Resource Tracking in Marine Parasites: Going with the ﬂ Ow?

Resource tracking in marine parasites: going with the ﬂ ow?

Ross M. Thompson , Robert Poulin , Kim N. Mouritsen and David W. Thieltges

R. M. Th ompson ([email protected]), Inst. for Applied Ecology, Univ. of Canberra, Bruce ACT 2601, Australia, Australian Centre for Biodiversity and School of Biological Sciences, Monash Univ., Clayton, VIC3800, Australia. – R. Poulin, Dept of Zoology, Univ. of Otago, PO Box 56, Dunedin, New Zealand. – K. N. Mouritsen, Dept of Bioscience, Marine Ecology, Ole Worms All é 1, DK-8000 Aarhus C, Denmark. – D. W. Th ieltges, NIOZ Royal Netherlands Inst. for Sea Research, PO Box 59, NL-1790 AB Den Burg Texel, the Netherlands.

Understanding how diversity interacts with energy supply is of broad ecological interest. Most studies to date have inves- tigated patterns within trophic levels, refl ecting a lack of food webs which include information on energy fl ow. We added parasites to a published marine energy-fl ow food web, to explore whether parasite diversity is correlated with energy fl ow to host taxa. Parasite diversity was high with 36 parasite taxa aff ecting 40 of the 51 animal taxa. Adding parasites increased the number of trophic links per species, trophic link strength, connectance, and food chain lengths. Th ere was evidence of an asymptotic relationship between energy fl owing through a food chain and parasite diversity, although there were clear outliers. High parasite diversity was associated with host taxa which were highly connected within the food web. Th is suggests that energy fl ow through a taxon may favour parasite diversity, up to a maximal value. Th e evolutionary and energetic basis for that limitation is of key interest in understanding the basis for parasite diversity in natural food webs and thus their role in food web dynamics.

Th e relationship between diversity and ecosystem functions should be directly related to productivity in adjacent trophic such as productivity has been, and remains, one of the levels. fundamental areas of research in ecology. Positive relation- Exploring the relationships between energy fl ows and ships between diversity and productivity were fi rst pro- diversity has traditionally been complicated by a lack of posed in the 1940s (Lindeman 1942), suggesting that suitable data sets which incorporate both diversity and higher basal productivity promoted higher predator diver- energy fl ows. Food web studies occupy the junction between sity. Th is was formalized into the ‘ productivity hypothesis ’ studies of diversity and ecosystem processes, in that they (Pimm 1982), which has been much explored across studies represent patterns of species diversity (the nodes) and move- ranging from bacteria in microcosms (Jenkins et al. 1992, ments of energy (connections between nodes) (Th ompson Kaunzinger and Morin 1998, Warren and Weatherby et al. 2012). Although describing such trophic networks has 2006) to large scale ecological manipulations of producti- a rich history (summarized by Pascual and Dunne 2004, vity (Nakano et al. 1999, Wallace et al. 1997), detailed Pimm 1982), it is only in the last decade that suffi cient rigor analyses of fi eld data (Monkkonen et al. 2006, Th ompson has been applied in terms of taxonomic resolution and sam- and Townsend 2005a), and meta-analyses (Field et al. pling eff ort that we can be confi dent that the resulting food 2009). webs refl ect biological reality rather than sampling artifacts. Donor-controlled dynamics would suggest that diversity Th ere is now a body of highly resolved food webs which have in the consumer trophic level is a function of the energy proven useful in testing fundamental ecological theory available from the resource trophic level. Lindeman’ s (1942) (Th ompson et al. 2007, 2012). Th ese food webs are greatly classic study belongs within this group, suggesting that improved in terms of the degree of taxonomic resolution increased productivity promotes increased diversity through (Th ompson and Townsend 2000), inclusion of spatial additional trophic levels (lengthening of food chains). Th ere and temporal variability (Martinez 1993, Th ompson and have been a number of studies which have found a positive Townsend 2005b), and sampling of formerly poorly correlation between basal productivity and consumer re presented groups (Schmid-Araya and Schmid 2000). Th e diversity (Th ompson and Townsend 2005a) although the inclusion of parasites into highly resolved food webs has pattern is not universal (Arim et al. 2007). A simpler been the most recent challenge in food web ecology (Laff erty donor-controlled mechanism would be that higher resource et al. 2008). Research has shown that including parasites in productivity provides additional energetic niche space, food webs can dramatically alter perceptions of food web allowing increased diversity within the consumer trophic topology (Huxham et al. 1996, Th ompson et al. 2005, level (Hashmi and Causey 2008). In this case diversity Amundsen et al. 2009). For example, inclusion of parasites

