temporary-translocation-entire-mistletoe-plants-to-understand

Temporary Translocation of Entire Mistletoe Plants to Understand the Mechanistic Basis of Animal Foraging Decisions

Fruiting mistletoes present a model system for understanding decisions made by foraging animals when locating food. Where, when, and how animals find food ...

Charles Sturt University

The importance of litter in regulating ecosystem processes has long been recognised, with a growing appreciation of the differential contribution of various functional plant groups. Despite the ubiquity of mistletoes in terrestrial ecosystems and their prominence in ecological studies, they are one group that have been overlooked in litter research. This study evaluated the litter contribution from a hemiparasitic mistletoe, Amyema miquelii (Lehm. ex Miq.) Tiegh., in an open eucalypt forest (Eucalyptus blakelyi, E. dwyeri and E. dealbata), at three scales; the forest stand, single trees and individual mistletoes. Litter from mistletoes significantly increased overall litterfall by up to 189%, the amount of mistletoe litter being proportional to the mistletoe biomass in the canopy. The high litter input was due to a much higher rate of mistletoe leaf turnover than that of host trees; the host litterfall and rate of leaf turnover was not significantly affected by mistletoe presence. The additional litter from mistletoes also affected the spatial and temporal distribution of litterfall due to the patchy distribution of mistletoes and their prolonged period of high litterfall. Associated with these changes in litterfall was an increase in ground litter mass and plant productivity, which reflects similar findings with root-parasitic plants. These findings represent novel mechanisms underlying the role of mistletoes as keystone resources and provide further evidence of the importance of parasites in affecting trophic dynamics.

Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest.

Various entities have been designated keystone resources, but few tests have been attempted and we are unaware of any experimental manipulations of purported keystone resources. Mistletoes (Loranthaceae) provide structural and nutritional resources within canopies, and their pervasive influence on diversity led to their designation as keystone resources. We quantified the effect of mistletoe on diversity with a woodland-scale experiment, comparing bird diversities before and after all mistletoe plants were removed from 17 treatment sites, with those of 11 control sites and 12 sites in which mistletoe was naturally absent. Three years after mistletoe removal, treatment woodlands lost, on average, 20.9 per cent of their total species richness, 26.5 per cent of woodland-dependent bird species and 34.8 per cent of their woodland-dependent residents, compared with moderate increases in control sites and no significant changes in mistletoe-free sites. Treatment sites lost greater proportions of birds recorded nesting in mistletoe, but changes in species recorded feeding on mistletoe did not differ from control sites. Having confirmed the status of mistletoe as a keystone resource, we suggest that nutrient enrichment via litter-fall is the main mechanism promoting species richness, driving small-scale heterogeneity in productivity and food availability for woodland animals. This explanation applies to other parasitic plants with high turnover of enriched leaves, and the community-scale influence of these plants is most apparent in low productivity systems.

Mistletoe as a keystone resource: an experimental test.

Many plants use birds to disperse their propagules, but mistletoes are especially reliant on their services. As aerial parasites, mistletoe seeds need to be deposited upon branches of suitable hosts, and mistletoe specialist frugivores (from eight different avian families) have long been regarded as their coevolved dispersers. Like the pioneer Johnny 'Appleseed' Chapman who established nurseries that helped open up land for settlement, these birds are considered benevolent dispersers of this keystone resource and often invoked as illustrative examples of mutualistic interactions. We have compared recent research on these specialists with studies of other birds with broader diets (generalists) which also disperse mistletoe seed. Rather than mutualists, we suggest that mistletoe specialist frugivores are better considered exploitative, with multiple lineages evolving independently to capitalize on this reliable, nutritious resource. Although mistletoe specialist frugivores are quantitatively important seed dispersers in some regions, their specialized diet restricts them to areas with high mistletoe densities, resulting in contagious dispersal patterns. By intensifying existing infections, mistletoe specialist frugivores increase their own medium-term food security-akin to market gardeners profiting from intensive cultivation. Exploring the ecological and evolutionary implications of this proposition, we evaluate the consequences of different dispersal patterns on mistletoe fitness and highlight the neglected role of dietary generalists in the stabilization of plant-animal interactions.

Mistletoe specialist frugivores: latterday "Johnny Appleseeds" or self‑serving market gardeners?

On pluralism in ecology: seeing the forest and the trees.

