Rev. Bio!. Trop., 48(2/3): 333-35 1, 2000 www.ucr.ac.cr www.ots.ac.cr www.ots.duke.edu

Disparity, decimation and the "explosion": comparison of eady Cambrian and Present faunal communities with emphasis on velvet worms ()

Julián Monge-Nájera1 and Xianguang HouZ 1 Biología Tropical, Universidad de Costa Rica, San José, Costa Rica. Fax (506) 2075550; [email protected] 2 Nanjing Institute of Geology and Palaeontology, Academia Sinica, Nanjing 210008, China; [email protected]

Abstract: The controversy about a Cambrian "explosion" of morphological disparity (followed by decima­ tion), eladogenesis and fossilization is of central importanee for the history of life. This paper revisits the con­ troversy (with emphasis in onychophorans, which inelude emblematic organisms such as ), pre­ sents new data about the Chengjiang (Cambrian of China) faunal community and compares it and Ihe (Cambrian of Canada) with an ecologically similar bul modern tropical marine site where onychopho­ rans are absent, and with a modern neotropical terrestrial onychophoran community. Biovolume was estimated from material collected in Costa Rica and morphometric measurements were made on enlarged images of fos­ sils. CaJTlbriantropical mudflats were characterized by the adaptive radiation of two contrasting groups: the va­ gile and the sessile poriferans. Arthropods were later replaced as the dominant benthic laxon by . Vagility and the exoskeleton may explain the success of arthropods from the Cambrian to the mo­ dernmarine and terrestrial communities, both in population and biovolume. Food ecological displacement was apparen t in the B. Shale, but not in Chengjiang or the terrestrial community. When only hard parts were pre­ served, marine and terrestrial fossil deposits of tropical origin are even less representative than deposits produ­ ced by temperate taxa, Chengjiang being an exception. Nutrient limitations might explain why deposit feeding is less important in terrestrial onychophoran communities, where carnivory, scavenging and omnivory (asso­ ciated with high motility and life over the substrate) became moreimportant. Fossil morphometry supports the interpretation of "lobopod s" as onychophorans, whose abundance in Chengjiang was equal lo their abundance in modern communities. The extinction of marine onychophorans may reflect domination of the in­ faunal habitat by polychaetes. We conclude tha! (1) a mature ecological community structure was generalized during the Cambrian, and even biodiversity and equitability indices were surprisingly elose lo modern values; (2) the morphological diversity and geographic distribution of onychophorans indicate a significantpre-Cam­ brian evolutionary history which does no! support the "explosion" hypothesis; (3) disparity among phyla was not as important as the explosion-decimation model predicIs, bu! in the case of onychophorans, disparíty wÍl­ hin the phylum was greater than it is today and ¡ts reduction may have been associated with migration into the sediment when large predators evolved.

Key words: Disparity, decimation, "explosion", community ecology, feeding, habitat, fossil, Metazoa, evolu­ lion, Chengjiang, Burgess Shale, Cambrian, Recent, Costa Rica.

The evolution of the earliest metazoans me nts have centered on how representative the has been the subject of debate in recent years, fossil record is and the usefulness of techni­ particularly regarding the speed of change and ques such as cladism and specially molecular the diversity of general body plims (Hou and analysís (Bergstrom 1986) whose varied re­ Bergstrom 1995, Fortey et al. 1996). Argu- sults have shown it to be premature (Hou and 334 REVISTA DE BIOLOGÍA TROPICAL