1187 has been shown to lengthen food chains, increase internal northern Europe (Baird et al. 2004). Th is is an earlier connectance and alter predator to prey ratios substantively version of the larger (but not fl ow-weighted) food web (Huxham et al. 1996). Th ere remains however, the challenge recently compiled by Th ieltges et al. (2011). Th e fl ow food of integrating parasites into food webs which refl ect web used here has been described over time using detailed dynamics (weighted fl ows of energy) rather than simply studies of all of the food web compartments. Briefl y, it is topology (binary indications of energy fl ow). Addressing based on autotrophic production by phytoplankton, macro- questions of the relationship between diversity and ecosys- phytes and microphytobenthos, with benthic sub-webs of tem function in real food webs requires food webs which are invertebrates channeling energy to fi sh and seabirds (see not only highly resolved and inclusive, but also include Baird et al. 2004 for details). Th e food web is unique in weighted measures of trophic links between all components that it is highly taxonomically resolved (particularly for birds of the food web. and fi sh), and includes weighted fl ows of energy based on Th e availability of food webs with weighted measures of productivity and biomass measurements. To this published energy fl ow which also include parasites provides us with food web we added a parasite-host sub-web. Information an opportunity to explore productivity/diversity relation- on parasites and their life cycles was compiled from the lit- ships in very closely coupled trophic levels. Food chains erature, following a thorough search of studies published on which supply larger amounts of energy might be expected parasites in the Wadden Sea fauna, and in that of adjacent to be ‘ targeted ’ by parasites through evolutionary time, seas (Supplementary material Appendix 1). In addition, leading to a higher diversity of parasite species in taxa we used unpublished data and local expert knowledge to which are in high energy food chains. Higher energy sup- complement life cycle information. Th e parasites and their plies of certain food chains might simply support higher transmission paths were then mapped onto the web. numbers of parasites. Th is will be valid for all types of To facilitate analysis, all non-feeding compartments were parasites. However, in trophically transmitted parasites removed. Bacteria were considered basal (curtailing energy (those transmitted by ingestion) higher energy fl ows looping through the microbial loop/detritus/decomposition might also increase chances for parasites to be transmitted. pathway). All taxa in the food web were classifi ed as basal Parasites may either target these high fl ow nodes or simply (non-consuming), intermediate (both consume other taxa accumulate there at higher rates. Productivity may also and are consumed) or top (not consumed). Flow based through evolutionary time favour speciation; it has been trophic position (TP) was calculated for all non-parasitic proposed that rates of parasite evolution may be higher taxa from the weighted matrix of energy fl ows (Williams when systems are more productive (Lopez-Pascua and and Martinez 2004). Th is attributes all basal components Buckling 2008). It is not only the total amount of energy a trophic position of 0. Trophic positions of consumers are fl owing into a node that can determine how many parasite calculated as the weighted average of all of the trophic species will exploit that node, however. For trophically- positions of all items consumed. Integer values for TP transmitted parasites, the number of paths of energy indicate species feeding at a defi ned trophic level (1 (i.e. links) fl owing into a node may be more important. herbivore, 2 primary predator, 3 secondary predator, Th ese parasites can be highly specifi c to particular inter- etc.) (Th ompson et al. 2007). mediate host species, and only defi nitive hosts at higher A range of standard food web attributes was calculated trophic levels with broad diets (many links) are likely to from the food web, fi rst without the parasites included, acquire diverse parasite communities (Poulin and Morand then with the parasite community included. Attributes cal- 2000, Poulin and Rohde 1997). Th us, the position of culated were; total number of taxa (S), total number of a node within the network can matter as much, if not trophic links (L), links per species (L/S) summed link more, than the amount of energy it receives. Using a modi- strength, average link strength, simple connectance (Cs), fi ed version of a very highly resolved food web from the parasite adjusted connectance (Cp), average food chain Sylt – R ø m ø Bight, in the Wadden Sea we sought to explore length and maximum food chain length. We excluded three fundamental questions: predator – parasite links as suggested by Laff erty et al. (2006). Summed link strength (the sum of all the link weights in 1. Are parasite transmission routes preferentially associated the matrix) and average link strength (summed link with food chains that have the highest fl ows of energy? strength divided by the number of taxa in the web) were 2. Does parasite diversity peak in hosts with the highest calculated from the raw data matrices. Connectance was energy fl ow? calculated in two ways. Simple connectance (C s) (Hall and 3. Does parasite diversity correlate with how highly con- Raff aelli 1991) is the number of links that do occur in nected hosts are in food webs? a matrix (L ) divided by the total number of links if all links were possible (calculated as the square of the We predict that parasite diversity will be highest in hosts that 2 receive the most energy in a food web, i.e. those that are number of nodes, S ), and is calculated as L/ (S ) . Realised embedded in food chains with high energy fl ow and are at connectance (Th ompson and Townsend 2005b) is the positions in the food web with high fl ow through of energy. proportion of food web links which actually occur divided by the number that could conceivably occur. Th is excludes from the denominator of the connectance formula links Methods from basal taxa to basal taxa and parasites to basal taxa. Formally, realised connectance (CR ) is calculated as Th e food web used for the analysis is a highly resolved L /[(S S ) (b S ) (p b)], where b is the number of food web from the Sylt – R ø m ø Bight in the Wadden Sea, basal species and p is the number of parasite species. Th ese