Reproductive investment is typically considered in terms of size and number of propagules produced. Compared with a thorough understanding of the overall patterns and ecological correlates of avian clutch size, egg size has received less attention and the total effort invested in laying a clutch of eggs is rarely considered. We used clutch volume as an alternative estimate of reproductive investment and present the first class-level analysis of clutch volume in birds using 1,364 randomly-selected species in 204 families. The relationship between body mass and egg volume was very strong (r2 = 0.946), validating previous studies identifying four families (Apterygidae, Pelecanoidiididae, Sternidae and Dromadidiae) with disproportionately large eggs. Clutch volume was also closely related to body mass (r2 = 0.909) and all but one of the taxa with disproportionately large eggs conformed to the overall relationship, their greater egg dimensions compensated by diminished clutch size. The only family which departed significantly from the relationship between body mass and clutch volume was the mound builders (Megapodiidae)-the only group of birds that do not rely on body heat for incubation. Although previously known for laying large clutches of large eggs containing disproportionately large yolks, the remarkable investment of megapodes in reproduction (more than seven times greater than other birds of comparable mass) has been hitherto overlooked. We consider the evolutionary basis and ecological implications of this finding, suggesting that energetic costs associated with incubation act as an upper limit on reproductive output of other birds. We recommend clutch volume as a sensitive, fine-grained measure of reproductive effort for research at a wide range of scales and advocate further analysis of ecological correlates of clutch volume in birds and amniotes generally. 

Reassessing breeding investment in birds: class-wide analysis of clutch volume reveals a single outlying family.

Insectivorous birds have been recognized as disproportionately sensitive to land-use intensification and habitat loss, with those species feeding primarily on the ground exhibiting some of the most dramatic declines. Altered litter inputs and availability of epigeic arthropods have been suggested to underlie reduced abundances and shrinking distributions but direct evidence is lacking. I used a patch-scale removal experiment in southern Australia to evaluate whether ground-feeding insectivores are especially vulnerable to altered litter-fall. Building on work demonstrating the importance of mistletoe litter to nutrient dynamics, litter was reduced by removing mistletoe (Loranthaceae) from one set of eucalypt woodlands, responses of birds three years after mistletoe removal compared with otherwise similar control woodlands containing mistletoe. Despite not feeding on mistletoes directly, insectivores exhibited the greatest response to mistletoe removal. Among woodland residents, ground-foraging insectivores showed the most dramatic response; treatment woodlands losing an average of 37.4% of their pre-treatment species richness. Once these 19 species of ground-foraging insectivores were excluded, remaining woodland species showed no significant effect of mistletoe removal. This response reflects greater initial losses in treatment woodlands during the study (which coincided with a severe drought) and double the number of species returning to control woodlands (where mistletoe numbers and litter were not manipulated) post-drought. These findings support the productivity-based explanation of declining insectivores, suggesting diminished litter-fall reduced habitat quality for these birds via decreased availability of their preferred prey. In addition to altered prey availability, interactions between litter-fall and epigeic arthropods exemplify the importance of below-ground / above-ground linkages driving ecosystem function. 

Disproportionate Declines in Ground-Foraging Insectivorous Birds after Mistletoe Removal.

803 I. 803 II. 804 III. 804 IV. 805 V. 805 VI. 806 References 807 SUMMARY: Rather than direct plant-plant interactions, research on the community-scale influence of mistletoes reveals hitherto unappreciated roles of animals in mediating facilitation. Lacking roots and reliant upon animal vectors, mistletoes represent model systems with which to understand mechanisms underlying interaction networks. In addition to direct effects on nutrient dynamics via enriched litter-fall, mistletoes are visited by pollinators, seed dispersers and natural enemies, complementing increased heterogeneity in nutrient returns reallocated from infected hosts with increased external inputs. These amplified bottom-up effects are coupled with top-down influences of insectivores attracted to infected hosts and stands by increased availability of favoured prey. Simultaneously influencing nutrient dynamics and plant-plant interactions from below and above, visiting animals help explain variation in the context dependence of facilitation.

Fleshing out facilitation - reframing interaction networks beyond top-down versus bottom-up.

