Dispersal of aquatic and terrestrial organisms by waterbirds: A review of current knowledge and future priorities

1. We review progress in our understanding of the importance of waterbirds as dispersal vectors of other organisms, and identify priorities for further research. 2. Waterbirds are excellent for long-distance dispersal (LDD), whereas other vectors such as fish and mammals disperse similar propagules, but over shorter distances. Empirical studies of internal and external transport by waterbirds have shown that the former mechanism generally is more important. Internal transport is widely recognised for aquatic plants and aquatic invertebrates with resting eggs, but also is important for other organisms (e.g., terrestrial flowering plants not dispersed by frugivores, bryophytes, tardigrades, fish eggs). 3. Waterbird vectors also are important in terrestrial habitats, and provide connectivity across terrestrial–aquatic boundaries. There are important differences in the roles of different waterbird species, especially those using different habitats along the aquatic–terrestrial gradient. Early attempts to predict zoochory based on propagule morphology have been found wanting, and more research is needed into how the traits of vectors and vectored organisms (including life history, dormancy and growth traits) explain dispersal interactions. Experimental studies have focused on the potential of propagules to survive internal or external transport, and research into factors determining the establishment success of propagules after dispersal is lacking. 4. Recent spatially explicit models of seed dispersal by waterbirds should be expanded to include invertebrate dispersal, and to compare multiple bird species in the same landscape. Network approaches have been applied to plant–waterbird dispersal interactions, and these are needed for invertebrates. Genetic studies support effective LDD of plants and invertebrates along waterbird flyways, but there remains a lack of examples at a local scale. Next Generation Sequencing and genomics should be applied to waterbird-mediated dispersal across the landscape. More studies of biogeography, community ecology, or population genetics should integrate waterbird movements at the design stage. 5. Zoochory research has paid little attention to the dispersal of non-pathogenic microbes (both eukaryotic and prokaryotic). Nevertheless, there is evidence that dispersal via avian guts can be central to the connectivity of aquatic microbial metacommunities. More work on microbial dispersal by waterbirds should explore its implications for biogeochemistry, and the interchange with gut flora of other aquatic organisms. In the Anthropocene, the role of migratory waterbirds in LDD of plants and other organisms is particularly important, for example in compensating for loss of large migratory mammals and fish, allowing native species to adjust their distributions under global warming, and spreading alien species along flyways after their initial introductions by human vectors. Recent technological advances have opened exciting opportunities that should be fully exploited to further our understanding of dispersal by waterbirds.AJG was supported by projects from the Ministerio de Ciencia e Innovación (PID2020-112774GB-I00/AEI/10.13039/501100011033) and Ministerio de Economía y Competitividad (CGL2016-76067-P). ESG received the grant RYC2019-027216-I funded by MCIN/AEI/10.13039/501100011033 and from ESF Investing in your future. GGS received a postdoctoral fellowship from CNPq (grant no. 150887/2022-1) ÁLK was supported by a János Bolyai Research Scholarship of the Hungarian Academy of Sciences, New National Excellence Programme of the Ministry of Innovation and Technology ÚNKP-21-5-DE-457, NKFIH FK-138698 grants

Effects of Rising Temperature on the Growth, Stoichiometry, and Palatability of Aquatic Plants