1188 modifi cations make changes in connectance biologically rel- To visualize the food web, the matrix was plotted evant, as opposed to being simply an artefact of the number using Netdraw within UCINET 6 (Borgatti et al. 2002). of non-feeding or parasitic species (Laff erty et al. 2006). Th e network graph was then modifi ed by hand to generate a Average and maximum food chain lengths were calcu- food web arranged by trophic position (as calculated above), lated using network analysis tools. UCINET 6.0 (Borgatti and superimposed with the parasite diversity of each node. et al. 2002) was used to handle the data matrices and make them available to Pajek 0.96 (Batagelj and Mrvar 1998) for calculation of chain lengths. Results To ascertain factors relating to parasite diversity at each node, the number of parasites infecting each node was Th e parasite-inclusive version of the Sylt – R ø m ø Bight calculated from the data matrix. Attributes refl ecting food web included 94 taxa (Fig. 1, Table 1). Taxonomic reso- energy fl ows to each parasitised node were then calculated. lution was high, with 77% of nodes identifi ed to species Energy fl ow to each node was calculated in two ways. Firstly, level. Five nodes were classifi ed as basal, with primary the weighted links from the node’ s immediate resources production being derived from both planktonic and benthic were summed (‘ inlink weight’ ). Secondly, the total of all sources. Of the animal taxa present in the food web 22 weighted links in all trophic interactions in the food chain were clearly primary consumers, 24 could be classifi ed as leading to each node was calculated (‘ total chain weight’ ). predators and 5 as omnivores (Fig. 1). Th ere were 15 top Network position of each host was then described using predators if parasites were excluded from the food web. measures of centrality calculated in Pajek 0.96 (Batagelj Th irty-six parasitic taxa were included in the food web, pri- and Mrvar 1998), following the approach of Chen et al. marily trematodes (Table 1). Of the 51 free-living animal (2008). Closeness centrality indicates the position of a node taxa in the food web, only 11 were not recorded as being in a network relative to prey species, and is considered to parasitised, and only one predatory species was not para- refl ect a wider diet range and a better capacity to accumu- sitised. Parasite diversity ranged from 1 to 23 taxa, with an late resources from species at lower trophic levels (Chen average diversity of 9.7 taxa per host (SD 7.6). et al. 2008). A low value of closeness centrality indicates a Inclusion of the parasite sub-web in the food web altered node which is strongly linked to other nodes. Betweenness food web attributes considerably (Table 2). Number of centrality indicates the position in the network relative to trophic links, links per species, summed trophic link consumers, and is considered to refl ect vulnerability to strength and average link strength per species were all predators (Chen et al. 2008). A node with high betweenness higher in the parasite-inclusive food web. Connectance was centrality is important in that it mediates many indirect greater in the food web after the inclusion of parasites; interactions between pairs of nodes. Both centrality mea- adjusting connectance to take into account the limited sures were calculated for the food web with the parasite sub- number of possible links to parasites (parasitised con- web excluded. Inlink weight, total chain weight, closeness nectance) made the detected increase larger. Average and centrality and betweenness centrality for each node were maximum food chain lengths were slightly increased by plotted against the parasite diversity for that node. including the parasite sub-web (Table 2). As these attributes