Host range is a critical life history trait of parasites, influencing prevalence, virulence and ultimately determining their distributional extent. Current approaches to measure host range are sensitive to sampling effort, the number of known hosts increasing with more records. Here, we develop a novel application of results-based stopping rules to determine how many hosts should be sampled to yield stable estimates of the number of primary hosts within regions, then use species richness estimation to predict host ranges of parasites across their distributional ranges. We selected three mistletoe species (hemiparasitic plants in the Loranthaceae) to evaluate our approach: a strict host specialist (Amyema lucasii, dependent on a single host species), an intermediate species (Amyema quandang, dependent on hosts in one genus) and a generalist (Lysiana exocarpi, dependent on many genera across multiple families), comparing results from geographically-stratified surveys against known host lists derived from herbarium specimens. The results-based stopping rule (stop sampling bioregion once observed host richness exceeds 80% of the host richness predicted using the Abundance-based Coverage Estimator) worked well for most bioregions studied, being satisfied after three to six sampling plots (each representing 25 host trees) but was unreliable in those bioregions with high host richness or high proportions of rare hosts. Although generating stable predictions of host range with minimal variation among six estimators trialled, distribution-wide estimates fell well short of the number of hosts known from herbarium records. This mismatch, coupled with the discovery of nine previously unrecorded mistletoe-host combinations, further demonstrates the limited ecological relevance of simple host-parasite lists. By collecting estimates of host range of constrained completeness, our approach maximises sampling efficiency while generating comparable estimates of the number of primary hosts, with broad applicability to many host-parasite systems.

Novel application of species richness estimators to predict the host range of parasites.

It has long been recognized that primary foundation species (FS), such as trees and seagrasses, enhance biodiversity. Among the species facilitated are secondary FS, including mistletoes and epiphytes. Case studies have demonstrated that secondary FS can further modify habitat-associated organisms ('inhabitants'), but their net effects remain unknown. Here we assess how inhabitants, globally, are affected by secondary FS. We extracted and calculated 2,187 abundance and 397 richness Hedges' g effect sizes from 91 and 50 publications, respectively. A weighted meta-analysis revealed that secondary FS significantly enhanced the abundance and richness of inhabitants compared to the primary FS alone. This indirect facilitation arising through sequential habitat formation was consistent across environmental and experimental conditions. Complementary unweighted analyses on log response ratios revealed that the magnitude of these effects was similar to the global average strength of direct facilitation from primary foundation species and greater than the average strength of trophic cascades, a widely recognized type of indirect facilitation arising through sequential consumption. The finding that secondary FS enhance the abundance and richness of inhabitants has important implications for understanding the mechanisms that regulate biodiversity. Integrating secondary FS into conservation practice will improve our ability to protect biodiversity and ecosystem function.

Secondary foundation species enhance biodiversity.

Ethical birding call playback and conservation.

Mistletoes: Pathology, Systematics, Ecology, and Management.

In an era characterized by recurrent large wildfires in many parts of the globe, there is a critical need to understand how animal species respond to fires, the rates at which populations can recover, and the functional changes fires may cause. Using quantified changes in habitat parameters over a ~400-yr post-fire chronosequence in an obligate-seeding Australian eucalypt woodland, we build and test predictions of how birds, as individual species and aggregated into functional groups according to their use of specific habitat resources, respond to time since fire. Individual bird species exhibited four generalized response types to time since fire: incline, decline, delayed, and bell. All significant relationships between bird functional group richness or abundance and time since fire were consistent with predictions based on known time-since-fire-associated changes in habitat features putatively important for these bird groups. Consequently, we argue that the bird community is responding to post-fire successional changes in habitat as per the habitat accommodation model, rather than to time since fire per se, and that our functional framework will be of value in predicting bird responses to future disturbances in this and other obligate-seeder forest and woodland ecosystems. Most bird species and functional groups that were affected by time since fire were associated with long-unburned woodlands. In the context of recent large, stand-replacement wildfires that have affected a substantial proportion of obligate-seeder eucalypt woodlands, and the multi-century timescales over which post-fire succession occurs, it would appear preferable from a bird conservation perspective if fires initiating loss of currently long-unburned woodlands were minimized. Once long-unburned woodlands are transformed by fire into recently burned woodlands, there is limited scope for alternative management interventions to accelerate the rate of habitat development after fire, or supplement the resources formerly provided to birds by long-unburned woodlands, with the limited exception of augmenting hollow availability for key hollow-nesting species.

Fire-mediated habitat change regulates woodland bird species and functional group occurrence.

Conditions capable of supporting multicellular life are predicted to continue for another billion years, but humans will inevitably become extinct within several million years. We explore the paradox of a habitable planet devoid of people, and consider how to prioritise our actions to maximise life after we are gone.