Global warming is expected to strengthen herbivore-plant interactions leading to enhanced top-down control of plants. However, latitudinal gradients in plant quality as food for herbivores suggest lower palatability at higher temperatures, but the underlying mechanisms are still unclear. If plant palatability would decline with temperature rise, then this may question the expectation that warming leads to enhanced top-down control. Therefore, experiments that directly test plant palatability and the traits underlying palatability along a temperature gradient are needed. Here we experimentally tested the impact of temperature on aquatic plant growth, plant chemical traits (including stoichiometry) and plant palatability. We cultured three aquatic plant species at three temperatures (15, 20, and 25°C), measured growth parameters, determined chemical traits and performed feeding trial assays using the generalist consumer Lymnaea stagnalis (pond snail). We found that rising temperature significantly increased the growth of all three aquatic plants. Plant nitrogen (N) and phosphorus (P) content significantly decreased, and carbon (C):N and C:P stoichiometry increased as temperature increased, for both Potamogeton lucens and Vallisneria spiralis, but not for Elodea nuttallii. By performing the palatability test, we found that rising temperatures significantly decreased plant palatability in P. lucens, which could be explained by changes in the underlying chemical plant traits. In contrast, the palatability of E. nuttallii and V. spiralis was not affected by temperature. Overall, P. lucens and V. spiralis were always more palatable than E. nuttallii. We conclude that warming generally stimulates aquatic plant growth, whereas the effects on chemical plant traits and plant palatability are species-specific. These results suggest that the outcome of the impact of temperature rise on macrophyte stoichiometry and palatability from single-species studies may not be broadly applicable. In contrast, the plant species tested consistently differed in palatability, regardless of temperature, suggesting that palatability may be more strongly linked to species identity than to intraspecific variation in plant stoichiometry

A seed dispersal effectiveness framework across the mutualism–antagonism continuum

Many angiosperms rely on vertebrates for seed dispersal via gut passage, an interaction that has been traditionally classified as a mutualism. The seed dispersal effectiveness (SDE) framework provides a mechanistic approach to evaluate evolutionary and ecological characteristics of animal-mediated seed dispersal, by synthesising the quantity and the quality of the dispersal that a plant species receives from each of its animal dispersers. However, the application of the SDE framework has been largely restricted to plant–frugivore interactions, whereas animal-mediated seed dispersal results from plant–disperser interactions that cover a continuum from pure mutualisms to antagonisms. This biases ecological and evolutionary knowledge on plant–disperser interactions. Here, we propose an extended SDE framework (‘eSDE') that allows comparing plant–disperser interactions in the full mutualism–antagonism continuum ranging from pure mutualisms (frugivores) to conditional mutualisms (scatter-hoarding granivores and folivores) and antagonisms (pure granivores). We present the eSDE framework, and use examples to illustrate how it can be applied to compare effectiveness among plant–disperser interaction types. Our initial comparison based on available data suggests that vertebrate species differ more in the number of seeds they deposit away from the mother plant (quantity), than in the effects such dispersal processes have on seed fate (quality). Scatter-hoarding granivores provide the most effective dispersal due to high removal rates, closely followed by frugivores due to high deposition rates. Folivores and pure granivores provide low quantity dispersal, but of high and moderate quality, respectively. These early comparative insights illustrate the necessity and usefulness of more standardized data collection protocols, for which we provide recommendations. Applying the eSDE framework can reveal broad-scale patterns across and within plant–disperser interaction types, which will advance our evolutionary understanding of plant–animal interactions. This will provide new insights into the consequence of anthropogenic impacts on vertebrate-mediated seed dispersal in a world in which plant–animal interactions are increasingly threatened

Evaluation of sexual history-based screening of anatomic sites for chlamydia trachomatis and neisseria gonorrhoeae infection in men having sex with men in routine practice

<p>Abstract</p> <p>Background</p> <p>Sexually transmitted infection (STI) screening programmes are implemented in many countries to decrease burden of STI and to improve sexual health. Screening for <it>Chlamydia trachomatis </it>and <it>Neisseria gonorrhoeae </it>has a prominent role in these protocols. Most of the screening programmes concerning men having sex with men (MSM) are based on opportunistic urethral testing. In The Netherlands, a history-based approach is used. The aim of this study is to evaluate the protocol of screening anatomic sites for <it>C. trachomatis </it>and <it>N. gonorrhoeae </it>infection based on sexual history in MSM in routine practice in The Netherlands.</p> <p>Methods</p> <p>All MSM visiting the clinic for STI in The Hague are routinely asked about their sexual practice during consulting. As per protocol, tests for urogenital, oropharyngeal and anorectal infection are obtained based on reported site(s) of sexual contact. All consultations are entered into a database as part of the national STI monitoring system. Data of an 18 months period were retrieved from this database and analysed.</p> <p>Results</p> <p>A total of 1455 consultations in MSM were registered during the study period. The prevalence of <it>C. trachomatis </it>and <it>N. gonorrhoeae </it>per anatomic site was: urethral infection 4.0% respectively and 2.8%, oropharynx 1.5% and 4.2%, and anorectum 8.2% and 6.0%. The majority of chlamydia cases (72%) involved a single anatomic site, which was especially manifest for anorectal infections (79%), while 42% of gonorrhoea cases were single site. Twenty-six percent of MSM with anorectal chlamydia and 17% with anorectal gonorrhoea reported symptoms of proctitis; none of the oropharyngeal infections were symptomatic. Most cases of anorectal infection (83%) and oropharyngeal infection (100%) would have remained undiagnosed with a symptom-based protocol.</p> <p>Conclusions</p> <p>The current strategy of sexual-history based screening of multiple anatomic sites for chlamydia and gonorrhoea in MSM is a useful and valid guideline which is to be preferred over a symptom-based screening protocol.</p

