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Importance of Dominican Republic amber for determining taxonomic bias of fossil resin preservation—A case study of spiders
Palaeogeography, Palaeoclimatology, Palaeoecology 223 (2005) 1 – 8 www.elsevier.com/locate/palaeo
Importance of Dominican Republic amber for determining taxonomic bias of fossil resin preservation—A case study of spiders David PenneyT Earth, Atmospheric and Environmental Sciences, The University of Manchester, Manchester M13 9PL, United Kingdom Received 13 November 2004; received in revised form 3 March 2005; accepted 21 March 2005
Abstract Fossils preserved in amber represent only a small fraction of the biota which was alive in the amber forest. In order to make accurate palaeoenvironmental reconstructions, it is necessary to determine the biases which affect preservation. Only the Baltic and Dominican Republic amber deposits have had inclusions described in sufficient quantities suitable for quantitative analyses. Baltic amber is twice the age of Dominican, with a correspondingly higher proportion of extinct supraspecific taxa, and was produced in a climate very different to that in the region today. Dominican Republic amber was formed in a tropical climate similar to that in the region today and many of the preserved spider supraspecific taxa are extant. Therefore, the fossil and Recent Hispaniolan faunas are directly comparable ecologically. Spiders (extinct and extant) are significantly more diverse than other groups for which Hispaniolan species diversity data are available. Thus, they form an ideal model for assessing taxonomic bias of Dominican amber preservation. This is the first time that taxonomic richness estimates have been made and compared quantitatively between extant and fossil amber faunas. Extant and extinct (Dominican Republic amber) Hispaniolan spiders are compared at family level. Overall, the two faunas are similar but some distinct differences are apparent. Hispaniolan representatives of the families Cyrtaucheniidae, Microstigmatidae, Ochyroceratidae, Palpimanidae, Tetrablemmidae, Agelenidae, Anapidae and Mysmenidae are known only from amber, whereas Drymusidae, Deinopidae, Desidae, Amaurobiidae, Prodidomidae and Zoridae are known only from the extant fauna. Many families have similar fossil and extant species diversities. Oonopidae and Dictynidae are significantly more diverse in amber. Many families currently known only from Dominican amber probably have undiscovered extant species on Hispaniola. Family species richness estimates were calculated for both fossil and extant spider faunas, but only those for the extant fauna provide results consistent with a neotropical spider assemblage. Fossil richness estimates were excessively high as a result of the large number of singletons. Nevertheless, the Dominican Republic is the only place on Earth where fossils in amber occur in sufficient numbers and that are closely related to the extant fauna, such that direct diversity/ ecological comparisons can be made. Given future research directed at identifying spiders and other inclusions in the large
T Fax: +44 161 275 3947. E-mail address: [email protected]. 0031-0182/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2005.03.022
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amber collections amassed in Museums around the world, detailed comparisons of these faunas will allow us to better determine taxonomic biases associated with amber preservation. D 2005 Elsevier B.V. All rights reserved. Keywords: Arachnida; Araneae; Dominican Republic amber; Fossil; Taxonomic bias
1. Introduction Amber, fossilized tree resin, is a particularly important resource of fossil data for recreating terrestrial palaeoecosystems. In contrast to sedimentary fossil deposits, where terrestrial invertebrates are usually allochthonous, amber contains primarily terrestrial fossils, which were sampled in situ, in the palaeohabitat. However, fossils preserved in amber still represent only a small fraction of the biota alive in the amber-producing forest. Amber, as with all other forms of fossilization, is subject to unique preservation biases. It is equally important that we elucidate what other organisms were present in the palaeoenvironment at the same time as those preserved as fossils, but which evaded entrapment in the resin. That is, we need to understand the taxonomic bias of resin entrapment before we can draw a more complete picture of the palaeoenvironment. Few authors have investigated bias of amber inclusions. Henwood (1993a) and Ross (1997) acknowledged, with qualitative examples, biases in relation to size, phenology and behaviour of the amber insect fauna. Martı´nez-Delclo`s et al. (2004) discussed a number of factors which may have promoted the preservation of some groups of invertebrates in preference to others, including resin viscosity, insect behaviour, insect habitat preferences, resin chemistry and abiotic environmental factors. Pike (1993, 1994) recognized the necessity of quantifying the biases associated with resin as an arthropod trap, prior to addressing diversity and community structure through amber inclusions, but stated that no published data were suitable for assessing them. Despite recognizing the importance of understanding these biases, Pike (1994), with some reservation, assumed that different resins sampled insect faunas in similar ways, and thus had the same taphonomic biases. I doubt that this assumption will prove to be true, but it requires further investigation. The general, oft-encountered,
statement that small organisms get trapped whereas larger ones do not because they are strong enough to escape, has not been thoroughly tested and appears to be incorrect. For example, tiny araneoid spiders can often walk over sticky surfaces relatively unhindered, because they walk on the tips of their tarsi with their bodies raised off the ground (pers. obs.), which minimizes the surface area of the organism in contact with the substrate. However, larger jumping spiders (Salticidae) and flat crab spiders (Selenopidae) have great difficulty due to their gait, and morphological adaptations e.g. tarsal scopulae (designed for increasing surface area and thus adhesion potential) and often get stuck in resin (pers. obs.). Early studies by Brues (1933, 1951) investigated progressive change in forest insect populations since the early Tertiary by comparing Baltic amber inclusions with extant specimens collected in a hilly, forested area of New England. He concluded that the insect population had changed considerably over time. The only collecting method used for the