene. If a lin ear re gres sion were re stricted to the Up per Cre ta ceous–Re cent in ter -val (the last c. 100 Ma), two dis tinct pat terns arose (based on 26 data points). When ana lysed for eight in ter vals (Fig. 1B), lin ear re gres sion in di cated no sig nif i cant re la tion ship (R2 = 0.2; p = 0.26). Al ter na tively, when ana lysed for more
or less timely, stand ard ised in ter vals, with the Palaeo cene, Eocene, Oligocene, Plio cene and Pleis to cene grouped to ad ja cent in ter vals in five time bins, the same an a lyt i cal tech -nique showed a strong re la tion ship near to or exactly 1 (R2 »1; p < 0.01; and R2 = 0.97; p = 0.02), de pend ing on how the bins were amal gam ated. The lat ter anal y sis, i.e., for stand ard ised time bins, should be re garded as valid.
The dy nam ics of encrustation rate (Fig. 1B), spe cif i -cally the mag ni tude of vari a tion in the num ber of encrusta-tion cases, var ies be tween in ter vals. Be tween two bins in the Up per Cre ta ceous, a two-fold in crease was ob served, while there was a de crease in encrustation rate by a fac tor of about 2.5 from the Santonian–Maastrichtian bin to the Pa-leocene bin. This tran si tion, cross ing the Cre ta ceous– Paleogene bound ary, is the sole ex am ple of a de creas ing tra -jec tory, since the start of con tin u ous re cords of echinoid encrustation in the Late Cre ta ceous. From the Paleocene to the Mio cene, the rate of encrustation in creased eight times, and from the Mio cene to the pres ent, this in crease was about 30 per cent.
On the ba sis of avail able data (Ta ble 1), in the past and pres ent, encrusters have uti lised var i ous echinoid clades as sub strate, with out strong pref er ences. Dur ing the Car bon if -er ous, encrust-ers used cidaroids as they do to day. In Re cent com mu ni ties, clypeasteroids, spatangoids, and camarodonts are also oc cu pied by encrusters. In the Cre ta ceous, var i ous ex ist ing clades, such as spatangoids, holasteroids, echino-neids, and holectypoids, among oth ers, were set tled upon. Dur ing the Ce no zoic, most encrustation took place on clypeas ter oids and as so ci ated cassiduloids and spatangoids.
DIS CUS SION
Benton (2009), among oth ers, showed that pat terns, in ferred from the fos sil re cord, may be in ter preted as bi o log i cal and geo log i cal sig nals, that is, as real, bi o log i cal phe -nom ena and bi ases. In the pres ent in ves ti ga tion, the trends de tected may re sult from both. Two ma jor points must be dis cussed: (i) the trend of in creased echinoid encrustation
Fig. 1. Num ber of encrustation cases per time in ter val, plot ted against geo log i cal time scale. (A) lower time res o lu tion for data, since echinoids first ap peared to Re cent (N = 29 data points) and (B) higher time res o lu tion for last ca. 100 Ma of echinoid encrustation (N = 26 data points). Data from Ta ble 1
to wards the pres ent and the re lated sta bili sa tion of “re cent level”, tim ing and mag ni tude of re cog nised changes and (ii) the de tected time gaps in echinoid encrustation.
The ob served in crease in encrustation to wards the pres -ent may be un der stood both as a real sig nal, e.g. caused by par al lel in crease in pro duc tiv ity to wards the pres ent, and as a re sult of bi ases (see Kidwell, 2001). Some of these lat ter may in clude an in crease in out crop area to ward the pres ent and re lated fluc tu a tions over time, im prove ments in the qual ity and fi del ity of the fos sil re cord, ob served as a “Pull of the Re cent” ef fect (but see Jablonski et al., 2003), or se -lec tive re cord ing, which may also serve as an ex pla na tion for the gaps, de tected in echinoid encrustation. Other fac tors (see also e.g., Si gnor, 1982; Allison and Bottjer, 2010), bi as ing palaeobiodiversity es ti mates, may also in clude het er o -ge neous worker ef forts (the “paleontologic in ter est units” of Sheehan [1977]; see also Ber nard et al. [2010]), fluc tu a tions in rock lithification through time (Hendy, 2009; Sessa et al., 2009), sam pling in ten sity (e.g., Westrop and Adrain, 2001), and socio-eco nomic ef fects.