Skewed X-inactivation is common in the general female population

X-inactivation is a well-established dosage compensation mechanism ensuring that X-chromosomal genes are expressed at comparable levels in males and females. Skewed X-inactivation is often explained by negative selection of one of the alleles. We demonstrate that imbalanced expression of the paternal and maternal X-chromosomes is common in the general population and that the random nature of the X-inactivation mechanism can be sufficient to explain the imbalance. To this end, we analyzed blood-derived RNA and whole-genome sequencing data from 79 female children and their parents from the Genome of the Netherlands project. We calculated the median ratio of the paternal over total counts at all X-chromosomal heterozygous single-nucleotide variants with coverage ≥10. We identified two individuals where the same X-chromosome was inactivated in all cells. Imbalanced expression of the two X-chromosomes (ratios ≤0.35 or ≥0.65) was observed in nearly 50% of the population. The empirically observed skewing is explained by a theoretical model where X-inactivation takes place in an embryonic stage in which eight cells give rise to the hematopoietic compartment. Genes escaping X-inactivation are expressed from both alleles and therefore demonstrate less skewing than inactivated genes. Using this characteristic, we identified three novel escapee genes (SSR4, REPS2, and SEPT6), but did not find support for many previously reported escapee genes in blood. Our collective data suggest that skewed X-inactivation is common in the general population. This may contribute to manifestation of symptoms in carriers of recessive X-linked disorders. We recommend that X-inactivation results should not be used lightly in the interpretation of X-linked variants

Coronary Artery Calcium Scores After Prophylactic Premenopausal Bilateral Salpingo-Oophorectomy

Background: Premenopausal risk-reducing salpingo-oophorectomy (RRSO) in women at high familial risk of ovarian cancer leads to immediate menopause. Although early natural menopause is associated with increased cardiovascular disease risk, evidence on long-term cardiovascular disease risk after early surgical menopause is scarce. Objectives: We sought to determine the long-term influence of the timing of RRSO on the development of coronary artery calcium (CAC), an established marker for cardiovascular disease risk. Methods: We conducted a cross-sectional study (N = 733) nested in a nationwide cohort of women at high familial risk of ovarian cancer. In women aged 60-70 years (n = 328), we compared CAC scores between women with a premenopausal RRSO (age ≤45 years) and women with a postmenopausal RRSO (age ≥54 years), using multivariable Poisson analyses. Within the premenopausal RRSO group (n = 498), we also examined the effect of age at RRSO. In addition, we compared the premenopausal RRSO group with an external reference cohort (n = 5,226). Results: Multivariable analyses showed that the prevalence rates of any CAC (CAC >0), at least moderate CAC (CAC >100), and severe CAC (CAC >400) were comparable between the premenopausal and postmenopausal RRSO groups (relative risk [RR]: 0.93; 95% CI: 0.75-1.15 for any CAC; RR: 0.71; 95% CI: 0.43-1.17 for at least moderate CAC; RR: 0.81; 95% CI: 0.30-2.13 for severe CAC). There was no difference in CAC between the premenopausal RRSO group and a similar aged reference cohort. Timing of premenopausal RRSO (early premenopausal RRSO [<41 years] vs late premenopausal RRSO [41-45 years]) did not affect the outcomes. Conclusions: Our results do not show a long-term adverse effect of surgical menopause on the development of CAC