Recent fauna was to tack sticky dtanglefootT fly paper around the tree trunks. This may have sampled the fauna in a similar way to resin, by entrapping arthropods that walked over it, or that were blown on to it, but it would not have sampled organisms living in the cracks of the bark, nor would it have sampled in a similar manner to falling resin. In a natural situation, it would be unlikely that resin would form a ring around the tree trunk, as with the dtanglefootT fly paper, rather it would seep vertically downwards giving animals ascending, or descending the tree trunk the opportunity to avoid the potentially lethal trap, be it intentional or not. Brues only sampled for 5 months of the year and only sampled tree trunks. His lower finds of the orders Collembola and Thysanura in his Recent sample may have been a result of not sampling the ground fauna or beneath or within the cracks of the trunk bark. Brues (1933) also assumed the difference in odour between the resin and the dtanglefootT was insignif-
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icant in its attractant or repellent actions on the insects. Based on his earlier data, Brues (1951) commented on the presence of flies and ants in his samples. He stated that in amber Diptera accounted for 54% of all the insects trapped. In his fly paper census their proportion had risen to 72%, and in particular the Muscoidea (house flies, fruit flies, etc.) had showed a great relative increase. This should hardly have been surprising, as the main purpose of fly paper is to attract and kill flies, particularly muscoid flies. It can be assumed that the fly paper had positively attracted the flies, and his findings are an artefact of sampling bias resulting from this attractant affect. Another bstrikingQ example Brues (1951) mentioned were the ants. In his fly paper survey they were only about one ninth as abundant as they were in the amber. Brues proposed that their numbers had declined in the same forest habitat, for some reason, over time. The climate in the Baltic region was subtropical at the time of the Baltic amber forests, quite unlike the Recent nearctic conditions found in New England. Today, ants increase in biomass and diversity towards the tropics. Thus, the different climatic conditions may account for the observed differences. Henwood (1993b) compared the inclusions found in Dominican Republic amber with data from different collecting techniques of Recent faunas and produced dendrograms of assemblage relatedness to identify the nearest modern sampling equivalent. Because the amber inclusion data most closely resembled emergence trap data, closely followed by pitfall trap data, she proposed that this could reflect beither falling resin, ground–subterranean level resin production or bothQ. Using similar techniques, but data at higher taxonomic resolution, Penney (2002) demonstrated that Dominican amber preferentially preserves active, trunk-dwelling faunas, as one might expect. Amber is diverse geographically, geologically and in terms of its botanical origins and associated chemistry; Martı´nez-Delclo`s et al. (2004: Appendix) listed 167 known deposits. Despite the large number of amber deposits listed by Martı´nez-Delclo`s et al. (2004: Appendix), few have had inclusions described in sufficient numbers to provide datasets suitable for quantitative analysis. The further one goes back in
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geological time, fewer extant genera and families are recorded as amber inclusions, which makes trying to determine biases based on a knowledge of the behaviour of Recent taxa problematic. In reality, the only two amber sources that are consistently producing identifiable inclusions in large numbers and which have many described taxa, are those from the Baltic region and the Dominican Republic. Baltic amber is approximately twice as old as Dominican amber and accordingly contains considerably more extinct supraspecific taxa. For example, five strictly fossil spider families are known from Baltic amber (see Wunderlich, 2004), whereas none are recorded from Dominican amber (Penney and Pe´rez-Gelabert, 2002; Penney, 2004a). The Baltic amber forest existed in a climate of early Tertiary equability, i.e. low temperature seasonality (Archibald and Farrell, 2003), very different to the climatic regime of high seasonality in the region at present. Therefore, it is not possible to make direct comparisons of the fossil fauna with the Recent fauna to try and determine biases. This is not true for Dominican amber. The amber was formed in a tropical climate similar to that in the region today, therefore the fossil and Recent faunas should be directly comparable ecologically. The geological history and palaeogeography of the Caribbean is exceedingly complex and not fully understood, with different authors having proposed different scenarios based on the same evidence (Hedges, 2001). However, the Greater Antilles, in their current guise, appear to be young geographical features (IturraldeVinent and Macphee, 1999). As a result of repeated transgressions, subsidence, the K/T bolide impact and associated mega-tsunamis, on-island lineages must be younger than mid-Eocene (Iturralde-Vinent and Macphee, 1999). During the amber-forming resin secretion period (15–20 Ma) (Iturralde-Vinent and Macphee, 1996) Hispaniola was probably a distinct island, although this remains to be confirmed; there may have been a connection to Puerto Rico via a narrow neck of land, but this is not certain (Iturralde-Vinent and Macphee, 1999). This paper investigates the completeness of our knowledge, and degree of similarity of the fossil and Recent Hispaniolan spider faunas, in order to ascertain whether or not comparing them would help determine taxonomic bias of amber preservation. This is the first
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Zoridae Uloboridae Trochanteriidae Thomisidae Theridiosomatidae Theridiidae Theraphosidae Tetragnathidae Tetrablemmidae Sparassidae Sicariidae Selenopidae Segestriidae Scytodidae Salticidae Prodidomidae
Family
Pisauridae Pholcidae Philodromidae Palpimanidae Oxyopidae Oonopidae Oecobiidae Ochyroceratidae
extant species amber species
Nesticidae Mysmenidae Miturgidae Mimetidae Microstigmatidae Lycosidae Liocranidae Linyphiidae Hersiliidae Gnaphosidae Filistatidae Drymusidae Dipluridae Dictynidae Desidae Deinopidae Cyrtaucheniidae Ctenidae Corinnidae Clubionidae Caponiidae Barychelidae Araneidae Anyphaenidae Anapidae Amaurobiidae
0
10
20
30 40 Number of species
50
60
Fig. 1. Hispaniolan spider families with numbers of species for the amber and extant faunas.
