Anthonie Hellemond (Belgium)
Spiders represent the most diverse group of obligate predators (that is, predators that feed solely on other animals) in terrestrial ecosystems today, with almost 48,000 extant species in 118 families described to date. The number increases annually by approximately 500 species as a result of new discoveries and it has been estimated that the true diversity may number around 160,000 extant species. This great diversity is no doubt at least in part due to their geological longevity, with the oldest known fossil spider dating back to the Carboniferous. In addition, spiders appear to have co-radiated along with their insect prey over geological time and they also appear to have been relatively resistant to extinction during the major events that eliminated many other terrestrial animal groups, such as the dinosaurs (Penney and Selden, 2011).
Most people seem to presume that spiders do not have a very good fossil record on account of their very small size and their lack of a mineralised, bony skeleton. However, spiders actually have a very good fossil record, with 1,347 fossil species currently recognised. Fossil spiders occur in rocks of various different types, but the vast majority and best-preserved spiders are found as inclusions in amber from various localities dating back to the Cretaceous, although preservation tends to be better in the younger (for example, Miocene and Eocene) ambers. The best known of these deposits is Baltic amber, with more than 650 fossil spider species recognised (Penney et al., 2012), representing close to half of the known fossil spider species described to date.
The Baltic amber forest
Baltic amber is by far the most famous and richly-endowed fossiliferous amber deposit anywhere in the world, with more than 3,500 described arthropod species to date. It is often dated as mid-Eocene (that is, Lutetian, about 44 to 49 million years old) and is thought to have been produced by an umbrella pine (Sciadopitys sp), although the identity of the Baltic amber tree is still somewhat of an enigma. In many respects, the fossil assemblage is indicative of a tropical-subtropical forest, with lightly wooded areas and plenty of freshwater habitats (Weitschat and Wichard, 2010). However, more recent work has proposed a late Eocene age and that the palaeoenvironment consisted of warm temperate humid conditions (Sadowski et al., 2017). The Baltic amber forest covered a vast area of Northern and Central Europe, so no doubt included a wide range of different habitat types and palaeoenvironmental settings.
History of Baltic amber spider research
Research on Baltic amber spiders has spanned almost two centuries, with major monographic contributions by Koch and Berendt (1854), Petrunkevitch (1942, 1958) and Wunderlich (2004). All of the spider species in Baltic amber are extinct, but the majority are assigned to extant families. There are also a few strictly fossil families (for example, Baltsuccinidae, Praetheridiidae, Protheridiidae and Succinomidae), the papers on which were self-published in non-peer-reviewed journals by Wunderlich, so these would benefit from independent scrutiny to confirm their taxonomic validity. Extinct families described by earlier workers, such as Koch and Berendt, and also Petrunkevitch, have subsequently been synonymised with extant families, apart from Insecutoridae, Spatiatoridae (Fig. 1) and Ephalmatoridae, which are still considered valid for the time being.
As a very crude estimate, spiders represent around 20% of all described Baltic amber species, yet they only represent around 4% to 6% of inclusions in a ‘random’ sample. However, the Baltic amber fauna is poorly known, with a mere 3,500 species described to date out of a predicted 193,000 species in total (Penney and Preziosi, 2014). Hence, the relative spider quotient (in terms of described fossil species) of Baltic amber is exceptionally high compared to other orders that we would expect to greatly exceed them in terms of palaeodiversity, for example, Diptera (flies, with about 800 species), Coleoptera (beetles, with 130 species), Hymenoptera (ants, bees and wasps, with 448 species) and Hemiptera (true bugs, with 111 species) (Baltic amber insect data from Weitschat and Wichard, 2010).
Described Baltic amber Diptera may be closer to 1,000 species. In extant arthropod samples from trees in both temperate and tropical forests, species from these insect orders far outnumber those of spiders. Thus, the described palaeodiversity of this deposit is still rather low in terms of the remaining taxonomic groups. Of course, there may be some unknown preferential entrapment bias operating for positive selection of spiders, but this is highly unlikely (Penney, 2016). The simplest explanation is that the high species richness of spiders in Baltic amber is significantly skewed as a result of the monographic studies mentioned above, which have preferentially chosen to cover spiders, particularly those of Wunderlich, who has described many of the species.
