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Body size has fundamental impacts on animal ecology and physiology but has been strongly influenced by recent climate change and human activities, such as size-selective harvesting. Understanding the ecological and life history consequences of body size has proved difficult due to the inseparability of direct effects of body size from processes connected to it (such as growth rate and individual condition). Here, we used the cnidarian Hydra oligactis to directly manipulate body size and understand its causal effects on reproduction and senescence. We found that experimentally reducing size delayed sexual development and lowered fecundity, while post-reproductive survival increased, implying that smaller individuals can physiologically detect their reduced size and adjust life history decisions to achieve higher survival. Our experiment suggests that ecological or human-induced changes in body size will have immediate effects on life history and population dynamics through a growth-independent link between body size, reproduction and senescence.
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Hydra , Animales , Tamaño Corporal , Fertilidad , Humanos , Dinámica Poblacional , ReproducciónRESUMEN
Facultative clonality is associated with complex life cycles where sexual and asexual forms can be exposed to contrasting selection pressures. Facultatively clonal animals often have distinct developmental capabilities that depend on reproductive mode (e.g., negligible senescence and exceptional regeneration ability in asexual individuals, which are lacking in sexual individuals). Understanding how these differences in life history strategies evolved is hampered by limited knowledge of the population structure underlying sexual and asexual forms in nature. Here we studied genetic differentiation of coexisting sexual and asexual Hydra oligactis polyps, a freshwater cnidarian where reproductive mode-dependent life history patterns are observed. We collected asexual and sexual polyps from 13 Central European water bodies and used restriction-site associated DNA sequencing to infer population structure. We detected high relatedness among populations and signs that hydras might spread with resting eggs through zoochory. We found no genetic structure with respect to mode of reproduction (asexual vs. sexual). On the other hand, clear evidence was found for phenotypic plasticity in mode of reproduction, as polyps inferred to be clones differed in reproductive mode. Moreover, we detected two cases of apparent sex change (males and females found within the same clonal lineages) in this species with supposedly stable sexes. Our study describes population genetic structure in Hydra for the first time, highlights the role of phenotypic plasticity in generating patterns of life history variation, and contributes to understanding the evolution of reproductive mode-dependent life history variation in coexisting asexual and sexual forms.
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Hydra , Adaptación Fisiológica , Animales , Femenino , Genotipo , Hydra/genética , Estadios del Ciclo de Vida , Masculino , Reproducción/genética , Reproducción Asexuada/genéticaRESUMEN
Asexual reproduction diversifies life-history priorities and is associated with unusual reproduction and somatic maintenance patterns, such as constant fertility with age, extensive regeneration ability and negligible senescence. While age-dependent plasticity in relative allocation to sexual versus asexual reproductive modes is relatively well studied, the modulation of somatic maintenance traits in parallel with age-dependent reproduction is much less well understood in clonal or partially clonal animals. Here, we asked how age-dependent investment into sexual and asexual reproduction co-varies with somatic maintenance such as regeneration in a partially clonal freshwater cnidarian Hydra oligactis, a species with remarkable regeneration abilities and experimentally inducible sex. We induced gametogenesis by lowering temperature at two ages, 1 or 4 weeks after detachment from an asexual parent, in animals of a male and a female clone. Then we measured phenotypically asexual and sexual reproductive traits (budding rate, start day and number of sexual organs) together with head regeneration rate, survival and the cellular background of these traits (number of reproductive and interstitial stem cells) for 2 or 5 months. Younger animals had higher asexual reproduction while individuals in the older group had more intensive gametogenesis and reproductive cell production. In parallel with these age-dependent reproductive differences, somatic maintenance of older individuals was also impacted: head regeneration, survival and interstitial stem cell numbers were reduced compared to younger polyps. Some of the traits investigated showed an ontogenetic effect, suggesting that age-dependent plasticity and a fixed ontogenetic response might both contribute to differences between age groups. We show that in H. oligactis asexual reproduction coupled with higher somatic maintenance is prioritized earlier in life, while sexual reproduction with higher maintenance costs occurs later if sex is induced. These findings confirm general life-history theory predictions on resource allocation between somatic maintenance and sexual reproduction applying in a partially clonal species. At the same time, our study also highlights the age-dependent integration of these resource allocation decisions with sexual/asexual strategies. Accounting for age-related differences might enhance repeatability of research done with clonal individuals derived from mass cultures.