TL3 35 3 36 37 4 4 42 18 46 51 18 48 49 16 45 19 19 41 38 40 33 18 14 50 15 4 47 23 23 39 29 30 31 23 1 43 44 34 20 32 5 25 5 20 21 4 4 TL2 28 1 14 22 2 27 4 18 4

20 17 54 52 26 13 15 19 21 5 23 24 6 7 8 9 10 11 12 16 56 53 2 2 2 4 8 13 5 8 14 6 1 4 5 TL1

3 4 1 55 2 TL0

Figure 1. Sylt – R ø m ø Bight food web, showing weighted links (thickness of connecting lines) between nodes (■ ). Numbers which are not circled indicate the taxa represented by each node (see Table 1 for codes). Taxa are arranged by trophic position (see methods for details), with trophic levels indicated by dotted lines (TL0 basal components, TL1 herbivore, TL2 primary predator, TL3 secondary predator). Numbers in circles indicate the diversity of parasites infecting each node, with the size of circles increasing with diversity.

1189 Table 1. Taxa present in the Sylt – R ø m ø Bight food web. Numbers Table 1. (Continued). indicate location on the food web graph shown in Fig. 1. 62 Microphallus pirum Basal 63 Microphallus oocysta 1 Phytoplankton 64 Maritrema subdolum 2 Microphytobenthos 65 Maritrema species 15 3 Macrophytes 66 Levinseniella brachysoma 4 Free-living bacteria 67 Himasthla elongata Zooplankton 68 Himasthla continua 5 Zooplankton 69 Himasthla interrupta Macrobenthos 70 Cryptocotyle concavum 6Hydrobia ulvae 71 Cryptocotyle jejuna 7Littorina littorea 72 Cryptocotyle lingua 8Arenicola marina 73 Cercaria ephemera 9Scoloplos armiger 74 Cercaria lebouri 10 Capitellidae 75 Psilostomum brevicolle 11 Oligochaeta 76 Psilochasmus aglyptorchis 12 Heteromastus fi liformis 77 Deropristis infl ata 13 Lanice conchilega 78 Renicola roscovita 14 Nereis diversicolor 79 Parvatrema minutus 15 Pygospio elegans 80 Gymnophallus gibberosus 16 Corophium arenarium 81 Gymnophallus choledochus 17 Corophium volutator 82 Gymnophalloides macomae 18 Gammarus spp. 83 Parvatrema affi nis 19 Mytilus edulis 84 Monorchis parvus 20 Cerastoderma edule 85 Bucephalus minimus 21 Mya arenaria 86 Podocotyle atomon 22 Small polychaetes Turbellaria 23 Tharyx killariensis 87 Paravortex cardii 24 Macoma balthica Nematodes 25 Phyllodocidae 88 Nematoda sp. 26 Small crustaceans Crustacean parasites 27 Carcinus maenas 89 Mytilicola intestinalis 28 Crangon crangon 90 Copepoda species 1 29 Nephthys spp. 91 Copepoda species 2 Fishes 92 Sacculina carcini 30 Pomatoschistus microps Acanthocephala 31 Pomatoschistus minutus 93 Profi licollis botulus 32 Pleuronectes platessa Cestodes 33 Pleuronectes fl esus 94 Cestoda species 2 34 Clupea harengus 35 Merlangius merlangus 36 Gadus morrhua do not simply scale with food-web size (Dunne et al. 37 Myoxocephalus scorpio 2002) these changes are not likely to be a result Birds of simply increasing the size of the food web, although that 38 Tadorna tadorna possibility cannot be discounted. 39 Somateria mollissima Th ere was evidence of an asymptotic relationship 40 Haematopus ostralegus between parasite diversity and total food chain link 41 Recurvirostra avosetta 42 Pluvialis apricaria strength (total amount of energy fl owing through a food 43 Calidris canutus chain (Fig. 2A). Th ere was no evidence of higher parasite 44 Calidris alpine diversity associated with inlink strength (amount of energy 45 Limosa lapponica fl owing in to the host) (Fig. 2B). However there were six 46 Numenius arquata 47 Larus ridibundus Table 2. Food web attributes for the Sylt – R ø m ø Bight food web with 48 Larus canus and without the inclusion of the parasite sub web. For defi nitions, 49 Larus argentatus see methods. 50 Other birds 51 Anas platyrhynchos Parasites Parasites 52 Anas acuta excluded included 53 Anas penelope Total number of taxa (S) 56 92 54 Branta bernicla Number of links (L) 190 570 Benthic microfauna Number of links per species (L/S) 3.39 6.20 55 Sediment bacteria Summed link strength 743.45 1746.25 56 Meiobenthos Average link strength 13.28 18.98

