Publications by authors named "Mark E Torchin"

40 Publications

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution.

PLoS Biol 2021 Aug 19;19(8):e3001322. Epub 2021 Aug 19.

UC Davis Genome Center, University of California, Davis, Davis, California, United States of America.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.
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http://dx.doi.org/10.1371/journal.pbio.3001322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8376202PMC
August 2021

Invasion history shapes host transcriptomic response to a body-snatching parasite.

Mol Ecol 2021 09 20;30(17):4321-4337. Epub 2021 Jul 20.

Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.

By shuffling biogeographical distributions, biological invasions can both disrupt long-standing associations between hosts and parasites and establish new ones. This creates natural experiments with which to study the ecology and evolution of host-parasite interactions. In estuaries of the Gulf of Mexico, the white-fingered mud crab (Rhithropanopeus harrisii) is infected by a native parasitic barnacle, Loxothylacus panopaei (Rhizocephala), which manipulates host physiology and behaviour. In the 1960s, L. panopaei was introduced to the Chesapeake Bay and has since expanded along the southeastern Atlantic coast, while host populations in the northeast have so far been spared. We use this system to test the host's transcriptomic response to parasitic infection and investigate how this response varies with the parasite's invasion history, comparing populations representing (i) long-term sympatry between host and parasite, (ii) new associations where the parasite has invaded during the last 60 years and (iii) naïve hosts without prior exposure. A comparison of parasitized and control crabs revealed a core response, with widespread downregulation of transcripts involved in immunity and moulting. The transcriptional response differed between hosts from the parasite's native range and where it is absent, consistent with previous observations of increased susceptibility in populations lacking exposure to the parasite. Crabs from the parasite's introduced range, where prevalence is highest, displayed the most dissimilar response, possibly reflecting immune priming. These results provide molecular evidence for parasitic manipulation of host phenotype and the role of gene regulation in mediating host-parasite interactions.
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http://dx.doi.org/10.1111/mec.16038DOI Listing
September 2021

Invasion of the body snatchers: the role of parasite introduction in host distribution and response to salinity in invaded estuaries.

Proc Biol Sci 2021 06 23;288(1953):20210703. Epub 2021 Jun 23.

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

In dynamic systems, organisms are faced with variable selective forces that may impose trade-offs. In estuaries, salinity is a strong driver of organismal diversity, while parasites shape species distributions and demography. We tested for trade-offs between low-salinity stress and parasitism in an invasive castrating parasite and its mud crab host along salinity gradients of two North Carolina rivers. We performed field surveys every six to eight weeks over 3 years to determine factors influencing parasite prevalence, host abundance, and associated taxa diversity. We also looked for signatures of low-salinity stress in the host by examining its response (time-to-right and gene expression) to salinity. We found salinity and temperature significantly affected parasite prevalence, with low-salinity sites (less than 10 practical salinity units (PSU)) lacking infection, and populations in moderate salinities at warmer temperatures reaching prevalence as high as 60%. Host abundance was negatively associated with parasite prevalence. Host gene expression was plastic to acclimation salinity, but several osmoregulatory and immune-related genes demonstrated source-dependent salinity response. We identified a genetic marker that was strongly associated with salinity against a backdrop of no neutral genetic structure, suggesting possible selection on standing variation. Our study illuminates how selective trade-offs in naturally dynamic systems may shape host evolutionary ecology.
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http://dx.doi.org/10.1098/rspb.2021.0703DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8220271PMC
June 2021

Asymmetry of marine invasions across tropical oceans.

Ecology 2021 08 14;102(8):e03434. Epub 2021 Jul 14.

Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, Maryland, 21037, USA.

Understanding the mechanisms of spatial variation of biological invasions, across local-to-global scales, has been a major challenge. The importance of evolutionary history for invasion dynamics was noted by Darwin, and several studies have since considered how biodiversity of source and recipient regions can influence the probability of invasions. For over a century, the Panama Canal has connected water bodies and biotas with different evolutionary histories, and created a global shipping hot spot, providing unique opportunities to test mechanisms that affect invasion patterns. Here, we test for asymmetry in both the extent of invasions and predation effects, a possible mechanism of biotic resistance, between two tropical oceans at similar latitudes. We estimated nonnative species (NNS) richness for sessile marine invertebrates, using standardized field surveys and literature synthesis, to examine whether invasions are asymmetrical, with more NNS present in the less diverse Pacific compared to the Atlantic. We also experimentally tested whether predation differentially limits the abundance and distribution of these invertebrates between oceans. In standardized surveys, observed total NNS richness was higher in the Pacific (18 NNS, 30% of all Pacific species) than the Atlantic (11 NNS, 13% of all Atlantic species). Similarly, literature-based records also display this asymmetry between coasts. When considering only the reciprocal exchange of NNS between Atlantic and Pacific biotas, NNS exchange from Atlantic to Pacific was eightfold higher than the opposite direction, exceeding the asymmetry predicted by random exchange based simply on differences of overall diversity per region. Predation substantially reduced biomass and changed NNS composition in the Pacific, but no such effects were detected on the Atlantic coast. Specifically, some dominant NNS were particularly susceptible to predation in the Pacific, supporting the hypothesis that predation may reduce the abundance of certain NNS here. These results are consistent with predictions that high diversity in source regions, and species interactions in recipient regions, shape marine invasion patterns. Our comparisons and experiments across two tropical ocean basins, suggest that global invasion dynamics are likely driven by both ecological and evolutionary factors that shape susceptibility to and directionality of invasions across biogeographic scales.
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http://dx.doi.org/10.1002/ecy.3434DOI Listing
August 2021

Stronger predation intensity and impact on prey communities in the tropics.