Bergstrom 1995, Fortey et al. 1996, Abouheif comm.) and a more meaningful comparison of et al. 1998, Valentine et al. 1999). the Cambrian tropical community requires in­ Early century attempts to place sorne dif­ formation about modero tropical biotas becau­ fícult taxa into extant phyla were abandoned se the best known Cambrian faunas were tropi­ for the proposal of new phyla in the 1970's, cal (Hou et al. 1991, Monge-Nájera 1995). but recent work with better fossil material re­ In the last decade, the Chinese Cheng­ sulted in another change of opinion, and now jiang fauna mentioned only briefly in a 1985 much material has been reassigned to known review of Cambrian soft-bodied faunas or "la­ phyla (Hou and Bergstrom 1994, Hou et al. gersUitten" (Conway Morrís 1985) has beco­ 1995, Fortey el al. 1996, Sprinkle and Co­ me a mayor source of significant díscoveries, llins 1998). among them, six of the nine species of fossil Limítations of the fossil record are less onychophorans reliably described to date important when softparts have been preserved (Hou et al. 1991, Chen et al. 1995, Hou and (Hou 1999). "Lobopod" worms are among the Bergstrom 1997). most interesting animal groups found in Cam­ It ¡neludes marine fauna of approxima­ brian soft-bodied communities. For almost a tely upper Atdabanian dating, about 10 mi­ century authors have disagreed about their ta­ llíon years older than B. Shale, thus provi­ xonomíc position, although recent studies have ding a unique view of a fauna that lived supported the hypothesis that they were early shortly after the so caBed "Cambrian explo­ ancestors of onychophorans (Hou and Bergs­ sion", a characteristic of the greatest interest trom 1995, Monge-Nájera 1995). even if such an "explosion" never took place Modern onychophorans are part of terres­ (Fortey et al. 1996). trial ecosystems in tropical and south tempera­ The Chengjiang fauna occurs in the te regions (Monge-Nájera 1994 a, b), but the Yu' anshan Member of the Lower Cambrian Cambrian species were marine and basically Qiongzhusi Formation in Yunnan Province, tropical (Hou & Bergstrom 1995, Monge-Ná­ but ít was first discovered in Chengjiang jera 1995, 1996). County, about 50 km from Kunming, the capi­ The only detailed quantitative synecologi­ tal of Yunnan Province (southeast China). The cal study of a fossil community with onychop­ good preservation of Chengjiang specimens horans described Burgess Shale (B. Shale) of significantly improved the reconstruction of southwest Canada (Briggs and Whittington several taxa (e.g. Hou et al. 1991, Hou and 1985, Conway Morrís 1986). However, at that Bergstrom 1994, Hou et al. 1995, Rigby and time no appropriate tropical data were availa­ Hou 1995). Despite the geographic and chro­ ble for comparison. Conway Morris (1986) ba­ nological distance, both sites have sorne gene­ sically compared B. Shale with temperate ra in common and were dominated by arthro­ communities and coneluded that they were si­ pods; differing mainly in the rarity of deuteros­ milar, particularly in the proportion of preda­ tomes (a chordate and a crinoid have been tors, in the presence of a few species that do­ found ú�cently, H.x., pers. observo 1999) and minate numerically, and when compared with the lower proportion of trilobites in Cheng­ modern deep sea communities, in the occu­ jiang (Hou el al. 1991). rrenceof certain types of ancient taxa (Conway This fauna ineluded a variety of inverte­ Morrís 1986). brates preserved in extraordinary detail (Jin et It ís now known that there are differences al. 1993, Hou and Bergstrom 1994, Hou et al. between tropical and temperáte mudflat com­ 1995, Rigby and Hou 1995). Sorne of these munities (for example, tropical communities have been identified as onychophorans, also tend to have smaller populations of each taxon known as "lobopods", "lobopodians" or "on­ and also individuals with smaller bodies: Alon­ copodophores" (Hou el al. 1995, Monge-Ná­ gi 1989, Vargas 1996, J.A. Vargas 1999 pers, jera 1995, Chen el al. 1995). However, the INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 335 identification of these , with which (1987, 1988a). The fossil communities deve­ most authors from temperate countries are not loped at a greater depth than the P. Morales familiar, is often difficult (e.g. Rhebergen and community, but still within the photic zone, Donovan 1994). so the overall patterns (precisely the type of This paper presents new data concerning patterns studied here) are not expected to dif­ the Chengjiang community and compares it fer greatly, the main probable difference and B. Shale with a similar but modern tropi­ being the greater physiological stress in the cal marine site where onychophorans are ab­ intertidal P. Morales habitat (J.A. Vargas sent, and with a modern neotropical terrestrial 1999 pers. comm.). Standard ecological indi­ onychophoran community. Terrestrial com­ ces, biodiversity (H) and equitability (J) we­ munities are expected to be different from re calculated from number of specimens per marine communities, and their inclusion here taxon reported by Vargas (1987, 1988a), requires justification: the Coronado terrestrial Conway Morris e 1986) and Hou et al. community was included because this paper e 1991). Habitat, fossilization potential and stresses our common group of interest: ony­ body length information was provided by chophorans, which were marine in the Cam­ Vargas (1995 pers. comm., Table 1). Biovo­ brian and are terrestrial in the Presento We lume was estimated ftom the Vargas collec­ wanted to examine how the assemblages in tions and from ten samples collected by the which they have evolved differed from the senior author in November 1992 with a cy­ beginning of the phylum to the present. The lindrical corer (core area 17.7 cm2) to a walking speed of Cambrian onychophorans is depth of 15 cm, preserved in 10 % buffered estimated and new data about the effectof se­ formalin in sea water stained with Rose Ben­ diment flattening in living onychophorans as gal and extracted under a dissection micros­ well as morphometry are used to support the cope at 10 X (same methods and place of hypothesis that the fossils represent onychop­ Vargas 1987, 1988 a, b). To measure biovolu­ horans. Even though the emphasis is on ony­ me the specimens were submerged (after chophorans, the analysis and the conclusions allowing preservative to evaporate) in a pi­ refer to whole animal communities and thus pette with a known volume of 70 % ethanol are of interest to readers outside the field of and measuring the difference in mI. onychophorology. The modern terrestrial community data are from a random sampling of macrofauna in Cascajal de Coronado, San José, Costa Ri­ MATERIALS AND METHODS ca (83°57'37" W, 10°00'18" N, 1 775 m ele­ vation, riparian forest and cattle grassland). Community comparisons: The B. Sha­ Details about the field methods and site ap­ le reconstruction is from Conway Morris pear in Monge-Nájera and Alfaro 1995). (1986). In aH cases the trophic nucleus, i. e. Their biovolume was measured by the pipet­ the group of food consumers (in contrast te method described aboye. This fauna is not with producers and decomposers) that are included in the comparison at the genus level numerical1y dominant in the community was because it was not possible to obtain detailed identified on the basis of individuals, for re­ taxonomic determinations. Vouchers are de­ liability (see Conway Morris 1986 for details posited in the Museo de Zoología, Universi­ about the trophic nucleus concept). For a dad de Costa Rica. modern marine mudflat community, Punta For counts and morphometry, the Morales (Gulf of Nicoya stuary, Pacific of Chengjiangfo ssils were photographed by the Costa Rica) the graphs for feeding habit, junior author (HX) and illustrated with a ca­ trophic nucleus, number of genera and num­ mera lucida; measurements were made on ber of individuals are based on data in Vargas the resulting enlargements and photographs. 336 REVISTA DE BIOLOGÍA TR OPICAL

To estimate walking speed of the fossil taxa, mum length and leg pair values known for which generaUy were smaller and with less fossils were used in a regression based on the legs than living onychophorans, the maxi- lowest equivalent values for living species.

TABLE 1

Characteristícs 01 a modern marine community (Punta Morales, Costa Rica).