Post-Anthropocene Conservation.

All organisms engage in parasitic relations, as either parasites or hosts. Some species may even play both roles simultaneously. Among flowering plants, the most widespread form of parasitism is characterized by the development of an intrusive organ called the haustorium, which absorbs water and nutrients from the host. Despite this functionally unifying feature of parasitic plants, haustoria are not homologous structures; they have evolved 12 times independently. These plants represent ca. 1% of all extant flowering species and show a wide diversity of life histories. A great variety of plants may also serve as hosts, including other parasitic plants. This phenomenon of parasitic exploitation of another parasite, broadly known as hyper- or epiparasitism, is well described among bacteria, fungi, and animals, but remains poorly understood among plants. Here, we review empirical evidence of plant hyperparasitism, including variations of self-parasitism, discuss the diversity and ecological importance of these interactions, and suggest possible evolutionary mechanisms. Hyperparasitism may provide benefits in terms of improved nutrition and enhanced host-parasite compatibility if partners are related. Different forms of self-parasitism may facilitate nutrient sharing among and within parasitic plant individuals, while also offering potential for the evolution of hyperparasitism. Cases of hyperparasitic interactions between parasitic plants may affect the ecology of individual species and modulate their ecosystem impacts. Parasitic plant phenology and disperser feeding behavior are considered to play a major role in the occurrence of hyperparasitism, especially among mistletoes. There is also potential for hyperparasites to act as biological control agents of invasive primary parasitic host species.

Parasites on parasites: hyper-, epi-, and autoparasitism among flowering plants.

Parasitic plants are mostly viewed as pests. This is caused by several species causing serious damage to agriculture and forestry. There is however much more to parasitic plants than presumed weeds. Many parasitic plans exert even positive effects on natural ecosystems and human society, which we review in this paper. Plant parasitism generally reduces the growth and fitness of the hosts. The network created by a parasitic plant attached to multiple host plant individuals may however trigger transferring systemic signals among these. Parasitic plants have repeatedly been documented to play the role of keystone species in the ecosystems. Harmful effects on community dominants, including invasive species, may facilitate species coexistence and thus increase biodiversity. Many parasitic plants enhance nutrient cycling and provide resources to other organisms like herbivores or pollinators, which contributes to facilitation cascades in the ecosystems. There is also a long tradition of human use of parasitic plants for medicinal and cultural purposes worldwide. Few species provide edible fruits. Several parasitic plants are even cultivated by agriculture/forestry for efficient harvesting of their products. Horticultural use of some parasitic plant species has also been considered. While providing multiple benefits, parasitic plants should always be used with care. In particular, parasitic plant species should not be cultivated outside their native geographical range to avoid the risk of their uncontrolled spread and the resulting damage to ecosystems.

The bright side of parasitic plants: what are they good for?

Artificial refuges are human-made structures that aim to create safe places for animals to breed, hibernate, or take shelter in lieu of natural refuges. Artificial refuges are used across the globe to mitigate the impacts of a variety of threats on wildlife, such as habitat loss and degradation. However, there is little understanding of the science underpinning artificial refuges, and what comprises best practice for artificial refuge design and implementation for wildlife conservation. We address this gap by undertaking a systematic review of the current state of artificial refuge research for the conservation of wildlife. We identified 224 studies of artificial refuges being implemented in the field to conserve wildlife species. The current literature on artificial refuges is dominated by studies of arboreal species, primarily birds and bats. Threatening processes addressed by artificial refuges were biological resource use (26%), invasive or problematic species (20%), and agriculture (15%), yet few studies examined artificial refuges specifically for threatened (Vulnerable, Endangered, or Critically Endangered) species (7%). Studies often reported the characteristics of artificial refuges (i.e. refuge size, construction materials; 87%) and surrounding vegetation (35%), but fewer studies measured the thermal properties of artificial refuges (18%), predator activity (17%), or food availability (3%). Almost all studies measured occupancy of the artificial refuges by target species (98%), and over half measured breeding activity (54%), whereas fewer included more detailed measures of fitness, such as breeding productivity (34%) or animal body condition (4%). Evaluating the benefits and impacts of artificial refuges requires sound experimental design, but only 39% of studies compared artificial refuges to experimental controls, and only 10% of studies used a before-after-control-impact (BACI) design. As a consequence, few studies of artificial refuges can determine their overall effect on individuals or populations. We outline a series of key steps in the design, implementation, and monitoring of artificial refuges that are required to avoid perverse outcomes and maximise the chances of achieving conservation objectives. This review highlights a clear need for increased rigour in studies of artificial refuges if they are to play an important role in wildlife conservation.