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Hydra , Animales , Femenino , Fertilidad , Masculino , Fenotipo , Reproducción , Reproducción AsexuadaRESUMEN
Parental care is one of the most variable social behaviors and it is an excellent model system to understand cooperation between unrelated individuals. Three major hypotheses have been proposed to explain the extent of parental cooperation: sexual selection, social environment, and environmental harshness. Using the most comprehensive dataset on parental care that includes 659 bird species from 113 families covering both uniparental and biparental taxa, we show that the degree of parental cooperation is associated with both sexual selection and social environment. Consistent with recent theoretical models parental cooperation decreases with the intensity of sexual selection and with skewed adult sex ratios. These effects are additive and robust to the influence of life-history variables. However, parental cooperation is unrelated to environmental factors (measured at the scale of whole species ranges) as indicated by a lack of consistent relationship with ambient temperature, rainfall or their fluctuations within and between years. These results highlight the significance of social effects for parental cooperation and suggest that several parental strategies may coexist in a given set of ambient environment.
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Evolución Biológica , Aves/fisiología , Animales , Femenino , Masculino , Filogenia , Razón de Masculinidad , Especificidad de la EspecieRESUMEN
Insulin/insulin-like growth factor signaling (IIS) is thought to be a central mediator of life history traits, but the generality of its role is not clear. Here, we investigated mRNA expression levels of three insulin-like peptide genes, the insulin-like receptor htk7, as well as several antioxidant genes, and the heat-shock protein hsp70 in the freshwater cnidarian Hydra vulgaris. Hydra polyps were exposed to a combination of different levels of food and perceived population density to manipulate life history traits (asexual reproduction and oxidative stress tolerance). We found that stress tolerance and the rate of asexual reproduction increased with food, and that these two effects were in significant interaction. Exposing animals to high perceived density resulted in increased stress tolerance or reduced reproduction only on lower food levels, but not on high food. The insulin-like receptor htk7 and the antioxidant gene catalase were significantly upregulated in the high density treatments. However, the expression level of insulin-like peptide genes, most antioxidant genes, and hsp70 were not affected by the experimental treatments. The higher expression level of htk7 may suggest that animals maintain a higher level of preparedness for insulin-like ligands at high population densities. However, the lack of difference between food levels suggests that IIS is not involved in regulating asexual reproduction and stress tolerance in hydra, or that its role is more subtle than a simple model of life history regulation would suggest.
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Hydra/fisiología , Insulina/fisiología , Péptidos/metabolismo , Transducción de Señal/fisiología , Animales , Conducta Alimentaria , Regulación de la Expresión Génica , Proteínas HSP70 de Choque Térmico/genética , Proteínas HSP70 de Choque Térmico/metabolismo , Péptidos/genética , ARN Mensajero/genética , ARN Mensajero/metabolismo , Estrés FisiológicoRESUMEN
Tumoural processes, ubiquitous phenomena in multicellular organisms, influence evolutionary trajectories of all species. To gain a holistic understanding of their impact on species' biology, suitable laboratory models are required. Such models are characterised by a widespread availability, ease of cultivation, and reproducible tumour induction. It is especially important to explore, through experimental approaches, how tumoural processes alter ecosystem functioning. The cnidarian Hydra oligactis is currently emerging as a promising model due to its development of both transmissible and non-transmissible tumours and the wide breadth of experiments that can be conducted with this species (at the individual, population, mechanistic, and evolutionary levels). However, tumoural hydras are, so far, only documented in Europe, and it is not clear if the phenomenon is local or widespread. In this study we demonstrate that Australian hydras from two independent river networks develop tumours in the laboratory consisting of interstitial stem cells and display phenotypic alterations (supernumerary tentacles) akin to European counterparts. This finding confirms the value of this model for ecological and evolutionary research on host-tumour interactions.