Ecology 2021 08 13;102(8):e03428. Epub 2021 Jul 13.

Smithsonian Environmental Research Center, Edgewater, Maryland, 21037-0028, USA.

The hypothesis that biotic interactions strengthen toward lower latitudes provides a framework for linking community-scale processes with the macroecological scales that define our biosphere. Despite the importance of this hypothesis for understanding community assembly and ecosystem functioning, the extent to which interaction strength varies across latitude and the effects of this variation on natural communities remain unresolved. Predation in particular is central to ecological and evolutionary dynamics across the globe, yet very few studies explore both community-scale causes and outcomes of predation across latitude. Here we expand beyond prior studies to examine two important components of predation strength: intensity of predation (including multiple dimensions of the predator guild) and impact on prey community biomass and structure, providing one of the most comprehensive examinations of predator-prey interactions across latitude. Using standardized experiments, we tested the hypothesis that predation intensity and impact on prey communities were stronger at lower latitudes. We further assessed prey recruitment to evaluate the potential for this process to mediate predation effects. We used sessile marine invertebrate communities and their fish predators in nearshore environments as a model system, with experiments conducted at 12 sites in four regions spanning the tropics to the subarctic. Our results show clear support for an increase in both predation intensity and impact at lower relative to higher latitudes. The predator guild was more diverse at low latitudes, with higher predation rates, longer interaction durations, and larger predator body sizes, suggesting stronger predation intensity in the tropics. Predation also reduced prey biomass and altered prey composition at low latitudes, with no effects at high latitudes. Although recruitment rates were up to three orders of magnitude higher in the tropics than the subarctic, prey replacement through this process was insufficient to dampen completely the strong impacts of predators in the tropics. Our study provides a novel perspective on the biotic interaction hypothesis, suggesting that multiple components of the predator community likely contribute to predation intensity at low latitudes, with important consequences for the structure of prey communities.
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http://dx.doi.org/10.1002/ecy.3428DOI Listing
August 2021

Seasonal upwelling reduces herbivore control of tropical rocky intertidal algal communities.

Ecology 2021 06 18;102(6):e03335. Epub 2021 Apr 18.

Smithsonian Tropical Research Institute, Panama City, Republic of Panama.

Communities are shaped by a variety of ecological and environmental processes, each acting at different spatial scales. Seminal research on rocky shores highlighted the effects of consumers as local determinants of primary productivity and community assembly. However, it is now clear that the species interactions shaping communities at local scales are themselves regulated by large-scale oceanographic processes that generate regional variation in resource availability. Upwelling events deliver nutrient-rich water to coastal ecosystems, influencing primary productivity and algae-herbivore interactions. Despite the potential for upwelling to alter top-down control by herbivores, we know relatively little about the coupling between oceanographic processes and herbivory on tropical rocky shores, where herbivore effects on producers are considered to be strong and nutrient levels are considered to be limiting. By replicating seasonal molluscan herbivore exclusion experiments across three regions exposed to varying intensity of seasonal upwelling, separated by hundreds of kilometers along Panama's Pacific coast, we examine large-scale environmental determinants of consumer effects and community structure on tropical rocky shores. At sites experiencing seasonal upwelling, grazers strongly limited macroalgal cover when upwelling was absent, leading to dominance by crustose algae. As nutrients increased and surface water cooled during upwelling events, increases in primary productivity temporarily weakened herbivory, allowing foliose, turf and filamentous algae to replace crusts. Meanwhile, grazer effects were persistently strong at sites without seasonal upwelling. Our results confirm that herbivores are key determinants of tropical algal cover, and that the mollusk grazing guild can control initial stages of macroalgal succession. However, our focus on regional oceanographic conditions revealed that bottom-up processes regulate top-down control on tropical shorelines. This study expands on the extensive body of work highlighting the influence of upwelling on local ecological processes by demonstrating that nutrient subsidies delivered by upwelling events can weaken herbivory in tropical rocky shores.
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http://dx.doi.org/10.1002/ecy.3335DOI Listing
June 2021

Variable host responses mediate host preference in marine flatworm-snail symbioses.

PLoS One 2021 2;16(3):e0247551. Epub 2021 Mar 2.

Smithsonian Tropical Research Institute, Balboa, Ancon, Republic of Panama.

Host preference of symbionts evolves from fitness trade-offs. However, it is often unclear how interspecific variations in host response traits influence this evolutionary process. Using the association between the polyclad flatworm Paraprostatum echinolittorinae and its intertidal snail hosts on the Pacific Coast of Panama, we assessed how a symbiont's host preference is associated with varying host defenses and post-infestation performances. We first characterized the prevalence and intensity of worm infestation in five snail hosts (Tegula pellisserpentis, Nerita scabricosta, N. funiculata, Planaxis planicostatus, and Cerithium stercusmuscarum). We then used manipulative experiments to test flatworm's host choice, hosts' behavioral rejection of flatworms, and hosts' growth and survival following the infestation. In the field, flatworms were orders of magnitude more prevalent and dense in T. pellisserpentis, N. scabricosta, N. funiculata than P. planicostatus and C. stercusmuscarum, although the three former hosts were not necessarily more abundant. The results from our laboratory host selection trials mirrored these patterns; flatworms were 3 to 14 times more likely to choose T. pellisserpentis, N. scabricosta, N. funiculata over P. planicostatus and C. stercusmuscarum. The less preferred hosts frequently rejected flatworms via mantle contractions and foot withdrawals, which reduced the infestation rate by 39%-67%. These behaviors were less frequent or absent in the preferred hosts. Flatworm infestation variably influenced host performances in the field, negligibly affecting the growth and survival of T. pellisserpentis and N. funiculata but reducing the growth of P. planicostatus. Flatworms thus preferred less defended hosts that can also support higher worm densities without being harmed. Stable isotope analysis further revealed that flatworms are unlikely to feed on snail tissues and may live as a commensal in their preferred hosts. Our study demonstrates that host response traits can modulate a symbiont's host choice and calls for more explicit considerations of host response variability in host preference research.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0247551PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924752PMC
September 2021

A new wave of marine fish invasions through the Panama and Suez canals.