Trematodes Simple connectance (Cs ) 0.061 0.067 60 Microphallus claviformis Parasite adjusted connectance (Cp ) 0.067 0.087 61 Microphallus pygmaeus Average food chain length 1.612 1.737 Maximum food chain length 3 4 (Continued)

1190 Figure 2. Relationships between parasite diversity (expressed as number of parasites linking to a food web node) and: (A) summed food chain weight, the total amount of energy fl owing through a food chain; (B) inlink weight, the amount of energy fl owing into the food web node; (C) closeness centrality, refl ecting distance from other nodes in the network; and (D) betweenness centrality, refl ecting importance in mediating indirect interactions between pairs of nodes. Trematode parasites are shown as white squares, with all other parasite types shown as black diamonds. clear outliers which were involved in chains with large Discussion amounts of energy fl owing through them, but had relatively low parasite diversity. Th ese species were the brown shrimp Parasites are ubiquitous in natural systems, but it is only Crangon crangon and fi ve species of fi sh; European plaice recently that they have been eff ectively incorporated into and fl ounder, Pleuronectes platessa and P. fl esus, whiting detailed analyses of food webs (Laff erty et al. 2008). Here Merlangius merlangus , cod Gadus morrhua and sculpin we have integrated the parasite sub-web with an existing Myoxocephalus scorpio . published food web from the Sylt – R ø m ø Bight. Consistent Th ere was a general pattern that the highest parasite with previous parasite-inclusive food webs (Huxham et al. diversity nodes were associated with low values of closeness 1996, Laff erty et al. 2006, Th ompson et al. 2005) we centrality; no node with parasite diversity of 15 had a found parasites had a major eff ect on the topology of the closeness value of 50 (Fig. 2C). Th is shows that hosts food web. In the Sylt– R ø m ø Bight food web numbers of which had the highest parasite diversity were generally trophic links were greatly increased, food chains lengthened highly connected to other nodes in the food web. Th ere and connectivity increased. was no evidence of strong relationship between parasite Of particular interest in this analysis was the relationship diversity and betweenness centrality, although there was between parasite diversity at a node and the amount of some evidence that high parasite diversity primarily occurred energy passing through that node. If productivity does in nodes with low–intermediate values of betweenness indeed generate or maintain diversity, then it might be (Fig. 2D) suggesting the vulnerability to predators was not expected that species that have large volumes of energy strongly associated with diversity of parasites. passing through them would also have the highest parasite Th ere was no evidence of diff ering relationships when dif- diversity. Patterns might be expected to be particularly ferent types of parasites were considered separately. Trema- strong for parasites, if the underlying causes of such rela- todes numerically dominated the data and were the main tionships are metabolic in origin (Hawkins et al. 2007), drivers of all patterns (Fig. 2). Nor were there any changes to as the host is a relatively closed habitat isolated from the patterns when we considered particular parasite lifestyles other factors such as disturbance. While there was some or single trophic levels within the food web. It appears that hint of a saturating relationship between summed food the patterns seen here are general to the food web. chain weight (representing the total energy fl owing in a