D. Penney / Palaeogeography, Palaeoclimatology, Palaeoecology 223 (2005) 1–8
5
25
Number of families
20
extant amber
15
10
5
0 1
4
7
10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55
Number of known species Fig. 2. Ranked species frequency occurrence for the Hispaniolan amber and extant spider faunas.
quantitative analysis of the dataset sizes required to investigate taxonomic bias of amber preservation. Spiders are appropriate taxa for this study because of their frequent occurrence as amber inclusions (ratio of extant : fossil species = 1 : 0.55, N = 473). In contrast, other groups for which extant and fossil Hispaniolan species data are readily available are poorly known as fossils, e.g. Trichoptera (ratio = 1 : 0.29, N = 99, Flint and Pe´rez-Gelabert, 1999), Blattodea (ratio = 1 : 0.08, N = 92, Gutie´rrez and Pe´rez-Gelabert, 2000), Neuroptera (ratio = 1 : 0.06, N = 55, Pe´rez-Gelabert and Flint, 2001), Orthoptera (ratio = 1 : 0.08, N = 111, Pe´rezGelabert, 2001) and Diplopoda (ratio = 1 : 0.11, N = 162, Pe´rez-Asso and Pe´rez-Gelabert, 2001).
2. Methods The number of species per family for the amber and extant faunas were derived from the following literature sources: Alayo´n-Garcı´a (2004), Penney and Pe´rez-Gelabert (2002), Penney (2004a, 2005). The family species richness frequencies for both faunas were ranked and Chao 1 and abundance-based coverage (ACE) estimators of richness were calculated using Colwell (1997). The former technique is a nonparametric estimator of the number of classes in a population (Chao, 1984) and the latter is an estimator based on those classes with ten or fewer individuals in
the sample and is particularly useful when some classes are very common and others very rare (Chao et al., 1993).
3. Results Fig. 1 shows the spider families present on Hispaniola and the number of species known from the amber and extant faunas. Overall, the two faunas are similar at family level, but some distinct differences are apparent. Hispaniolan records of the families Cyrtaucheniidae, Microstigmatidae, Ochyroceratidae, Palpimanidae, Tetrablemmidae, Agelenidae, Anapidae and Mysmenidae are known only from amber, whereas Drymusidae, Deinopidae, Desidae, Amaurobiidae, Prodidomidae and Zoridae are known only from the extant fauna. Fig. 2 shows the frequencies of families known from only one species (singletons), two species (doubletons), three species (tripletons), etc. (data from
Table 1 Amber and extant fauna family richness estimations calculated using Colwell (1997) Fauna
N (families)
Amber 44 Extant 42
N (species)
ACE
Chao 1
Chao 1 s.d.
168 305
91.79 51.17
90.33 53.16
35.69 11.17
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Fig. 1) for both amber and extant faunas. Family richness estimations are given in Table 1.
4. Discussion This is the first time that taxonomic richness comparisons have been made quantitatively between extant and fossil amber spider faunas. Hispaniola is unique in that more spider families are recorded from fossil species than are recorded from extant species, and many spider families on Hispaniola are known as fossils only from Dominican amber. Theridiidae and Pholcidae are known from both the amber and extant faunas but are more diverse as fossils, however, these differences are insignificant (Fig. 1). Oonopidae is also known from both faunas and appears significantly more diverse as fossils. This family is superabundant in many inclusion-bearing ambers (Penney, in press a), so their high occurrence here is not unexpected. Also, given the tiny size of these spiders (b3 mm), they are easily overlooked when collecting extant specimens, especially if the collectors are entomologists opportunistically collecting spiders, rather than arachnologists, as was the case with most spider collections made from Hispaniola (see Penney and Pe´rez-Gelabert, 2002). Dictynidae are significantly more diverse in the fossil fauna (15 fossil species, one extant) and this observation remains unexplained. Again, the family consists of tiny spiders, which could easily be overlooked. The fossils placed in the family Trochanteriidae (unknown from the extant fauna) all belong in the fossil genus Veterator (Petrunkevitch, 1963), which was only tentatively placed in this family by Wunderlich (2004). The remaining families known as fossils but unrecorded for the extant fauna are all small spiders and again have probably been overlooked. For example, Ochyroceratidae is recorded from Isla de Navassa (Alayo´n-Garcı´a, 2001), a very small island (5.2 km2) 64 km west of Hispaniola. Based on a large proportion of new species records (and a new family record—Prodidomidae [see Platnick and Penney, 2004]) for Hispaniola from a small collection made by the author (Penney, 2004a), it is evident that the extant fauna is poorly known. Thus, it can be expected that many of the families known only from amber can be expected to have extant relatives