Nat Ecol Evol 2020 11;4(11):1444-1446

Smithsonian Tropical Research Institute - STRI, Balboa, Republic of Panama.

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http://dx.doi.org/10.1038/s41559-020-01301-2DOI Listing
November 2020

Fluid preservation causes minimal reduction of parasite detectability in fish specimens: A new approach for reconstructing parasite communities of the past?

Ecol Evol 2020 Jul 15;10(13):6449-6460. Epub 2020 Jun 15.

School of Aquatic and Fishery Sciences University of Washington Seattle WA USA.

Long-term datasets are needed to evaluate temporal patterns in wildlife disease burdens, but historical data on parasite abundance are extremely rare. For more than a century, natural history collections have been accumulating fluid-preserved specimens, which should contain the parasites infecting the host at the time of its preservation. However, before this unique data source can be exploited, we must identify the artifacts that are introduced by the preservation process. Here, we experimentally address whether the preservation process alters the degree to which metazoan parasites are detectable in fluid-preserved fish specimens when using visual parasite detection techniques. We randomly assigned fish of three species () to two treatments. In the first treatment, fish were preserved according to the standard procedures used in ichthyological collections. Immediately after the fluid-preservation process was complete, we performed parasitological dissection on those specimens. The second treatment was a control, in which fish were dissected without being subjected to the fluid-preservation process. We compared parasite abundance between the two treatments. Across 298 fish individuals and 59 host-parasite pairs, we found few differences between treatments, with 24 of 27 host-parasite pairs equally abundant between the two treatments. Of these, one pair was significantly more abundant in the preservation treatment than in the control group, and two pairs were significantly less abundant in the preservation treatment than in the control group. Our data suggest that the fluid-preservation process does not have a substantial effect on the detectability of metazoan parasites. This study addresses only the effects of the fixation and preservation process; long-term experiments are needed to address whether parasite detectability remains unchanged in the months, years, and decades of storage following preservation. If so, ecologists will be able to reconstruct novel, long-term datasets on parasite diversity and abundance over the past century or more using fluid-preserved specimens from natural history collections.
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http://dx.doi.org/10.1002/ece3.6379DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381554PMC
July 2020

Recent introductions reveal differential susceptibility to parasitism across an evolutionary mosaic.

Evol Appl 2020 Mar 25;13(3):545-558. Epub 2019 Sep 25.

Smithsonian Environmental Research Center Edgewater MD USA.

Parasitism can represent a potent agent of selection, and introduced parasites have the potential to substantially alter their new hosts' ecology and evolution. While significant impacts have been reported for parasites that switch to new host species, the effects of macroparasite introduction into naïve populations of host species with which they have evolved remain poorly understood. Here, we investigate how the estuarine white-fingered mud crab () has adapted to parasitism by an introduced rhizocephalan parasite () that castrates its host. While the host crab is native to much of the East and Gulf Coasts of North America, its parasite is native only to the southern end of this range. Fifty years ago, the parasite invaded the mid-Atlantic, gradually expanding through previously naïve host populations. Thus, different populations of the same host species have experienced different degrees of historical interaction (and thus potential evolutionary response time) with the parasite: long term, short term, and naïve. In nine estuaries across this range, we examined whether and how parasite prevalence and host susceptibility to parasitism differs depending on the length of the host's history with the parasite. In field surveys, we found that the parasite was significantly more prevalent in its introduced range (i.e., short-term interaction) than in its native range (long-term interaction), a result that was also supported by a meta-analysis of prevalence data covering the 50 years since its introduction. In controlled laboratory experiments, host susceptibility to parasitism was significantly higher in naïve hosts than in hosts from the parasite's native range, suggesting that host resistance to parasitism is under selection. These results suggest that differences in host-parasite historical interaction can alter the consequences of parasite introductions in host populations. As anthropogenically driven range shifts continue, disruptions of host-parasite evolutionary relationships may become an increasingly important driver of ecological and evolutionary change.
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http://dx.doi.org/10.1111/eva.12865DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7045710PMC
March 2020

Social trematode parasites increase standing army size in areas of greater invasion threat.

Biol Lett 2020 02 26;16(2):20190765. Epub 2020 Feb 26.

Scripps Institution of Oceanography, Marine Biology Research Division, University of California-San Diego, La Jolla, CA, USA.

Organisms or societies are resource limited, causing important trade-offs between reproduction and defence. Given such trade-offs, optimal allocation theory predicts that, for animal societies with a soldier caste, allocation to soldiers should reflect local external threats. Although both threat intensity and soldier allocation can vary widely in nature, we currently lack strong evidence that spatial variation in threat can drive the corresponding variation in soldier allocation. The diverse guild of trematode parasites of the California horn snail provides a useful system to address this problem. Several of these species form colonies in their hosts with a reproductive division of labour including a soldier caste. Soldiers are non-reproductive and specialized in defence, attacking and killing invading parasites. We quantified invasion threat and soldier allocation for 168 trematode colonies belonging to six species at 26 sites spread among 10 estuaries in temperate and tropical regions. Spatial variation in invasion threat was matched as predicted by the relative number of soldiers for multiple parasite species. Soldier allocation correlated with invasion threat at fine spatial scales, suggesting that allocation is at least partly inducible. These results may represent the first clear documentation of a spatial correlation between allocation to any type of caste and a biotic selective agent.
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http://dx.doi.org/10.1098/rsbl.2019.0765DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058954PMC
February 2020

Predation shapes invertebrate diversity in tropical but not temperate seagrass communities.