Much of the research on Baltic amber spiders has employed traditional light microscopy, but, in recent years, more advanced technological approaches have been applied, including X-ray computed tomography (CT). CT provides a non-destructive, minimum preparation method for imaging minute morphological details, including internal morphology, and generates three-dimensional reconstructions that can be sectioned and viewed from multiple angles. Essentially, it is possible to digitally dissect an amber inclusion and the technique can also be used to overcome the problem of the white emulsion coating (often referred to using the German word ‘Verlumung’) commonly encountered and obscuring important taxonomic features of fossils in Baltic amber (Fig. 2).
Dunlop et al. (2011) used CT to restudy a historical huntsman spider (Sparassidae) specimen of Koch and Berendt (1854), in which the amber had darkened over time due to oxidation, to the extent that the inclusion was difficult to view using traditional methods. Dunlop et al. (2012) used the technique to investigate a minute phoretic mite, which they were able to digitally dissect off the carapace of a Baltic amber spider and which (at just 176 microns body length) represents the smallest amber inclusion to be scanned to date using this technique. Most recently, I have had the technique applied to the undescribed female of the Baltic amber Tetrablemmidae spider, Balticoblemma unicorniculum (Fig. 3).
The resulting data from these methods can be loaded into three-dimensional printers to make a large physical model of the inclusion (Fig. 4). This also creates the opportunity for virtual libraries of CT data or even 3D reconstructions that can be electronically dissected on, or printed from, any computer anywhere in the world. The scan data can also be used to make video clips, which are now increasingly used as online supporting materials to published papers and some have also been made freely available on the internet. These videos are a great way for engaging the public in our science. For example, the video clip of the CT study of a huntsman spider mentioned above (https://www.youtube.com/watch?v=IL4f_x4CFQA) has received (at the time of writing in December 2018) 190,613 views on YouTube. Compare this to how many people probably read the actual paper in the printed journal and the fact that the paper has been cited only 29 times over about nine years.
In the past, people have passed off African copals (sub-fossil resin, in many cases less than 100 years old) as Baltic amber and some of these specimens remain misidentified as Baltic amber in museum collections today. Even more unscrupulous are those folks who have created fake ‘amber’ specimens with extant species inclusions inside for their own personal profit and some forgeries can be very difficult to detect.
Tests are available to provenance Baltic amber, and range from simple examination of other inclusions, for example, oak stellate hairs (see Fig. 6) and coatings of white emulsion are common in Baltic amber, to more sophisticated techniques, such as infra-red spectroscopy (Baltic amber has a unique ‘shoulder’ in its spectrograph), pyrolysis gas chromatography and mass spectroscopy for determining chemical signatures (Baltic amber contains succinic acid). Baltic amber also fluoresces under UV light, providing a quick and easy way to determine whether a specimen is likely to be genuine or not.
What can we learn from the Baltic amber spider fauna?
Of course, there are a great many things we can infer from fossils preserved in amber from any deposit, but in this short article, I will restrict the discussion to Baltic amber spiders.
Evolutionary origins and radiations
From looking at the evolutionary history of spiders (Penney and Selden, 2011), it is immediately obvious that many extant spider families have a very long geological record, extending back to the time of the non-avian dinosaurs. It is also significant that some of the most diverse spider families on the planet today do not have such an extensive fossil record and make their first appearance after the end-Cretaceous (KT) event.
For example, two of the most diverse families today – Salticidae (jumping spiders: 6,097 extant species) and Theridiidae (cobweb spiders: 2,509 extant species) – are unknown from the Cretaceous, despite extensive spider fossils, but they are relatively diverse in Baltic amber, suggesting their initial origins and radiations occurred post K/T. Jumping spiders occur frequently as fossils in Baltic amber (Fig. 5). As visual predators, they were presumably attracted to struggling insects trapped in sticky resin and eventually became entombed themselves, thus explaining the high frequency of this family in amber deposits where they occur. They are also highly distinctive as a result of their huge anterior median eyes, even as very tiny spiderlings, so it is unlikely they have been overlooked in Cretaceous deposits to date. Enigmatic is the absence of jumping spiders in Lowermost Eocene amber from Oise, France, which contains an otherwise diverse spider assemblage including Theridiidae. Hence, Baltic amber is significant in that jumping spiders make their first appearance as fossils in this deposit. It is also interesting to note that only a single, primitive salticid subfamily occurs in Baltic amber, whereas four subfamilies have been recorded from the younger (Miocene) amber deposits of the Dominican Republic.