on the island today (Penney, 1999). For example, the family Hersiliidae, known from the fossil fauna since the description by Schawaller (1981), has only recently been reported in the extant fauna by Rheims and Brescovit (2004). Penney (1999) suggested that some, if not all families known from the Recent, but not amber Hispaniolan spider fauna may have colonized Hispaniola since the period of amberforming resin secretion in the Tertiary. This hypothesis is unequivocally falsifiable though the future discovery of these families in Dominican amber as has occurred with Mysmenidae (Penney, 2000; the specimens described by Wunderlich (1998) are actually in Madagascan copal [Wunderlich, 2004]) and Filistatidae (Penney, in press b,c). Given the young age of the amber and the similarity of the extant and amber faunas at family level, the a priori assumption is that the Hispaniolan spider fauna had a similar diversity in the Miocene to that observed/ expected today. Because not all Miocene species will have been preserved in amber, and because only a relatively small proportion of the individuals of those that have, will be found as fossils, there will be a higher likelihood of more taxa occurring as singletons for the fossil fauna than for the extant, thus producing overly skewed data. Indeed, this is observed (Fig. 2): singletons-fossil = 54.5%, extant = 28.6%; the doubletons are similar-fossil = 11.4%, extant = 11.9%. This exceptionally high proportion of singletons for the fossil fauna accounts for the overestimation of the richness values for the amber taxa (Table 1). The values for the extant taxa are closer to that expected for a neotropical spider assemblage, but the standard deviation is still slightly high. Large collections of unstudied Dominican amber spiders exist in museums around the world and new material is continually being mined. Future research on these fossil collections will identify new amber species and reduce the number of families in the lower frequency classes, which will in turn lower the richness estimates. Additional work on the Recent fauna will reduce the standard deviation to provide a more reliable richness estimate. Thus, future research on both fossil and Recent faunas should minimize data-related differences at family level and leave only those that relate to bias of entrapment. Poinar and Poinar (1999) commented on the relative frequency of different guilds preserved in
D. Penney / Palaeogeography, Palaeoclimatology, Palaeoecology 223 (2005) 1–8
amber, noting that the most common inclusions were those that lived or foraged on the bark of trees, followed by winged insects that may have alighted, or been blown against, the sticky resin. Other organisms may have been directly attracted to the resin, such as bees that collect the resin, and predators or scavengers trying to extricate potential prey. It is possible to further divide such guilds (e.g. Penney, 2002) and given more complete data it will be possible to compare fossil and extant datasets to distinguish taxonomic biases of amber preservation. For example, an investigation to identify the different guilds in the Recent fauna present on tree trunks could be compared against those preserved as amber inclusions to determine what proportion of the total trunk fauna had been captured. Hypotheses regarding entrapment bias could be generated and tested using living organisms and a present day resin analogue. When it is known what fraction of the overall fauna the Recent trunk fauna represents, it will be possible to extrapolate the amber inclusion data to predict the overall Miocene palaeodiversity in the Dominican Republic amber-producing forest. However, given the overly incomplete nature of our knowledge of both fossil and Recent Hispaniolan spider faunas, it would be premature to attempt this at present. Other invertebrate groups should show similar trends towards similarities and dissimilarities and a better picture of bias would be gained through experts on different groups working together. This paper is, in part, a call for such a concerted and collaborative effort. Despite the general similarities of the fossil and Recent Hispaniolan spider fauna discussed above, some distinct differences occur in other orders, such as certain extant genera of Hymenoptera, Isoptera and Coleoptera that were present on Hispaniola in the Miocene but which are absent on the island today (Wilson, 1985; Nagel, 1997; Poinar and Poinar, 1999). Many insects are more susceptible to extinction than spiders because they form specialized associations with other organisms, such as plants, whereas most spiders are generalist predators and if one prey item becomes extinct they can easily switch to another source (Penney et al., 2003; Penney, 2004b). In addition, extinction resistance in spiders may be facilitated by their ability to survive extended periods of starvation, or other adverse conditions, by entering a state of metabolic torpor.
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The Dominican Republic is the only place on Earth where fossils in amber occur in sufficient numbers and that are closely related to the extant fauna, such that direct diversity/ecological comparisons can be made. A number of inroads have been made, which will assist as the basis for such a research project. Dominican amber spiders were sorted to predation guilds by Penney (2002), a checklist of fossil and Recent Hispaniolan spiders was provided by Penney and Pe´rez-Gelabert (2002; updated by Penney, 2004a) and an annotated systematic catalogue of Dominican amber spiders which lists all individual specimens cited in the literature is in preparation and will serve as an initial database for quantitative investigations of relative abundance. Similar research could be undertaken on copal (e.g., from Madagascar, East Africa, the Dominican Republic or Colombia) or Recent resins set in their present environment and compared against the extant community, but no large datasets exist for the former and the latter would not be based on direct evidence from the fossil record. It may be possible to extrapolate future conclusions derived from Dominican Republic amber to other ambers, but care should be taken in doing so until it is determined whether or not the trapping mechanisms are uniform between ambers of different botanical origins.
Acknowledgements I thank Drs P.A. Selden and W.R. Cullen (University of Manchester), Drs A.M. Langan and C.P. Wheater (Manchester Metropolitan University) and two anonymous reviewers for their comments on the manuscript. I acknowledge a Leverhulme Trust grant.