Taxon Group Habital Die! % indv % vol total

Cyprideis pacifica Crust EV S 22.64 6.10 Caricuma nicayensis Crust EV S 20.70 9.34 Mediamastus califarniensis * Polyc IS D 11.09 26.43 Turbellaria * Platy EV O 8.33 0.15 Paraprionaspia pinnata * Polyc IS D 4.59 0.45 Lumbrineris tetraura * Polyc IV D 3.58 0.05 Oligochaeta sp 1 * Oligoc IV D 3.32 0.05 Spiaphanes saederstroemi * Polyc IS D 2.55 0.06 Tellina rubescens Mollu IV D 2.01 13.58 Ceratacephale crosslandi * Polyc IV C 1.94 0.87 Prianospia delta * Polye IS D 1.31 0.02 Neanthes succinea * Polyc IV C 1.13 0.07 Glycinde annigera * Polye IV C 1.06 0.06 Pectinaria californíensis * Polye IS D 1.02 2.28 , juvenile sp. I MoJlu IV D 0.8 1 21.34 Hemichordata sp. I * Hemic IV D 0.81 1.81 Línopherus sp. 1 * Polye EV C 0.78 0.00 Pinnixia valerii Crust EV O 0.71 0.64 Acesta lopezi * Polyc IV D 0.68 0.00 Glottidia audebarti Brach IV D 0.61 1.36 Tharyx parvus * PoIye IS D 0.58 0.00 Panapeus sp. 1 Crust EV O 0.51 0.22 Sigambra tentaculata * PoIye IV C 0.44 5.41 Nephtys monroi * Polyc IV C 0.43 0.17 Notomastus hemipodus * Polyc IV D 0.43 0.19 Tage/us bourgeaisae MoJlu IV D 0.42 0.56 Ophiuroidea sp. 1 Echin IV D 0.42 0.23 Chane mollis * Polyc ES S 0.37 0.00 Ostracoda sp. 2 Ostra EV O 0.36 0.83 Magelona pacifica * Polyc ES D 0.35 0.00 Nemertina sp. 1 * Nemer IV C 0.35 0.22 dunkeri Mollu IV D 0.31 2.77 Ophiuroidea sp. 2 Echin IV D 0.3 1 0.80 Natica unifasciata Mollu EV C 0.27 3.14 Encape stakesi chin EV D 0.26 0.80

Brach Brachiopoda, Crus! Crustacea, Echin Echinodermata,Hemic Hemichordata, Mollu , Nemer Nemertina, Oligoc Oligochaeta, Ostra Ostracoda, Platy Platyhelminthes, Polyc Polychaeta. E Epifaunal, 1 Infaunal, S Sessile, V Vagrant. C Carnivore, D Detritus feeder, O Omnivore, S Suspension feeder. * Taxon without hard parts, indv individuals, vol volume. INTERNATIONAL JOURNAL.OF TROPICAL BIOLOOY AND CONSERVATION 337

RESULTS with hard parts that are likely to fossilize) is high in 14 % (bivalve and gastropod mo­ Comparison of Cambrian lluscs), intermediate in 26 % (brachiopods, onycbopboran marine communities echinoderms, arthropods) and low in 60 % witb a similar modem marine community that have only soft parts (polychaetes, turbe­ Number of genera: In comparison with the Ilarians, oligochaetes, hemichordates and ne­ modern community in which polychaetes have merteans) (see Vargas 1987, 1988 b). If indi­ more genera than any other group (Fig. 1), both viduals rather than species are considered, Cambrian communities were rich in genera of only 4 % have a high fossilization potential arthropods and poriferans. Chordates and mo­ (Vargas 1987, 1988 b). Thus, individuals are Buses a1so are more diverse today, while porife­ more likely to be underestímated than species fans, priapulids, cnidarians and hyoJithids are or higher taxa. absent from the modem community. Biodiver­ Albeit the fossilization potential for B. sity (H') and equitability (J) indices were H' = Shale species was not reported (Conway Mo­ 2.094 and J = 0.46 in B. Shale (Conway Morris rris 1986), most genera were monospecific 1986) and H' = 1.10 and J = 0.57 in Chengjiang. (Hou et al. 1991) so the value for high fossili­ Fossilization potential: When conside­ zation potential is close to 14 %, much lower ring the 35 species that represent the majority than in Chengjiang (50 %) and the modern of specimens in the modern community, the community (40 %). By contrast, only small fossilization potential (i.e. proportion of taxa fractions of individuals had a good probability of fossilization in B. Shale (2 %) and the mo­ 40r------� CAMBRIAN/CHINA dern community (4 %) against a very higlFpro­ 30 < portion (90 %) in Chengjiang. o�� o ;itl)¡;¡ a � iE 12o � ..:« Individuals and biovolume by taxa:The 20 Chengjiang population was more clearly do­ minated by arthropods (84 %) than the B. Sha­ lO I¡UUIIIU le population (61 %). Arthropods were domi- o . nant in the three communities (Fig. 2), but in CAMBRIANI CANADA contrast with the Cambrian, in the modern community polychaetes are the second group 20 < ¡:S ..: in importance instead of hemichordates. B. � 8 � oª Shale biovolume was dominated by arthro­ ffi 2� �,..¡ ;3::r.: ffi lO pods, with poriferans, echinoderms and pria­ o < ��3� 2 Q:l pulids following. Molluscs and polychaetes � �- � ::¿ i ..: dominate biovolume in the modern marine o community, followed by arthropods. PRESENTI MARINE Habitat: The sessile infauna was more 40 < o common in B. Shale than in Chengjiang. In .-: u 30 2 '" number of individuals, the Cambrian commu­ o ;:¡ � ¡¡J� u :l nities were dominated by epifaunal vagrant 20 ti) o � 51 ::¿ taxa, while in comparison the modern com­ 10 ! munity is rich in infaunal vagrant taxa, has G; less epifaunal vagrant species and lacks sessi­ le groups (Fig. 3). The same applies to biovo­ lume except for B. Shale where sessile epi- Fig. 1. Proportion (%) of genera per taxon in marine Cam­ . brian and modero communities. fauna dominated. INDIVIDUALS (%) w w v. '" -J 00 o <5 \5 O � \5 O �

ARTHROPODA ARTHROPODA J BRACHIOPODA J HEMICHORDATA CNIDARIA ft !l PRlAPULlDA ::¡t!" NEMATOMORPHA � IV PORlFERA [:J. � ECHINODERMATA ne:.. 'O a O O POLYCHAETA ." n g. J en� §e '" INSERTAE SEDIS � ::1� m ':"�;::. � O MOLLUSCA !í J MISCELLANEA ;s: � '"�:: ::1 n 11 BRACHlOPODA ::r: ..2s � Z . i5.: �m :> .., � CNIDARlA 2'..0>c: a¡;¡{b Vi' � CHORDATA HYOLITHlDA .., .... w v. --J o � o o o00 '" w v. '-.1 � ;:; o o � o 8 C> �S-� O ""'" O �. .... ::1 ARTHROPODA ARTHROPO J DA J g.g" MOLLUSCA HEMICHORDATA .., J 2..3 . PRIAPULIDA HIRUDINEA 3c: 8- (1) PORIFERA � 3 OLIGOCHAETA P P ECHINODERMATA 5 '"ti � ONICHOPHORA e¡ � � POLYCHAETA '"@ 8 INSERTAE SEDIS n