Skewed X-inactivation is common in the general female population

X-inactivation is a well-established dosage compensation mechanism ensuring that X-chromosomal genes are expressed at comparable levels in males and females. Skewed X-inactivation is often explained by negative selection of one of the alleles. We demonstrate that imbalanced expression of the paternal and maternal X-chromosomes is common in the general population and that the random nature of the X-inactivation mechanism can be sufficient to explain the imbalance. To this end, we analyzed blood-derived RNA and whole-genome sequencing data from 79 female children and their parents from the Genome of the Netherlands project. We calculated the median ratio of the paternal over total counts at all X-chromosomal heterozygous single-nucleotide variants with coverage ≥10. We identified two individuals where the same X-chromosome was inactivated in all cells. Imbalanced expression of the two X-chromosomes (ratios ≤0.35 or ≥0.65) was observed in nearly 50% of the population. The empirically observed skewing is explained by a theoretical model where X-inactivation takes place in an embryonic stage in which eight cells give rise to the hematopoietic compartment. Genes escaping X-inactivation are expressed from both alleles and therefore demonstrate less skewing than inactivated genes. Using this characteristic, we identified three novel escapee genes (SSR4, REPS2, and SEPT6), but did not find support for many previously reported escapee genes in blood. Our collective data suggest that skewed X-inactivation is common in the general population. This may contribute to manifestation of symptoms in carriers of recessive X-linked disorders. We recommend that X-inactivation results should not be used lightly in the interpretation of X-linked variants

Internal and External Dispersal of Plants by Animals: An Aquatic Perspective on Alien Interference

Many alien plants use animal vectors for dispersal of their diaspores (zoochory). If alien plants interact with native disperser animals, this can interfere with animal-mediated dispersal of native diaspores. Interference by alien species is known for frugivorous animals dispersing fruits of terrestrial plants by ingestion, transport and egestion (endozoochory). However, less attention has been paid to possible interference of alien plants with dispersal of diaspores via external attachment (ectozoochory, epizoochory or exozoochory), interference in aquatic ecosystems, or positive effects of alien plants on dispersal of native plants. This literature study addresses the following hypotheses: (1) alien plants may interfere with both internal and external animal-mediated dispersal of native diaspores; (2) interference also occurs in aquatic ecosystems; (3) interference of alien plants can have both negative and positive effects on native plants. The studied literature revealed that alien species can comprise large proportions of both internally and externally transported diaspores. Because animals have limited space for ingested and adhering diaspores, alien species affect both internal and external transport of native diaspores. Alien plant species also form large proportions of all dispersed diaspores in aquatic systems and interfere with dispersal of native aquatic plants. Alien interference can be either negative (e.g., through competition with native plants) or positive (e.g., increased abundance of native dispersers, changed disperser behavior or attracting additional disperser species). I propose many future research directions, because understanding whether alien plant species disrupt or facilitate animal-mediated dispersal of native plants is crucial for targeted conservation of invaded (aquatic) plant communities

Great cormorants reveal overlooked secondary dispersal of plants and invertebrates by piscivorous waterbirds

In wetland ecosystems, birds and fish are important dispersal vectors for plants and invertebrates, but the consequences of their interactions as vectors are unknown. Darwin suggested that piscivorous birds carry out secondary dispersal of seeds and invertebrates via predation on fish. We tested this hypothesis in the great cormorant (Phalacrocorax carbo L.). Cormorants regurgitate pellets daily, which we collected at seven European locations and examined for intact propagules. One-third of pellets contained at least one intact plant seed, with seeds from 16 families covering a broad range of freshwater, marine and terrestrial habitats. Of 21 plant species, only two have an endozoochory dispersal syndrome, compared with five for water and eight for unassisted dispersal syndromes. One-fifth of the pellets contained at least one intact propagule of aquatic invertebrates from seven taxa. Secondary dispersal by piscivorous birds may be vital to maintain connectivity in meta-populations and between river catchments, and in the movement of plants and invertebrates in response to climate change. Secondary dispersal pathways associated with complex food webs must be studied in detail if we are to understand species movements in a changing world.Peer reviewe