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Penney, D., 2005. First Caribbean Floricomus (Araneae: Linyphiidae), a new species in Miocene Dominican Republic amber. A new synonymy for the extant American fauna. Geologica Acta 3, 59 – 64. Penney, D., in press-a. Fossil oonopid spiders in Cretaceous ambers from Canada and Myanmar. Palaeontology. Penney, D., in press-b. First Filistatidae in the fossil record: a new species of Misionella in Miocene amber from the Dominican Republic. Journal of Arachnology 33. Penney, D., in press-c. Fossil blood droplets in Miocene Dominican amber yield clues to speed and direction of resin secretion. Palaeontology. Penney, D., Pe´rez-Gelabert, D.E., 2002. Comparison of the Recent and Miocene Hispaniolan spider faunas. Re´vista Iberica de Aracnologı´a 6, 203 – 223. Penney, D., Wheater, C.P., Selden, P.A., 2003. Resistance of spiders to Cretaceous–Tertiary extinction events. Evolution 57, 2599 – 2607. Pe´rez-Asso, A.R., Pe´rez-Gelabert, D.E., 2001. Checklist of the millipedes (Diplopoda) of Hispaniola. Boletin de la Sociedad Entomolo´gica Aragonesa 28, 67 – 80. Pe´rez-Gelabert, D.E., 2001. Preliminary checklist of the Orthoptera (Saltatoria) of Hispaniola. Journal of Orthoptera Research 10, 63 – 74. Pe´rez-Gelabert, D.E., Flint Jr., O.S., 2001. Annotated list of the Neuroptera of Hispaniola with new faunistic records of some species. Journal of Neuropterology 3, 9 – 23 (for 2000). Petrunkevitch, A., 1963. Chiapas amber spiders. University of California Publications in Entomology 31, 1 – 40. Pike, E.M., 1993. Amber taphonomy and collecting biases. Palaios 8, 411 – 419. Pike, E.M., 1994. Historical changes in insect community structure as indicated by hexapods of Upper Cretaceous Alberta (Grassy Lake) amber. Canadian Entomologist 126, 695 – 702. Platnick, N.I., Penney, D., 2004. A revision of the widespread spider genus Zimiris (Araneae, Prodidomidae). American Museum Novitates 3450, 1 – 12. Poinar Jr., G.O., Poinar, R., 1999. The Amber Forest: A Reconstruction of a Vanished World. Princeton University Press, New Jersey. Rheims, C.A., Brescovit, A.D., 2004. Revision and cladistic analysis of the spider family Hersiliidae (Arachnida, Araneae) with emphasis on Neotropical and Nearctic species. Insect Systematics and Evolution, vol. 35, pp. 189 – 239. Ross, A.J., 1997. Insects in amber. Geology Today 13, 24 – 28. Schawaller, W., 1981. Die spinnefamilie hersiliidae in Dominikanischem Bernstein (Stuttgarter Bernsteinsammlung: Arachnida, Araneae). Stuttgarter Beitr7ge zur Naturkunde. Serie B, Geologie und Pal7ontologie 79, 1 – 10. Wilson, E.O., 1985. Invasion and extinction in the West Indian ant fauna: evidence from Dominican amber. Science 229, 265 – 267. Wunderlich, J., 1998. Beschreibung der ersten fossilen Spinnen der Unterfamilien Mysmeninae (Anapidae) und Erigoninae (Linyphiidae) im Dominikanischen Bernstein (Arachnida: Araneae). Entomologische Zeitschrift 108, 363 – 367. Wunderlich, J., 2004. Fossil spiders in amber and copal. Beitr7ge zur Araneologie 3ab, 1 – 1908.
Importance of Dominican Republic amber for determining taxonomic bias of fossil resin preservation—A case study of spiders David PenneyT Earth, Atmospheric and Environmental Sciences, The University of Manchester, Manchester M13 9PL, United Kingdom Received 13 November 2004; received in revised form 3 March 2005; accepted 21 March 2005
Abstract Fossils preserved in amber represent only a small fraction of the biota which was alive in the amber forest. In order to make accurate palaeoenvironmental reconstructions, it is necessary to determine the biases which affect preservation. Only the Baltic and Dominican Republic amber deposits have had inclusions described in sufficient quantities suitable for quantitative analyses. Baltic amber is twice the age of Dominican, with a correspondingly higher proportion of extinct supraspecific taxa, and was produced in a climate very different to that in the region today. Dominican Republic amber was formed in a tropical climate similar to that in the region today and many of the preserved spider supraspecific taxa are extant. Therefore, the fossil and Recent Hispaniolan faunas are directly comparable ecologically. Spiders (extinct and extant) are significantly more diverse than other groups for which Hispaniolan species diversity data are available. Thus, they form an ideal model for assessing taxonomic bias of Dominican amber preservation. This is the first time that taxonomic richness estimates have been made and compared quantitatively between extant and fossil amber faunas. Extant and extinct (Dominican Republic amber) Hispaniolan spiders are compared at family level. Overall, the two faunas are similar but some distinct differences are apparent. Hispaniolan representatives of the families Cyrtaucheniidae, Microstigmatidae, Ochyroceratidae, Palpimanidae, Tetrablemmidae, Agelenidae, Anapidae and Mysmenidae are known only from amber, whereas Drymusidae, Deinopidae, Desidae, Amaurobiidae, Prodidomidae and Zoridae are known only from the extant fauna. Many families have similar fossil and extant species diversities. Oonopidae and Dictynidae are significantly more diverse in amber. Many families currently known only from Dominican amber probably have undiscovered extant species on Hispaniola. Family species richness estimates were calculated for both fossil and extant spider faunas, but only those for the extant fauna provide results consistent with a neotropical spider assemblage. Fossil richness estimates were excessively high as a result of the large number of singletons. Nevertheless, the Dominican Republic is the only place on Earth where fossils in amber occur in sufficient numbers and that are closely related to the extant fauna, such that direct diversity/ ecological comparisons can be made. Given future research directed at identifying spiders and other inclusions in the large
T Fax: +44 161 275 3947. E-mail address: [email protected]. 0031-0182/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2005.03.022
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amber collections amassed in Museums around the world, detailed comparisons of these faunas will allow us to better determine taxonomic biases associated with amber preservation. D 2005 Elsevier B.V. All rights reserved. Keywords: Arachnida; Araneae; Dominican Republic amber; Fossil; Taxonomic bias
1. Introduction Amber, fossilized tree resin, is a particularly important resource of fossil data for recreating terrestrial palaeoecosystems. In contrast to sedimentary fossil deposits, where terrestrial invertebrates are usually allochthonous, amber contains primarily terrestrial fossils, which were sampled in situ, in the palaeohabitat. However, fossils preserved in amber still represent only a small fraction of the biota alive in the amber-producing forest. Amber, as with all other forms of fossilization, is subject to unique preservation biases. It is equally important that we elucidate what other organisms were present in the palaeoenvironment at the same time as those preserved as fossils, but which evaded entrapment in the resin. That is, we need to understand the taxonomic bias of resin entrapment before we can draw a more complete picture of the palaeoenvironment. Few authors have investigated bias of amber inclusions. Henwood (1993a) and Ross (1997) acknowledged, with qualitative examples, biases in relation to size, phenology and behaviour of the amber insect fauna. Martı´nez-Delclo`s et al. (2004) discussed a number of factors which may have promoted the preservation of some groups of invertebrates in preference to others, including resin viscosity, insect behaviour, insect habitat preferences, resin chemistry and abiotic environmental factors. Pike (1993, 1994) recognized the necessity of quantifying the biases associated with resin as an arthropod trap, prior to addressing diversity and community structure through amber inclusions, but stated that no published data were suitable for assessing them. Despite recognizing the importance of understanding these biases, Pike (1994), with some reservation, assumed that different resins sampled insect faunas in similar ways, and thus had the same taphonomic biases. I doubt that this assumption will prove to be true, but it requires further investigation. The general, oft-encountered,