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Growing evidence indicates that human activities are causing cancer rates to rise in both human and wildlife populations. This is due to the inability of ancestral anti-cancer defences to cope with modern environmental risks. The evolutionary mismatch between modern oncogenic risks and evolved cancer defences has far-reaching effects on various biological aspects at different timeframes, demanding a comprehensive study of the biology and evolutionary ecology of the affected species. Firstly, the increased activation of anti-cancer defences leads to excessive energy expenditure, affecting other biological functions and potentially causing health issues like autoimmune diseases. Secondly, tumorigenesis itself can impact important fitness-related parameters such as competitiveness, predator evasion, resistance to parasites, and dispersal capacity. Thirdly, rising cancer risks can influence the species' life-history traits, often favoring early reproduction to offset fitness costs associated with cancer. However, this strategy has its limits, and it may not ensure the sustainability of the species if cancer risks continue to rise. Lastly, some species may evolve additional anti-cancer defences, with uncertain consequences for their biology and future evolutionary path. In summary, we argue that the effects of increased exposure to cancer-causing substances on wildlife are complex, ranging from immediate responses to long-term evolutionary changes. Understanding these processes, especially in the context of conservation biology, is urgently needed.
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Temperature is a key abiotic factor controlling population dynamics. In facultatively sexual animals inhabiting the temperate zone, temperature can regulate the switch between asexual and sexual modes of reproduction, initiates growth or dormancy, and acts together with photoperiod to mediate seasonal physiological transitions. Increasing temperature due to recent global warming is likely to disrupt population dynamics of facultatively sexual animals because of the strong temperature dependence of multiple fitness components. However, the fitness consequences of warming in these animals are still poorly understood. This is unfortunate since facultatively sexual animals-through their ability for asexual reproduction resulting in quick population growth and sexual reproduction enabling long-term persistence-are key components of freshwater ecosystems. Here, I studied the fitness effects of warming in Hydra oligactis, a freshwater cnidarian that reproduces asexually throughout most of the year but switches to sexual reproduction under decreasing temperatures. I exposed hydra polyps to a simulated short summer heatwave or long-term elevated winter temperature. Since sexual development in this species is dependent on low temperature, I predicted reduced sexual investment (gonad production) and elevated asexual fitness (budding) in polyps exposed to higher temperatures. The results show a complex effect of warming on sexual fitness: While gonad number decreased in response to warming, both male and female polyps exposed to high winter temperature were capable of multiple rounds of gamete production. Asexual reproduction and survival rate, on the contrary, clearly increased in response to higher temperature, especially in males. These results predict increased population growth of H. oligactis in temperate freshwater habitats, which will likely affect the population dynamics of its main prey (freshwater zooplankton), and through that, the whole aquatic ecosystem.
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Within-species variation in animal body size predicts major differences in life history, for example, in reproductive development, fecundity, and even longevity. Purely from an energetic perspective, large size could entail larger energy reserves, fuelling different life functions, such as reproduction and survival (the "energy reserve" hypothesis). Conversely, larger body size could demand more energy for maintenance, and larger individuals might do worse in reproduction and survival under resource shortage (the "energy demand" hypothesis). Disentangling these alternative hypotheses is difficult because large size often correlates with better resource availability during growth, which could mask direct effects of body size on fitness traits. Here, we used experimental body size manipulation in the freshwater cnidarian Hydra oligactis, coupled with manipulation of resource (food) availability to separate direct effects of body size from resource availability on fitness traits (sexual development time, fecundity, and survival). We found significant interaction between body size and food availability in sexual development time in both males and females, such that large individuals responded less strongly to variation in resource availability. These results are consistent with an energy reserve effect of large size in Hydra. Surprisingly, the response was different in males and females: small and starved females delayed their reproduction, while small and starved males developed reproductive organs faster. In case of fecundity and survival, both size and food availability had significant effects, but we detected no interaction between them. Our observations suggest that in Hydra, small individuals are sensitive to fluctuations in resource availability, but these small individuals are able to adjust their reproductive development to maintain fitness.