Assassin spiders (Fig. 6) or dawn spiders as they are commonly known belong to the family Archaeidae and have a unique history amongst spiders. It is the only extant spider family to have initially been described from fossils before being found in the extant fauna. The family was first described from Baltic amber fossils in the monograph of Koch and Berendt (1854), before living examples were discovered in Madagascar some 27 years later. Today, this family is restricted to the Southern Hemisphere, which would (in the absence of a fossil record) suggest a Gondwanan origin and radiation for this family. However, these spiders have a rather diverse fossil record in the Northern Hemisphere (and especially in Baltic amber), which falsifies this hypothesis. That is, the current distribution is merely a product of a formerly widespread distribution and the extant species can be referred to as ousted relicts. This pattern is not restricted to this family; another example would be the spider family Cyatholipidae, which has a similar Southern Hemisphere distribution today and is also rather diverse and frequently encountered in Baltic amber (Fig. 7).
Palaeoecology of the amber forest (quantitative studies)
The large number of spider species described from Baltic and other ambers (for example, Dominican) means that datasets can be compiled that are of a size large enough for quantitative investigations, although few studies have taken advantage of these data. With regard to Baltic amber spiders, the only study to date is that of Penney and Langan (2006). They compared Baltic and Dominican amber spider faunas in connection with the size of the inclusions preserved, analysing data from 671 different species in 51 families. The species of spiders were spread across the entire phylogeny and included several different hunting guilds, such as web-weavers, hunters and sit-and-wait predators.
The study showed that there were no significant differences between amber type and presence of certain behavioural guilds. However, spiders in Baltic amber were significantly larger than those in Dominican amber, which was further investigated by looking more closely at those families common to both deposits and which included reasonable numbers in both deposits, that is, Salticidae, Theridiidae and Dictynidae. Significant differences were found for two of the families but not the other. Interestingly, those that were different came from the same behavioural guild, that is, web-weavers.
There was no difference in Salticidae (jumping spiders), which do not construct capture webs. It has been demonstrated experimentally that larger web-weaving spiders are found in more structurally complex habitats and, given that the Baltic amber producing tree was more structurally complex than the Dominican amber tree, the observed differences were attributed to this variation in structural complexity. The lack of difference in non-web-weavers suggested the different amber-forming resins were trapping organisms in the same way. Hence, the authors were able to demonstrate for the first time that the different amber faunas are directly comparable ecologically in terms of the resin sampling as a trap.
Palaeoecology of the amber forest (qualitative studies)
Certain types of spiders today are found only in specific habitat types or within a narrow range of environmental tolerances. These can be considered as indicator taxa and, as a general rule of thumb, it is not unreasonable to expect their close relatives in the fossil record to have had similar preferences. Similarly, the relative abundance of species within different families within the fossil amber assemblage can be compared with those of extant faunas to help facilitate palaeoenvironmental reconstructions. For example, in temperate regions, the spider family Linyphiidae tends to be more diverse than Theridiidae, whereas in more tropical latitudes, the reverse is the case – the latter family is much more diverse in Baltic amber. Obviously, quantitative approaches could also be applied to these data.
In many cases, it is possible to infer the behaviour of certain species based on the premise of behavioural fixity, which proposes that organisms in the past would have behaved in a similar manner to their close living relatives. For example, amber orb-web weaving spiders of the family Araneidae (Fig. 8), which are practically identical (in terms of gross morphology; species specific genitalia excluded) to modern araneids, almost certainly constructed orb-webs like their modern descendants do today.
In other instances, more direct evidence of behaviour and ecological interactions can be preserved in amber. For instance, spiders webs (sometimes with silk-wrapped prey) and, more rarely, egg cocoons are found as inclusions. Hunting spiders that do not construct capture webs may be found in association with their potential prey, for example, many armoured spiders (family, Zodariidae) are specialised predators of ants and Fig. 9 shows a specimen preserved close to an ant.
In addition to the example of mite phoresy mentioned earlier in connection with CT scanning, interesting spider associations described from Baltic amber include a pair of goblin spiders Orchestina sp (family Oonopidae) trapped during copulation (Wunderlich, 1982); Poinar (2000) described the parasitic mermithid nematode Heydenius araneus in the same piece of amber as its supposed crab spider host (Thomisidae); and Ohl (2011) described a phoretic mantispid larva attached to a clubionid-like spider.