J Anim Ecol 2020 02 4;89(2):323-333. Epub 2019 Dec 4.

Department of Biology, Temple University, Philadelphia, PA, USA.

The hypothesis that biotic interactions are stronger at lower relative to higher latitudes has a rich history, drawing from ecological and evolutionary theory. While this hypothesis suggests that stronger interactions at lower latitudes may contribute to the maintenance of contemporary patterns of diversity, there remain few standardized biogeographic comparisons of community effects of species interactions. Using marine seagrasses as a focal ecosystem of conservation importance and sessile marine invertebrates as model prey, we tested the hypothesis that predation is stronger at lower latitudes and can shape contemporary patterns of prey diversity. To further advance understanding beyond prior studies, we also explored mechanisms that likely underlie a change in interaction outcomes with latitude. Multiple observational and experimental approaches were employed to test for effects of predators, and the mechanisms that may underlie these effects, in seagrass ecosystems of the western Atlantic Ocean spanning 30° of latitude from the temperate zone to the tropics. In predator exclusion experiments conducted in a temperate and a tropical region, predation decreased sessile invertebrate abundance, richness and diversity on both natural and standardized artificial seagrass at tropical but not temperate sites. Further, predation reduced invertebrate richness at both local and regional scales in the tropics. Additional experiments demonstrated that predation reduced invertebrate recruitment in the tropics but not the temperate zone. Finally, direct observations of predators showed higher but variable consumption rates on invertebrates at tropical relative to temperate latitudes. Together, these results demonstrate that strong predation in the tropics can have consequential impacts on prey communities through discrete effects on early life stages as well as longer-term cumulative effects on community structure and diversity. Our detailed experiments also provide some of the first data linking large-scale biogeographic patterns, community-scale interaction outcomes and direct observation of predators in the temperate zone and tropics. Therefore, our results support the hypothesis that predation is stronger in the tropics, but also elucidate some of the causes and consequences of this variation in shaping contemporary patterns of diversity.
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http://dx.doi.org/10.1111/1365-2656.13133DOI Listing
February 2020

100-year time series reveal little morphological change following impoundment and predator invasion in two Neotropical characids.

Evol Appl 2019 Aug 27;12(7):1385-1401. Epub 2019 Feb 27.

Redpath Museum and Department of Biology McGill University Montreal Quebec Canada.

Human activities are dramatically altering ecosystems worldwide, often resulting in shifts in selection regimes. In response, natural populations sometimes undergo rapid phenotypic changes, which, if adaptive, can increase their probability of persistence. However, in many instances, populations fail to undergo any phenotypic change, which might indicate a variety of possibilities, including maladaptation. In freshwater ecosystems, the impoundment of rivers and the introduction of exotic species are among the leading threats to native fishes. We examined how the construction of the Panama Canal, which formed Lake Gatun, and the subsequent invasion of the predatory influenced the morphology of two native fishes: and spp. Using a 100-year time series, we studied variation in overall body shape over time (before vs. after impoundment and invasion) as well as across space (between an invaded and an uninvaded reservoir). In addition, we examined variation in linear morphological traits associated with swim performance and predator detection/avoidance. Notwithstanding a few significant changes in particular traits in particular comparisons, we found only limited evidence for morphological change associated with these two stressors. Most observed changes were subtle, and tended to be site- and species-specific. The lack of a strong morphological response to these stressors, coupled with dramatic population declines in both species, suggests they may be maladapted to the anthropogenically perturbed environment of Lake Gatun, but direct measures of fitness would be needed to test this. In general, our results suggest that morphological responses to anthropogenic disturbances can be very limited and, when they do occur, are often complex and context-dependent.
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http://dx.doi.org/10.1111/eva.12763DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6691216PMC
August 2019

Can marine reserves restore lost ecosystem functioning? A global synthesis.

Ecology 2019 04;100(4):e02617

Smithsonian Environmental Research Center, Edgewater, Maryland, 21037, USA.

Marine protected areas (MPAs) have grown exponentially, emerging as a widespread tool to conserve biodiversity and enhance fisheries production. Although numerous empirical studies and global syntheses have evaluated the effects of MPAs on community structure (e.g., biodiversity), no broad assessment concerning their capacity to influence ecological processes (e.g., species interactions) exists. Here, we present meta-analyses that compare rates of predation and herbivory on a combined 32 species across 30 MPAs spanning 85° of latitude. Our analyses synthesize the fate of 15,225 field experiment assays, and demonstrate that MPAs greatly increased predation intensity on animals but not herbivory on macroalgae or seagrass. Predation risk, quantified as the odds of prey being eaten, was largely determined by predator abundance and biomass within reserves. At MPAs with the greatest predator accumulation, the odds of predation increased to nearly 49:1, as opposed to 1:1 at MPAs where predators actually declined. Surprisingly, we also found evidence that predation risk declined with increased sea-surface temperature. Greater predation risk within MPAs was consistent with predator and prey population abundance estimates, where predators increased 4.4-fold within MPAs, whereas prey decreased 2.2-fold. For herbivory, the lack of change may have been driven by functional redundancy and the inability of reserves to increase herbivore abundance relative to fished zones in our sample. Overall, this work highlights the capacity of MPAs to restore a critical ecosystem function such as predation, which mediates energy flows and community assembly within natural systems. However, our review of the literature also uncovers relatively few studies that have quantified the effects of MPAs on ecosystem function, highlighting a key gap in our understanding of how protected areas may alter ecological processes and deliver ecosystem services. From a historical perspective, these findings suggest that modern levels of predation in the coastal oceans may currently only be a fraction of the baseline prior to human exploitation.
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http://dx.doi.org/10.1002/ecy.2617DOI Listing
April 2019

Negative effects of parasitic lung nematodes on the fitness of a Neotropical toad (Rhinella horribilis).