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Multicellular organisms engage in complex ecological interactions with microorganisms, some of which are harmful to the host's health and fitness (e.g., pathogens or toxin-producing environmental microbiota), while others are either beneficial or have a neutral impact (as seen in components of host-associated microbiota). Although environmental microorganisms are generally considered to have no significant impact on animal fitness, there is evidence suggesting that exposure to these microbes might be required for proper immune maturation and research in vertebrates has shown that developing in a sterile environment detrimentally impacts health later in life. However, it remains uncertain whether such beneficial effects of environmental microorganisms are present in invertebrates that lack an adaptive immune system. In the present study, we conducted an experiment with field-collected Hydra oligactis, a cold-adapted freshwater cnidarian. We cultured these organisms in normal and autoclaved lake water at two distinct temperatures: 8°C and 12°C. Our findings indicated that polyps maintained in sterilized lake water displayed reduced population growth that depended on temperature, such that the effect was only present on 8°C. To better understand the dynamics of microbial communities both inhabiting polyps and their surrounding environment we conducted 16S sequencing before and after treatment, analyzing samples from both the polyps and the water. As a result of culturing in autoclaved lake water, the polyps showed a slightly altered microbiota composition, with some microbial lineages showing significant reduction in abundance, while only a few displayed increased abundances. The autoclaved lake water was recolonized, likely from the surface of hydra polyps, by a complex albeit different community of bacteria, some of which (such as Pseudomonas, Flavobacteriaceae) might be pathogenic to hydra. The abundance of the intracellular symbiont Polynucleobacter was positively related to hydra population size. These findings indicate that at low temperature environmental microbiota can enhance population growth rate in hydra, suggesting that environmental microorganisms can provide benefits to animals even in the absence of an adaptive immune system.
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Hydras are freshwater cnidarians widely used as a biological model to study different questions such as senescence or phenotypic plasticity but also tumoral development. The spontaneous tumors found in these organisms have been so far described in two female lab strains domesticated years ago (Hydra oligactis and Pelmatohydra robusta) and the extent to which these tumors can be representative of tumors within the diversity of wild hydras is completely unknown. In this study, we examined individuals isolated from recently sampled wild strains of different sex and geographical origin, which have developed outgrowths looking like tumors. These tumefactions have common features with the tumors previously described in lab strains: are composed of an accumulation of abnormal cells, resulting in a similar enlargement of the tissue layers. However, we also found diversity within these new types of tumors. Indeed, not only females, but also males seem prone to form these tumors. Finally, the microbiota associated to these tumors is different from the one involved in the previous lineages exhibiting tumors. We found that tumorous individuals hosted yet undescribed Chlamydiales vacuoles. This study brings new insights into the understanding of tumor susceptibility and diversity in brown hydras from different origins.
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Chlamydiales , Hydra , Animales , Masculino , Humanos , Femenino , Agua DulceRESUMEN
The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, changes in food availability have been linked to increased cancer incidence in humans, as an outcome of evolutionary mismatch. Here, we apply evolutionary oncology principles to test whether food availability, regardless of the multicellular lineage considered, has an impact on tumorigenesis. We used two phylogenetically unrelated model systems, the cnidarian Hydra oligactis and the fish Danio rerio, to investigate the impact of resource availability on tumor occurrence and progression. Individuals from healthy and tumor-prone lines were placed on four diets that differed in feeding frequency and quantity. For both models, frequent overfeeding favored tumor emergence, while lean diets appeared more protective. In terms of tumor progression, high food availability promoted it, whereas low resources controlled it, but without having a curative effect. We discuss our results in light of current ideas about the possible conservation of basic processes governing cancer in metazoans (including ancestral life history trade-offs at the cell level) and in the framework of evolutionary medicine.