Despite the large number of fossil spider species currently known from Baltic amber, any data derived from the taxonomic literature must be assessed carefully before they are used to address palaeoecological questions. Many of the species descriptions do not conform to the high standards expected of modern spider taxonomy and systematics, and many of the type specimens of those described in the nineteenth century are currently considered lost. Plenty of new taxa, including new fossil genera and even families, have been described based on juvenile specimens, a practice which is, on the whole, inappropriate.
Also, the majority of the more recently described fossil spider species names (even in the twenty first century) have been self-published in non-peer reviewed journals. As the data set of fossil spiders is refined as a result of new taxonomic and systematic studies and is updated to conform to current hypothesised relationships for extant spiders, using more modern techniques, such as CT scanning, it will become more useful to both palaeontologists and neontologists, including ecologists, biogeographers and other biologists. Unfortunately, there are very few people currently working on fossil spiders, so this may take some time.
About the author
David Penney has a PhD in fossil spiders preserved in amber and a DSc in amber palaeobiology. He has published more than 100 academic contributions to research in these areas. For a full author profile, see Deposits Issue 47, pp. 38–39. The author thanks David I Green for photographic assistance.
Dunlop, J.A., Penney, D., Daluge, N., Jager, P., McNeil, A., Bradley, R., Whithers, P.J. & Preziosi, R.F. 2011. Computed tomography recovers data from historical amber: an example from huntsman spiders. Naturwissenschaften, 98: 519–527.
Dunlop, J.A., Wirth, S., Penney, D., McNeil, A., Bradley, R.S., Withers, P.J. & Preziosi, R.F. 2012. A minute fossil phoretic mite recovered by X-ray computed tomography. Biology Letters, 8: 457–460.
Koch, C.L. & Berendt, G.C. 1854. Die im Bernstein befindlichen Crustaceen, Myriapoden, Arachniden und Apteren der Vorwelt. In Die im Bernstein befindlichen organischen Reste der Vorwelt. Vol. 1, part II (ed. G.C. Berendt). Nicholaischen Buchhandlung, Berlin. i–iv + 1–124 pp., 17 pls.
Ohl, M. 2011. Aboard a spider – a complex developmental strategy fossilized in amber. Naturwissenschaften, 98: 453–456.
Penney, D. 2016. Amber Palaeobiology: Research trends and perspectives for the 21st century. Siri Scientific Press, Manchester.
Penney, D. & Langan, A.M. 2006. Comparing amber fossils across deep time. Biology Letters, 2: 266–270.
Penney, D., Dunlop, J.A. & Marusik, Y.M. 2012. Summary statistics for fossil spider species taxonomy. ZooKeys, 192: 1–13.
Penney, D. & Preziosi, R.F. 2014. Estimating fossil ant species richness in Eocene Baltic amber. Acta Palaeontologica Polonica, 59: 927–929.
Penney, D. & Selden, P.A. 2011. Fossil Spiders: The evolutionary history of a mega-diverse order. Siri Scientific Press, Manchester.
Petrunkevitch, A.I. 1942. A study of amber spiders. Transactions of the Connecticut Academy of Arts and Sciences, 34: 119–464. Pls I–LXIX.
Petrunkevitch, A.I. 1958. Amber spiders in European collections. Transactions of the Connecticut Academy of Arts and Sciences, 41: 97–400.
Poinar, G.O. 2000. Heydenius araneus n. sp (Nematoda: Mermithidae), a parasite of a fossil spider, with an examination of helminths from extant spiders (Arachnida: Araneae). Invertebrate Biology, 119: 388–393.
Sadowski, E.-M., Schmidt, A.R., Seyfullah, L.J. & Kunzmann, L. 2017. Conifers of the ‘Baltic amber forest’ and their palaeoecological significance. Stapfia, 106: 1–73.
Weitschat, W. & Wichard, W. 2010. Baltic amber. Pp. 80–115 in: Penney, D. (ed.) Biodiversity of fossils in amber from the major world deposits. Siri Scientific Press, Manchester.
Wunderlich, J. 1982. Sex im Bernstein: ein fossiles Spinnenpaar. Neue Entomologische Nachrichten, 2: 9–11.
Wunderlich, J. (ed.) 2004. Fossil spiders in amber and copal. Beitrage Araneologie, 3: 1–1908.