11 Q � MOLLUSCA r:t. ::l � .., o­ ¡:;j (1) :J. MISCELLANEA �§ BRACHIOPODA Ei" en� -� � 3 n ['5. CNIDARIA � � go.. n CHORDATA 'O O � El HYOLITHIDA :> � O e § � =. � r::t. �. " f1'I en

S�O � 0.. " VOLUME(%) O> ::: ¡; � a' �. .... '" i3 � i!l ::; - - - - - (jo> � � �

'"2:� ro e� . ARTIlROPODA ARTIlROPODA ARTIlROPODA . ] �HEMICHORDATA PORIFERA ;i. MOLLUSCA I U PRIAPULIDA I ECHINODERMATA HIRUDINEA PORIFERA ECHINODERMATA OLIGOCHAETA "' CNIDARIA P POLYCHAETA I MISCELLANEA ONYCHOPHORA 1:: n en MOLLUSCA l » �'-�'"INSERTAE SEDIS BRACHIOPODA � � HEMICHORDATA � CNIDARIA ¡:: ;;l � POLYCHAETA '" CHORDATA Sí 1:: HYOLITHIDA � BRACHIOPODA n en NEMERTINA MOLLUSCA Sí '"� �» PLATYHELMINTES CHORDATA fE r » OLIOOCHAETA HYOLITHlDA

'1V::>IdOlIl.VJD0'10Iff tIa Vl.SIAtIlI 8¡;¡; INTERNATIONAL JOURNAl..OF TROPICALBIOLOGY AND CONSERVATION 339

70 CAMBRIANI CHINA CAMBRIANI CANADA -

Fig. 3. Proportion (%) of individuals occupying each habitat in marine Cambrian communities, and modero marine and te­ rrestriaI. communities. The equivalent vaI.ues for biovoI.llme appear in second part of Fig. (no data for China).

Feeding habit: Deposit feeders were nu­ Trophic nucleus: Arthropods dominated merieally dominan:t !n all eommunities, but in the trophie nucleus (as defined above) in all the modem eommunity the number of suspen­ eommunities (Fig. 5). Hemiehordates and sionfeeders decreased while that of earnivores­ priapulids are absent from the modern nu­ seavengers inereased (Fig. 4). Two eategories, cleus, in which polyehaetes and turbelIarids omnivores and herbivores, were not identified are important. In the modern eommunity nu­ in the Cambrian sites. Community biovolume merie domination is Iess extreme beeause was divided almost equally among all feeding two groups (Cyprideis and Bodotriinae) have habits in B. Shale, but deposit feeders domina­ similar proportions in the nucleus. te biovolume in the modem eommunity. 340 REVISTA DE.BIOLOGíA TROPICAL

80 CAMBRIAN I CANADA r---_

- 60

40

20

úJ � 60 :3O >

g: 40 � O z 20 O ¡.tJ ¡.tJ ""'

PRESENT/TERRESTRlAL

�

40

20

Fig. 4. Proportion (%) of individuals according to feeding habit in a marine Cambrian community and modero marine and terrestrial communities. Equivalent values for biovolume appear in second part of Fig.

Body length: Species with small bodies Bodotriinae sp. 1 (Crustacea), Mediomastus dominated all communities numerically. The californiensis (Polychaeta), Turbellaria sp. 1 ' B. Shale community had more medium and and Oligochaeta sp. 1 are in the 3-19 mm large-bodied animals than Chengjiang and range, Lumbrineris tetraura (Polychaeta) is than the modern marine habitat (Fig. 6) (No­ in the 20-35 mm range and Paraprionospio te: for modern marine habitat: Cyprideis pa­ pinnata (Polychaeta) is aboye 36 mm long). cifica (Crustacea) is under 3 mm in length, INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 341

CAMBRIANI CHINA CAMBRIANI CANADA CAMBRIAN I CH1NA CAMBRIANICANADA 80 'r-- 70 40 80

60 .- 60 60 30 50 �

40 40 40 '"� '" 5 « 30 8 '" ,.- ;:J � a.:� '" Q � 20 o o ¡g é � lI'l ;;:: 20 � -h � a '" o :?E n� I 1-- � PRESENTI MARINE PRESENTI 80' lERRESTRIAL • r-- PRESENTI TERRESTRIAL ,...... -- 60 60 20 - '" '" 40 40

� �a.: o a.: <:> o o '" o .,., '" lI'l � � '" o :q � � '"¿, � � o -, r1 BODY LENGTH (mm)

Fig. 6. Proportion (%) of individuals by body length ca­ tegory in marine Cambrian and modern communities and in a modernterrestrial cornrnuni ty. Fig. 5. Proportion (%) of individual s in the trophic nucleus (see text for definition) of Cambrian and modern marine communi­ ties, and in a modernterrestrial cornmunity.

Comparison 01 Cambrian community, the bodies are not as hard as the onychophonm communities with a calcareous parts of a bivalve, but 75 % of in­ modern terrestrial onychophoran dividuals are intermediate in fossilization po­ commnnity , tential (mainly arthropods) and 25 % only ha­ Individuals and biovolume by taxa, ve soft parts (e.g. hirudineans). and fossilization potential: The following In the B. Shale cOmmunity onychopho­ trends are similar for number of individuals rans were only 0.042 % of individuals (calcu­ and volume: arthropods were numerically im­ lated from data in Whittington 1978 and Con­ portant in all communities, but the Oligo­ way Morris 1986). In Chengjiang the value chaeta are significant only in the modern te­ was 1 %, much closer to the modem terres­ rrestrial community where, even if not as trial community where 0.83 % were onychop­ outstanding in number of individuals, mo­ horans (TabIe 2). lluses also represent a significant part of the Habitat: Epifaunal vagrant species were biovolume (TabIe 2, Fig. 2). Inthis terrestrial dominant in bothco mmunities (TabIe 2,Hg. 3). 342 REVISTA DE BIOLOGÍATROPICAL

