C
ONRADC. L
ABANDEIRA1, J
ENNIFERA. D
UNNE2, R
ICHARDJ. W
ILLIAMS31Smithsonian Institution, National Museum of Natural History, Department of Paleobiology, P.O. Box 37012, Washington, DC 20013, USA, LABANDEC@si.edu; 2Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA; 3 Microsoft Research, Computational Ecology and Environmental Science Group, Cambridge, CB3 0FB, UK.
Although many paleoecological studies focus on species diversity and distribution, there are few opportunities to analyze species interactions in depth within the fossil record. We present highly and evenly resolved food-web data for the Messel Shale deposit.
Our dataset includes species that occurred in the immediately surrounding paratropical forest and those that occupied the water column and sub-stratum of a maar lake. Our data is notable for the detailed resolution of terrestrial plant insect associa-tions, representation of multiple habitats, the pres-ence of terrestrial and aquatic feeding chains, and the elevated certainty for most of the interaction data, particularly between plants and their insect and vertebrate consumers. Using various techniques of network structure analysis, including the recently developed probabilistic niche model (Williams et al., 2010), we assess the organization of this paleo food web with comparisons to published, extant ecological networks.
The lacustrine deposit at Messel, near Darmstadt, in central Germany, is of earliest middle Eocene age, equivalent to the early Lutetian stage, and corresponding to an absolute radioisotopic age of 47 Ma based on an 40Ar/39Ar date from a basalt frag-ment (Mertz and Renne, 2005). The included strata consist of 190 m of oil shale and other fine-grained sedimentary rocks (Felder and Harms, 2004), occur-ring in an area of 0.7 km2 (Schaal and Ziegler, 1992).
The time represented by this deposit is moderately time averaged, representing 1 to 1.5 million yr, esti-mated from sedimentation rates of 0.1 to 0.15 mm/yr, resulting in an average rate of 0.14 mm/yr (Lenz et al., 2010). These highly resolved, varved sed-imentary strata contain annual, lightly hued spring/summer laminae and darkly hued fall/winter laminae over 600 kyr, straddling almost half of the total time represented and indicating a direct
connec-ion i h g eenho e middle Eocene El Ni o So h-ern Oscillation climate dynamics (Lenz et al., 2010).
In addition to the resolved temporal, stratigraphic and paleoclimatic settings, Messel represents
older deposits. Third, the taxa documented at Messel represent a trophically balanced spectrum of pro-ducers, herbivores, carnivores and decomposers ranging from bacteria to crocodylians. Fourth, there is a breadth of host resource use in the terrestrial environment that is unparalleled in the fossil record, including, in the case of insects, fine-tuned associa-tions as varied as external foliage feeding, piercing-and-sucking, leaf mining, galling, seed predation, oviposition, and even predation and parasitoid interactions (e.g., Hughes et al., 2011). Fifth, preserved Messel fossils are overwhelmingly autochthonous, and signify deposition of a highly local biota in a geologically narrow time period, an unusual circumstance for the fossil record. Sixth, the number of trophically distinct taxa included in the dataset is greater than in published food webs for extant ecosystems (Dunne et al., 2004). Last, the interdisciplinary study of Messel, especially during the last 30 years by teams of specialist paleo-biologists, have provided one of the best-documented examples in a fossil assemblage of co-occurring taxa that were once living and feeding in a contiguous environment.
A limited sample of 25 trophic associations at Messel is presented in Figure 1. Evidence for determination of these associations include gut contents, vertebrate dentition and insect mouthpart structure, dispersed coprolites, plant insect interac-tions, feeding structures penetrating prey items (Labandeira, 2002), and other lines of inference such as isotopic geochemical relationships in the case of bacteria and other microorganisms. Documented associations include herbivory by vertebrates [Fig.
1(A): a,c; 1(B): a,c,d,h,i,k,l] and insects [Fig. 1(A): f l,n], vertebrate carnivory [Fig. 1(A): d,j] and insectivory [Fig. 1(A): m; 1(B): b,e g], and saprobic associations [Fig. 1(A): b,e]. Within insects, specific functional feeding groups include external foliage feeding [Fig.
1(A): k], leaf mining [Fig. 1(A): g,i,n], seed predation [Fig. 1(A): l], palynivory with or without pollination [Fig.
1(A): j,l], and oviposition [Fig. 1(A): f] an association that uses plant resources analogous to that of
and prokaryotes. Seventy-seven percent of the links are rated as middle or of high certainty. The web can be split into a terrestrial web of 633 taxa and 5551 links, and an aquatic web with 94 taxa and 517 links.
While levels of maximum generality are similar
between the two habitats, in particular with a species in each habitat that feeds on ca. 30 percent of the taxa, there nevertheless is much greater trophic specialization in the terrestrial web, as reflected in its low connectance (0.014), compared to the aquatic Figure 1. (A) Associations emphasizing plant insect associations and vertebrate dentition. (B) Associations emphasizing vertebrate gut contents and dentition.
B A
web (0.059). Probabilistic niche model (PNM) analy-sis (Williams et al., 2010) indicates that the niche model structure of the aquatic web is within the range observed for extant webs, while the PNM performs poorly for the terrestrial web, even when it is strongly aggregated by trophic similarity. Adding a second niche dimension increases fit of the PNM for both webs. The results are very robust to the removal of low certainty links. Reasons for the poor PNM fit of the terrestrial web are considered, and potentially include factors such as its size, high resolution of
specialized plant insect associations, differences between extinct and extant ecosystems, and methodology.
ACKNOWLEDGEMENTS
The authors thank Finnegan Marsh for formatting Figures 1 and 2. This is contribution 172 of the Evolution of Terrestrial Ecosystems consortium of the National Museum of Natural History, Washington, D.C.
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