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Cnidarios , Hydra , Neoplasias , Animales , Humanos , Evolución Biológica , Carcinogénesis , Neoplasias/etiologíaRESUMEN
Most animals co-exist with diverse host-associated microbial organisms that often form complex communities varying between individuals, habitats, species and higher taxonomic levels. Factors driving variation in the diversity of host-associated microbes are complex and still poorly understood. Here, we describe the bacterial composition of field-collected Hydra, a freshwater cnidarian that forms stable associations with microbial species in the laboratory and displays complex interactions with components of the microbiota. We sampled Hydra polyps from 21 Central European water bodies and identified bacterial taxa through 16S rRNA sequencing. We asked whether diversity and taxonomic composition of host-associated bacteria depends on sampling location, habitat type, host species or host reproductive mode (sexual vs. asexual). Bacterial diversity was most strongly explained by sampling location, suggesting that the source environment plays an important role in the assembly of bacterial communities associated with Hydra polyps. We also found significant differences between host species in their bacterial composition that partly mirrored variations observed in lab strains. Furthermore, we detected a minor effect of host reproductive mode on bacterial diversity. Overall, our results suggest that extrinsic (habitat identity) factors predict the diversity of host-associated bacterial communities more strongly than intrinsic (species identity) factors, however, only a combination of both factors determines microbiota composition in Hydra.
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Facultative sexual organisms combine sexual and asexual reproduction within a single life cycle, often switching between reproductive modes depending on environmental conditions. These organisms frequently inhabit variable seasonal environments, where favorable periods alternate with unfavorable periods, generating temporally varying selection pressures that strongly influence life history decisions and hence population dynamics. Due to the rapidly accelerating changes in our global environment today, understanding the population dynamics and genetic changes in facultative sexual populations inhabiting seasonal environments is critical to assess and prepare for additional challenges that will affect such ecosystems. In this study, we aimed at obtaining insights into the seasonal population dynamics of the facultative sexual freshwater cnidarian Hydra oligactis through a combination of restriction site-associated sequencing (RAD-Seq) genotyping and the collection of phenotypic data on the reproductive strategy of field-collected hydra strains in a standard laboratory environment. We reliably detected 42 MlGs from the 121 collected hydra strains. Most of MLGs (N = 35, 83.3%) were detected in only one season. Five MLGs (11.9%) were detected in two seasons, one (2.4%) in three seasons and one (2.4%) in all four seasons. We found no significant genetic change during the 2 years in the study population. Clone lines were detected between seasons and even years, suggesting that clonal lineages can persist for a long time in a natural population. We also found that distinct genotypes differ in sexual reproduction frequency, but these differences did not affect whether genotypes reappeared across samplings. Our study provides key insights into the biology of natural hydra populations, while also contributing to understanding the population biology of facultative sexual species inhabiting freshwater ecosystems.
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While it is often assumed that oncogenic processes in metazoans can influence species interactions, empirical evidence is lacking. Here, we use the cnidarian Hydra oligactis to experimentally explore the consequences of tumor associated phenotypic alterations for its predation ability, relationship with commensal ciliates and vulnerability to predators. Unexpectedly, hydra's predation ability was higher in tumorous polyps compared to non-tumorous ones. Commensal ciliates colonized preferentially tumorous hydras than non-tumorous ones, and had a higher replication rate on the former. Finally, in a choice experiment, tumorous hydras were preferentially eaten by a fish predator. This study, for the first time, provides evidence that neoplastic growth has the potential, through effect(s) on host phenotype, to alter biotic interactions within ecosystems and should thus be taken into account by ecologists.
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Cnidarios , Hydra , Neoplasias , Animales , Ecosistema , Agua DulceRESUMEN
Although tumors can occur during the lifetime of most multicellular organisms and have the potential to influence health, how they alter life-history traits in tumor-bearing individuals remains poorly documented. This question was explored using the freshwater cnidarian Hydra oligactis, a species sometimes affected by vertically transmitted tumors. We found that tumorous polyps have a reduced survival compared to healthy ones. However, they also displayed higher asexual reproductive effort, by producing more often multiple buds than healthy ones. A similar acceleration is observed for the sexual reproduction (estimated through gamete production). Because tumoral cells are not transmitted through this reproductive mode, this finding suggests that hosts may adaptively respond to tumors, compensating the expected fitness losses by increasing their immediate reproductive effort. This study supports the hypothesis that tumorigenesis has the potential to influence the biology, ecology, and evolution of multicellular species, and thus should be considered more by evolutionary ecologists.