Trends, in ferred in the pres ent study, are in agree ment with pre dic tions of in creases in pro duc tiv ity, energetics, ecospace and guild oc cu pa tion (uti li sa tion), and nu tri ent lev els through out the Phanerozoic (e.g., Vermeij, 1977, 1995; Bambach, 1993, 1999; Wood, 1993; Mar tin, 1996, 2003; Finnegan et al., 2011). This pre dic tion is prob a bly the most ad e quate, bi o log i cal ex pla na tion for this trend and is re garded as their nu mer i cal rep re sen ta tion. This is also strongly sup ported by ev i dence from mod ern en vi ron ments. For ex am ple, Lescinsky et al. (2002) showed that mod ern encrustation was linked with pro duc tiv ity. The ris ing trend is also in agree ment with other known pat terns in the fos sil re cord that show in creases to the pres ent day, such as palaeobiodiversity and drill ing pre da tion in ten sity (e.g., Hunt ley and Kowalewski, 2007), max i mum body size (Payne et al., 2009), num ber of shell beds per time in ter val and their thick ness (Kidwell and Brenchley, 1994; Oji et al., 2003), and echinoid biodiversity (e.g., Kier, 1974, 1977a; Smith, 1984). This fact points to two pos si bil i ties: all of these trends rep re sent bi ases, aris ing from the same source – the fos sil re cord (= ‘com mon cause’), or all of them are true sig nals that are af fected, only by in di vid ual bi ases to some de gree. Encrustation tra jec tory, like in fer ences of pro duc -tiv ity in the fos sil re cord and other pat terns, may be bi ased by a num ber of fac tors. Sheehan (1977) noted that there were many more re search ers, work ing on Cre ta ceous and Ce no zoic strata, than on older rocks. In fact, vir tu ally all re ports, used in this study, con cern the Cre ta ceous and the Ce no zoic, so sam pling ef fort is prob a bly not a suf fi cient ex pla -na tion. Fur ther, se ri ous is sues are out crop area, qual ity and com plete ness of the fos sil re cord. Nu mer ous stud ies (e.g. Raup, 1972; Smith, 2007b; McGowan and Smith, 2008; Smith and McGowan, 2007; Wall et al., 2009; Hannisdal and Pe ters, 2010; Pe ters and Heim, 2010; Dunhill, 2011) sug gest an in crease in out crop area or rock ex po sure for youn ger de pos its and in their in flu ence on the per cep tion of pat terns, in ferred from the fos sil re cord. On the other hand, be tween the Ju ras sic and the Cre ta ceous, as well as in par -tic u lar ad ja cent in ter vals of the Ce no zoic, there are no such dras tic dif fer ences be tween out crops, avail able for the sam
pling of en crusted echinoids. These changes may cause dis -crep an cies in encrustation pat terns. For ex am ple, there are few encrustation cases in the Late Cre ta ceous, but twice as many in the Mio cene. De tected tra jec to ries are there fore re -garded as bi o log i cal in di ca tors. Other types of bias, such as a con cen tra tion of re cords from Eu rope, might af fect the re -sults. Tra di tions of study ing echinoids, great in ter est in study ing encrustation and other agents, re lated to ed u ca tion or fund ing level, all of which may be re garded as ‘socio-eco nomic’ ef fects, are ex pected to be im por tant fac tors in per cep tion (see also Allison and Briggs, 1993b). The ob served trend may also be the re sult of dif fer ences in sam -pling in ten sity (i.e. sam -pling ef fort), which prob a bly could be de tected, when com pared to gen eral ten den cies of encrustation in ves ti ga tions, re corded in the “ma rine hard sub -strate bib li og ra phy” (Wil son, 2008). Fur ther more, in ter est in encrustation in Ju ras sic and Cre ta ceous cases is high and com pa ra ble to lev els in stud ies of the Ce no zoic. There fore, dif fer ences in the num ber of encrustation cases for par tic u -lar in ter vals of the Late Me so zoic and Ce no zoic should not be re garded ex clu sively as the re sult of sam pling ef fort. Se lec tive re cord ing in this case is linked to the fact that Cre ta -ceous and Ce no zoic ma te ri als are en crusted by more di verse epibionts and are more abun dant and more heavily colo -nised, than those of the Ju ras sic and ear lier ma te ri als, thus in creas ing their at trac tive ness to re search ers. This bias may have a strong ef fect on per cep tions of the dis tri bu tion of echinoid encrustation.
