Biogeographic and seasonal differences in consumer pressure underlie strong predation in the tropics.

Biotic interactions play a critical role in shaping patterns of global biodiversity. While several macroecological studies provide evidence for stronger predation in tropical regions compared with higher latitudes, results are variable even within the tropics, and the drivers of this variability are not well understood. We conducted two complementary standardized experiments on communities of sessile marine invertebrate prey and their associated predators to test for spatial and seasonal differences in predation across the tropical Atlantic and Pacific coastlines of Panama. We further tested the prediction that higher predator diversity contributes to stronger impacts of predation, using both direct observations of predators and data from extensive reef surveys. Our results revealed substantially higher predation rates and stronger effects of predators on prey in the Pacific than in the Atlantic, demonstrating striking variation within tropical regions. While regional predator diversity was high in the Atlantic, functional diversity at local scales was markedly low. Peak predation strength in the Pacific occurred during the wet, non-upwelling season when ocean temperatures were warmer and predator communities were more functionally diverse. Our results highlight the importance of regional biotic and abiotic drivers that shape interaction strength and the maintenance of tropical communities, which are experiencing rapid environmental change.

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

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.

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

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.

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

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.

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

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.

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

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.

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

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.

Bioerosion in a changing world: a conceptual framework.

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.

Richness and distribution of tropical oyster parasites in two oceans.

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.

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

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.

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

Ecosystem energetic implications of parasite and free-living biomass in three estuaries.

Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.

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

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.

Do invasive species perform better in their new ranges?

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.

Biological invasions alter the structure of a tropical freshwater food web.

Biological invasions are expected to alter food web structure, but there are limited empirical data directly comparing invaded versus uninvaded food webs, particularly in species-rich, tropical systems. We characterize for the first time the food web of Lake Gatun-a diverse and highly invaded tropical freshwater lake within the Panama Canal. We used stable isotope analysis to reconstruct the trophic structure of the fish community of Lake Gatun and to compare it to that of a minimally invaded reference lake, Lake Bayano. We found significant differences between the trophic structures of these two Neotropical lakes, notably that Lake Gatun's fish community was characterized by a longer food chain, greater isotopic diversity, a broader range of trophic positions and body sizes, and shifts in the isotopic positions of several native taxa relative to Lake Bayano. The degree of isotopic overlap between native and non-native trophic guilds in Lake Gatun was variable, with herbivores exhibiting the lowest (20%-29%) overlap and carnivores the greatest (81%-100%). Overall, our results provide some of the first empirical evidence for the ways in which multiple introduced and native species may partition isotopic space in a species-rich tropical freshwater food web.

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

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.

Introduced mangroves escape damage from marine and terrestrial enemies.

The enemy release hypothesis (ERH) posits that introduced species often leave their enemies behind when introduced to a new range. This release from enemies may allow introduced species to achieve higher growth and reproduction and may explain why some invaders flourish in new locations. Red mangroves (Rhizophora mangle) were introduced to Hawai'i from Florida over a century ago. Because Hawai'i has no native mangroves, the arrival of R. mangle fundamentally changed the structure and function of estuarine shorelines. While numerous enemies affect red mangroves in their native range (tropical America), in Hawai'i, mangroves apparently experience little herbivory, which may explain why introduced mangroves are so productive, fecund, and continue to spread. In this study, we compared the effects of enemies in native and introduced populations of brackish red mangroves (R. mangle) in 8-10 sites in the native range (Florida, Belize, and Panama) and introduced range of mangroves (Hawai'i). At each site, we measured the (1) occurrence of enemies using timed visual surveys, (2) occurrence of damage to different mangrove structures (leaves, apical buds, dead twigs, roots, propagules, and seedlings), and (3) rate of propagule herbivory using tethering experiments. Consistent with the ERH, we found an order of magnitude less damage and fewer enemies in introduced than native mangrove sites. While introduced mangroves harbored few enemies and minimal damage, native mangroves were affected by numerous enemies, including leaf-eating crabs, specialist bud moths, wood-boring insects and isopods, and propagule predators. These patterns were consistent across all plant structures (roots to leaves), among marine and terrestrial enemies, and across functional groups (browsers, borers, pathogens, etc.), which demonstrates enemy escape occurs consistently among different functional groups and via trophic (e.g., herbivores) and non-trophic (e.g., root borers) interactions. Our study is among the first biogeographical enemy release studies to take a comprehensive approach to quantifying the occurrence of damage from a broad suite of marine and terrestrial taxa across an array of wetland plant structures. Understanding how natural enemies alter this key foundation species will become increasingly relevant globally as mangroves continue to invade new regions through intentional plantings or range expansion driven by climate change.

Predator control of marine communities increases with temperature across 115 degrees of latitude.

Early naturalists suggested that predation intensity increases toward the tropics, affecting fundamental ecological and evolutionary processes by latitude, but empirical support is still limited. Several studies have measured consumption rates across latitude at large scales, with variable results. Moreover, how predation affects prey community composition at such geographic scales remains unknown. Using standardized experiments that spanned 115° of latitude, at 36 nearshore sites along both coasts of the Americas, we found that marine predators have both higher consumption rates and consistently stronger impacts on biomass and species composition of marine invertebrate communities in warmer tropical waters, likely owing to fish predators. Our results provide robust support for a temperature-dependent gradient in interaction strength and have potential implications for how marine ecosystems will respond to ocean warming.

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

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.

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

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.