Parasitology 2019 06 12;146(7):928-936. Epub 2019 Mar 12.

Smithsonian Tropical Research Institute,Apartado 0843-03092, Ancon, Panama,Republic of Panama.

Pathogens are increasingly implicated in amphibian declines but less is known about parasites and the role they play. We focused on a genus of nematodes (Rhabdias) that is widespread in amphibians and examined their genetic diversity, abundance (prevalence and intensity), and impact in a common toad (Rhinella horribilis) in Panama. Our molecular data show that toads were infected by at least four lineages of Rhabdias, most likely Rhabdias pseudosphaerocephala, and multiple lineages were present in the same geographic locality, the same host and even the same lung. Mean prevalence of infection per site was 63% and mean intensity of infection was 31 worms. There was a significant effect of host size on infection status in the wild: larger toads were more likely to be infected than were smaller conspecifics. Our experimental infections showed that toadlets that were penetrated by many infective Rhabdias larvae grew less than those who were penetrated by few larvae. Exposure to Rhabdias reduced toadlet locomotor performance (both sustained speed and endurance) but did not influence toadlet survival. The effects of Rhabdias infection on their host appear to be primarily sublethal, however, dose-dependent reduction in growth and an overall impaired locomotor performance still represents a significant reduction in host fitness.
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http://dx.doi.org/10.1017/S0031182019000106DOI Listing
June 2019

Bioerosion in a changing world: a conceptual framework.

Ecol Lett 2018 03 4;21(3):422-438. Epub 2018 Jan 4.

Smithsonian Tropical Research Institute, Apartado, 0843-03092, Ancon, Panama.

Bioerosion, the breakdown of hard substrata by organisms, is a fundamental and widespread ecological process that can alter habitat structure, biodiversity and biogeochemical cycling. Bioerosion occurs in all biomes of the world from the ocean floor to arid deserts, and involves a wide diversity of taxa and mechanisms with varying ecological effects. Many abiotic and biotic factors affect bioerosion by acting on the bioeroder, substratum, or both. Bioerosion also has socio-economic impacts when objects of economic or cultural value such as coastal defences or monuments are damaged. We present a unifying definition and advance a conceptual framework for (a) examining the effects of bioerosion on natural systems and human infrastructure and (b) identifying and predicting the impacts of anthropogenic factors (e.g. climate change, eutrophication) on bioerosion. Bioerosion is responding to anthropogenic changes in multiple, complex ways with significant and wide-ranging effects across systems. Emerging data further underscore the importance of bioerosion, and need for mitigating its impacts, especially at the dynamic land-sea boundary. Generalised predictions remain challenging, due to context-dependent effects and nonlinear relationships that are poorly resolved. An integrative and interdisciplinary approach is needed to understand how future changes will alter bioerosion dynamics across biomes and taxa.
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http://dx.doi.org/10.1111/ele.12899DOI Listing
March 2018

Phylogeography and connectivity of molluscan parasites: Perkinsus spp. in Panama and beyond.

Int J Parasitol 2018 02 3;48(2):135-144. Epub 2017 Nov 3.

Marine Invasions Research Laboratory, Smithsonian Environmental Research Center, Edgewater, MD 21037, USA.

Panama is a major hub for commercial shipping between two oceans, making it an ideal location to examine parasite biogeography, potential invasions, and the spread of infectious agents. Our goals were to (i) characterise the diversity and genetic connectivity of Perkinsus spp. haplotypes across the Panamanian Isthmus and (ii) combine these data with sequences from around the world to evaluate the current phylogeography and genetic connectivity of these widespread molluscan parasites. We collected 752 bivalves from 12 locations along the coast of Panama including locations around the Bocas del Toro archipelago and the Caribbean and Pacific entrances to the Panama Canal, from December 2012 to February 2013. We used molecular genetic methods to screen for Perkinsus spp. and obtained internal transcribed spacer region (ITS) ribosomal DNA (rDNA) sequences for all positive samples. Our sequence data were used to evaluate regional haplotype diversity and distribution across both coasts of Panama, and were then combined with publicly available sequences to create global haplotype networks. We found 26 ITS haplotypes from four Perkinsus spp. (1-12 haplotypes per species) in Panama. Perkinsus beihaiensis haplotypes had the highest genetic diversity, were the most regionally widespread, and were associated with the greatest number of hosts. On a global scale, network analyses demonstrated that some haplotypes found in Panama were cosmopolitan (Perkinsus chesapeaki, Perkinsus marinus), while others were more geographically restricted (Perkinsus olseni, P. beihaiensis), indicating different levels of genetic connectivity and dispersal. We found some Perkinsus haplotypes were shared across the Isthmus of Panama and several regions around the world, including across ocean basins. We also found that haplotype diversity is currently underestimated and directly related to the number of sequences. Nevertheless, our results demonstrate long-range dispersal and global connectivity for many haplotypes, suggesting that dispersal through shipping probably contributes to these biogeographical patterns.
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http://dx.doi.org/10.1016/j.ijpara.2017.08.014DOI Listing
February 2018

Protistan Biogeography: A Snapshot Across a Major Shipping Corridor Spanning Two Oceans.