1191 food chain) and parasite diversity, there were notable out- Similarly, our estimates of parasitisation are based on a liers. A number of taxa were members of chains with literature review and may not be suffi cient to include all of large fl ows of energy, but had relatively low parasite diver- the parasites in the food web. Parasite richness increases sity. Th is might partly be explained by underestimated with the number of hosts that have been inspected for parasite diversity resulting from sampling artifacts. While parasites. Parasite links based on literature review alone, trematodes are the best studied group in intertidal systems and not systematic sampling, may bias results as some taxa due to their relatively easy identifi cation in intermediate will have been studied more intensively than others. In hosts (Mouritsen and Poulin 2002), the presence and life addition, well-studied hosts (or hosts that support a cycles of other parasites likes cestodes and nematodes high degree of energy fl ow) may be more likely to have are less known, particularly for fi sh. In addition, fi shes are received more attention to their diet and predators, making generally not well integrated in intertidal parasite – hosts sys- them seem more connected in a food web compared to tems where birds prevail as defi nitive hosts for trematodes more obscure species. In this system we were able to (Mouritsen and Poulin 2002). However, it might also be complement information from the literature with informa- that for some species like whiting, cod and sculpin, the tion on parasite richness in the intermediate hosts (e.g. relatively low parasite diversity in chains with large fl ows molluscs, crustaceans, polychaetes, some fi sh species) from of energy refl ects the fact that they occur high in food actual surveys that have systematically screened hosts chains that have large amounts of energy fl owing through for parasites. As most parasites have complex life cycles the lower portions of the chain. Th is energy may not which involve just these taxa as intermediate hosts, we have be eff ectively reaching the fi sh predators at the top of the a good understanding of what parasites are present in a chain due to ineffi ciencies of energy transfers. Nevertheless, system. As a result the food web is likely to be quite robust there is some support for further investigation of the role to sampling bias, but may overestimate the actual parasite of donor controlled processes in driving parasite diversity. richness in some host species, without any systematic bias. Our approach to investigating the relationship between We are unlikely to have sampled all of the parasites, but productivity and parasite diversity has some signifi cant we will have sampled the majority, given the large number limitations. Productivity has been proposed to increase rates of detailed studies which have taken place in this region. of parasite evolution (Lopez-Pascua and Buckling 2008). We did not consider it wise to bring in literature from Th e lack of association between parasite diversity and the outside of the study area, as one of the strengths of this amount of energy fl owing through a food chain or into a study is that it is clearly spatially delimited. As the parasites host node may refl ect other evolutionary constraints. Some in this system mainly cycle in the intertidal, the part of associations between hosts and parasites have ancient phylo- the food web is probably quite robust but potential para- genetic histories, and parasites show strong coevolutionary sites moving in via large mobile consumers (fi sh and birds) ties with particular host taxa, whether or not the latter may not all be included. Th is is a potential for all food web happen to be part of strong energy fl ows in a web (Brooks studies, which must necessarily be spatially delimited in 1988, Poulin 2007a). Compatibility between a parasite some way. and potential host species depends on behavioural, morpho- Th e food web is the long-term product of systematic logical, and immunological factors (Adamson and Caira sampling of all free-living taxa in the system coupled with 1994, Poulin 2007b). Th us although natural selection would estimates of energy fl ow among them. In parallel, the few favor parasites that follow the strongest energy fl ows in a fi sh species in this system, as well as many birds and all food web, constraints acting on host specifi city may pose large species of molluscs and crustaceans, have all been insurmountable obstacles. Th is may in part explain the individually targeted by parasitological studies in the past observed outliers discussed above (members of chains with (Supplementary material Appendix 1), making the Wadden large fl ows of energy, but relatively low parasite diversity). Sea one of the best-studied marine ecosystems in the Birds prevail as defi nitive hosts in intertidal systems (Mou- world. Although the exact number of individuals examined ritsen and Poulin 2002) and fi sh may harbour lower parasite for parasites cannot be retrieved from most of the sources diversity than expected based on energy fl ows because of used in order to test for a relationship between parasite host specifi city constraints. richness and host sampling eff ort, the lack of published Another limitation is that estimates of energy fl ow to reports of new host-parasite associations in the Wadden particular nodes are fraught with diffi culty, and can be Sea over the past several years suggests that present know- highly variable between individuals and through time. If ledge of parasitism in this system is as exhaustive as it can variability in energy fl ow is large at an individual to indivi- get (without molecular prospecting for cryptic species). dual level, this may act against a parasite ’ s ability to evolve Our second approach to relating parasite diversity to to track resources through time. Similarly, temporal variabil- energy fl ows through the Sylt – R ø m ø Bight food web ity in patterns of energy fl ow may create resource limitation involved using a network analytic approach. Chen et al. which prevents high levels of diversity persisting in a con- (2008), by studying relationships between parasite diversity sumer. Perhaps parasite diversity depends more on low and network position of hosts, found that host species variance than on high amounts of energy passing through with high parasite diversity tended to have low values of a node. Many of these constraints could be addressed by closeness centrality. Low values for closeness centrality are studying similar food webs along productivity gradients. associated with a wide diet range and an ability to readily It would then be expected that at a whole food web accumulate resources from species at lower trophic levels level parasite diversity would be higher in more productive (Chen et al. 2008). Th is supports the concept that donor environments. control may infl uence parasite diversity. Our results for the