In comparison with the Cambrian, the modem michordates and priapulids were also impor­ tertestri¡U onychóphoran cornmunity has slight­ tanto In the modem terrestrial community, ly more infaunal vagrant individuals (sessile ta- oligochaetes are part of the nucleus which is . xa are absent). In biovolume the sessile epifau­ dominated by arthropods (isopods). na dominated the Cambrian and the vagrant epi­ Length: The terrestrial community is . fauna the modem cornmunity. clearly dominated by small-bodied animals and Feeding habit: In comparison with the has less large and medium sized specimens than Cambrian, in theterrestrial.community, carnivo­ the Cambrian cornmunity (Table 2, Fig: 6). res-scavengers dominate and deposit feeders are Fossil morphometry: The basic morpho­ less frequent and limited to oligochaetes (Table metric data from mne Microdictyonsinicum, fi­ 2, Fig. 4). However, carnivores-scavengers oc­ ve Cardiodityon catenulurh, two Hallucigenia cupy less biovolume. Sorne {eeding categories tortis and one Luolishania longicruris appear in that are important in the terrestrial cornmunity Table 3. There is a positive but insignificant co­ (including the dominant omnivores) were not rrelation between body length and number of . identified in the Cambrian specimens. leg pairs in fossil onychophoran species, and Trophic nucleus: In both communities the correlation coefficient is within the range of the trophic nucleus was dominated by arthro­ extant species when males and females arecon­ pods (Table 2, Fig. 5). In the Cambrian, he- sidered independentIy (Fig. 7).

TABLE 2

Characteristics o[ a modero terrestrial onychophoran community (Coronado. San José. Costa Rica).

Taxon Biovolume Individuals Size Habitat Fossilization Diet (% ml) (%) class potential

Acari 1.83 0.28 1 Epifauna Low Carnivore Araneae 0.99 4.96 1 Epifauna Low Carnivore Blattaria 3.69 7.16 1 Epifauna Low Omnivore Chilopoda 2.15 4.96 2 Epifauna Low Carnivore Coleoptera 4.24 8.26 1 Epifauna Low Several Coleoptera (larvae) 1.83 6.06 1 Infauna Ver y low Scavenger Collembola 0.07 2.48 1 Epifauna Low Herbivore Dermaptera O 0.28 M Epifauna Low Omnivore Diplopoda 2.26 12.1 1 Epifauna Low Scavenger Diptera 1.83 0.55 1 Epifauna Low Severa! Formicidae 0.58 2.48 1 Epifauna Low Omnivore Gastropoda 3.65 1.65 1 Epifauna High Herbivore Grillidae 3.83 1.1 1&2 Epifauna Low Herbivore Hemiptera 22.6 2.75 1 Epifauna Low Omnivore Hirudinea O 0.28 M Epifauna Very low Carnivore lsopoda 8.98 24.5 1 Epifauna Low Scavenger Lepidoptera (larvae) 0.73 1.38 Epifauna Verylow Herbivore Lepidoptera (pupae) 0.37 0.28 2 Epifauna Low None Oligochaeta 7.67 13.5 3 Infauna Very low Scavenger Onychophora 0.73 0.83 3 Epifauna Low Carnivore Opiliones 32 4.13 4&6 Epifauna Low Omnivore

Size classes Oength): 1: under 3 mm, 2: 3-19 mm, 3: 20-35 mm, 4: 36 mm or higher. M: missing value. Adapted from Monge-Nájera and Alfaro (1995). INTERNATIONAL JOURNALOF TRO PICAL BIOLOGY AND CONSERVATION 343

TABLE 3 Scute height M 4 8 5-11 Scute height P 4 7 5-9 Number of body wall folds and morphological Scute width A 5 4 3-6 measurements offossil onychophorans (in cm x ]0-2) Seute width M 4 4 2-6 made on the A anterior, M medium and P posterior parl Seute width P 4 4 3-5 of each animal. Distanee between legs A 3 5 3-7 Distanee between legs M 2 5 3-7 Microliictyon sinicum (nine individual s) Distanee between legs P 2 5 5-6 Distanee between seutes A 5 4 4-6 Variable Sample Mean Range Distanee between seutes M 4 5 3-7 size Distanee between seutes P 4 3 2-4 Claw length A Body diameter A 7 16 8-21 Claw length M Body diameter M 7 21 13-29 Claw length P 1 Body diame ter P 7 21 13-34 Folds per segment A 8 Maximum leg width A 6 6 3-9 Maximum leg width M 5 6 3-8 Maximum leg width P 5 7 3-9 Hal/ucigenia fortis (two individuals) Leg length A 5 37 18-5 1 Leg length M 5 44 15-62 Variable Sample Mean Range Leg length P 5 42 16-60 size Scute height A 9 13 6-22 Seute height M 8 16 9-24 Body diameter A 10 Seute height P 7 15 9-24 Body diameter M 10 Seute width A 9 11 7-22 Body diameter P 10 Scute width M 8 10 7- 15 Maximum leg width A 3 Seute width P 7 12 7-18 Maximum leg width M 2 Distanee between legs A 4 10 5-14 Maximum leg width P 2 Distanee between legs M 5 17 9-23 Leg length A 1 42 Distanee between legs P 5 14 6-27 Spine length A 2 20 15-25 Distance between seutes A 9 9 4-18 Spine length M 2 19 15-22 21-32 Distanee between seu tes M 8 13 6-22 Spine length P 2 27 Distance between seutes P 7 9 4- 14 . Spine width (at base) A 2 5 2-7 3-6 Claw length A 1 5 Spine width (at base) M 2 5 Claw length P 3 3 2-4 Spine width (al base) P 2 4 3-5 2 Folds per segment A 6 Distanee between spines A 10 9-11 Folds per segment M 6 Distanee between spines M 2 11 11-12 Folds per segment P 6 Distance between spines P 11

Cardiodiclyon catenulum (five individuals) Luolishania longicruris (one individual)