Protist 2017 04 6;168(2):183-196. Epub 2017 Jan 6.

Marine Invasions Research Laboratory, Smithsonian Environmental Research Center, Edgewater, MD 21037, USA.

Deciphering patterns of protistan taxa is a crucial step for understanding anthropogenic and environmental impacts on biogeography. We characterized and compared protistan communities from environmental samples collected along a major shipping corridor, the Panama Canal, and the Bocas del Toro archipelago. We used metabarcoding with high throughput sequencing (HTS) with the V4 hypervariable region of the ribosomal gene complex (rDNA). We detected many protistan taxa, including a variety of parasitic and toxic taxa. There were 1,296 OTUs shared across all three regions, with an additional 342-1,526 OTUs occurring across two or more regions, suggesting some mixing within the Caribbean and across the Isthmus. In general, this mixing did not impact community similarity, which was primarily distinct across regions. When OTUs identified as gregarines were analyzed separately, most samples grouped by region and communities were distinct across the Canal. Shipping traffic through the Panama Canal could move some taxa across regions; however, different environmental conditions in the two oceans may limit their establishment. Overall our results suggest that contemporary protistan biogeographic patterns are likely caused by a complex combination of factors, including anthropogenic dispersal and environmental tolerance.
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http://dx.doi.org/10.1016/j.protis.2016.12.003DOI Listing
April 2017

Richness and distribution of tropical oyster parasites in two oceans.

Parasitology 2016 08 6;143(9):1119-32. Epub 2016 Jun 6.

Marine Invasions Laboratory,Smithsonian Environmental Research Center,Edgewater,Maryland 21037,USA.

Parasites can exert strong effects on population to ecosystem level processes, but data on parasites are limited for many global regions, especially tropical marine systems. Characterizing parasite diversity and distributions are the first steps towards understanding the potential impacts of parasites. The Panama Canal serves as an interesting location to examine tropical parasite diversity and distribution, as it is a conduit between two oceans and a hub for international trade. We examined metazoan and protistan parasites associated with ten oyster species collected from both Panamanian coasts, including the Panama Canal and Bocas del Toro. We found multiple metazoan taxa (pea crabs, Stylochus spp., Urastoma cyrinae). Our molecular screening for protistan parasites detected four species of Perkinsus (Perkinsus marinus, Perkinsus chesapeaki, Perkinsus olseni, Perkinsus beihaiensis) and several haplosporidians, including two genera (Minchinia, Haplosporidium). Species richness was higher for the protistan parasites than for the metazoans, with haplosporidian richness being higher than Perkinsus richness. Perkinsus species were the most frequently detected and most geographically widespread among parasite groups. Parasite richness and overlap differed between regions, locations and oyster hosts. These results have important implications for tropical parasite richness and the dispersal of parasites due to shipping associated with the Panama Canal.
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http://dx.doi.org/10.1017/S0031182015001900DOI Listing
August 2016

Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts.

Ecology 2015 Nov;96(11):3033-42

Although the latitudinal diversity gradient is a well-known and general pattern, the mechanisms structuring it remain elusive. Two key issues limit differentiating these. First, habitat type usually varies with latitude, precluding a standardized evaluation of species richness. Second, broad-scale and local factors hypothesized to shape diversity patterns covary with one another, making it difficult to tease apart independent effects. Examining communities of parasites in widely distributed hosts can eliminate some of these confounding factors. We quantified diversity and interspecific interactions for trematode parasites infecting two similar snail species across 27 degrees of latitude from 43 locations in tropical and temperate oceans. Counter to typical patterns, we found that species richness, levels of parasitism, and intensity of intraguild predation increased with latitude. Because speciation rates are precluded from driving diversity gradients in this particular system, the reversed gradients are likely due to local ecological factors, specifically, increased productivity and stability. We highlight how this system may serve as a useful tool to provide insight into what processes drive diversity gradients in general.
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http://dx.doi.org/10.1890/15-0518.1DOI Listing
November 2015

Regional Variation in Parasite Species Richness and Abundance in the Introduced Range of the Invasive Lionfish, Pterois volitans.

PLoS One 2015 22;10(6):e0131075. Epub 2015 Jun 22.

Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Panama, Republic of Panama.

Parasites can play an important role in biological invasions. While introduced species often lose parasites from their native range, they can also accumulate novel parasites in their new range. The accumulation of parasites by introduced species likely varies spatially, and more parasites may shift to new hosts where parasite diversity is high. Considering that parasitism and disease are generally more prevalent at lower latitudes, the accumulation of parasites by introduced hosts may be greater in tropical regions. The Indo-Pacific lionfish (Pterois volitans) has become widely distributed across the Western Atlantic. In this study, we compared parasitism across thirteen locations in four regions, spanning seventeen degrees of latitude in the lionfish's introduced range to examine potential spatial variation in parasitism. In addition, as an initial step to explore how indirect effects of parasitism might influence interactions between lionfish and ecologically similar native hosts, we also compared parasitism in lionfish and two co-occurring native fish species, the graysby grouper, Cephalopholis cruentata, and the lizardfish, Synodus intermedius, in the southernmost region, Panama. Our results show that accumulation of native parasites on lionfish varies across broad spatial scales, and that colonization by ectoparasites was highest in Panama, relative to the other study sites. Endoparasite richness and abundance, on the other hand, were highest in Belize where lionfish were infected by twice as many endoparasite species as lionfish in other regions. The prevalence of all but two parasite species infecting lionfish was below 25%, and we did not detect an association between parasite abundance and host condition, suggesting a limited direct effect of parasites on lionfish, even where parasitism was highest. Further, parasite species richness and abundance were significantly higher in both native fishes compared to lionfish, and parasite abundance was negatively associated with the condition index of the native grouper but not that of the lionfish or lizardfish. While two co-occurring native fishes were more heavily parasitized compared to lionfish in Panama any indirect benefits of differential parasitism requires further investigation. Future parasitological surveys of lionfish across the eastern coast of North America and the Lesser Antilles would further resolve geographic patterns of parasitism in invasive lionfish.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0131075PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4476800PMC
April 2016

Host preference of an introduced 'generalist' parasite for a non-native host.