The pri mary ob jec tive of the pres ent study was to find how many ex am ples of echinoid encrustation oc curred through geo log i cal time. The in tense fo cus by pre vi ous re -search ers on cases, where en crusted echinoids were fre -quent and wide spread, in fact may have cre ated a re al is tic pic ture of the ex tent, to which each of these in ter vals was pro duc tive for echinoid encrustation.
The tem po ral gaps in echinoid encrustation, noted ear -lier, arise in part from prob lems in meth od ol ogy, but in part they also re flect real ab sences. Some gaps re flect low sam -pling ef fort. For ex am ple, there are a num ber of re cords of en crusted Ju ras sic echinoids (e.g., Hess, 1975), yet the re -ports are not ex plic itly pre sented and they were there fore omit ted from the data com pi la tion. How ever, this ap proach was also ap plied to data from other time in ter vals for sim i lar rea sons and thus the omis sions are prob a bly of rather low sig nif i cance. Fur ther more, from the per sonal field ex pe ri -ence of the au thor, there are nu mer ous lo ca tions in south-cen tral Po land, where Mid dle and Late Ju ras sic en crusted tests and spines have been found, some times even abun -dantly, but these have never been re ported in the lit er a ture. An anal y sis of pub lished data, es pe cially plates in se lected pa pers de scrib ing Palaeozoic echinoids (e.g., Jack son, 1912; Hawkins, 1946; Kier, 1965), echinoid bib lio graphic com pi la tions (Weisbord, 1971) and taphonomic pa pers, deal ing with echinoids and/or echinoderm con tent (e.g., Don o van, 1991; Ausich, 2001), did not show any other ex -am ples like those in Schnei der’s (2003) work and did not in clude epibionts, pre served on il lus trated spec i mens from the Palaeozoic. Only Smith and Hollingworth (1990, fig. 3.1) il lus trated (with out com ment) an interambulacral seg -ment of a Late Perm ian echinoid, colo nised by epibionts on
its in ner sur face, in di cat ing encrustation af ter death. Ad di -tion ally, there are no stud ies that fo cused spe cif i cally on the encrustation of echinoids in Tri as sic and Lower Cre ta ceous de pos its. Il lus tra tions in stud ies of Tri as sic echinoids (e.g., Bather, 1909; Kier, 1968, 1977b, 1984; Hagdorn, 1995; Salamon and NiedŸwiedzki, 2003) show no ex am ples of encrustation. There may be sev eral ex pla na tions for the ap -par ent rar ity of echinoid encrustation in the Palaeozoic and the Tri as sic, in clud ing bi o log i cal sig nals, taphonomic or lit -er a ture ar ti facts (sam pling bi ases). At ten tion should be paid to the fact that echinoids were a group of mi nor, eco log i cal im por tance, with very low abun dance and rich ness, in Palaeozoic com mu ni ties, in di cated e.g., by di ver sity es ti mates (e.g., Smith, 1984), but await ing more re li able quan ti -fi ca tion. They were char ac ter ised by short, thin spines, so colo nis ing or gan isms pref er ences may have been skewed to other ben thic groups that were more abun dant, more re sis -tant, and more sta ble on the sea floor af ter death, such as brachi o pods (e.g., Zatoñ and Borszcz, 2012). Ad di tion ally, this lack of encrustation may be the re sult of the anti-foul ing prop er ties of echinoids, spe cif i cally the cov er ing of tests and ap pend ages by an epi der mis, which pre cluded colo nis ation. Cidaroidlike echinoids are suit able for host ing colo nis ing or gan isms, while alive. They lack an epi der mal cov -er ing on their spines and have only been known to ex ist from the Late De vo nian (e.g., Schnei der et al., 2005) to the Perm ian, a time in ter val, also lack ing sam ples with encrustation of them. Perm ian gaps may be also ex plained sim ply by the over all rar ity of echinoids. This