1192 Sylt – R ø m ø Bight food web are consistent with Chen et al. ’ s the National Center for Ecological Analysis and Synthesis (2008) results, with the highest parasite diversity nodes (NCEAS), a center funded by NSF (grant no. DEB-0553768), the tending to be close to other nodes in the food web. Chen Univ. of California, Santa Barbara, and the State of California. et al. (2008) also found a weak positive relationship between parasite diversity and betweenness centrality. High values for betweenness centrality indicate involvement in a large num- References ber of food chains and a high vulnerability to predators (Chen et al. 2008). In our food web there was no evidence Adamson, M. L. and Caira, J. N. 1994. Evolutionary factors infl uencing the nature of parasite specifi city. – Parasitology of a positive relationship between diversity and betweenness; 109: S85 – S95. rather there was a general absence of parasites in the taxa Amundsen, P. A. et al. 2009. 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Productivity controls and which receive higher amounts of energy fl ow. However food-chain properties in microbial communities. – Nature there are clearly other factors which act to limit total parasite 395: 495 – 497. diversity (i.e. the relationship is asymptotic) and allow Laff erty, K. D. et al. 2006. Parasites dominate food web links. some taxa to have low parasite diversity despite high amounts – Proc. Natl Acad. Sci. USA 103: 11211 – 11216. of energy fl ow. As with relationships between energy supply Laff erty, K. D. et al. 2008. Parasites in food webs: the ultimate and diversity in non-parasite food webs, factors such as missing links. – Ecol. Lett. 11: 533 – 546. Lindeman, R. L. 1942. Th e trophic-dynamic aspect of ecology. ecosystem size (in this case competition for space within – Ecology 23: 399 – 418. hosts) and disturbance (a variety of factors including host Lopez-Pascua, L. D. C. and Buckling, A. 2008. Increasing pro- defenses against parasites and predation on hosts) may have ductivity accelerates host – parasite coevolution. – J. Evol. Biol. important interactions with energy supply in driving pat- 21: 853 – 860. terns of diversity. Martinez, N. D. 1993. Eff ects of resolution on food web structure. – Oikos 66: 403 – 412. Monkkonen, M. et al. 2006. Energy availability, abundance, Acknowledgements – Th anks to Martin Hemberg for use of his energy-use and species richness in forest bird communities: code for calculating trophic position. DWT acknowledges support a test of the species-energy theory. – Global Ecol. Biogeogr. from a personal grant (Th 1361/1-1) from the German Research 15: 290 – 302. Foundation (DFG). RT was funded in part by an ARC Future Mouritsen, K. N. and Poulin, R. 2002. Parasitism, community Fellowship (ARC-FT110100957). Th is work was conducted as structure and biodiversity in intertidal ecosystems. – Parasitology part of the Parasites and Food Webs Working Group supported by 124: S101 – S117.

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Supplementary material (available online as Appendix oik- 00245 at www.oikosoﬃ ce.lu.se/appendix ). Appendix 1.

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