statement that small organisms get trapped whereas larger ones do not because they are strong enough to escape, has not been thoroughly tested and appears to be incorrect. For example, tiny araneoid spiders can often walk over sticky surfaces relatively unhindered, because they walk on the tips of their tarsi with their bodies raised off the ground (pers. obs.), which minimizes the surface area of the organism in contact with the substrate. However, larger jumping spiders (Salticidae) and flat crab spiders (Selenopidae) have great difficulty due to their gait, and morphological adaptations e.g. tarsal scopulae (designed for increasing surface area and thus adhesion potential) and often get stuck in resin (pers. obs.). Early studies by Brues (1933, 1951) investigated progressive change in forest insect populations since the early Tertiary by comparing Baltic amber inclusions with extant specimens collected in a hilly, forested area of New England. He concluded that the insect population had changed considerably over time. The only collecting method used for the Recent fauna was to tack sticky dtanglefootT fly paper around the tree trunks. This may have sampled the fauna in a similar way to resin, by entrapping arthropods that walked over it, or that were blown on to it, but it would not have sampled organisms living in the cracks of the bark, nor would it have sampled in a similar manner to falling resin. In a natural situation, it would be unlikely that resin would form a ring around the tree trunk, as with the dtanglefootT fly paper, rather it would seep vertically downwards giving animals ascending, or descending the tree trunk the opportunity to avoid the potentially lethal trap, be it intentional or not. Brues only sampled for 5 months of the year and only sampled tree trunks. His lower finds of the orders Collembola and Thysanura in his Recent sample may have been a result of not sampling the ground fauna or beneath or within the cracks of the trunk bark. Brues (1933) also assumed the difference in odour between the resin and the dtanglefootT was insignif-
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icant in its attractant or repellent actions on the insects. Based on his earlier data, Brues (1951) commented on the presence of flies and ants in his samples. He stated that in amber Diptera accounted for 54% of all the insects trapped. In his fly paper census their proportion had risen to 72%, and in particular the Muscoidea (house flies, fruit flies, etc.) had showed a great relative increase. This should hardly have been surprising, as the main purpose of fly paper is to attract and kill flies, particularly muscoid flies. It can be assumed that the fly paper had positively attracted the flies, and his findings are an artefact of sampling bias resulting from this attractant affect. Another bstrikingQ example Brues (1951) mentioned were the ants. In his fly paper survey they were only about one ninth as abundant as they were in the amber. Brues proposed that their numbers had declined in the same forest habitat, for some reason, over time. The climate in the Baltic region was subtropical at the time of the Baltic amber forests, quite unlike the Recent nearctic conditions found in New England. Today, ants increase in biomass and diversity towards the tropics. Thus, the different climatic conditions may account for the observed differences. Henwood (1993b) compared the inclusions found in Dominican Republic amber with data from different collecting techniques of Recent faunas and produced dendrograms of assemblage relatedness to identify the nearest modern sampling equivalent. Because the amber inclusion data most closely resembled emergence trap data, closely followed by pitfall trap data, she proposed that this could reflect beither falling resin, ground–subterranean level resin production or bothQ. Using similar techniques, but data at higher taxonomic resolution, Penney (2002) demonstrated that Dominican amber preferentially preserves active, trunk-dwelling faunas, as one might expect. Amber is diverse geographically, geologically and in terms of its botanical origins and associated chemistry; Martı´nez-Delclo`s et al. (2004: Appendix) listed 167 known deposits. Despite the large number of amber deposits listed by Martı´nez-Delclo`s et al. (2004: Appendix), few have had inclusions described in sufficient numbers to provide datasets suitable for quantitative analysis. The further one goes back in
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geological time, fewer extant genera and families are recorded as amber inclusions, which makes trying to determine biases based on a knowledge of the behaviour of Recent taxa problematic. In reality, the only two amber sources that are consistently producing identifiable inclusions in large numbers and which have many described taxa, are those from the Baltic region and the Dominican Republic. Baltic amber is approximately twice as old as Dominican amber and accordingly contains considerably more extinct supraspecific taxa. For example, five strictly fossil spider families are known from Baltic amber (see Wunderlich, 2004), whereas none are recorded from Dominican amber (Penney and Pe´rez-Gelabert, 2002; Penney, 2004a). The Baltic amber forest existed in a climate of early Tertiary equability, i.e. low temperature seasonality (Archibald and Farrell, 2003), very different to the climatic regime of high seasonality in the region at present. Therefore, it is not possible to make direct comparisons of the fossil fauna with the Recent fauna to try and determine biases. This is not true for Dominican amber. The amber was formed in a tropical climate similar to that in the region today, therefore the fossil and Recent faunas should be directly comparable ecologically. The geological history and palaeogeography of the Caribbean is exceedingly complex and not fully understood, with different authors having proposed different scenarios based on the same evidence (Hedges, 2001). However, the Greater Antilles, in their current guise, appear to be young geographical features (IturraldeVinent and Macphee, 1999). As a result of repeated transgressions, subsidence, the K/T bolide impact and associated mega-tsunamis, on-island lineages must be younger than mid-Eocene (Iturralde-Vinent and Macphee, 1999). During the amber-forming resin secretion period (15–20 Ma) (Iturralde-Vinent and Macphee, 1996) Hispaniola was probably a distinct island, although this remains to be confirmed; there may have been a connection to Puerto Rico via a narrow neck of land, but this is not certain (Iturralde-Vinent and Macphee, 1999). This paper investigates the completeness of our knowledge, and degree of similarity of the fossil and Recent Hispaniolan spider faunas, in order to ascertain whether or not comparing them would help determine taxonomic bias of amber preservation. This is the first
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Zoridae Uloboridae Trochanteriidae Thomisidae Theridiosomatidae Theridiidae Theraphosidae Tetragnathidae Tetrablemmidae Sparassidae Sicariidae Selenopidae Segestriidae Scytodidae Salticidae Prodidomidae
Family
Pisauridae Pholcidae Philodromidae Palpimanidae Oxyopidae Oonopidae Oecobiidae Ochyroceratidae
extant species amber species
Nesticidae Mysmenidae Miturgidae Mimetidae Microstigmatidae Lycosidae Liocranidae Linyphiidae Hersiliidae Gnaphosidae Filistatidae Drymusidae Dipluridae Dictynidae Desidae Deinopidae Cyrtaucheniidae Ctenidae Corinnidae Clubionidae Caponiidae Barychelidae Araneidae Anyphaenidae Anapidae Amaurobiidae
0
10
20
30 40 Number of species
50
60
Fig. 1. Hispaniolan spider families with numbers of species for the amber and extant faunas.