Artificial refuges for wildlife conservation: what is the state of the science?

The arboreal marsupial monito del monte (genus , with two recognized species) is a paradigmatic mammal. It is the sole living representative of the order Microbiotheria, the ancestor lineage of Australian marsupials. Also, this marsupial is the unique frugivorous mammal in the temperate rainforest, being the main seed disperser of several endemic plants of this ecosystem, thus acting as keystone species.  is also one of the few hibernating mammals in South America, spending half of the year in a physiological dormancy where metabolism is reduced to 10% of normal levels. This capacity to reduce energy expenditure in winter contrasts with the enormous energy turnover rate they experience in spring and summer. The unique life history strategies of this living Microbiotheria, characterized by an alternation of life in the slow and fast lanes, putatively represent ancestral traits that permitted these cold-adapted mammals to survive in this environment. Here, we describe the ecological role of this emblematic marsupial, summarizing the ecophysiology of hibernation and sociality, updated phylogeographic relationships, reproductive cycle, trophic relationships, mutualisms, conservation, and threats. This marsupial shows high densities, despite presenting slow reproductive rates, a paradox explained by the unique characteristics of its three-dimensional habitat. We finally suggest immediate actions to protect these species that may be threatened in the near future due to habitat destruction and climate change.

The ecology and evolution of the monito del monte, a relict species from the southern South America temperate forests.

We introduce a new approach-acoustic restoration-focusing on the applied utility of soundscapes for restoration, recognising the rich ecological and social values they encapsulate. Broadcasting soundscapes in disturbed areas can accelerate recolonisation of animals and the microbes and propagules they carry; long duration recordings are also ideal sources of data for benchmarking restoration initiatives and evocative engagement tools.

Article	Year
Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia\| PubMed ID: 17713788	2007
Mistletoe as a keystone resource: an experimental test. Proceedings. Biological sciences\| PubMed ID: 22787026	2012
Mistletoe specialist frugivores: latterday "Johnny Appleseeds" or self‑serving market gardeners? Oecologia\| PubMed ID: 23797409	2013
On pluralism in ecology: seeing the forest and the trees. Proceedings. Biological sciences\| PubMed ID: 24403335	2014
Reassessing breeding investment in birds: class-wide analysis of clutch volume reveals a single outlying family. PloS one\| PubMed ID: 25633998	2015
Disproportionate Declines in Ground-Foraging Insectivorous Birds after Mistletoe Removal. PloS one\| PubMed ID: 26640895	2015
Fleshing out facilitation - reframing interaction networks beyond top-down versus bottom-up. The New phytologist\| PubMed ID: 27322844	2016
Novel application of species richness estimators to predict the host range of parasites. International journal for parasitology\| PubMed ID: 27899327	2017
Secondary foundation species enhance biodiversity. Nature ecology & evolution\| PubMed ID: 29507379	2018
Ethical birding call playback and conservation. Conservation biology : the journal of the Society for Conservation Biology\| PubMed ID: 30054953	2019
Mistletoes: Pathology, Systematics, Ecology, and Management. Plant disease\| PubMed ID: 30769529	2008
Fire-mediated habitat change regulates woodland bird species and functional group occurrence. Ecological applications : a publication of the Ecological Society of America\| PubMed ID: 31483902	2019
Post-Anthropocene Conservation. Trends in ecology & evolution\| PubMed ID: 31784122	2020
Parasites on parasites: hyper-, epi-, and autoparasitism among flowering plants. American journal of botany\| PubMed ID: 33403666	2021
The bright side of parasitic plants: what are they good for? Plant physiology\| PubMed ID: 33793868	2021
Artificial refuges for wildlife conservation: what is the state of the science? Biological reviews of the Cambridge Philosophical Society\| PubMed ID: 34269510	2021
The ecology and evolution of the monito del monte, a relict species from the southern South America temperate forests. Ecology and evolution\| PubMed ID: 35261741	2022
Acoustic restoration: Using soundscapes to benchmark and fast-track recovery of ecological communities. Ecology letters\| PubMed ID: 35474408	2022

David M. Watson

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