Variable Sample Mean Range Variable Sample Value size size

Body diameter A 5 7 4- 10 Body diameler A 8 Body diameter M 4 7 4- 12 Body diameter M 10 Body diameter P 4 7 4-11 Body diameter P 7 Maximum leg width A 3 3 3-4 Maximum leg width P 3 Maximum leg width M 2 2 2-2 Leg length P 20 Maximum leg width P 2 2 2-2 Distanee between legs P 7 Leg length A 3 20 16-23 Folds per segment A 5 M Leg length M 2 17 15-19 Folds per segment 7 Leg length P 1 10 Folds per segment P 4 Scute height A 5 8 4- 10 344 REVISTA DE BIOLOGÍA TROPICAL

earlier forms tended to move fas ter if the 20 " N = 8 FOSSlL SPECIES Monge-Nájera (1995) cladogram is correet, SPEARMAN RANK CORRELAnON RHO 0.29. P 0.44 but there is no clear trend if the Hou and 16 = = Bergstrom (1995) cladogram is used. The fos­

12 sil species might have had individual weights ranging between 100 mg in the case of Luolis­ 8 hania longicruris (the weight of an Epiperipa­ @ e e tus biolleyi of similar size, Monge-Nájera and 4 .. Morera 1994) and more than 5000 mg in the " .. case of the 20 cm long (one of the ·0 ID 12 14 16 18 20 22 largest onychophorans, Epiperipatus torqua­ 100 24 tus, can reach 15 cm and 4000 mg, Read

N = 50 EXTANT ESPECIES (MALESONLYl E SPEARMAN IMNK CORRELAnON 1985). A recently discovered and still undes­ RHO -0.09. P > 0.05 g = :t 70 cribed Costa Riean species (Limón Province) ¡... " Z measures 20 cm in length, equal to the fossil � .. .. " " .. .. Xenusion . � 40 ...... O " C!l " G ...... " ...... eGo (9 .. .. " e. r&OO .. TABLE 4 " .. G e \O Basic body characteristics and estimated walking speed of 14 21 28 35 42 fossil onychopho/'ans calculaled from the speed of living

.. species with ¡he equation: Speed == 88.62 - (2.13) (number N = 69 EXTANT ESPECIES (FEMALES ONLY) SPEARMANRANK CORRELAnON of leg pairsJ. Equatíoflproduced by a simple reggresiofl RHO 0.39. P < 0.05 = procedure applied to data in this tableo 110 ...... • Taxon Speed Length Leg .. .. • .. " .. (cm/min) (cm) pairs .. " . .. .. e"" .. .. " 60 " ...... ee@ ti • ...... - . Fossil taxa e ...... • • .. .. Hallucigenia 69 1.7 9 10 67 6 10 13 21 29 37 45 Microdictyoll 67 4.6 10 NUMBEROF LEO PAIRS Onyc!zodictyon 65 6 11 Luolishania 55 1.5 16 Fig. 7. Plot of the relationship between body length and Xenusion 46 20 20 number of leg pairs in fossil and extant onychophorans. Helenodo/'a 44 6.4 21 Maximum values were used for each species. Data sour­ Cardiodictyon 37 3.1 24 ces: Hou pers. observ., Hou and Bergstrom (1995), Mon­ ge-Nájera (l994a) and Monge-Nájera (1995). Living taxa

Peripatopsis sp. 60 6 16 Epiperipatus biolleyi 60 22 25 Speed and weight estimates for fossil Epiperipatus imtlzumi 12 25 29 species: In the living species for which data MacroperipalUs are available (Table 4), speed was more corre­ torquatus 11 100 41 Epiperipatus lated with the number of legs (Rho = -0.62) trinidadensis 5.5 21 27 than with length (Rho = -0.27) but neither is [2 significant (p = 0.21 and p = 0.58 respecti­ Regression equation data: N == 5, adjusted 0.30, RMS p c vely; Fig. 8). Nevertheless, the speed-number residual 23. intercept p == 0. 1. leg pairs = 0.2, predi tion error when equation is applied lo original living species of legs regression allowed a rough estimate of data 10-91 %. Fossil data: Hou pers. observo and Monge­ speed in fossil taxa (Table 4). When compared Nájera 1995; living laxa data from Manton 1953. Read with the cladograms of Fig. 9, it suggests that 1985 and Monge-Nájera et al. 1993. INTERNATIONALJOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 345

70 1"""...... --- ...... """""""" .... DISCUSSION 60' .. 50 .S N=5 SPECIES Community comparisons: This analysis 4 SPEARMAN RANK CORRELAnON � 0 RHO = .0.62, P = 0.21 addresses only the general patterns because ¡ 30 more detailed statistical enquires seem unwa­ til 20 rranted for data from such different methodo­ !O .. logies as fossil counts and observation of li­ 0 ving organisms. �15��20�--�r---�3 0�� 35�--���45 Number oC genera: Genera are categories MIN.LEO PAIRS that reflectthe opinions of taxonomists but we Fig. 8. Plot of the relationship between speed and numberof consider them to be rough estimates of biodi­ leg pairs in living onychophoran species (used as basis for versity. They suggest that Cambrian tropical estimates in fossil onychophorans). Data sources in Table 4. mudflats favored the adaptive radiation of two deeply different groups: the highly vagile and complex arthropods and the sessile and sim­ pler poriferans. Why arthropods were so ob­ viously replaced as dominant members of the EXTANT ONYCHOPHORANS � community by polychaetes (with vagile and HELENODORA sessile taxa) deserves attention in the future l'iJ�I'� (see Fauchald 1975). Biodiversity and equitability in B. Shale CARDIODICTYON �:v:� were within the modern seasonal ranges of P. HALLUCIGENIA Morales CH' 1.61-3.36, J = 0.46-0.87; Vargas MICRODlCTYON ;�';�JI1i�F" 1987, 1988 a, b), and in Chengjiang H' was

AYSHEAIA low but J was also within the modernrange. If B. Shale followed the moderncommunit y pat­ XENUSION ��';,;:� tem (Vargas 1988 b) biodíversity was higher LUOLISHANIA �� during a rainy season, when nutrient concen­ NEOPlLlNA trations increased.