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5
25
Number of families
20
extant amber
15
10
5
0 1
4
7
10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55
Number of known species Fig. 2. Ranked species frequency occurrence for the Hispaniolan amber and extant spider faunas.
quantitative analysis of the dataset sizes required to investigate taxonomic bias of amber preservation. Spiders are appropriate taxa for this study because of their frequent occurrence as amber inclusions (ratio of extant : fossil species = 1 : 0.55, N = 473). In contrast, other groups for which extant and fossil Hispaniolan species data are readily available are poorly known as fossils, e.g. Trichoptera (ratio = 1 : 0.29, N = 99, Flint and Pe´rez-Gelabert, 1999), Blattodea (ratio = 1 : 0.08, N = 92, Gutie´rrez and Pe´rez-Gelabert, 2000), Neuroptera (ratio = 1 : 0.06, N = 55, Pe´rez-Gelabert and Flint, 2001), Orthoptera (ratio = 1 : 0.08, N = 111, Pe´rezGelabert, 2001) and Diplopoda (ratio = 1 : 0.11, N = 162, Pe´rez-Asso and Pe´rez-Gelabert, 2001).
2. Methods The number of species per family for the amber and extant faunas were derived from the following literature sources: Alayo´n-Garcı´a (2004), Penney and Pe´rez-Gelabert (2002), Penney (2004a, 2005). The family species richness frequencies for both faunas were ranked and Chao 1 and abundance-based coverage (ACE) estimators of richness were calculated using Colwell (1997). The former technique is a nonparametric estimator of the number of classes in a population (Chao, 1984) and the latter is an estimator based on those classes with ten or fewer individuals in
the sample and is particularly useful when some classes are very common and others very rare (Chao et al., 1993).
3. Results Fig. 1 shows the spider families present on Hispaniola and the number of species known from the amber and extant faunas. Overall, the two faunas are similar at family level, but some distinct differences are apparent. Hispaniolan records of the families Cyrtaucheniidae, Microstigmatidae, Ochyroceratidae, Palpimanidae, Tetrablemmidae, Agelenidae, Anapidae and Mysmenidae are known only from amber, whereas Drymusidae, Deinopidae, Desidae, Amaurobiidae, Prodidomidae and Zoridae are known only from the extant fauna. Fig. 2 shows the frequencies of families known from only one species (singletons), two species (doubletons), three species (tripletons), etc. (data from
Table 1 Amber and extant fauna family richness estimations calculated using Colwell (1997) Fauna
N (families)
Amber 44 Extant 42
N (species)
ACE
Chao 1
Chao 1 s.d.
168 305
91.79 51.17
90.33 53.16
35.69 11.17
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Fig. 1) for both amber and extant faunas. Family richness estimations are given in Table 1.