Int J Parasitol 2015 Sep 6;45(11):703-9. Epub 2015 Jun 6.

Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Panama.

Parasites can invade new ecosystems if they are introduced with their native hosts or if they successfully infect and colonise new hosts upon arrival. Here, we ask to what extent an introduced parasite demonstrates specialisation among novel host species. Infection surveys across three field sites in Gatun Lake, Panama, revealed that the invasive peacock bass, Cichla monoculus, was more commonly infected by the introduced trematode parasite Centrocestus formosanus than were three other common cichlid fishes. Laboratory infection experiments were conducted to determine whether parasitism might be driven by differential encounter/exposure to parasites or by differential infection susceptibility/preference across different host species. These experiments were performed by controlling for parasite exposure in single host (compatibility) experiments and in mixed host (preference) experiments. In all cases, the peacock bass exhibited higher infection rates with viable metacercariae relative to the other potential fish hosts. Our experiments thus support that an introduced generalist parasite shows apparent specialisation on a specific novel host. Further studies are needed to determine whether these patterns of specialisation are the result of local adaptation following invasion by the parasite.
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http://dx.doi.org/10.1016/j.ijpara.2015.03.012DOI Listing
September 2015

An introduced pentastomid parasite (Raillietiella frenata) infects native cane toads (Rhinella marina) in Panama.

Parasitology 2015 Apr 14;142(5):675-9. Epub 2014 Nov 14.

Smithsonian Tropical Research Institute,Apartado 0843-03092,Balboa,Ancon,Republic of Panama.

The pentastomid parasite, Raillietiella frenata, is native to Asia where it infects the Asian House gecko, Hemidactylus frenatus. This gecko has been widely introduced and recently R. frenata was found in introduced populations of cane toads (Rhinella marina) in Australia, indicating a host-switch from introduced geckos to toads. Here we report non-native adult R. frenata infecting the lungs of native cane toads in Panama. Eight of 64 toads were infected (median = 2.5, range = 1-80 pentastomids/toad) and pentastomid prevalence was positively associated with the number of buildings at a site, though further sampling is needed to confirm this pattern. We postulate that this pattern is likely due to a host shift of this parasite from an urban-associated introduced gecko. This is the first record of this parasite infecting cane toads in their native range, and the first instance of this parasite occurring in Central America.
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http://dx.doi.org/10.1017/S0031182014001759DOI Listing
April 2015

Stronger biotic resistance in tropics relative to temperate zone: effects of predation on marine invasion dynamics.

Ecology 2013 Jun;94(6):1370-7

Department of Biology, Temple University, Philadelphia, Pennsylvania 19122, USA.

Latitudinal patterns of nonnative species richness suggest fewer successful invasions in the tropics, relative to temperate regions. One main hypothesis for this pattern is that biotic resistance to invasion is stronger in the tropics than at higher latitudes. Biotic resistance can limit the distribution and abundance of nonnative species and, in extreme cases, can prevent establishment. We provide the first experimental test of this hypothesis, comparing the strength of biotic resistance in a tropical and a temperate marine ecosystem. Predation is one mechanism of biotic resistance, and since predation can be stronger at lower latitudes, we predicted that predation will serve to increase biotic resistance more in the tropics than at higher latitude. We conducted predator-exclusion experiments on marine epifaunal communities, a heavily invaded system, focusing on nonnative tunicates as a model fauna. The effect of predation on species richness of nonnative tunicates was more than three times greater at sites in tropical Panama than in temperate Connecticut, consistent with the prediction of stronger biotic resistance in the tropics. In Connecticut, predation reduced the abundance of one nonnative tunicate but did not affect the abundances of any other nonnative tunicate species, and no species were excluded from communities. In contrast, predation resulted in striking reductions in abundance and often exclusion of nonnative tunicates from experimental communities in Panama. If proved to be general, latitudinal differences in the biotic resistance of communities to nonnative species establishment may help explain emerging patterns of global invasions.
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http://dx.doi.org/10.1890/12-1382.1DOI Listing
June 2013

Do invasive species perform better in their new ranges?

Ecology 2013 May;94(5):985-94

Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, Maryland 21037, USA.

A fundamental assumption in invasion biology is that most invasive species exhibit enhanced performance in their introduced range relative to their home ranges. This idea has given rise to numerous hypotheses explaining "invasion success" by virtue of altered ecological and evolutionary pressures. There are surprisingly few data, however, testing the underlying assumption that the performance of introduced populations, including organism size, reproductive output, and abundance, is enhanced in their introduced compared to their native range. Here, we combined data from published studies to test this hypothesis for 26 plant and 27 animal species that are considered to be invasive. On average, individuals of these 53 species were indeed larger, more fecund, and more abundant in their introduced ranges. The overall mean, however, belied significant variability among species, as roughly half of the investigated species (N=27) performed similarly when compared to conspecific populations in their native range. Thus, although some invasive species are performing better in their new ranges, the pattern is not universal, and just as many are performing largely the same across ranges.
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http://dx.doi.org/10.1890/12-1810.1DOI Listing
May 2013

Flying shells: historical dispersal of marine snails across Central America.