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The role of anthropogenically influenced habitats in conserving elements of the original wildlife has increased worldwide simultaneously with the disappearance of natural sites. Burial places are able to conserve original elements of the wildlife, and this fact has been known for at least a century. To this day, little is known about long-time changes and the effect of long-time management methods in cemeteries on the flora they harbor. The utility of historical maps in research focused on natural values, as well as in answering questions related to conservation was recently demonstrated, but the use of digitized historical maps in biodiversity research of the Carpathian Basin is very limited. In the present paper, we aimed to predict the conservation potential of long-established and newly established cemeteries of Hungarian settlements with various population sizes based on the digitized maps of the 2nd Military Survey of the Austrian Empire (1819-1869), by categorizing cemeteries into 3 distinct (anthropogenic habitat, cemetery, or natural habitat) types. To build our models, we used records of the protected flora from Hungarian cemeteries, based on data of thematic botanical surveys of 991 cemeteries. Out of the surveyed cemeteries, 553 (56%) harbored protected plants, totaling 306.617 estimated individuals of 92 protected species, belonging to 28 plant families. These species represent 12% of the entire protected flora of Hungary. Hungarian cemeteries play a key role mainly in preserving steppe and dry grassland plant species. Long-established and large cemeteries harbor more protected plant species than small and newly established ones. Human population size of the settlements correlated negatively with the number of protected species and individuals. Moreover, woodland cover and proportion of grassland also significantly positively affected the number of protected plant species in cemeteries.
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Freshwater hydra are among the few animal groups that show negligible senescence and can maintain high survival and reproduction rates when kept under stable conditions in the laboratory. Yet, one species of Hydra (H. oligactis) undergoes a senescence-like process in which polyps degenerate and die after sexual reproduction. The ultimate factors responsible for this phenomenon are unclear. High mortality in reproducing animals could be the consequence of increased allocation of resources to reproduction at the expense of somatic maintenance. This hypothesis predicts that patterns of reproduction and survival are influenced by resource availability. To test this prediction we investigated survival and reproduction at different levels of food availability in 10 lineages of H. oligactis derived from a single Hungarian population. Sexual reproduction was accompanied by reduced survival, but a substantial proportion of animals regenerated after sexual reproduction and continued reproducing asexually. Polyps belonging to different lineages showed differences in their propensity to initiate sexual reproduction, gonad number and survival rate. Food availability significantly affected fecundity (number of eggs or testes produced), with the largest number of gonads being produced by animals kept on a high food regime. On the other hand, survival rate was not affected by the amount of food. These results show that survival is conserved at the expense of reproduction in this population when food is low. It remains a question still to be answered why survival is prioritized over reproduction in this population.
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Hydra/fisiología , Animales , Metabolismo Energético/fisiología , Hungría , Reproducción/fisiología , RíosRESUMEN
Harvest of orchid tubers for salep production is widespread in southwestern Asia and the Balkans and constitutes a major conservation risk for wild orchid populations. Synanthropic habitats, such as graveyards, are important refuges for orchids and other organisms and could offer protection from salep harvesting because of their special cultural role. However, little is known about the occurrence and factors influencing harvesting of salep in graveyards. During field surveys of 474 graveyards throughout Turkey, we observed 333 graveyards with orchids, 311 graveyards with tuberous orchids, and salep harvest in 14 graveyards. Altogether, 530 individuals of 17 orchid species were collected, representing 9% of the individuals recorded. Harvesting intensity was relatively low, and populations were usually not wholly destroyed. However, some species were clearly more affected than others. Salep harvesting risk of orchid species was significantly associated with flowering time, with early-flowering species being more affected. A marginally significant positive relationship between harvesting risk and species-specific tuber size was also detected. Our data suggest that graveyards might offer some protection against salep harvesting in Turkey, but they also show that some orchid taxa are much more affected than others. Overall, our observations add more weight to the conservation value of these special habitats.