HOU & BERGSTROM (1995) The advantages of rapid displacements and an exoske1eton may explain the success of arthropods from the Cambrian to the modern EXTANT ONYCHOPHORANS � marineand terrestrialcornmunities, bothin po­ HELLENODORA pulatíon and biovolume. Onychophoran abun­ AYS HEAlA <'ffí;¡'Iiií;;;;��. dance is similar in modern terrestrial commu­ nities and in Chengjiang, possibly because onychophorans did not evolve tracheal val ves ONYCHODlCTYON �� � to control water los s on land (Monge-Nájera MICRODlCTYON jJW':'!í�'f",,.,,,,- and Louren<;o 1995). The rarity of onychopho­ fans in B. Shale stresses the difference bet­ ween this sire and Chengjiang. Fossilizationpotential: The low proportíon of species with hard POLYCHAETA _� parts in B. Shale (14 %, see Conway Morris MONGE-NAJERA (1995) 1986) indicates that similar communities for

Fig. 9. TINo hypotheses about the evolutionary relations­ which only hard parts are known were greatly hips of fossil onychophorans (from Hou and Bergstrtlm undersampled by fossilization, in contrast with 1995 and Monge-Nájera 1995). Chengjiang where fossilization potential was 346 REVISTA DE BIOLOGÍA TROPICAL

extraordinarily high according to our results meter, reproductive pattems that ranged from (50 % of taxa had hard body parts). seasonal peaks to a continuous reproductive Less than 30 % of the modem marine ma­ effort, a relatively constant taxonomic compo� crobiota has a significant fossilization poten­ sition and a population dynamics affected tial in temperate areas (see Conway Morris mainly the amount oC organic matter that in 1986). Ourtropical data indicate lower values tum reflected the proportion of silt, elay and for modem marine species and individual s, shell fragments (see Vargas 1987, 1988 a, b, and an even worse fossilization potential for Alongi 1989). terrestrial communities.· Marine and terrestrial Habitat: In contrast with the modero ma­ fossil deposits of tropical origin should be con� rine community the B. Shale fossils inelude sidered even les s representative than deposits epifaunal and nektobenthic species that Con­ produced by temperate taxa. way Morris (1986) suggested had been acci­ Sorne early Cambrian taxa later lost hard dentally ineluded during the deposit forma­ parts, reducing fossilization potential (Conway tion. However, it is improbable that their pre­ Morris 1985); the same trend was noticed in sence was accidental because the same trend onychophorans (Monge-Nájera 1995). The si­ was found in Chengjiang. Apparently natural milarity of onychophoran mandibles with so­ selection favored a migration from the surfa­ rne microfossils labeled as "conodonts" has ce to life inside the sediment, maybe to esca­ been mentioned (Monge-Nájera 1995) but re­ pe from increasing predator pressure; the sa­ mains to be studied in detail. me can explain why sessile taxa began to di­ The reason why the B. Shale organisms sappear from the mudflats. Sponges and tuni­ ' soon stopped decomposing is unknown but cates are sessile and exposed but have Httle anoxic or deep sea cold water conditions ha­ edible tissue or are chemically protected (J.A. ve been mentioned as a possibility (Conway Vargas 1999 pers. comm.). To our knowled­ Morris 1986), albeit the subject is controver­ ge, the literature does not deal with why ony­ sial (Orr et al. 1998). However, the anoxia chophorans became extinct in marine habi­ hypothesis is consistent with the discovery tats. These results suggest the working hyput­ that tropical mudflatsbecome anoxic with so­ hesis that domination of the infaunal habitat rneperiodic ity (Alongi 1989) and makes the by polychaetes deprived onychophorans of deep sea hypothesis of Conway Morris the burrowing habitat that they need (see (1986) unnecessary. The detailed preserva­ 'Monge-Nájera et al. 1993, Monge-Nájera tion of structures in both Cambrian communi­ 1995). In that case, only the species that ties (Hou and Bergstrom 1997) indicates that adapted to land -via the intertidal zone- survi­ scavengers and bacteria, even if anaerobic ved (Monge-Nájera 1995). bacteria were present as suggested by Briggs Life on land resembles more elosely the (1999) did not cause significantdamage. habitat distribution of Cambrian communities Individuals and biovolume by taxa: than distribution of modero marine communi­ When individuals and biovolume are exami­ ties because the epifauna predominated in ned, the pattem becomes more complicated both. Again, predation may have played a ro­ because molluscs and polychaetes respectively le, but there are not enough data to evaluate replace or approach arthropods as the domi­ the idea. nant group. Feeding habits: Modero infaunal com­ Seasonality and density data are lacking munities, in which energy and matter are ex­ for B. Shale, but considering its overall ecolo­ ported more by larvae than by macropreda­ gical similarity with the modem community, it tors, are composed mainly of small opportu­ may havebeen characterized by densities nists that are surface deposit and suspension . around 40 000 macroinvertebrates per square feeders (Alongi 1989) in food webs based on INTERNATIONAL JOURNAL OF TROPICAL BIOLOGY AND CONSERVATION 347 microalgal detritus and coastal vegetation de­ bability of surviving predator attacks but ob­ bris (Vargas 1987). The Cambrian coastal viously this Hne of defense was not developed communities seem to have been similar ex­ in the mud flat orthe terrestrial community. If cept for the input of terrestrial vegetation re­ fish became the main marine predators, burro­ mains that were nonexistent at that time (the wing may have been an easier strategy for in­ basis of the food web were strictly algae, vertebrates than trying to outcompete verte­ Conway Morris 1986). Predator biovolume brate size. was high (52 %), but by number of indivi­ The fossil values of (1) body length - duals it was similar to recent communities number of legs relationship and (2) body sizes (Conway Morris 1986). The reduction of sus­ that fit equivalent living species ranges lend pension feeding in the modern community further support to interpreting lobopods as apparently reflects the absence of sponges, onychophorans (Hou and Bergstrom 1995, while the absence of omnivores and herbivo­ Monge-Nájera 1995, Tait et al. 1995). A hy­ res in B. Shale may simply be the result of our pothetical relationship with tardigrades (e.g. ignorance about the diets of fossil species and Chen et al. 1995), favored by Fortey et al. not a real ecological condition. (1996), is not supported by our morphometric A greater difficulty in finding and extrac­ analysis. A detailed cladistic analysis also fai­ ting nutrients from the soil than from inunda­ led to find a cIose relationship between ony­ ted marine sediments might explain why depo­ chophorans and tardigrades (Monge-Nájera sit feeding is les s important on land, where car­ 1995). Common methodological errors in nivory, scavenging and omnivory (associated cladism were discussed by Rouse and with high motility and life over the substrate) Fauchald (1995). became more important. Theinf erred greater speed of earlierforms Trophic nucleus: Trophic nucleus (80 % is in agreement with the general trend propo­ of biomass, individuals necessarily in this ca­ sed earlier on morphological evideI1ce: later se) were compact: a few but common specíes forms used burrowing rather than armoring dominated, similar to modem temperate (Con­ and high speed for protection (Monge-Nájera way Morris 1986) and tropical (Vargas 1987) el al. 1993, Monge-Nájera 1995). communities. In B. Shale, the numerically do­ Cladograms: A1though the two available minant species did not compete for food (Con­ cladograms for fossil onychophorans (Fig. 9) way Morris 1986), but in Chengjiang and the are similar in showing Helenodora as derived modern community the dominant species sha­ ("advanced") and Luolishania as underived red feeding habits. ("primitive") and in the associations Xenusion­ No adjacent species in trophic nucleus Aysheaia and -Cardiodictyon, share a feeding habit, phytoplankton and they also differ significantly, perhaps because benthic algae were the base of the food web they used differentoutgroups. In any case, spe­ (Conway Morris 1986). Ecological displace­ cies hypothesized to move faster because they ment, apparent in B. Shale (Conway Morris had les s legs tend to have developed scutes as 1986), lacks evidence in Chengjiang and the Well as large and strong spines. Monge-Nájera terrestrial community. The only quantitative (1995) suggested that the evolution of life in study of the biota associated with modern microcaverns made long legs, scutes and spi­ onychophorans refers to Epiperipatus biolleyi nes a disadvantage and suggested that the top in Coronado, Costa Rica and shows that a sig­ speed of fossil species was under the 6-34 cm­ nificant variety of taxa share feeding guilds /min of living E. biolleyi. Our speed estimates, (Monge-Nájera 1995). based on measurements in air, are higher but Length, oncopods and speed: The evolu­ under water the viscosity of the medium would tion of larger body sizes may increase the pro- result in reduced speed (Manton 1953). 348 REVISTA DE BIOLOGÍA TROPICAL

