Human Land Use and Amphibian Decline in Temperate Wetlands.

[Alyrium Denryle]

Of the approximately 5700 species of amphibians that are currently extant, a third of them are in a state of rapid decline [1,2]. This decline is due a number of causes, from UV radiation, to disease, to habitat destruction and introduced species [1,3,4]. Most of these declines have occurred in the tropics however a large percentage have effected pond and stream dwelling amphibians regardless of geographic location [5], and this leads to questions regarding why amphibians are under particular strain in these areas. One potential hypothesis is that these habitats are more prone to decline because human activities essentially hit them twice. Pond and stream breeding amphibian habitat has two components, the aquatic breeding habitat and surrounding terrestrial habitat [6,7,8] which serves as a corridor for dispersal as well as habitat used when not breeding (depending on specific species biology). Both of these habitats are required for amphibians to persist in an area. Human land use such as agriculture and urbanization is hypothesized to have effects upon not only the terrestrial habitat which is directly modified for human use, but also on the aquatic environment which is used by amphibians to breed. The following review will focus on the effects of land conversion for agriculture and human habitation on amphibian habitat and resulting declines and changes in local species composition. In order to do this, it is necessary to first talk about the factors that shape the ability of a species to exist within a region, and what mediates the effects of location on amphibian persistence. Then it becomes possible to discuss why land conversion would adversely change these factors.
Amphibian metapopulation dynamics have often been viewed as a kind of “ponds as patches” model [6]. This model entails that breeding ponds are used to delineate subpopulations that exchange migrants and define the units in which local extinction and recolonization occur. When this is examined, the effect of terrestrial habitat fragmentation is a stronger predictor than pond isolation of local extinction. However it is worth noting that many amphibians have short maximum dispersal distances [9] and the actual distribution of amphibian dispersal is log-normal. This means that most amphibians are site loyal but there are occasional long range dispersers. These individuals would be heavily impacted by the terrestrial habitat between ponds. If it is unsuitable the rare individual that attempts a long range movement will simply not survive the journey. This was shown using Lithobates sylvaticus [10]. Newly metamorphosed frogs selected experimentally manipulated habitat at a coarse grain. They showed no preference for fine grained patches of suitable habitat, and no evidence of habitat selection at large scales seems to exist. Effectively they set out at random from the breeding pond once metamorphosis is complete and try to find a sizeable patch. This would have the effect of increasing their density in these areas to the point that it cannot support them, or they increase the risk of disease and thus decrease survival [11]. However it is worth asking why dispersal and habitat patches matter. They matter because not only is there gene flow between patches of habitat patches[12], but because within an unmodified habitat ponds and streams have variable hydroperiods[13]. Some ponds are permanent, others reliably seasonal, drying within years, other ponds are semi-permanent and dry among years. This creates situations where an amphibian species can become locally extinct and recolonize breeding ponds across a landscape. This recolonization cannot occur if migrants cannot cross the distance between the nearest inhabited breeding pond. This same thing occurs when a pond or stream becomes otherwise unsuitable at intervals. This dynamic between hydroperiods and pond suitability, extinction, and recolonization can set up a phenotypic trade-off.

In principle the trade-off works like this: If hydroperiod is short (IE. The pond or stream is temporary), then it is in the animal’s best interest to metamorphose quickly. In effect they need to get out of the pond before they die. This should mean that tadpoles should engage in both exploitative and interference competition against con and heterospecifics in order to ensure against death from desiccation. This has been found in the genus Pseudacris [14], where Pseudacris trisceriata inhabits temporary ponds and under experimental and field conditions reaches metamorphosis much faster than Pseudacris crucifer which breeds in more permanent water. In this same system it was found that this difference is mediated by foraging behavior and essentially activity level [15]and is the result of a trade-off between anti-predator behavior and growth. Activity level in this system is known to have an effect because it has been experimentally manipulated by tricaine anesthesia [16]. Lithobates sylvaticus tadopoles were either left as controls or anesthetized with tricaine and both groups were exposed to larval Anax. The sharp decrease in activity was associated with an equivalently sharp drop in predation risk. Relative activity level has been shown to mediate interspecific exploitative competition in a Lithobates sylvaticus-Lithobates pipiens competitive system[17]. In this case two frogs which both primarily breed in temporary or semi-permanent ponds were tested in a multifactor experiment. This experiment ruled out the effects of absolute tadpole density (and it in fact appeared that there was facilitation among L. sylvaticus tadpoles raised together at high density), and controlled for the effects of size by reversing the size difference between tadpoles across species through the use of more or less mature tadpoles. The author found that the more effective competitor L. pipiens was also significantly more active and that this was enough for them to even overcome an initial size disadvantage when this effect was controlled for. This result is not robust however. It was found in another experiment that under field conditions (raised in a pen in a natural pond) L. sylvaticus fares better in competition with L pipiens so well in fact that they depress growth in the leopard frogs without themselves having their growth depressed [18]. With the addition of predator cues from caged invertebrate and fish predators however the effect was reversed and the leopard frogs asymmetrically depressed wood frog growth. The result of the prior experiment with regard to the competition was probably an artifact of cage design. In the laboratory component of this experiment it was also shown that wood frogs were consistently more active, even when exposed to predators (save for fish, activity was not significantly different between species in this treatment). This was enough for leopard frogs, perhaps with the addition of predator or competitor-induced morphology [19] changes to reverse the asymmetry of competitive interactions. It was also found that changes in morphology that grant anti-predator advantages in wood frogs are the opposite of changes that enhance competitive ability [19]. This probably mediates the interaction between wood frogs and leopard frogs observed by Relyea (2000). These anti-predator phenotypes are subject to something called phenotypic plasticity, when one genotype dictates multiple phenotypes that are dependent on environmental context. Plastic phenotypes tend to evolve when an organism is subject to a variable environment [20,21,22]. These results can also be generalized to salamanders [23].