4. Discussion This is the first time that taxonomic richness comparisons have been made quantitatively between extant and fossil amber spider faunas. Hispaniola is unique in that more spider families are recorded from fossil species than are recorded from extant species, and many spider families on Hispaniola are known as fossils only from Dominican amber. Theridiidae and Pholcidae are known from both the amber and extant faunas but are more diverse as fossils, however, these differences are insignificant (Fig. 1). Oonopidae is also known from both faunas and appears significantly more diverse as fossils. This family is superabundant in many inclusion-bearing ambers (Penney, in press a), so their high occurrence here is not unexpected. Also, given the tiny size of these spiders (b3 mm), they are easily overlooked when collecting extant specimens, especially if the collectors are entomologists opportunistically collecting spiders, rather than arachnologists, as was the case with most spider collections made from Hispaniola (see Penney and Pe´rez-Gelabert, 2002). Dictynidae are significantly more diverse in the fossil fauna (15 fossil species, one extant) and this observation remains unexplained. Again, the family consists of tiny spiders, which could easily be overlooked. The fossils placed in the family Trochanteriidae (unknown from the extant fauna) all belong in the fossil genus Veterator (Petrunkevitch, 1963), which was only tentatively placed in this family by Wunderlich (2004). The remaining families known as fossils but unrecorded for the extant fauna are all small spiders and again have probably been overlooked. For example, Ochyroceratidae is recorded from Isla de Navassa (Alayo´n-Garcı´a, 2001), a very small island (5.2 km2) 64 km west of Hispaniola. Based on a large proportion of new species records (and a new family record—Prodidomidae [see Platnick and Penney, 2004]) for Hispaniola from a small collection made by the author (Penney, 2004a), it is evident that the extant fauna is poorly known. Thus, it can be expected that many of the families known only from amber can be expected to have extant relatives
on the island today (Penney, 1999). For example, the family Hersiliidae, known from the fossil fauna since the description by Schawaller (1981), has only recently been reported in the extant fauna by Rheims and Brescovit (2004). Penney (1999) suggested that some, if not all families known from the Recent, but not amber Hispaniolan spider fauna may have colonized Hispaniola since the period of amberforming resin secretion in the Tertiary. This hypothesis is unequivocally falsifiable though the future discovery of these families in Dominican amber as has occurred with Mysmenidae (Penney, 2000; the specimens described by Wunderlich (1998) are actually in Madagascan copal [Wunderlich, 2004]) and Filistatidae (Penney, in press b,c). Given the young age of the amber and the similarity of the extant and amber faunas at family level, the a priori assumption is that the Hispaniolan spider fauna had a similar diversity in the Miocene to that observed/ expected today. Because not all Miocene species will have been preserved in amber, and because only a relatively small proportion of the individuals of those that have, will be found as fossils, there will be a higher likelihood of more taxa occurring as singletons for the fossil fauna than for the extant, thus producing overly skewed data. Indeed, this is observed (Fig. 2): singletons-fossil = 54.5%, extant = 28.6%; the doubletons are similar-fossil = 11.4%, extant = 11.9%. This exceptionally high proportion of singletons for the fossil fauna accounts for the overestimation of the richness values for the amber taxa (Table 1). The values for the extant taxa are closer to that expected for a neotropical spider assemblage, but the standard deviation is still slightly high. Large collections of unstudied Dominican amber spiders exist in museums around the world and new material is continually being mined. Future research on these fossil collections will identify new amber species and reduce the number of families in the lower frequency classes, which will in turn lower the richness estimates. Additional work on the Recent fauna will reduce the standard deviation to provide a more reliable richness estimate. Thus, future research on both fossil and Recent faunas should minimize data-related differences at family level and leave only those that relate to bias of entrapment. Poinar and Poinar (1999) commented on the relative frequency of different guilds preserved in
D. Penney / Palaeogeography, Palaeoclimatology, Palaeoecology 223 (2005) 1–8
amber, noting that the most common inclusions were those that lived or foraged on the bark of trees, followed by winged insects that may have alighted, or been blown against, the sticky resin. Other organisms may have been directly attracted to the resin, such as bees that collect the resin, and predators or scavengers trying to extricate potential prey. It is possible to further divide such guilds (e.g. Penney, 2002) and given more complete data it will be possible to compare fossil and extant datasets to distinguish taxonomic biases of amber preservation. For example, an investigation to identify the different guilds in the Recent fauna present on tree trunks could be compared against those preserved as amber inclusions to determine what proportion of the total trunk fauna had been captured. Hypotheses regarding entrapment bias could be generated and tested using living organisms and a present day resin analogue. When it is known what fraction of the overall fauna the Recent trunk fauna represents, it will be possible to extrapolate the amber inclusion data to predict the overall Miocene palaeodiversity in the Dominican Republic amber-producing forest. However, given the overly incomplete nature of our knowledge of both fossil and Recent Hispaniolan spider faunas, it would be premature to attempt this at present. Other invertebrate groups should show similar trends towards similarities and dissimilarities and a better picture of bias would be gained through experts on different groups working together. This paper is, in part, a call for such a concerted and collaborative effort. Despite the general similarities of the fossil and Recent Hispaniolan spider fauna discussed above, some distinct differences occur in other orders, such as certain extant genera of Hymenoptera, Isoptera and Coleoptera that were present on Hispaniola in the Miocene but which are absent on the island today (Wilson, 1985; Nagel, 1997; Poinar and Poinar, 1999). Many insects are more susceptible to extinction than spiders because they form specialized associations with other organisms, such as plants, whereas most spiders are generalist predators and if one prey item becomes extinct they can easily switch to another source (Penney et al., 2003; Penney, 2004b). In addition, extinction resistance in spiders may be facilitated by their ability to survive extended periods of starvation, or other adverse conditions, by entering a state of metabolic torpor.
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The Dominican Republic is the only place on Earth where fossils in amber occur in sufficient numbers and that are closely related to the extant fauna, such that direct diversity/ecological comparisons can be made. A number of inroads have been made, which will assist as the basis for such a research project. Dominican amber spiders were sorted to predation guilds by Penney (2002), a checklist of fossil and Recent Hispaniolan spiders was provided by Penney and Pe´rez-Gelabert (2002; updated by Penney, 2004a) and an annotated systematic catalogue of Dominican amber spiders which lists all individual specimens cited in the literature is in preparation and will serve as an initial database for quantitative investigations of relative abundance. Similar research could be undertaken on copal (e.g., from Madagascar, East Africa, the Dominican Republic or Colombia) or Recent resins set in their present environment and compared against the extant community, but no large datasets exist for the former and the latter would not be based on direct evidence from the fossil record. It may be possible to extrapolate future conclusions derived from Dominican Republic amber to other ambers, but care should be taken in doing so until it is determined whether or not the trapping mechanisms are uniform between ambers of different botanical origins.
Acknowledgements I thank Drs P.A. Selden and W.R. Cullen (University of Manchester), Drs A.M. Langan and C.P. Wheater (Manchester Metropolitan University) and two anonymous reviewers for their comments on the manuscript. I acknowledge a Leverhulme Trust grant.
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