prob a bly ex -plains why all other Palaeozoic echinoids had spines and tests, cov ered by this anti-foul ing pro tec tion, while they were alive, and so they were not en crusted. It should also be noted that tests of all Pa leo zoic echinoids con sist of imbri-cated plates (e.g., Smith, 1984, 2005) that rap idly disarticu-late into iso disarticu-lated os si cles af ter death, and these may have been too small to serve as a sta ble colo nis ation ground. This is in con trast to brachi o pods, which were one of the main hard sub strates of the Palaeozoic (e.g., Bor deaux and Brett, 1990; Tay lor and Wil son, 2003). A third prob a ble in ter pre -ta tion could be that iso lated os si cles of echinoids, which might pre serve epibionts, are of mi nor sig nif i cance to re -search ers, who ne glect them, in fa vour of oth ers groups and ar tic u lated ma te rial if avail able, thus mask ing the real pic -ture (see also e.g., Don o van, 2001 for sim i lar rea son ing in an other case). It is also worth not ing that the “sam pling ar ti -fact” ex pla na tion ex tends to a sug ges tion that palaeontolo-gists may have pre ferred to il lus trate clean, unencrusted spec i mens, and that they may have ig nored in for ma tion, other than the tax o nomic con text of their finds, which may be es pe cially true in cases, where epibionts were over -looked (see also Lescinsky, 1996).
CON CLU SIONS
Echinoids and their encrusters have been poorly ex -plored as a po ten tial tool for as sess ing quan ti ta tive, large-scale pat terns in the ma rine en vi ron ment. The pres ent study fills this gap, and shows an in crease in echinoid encrustation through time. This rise is more or less par al lel to the tra jec
-tory of palaeobiodiversity and other in creas ing trends in the fos sil re cord, and is in ter preted mainly as a prob a ble re sponse to a si mul ta neous rise in pro duc tiv ity and con com i -tant op por tu ni ties for or gan isms and eco sys tems. The encrustation in ten sity level has sta bi lised since the Mio cene, yet since the Late Cre ta ceous there is nearly a con tin u ous re cord. Such a con tin u ous re cord for nearly one hun dred mil lion years makes echinoids a model group for this time in ter val. Fu ture works (see also Brett et al., 2012) should in clude a larger di ver sity of an i mals, as well as a larger num -ber of pa ram e ters, in clud ing, for ex am ple, the per cent age of encrustation cov er age or encrustation in ten sity, mea sured as a ra tio of en crusted to non-en crusted shells. Ad di tion ally, the pres ent study has iden ti fied some gaps in the timeline of echinoid encrustation that war rant fur ther field study, spe -cif i cally in the Ju ras sic.
Ac knowl edge ments
The au thor is very grate ful to Prof. Piotr Kukliñski, Roy Lagemann, Dr Micha³ Zatoñ, Prof. Mark Wil son and es pe cially to Dr Monika Kêdra, Prof. Frank Simpson, Dr John Jagt and Prof. Mike Benton for their valu able prere view com ments and cor rec -tions, lead ing to im prove ment of this pa per. He also thanks Prof. Adam Bodzioch for stim u lat ing dis cus sion and to Dr Paul D. Tay lor for his crit i cal com ments on an ear lier ver sion of the manu -script. Ed i tor, Dr Micha³ Zatoñ, and jour nal re view ers, Prof. Mark A. Wil son and Dr Olev Vinn, are thanked for their kind and help -ful re views. How ever, the au thor alone is re spon si ble for the en tire con tent of this pa per, de spite the crit i cal com ments, pre sented to him. This study was com pleted, thanks to grants from the Na tional Sci ence Cen tre (2011/03/N/ST10/05776 to Tomasz Borszcz) and the Pol ish Min is try of Sci ence and Higher Ed u ca tion (396/N-EOL-ENC/2009/0 to Piotr Kukliñski).
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