Anti--predator behavior has the opposite relationship to hydroperiod that competitive behavior does, just as it has opposite effects on phenotype[24]. Amphibians which breed in primarily temporary water where less able to engage in effective anti-predator behavior than those which had fixed defenses against predators that bred in permanent water. Those that breed in variable water bodies (either those with a temporally variable hydroperiod, or if the variability was the result of broad preferences in breeding pond) tended to display plastic phenotypes. It has been shown the behavioral phenotypes tend to be more plastic than morphology [25] and that prey species can differentiate between predators (that are all distantly related) and respond accordingly with different phenotypes [24]. It has also been shown that amphibians evaluate predation risk and respond in a way which is proportionate to that risk, rather than the risk being a threshold based binary [26,27]

Now that the basics of the tradeoff have been examined, how does human land modification affect amphibian assemblages and why? There are two types of modification to be examined. The first is urbanization, which in broad terms is the modification of habitat in order to be suitable for human habitation. The second is agriculture, which is the modification of habitat for food production.

One way to analyze the effects of urbanization on amphibian assemblages is to survey for species in sites along an environmental gradient and then identify factors that modify local abundance and species richness using Canonical Correspondence Analysis (or some other sort of factor analysis). This was done in central Iowa on the local anuran assemblages[28], and it was found that urbanization had a strong impact on local amphibian species richness. One of the factors identified in the analysis as negatively impacting species was fragmentation of upland habitat and road cover. The species found to be most resilient to these factors is the bullfrog Lithobates catesbeianus. The most vulnerable species are Anaxyrus americanus, L. pipiens, Hyla versicolor, and H. chrysoscielus. These are spring breeding amphibians that all rely heavily on upland habitat for foraging and with the exception of L. pipiens, hibernation. Urbanization is also correlated with longer hydroperiods, which gives Acris crepitans and L. catesbeianus and advantage over the other species which breed mostly in temporary ponds. The authors specify that this may be due to a competitive advantage which excludes the temporary pond species, however given the phenotypic tradeoff involved, it is more likely that Acris and L. catesbeianus are less vulnerable to predation, and possess fixed anti-predator phenotypes.

Similar results were found with stream breeders in California. Stream permanence and structure changes were correlated with urbanization. These changes seem to have allowed for the persistence of invasive organisms such as fish, crayfish, and bullfrogs which excluded native amphibians[29]. Additionally the urban streams had longer hydroperiods, which contributed to predator persistence and probably negatively impacted amphibian larval survival. Though in the case of Tarichia granulosa, I am not sure how much of an impact the fish would have had considering their toxic skin secretions [30,31], however it is doubtful that fish would do particularly well if they swallowed eggs, larvae, or adults of these salamanders. The effects of predators are not limited to the aquatic environment either. Terrestrial predators such as skunks and raccoons are also major concerns, as their populations are artificially maintained by human refuse and man-made shelter[32].

Agriculture is probably worse for amphibian populations and communities. Agriculture can generally be divided into two categories, crop land, and cattle. Each of these types of agriculture has different effects on amphibian communities but with a lot of overlap. The first factor in which there is overlap is watershed pollution. Agrochemicals are rarely applied in a carefully controlled way. This creates runoff. Cattle also produce a lot of dung and urine from which nutrients and metabolites from whatever antibiotics and artificial hormones the cattle consumed will leach into the soil and eventually the watershed.