Implications for tlle "explosion"-dis­ Hallucigenia was noí a new phylum but an parity-decimation model: Few recent pa­ onychophoran: the spines were dorsal (de­ pers seem to support the explosion model, fenses) and the "tentacles" were ventral legs among them Geyer (1998), Holland (1998) (Hou el al. 1991). The same applies to other and Valentine el al. (1999) while most aut­ groups (Hou and Bergstrom 1995, Hou el al. hors reject it on the basis of molecular 1995, Fortey et al. 1996) and weakens the (Brornham el al. 1998, Hoshiyama el al. disparity explosion-decimation model, which 1998, Regier and Schultz 1998, Smith 1998) nevertheless was very useful as a motivation or morphologica! evidence (Wills 1998 a,b). for additional work (the present paper being The remarkably "modern" ecological organi­ an example). Our results agree with recent zation of B. Shale was described years ago morphospace disparity studies (Wills 1998 (Briggs and Whittington 1985, Conway Mo­ a,b). The taxonomic diversity, morphological rris 1986), but that finding could not be gene­ disparity and geographic distribution of ony­ ralized for lack of equivalent data from other chophorans (Hou and Bergstrom. 1995, Cambrian sites. Our results for Chengjiang Monge-Nájera 1995) indicate a significant not only suggest that a mature ecologieal pre-Cambrian evolutionary history that also community strueture was generalized during fails to support the explosion model. Howe­ the Cambrian, but even show that Cambrian ver, even though disparity among phyla was biodiversity and equitability indices were sur­ not as important as the model predicts, at prisingly close to modern values. The faet least for onychophorans morphological dis­ that niches rather than organisms were simi­ parity within the phylum was greater than it lar is not unexpected because this is frequent is today (Monge-Nájera and Hou 2000). The in modern communities (Barrientos and Mon­ reduetion in onychophoran morphological ge-Nájera 1995). However, this finding disparity may have been associated with mi­ should not be exaggerated: there were also gration into the sediment when large preda­ sorne important differences between the two tors evolved, because life in burrows can fa­ Cambrian sites, which were distant both in ti­ vor the evolution of simple, cylindrical body me and geographically. Hypotheses about the shapes (see Monge-Nájera 1995). scarcity of pre-Cambrian fossils often refer to lack of hardparts, small size and destruction of plankton fossils (Fortey el al. 1996). Our ACKNOWLEDGMENTS finding that even early Cambrian communi­ lies were complex and indicative of a long We thank José A. Vargas Z. for particu­ evolutionary history, is éonsistent with the th­ larly vaIuable assistance and support; Berna! ree hypotheses -which are not mutually ex­ Morera, Harlan Dean and Sergio Salazar Va­ clusive- but indicates a post-Cambrian loss of llejo for providing valuable literature and in­ hard parís in onyehophorans. formatíon; Zaidett Barrientos LL. and Fernan­ Strange fossils such as Hallucigenia, do Barrientos LL. for field assistance; Karina described as a leg-less cylindrical animal that Rodríguez, Juan C. Solano and V. Ariasfor la­ anchored itself to the bottom with movable boratory assistance, Marisol Rodríguez for the spines and fed with several tentacles that had illustrations; Alvaro Wille and Bernal Morera individual "gullets" (Conway Morris 1977) for supporting the senior author's ¡nterest in were the basis for the idea of a rapid increa­ onychophorans and D.E.G. Briggs (University se in morphological disparíty, later decima­ of Bristol), Teresita Aguilar (Universidad de ted when only a few body organizations sur­ Costa Rica) and several anonymous reviewers, vived (Gould 1989). However, when additio­ for comments that led us to signifieantly im­ nal material was found, it became clear that prove an earlier draft. INTERNATIONAL JOURNAL, OF TROPICAL BIOLOGY AND CONSERVATION 349

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Editor: José A. Vargas Received 29-IV- 1999. Corrected 23-Ill-2000. Accepted 24-IV-2000.