Proc Biol Sci 2012 Mar 14;279(1731):1061-7. Epub 2011 Sep 14.

Smithsonian Tropical Research Institute, Balboa, Ancon, Republic of Panama.

The geological rise of the Central American Isthmus separated the Pacific and the Atlantic oceans about 3 Ma, creating a formidable barrier to dispersal for marine species. However, similar to Simpson's proposal that terrestrial species can 'win sweepstakes routes'-whereby highly improbable dispersal events result in colonization across geographical barriers-marine species may also breach land barriers given enough time. To test this hypothesis, we asked whether intertidal marine snails have crossed Central America to successfully establish in new ocean basins. We used a mitochondrial DNA genetic comparison of sister snails (Cerithideopsis spp.) separated by the rise of the Isthmus. Genetic variation in these snails revealed evidence of at least two successful dispersal events between the Pacific and the Atlantic after the final closure of the Isthmus. A combination of ancestral area analyses and molecular dating techniques indicated that dispersal from the Pacific to the Atlantic occurred about 750 000 years ago and that dispersal in the opposite direction occurred about 72 000 years ago. The geographical distribution of haplotypes and published field evidence further suggest that migratory shorebirds transported the snails across Central America at the Isthmus of Tehuantepec in southern Mexico. Migratory birds could disperse other intertidal invertebrates this way, suggesting the Central American Isthmus may not be as impassable for marine species as previously assumed.
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http://dx.doi.org/10.1098/rspb.2011.1599DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3267146PMC
March 2012

Stronger predation in the tropics shapes species richness patterns in marine communities.

Ecology 2011 Apr;92(4):983-93

Department of Biology, Temple University, Philadelphia, Pennsylvania 19122, USA.

Species interactions are widely assumed to be stronger at lower latitudes, but surprisingly few experimental studies test this hypothesis, and none ties these processes to observed patterns of species richness across latitude. We report here the first experimental field test that predation is both stronger and has a disproportionate effect on species richness in the tropics relative to the temperate zone. We conducted predator-exclusion experiments on communities of sessile marine invertebrates in four regions, which span 32 degrees latitude, in the western Atlantic Ocean and Caribbean Sea. Over a three-month timescale, predation had no effect on species richness in the temperate zone. In the tropics, however, communities were from two to over ten times more species-rich in the absence of predators than when predators were present. While micro-and macro-predators likely compete for the limited prey resource in the tropics, micropredators alone were able to exert as much pressure on the invertebrate communities as the full predator community. This result highlights the extent to which exposure to even a subset of the predator guild can significantly impact species richness in the tropics. Patterns were consistent in analyses that included relative and total species abundances. Higher species richness in the absence of predators in the tropics was also observed when species occurrences were pooled across two larger spatial scales, site and region, demonstrating a consistent scaling relationship. These experimental results show that predation can both limit local species abundances and shape patterns of regional coexistence in the tropics. When preestablished diverse tropical communities were then exposed to predation for different durations, ranging from one to several days, species richness was always reduced. These findings confirmed that impacts of predation in the tropics are strong and consistent, even in more established communities. Our results offer empirical support for the long-held prediction that predation pressure is stronger at lower latitudes. Furthermore, we demonstrate the magnitude to which variation in predation pressure can contribute to the maintenance of tropical species diversity.
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http://dx.doi.org/10.1890/09-2379.1DOI Listing
April 2011

Introduction of Armand Kuris, recipient of the 2010 Clark P. Read Mentor Award.

J Parasitol 2010 Dec 8;96(6):1041-3. Epub 2010 Sep 8.

Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Panama, Republic of Panama

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http://dx.doi.org/10.1645/GE-2636.1DOI Listing
December 2010

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes.

Int J Parasitol 2010 Nov 25;40(13):1525-30. Epub 2010 Jun 25.

Department of Biology, McGill University, Montreal, Quebec, Canada.

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.
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http://dx.doi.org/10.1016/j.ijpara.2010.05.007DOI Listing
November 2010

Molecular phylogenetics reveals differential divergence of coastal snails separated by the Isthmus of Panama.

Mol Phylogenet Evol 2010 Jul 23;56(1):40-8. Epub 2010 Apr 23.

Smithsonian Tropical Research Institute, Balboa, Ancon, Panama.

We used 20 species of coastal marine snails in the genus Cerithidea and Cerithium collected along the Pacific and Atlantic coasts of Central America to investigate the role of the rise of the Isthmus of Panama in the speciation of this group. Of particular interest was the identification of geminate species pairs presumably established by the disruption of gene flow across the isthmian barrier. Hypotheses of phylogenetic relationships were based on approximately 2.4 Kb of the mitochondrial cytochrome oxidase c subunit I gene, 16S ribosomal RNA gene and the nuclear 28S ribosomal gene. We identified four putative geminate species pairs out of the 20 species evaluated, but the level of sequence divergence among the pairs differed more than two-fold. A geminate pair, in which both species live in the high intertidal of mangrove habitats, exhibited less sequence divergence compared to other pairs occupying lower intertidal and subtidal habitats. Mangrove dwelling species were probably the last to be separated by the final closure of the Central American Seaway, and thus their divergence times correspond most accurately to the completion of the Isthmus.
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http://dx.doi.org/10.1016/j.ympev.2010.04.012DOI Listing
July 2010
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