This was experimentally determined by cross fostering frog and salamander eggs into agricultural areas, reference sites that were non-agricultural, and in the laboratory [33]. It was found that hatching success in the agricultural sites was reduced, and that high levels of phosphate, ammonia, and biotic oxygen demand were implicated. Another experiment tested eggs and larvae of six European species ( Pleurodeles waltl, Discoglossus galganoi, Pelobates cultripes, Bufo bufo, Bufo calamita, and Hyla arborea) by exposing them to ammonium nitrate ( a common fertilizer) at ecologically relevant doses [34]. The hylid was extremely sensitive and mortality was extremely high, the Discoglussus, and B. bufo, also suffered high mortality. The other species experienced developmental malformations at high doses.

High concentrations of agricultural fertilizers impacts not only embryos but also adults, often mediated through parasites. This was demonstrated using bullfrogs [35]. There was lower parasite richness in agricultural areas, but bullfrogs were more negatively affected by the parasite loads that they did possess. This indicates that while the effect of nutrient runoff into the watershed reduces parasite species richness, it facilitates the parasites that survive. Tadpoles are also affected, Hyla versicolor when exposed to a parasite common in agricultural landscapes (a trematode that uses snails as an intermediate host) had reduced growth and survivorship to metamorphosis under a drying regime than did those exposed to no snails, or uninfected snails. Tadpoles are able to compensate for the parasite infection when ponds are permanent by metamorphosing later, and agricultural landscapes have been found to have shorter hydroperiods[36].

Pesticides have also been found to negatively impact amphibians, particularly larvae. In a mesocosm experiment using a complete block design it was found that individually and in concert pesticides at low concentrations caused reduced survivorship, increased time to metamorphosis, and decreased metamorph mass in tree frogs and leopard frogs [37]. The common herbicide roundup causes 90% mortality in amphibians with concentrations as low as .8 mg acid equivalent. [38]. These chemicals have been implicated in the decline of several imperiled American species; the California red-legged frog (Rana draytonii), foothill yellow-legged frog (R. boylii), Cascades frog (R. cascadae), and the mountain yellow-legged frog (R. muscosa). In these cases they are not carried in the watershed but are actually moved via air currents to the higher elevation positions that these amphibian occupies. In this way even protected habitats are not guaranteed to be free of contamination [39,40]. There also seems to be synergistic effect of pesticides and predation. When combined with predation, it was found that in several amphibian species the pesticide carbaryl increased the deadliness of predation on several species of amphibian paricularly Hyla versicolor, where it made predation 2-4 times deadlier [41]. It was even found later that actual predation was not required[42], only the predator cues, and in Green and Bullfrogs, the presence of predator cues alone increased mortality by a factor of 8 and 46 respectively. Actual predation was not the cause of this, only the physiological stress of the predator cue combined with the pesticide. What would occur with actual predation is unknown.

If all of this was not enough, it has been found that the chemical herbicide Atrazine is implicated in chemical castration and even sex reversal in the frog Xenopus laevis [43] and others [44]. This would alter the operational sex ratio in an amphibian population and damage its ability to sustain itself. After this was suggested, studies were done (and funded by the chemical manufacturer of said Atrazine) that showed negative results. However Hayes responded by showing that the researches involved in said studies had engaged in academic fraud at the manufacturer’s behest and he used a fisher’s exact test to do it [44]. It has thus been fairly well established that sex reversal occurs as a result of atrazine exposure.

With all of these mechanisms for decline, we would expect to see reduced species richness and abundance in areas with agriculture. The results are mixed. When amphibian larvae are surveyed there is a tendency to show reduced richness and abundance in areas where there is agriculture [36,45]. However when call surveys are performed, agricultural area, particularly in a forest/agriculture mosaic is positively related with amphibian richness [46]. How is this possible?
It has actually been suggested based upon some studies that a mosaic of forest and agriculture is ideal for amphibian species richness. The solution to the quandary becomes apparent when the methods are examined. Call surveys only indicate that adults are present and attempting to reproduce. It says nothing about whether or not those efforts are successful. Forested areas can act as population source with dispersing amphibians moving into nearby agricultural areas. The tadpoles do not survive [35,38,41,47,48] and thus would not be found in a larval survey and thus despite the presence of adults the agricultural areas act as a population sink. The ability of the population to sustain itself is removed and they rely upon sources within a metapopulation structure in order to persist. As Habitat becomes more fragmented the probability of successful migration decreases and species richness is eventually lost.

In summation, human land conversion is damaging to amphibian populations and is in part responsible for amphibian declines. The mechanisms by which this occurs are at least in part through the modification of hydroperiods and the introduction of toxic compounds that either kill amphibians directly or modify the dynamics of their morphology and life history trade-offs with regard to predation risk and metamorphosis. This is in addition to sex reversal turns these areas into population sinks, and the habitat fragmentation caused by both forms of land conversion inhibits successful immigration.







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[Alyrium Denryle]

Seems I managed to get the pre-proof version somehow. If a sentence seems awkward, bear in mind that it is the rough draft.